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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Antiplasmodial natural products: an update</title><author><name sortKey="Tajuddeen, Nasir" sort="Tajuddeen, Nasir" uniqKey="Tajuddeen N" first="Nasir" last="Tajuddeen">Nasir Tajuddeen</name><affiliation><nlm:aff id="Aff1"></nlm:aff></affiliation></author><author><name sortKey="Van Heerden, Fanie R" sort="Van Heerden, Fanie R" uniqKey="Van Heerden F" first="Fanie R." last="Van Heerden">Fanie R. Van Heerden</name><affiliation><nlm:aff id="Aff1"></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">31805944</idno><idno type="pmc">6896759</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6896759</idno><idno type="RBID">PMC:6896759</idno><idno type="doi">10.1186/s12936-019-3026-1</idno><date when="2019">2019</date><idno type="wicri:Area/Pmc/Corpus">000243</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000243</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Antiplasmodial natural products: an update</title><author><name sortKey="Tajuddeen, Nasir" sort="Tajuddeen, Nasir" uniqKey="Tajuddeen N" first="Nasir" last="Tajuddeen">Nasir Tajuddeen</name><affiliation><nlm:aff id="Aff1"></nlm:aff></affiliation></author><author><name sortKey="Van Heerden, Fanie R" sort="Van Heerden, Fanie R" uniqKey="Van Heerden F" first="Fanie R." last="Van Heerden">Fanie R. Van Heerden</name><affiliation><nlm:aff id="Aff1"></nlm:aff></affiliation></author></analytic><series><title level="j">Malaria Journal</title><idno type="eISSN">1475-2875</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p id="Par1">Malaria remains a significant public health challenge in regions of the world where it is endemic. An unprecedented decline in malaria incidences was recorded during the last decade due to the availability of effective control interventions, such as the deployment of artemisinin-based combination therapy and insecticide-treated nets. However, according to the World Health Organization, malaria is staging a comeback, in part due to the development of drug resistance. Therefore, there is an urgent need to discover new anti-malarial drugs. This article reviews the literature on natural products with antiplasmodial activity that was reported between 2010 and 2017.</p></sec><sec><title>Methods</title><p id="Par2">Relevant literature was sourced by searching the major scientific databases, including Web of Science, ScienceDirect, Scopus, SciFinder, Pubmed, and Google Scholar, using appropriate keyword combinations.</p></sec><sec><title>Results and Discussion</title><p id="Par3">A total of 1524 compounds from 397 relevant references, assayed against at least one strain of <italic>Plasmodium</italic>, were reported in the period under review. Out of these, 39% were described as new natural products, and 29% of the compounds had IC<sub>50</sub> ≤ 3.0 µM against at least one strain of <italic>Plasmodium</italic>. Several of these compounds have the potential to be developed into viable anti-malarial drugs. Also, some of these compounds could play a role in malaria eradication by targeting gametocytes. However, the research into natural products with potential for blocking the transmission of malaria is still in its infancy stage and needs to be vigorously pursued.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Kiszewski, A" uniqKey="Kiszewski A">A Kiszewski</name></author><author><name sortKey="Mellinger, A" uniqKey="Mellinger A">A Mellinger</name></author><author><name sortKey="Spielman, A" uniqKey="Spielman A">A Spielman</name></author><author><name sortKey="Malaney, P" uniqKey="Malaney P">P Malaney</name></author><author><name sortKey="Sachs, Se" uniqKey="Sachs S">SE Sachs</name></author><author><name sortKey="Sachs, J" uniqKey="Sachs J">J Sachs</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Snow, Rw" uniqKey="Snow R">RW Snow</name></author><author><name sortKey="Guerra, Ca" uniqKey="Guerra C">CA Guerra</name></author><author><name sortKey="Noor, Am" 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Malar J</journal-id><journal-id journal-id-type="iso-abbrev">Malar. J</journal-id><journal-title-group><journal-title>Malaria Journal</journal-title></journal-title-group><issn pub-type="epub">1475-2875</issn><publisher><publisher-name>BioMed Central</publisher-name><publisher-loc>London</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31805944</article-id><article-id pub-id-type="pmc">6896759</article-id><article-id pub-id-type="publisher-id">3026</article-id><article-id pub-id-type="doi">10.1186/s12936-019-3026-1</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review</subject></subj-group></article-categories><title-group><article-title>Antiplasmodial natural products: an update</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Tajuddeen</surname><given-names>Nasir</given-names></name><xref ref-type="aff" rid="Aff1"></xref></contrib><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0002-5710-7525</contrib-id><name><surname>Van Heerden</surname><given-names>Fanie R.</given-names></name><address><email>vanheerdenf@ukzn.ac.za</email></address><xref ref-type="aff" rid="Aff1"></xref></contrib><aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0723 4123</institution-id><institution-id institution-id-type="GRID">grid.16463.36</institution-id><institution>School of Chemistry and Physics,</institution><institution>University of KwaZulu-Natal,</institution></institution-wrap>Private Bag X01, Scottsville, Pietermaritzburg, 3209 South Africa</aff></contrib-group><pub-date pub-type="epub"><day>5</day><month>12</month><year>2019</year></pub-date><pub-date pub-type="pmc-release"><day>5</day><month>12</month><year>2019</year></pub-date><pub-date pub-type="collection"><year>2019</year></pub-date><volume>18</volume><elocation-id>404</elocation-id><history><date date-type="received"><day>3</day><month>8</month><year>2019</year></date><date date-type="accepted"><day>21</day><month>11</month><year>2019</year></date></history><permissions><copyright-statement>© The Author(s) 2019</copyright-statement><license license-type="OpenAccess"><license-p><bold>Open Access</bold>This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.</license-p></license></permissions><abstract id="Abs1"><sec><title>Background</title><p id="Par1">Malaria remains a significant public health challenge in regions of the world where it is endemic. An unprecedented decline in malaria incidences was recorded during the last decade due to the availability of effective control interventions, such as the deployment of artemisinin-based combination therapy and insecticide-treated nets. However, according to the World Health Organization, malaria is staging a comeback, in part due to the development of drug resistance. Therefore, there is an urgent need to discover new anti-malarial drugs. This article reviews the literature on natural products with antiplasmodial activity that was reported between 2010 and 2017.</p></sec><sec><title>Methods</title><p id="Par2">Relevant literature was sourced by searching the major scientific databases, including Web of Science, ScienceDirect, Scopus, SciFinder, Pubmed, and Google Scholar, using appropriate keyword combinations.</p></sec><sec><title>Results and Discussion</title><p id="Par3">A total of 1524 compounds from 397 relevant references, assayed against at least one strain of <italic>Plasmodium</italic>, were reported in the period under review. Out of these, 39% were described as new natural products, and 29% of the compounds had IC<sub>50</sub> ≤ 3.0 µM against at least one strain of <italic>Plasmodium</italic>. Several of these compounds have the potential to be developed into viable anti-malarial drugs. Also, some of these compounds could play a role in malaria eradication by targeting gametocytes. However, the research into natural products with potential for blocking the transmission of malaria is still in its infancy stage and needs to be vigorously pursued.</p></sec></abstract><kwd-group xml:lang="en"><title>Keywords</title><kwd>Malaria</kwd><kwd><italic>Plasmodium</italic></kwd><kwd>Antiplasmodial</kwd><kwd>Natural products</kwd><kwd>Plant metabolites</kwd><kwd>Marine natural products</kwd></kwd-group><funding-group><award-group><funding-source><institution>National Research Foundation (ZA)</institution></funding-source><award-id>98345</award-id><principal-award-recipient><name><surname>Van Heerden</surname><given-names>Fanie R.</given-names></name></principal-award-recipient></award-group></funding-group><custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name><meta-value>© The Author(s) 2019</meta-value></custom-meta></custom-meta-group></article-meta></front><body><sec id="Sec1"><title>Background</title><p id="Par36">Malaria remains a serious parasitic disease in the world, with 219 million infections and 435,000 deaths cited for 2017 in the latest World Malaria Report [<xref ref-type="bibr" rid="CR1">1</xref>]. An assessment of older and more recent malaria maps shows that the disease has been geographically restricted during the twentieth century, and has remained endemic in the poor regions of the world where the climate is suitable for transmission [<xref ref-type="bibr" rid="CR2">2</xref>–<xref ref-type="bibr" rid="CR5">5</xref>]. In Africa, where the disease burden is the highest, there has been a general decline in the trend of <italic>Plasmodium falciparum</italic> malaria, from a prevalence of 40% in 1910–1929 to about 24% in 2010–2015 [<xref ref-type="bibr" rid="CR6">6</xref>]. However, in the high transmission belt covering large parts of West and Central Africa, there is little change. This shrinkage of the malaria map has been interrupted by periods of rapid increase and decline in transmission [<xref ref-type="bibr" rid="CR6">6</xref>]. The significant decline in malaria prevalence between 1945 and 1949 and again between 2005 and 2009 correlates with deliberate intervention programs. Each of these declines was preceded by a rise in malaria prevalence. The introduction of chloroquine (<bold>1</bold>) (Fig. <xref rid="Fig1" ref-type="fig">1</xref>) and dichlorodiphenyltrichloroethane (DDT) in 1945 and widespread use of insecticide-treated bed nets and artemisinin-based combination therapy (ACT) between 2005 and 2009 are partly credited for these declines. The rapid spread of resistance to chloroquine and emerging resistance to ACT in Africa, coupled with an increase in cases of vector-borne diseases in places like the USA, poses a threat to the gains that have been achieved in malaria control [<xref ref-type="bibr" rid="CR6">6</xref>–<xref ref-type="bibr" rid="CR9">9</xref>]. A World Health Organization (WHO) malaria report already shows a rise in malaria incidences in 2016 compared to 2015 [<xref ref-type="bibr" rid="CR1">1</xref>]. Also, the sustained decline in mortality due to malaria since 2010 has stalled in some regions between 2015 and 2016 and has increased in other regions [<xref ref-type="bibr" rid="CR1">1</xref>]. Therefore, the continued search for new anti-malarial agents remains an urgent priority.<fig id="Fig1"><label>Fig. 1</label><caption><p>Structures of anti-malarial drugs</p></caption><graphic xlink:href="12936_2019_3026_Fig1_HTML" id="MO1"></graphic></fig></p><p id="Par37">Malaria chemotherapy has a strong historical link to natural products. The most successful anti-malarial agents have their origins in plant metabolites. The first successful anti-malarial drug was quinine (<bold>2</bold>), isolated from the bark of the South American <italic>Cinchona</italic> tree. This compound served as a lead structure in the development of the successful synthetic anti-malarial chloroquine (<bold>1</bold>), which, in recent years, has fallen out of favour as a result of the development of drug resistance by the parasite. Likewise, artemisinin (<bold>3</bold>) was isolated from the leaves of a Chinese medicinal plant, <italic>Artemisia annua</italic>. <italic>Cinchona</italic> bark and <italic>Artemisia annua</italic> were historically used to treat fever. Sophisticated target identification strategies following the sequencing of the <italic>P. falciparum</italic> genome in addition to the application of combinatorial chemistry hit identification strategies, did not lead to the expected increase in the number of new successful anti-malarial agents, and it is plausible that the next anti-malarial agents will be identified from a natural source again [<xref ref-type="bibr" rid="CR10">10</xref>]. Due to structural characteristics such as multiple stereocenters, flexible conformations, presence of heteroatoms, natural products are more likely than synthetic compounds to have multiple targets and/or new targets. Researchers investigating natural products as potential anti-malarial drugs need to incorporate the screening of the compounds for the interaction with newly identified druggable targets, such as PfATP4 and DHODH, in order to identify hits/leads. Therefore, the continued exploration of natural products as antiplasmodial agents is of great scientific interest. Equally important is the need to review the literature in the field of malaria chemotherapy to provide a perspective for future research.</p><p id="Par38">Plant-derived antiplasmodial compounds organized according to plant families covering the literature from 1990 to 2000 have been reviewed [<xref ref-type="bibr" rid="CR11">11</xref>]. Similarly, reviews categorizing antiplasmodial compounds isolated from plants according to phytochemical classes have been conducted by Bero et al. (2005–2011) [<xref ref-type="bibr" rid="CR12">12</xref>, <xref ref-type="bibr" rid="CR13">13</xref>], Nogueira and Lopes (2009–2010) [<xref ref-type="bibr" rid="CR14">14</xref>], and Wright (2000–2010) [<xref ref-type="bibr" rid="CR15">15</xref>]. Finally, reviews covering antiplasmodial marine natural products up to 2009 have been published by Laurent and Pietra, and Fattorusso and Taglialatela-Scafati [<xref ref-type="bibr" rid="CR16">16</xref>, <xref ref-type="bibr" rid="CR17">17</xref>]. However, several new antiplasmodial chemotypes have been reported in the literature since 2010, in addition to the recent increase in antiplasmodial chemical scaffolds emerging from non-vegetal sources. Against this background, this article reviews the literature on natural products with antiplasmodial activity from 2010 to the end of 2017 and is organized according to structural types of compounds.</p><p id="Par39">A thorough search of the relevant scientific databases, including Web of Science, ScienceDirect, Scopus, SciFinder, Pubmed, and Google Scholar, was conducted. The keyword combinations of antiplasmodial, anti-malarial, <italic>Plasmodium</italic>, and malaria compounds together with plant, phytochemical, marine sponge, nudibranch, alga, cyanobacteria, mushroom, fungi, and <italic>Streptomyces</italic> were used in the search. Within the period under review, a total of 1524 compounds from 397 relevant references, assayed against at least one strain of <italic>Plasmodium</italic>, were reported. Of these compounds, 593 (39%) were described as new natural products. The number of compounds isolated from vegetal material was 1165 (76%), while 359 were from non-plant sources. Among the compounds isolated from non-plant sources, 192 (53%) were described as new, while 401 (34%) of the compounds isolated from plants were new. These numbers show that medicinal plants are still the most comprehensively explored source for antiplasmodial compounds, which may be related to ease of access. However, this review also shows the potential of non-plant material to furnish new chemotypes. Regarding the potency of these compounds, 857 (56%) had IC<sub>50</sub> ≤ 10 µM, 625 (41%) had IC<sub>50</sub> ≤ 5.0 µM, and 447 (29%) had IC<sub>50</sub> ≤ 3.0 µM against at least one strain of <italic>Plasmodium</italic>. The cut-off value for potency remains an issue of ongoing debate, but the industry standard for considering a pure compound to be active is generally accepted as IC<sub>50</sub> ≤ 10 µM [<xref ref-type="bibr" rid="CR18">18</xref>].</p><p id="Par40">The in vitro antiplasmodial activities described in this review were obtained with various <italic>P. falciparum</italic> strains with different drug sensitivities. The chloroquine-sensitive strains were 3D7, NF54, D6, HB3, F32, D10, TM4/8.2, and MRC-pf-20. Other strains used were the chloroquine-resistant strains Dd2, FcB1, <italic>Pf</italic>INDO, FcM29, MRC-pf-303, and the multidrug-resistant K1, TM90-C2A, TM93-C1088, W2, TM90-C2B, TM91-C235, NHP1337, FCR3, K1CB1, and W2mef strains. Different assays were used to determine the in vitro antiplasmodial activities of the compounds. The most commonly cited methods were the radioactive hypoxanthine-incorporation assay, the colourimetric enzyme-linked immunosorbent assays (ELISA) that measure <italic>P. falciparum</italic> lactate dehydrogenase protein (pLDH) and histidine-rich protein 2 (HRP2), a DNA-based fluorometric method using the PicoGreen (SYBR) assay, and microscopy. These methods have different sensitivities and the advantages and disadvantages have been investigated and reviewed [<xref ref-type="bibr" rid="CR19">19</xref>–<xref ref-type="bibr" rid="CR21">21</xref>]. Regardless of the in vitro assay method, in this review, only compounds with IC<sub>50</sub> ≤ 3.0 µM were considered to be of interest for further studies. Compounds with higher IC<sub>50</sub> values are listed in Additional file <xref rid="MOESM1" ref-type="media">1</xref>. Among the compounds that are discussed, 317 (70.9%) were isolated from 50 different plant families, while 130 were from non-plant sources comprising of different species of marine sponges, alga, fungi, ascidians, nudibranch, cyanobacteria and actinobacteria (Fig. <xref rid="Fig2" ref-type="fig">2</xref>).<fig id="Fig2"><label>Fig. 2</label><caption><p>Breakdown of sources for antiplasmodial compounds discussed in this review</p></caption><graphic xlink:href="12936_2019_3026_Fig2_HTML" id="MO2"></graphic></fig></p><p id="Par41">The antiplasmodial natural products are organized in seven classes, i.e. endoperoxides, alkaloids, terpenes, polyphenols, quinones and polyketides, macrocycles, and cyclic phosphotriesters, with subclasses where applicable. The review concludes with a summary of the cellular targets in <italic>Plasmodium</italic> identified for natural products and natural products with transmission-blocking potential.</p></sec><sec id="Sec2"><title>Endoperoxides</title><p id="Par42">The profound success of artemisinin (<bold>3</bold>) and derivatives as drugs for the treatment of malaria prompted the selection of endoperoxides as the first class of compounds to be discussed in this review. Endoperoxide polyketides (Fig. <xref rid="Fig3" ref-type="fig">3</xref>) belonging to the 1,2-dioxane and 1,2-dioxolane structural class with proven antiplasmodial activity have been isolated from marine sponges. The structural variability includes different lengths of the ‘western’ side chain, different branching patterns, and a fully saturated or monounsaturated cyclohexane ring, all of which affect the bioactivity [<xref ref-type="bibr" rid="CR22">22</xref>]. Plakortin (<bold>4</bold>), isolated from the marine sponge <italic>Plakortis simplex</italic>, is the archetype compound of this class. It demonstrated potent submicromolar antiplasmodial activity against chloroquine-sensitive and -resistant parasites [<xref ref-type="bibr" rid="CR23">23</xref>, <xref ref-type="bibr" rid="CR24">24</xref>]. A plausible mechanism of action, inspired by results obtained with artemisinin and other trioxanes, was proposed for these structurally simpler molecules. It involves an initial reaction of the peroxidic bond with Fe(II) heme to form an <italic>O</italic>-centred radical, which is transformed into a <italic>C</italic>-centred radical following intramolecular rearrangement. The rearranged <italic>C</italic>-centred radical on the ‘western’ alkyl side-chain represents the toxic species that kills parasites. The minimum structural requirements for antiplasmodial activity of this class of compounds have been identified. The oxygen atoms of the endoperoxide bond must be accessible to Fe(II), and the molecule must adopt the appropriate conformation for the intramolecular rearrangement through a concerted intramolecular electron transfer [<xref ref-type="bibr" rid="CR25">25</xref>]. The lower antiplasmodial activity of the peroxyketal derivative manadoperoxide C (<bold>5</bold>) and its analogues isolated from Indonesian-sourced <italic>Plakortis</italic> cfr. <italic>simplex</italic> was rationalized on the basis of these structural requirements. The 6-methoxy substituent of the manadoperoxides constitutes a hindrance for Fe(II) to the peroxide bond, leading to lower activity [<xref ref-type="bibr" rid="CR23">23</xref>]. The isolation of endoperoxide analogues <bold>6</bold>–<bold>8</bold> with a 1,2-diox-4-ene ring from <italic>Plakortis simplex</italic> allowed an extension of the structure-activity relationship (SAR). For structurally similar compounds, the unsaturated derivatives were more active due to stereochemical influence, although they were still less active than <bold>4</bold>. The lower activity compared to <bold>4</bold> could also be explained by the relative inaccessibility of the peroxide oxygen due to steric hindrance [<xref ref-type="bibr" rid="CR22">22</xref>]. These results indicate that structural changes affecting the conformational behaviour of this class of compounds, profoundly influence the antiplasmodial activity, and this knowledge will be beneficial for the design of optimized analogues [<xref ref-type="bibr" rid="CR23">23</xref>]. The related 1,2-dioxolane epiplakinidioic acid (<bold>9</bold>) was isolated from Puerto Rican-sourced <italic>P. halichondrioides</italic> and inhibited <italic>P. falciparum</italic> W2 strain. However, it was also cytotoxic against a panel of cancerous cell lines [<xref ref-type="bibr" rid="CR26">26</xref>].<fig id="Fig3"><label>Fig. 3</label><caption><p>Structures of polyketide-derived endoperoxides</p></caption><graphic xlink:href="12936_2019_3026_Fig3_HTML" id="MO3"></graphic></fig></p><p id="Par43">The norditerpenoid cycloperoxides, diacarperoxides A (<bold>10</bold>), J (<bold>11</bold>), diacarnuperoxide N (<bold>12</bold>), and 2,3,6-epihurghaperoxide (<bold>13</bold>) (Fig. <xref rid="Fig4" ref-type="fig">4</xref>) were isolated from the South China Sea sponge <italic>Diacarnus megaspinorhabdosa</italic> and inhibited both the W2 and D6 <italic>P. falciparum</italic> strains. In contrast to the polyketide-derived counterparts, the SAR of the norditerpene endoperoxides has not been studied in detail. It was suggested that variations in the configuration at C-2, C-3, and C-6, or the cyclohexane ring and the side chains do not significantly affect activity [<xref ref-type="bibr" rid="CR27">27</xref>, <xref ref-type="bibr" rid="CR28">28</xref>]. However, more detailed SAR studies need to be conducted to gain a better understanding of the activity.<fig id="Fig4"><label>Fig. 4</label><caption><p>Structures of norditerpene endoperoxides</p></caption><graphic xlink:href="12936_2019_3026_Fig4_HTML" id="MO4"></graphic></fig></p></sec><sec id="Sec3"><title>Alkaloids</title><p id="Par44">Among the 447 isolated natural products with IC<sub>50</sub> ≤ 3.0 µM reported in this review, 31.9% are alkaloids.</p><sec id="Sec4"><title>Naphthylisoquinolines</title><p id="Par45">The naphthylisoquinolines are a unique class of polyketide-derived biaryls of natural origin. These compounds are found exclusively in the Ancistrocladaceae from Central Africa and Southeast Asia, and Dioncophyllaceae endemic to the coast of West Africa. The compounds are composed of naphthalene and isoquinoline moieties and are biosynthetically derived from the acetate-polymalonate pathway [<xref ref-type="bibr" rid="CR29">29</xref>, <xref ref-type="bibr" rid="CR30">30</xref>]. The naphthalene and isoquinoline regions are coupled through a rotationally restricted C–C or C–N axes. This rotational hindrance gives rise to axial chirality, while the isoquinoline unit can have up to three stereocentres. Twelve of the monomeric naphthylisoquinolines (<bold>14</bold>–<bold>25</bold>) (Fig. <xref rid="Fig5" ref-type="fig">5</xref>) are discussed in this review. Dimeric naphthylisoquinolines have been described from species of the <italic>Ancistracladus</italic> genus, and these dimers join four aryl units through three biaryl axes and thereby potentially doubling the number of stereocentres [<xref ref-type="bibr" rid="CR31">31</xref>]. Seventeen of the dimeric naphthylisoquinolines (<bold>26</bold>–<bold>42</bold>) (Fig. <xref rid="Fig6" ref-type="fig">6</xref>) are mentioned in this report. The Ancistrocladaceae mostly produce C-6 oxygenated alkaloids with an <italic>S</italic>-configuration at C-3, and these are called the Ancistrocladaceae-type, while the alkaloids of Dioncophyllaceae exclusively have an <italic>R</italic>-configuration at C-3 and lack oxygenation at C-6 and are called the Dioncophyllaceae-type [<xref ref-type="bibr" rid="CR30">30</xref>]. Several of these compounds displayed nanomolar selective inhibition of the <italic>Plasmodium</italic> parasite viability.<fig id="Fig5"><label>Fig. 5</label><caption><p>Structures of monomeric naphthylisoquinolines</p></caption><graphic xlink:href="12936_2019_3026_Fig5_HTML" id="MO5"></graphic></fig><fig id="Fig6"><label>Fig. 6</label><caption><p>Structures of dimeric naphthylisoquinolines</p></caption><graphic xlink:href="12936_2019_3026_Fig6_HTML" id="MO6"></graphic></fig></p><p id="Par46">Ancistectorines A<sub>1</sub> (<bold>14</bold>), <italic>N</italic>-methyl A<sub>1</sub> (<bold>15</bold>), A<sub>2</sub> (<bold>16</bold>), 5-<italic>epi</italic>-A<sub>2</sub> (<bold>17</bold>), A<sub>3</sub> (<bold>20</bold>), and C<sub>1</sub> (<bold>22</bold>) were isolated from the twigs of Chinese <italic>Ancistrocladus tectorius</italic> [<xref ref-type="bibr" rid="CR32">32</xref>]. The six alkaloids potently inhibited the K1 strain of <italic>P. falciparum</italic> without cytotoxicity against rat skeletal myoblast (L6) cells. The 5,1′-coupled compounds <bold>15</bold>, <bold>16</bold>, and <bold>17</bold> were 3–7 times more active than chloroquine with <bold>17</bold> having an SI > 3000 [<xref ref-type="bibr" rid="CR32">32</xref>]. The known <italic>N</italic>-methylated 5,1′-coupled ancistrocline (<bold>18</bold>) from the same plant also showed encouraging antiplasmodial activity against the K1 and NF54 strains. In addition to low cytotoxicity against L6 cells, compound <bold>18</bold> was 2–3 times more active against chloroquine-resistant K1 than the chloroquine-sensitive NF54 strain [<xref ref-type="bibr" rid="CR33">33</xref>]. However, the additional methoxy group on the naphthalene unit of <bold>18</bold> led to > 30 fold decrease in activity compared to <bold>15</bold>. The new dioncophyllines C<sub>2</sub> (<bold>19</bold>) and F (<bold>21</bold>), and the known ancistrocladisine A (<bold>25</bold>) and 5′-<italic>O</italic>-methyldioncophylline D (<bold>23</bold>) were isolated from the root bark of Congolese <italic>Ancistrocladus ileboensis</italic> [<xref ref-type="bibr" rid="CR30">30</xref>]. The total synthesis of <bold>21</bold>, which was the first reported natural 5,8′-coupled dioncophyllaceous alkaloid, was achieved by palladium-catalyzed Suzuki–Miyaura cross-coupling of the two aryl moieties. Furthermore, the leaves of <italic>Ancistrocladus ileboensis</italic> yielded the 7,8′-coupled dioncophylline D<sub>2</sub> (<bold>24</bold>), which was also previously unreported. Compounds <bold>19</bold>, <bold>21</bold>, <bold>23</bold>, <bold>24</bold>, and <bold>25</bold> were found to be active against the NF54 strain, with <bold>21</bold> displaying double the activity against the K1 over the NF54 strain. Furthermore, the new compounds were non-toxic to L6 cells with SI values ranging from 61 to 586 [<xref ref-type="bibr" rid="CR30">30</xref>]. It is worthy to note that axial chirality influences the antiplasmodial activity of the naphthylisoquinolines when they exist as atropo-diastereomers. The <italic>M</italic>-configured analogues such as <bold>17</bold> generally showed superior selective antiplasmodial activity compared to the <italic>P</italic>-configured counterparts such as <bold>16</bold>.</p><p id="Par47">Dimerization of the naphthylisoquinoline core resulted in the rotationally-hindered 1,1′- or 3,3′-inked shuangancistrotectorines A–E (<bold>26</bold>–<bold>30</bold>) from the twigs of the Chinese <italic>Ancistrocladus tectorius</italic>. This was the first report of a natural product featuring three consecutive stereo axes, which in addition to the tetrahydroquinoline stereocentres, confers up to seven stereogenic units [<xref ref-type="bibr" rid="CR34">34</xref>]. Biological assessment of these compounds revealed sub-micromolar antiplasmodial activity against the K1 strain coupled to low toxicity against L6 cells (SI = 99.8–610.6), with compounds <bold>26</bold>, <bold>27</bold>, and <bold>30</bold>, in particular, displaying antiplasmodial activity superior to that of chloroquine [<xref ref-type="bibr" rid="CR34">34</xref>]. Similarly, jozimine A<sub>2</sub> (<bold>31</bold>), the first reported dioncophyllaceae-type sterically-hindered 3,3′-coupled dimeric naphthylisoquinoline isolated from a Congolese <italic>Ancistrocladus</italic> sp., displayed sub-nanomolar inhibitory activity, superior to that of chloroquine against the NF54 strain coupled to low cytotoxicity against L6 cells (SI > 11,400) [<xref ref-type="bibr" rid="CR35">35</xref>]. Mbandakamines A (<bold>32</bold>) and B (<bold>33</bold>), the first dimeric naphthylisoquinolines featuring the unsymmetrical 6′,1″-coupling of the naphthalene units were isolated from the leaf of another uncharacterized Congolese <italic>Ancistrocladus</italic> sp. The diacetate salts of these highly sterically-hindered compounds were more active against the NF54 strain than the free bases, possibly due to increased solubility [<xref ref-type="bibr" rid="CR36">36</xref>]. Another unidentified Congolese <italic>Ancistrocladus</italic> sp. yielded the unsymmetrically 6′,1″-coupled mbandakamine B<sub>2</sub> (<bold>34</bold>), together with two other unique dimers named spirombandakamines A<sub>1</sub> (<bold>35</bold>) and A<sub>2</sub> (<bold>36</bold>). Compounds <bold>35</bold> and <bold>36</bold>, which incorporate both a five-membered ketone ring alongside seven- and five-membered oxygenated heterocyclic rings into the dimeric structure, exhibited nanomolar antiplasmodial activity against both the K1 and NF54 parasite strains. The open-chain <bold>34</bold> was proposed as the biosynthetic precursor to the spiro-fused <bold>35</bold>, but the higher antiplasmodial activity of <bold>34</bold> as compared to <bold>35</bold> and <bold>36</bold> implies that cyclization is not beneficial to activity [<xref ref-type="bibr" rid="CR37">37</xref>]. Jozilebomines A (<bold>37</bold>) and B (<bold>38</bold>), two unsymmetrical 3,6″-coupled dimers isolated from the root extract of the Congolese <italic>Ancistrocladus ileboensis</italic>, exhibited selective antiplasmodial activity against NF54 <italic>P. falciparum</italic> strain, with weak toxicity towards L6 cells (SI = 160 and 52.3, respectively). However, this activity was lower than the related symmetrically coupled jozimine A<sub>2</sub> (<bold>31</bold>) [<xref ref-type="bibr" rid="CR38">38</xref>]. Three structurally unique heterodimeric naphthylisoquinolines, ealapasamines A–C (<bold>39</bold>–<bold>41</bold>), were isolated from the leaf of <italic>Ancistrocladus ealensis</italic>. The ealapasamines are the first reported unsymmetrical dimers in which the constituent monomeric naphthylisoquinoline units are linked at different positions, i.e. one 5,8′-coupled monomer links to another 7,8′-coupled unit at the 6′ position of the respective naphthanyl subunits. This subsequently results in three different biaryl linkages, with the inter-naphthanyl biaryl axis being configurationally unstable. Compounds <bold>39</bold>–<bold>41</bold> were active against <italic>P. falciparum</italic> (K1 and NF54) with low nanomolar IC<sub>50</sub> values and low toxicity to L6 cells [<xref ref-type="bibr" rid="CR39">39</xref>].</p><p id="Par48">The bioactivity of the dimeric naphthylisoquinolines, as with the monomers, is influenced by axial chirality as, for example, seen in the superior activity of jozimine A<sub>2</sub> over the atropo-diastereomer, 3′-<italic>epi</italic>-jozimine A2 (<bold>42</bold>) [<xref ref-type="bibr" rid="CR29">29</xref>, <xref ref-type="bibr" rid="CR35">35</xref>]. So far, jozimine A<sub>2</sub> demonstrated the best antiplasmodial activity (IC<sub>50</sub> = 1.4 nM) against the chloroquine-sensitive NF54 strain, while mbandakamine B<sub>2</sub> is the most active dimer against the chloroquine-resistant K1 strain (IC<sub>50</sub> = 4.0 nM). With potent in vitro activities and high selectivity for the parasites over mammalian cell lines, the dimeric naphthylisoquinolines can be considered as viable anti-malarial hits. It will be worthwhile to study the mechanism of action as well as in vitro and in vivo potency against a comprehensive panel of drug-sensitive and -resistant parasites. Equally important for an anti-malarial drug is the need for oral bioavailability, and hence pharmacokinetic studies are highly desirable. The synthesis of some dimeric naphthylisoquinolines has been reported, and since only small amounts of these potent compounds are present in plant material, the syntheses of these compounds will be essential for further developments [<xref ref-type="bibr" rid="CR40">40</xref>].</p></sec><sec id="Sec5"><title>Benzylisoquinolines and other isoquinolines</title><p id="Par49">Three new tricyclic isoquinoline alkaloids (Fig. <xref rid="Fig7" ref-type="fig">7</xref>) were isolated from the leaf extract of <italic>Cassia siamea</italic> (Fabaceae), a plant traditionally used to treat periodic fever and malaria in Indonesia. Among the isolated compounds, cassiarin J (<bold>43</bold>) and the first halogenated cassiarin congener, cassiarin K (<bold>44</bold>), inhibited the in vitro growth of 3D7 <italic>P. falciparum</italic> [<xref ref-type="bibr" rid="CR41">41</xref>]. However, both compounds <bold>43</bold> and <bold>44</bold> were less active than chemically simpler and the potent cassiarin A (<bold>45</bold>), suggesting that the role of the pyran ring of the cassiarins in antiplasmodial activity should be further explored in structure–activity relationship (SAR) investigations [<xref ref-type="bibr" rid="CR42">42</xref>].<fig id="Fig7"><label>Fig. 7</label><caption><p>Structures of cassiarins</p></caption><graphic xlink:href="12936_2019_3026_Fig7_HTML" id="MO7"></graphic></fig></p><p id="Par50">The <sc>l</sc>-tyrosine-derived benzylisoquinoline alkaloids form a structurally diverse group of plant-derived compounds, many of which are associated with potent biological activities, and antiplasmodial activity is no exception. During the review period, the activity of one morphinanedienone alkaloid (<bold>46</bold>) (Fig. <xref rid="Fig8" ref-type="fig">8</xref>), six aporphines (<bold>47</bold>–<bold>52</bold>), six berberine-type compounds (<bold>53</bold>–<bold>58</bold>) and seven bisbenzyltetrahydroisoquinoline alkaloids (<bold>59</bold>–<bold>65</bold>) (Fig. <xref rid="Fig9" ref-type="fig">9</xref>) were reported. The morphinanedienone alkaloid, (−)-milonine (<bold>46</bold>) from the bark of <italic>Dehaasia longipedicellata</italic> (Lauraceae), exhibited sub-micromolar selective antiplasmodial activity against K1 parasites [<xref ref-type="bibr" rid="CR43">43</xref>]. Carraz et al. reported that a derivative of a related morphinan, tazopsine, is active against the liver stages of the parasite and that this class of compounds may have potential as anti-malarial leads [<xref ref-type="bibr" rid="CR44">44</xref>].<fig id="Fig8"><label>Fig. 8</label><caption><p>Structure of (−)-milonine</p></caption><graphic xlink:href="12936_2019_3026_Fig8_HTML" id="MO8"></graphic></fig><fig id="Fig9"><label>Fig. 9</label><caption><p>Structures of benzylisoquinoline alkaloids</p></caption><graphic xlink:href="12936_2019_3026_Fig9_HTML" id="MO9"></graphic></fig></p><p id="Par51">Following the screening of crude extracts of Malaysian medicinal plants, the extract of <italic>Dehaasia longipedicellata</italic> was identified as a promising antiplasmodial starting point. Chemical investigation of the bark extract afforded boldine (<bold>47</bold>) and (−)-<italic>O</italic>,<italic>O</italic>-dimethylgrisabine (<bold>59</bold>) as the most active constituents, both of which were active against the K1 strain of <italic>P. falciparum,</italic> with <bold>59</bold>, in particular, outperforming chloroquine in this assay. The compounds were not cytotoxic to a pancreatic cancer cell line (hTERT-HPNE) at 200 µM, indicating selective toxicity to the parasite [<xref ref-type="bibr" rid="CR43">43</xref>]. Based on the antiplasmodial screening of 794 plant extracts from Papua New Guinea and Australia, four species were selected for further investigation, one of which was <italic>Stephania zippeliana</italic> (Menispemaceae) [<xref ref-type="bibr" rid="CR45">45</xref>]. <italic>Stephania zippeliana</italic> yielded xylopine (<bold>48</bold>), which selectively inhibited the 3D7, FCR3, HB3, and K1, in addition to the D6 and W2 <italic>P. falciparum</italic> strains [<xref ref-type="bibr" rid="CR46">46</xref>, <xref ref-type="bibr" rid="CR47">47</xref>]. Bioassay-guided fractionation of <italic>Stephania venosa</italic> tubers yielded the aporphine alkaloids stephanine (<bold>49</bold>), crebanine (<bold>50</bold>), and <italic>O</italic>-methylbulbocapnine (<bold>51</bold>) as antiplasmodial principles. Unfortunately, the most active alkaloid against 3D7 and W2 parasites, stephanine (<bold>49</bold>), was also the most cytotoxic to cancerous and non-cancerous cell lines [<xref ref-type="bibr" rid="CR48">48</xref>]. Chemical interrogation of the root of <italic>Thalictrum flavum</italic> (Ranunculaceae) yielded the aporphine alkaloid, preocoteine (<bold>52</bold>), the protoberberines, pseudoberberin (<bold>54</bold>) and berberin (<bold>55</bold>), and the bisbenzylisoquinoline thaligosidine (<bold>60</bold>). The compounds exhibited antiplasmodial activity against the FcB1 strain. However, the activity of the quaternary protoberberines was not selective towards the parasite [<xref ref-type="bibr" rid="CR49">49</xref>]. The tetrahydroprotoberberine alkaloid cheilanthifoline (<bold>53</bold>), isolated from <italic>Corydalis calliantha</italic> (Papaveraceae), an annual herb used in Bhutanese traditional medicine to treat malaria, also displayed activity against the TM4 strain of <italic>P. falciparum</italic> [<xref ref-type="bibr" rid="CR50">50</xref>]. The aerial part of <italic>Meconopsis simplicifolia</italic> (Papaveraceae) is an ingredient in more than eight Bhutanese traditional medicine formulations and has displayed potent antiplasmodial activity against TM4/8.2 and K1CB1 strains of <italic>P. falciparum</italic> (IC<sub>50</sub> = 0.4 and 6.39 µg/mL, respectively) [<xref ref-type="bibr" rid="CR51">51</xref>]. Extraction and purification of the aerial components of <italic>Meconopsis simplicifolia</italic> yielded the protoberberine-type benzylisoquioline, simplicifolianine (<bold>56</bold>), which showed potent antiplasmodial activity against the TM4/8.2 and K1CB1 strains in the absence of significant cytotoxicity to Vero and human oral carcinoma (KB) cells [<xref ref-type="bibr" rid="CR52">52</xref>].</p><p id="Par52">Three bisbenzylisoquinoline alkaloids, 2-norcepharanthine (<bold>61</bold>), cepharanoline (<bold>62</bold>), and fangchinoline (<bold>63</bold>), which were isolated from <italic>Stephania rotunda</italic> tuber as minor constituents, all showed potent antiplasmodial activity against the W2 strain with SI ≥ 40 [<xref ref-type="bibr" rid="CR53">53</xref>]. Encouragingly, these compounds were twice as active as the major alkaloid of <italic>Stephania rotunda</italic>, cepharanthine (<bold>64</bold>), which was previously reported to inhibit parasites in vitro and in vivo [<xref ref-type="bibr" rid="CR54">54</xref>]. Further investigation found that the <italic>Stephania rotunda</italic> alkaloid <bold>64</bold> and the protoberberine-type benzylisoquinolines palmatine (<bold>57</bold>) and pseudopalmatine (<bold>58</bold>) also inhibited the in vitro viability of <italic>P. falciparum</italic> W2. However, while <bold>64</bold> was found to be cytotoxic against K562S cells, this was not the case for <bold>58</bold> at the highest tested concentration (IC<sub>50</sub> > 25 µM). These findings supported the use of <italic>Stephania rotunda</italic> in malaria treatment by traditional healers in Cambodia [<xref ref-type="bibr" rid="CR55">55</xref>]. Desgrouas et al. concluded that cepharanthine (<bold>64</bold>) affected the ring stage of the parasite [<xref ref-type="bibr" rid="CR56">56</xref>, <xref ref-type="bibr" rid="CR57">57</xref>]. Furthermore, in in vitro studies, <bold>64</bold> had a synergistic antiplasmodial effect with the anti-malarial drugs chloroquine, atovaquone, and piperaquine, but had an antagonistic effect with dihydroartemisinin and mefloquine [<xref ref-type="bibr" rid="CR56">56</xref>, <xref ref-type="bibr" rid="CR57">57</xref>]. In in vivo experiments, combinations of <bold>64</bold> and chloroquine, and <bold>64</bold> and amodiaquine were assayed in mice. Both combinations delayed parasitic growth and extended the life expectancies of the mice compared to the drugs alone [<xref ref-type="bibr" rid="CR57">57</xref>]. Fangchinoline (<bold>63</bold>) and the methyl ether tetrandrin (<bold>65</bold>), both produced by <italic>Stephania tetrandra</italic>, are not only cytotoxic against cancer cell lines, but also reverse resistance of multidrug-resistant human cancer cells by inhibiting P-glycoprotein activity, thereby increasing drug concentration in the cells [<xref ref-type="bibr" rid="CR58">58</xref>]. The resistance-reversal effect was also observed with <italic>Plasmodium</italic>; Ye and Van Dyke reported that <bold>65</bold> in combination with chloroquine resulted in a 44 fold potentiation of parasite killings [<xref ref-type="bibr" rid="CR59">59</xref>]. These authors also reported on the structure–activity relationship of bisbenzylisoquinoline [<xref ref-type="bibr" rid="CR59">59</xref>]. For activity, the configuration of C-1′ of the ‘right-hand’ ring should be <italic>S</italic>. The configuration of C-1 of the ‘left-hand’ ring has little influence on the antiplasmodial activity. Furthermore, the position of the bridges connecting the two monomeric benzylisoquinolines also plays a role and compounds with ether bridges between C-8 to C-7′, and between 11 and 12′ (head–head and tail–tail dimer) have the highest antiplasmodial activity.</p></sec><sec id="Sec6"><title>Phenanthrene derivatives: phenanthridine, phenanthroindolizidine, and phenanthrene alkaloids</title><p id="Par53">The dichloromethane bark extract of <italic>Cryptocarya nigra</italic> (Lauraceae) afforded the phenanthrene alkaloid 2-hydroxyatherosperminine (<bold>66</bold>) (Fig. <xref rid="Fig10" ref-type="fig">10</xref>), which was found to be active against the <italic>P. falciparum</italic> K1 strain. The significantly improved activity of <bold>66</bold> over the C-2 deoxy analogue atherosperminine indicates a possible important region of the pharmacophore [<xref ref-type="bibr" rid="CR60">60</xref>].<fig id="Fig10"><label>Fig. 10</label><caption><p>Structures of phenanthrene alkaloids</p></caption><graphic xlink:href="12936_2019_3026_Fig10_HTML" id="MO10"></graphic></fig></p><p id="Par54">The methanol extract of <italic>Ficus septica</italic> (Moraceae) twigs exhibited in vitro antiplasmodial activity against the 3D7 strain (IC<sub>50</sub> = 2.0 µg/mL). Bioassay-guided fractionation of the chloroform fraction of the active methanol extract led to the isolation of the known compounds, dehydrotylophorine (<bold>67</bold>), dehydroantofine (<bold>68</bold>) and tylophoridicine (<bold>69</bold>) (Fig. <xref rid="Fig10" ref-type="fig">10</xref>). The three phenanthroindolizidine alkaloids inhibited the 3D7 strain with sub-micromolar IC<sub>50</sub> and had low cytotoxicity. The selective antiplasmodial activity of these alkaloids indicates that other alkaloids of this class should be further explored [<xref ref-type="bibr" rid="CR61">61</xref>].</p><p id="Par55">The benzophenanthridine alkaloid nitidine (<bold>70</bold>) (Fig. <xref rid="Fig11" ref-type="fig">11</xref>) was isolated as the main antiplasmodial compound from <italic>Zanthoxylum chalybeum</italic> (Rutaceae) and <italic>Zanthoxylum rhoifolium</italic> [<xref ref-type="bibr" rid="CR62">62</xref>, <xref ref-type="bibr" rid="CR63">63</xref>]. Compound <bold>70</bold> displayed rapid activity against chloroquine-sensitive and -resistant parasites with little evidence of cross-resistance, consistent with previous reports [<xref ref-type="bibr" rid="CR64">64</xref>]. Treatment of <italic>Plasmodium berghei</italic>-infected mice with <bold>70</bold> gave an ED<sub>50</sub> value of 18.9 mg/kg/day without mice mortality. Nitidine (<bold>70</bold>) did not interfere with parasite DNA replication and was found to localize in the parasite cytoplasm. The mechanism of action of <bold>70</bold> might be similar to that of chloroquine since it formed a complex with heme and inhibited the formation of β-haematin in vitro [<xref ref-type="bibr" rid="CR62">62</xref>]. In contrast to the rapid activity of <bold>70</bold>, dihydronitidine (<bold>71</bold>), isolated from <italic>Zanthoxylum heitzii</italic> bark, displayed a slow-acting drug effect against 3D7 parasites. This slow-acting effect, coupled with the fact that <bold>71</bold> will not carry a charge at the digestive vacuole pH, which is purportedly necessary for drug accumulation, suggests that the compound might act via a different mechanism of action [<xref ref-type="bibr" rid="CR65">65</xref>]. The poor water solubility of <bold>71</bold> might also limit its viability as an anti-malarial lead.<fig id="Fig11"><label>Fig. 11</label><caption><p>Structures of nitidine (<bold>70</bold>) and dihydronitidine (<bold>71</bold>)</p></caption><graphic xlink:href="12936_2019_3026_Fig11_HTML" id="MO11"></graphic></fig></p></sec><sec id="Sec7"><title>Terpenylindoles</title><p id="Par56">The monoterpenoid indole alkaloid uleine (<bold>72</bold>) (Fig. <xref rid="Fig12" ref-type="fig">12</xref>) was isolated as the major antiplasmodial alkaloid from the trunk bark of the Brasilian tree <italic>Aspidosperma parvifolium</italic> (Apocynaceae) and was more active against the W2 than the 3D7 strain, with low cytotoxicity against the Hep G2A16 and Vero cell lines [<xref ref-type="bibr" rid="CR66">66</xref>]. Compound <bold>72</bold> was found to localize in the parasite digestive vacuole as a result of the presence of a basic aliphatic amino group, which undergoes protonation in the acidic digestive vacuole and accumulates in suitable concentrations to inhibit heme polymerization [<xref ref-type="bibr" rid="CR67">67</xref>]. Uleine has also been isolated from <italic>Aspidosperma olivaceum</italic> [<xref ref-type="bibr" rid="CR68">68</xref>]. Traditionally, the Nkundo people in the DR Congo use various parts of <italic>Greenwayodendron suaveolens</italic> (Annonaceae) to treat malaria. Some species of monkeys chew the bitter leaves, presumably for zoopharmacognostic purposes [<xref ref-type="bibr" rid="CR69">69</xref>]. Two sesquiterpenyl indole alkaloids, <italic>N</italic>-acetylpolyveoline (<bold>73</bold>) and polyalthenol (<bold>74</bold>) (Fig. <xref rid="Fig12" ref-type="fig">12</xref>), isolated from the root bark of <italic>Greenwayodendron suaveolens</italic>, are active against the K1 strain. While polyathenol was found to be cytotoxic against MRC-5 cells, <bold>73</bold> was more selective (SI = 10.6) [<xref ref-type="bibr" rid="CR69">69</xref>].<fig id="Fig12"><label>Fig. 12</label><caption><p>Structures of terpenyl alkaloids</p></caption><graphic xlink:href="12936_2019_3026_Fig12_HTML" id="MO12"></graphic></fig></p></sec><sec id="Sec8"><title>Bisindoles and related indoles</title><p id="Par57">Flinderole A (<bold>75</bold>) and isoborreverine (<bold>78</bold>) were isolated from the bark of the Australian tree <italic>Flindersia acuminata</italic> (Rutaceae) and flinderoles B (<bold>76</bold>) and C (<bold>77</bold>), and dimethylisoborreverine (<bold>79</bold>) from <italic>Flindersia amboinensis</italic> from Papua New Guinea [<xref ref-type="bibr" rid="CR56">56</xref>]. These indole alkaloids (Fig. <xref rid="Fig13" ref-type="fig">13</xref>) exhibited selective antiplasmodial activity against a wide panel of drug-sensitive and -resistant parasites. In a further investigation to ascertain which stage of the development cycle of the parasite is affected by the most active compound <bold>79</bold>, it was observed that <bold>79</bold> was more active against <italic>P. falciparum</italic> trophozoites, with treated parasites showing changes in digestive vacuole morphology and a reduced formation of haemozoin [<xref ref-type="bibr" rid="CR46">46</xref>, <xref ref-type="bibr" rid="CR70">70</xref>]. A different <italic>Flindersia</italic> species, <italic>Flindersia pimenteliana</italic>, was the source of the new pimentelamine C (<bold>80</bold>), the known borreverine (<bold>81</bold>), and 4-methylborreverine (<bold>82</bold>), which were reported to be active against <italic>P. falciparum</italic> 3D7 and Dd2 with low toxicity to HEK-293 cells [<xref ref-type="bibr" rid="CR71">71</xref>]. Compound <bold>80</bold>, which was isolated as the trifluoroacetate salt from the plant leaves, is one of three new indole alkaloids incorporating an ascorbic acid moiety. Interestingly, the other two analogues without a polar <italic>N</italic>-oxide moiety on the ethylamine unit attached to the indoleskeleton, were inactive [<xref ref-type="bibr" rid="CR71">71</xref>]. This suggests a SAR role for the ethylamine unit that could be further explored.<fig id="Fig13"><label>Fig. 13</label><caption><p>Structures of bisindole alkaloids <bold>75</bold>–<bold>82</bold></p></caption><graphic xlink:href="12936_2019_3026_Fig13_HTML" id="MO13"></graphic></fig></p><p id="Par58">Two bisindole alkaloids with a vobasinyl-iboga skeleton tabernaelegantine B (<bold>83</bold>) and D (<bold>84</bold>) (Fig. <xref rid="Fig14" ref-type="fig">14</xref>), isolated from <italic>Muntafara sessilifolia</italic> (Apocynaceae) stem bark, inhibited the FcB1 plasmodial strain but these compounds were also cytotoxic against L6 and MRC-5 cells [<xref ref-type="bibr" rid="CR72">72</xref>]. However, the C-3′ oxidized analogues <bold>85</bold> and <bold>86</bold>, in particular, showed better selectivity towards the parasite suggesting the position of the linkage between the monomeric units might influence the bioactivities of these compounds [<xref ref-type="bibr" rid="CR72">72</xref>]. This observation is supported by the nanomolar antiplasmodial activity of another vobasinyl-iboga alkaloid, voacamine, which also has a C-3/C-11′ linkage [<xref ref-type="bibr" rid="CR73">73</xref>]. A reinvestigation of <italic>Geissospermum laeve</italic> (Apocynaceae) using a dereplication strategy led to the isolation of new bisindole alkaloids, 3′,4′,5′,6′-tetradehydrogeissospermine (<bold>87</bold>) and geissolosimine (<bold>88</bold>), from the bark of the tree [<xref ref-type="bibr" rid="CR74">74</xref>]. Compound <bold>88</bold> has also been isolated from the bark of <italic>Geissospermum vellosii</italic> [<xref ref-type="bibr" rid="CR75">75</xref>]. The compounds exhibited non-selective antiplasmodial activity against FcB1 parasites [<xref ref-type="bibr" rid="CR74">74</xref>]. Moreover, <bold>88</bold> was also active against the D10 strain with low toxicity to Chinese hamster ovarian cells [<xref ref-type="bibr" rid="CR75">75</xref>]. Divarine (<bold>89</bold>), longicaudatine (<bold>90</bold>), longicaudatine F (<bold>91</bold>), and longicaudatine Y (<bold>92</bold>) from the stem bark of <italic>Strychnos malacoclados</italic> (Loganiaceae) inhibited the growth of the 3D7 and W2 parasite strains. A cytotoxicity assay on WI-38 human fibroblasts with the most active <bold>90</bold> showed that the antiplasmodial activity is not specific. However, the structurally similar longicaudatine F (<bold>91</bold>), possessing an open ring in place of the six-membered oxygen heterocycle in <bold>90</bold>, was 40 times more selective against the parasite, despite the slightly lower antiplasmodial activity [<xref ref-type="bibr" rid="CR76">76</xref>]. A phytochemical investigation of <italic>Strychnos icaja</italic> root provided a new bisindole, strychnobaillonine (<bold>93</bold>), and the known strychnohexamine (<bold>94</bold>) (Fig. <xref rid="Fig14" ref-type="fig">14</xref>). The alkaloids were active against the 3D7 strain of <italic>P. falciparum</italic>, and the trisindole <bold>94</bold> was also cytotoxic against WI-38 cells (SI < 10), whereas <bold>93</bold> was not cytotoxic at the highest tested concentration (10 µg/mL) [<xref ref-type="bibr" rid="CR77">77</xref>]. Interestingly, while monomers of <italic>Strychnos</italic> alkaloids do not have antiplasmodial activity, polymerization increases the basic nature of the monomers and confers antiplasmodial potency. This suggests that some degree of basicity is essential for antiparasitic activity of the <italic>Strychnos</italic> alkaloids and that compounds might localize in the parasite acidic digestive vacuole [<xref ref-type="bibr" rid="CR78">78</xref>].<fig id="Fig14"><label>Fig. 14</label><caption><p>Structures of bisindole alkaloids <bold>83</bold>–<bold>94</bold></p></caption><graphic xlink:href="12936_2019_3026_Fig14_HTML" id="MO14"></graphic></fig></p><p id="Par59">It was previously reported that ellipticine (<bold>95</bold>) (Fig. <xref rid="Fig15" ref-type="fig">15</xref>), isolated from <italic>Aspidosperma vargasii</italic> (Apocynaceae) bark, has in vitro and in vivo anti-malarial activity [<xref ref-type="bibr" rid="CR79">79</xref>]. In search of more active analogues, semi-synthetic derivatives of <bold>95</bold> were prepared. 9-Nitroellipticine (<bold>96</bold>), in which ring A was modified, was more active than <bold>95</bold>, while the 7-nitro derivative was the least active [<xref ref-type="bibr" rid="CR80">80</xref>]. The indole-quinazoline alkaloid tryptoquivaline (<bold>97</bold>), obtained from the culture broth of <italic>Neosartorya spinosa</italic> KKU-1NK1 (sexual state of <italic>Aspergillus</italic> fungus species), was active against K1 parasites. The compound was slightly cytotoxic to Vero cells (SI = 25) but was inactive against a panel of cancer cell lines [<xref ref-type="bibr" rid="CR81">81</xref>].<fig id="Fig15"><label>Fig. 15</label><caption><p>Structures of indole derivatives <bold>95</bold>–<bold>97</bold></p></caption><graphic xlink:href="12936_2019_3026_Fig15_HTML" id="MO15"></graphic></fig></p></sec><sec id="Sec9"><title>β-Carbolines</title><p id="Par60">The β-carboline-indole alkaloid hyrtiosulawesine (<bold>98</bold>) (Fig. <xref rid="Fig16" ref-type="fig">16</xref>), isolated from the root of <italic>Aristolochia cordigera</italic> (Aristolochiaceae), inhibited the in vitro viability of <italic>P. falciparum</italic> (3D7) without any toxicity to Hep G2 cells. Similar inhibition of the FcB1 strain was observed with synthetic <bold>98</bold> [<xref ref-type="bibr" rid="CR82">82</xref>]. However, the glucoside derivative of <bold>98</bold> was only half as active as <bold>98</bold> [<xref ref-type="bibr" rid="CR83">83</xref>]. Marinacarboline A (<bold>99</bold>) isolated from <italic>Marinactinospora thermotolerans</italic> SCSIO 00652, an actinomycetes species from South China Sea marine sediments, was 18 times more active against the multi-drug resistant Dd2 strain than against the chloroquine-sensitive 3D7. The compound was not significantly cytotoxic to a panel of tumour cell lines (IC<sub>50</sub> > 50 µM) [<xref ref-type="bibr" rid="CR84">84</xref>]. The New Zealand ascidian <italic>Pseudodistoma opacum</italic> was the source of a new antiplasmodial alkylguanidine-substituted β-carboline alkaloid, opacalin A (<bold>100</bold>). The poor cytotoxicity of <bold>100</bold> against L6 cells indicates a selective antiparasitic activity against the K1 strain [<xref ref-type="bibr" rid="CR85">85</xref>]. β-Carboline-1-propionic acid (<bold>101</bold>) was isolated from the root of <italic>Eurycoma longifolia</italic> (Simaroubaceae), a popular southeast Asian medicinal plant. It exhibited antiplasmodial activity against the 3D7 strain, but the cytotoxicity was not reported [<xref ref-type="bibr" rid="CR86">86</xref>].<fig id="Fig16"><label>Fig. 16</label><caption><p>Structures of β-carbolines</p></caption><graphic xlink:href="12936_2019_3026_Fig16_HTML" id="MO16"></graphic></fig></p></sec><sec id="Sec10"><title>Piperidine, pyridone, and pyrimidine alkaloids</title><p id="Par61">The leaf decoction of <italic>Carica papaya</italic> (Caricaceae), which is traditionally used to treat malaria in Indonesian Papua and Maluku islands, displayed in vitro antiplasmodial activity (51% inhibition at 4.8 µg/mL) [<xref ref-type="bibr" rid="CR87">87</xref>]. Purification of an alkaloid-enriched fraction of the plant leaves yielded the dimeric piperidine alkaloids <bold>102</bold>–<bold>104</bold> (Fig. <xref rid="Fig17" ref-type="fig">17</xref>) as the antiplasmodial principles, while the monomeric carpamic acid and methyl carpamate were inactive. Carpine (<bold>102</bold>), with the best activity, was the major alkaloid, but it was inactive in vivo (11.9% suppression of <italic>P. berghei</italic> parasite at 5 mg/kg). The in vivo activity of a hydroalcoholic extract of papaya leaves suggests that other metabolites in the extracts might potentiate the antiplasmodial activity of the active compounds [<xref ref-type="bibr" rid="CR87">87</xref>]. The observed lack of in vivo efficacy of <bold>102</bold> highlights the complex relationship between metabolites in natural extracts and emphasizes the need to validate in vitro potencies in animal models. Nevertheless, potent and selective activity of compounds can be exploited by medicinal chemistry methods in designing improved analogues. Cassine (<bold>105</bold>) and spectaline (<bold>106</bold>) from <italic>Senna spectabilis</italic> leaf were active against 3D7 <italic>P. falciparum</italic> in vitro. However, the 3-<italic>O</italic>-acetyl semi-synthetic derivatives were less active than the natural piperidine parents [<xref ref-type="bibr" rid="CR88">88</xref>]. Ingamine A (<bold>107</bold>), together with two new ingamine-type piperidine alkaloids, (22<italic>S</italic>)-hydroxyingamine A (<bold>108</bold>) and dihydroingenamine D (<bold>109</bold>), were isolated from the marine sponge <italic>Petrosid Ng5 Sp5</italic>. Compounds <bold>107</bold>–<bold>109</bold> showed sub-micromolar antiplasmodial activity against D6 and W2 parasites without cytotoxicity against cancerous and noncancerous cells at 10 µg/mL [<xref ref-type="bibr" rid="CR89">89</xref>]. An antiplasmodial high-throughput screen of the ethanolic extract of marine sponges from the Solomon Islands identified the active <italic>Heliclona</italic> sp. with an in vitro activity of < 1 µg/mL. Bioassay-guided fractionation of the extract from this sponge led to the isolation of haliclonacyclamine A (<bold>110</bold>). The bis-piperidine <bold>110</bold> was more active against chloroquine-resistant FcB1 than chloroquine-sensitive 3D7 parasites, with low cytotoxicity against MCF7 cancer cells. It suppressed parasitaemia in <italic>Plasmodium vinckei petteri</italic>-infected mice by 45% after 4 days of treatment with 10 mg/kg/day [<xref ref-type="bibr" rid="CR90">90</xref>]. Most of the antiplasmodial piperidine alkaloids mentioned here are cyclic dimers. The potent, selective activity of these compounds makes them attractive as lead templates in anti-malarial drug design.<fig id="Fig17"><label>Fig. 17</label><caption><p>Structures of piperidines <bold>102</bold>–<bold>110</bold>, pyridone <bold>111</bold>, and pyrimidine alkaloid <bold>112</bold></p></caption><graphic xlink:href="12936_2019_3026_Fig17_HTML" id="MO17"></graphic></fig></p><p id="Par62">The new pyridone alkaloid <bold>111</bold> (Fig. <xref rid="Fig17" ref-type="fig">17</xref>), with a 1,4-dihydroxy-5-phenyl-2-pyridinone skeleton, was isolated from the Ascomycetes fungus, <italic>Septoria pistaciarum.</italic> Compound <bold>111</bold> was active against <italic>P. falciparum</italic> D6 and W2 strains, but it was also cytotoxic against Vero cells. Three other analogues without a free <italic>N</italic>-hydroxy group on the pyridone heterocycle were inactive, suggesting a SAR role for substituents on the ring nitrogen [<xref ref-type="bibr" rid="CR91">91</xref>].</p><p id="Par63">The extract of <italic>Biemna laboutei</italic>, a marine sponge collected at Salary Bay in Madagascar, showed antiplasmodial activity with IC<sub>50</sub> of 3.2 µg/mL. Chemical investigation of the active extract yielded new tricyclic pyrimidine alkaloids named netamines. Among the isolated alkaloids, netamine K (<bold>112</bold>), with a Δ<sup>8,8a</sup>-double bond in the tricyclic skeleton, exhibited activity against <italic>P. falciparum</italic> without toxicity to KB cells at the highest tested concentration of 1 µM [<xref ref-type="bibr" rid="CR92">92</xref>].</p></sec><sec id="Sec11"><title>Pyrroles</title><p id="Par64">A series of 14 structurally related bromopyrrole alkaloids (Fig. <xref rid="Fig18" ref-type="fig">18</xref>) derived from sponges of the <italic>Agelas</italic> and <italic>Axinella</italic> genera were assayed for antiplasmodial activity against the K1 strain. Dibromopalau’amine (<bold>113</bold>) had the highest activity against the parasite, although it was also cytotoxic against L6 cells. The slightly less potent spongiadicin B (<bold>114</bold>) and dispacamide B (<bold>115</bold>) were more selective against the parasite (SI = 32.7 and > 67.2, respectively). Preliminary SAR observations in this series indicated that the aminoimidazole ring and the level of oxidation are important for antiplasmodial activity. Analogues lacking the imidazole ring were inactive while those in which the ring is not oxidized were less active. Some bromopyrrole alkaloids inhibited <italic>Plasmodium</italic> type II fatty acid synthase (FAS II) enzyme, suggesting that this might be part of the mechanism of action [<xref ref-type="bibr" rid="CR93">93</xref>]. The new bispyrroloiminoquinone tsitsikammamine C (<bold>116</bold>), with nanomolar antiplasmodial activity against 3D7 and Dd2 <italic>P. falciparum</italic> strains, together with the equally active makaluvamines G (<bold>117</bold>), J–L (<bold>118</bold>–<bold>120</bold>), were isolated from the marine sponge <italic>Zyzzya</italic> sp. [<xref ref-type="bibr" rid="CR94">94</xref>]. Compounds <bold>116</bold> and <bold>118</bold> were equally active against both parasite schizonts and trophozoites. Subcutaneous treatment of <italic>P. berghei</italic> infected mice with <bold>117</bold> at 8 mg/kg/day for 4 days suppressed parasitaemia by 48% with no apparent toxicity to mice. Damirone A (<bold>121</bold>), with a benzoquinone group in place of the iminoquinone moiety of the makaluvamines, was less active, suggesting that the iminoquinone group is crucial for activity. Methylation of the iminium nitrogen led to an increase in activity [<xref ref-type="bibr" rid="CR94">94</xref>]. Bioassay- and LC–MS-guided fractionation of an active extract from the Alaskan-sourced <italic>Latrunculia</italic> sp. sponge yielded discorhabdins A (<bold>122</bold>), and C (<bold>123</bold>), and dihydrodiscorhabdin C (<bold>124</bold>) [<xref ref-type="bibr" rid="CR95">95</xref>]. The most potent pyrroloiminoquinones, <bold>122</bold> and <bold>124</bold>, with nanomolar antiplasmodial activity against D6 and W2 strains, were also the most selective (SI = 130 and 75, respectively). In an in vivo experiment, <italic>P. berghei</italic>-infected mice were treated with <bold>122</bold> and <bold>124</bold> at 10 mg/kg/day and although 50% suppression of parasitaemia was observed with <bold>122</bold> after 2 days of treatment, both compounds resulted in symptoms of severe toxicity [<xref ref-type="bibr" rid="CR95">95</xref>].<fig id="Fig18"><label>Fig. 18</label><caption><p>Structures of pyrrole alkaloids</p></caption><graphic xlink:href="12936_2019_3026_Fig18_HTML" id="MO18"></graphic></fig></p></sec><sec id="Sec12"><title>Other alkaloids</title><p id="Par65">Concoctions prepared from <italic>Buxus</italic> plant species are used for the treatment of malaria in various traditional medicine systems [<xref ref-type="bibr" rid="CR96">96</xref>, <xref ref-type="bibr" rid="CR97">97</xref>]. An alkaloid-enriched fraction from the leaves of <italic>Buxus sempervirens</italic> (Buxaceae), which exhibited selective antiplasmodial activity (IC<sub>50</sub> = 0.36 µg/mL, SI = 20.3), was subjected to bioassay-guided fractionation and yielded the cycloartane alkaloid, <italic>O</italic>-tigloylcyclovirobuxeine B (<bold>125</bold>) (Fig. <xref rid="Fig19" ref-type="fig">19</xref>), as the major antiplasmodial compound. The antiplasmodial activity of <bold>125</bold> against the NF54 strain was slightly less than that of the crude alkaloid fraction, but the compound was not significantly cytotoxic against L6 cells. Compound <bold>125</bold> was also detected in significant quantities in a leaf decoction of <italic>Buxus sempervirens</italic> that was prepared in accordance with ethnobotanical protocols [<xref ref-type="bibr" rid="CR98">98</xref>]. Purification of the chloroform fraction of an extract from the combined twigs, leaves, and fruits of <italic>Buxus cochinchinensis</italic> yielded a number of bioactive triterpenoids, including the cycloartane alkaloid, <italic>N</italic>-benzoyldihydrocyclomicrophylline F (<bold>126</bold>). This compound inhibited both Dd2 <italic>P. falciparum</italic> and HT-29 human colon cancer cells, suggesting non-selective activity [<xref ref-type="bibr" rid="CR99">99</xref>]. Two pregnane-type steroidal alkaloids, mokluangin A (<bold>127</bold>) and irehline (<bold>128</bold>), isolated from the root of <italic>Holarrhena pubescens</italic> (Apocynaceae), were active against K1 <italic>P. falciparum</italic> with low cytotoxicity against NCI-H187 lung cancer cells (IC<sub>50</sub> = 30.6 and 27.7 µM, respectively) [<xref ref-type="bibr" rid="CR100">100</xref>]. Two new cassane diterpene alkaloids, caesalminines A (<bold>129</bold>) and B (<bold>130</bold>) (Fig. <xref rid="Fig19" ref-type="fig">19</xref>), possessing a tetracyclic furanoditerpenoid skeleton were isolated from the seeds of <italic>Caesalpinia minax</italic> (Fabaceae). The compounds, which were proposed to be biosynthetically derived from the aminolysis of the geranylgeranyl pyrophosphate precursor, inhibited K1 <italic>P. falciparum</italic> [<xref ref-type="bibr" rid="CR101">101</xref>].<fig id="Fig19"><label>Fig. 19</label><caption><p>Structures of steroidal alkaloids</p></caption><graphic xlink:href="12936_2019_3026_Fig19_HTML" id="MO19"></graphic></fig></p><p id="Par66">A new Amaryllidaceae alkaloid, (+)-5,6-dehydrolycorine (<bold>131</bold>) (Fig. <xref rid="Fig20" ref-type="fig">20</xref>), isolated from the bulbs of <italic>Lycoris radiata</italic> (Amaryllidaceae), inhibited the in vitro viability of <italic>P. falciparum</italic> (D6 and W2), albeit with associated cytotoxicity against eight human tumour cell lines, indicating non-specific antiparasitic activity [<xref ref-type="bibr" rid="CR102">102</xref>]. Similarly, the macrocyclic lactams cripowellin A–D (<bold>132</bold>–<bold>135</bold>) (Fig. <xref rid="Fig20" ref-type="fig">20</xref>), which were isolated from the alkaloid-enriched extract of <italic>Crinum erubescens</italic> (Amaryllidaceae), inhibited the Dd2 strain with nanomolar IC<sub>50</sub> values but were also cytotoxic against cancerous A2780 cells. Importantly, the presence of the 1,3,5-trioxepane-ring in <bold>132</bold> and <bold>134</bold> correlated with improved activity [<xref ref-type="bibr" rid="CR103">103</xref>]. Another bioassay-guided purification, this time of <italic>Crinim firmifolium</italic> leaf extract, led to the isolation of the new 2-alkylquinolinones <bold>136</bold> and the known <bold>137</bold>, which were both active against the 3D7 and Dd2 strains with mild cytotoxicity against A2780 mammalian ovarian cancer cells [<xref ref-type="bibr" rid="CR104">104</xref>]. Incorporation of a branched alkyl into <bold>137</bold> to form <bold>138</bold> improved antiplasmodial activity, suggesting that branching of the alkyl side chain is beneficial to potency [<xref ref-type="bibr" rid="CR104">104</xref>].<fig id="Fig20"><label>Fig. 20</label><caption><p>Structures of (+)-5,6-dehydrolycorine <bold>131</bold>, lactams <bold>132</bold>–<bold>135</bold> and quinolinone alkaloids <bold>136</bold>–<bold>138</bold></p></caption><graphic xlink:href="12936_2019_3026_Fig20_HTML" id="MO20"></graphic></fig></p><p id="Par67">The bromotyrosine alkaloid psammaplysin H (<bold>139</bold>) was isolated from a marine <italic>Pseudoceratina</italic> sponge together with the known psammaplysin F (<bold>140</bold>), previously isolated from a <italic>Hyattella</italic> sponge, and both exhibited antiplasmodial activity against the 3D7 strain (Fig. <xref rid="Fig21" ref-type="fig">21</xref>) [<xref ref-type="bibr" rid="CR105">105</xref>]. Psammaplysin H (<bold>139</bold>), which has a trimethylated quaternary terminal nitrogen, was not toxic to HEK293 and HepG2 mammalian cells, while <bold>140</bold> suffered from reduced activity coupled with significant cytotoxicity [<xref ref-type="bibr" rid="CR106">106</xref>]. Preliminary SAR studies indicated that substitution on the terminal nitrogen influences the selective antiplasmodial activity. Four other antiplasmodial bromotyrosine derivatives, aplysinone D (<bold>141</bold>), homoaerothionin (<bold>142</bold>), 11,19-dideoxyfistularin 3 (<bold>143</bold>), and 11-hydroxyfistularin (<bold>144</bold>), were isolated from <italic>Suberea ianthelliformis</italic>, a marine sponge from the Solomon Islands. Unfortunately, these compounds were also cytotoxic against Vero cells [<xref ref-type="bibr" rid="CR107">107</xref>].<fig id="Fig21"><label>Fig. 21</label><caption><p>Structures of bromotyrosine alkaloids</p></caption><graphic xlink:href="12936_2019_3026_Fig21_HTML" id="MO21"></graphic></fig></p><p id="Par68">Interrogation of the marine sponge <italic>Monanchora unguiculata</italic>, collected at the Mitsio islands of Madagascar, yielded four new guanidine alkaloids ptilomycalins E–H (<bold>145</bold>–<bold>148</bold>), along with the known crambescidin 800 (<bold>149</bold>) and fromiamycalin (<bold>150</bold>) (Fig. <xref rid="Fig22" ref-type="fig">22</xref>). The compounds exhibited sub-micromolar antiplasmodial activity against the 3D7 strain but were also cytotoxic against KB cells [<xref ref-type="bibr" rid="CR108">108</xref>]. Similarly, four new antiplasmodial tricyclic thiazine alkaloids thiaplakortones A–D (<bold>151</bold>–<bold>154</bold>) (Fig. <xref rid="Fig22" ref-type="fig">22</xref>), isolated from the Australian marine sponge <italic>Plakortis lita</italic>, showed nanomolar inhibition against the 3D7 and Dd2 parasites, with low toxicity to human HEK293 cells (SI = > 62 − > 500) [<xref ref-type="bibr" rid="CR109">109</xref>]. The decalin-tetramic acid metabolite phomasetin (<bold>155</bold>) was obtained following the culturing of the <italic>Pyrenochaetopsis</italic> sp. RK10-F058 fungus. Biological assessment revealed that <bold>155</bold> was active against <italic>P. falciparum</italic> 3D7 with moderate cytotoxicity against cancerous HeLa, HL-60, and src<sup>ts</sup>-NRK cells. The same culture broth yielded two more decalin metabolites, possessing a cyclopentanone-fused decalin skeleton and a serine-derived <italic>N</italic>-methylated amino acid instead of the tetramic acid moiety. However, they were > 21 times less active than <bold>155</bold>, indicating that the cyclized tetramic acid group might be crucial for potent activity [<xref ref-type="bibr" rid="CR110">110</xref>]. Aplidiopsamine A (<bold>156</bold>) (Fig. <xref rid="Fig22" ref-type="fig">22</xref>), with a rare pyrrolo-quinoline conjugated to an adenine nucleobase, was isolated from the Australian ascidian <italic>Aplidiopsis confluata.</italic> The new metabolite was active against the 3D7 and Dd2 strains without significant toxicity against HEK-293 cells [<xref ref-type="bibr" rid="CR111">111</xref>].<fig id="Fig22"><label>Fig. 22</label><caption><p>Structures of guanidines <bold>145</bold>–<bold>150</bold>, thiazines <bold>151</bold>–<bold>154</bold>, phomasetin <bold>155</bold> and aplidiopsamine A <bold>156</bold></p></caption><graphic xlink:href="12936_2019_3026_Fig22_HTML" id="MO22"></graphic></fig></p><p id="Par69">An extract from the leaves of <italic>Prosopis glandulosa</italic> (Fabaceae), collected in Nevada, yielded a new tertiary indolizidine alkaloid Δ<sup>1,6</sup>-juliprosopine (<bold>157</bold>) (Fig. <xref rid="Fig23" ref-type="fig">23</xref>). Interestingly, the leaf extract of the same plant collected in Texas produced the known quaternary alkaloid juliprosine (<bold>158</bold>) but not <bold>157</bold>. The two compounds inhibited the D6 and W2 strains without any toxicity to Vero cells at the highest tested concentration of 23.8 µg/mL [<xref ref-type="bibr" rid="CR112">112</xref>]. Allonorsecurinine (<bold>159</bold>), previously reported as a synthetic compound, was isolated with <italic>ent</italic>-norsecurinine (<bold>160</bold>) from the antiplasmodial plant <italic>Phyllanthus fraternus</italic> (Phyllanthaceae) (methanol extract IC<sub>50</sub> = 0.44 µg/mL against 3D7) [<xref ref-type="bibr" rid="CR113">113</xref>]. The two securinega alkaloids were more active against chloroquine-resistant W2 than against chloroquine-sensitive 3D7 parasites. No cytotoxicity was observed against human umbilical vein endothelial cells at the highest concentration of 100 µM [<xref ref-type="bibr" rid="CR114">114</xref>]. The root bark extract of the Ugandan anti-malarial medicinal plant <italic>Citropsis articulata</italic> (Rutaceae) displayed 77% inhibition of FcB1 <italic>P. falciparum</italic> at 10 µg/mL with low cytotoxicity against Vero cells. A pyranoacridone alkaloid, 5-hydroxynoracronycine (<bold>161</bold>), was isolated as the most active constituent against the same parasite strain. However, the compound was also moderately cytotoxic against Vero cells (SI = 10) [<xref ref-type="bibr" rid="CR115">115</xref>].<fig id="Fig23"><label>Fig. 23</label><caption><p>Structures of other alkaloids <bold>157</bold>–<bold>163</bold></p></caption><graphic xlink:href="12936_2019_3026_Fig23_HTML" id="MO23"></graphic></fig></p><p id="Par70">The polyamine diamide orthidine F (<bold>162</bold>) (Fig. <xref rid="Fig23" ref-type="fig">23</xref>) from the New Zealand-sourced ascidian <italic>Aplidium orthium</italic> was active against K1 <italic>P. falciparum</italic> without cytotoxicity against L6 cells. A synthetic 2-hydroxyphenylacetamide derivative <bold>163</bold> was > 100 times more active while retaining selectivity. Preliminary SAR indicated that the two arylamide terminals and the spermine fragment are essential for antiplasmodial activity. Similarly, the hydroxy group at C-2 of the aromatic rings is important for improved antiplasmodial activity [<xref ref-type="bibr" rid="CR116">116</xref>].</p></sec></sec><sec id="Sec13"><title>Terpenes</title><p id="Par71">Among the 447 isolated natural products with IC<sub>50</sub> ≤ 3.0 µM reported in this review, 30.8% are terpenoids.</p><sec id="Sec14"><title>Monoterpenes</title><p id="Par72">The iridoid specicoside (<bold>164</bold>) (Fig. <xref rid="Fig24" ref-type="fig">24</xref>), isolated from an antiplasmodial ethyl acetate extract of <italic>Kigelia africana</italic> (Bignoniaceae), was active against the <italic>P. falciparum</italic> W2, CAM10 and SHF4 strains without cytotoxicity against LLC/MK-2 cells. Specicoside (<bold>164</bold>) acted in synergy with artemether in inhibiting the W2mef strain but had an antagonistic effect with <italic>p</italic>-hydroxycinnamic acid, which is also present in <italic>Kigelia africana</italic> [<xref ref-type="bibr" rid="CR117">117</xref>, <xref ref-type="bibr" rid="CR118">118</xref>].<fig id="Fig24"><label>Fig. 24</label><caption><p>Structure of specioside</p></caption><graphic xlink:href="12936_2019_3026_Fig24_HTML" id="MO24"></graphic></fig></p></sec><sec id="Sec15"><title>Sesquiterpenes</title><p id="Par73">A phytochemical investigation of the active chloroform extract of <italic>Drimys brasiliensis</italic> (Winteraceae) stem bark (<italic>P. falciparum</italic> FcR3, IC<sub>50</sub> 3.0 µg/mL) led to the isolation of drimane sesquiterpenes but the most active compound was 1β-(<italic>p</italic>-coumaroyloxy)polygodial (<bold>165</bold>) (Fig. <xref rid="Fig25" ref-type="fig">25</xref>) [<xref ref-type="bibr" rid="CR119">119</xref>]. Preliminary antiplasmodial screening of <italic>Salacia longipes</italic> var<italic>. camerunensis</italic> (Celastraceae) seed extract showed that it was active against the W2 strain with an IC<sub>50</sub> of 2.28 µg/mL. Extensive purification of the active extract afforded the β-agarofuran sesquiterpenoids salaterpenes A–D (<bold>166</bold>–<bold>169</bold>) (Fig. <xref rid="Fig25" ref-type="fig">25</xref>), which were also active against W2 parasites [<xref ref-type="bibr" rid="CR120">120</xref>]. The root extract of <italic>Ferula pseudalliacea</italic> (Apiaceae) yielded an antiplasmodial metabolite sanandajin (<bold>170</bold>), the first isolated disesquiterpene-coumarin. This compound, a cadinenyl ester of the sesquiterpene coumarin glabanic acid, inhibited the K1 parasite and had moderate cytotoxicity against L6 cells [<xref ref-type="bibr" rid="CR121">121</xref>].<fig id="Fig25"><label>Fig. 25</label><caption><p>Structures of sesquiterpenes <bold>165</bold>–<bold>176</bold></p></caption><graphic xlink:href="12936_2019_3026_Fig25_HTML" id="MO25"></graphic></fig></p><p id="Par74">The eremophilane sesquiterpenoid sporogen-AO1 (<bold>171</bold>), produced by the soil fungus <italic>Penicillium copticola</italic> PSURSPG138, inhibited K1 parasites but was also cytotoxic against human oral epidermoid carcinoma (KB) and Vero cells [<xref ref-type="bibr" rid="CR122">122</xref>]. The endophytic fungus <italic>Phomopsis archeri</italic>, isolated from <italic>Vanilla albidia</italic> cortex stem, yielded an extract with antiplasmodial activity (IC<sub>50</sub> = 5.0 μg/mL) from which an aromatic sesquiterpene phomoarcherin B (<bold>172</bold>) (Fig. <xref rid="Fig25" ref-type="fig">25</xref>), with antiplasmodial activity but also moderate cytotoxicity against cholangiocarcinoma and KB cells, was isolated [<xref ref-type="bibr" rid="CR123">123</xref>]. The Australian nudibranch <italic>Phyllidia ocellata</italic> has produced three new isonitrile sesquiterpenes, 2-isocyanoclovene (<bold>173</bold>), 2-isocyanoclovane (<bold>174</bold>) and 4,5-<italic>epi</italic>-10-isocyanoisodauc-6-ene (<bold>175</bold>), with selective antiplasmodial activity against the 3D7 and Dd2 strains. The isothiocyanate and formamide analogues were significantly less active, further reinforcing the argument that the isonitrile functionality is crucial for the potent activity of isonitrile terpenes [<xref ref-type="bibr" rid="CR124">124</xref>]. Young et al. adapted a β-haematin inhibition assay to allow for the assaying of small amounts of marine natural products and was able to prove that six terpenoid isonitriles inhibit heme crystallization at different levels [<xref ref-type="bibr" rid="CR125">125</xref>]. The sesquiterpene-derived spiro heterocycle 3,4-dehydrotheaspirone (<bold>176</bold>) (Fig. <xref rid="Fig25" ref-type="fig">25</xref>) has been isolated from <italic>Laumoniera bruceadelpha</italic> (Simaroubaceae) bark extract and was found to inhibit 3D7 parasites selectively [<xref ref-type="bibr" rid="CR126">126</xref>].</p></sec><sec id="Sec16"><title>Sesquiterpene lactones</title><p id="Par75">Many species in the genus <italic>Chloranthus</italic> (Chloranthaceae), known in traditional Chinese medicine as “Sikuaiwa”, have been documented as a treatment for malaria. A library of 44 lindenane-type sesquiterpenoid monomers and dimers isolated from different <italic>Chloranthus</italic> species and <italic>Sarcandra glabra</italic> (Chloranthaceae) were assayed for antiplasmodial activity. Potent activity was observed for twenty-six of the compounds (<bold>177</bold>–<bold>202</bold>) (Fig. <xref rid="Fig26" ref-type="fig">26</xref>). Compounds with IC<sub>50</sub> ≤ 100 nM were also assessed for cytotoxicity on embryonic lung tissue (WI-38) cells, and some compounds, e.g. fortunilide A (<bold>177</bold>), sarglabolide J (<bold>186</bold>), and chlorajaponilide C (<bold>191</bold>) had potencies comparable to that of artemisinin and were not cytotoxic. Preliminary SAR observations indicated that all the active compounds were dimers, had a Δ<sup>4</sup> double bond and a hydroxy group at C-4′, and contain a (<italic>Z</italic>)-5-hydroxy-4-oxopent-2-enoate ester. The presence and nature of the ester groups at C-13′ and C-15′ affected the antiplasmodial activity, suggesting that these ester groups could be manipulated to optimize potency [<xref ref-type="bibr" rid="CR127">127</xref>]. The potent and selective antiplasmodial activity warrants further exploration of this group of compounds.<fig id="Fig26"><label>Fig. 26</label><caption><p>Structures of dimeric sesquiterpene lactones <bold>177</bold>–<bold>202</bold></p></caption><graphic xlink:href="12936_2019_3026_Fig26_HTML" id="MO26"></graphic></fig></p><p id="Par76">Thirteen plants used in Burkina Faso to treat malaria were investigated, and due to the promising in vitro and in vivo anti-malarial activity, <italic>Dicoma tomentosa</italic> (Asteraceae) was selected for further studies [<xref ref-type="bibr" rid="CR128">128</xref>]. Bioassay-guided purification of the whole plant extract yielded the known germacranolide sesquiterpene lactone, urospermal A 15-<italic>O</italic>-acetate (<bold>203</bold>) (Fig. <xref rid="Fig27" ref-type="fig">27</xref>) as the major antiplasmodial compounds. The compound exhibited antiplasmodial activity against the 3D7 and W2 strains without evidence of haemolysis, indicating a direct action on the parasite. However, <bold>203</bold> was cytotoxic against WI38 human fibroblasts SI = 3.3, suggesting non-selective activity [<xref ref-type="bibr" rid="CR129">129</xref>]. The root of an antiplasmodial <italic>Dicoma</italic> species from South Africa, <italic>Dicoma anomala</italic> subsp. <italic>gerrardii</italic> was the source of a eudesmanolide-type sesquiterpene lactone, dehydrobrachylaenolide (<bold>204</bold>), which inhibited D10 <italic>P. falciparum</italic> but was less active against the K1 strain and moderately cytotoxic against CHO cells (SI = 9). Semi-synthetic derivatives of <bold>204</bold>, in which the α-methylene ketone and lactone were reduced, were less active. This indicates that the exocyclic methylene group is essential for activity [<xref ref-type="bibr" rid="CR130">130</xref>]. The dichloromethane extract of <italic>Trichospira verticillata</italic> (Asteraceae) exhibited antiplasmodial activity against Dd2 <italic>P. falciparum</italic> with an IC<sub>50</sub> of approximately 5 µg/mL. Fractionation of the extract afforded the new germacranolide trichospirolide A (<bold>205</bold>) (Fig. <xref rid="Fig27" ref-type="fig">27</xref>) as the most active constituent. However, it was also toxic to A2780 ovarian cancer and HEK293 cells [<xref ref-type="bibr" rid="CR131">131</xref>]. Another antiplasmodial germacranolide, 15-<italic>O</italic>-methylgoyazensolide (<bold>206</bold>), was isolated from the leaf and twig extract of <italic>Piptocoma antillana</italic> (Asteraceae). It was equally active against the Dd2 strain and A2780 human ovarian cancer cells, indicating a non-selective antiplasmodial activity [<xref ref-type="bibr" rid="CR132">132</xref>]. Antiplasmodial screening of 12 plants used in traditional medicine against malaria in Benin resulted in an extract of the aerial parts of <italic>Acanthospermum hispidum</italic> (Asteraceae) with potent activity against 3D7 and W2 parasites (IC<sub>50</sub> = 7.5 and 4.8 µg/mL, respectively) [<xref ref-type="bibr" rid="CR133">133</xref>]. Two acanthospermolide-type sesquiterpene lactones (<bold>207</bold> and <bold>208</bold>) were subsequently isolated as the major antiplasmodial compounds without haemolytic activity [<xref ref-type="bibr" rid="CR134">134</xref>]. Compound <bold>208</bold> was less cytotoxic against WI38 human fibroblasts than <bold>207</bold>, indicating that <bold>208</bold> was more selective in the toxicity to 3D7 parasites [<xref ref-type="bibr" rid="CR134">134</xref>]. Two other sesquiterpene lactones, vernopicrin (<bold>209</bold>) and vernomelitensin (<bold>210</bold>), from <italic>Vernonia guineensis</italic> (Asteraceae) leaves were also active against Dd2 and Hb3 parasite strains without haemolysis [<xref ref-type="bibr" rid="CR135">135</xref>]. The dichloromethane extract of <italic>Eupatorium perfoliatum</italic> (Asteraceae) aerial parts inhibited <italic>P. falciparum</italic> with low cytotoxicity (IC<sub>50</sub> = 2.7 µg/mL and SI = 27). The new dimeric guaianolide, diguaiaperfolin (<bold>211</bold>), was isolated as the main antiplasmodial compound from the active extract, but the compound was moderately cytotoxic against L6 cells (SI = 8) [<xref ref-type="bibr" rid="CR136">136</xref>].<fig id="Fig27"><label>Fig. 27</label><caption><p>Structures of sesquiterpene lactones <bold>203</bold>–<bold>211</bold></p></caption><graphic xlink:href="12936_2019_3026_Fig27_HTML" id="MO27"></graphic></fig></p><p id="Par77">All the different classes of sesquiterpene lactones reported so far exhibited non-selective antiplasmodial activity. The bioactivities of sesquiterpene lactones have been ascribed to the presence of an α-methylene-γ-lactone moiety in the structures. The conjugate Michael acceptor property of this highly reactive functionality allows it to react with the thiol group of crucial cell proteins hence the unselective activity. SAR studies around this enigmatic functionality to make sesquiterpene lactones more selective are essential if these compounds are to enjoy further development as anti-malarial scaffolds.</p></sec><sec id="Sec17"><title>Diterpenes</title><p id="Par78">Three new cassane diterpenes (Fig. <xref rid="Fig28" ref-type="fig">28</xref>) from an active chloroform extract of <italic>Caesalpinia sappan</italic> (Fabaceae) seeds (IC<sub>50</sub> = 0.38 µg/mL against K1), caesalsappanins G–I (<bold>212</bold>–<bold>214</bold>), inhibited K1 <italic>P. falciparum</italic> [<xref ref-type="bibr" rid="CR137">137</xref>]. Cytotoxicity studies against a panel of cancer cell lines showed moderate selectivity for the parasite (SI = 10.5–17.6). The three active compounds have a hydroxy group at C-12, whereas compounds lacking the C-12 hydroxy were less active [<xref ref-type="bibr" rid="CR137">137</xref>]. The dichloromethane extract of <italic>Caesalpinia bonducella</italic> root showed in vivo dose-dependent antiplasmodial activity [<xref ref-type="bibr" rid="CR138">138</xref>]. A phytochemical investigation of the root afforded norcaesalpin D (<bold>215</bold>) as the antiplasmodial component. This cassane diterpenoid was active against 3D7, Dd2, and artemisinin-resistant (IPC 5202 Battambang, IPC 4912 Mondolkiri-Cambodia) strains. No cytotoxicity was observed against mammalian LLC-MK2 cells at the highest concentration (200 µg/mL) tested [<xref ref-type="bibr" rid="CR139">139</xref>].<fig id="Fig28"><label>Fig. 28</label><caption><p>Structures of cassane diterpenes <bold>212</bold>–<bold>215</bold></p></caption><graphic xlink:href="12936_2019_3026_Fig28_HTML" id="MO28"></graphic></fig></p><p id="Par79">The leaf extract of <italic>Aphanamixis grandifolia</italic> (Meliaceae) produced the diterpenoid lactones amphadilactones A–F and H–I (<bold>216</bold>–<bold>223</bold>) (Fig. <xref rid="Fig29" ref-type="fig">29</xref>) [<xref ref-type="bibr" rid="CR140">140</xref>, <xref ref-type="bibr" rid="CR141">141</xref>]. The structures of amphadilactones E and F feature a novel carbon skeleton with a 1,1,2,2-tetrasubstituted cyclobutane moiety. Compounds <bold>216</bold>–<bold>223</bold> inhibited the Dd2 strain with sub-micromolar IC<sub>50</sub> values. The interesting structures and antiplasmodial activity of <bold>216</bold>–<bold>219</bold> have motivated the total synthesis of the compounds [<xref ref-type="bibr" rid="CR142">142</xref>]. Furthermore, compounds <bold>216</bold>–<bold>219</bold> showed potent inhibition of diacylglycerol <italic>O</italic>-acyltransferase-1 (DGAT-1) isozyme. <italic>P. falciparum</italic> encodes only one DGAT enzyme, <italic>Pf</italic>DGAT, and it is necessary for parasite proliferation during the intraerythrocytic stage [<xref ref-type="bibr" rid="CR143">143</xref>]. With the unprecedented carbon frameworks, it is worthwhile to investigate whether the new amphadilactones exert antiplasmodial activity by inhibiting <italic>Pf</italic>DGAT [<xref ref-type="bibr" rid="CR140">140</xref>, <xref ref-type="bibr" rid="CR141">141</xref>]. The hexane and dichloromethane bark extracts of <italic>Cupania cinerea</italic> (Sapindaceae), an Ecuadorian ethnobotanical plant, were active against <italic>P. falciparum</italic> K1 strain (IC<sub>50</sub> = 2.9 and 3.1 µg/mL, respectively) [<xref ref-type="bibr" rid="CR144">144</xref>]. Subsequent bioassay-guided purification of the extracts yielded the new linear diterpenoid glycosides cupacinoside (<bold>224</bold>) and 6′-de-<italic>O</italic>-acetylcupacinoside (<bold>225</bold>), both displaying antiplasmodial activity against K1 parasites but also cytotoxicity against L6 cells [<xref ref-type="bibr" rid="CR145">145</xref>].<fig id="Fig29"><label>Fig. 29</label><caption><p>Structures of diterpenes <bold>216</bold>–<bold>225</bold></p></caption><graphic xlink:href="12936_2019_3026_Fig29_HTML" id="MO29"></graphic></fig></p><p id="Par80">The serrulatane diterpenoid <bold>226</bold>, which was isolated from the aerial parts of <italic>Eremophila microtheca</italic> (Scrophulariaceae), was not active at 10 µM against <italic>P. falciparum</italic>. However, a semi-synthetic amide derivative <bold>227</bold> exhibited antiplasmodial activity against the 3D7 and Dd2 strains without being cytotoxic to HEK293 cells at 80 µM [<xref ref-type="bibr" rid="CR146">146</xref>]. Two new pre-segetane and jatrophane diterpenoids euphorbesulins A (<bold>228</bold>) and G (<bold>229</bold>) (Fig. <xref rid="Fig30" ref-type="fig">30</xref>), from the twigs of <italic>Euphorbia esula</italic> (Euphorbiaceae), have also shown activity against the <italic>P. falciparum</italic> Dd2 strain [<xref ref-type="bibr" rid="CR147">147</xref>]. Antiplasmodial screening of 150 Iranian ethnomedicinal plants identified <italic>Salvia sahendica</italic> (Lamiaceae) hexane root extract with potent activity against the K1 strain (70% inhibition at 0.85 µg/mL) [<xref ref-type="bibr" rid="CR148">148</xref>]. A subsequent phytochemical investigation led to the isolation of abietane diterpenoids as the bioactive constituents and ferruginol (<bold>230</bold>), Δ<sup>9</sup>-ferruginol (<bold>231</bold>), and 7α-acetoxyroyleanone (<bold>232</bold>) inhibited K1 parasites. However, <bold>232</bold> was also toxic to L6 cells, indicating a non-selective antiplasmodial activity. Chemical modifications, which included deacetylation and dehydrogenation of ring B, and hydroxylation of the benzoquinone ring of <bold>232</bold>, led to a reduction in activity without improving selectivity [<xref ref-type="bibr" rid="CR148">148</xref>]. However, the semi-synthetic phthalimide derivative <bold>233</bold> of ferruginol had an improved selective antiplasmodial activity. Preliminary SAR studies of a library of semi-synthetic derivatives of ferruginol indicated that a hydroxy group at C-12 is beneficial for activity while an acetate group at C-12 reduced the activity against the K1 strain, but improved the activity against the 3D7 strain. Chlorination of the phthalimide group was detrimental to activity [<xref ref-type="bibr" rid="CR149">149</xref>].<fig id="Fig30"><label>Fig. 30</label><caption><p>Structures of diterpenes <bold>226</bold>–<bold>233</bold></p></caption><graphic xlink:href="12936_2019_3026_Fig30_HTML" id="MO30"></graphic></fig></p><p id="Par81">A marine sponge from Thailand, <italic>Stylissa cf. massa</italic>, has produced some bifunctionalized amphilectane diterpenoids. The most active metabolite, 8-isocyano-15-formamidoamphilect-11(20)-ene (<bold>234</bold>) (Fig. <xref rid="Fig31" ref-type="fig">31</xref>), exhibited antiplasmodial activity against the K1 strain and was not cytotoxic against MCF-7 breast cancer cells. Analogues bearing an isocyanate and isothiocyanate functionalities were up to ten times less active, indicating that the isonitrile group improved activity. Also, an analogue with only the formamide functional group but lacking an isonitrile group, was not active against <italic>P. falciparum</italic>, suggesting that the formamide group does not contribute to antiplasmodial activity [<xref ref-type="bibr" rid="CR150">150</xref>]. Two more isonitrile amphilectanes, monamphilectines B (<bold>235</bold>) and C (<bold>236</bold>), were isolated from the Carribean marine sponge <italic>Svenzea flava</italic> collected off the coast of Puerto Rico [<xref ref-type="bibr" rid="CR151">151</xref>]. The new metabolites were described as the first marine natural products with an α-substituted monocyclic β-lactam ring. The compounds were active against the 3D7 parasites with nanomolar IC<sub>50</sub> values. Interestingly, 8,15-diisocyano-11(20)-amphilectene (<bold>237</bold>), which differs from the new compound by the absence of the substituted β-lactam moiety, was also active, which suggests that the β-lactam moiety does not contribute to antiplasmodial potency and further confirms the crucial role of the isocyanide (isonitirile) functionality [<xref ref-type="bibr" rid="CR151">151</xref>]. Potent antiplasmodial activity against W2 parasites was also reported for monamphilectine A (<bold>238</bold>), with an unsubstituted β-lactam ring [<xref ref-type="bibr" rid="CR152">152</xref>]. Pustulosaisonitrile-1 (<bold>239</bold>), which was isolated from the Australian nudibranch <italic>Phyllidiella pustulosa</italic>, exhibited antiplasmodial activity against 3D7 and Dd2 <italic>P. falciparum</italic> strains [<xref ref-type="bibr" rid="CR153">153</xref>]. Diastereoisomers of <bold>239</bold>, obtained by enantio- and stereoselective total synthesis, were as active as the natural compound, but also showed cross-resistance [<xref ref-type="bibr" rid="CR153">153</xref>]. The antiplasmodial activity of isonitrile terpenoids has been demonstrated to be due to inhibition of haemozoin formation [<xref ref-type="bibr" rid="CR125">125</xref>, <xref ref-type="bibr" rid="CR154">154</xref>]. Therefore, further development of this class of compound will depend on the ability to avoid cross-resistance. A new linear diterpenoid, bifurcatriol (<bold>240</bold>), featuring two stereogenic centres, was isolated from the Irish brown alga <italic>Bifurcaria bifurcata</italic> and was active against K1 <italic>P. falciparum</italic> with negligible cytotoxicity against L6 cells [<xref ref-type="bibr" rid="CR155">155</xref>].<fig id="Fig31"><label>Fig. 31</label><caption><p>Structures of isocyano diterpenes <bold>234</bold>–<bold>239</bold> and bifurcatriol</p></caption><graphic xlink:href="12936_2019_3026_Fig31_HTML" id="MO31"></graphic></fig></p><p id="Par82">The stem extract of <italic>Drypetes gerrardii</italic> var <italic>gerrardii</italic> (Putranjivaceae) exhibited potent antiplasmodial activity against <italic>P. falciparum</italic> (IC<sub>50</sub> = 0.5 µg/mL). Two new metabolites, the diterpene-derived phenanthrenone drypetenone D (<bold>241</bold>) and phenanthrenone heterodimer drypetenone E (<bold>242</bold>) (Fig. <xref rid="Fig32" ref-type="fig">32</xref>), were subsequently isolated from this extract. These compounds were active against the NF54 strain with low cytotoxicity against L6 cells (SI = 71 and 31, respectively). However, the more active and selective monomer <bold>241</bold> did not show in vivo activity in <italic>P. berghei</italic>-infected mice [<xref ref-type="bibr" rid="CR156">156</xref>]. The phenanthrenone derivatives fimbricalyx A (<bold>243</bold>) and B (<bold>244</bold>), isolated from <italic>Strophioblachia fimbricalyx</italic> (Euphorbiaceae) root, also inhibited <italic>P. falciparum</italic> K1. Interestingly, the new fimbricalyx B exhibited nanomolar antiplasmodial activity, better than mefloquine, without being cytotoxic against Vero and human cancerous cells at 10 µM [<xref ref-type="bibr" rid="CR157">157</xref>].<fig id="Fig32"><label>Fig. 32</label><caption><p>Structures of other diterpenoids</p></caption><graphic xlink:href="12936_2019_3026_Fig32_HTML" id="MO32"></graphic></fig></p></sec><sec id="Sec18"><title>Triterpenes</title><p id="Par83">The chloroform extract of a combination of <italic>Buxus cochinchinensis</italic> (Buxaceaea) leaves, twigs, and fruits yielded five betulin coumaroyl esters (<bold>245</bold>–<bold>249</bold>) (Fig. <xref rid="Fig33" ref-type="fig">33</xref>) [<xref ref-type="bibr" rid="CR99">99</xref>]. The lupane esters <bold>245, 248</bold>, and <bold>249</bold> were also isolated from the methanolic supercritical fluid extract of <italic>B. sempervirens</italic> together with five other new coumaroyl and feruloyl esters of betulin (<bold>250</bold>–<bold>254</bold>) [<xref ref-type="bibr" rid="CR158">158</xref>]. The coumaroyl and feruloyl esters have either a <italic>Z</italic>- or <italic>E</italic>-configuration and are attached to betulin at either C-3 or C-23. The esters were active against <italic>P. falciparum</italic> Dd2, HB3, and NHP1337 strains without cytotoxicity against HeLa cells. Ester <bold>250</bold>, with an <italic>E</italic>-feruloyl group attached at C-23, was the most active with sub-micromolar IC<sub>50</sub> values, whereas analogues with <italic>E</italic> or <italic>Z</italic> coumaroyl or <italic>Z</italic>-feruloyl at C-23 were slightly less active. Also, C-3 modified analogues were less active than the C-23 modified counterparts. These observations identify the importance of the <italic>E</italic>-feruloyl moiety and suggest that modification at C-23 is more advantageous for activity. Importantly, the esterified betulin derivatives were more active than betulin and 23-hydroxybetulin, and the diacetate ester was inactive [<xref ref-type="bibr" rid="CR99">99</xref>, <xref ref-type="bibr" rid="CR158">158</xref>]. Betulone (<bold>255</bold>), isolated from the bark of <italic>Cupania cinerea</italic> (Sapindaceae), inhibited <italic>P. falciparum</italic> K1 and had moderate cytotoxicity against L6 cells [<xref ref-type="bibr" rid="CR145">145</xref>].<fig id="Fig33"><label>Fig. 33</label><caption><p>Structures of betulin derivatives</p></caption><graphic xlink:href="12936_2019_3026_Fig33_HTML" id="MO33"></graphic></fig></p><p id="Par84">Happi et al. investigated the chemical constituents of <italic>Entandrophragma congoense</italic> (Meliaceae) bark, a plant used in Cameroonian traditional medicine against malaria. They isolated the apotirucallane triterpenoids prototiamins A–G (<bold>256</bold>–<bold>262</bold>) and the known <bold>263</bold> as the major constituents, and gladoral A (<bold>264</bold>) was obtained as a minor metabolite (Fig. <xref rid="Fig34" ref-type="fig">34</xref>) [<xref ref-type="bibr" rid="CR159">159</xref>]. The compounds displayed antiplasmodial activity against NF54 <italic>P. falciparum</italic> strain with varying levels of toxicity to L6 cells (SI = 4–107). Triterpenoid <bold>256</bold>, with a sub-micromolar IC<sub>50</sub> value, was the most selective against the parasite [<xref ref-type="bibr" rid="CR160">160</xref>, <xref ref-type="bibr" rid="CR161">161</xref>]. Comparing the activities of the compounds allowed some preliminary SAR assumptions. Compounds <bold>256</bold> and <bold>257</bold> differ only in the orientation of the hydroxy group at C-24 and presence or absence of acetylation at C-7 of ring B. Analogue <bold>256</bold>, with an α-oriented OH group and acetylation of the OH at C-7, was twice as active and four times more selective than <bold>257</bold>. Compound <bold>258</bold>, which has a similar structure to <bold>256</bold> but with an epoxide ring between C-24 and C-25 instead of the free α-OH in <bold>256</bold>, was > 8 times less selective. These observations suggest a SAR role for these positions that could be exploited further to optimize potency and selectivity. Another tirucallane triterpenoid, isoflindissone lactone (<bold>265</bold>), was isolated from the dichloromethane extract of <italic>Boswellia serrata</italic> (Burseraceae) oleo-gum resin by bioassay-guided purification of an extract that inhibited <italic>P. falciparum</italic> with IC<sub>50</sub> = 2.6 µg/mL. Compound <bold>265</bold> was active against the NF54 parasite strain with low toxicity against L6 cells (IC<sub>50</sub> = 40 µM) [<xref ref-type="bibr" rid="CR162">162</xref>]. The ethyl acetate stem bark extract of <italic>Kigelia africana</italic> (Bignoniaceae) inhibited <italic>P. falciparum</italic> W2 strain and two field isolates, CAM10 and SHF4 (IC<sub>50</sub> = 11.15, 4.74 and 3.91 µg/mL, respectively). Phytochemical investigations of this active extract yielded the known triterpenoid <bold>266</bold> alongside other metabolites. Compound <bold>266</bold> was active against the W2 and CAM10 strains, with moderate cytotoxic against monkey kidney (LLC-MK2) cells (IC<sub>50</sub> = 9.4 µg/mL) [<xref ref-type="bibr" rid="CR117">117</xref>]. A synergistic effect was observed with a combination of <bold>266</bold> and artemether on the W2mef parasite strain, but the compound had an antagonistic effect with quinine [<xref ref-type="bibr" rid="CR118">118</xref>].<fig id="Fig34"><label>Fig. 34</label><caption><p>Structures of triterpenes <bold>256</bold>–<bold>266</bold></p></caption><graphic xlink:href="12936_2019_3026_Fig34_HTML" id="MO34"></graphic></fig></p><p id="Par85">Bioassay-guided fractionation of the methanol extract of the aerial parts of <italic>Momordica balsamina</italic> (Cucurbitaceae) afforded the new curcurbitacin balsaminol F (<bold>267</bold>), the glycoside balsaminoside B (<bold>268</bold>), and the known kuguaglycoside A (<bold>269</bold>) (Fig. <xref rid="Fig35" ref-type="fig">35</xref>). Glycosides <bold>268</bold> and <bold>269</bold> displayed antiplasmodial activity against the 3D7 and Dd2 strains, while the aglycone <bold>267</bold> was much less active. This suggests that the sugar unit is beneficial to the antiplasmodial activity. However, the compounds were not selective when the cytotoxicity against MCF-7 breast cancer cells is compared to the antiplasmodial activity. Interestingly, the triacetyl semi-synthetic derivative <bold>270</bold> of balsaminol F was 22 and 50 times (for 3D7 and Dd2, respectively) more active than the parent compound without cytotoxicity against MCF-7 cells. However, the activity was lost with the corresponding tribenzoyl ester derivative of balsaminol F [<xref ref-type="bibr" rid="CR163">163</xref>]. Similar improvement in potency and selectivity was observed when karavilagenin C (<bold>271</bold>), which was isolated from <italic>Momordica balsamina</italic>, and was esterified at C-3 and/or C-23 to give different alkanoyl and benzoyl/cinnamoyl derivatives. For the alkanoyl analogues, the diacetyl and dipropanoyl derivatives were more active than the mono analogues, while the monobutanoyl compound was more active than the dibutanoyl counterpart. Moreover, all the mono-aroyl/cinnamoyl derivatives were superior compared to the diaroyl/cinnamoyl counterparts [<xref ref-type="bibr" rid="CR164">164</xref>]. These observations allow the conclusion that for bulky groups, mono-esterification is optimal for activity, while di-esterification is favoured for the smaller groups. It will be worthwhile to study the preferred point of esterification for the monoesters.<fig id="Fig35"><label>Fig. 35</label><caption><p>Structures of triterpenes <bold>267</bold>–<bold>280</bold></p></caption><graphic xlink:href="12936_2019_3026_Fig35_HTML" id="MO35"></graphic></fig></p><p id="Par86">The root bark of <italic>Greenwayodendron suaveolens</italic> (Annonaceae) afforded polycarpol (<bold>272</bold>) as one of the active metabolites against K1 <italic>P. falciparum</italic>, but it was also cytotoxic against MRC-5 cells (SI = < 1) [<xref ref-type="bibr" rid="CR69">69</xref>]. Antiplasmodial assay of 14 Kenyan medicinal plants identified the methanol root bark extract of <italic>Turraea robusta</italic> (Meliaceae) as the most active against NF54 and K1 parasites (IC<sub>50</sub> = 2.4 and 3.5 µg/mL, respectively) [<xref ref-type="bibr" rid="CR165">165</xref>]. Azadironolide (<bold>273</bold>) was subsequently isolated as the most active antiplasmodial compound from the plant stem bark with moderate cytotoxicity against Vero cells [<xref ref-type="bibr" rid="CR166">166</xref>]. An ethnomedicinal survey of plant use in the Northern sector of Kibale National Park in western Uganda indicated that <italic>Neoboutonia macrocalyx</italic> (Euphorbiaceae) is used to treat malaria [<xref ref-type="bibr" rid="CR167">167</xref>]. Chemical investigation of the plant leaf afforded the new cycloartane triterpenoids neomacrolactone (<bold>274</bold>), 22α-acetoxyneomacrolactone (<bold>275</bold>), 6-hydroxyneomacolactone (<bold>276</bold>), 22α-acetoxy-6-hydroxyneomacrolactone (<bold>277</bold>), and 4-methylene-neomacrolactone (<bold>278</bold>), and the previously reported 22-de-<italic>O</italic>-acetyl-26-deoxyneoboutomellerone (<bold>279</bold>) (Fig. <xref rid="Fig35" ref-type="fig">35</xref>). These compounds exhibited antiplasmodial activity against FcB1 <italic>P. falciparum</italic>, but were generally cytotoxic against KB and MRC-5 cells. Interestingly, neomacroin (<bold>280</bold>) with an open ring A, thus lacking an α,β-unsaturated carbonyl conjugated to the cyclopropane ring, showed low cytotoxicity but was slightly less potent (IC<sub>50</sub> = 3.2 µM) [<xref ref-type="bibr" rid="CR168">168</xref>]. Two novel triterpenoids, salvadione C (<bold>281</bold>) and perovskone B (<bold>282</bold>) (Fig. <xref rid="Fig36" ref-type="fig">36</xref>), with rare carbon skeletons, were isolated from an antiplasmodial hexane extract of <italic>Salvia hydrangea</italic> (Lamiaceae). The antiplasmodial activity against K1 parasites was selective when compared to cytotoxicity against L6 cells. The rare carbon scaffolds can be rationalized by a Diels–Alder-type addition of an acyclic monoterpene to a diterpenoid. The monoterpene in the case of <bold>281</bold> is myrcene and <italic>trans</italic>-β-ocimene for <bold>282</bold>, and the additional oxepane ring in <bold>281</bold> confers structural rigidity. These structural types were only previously reported in salvadiol from <italic>Salvia bucharica</italic> and perovskone from <italic>Perovskia abrotanoides</italic> (Lamiaceae) [<xref ref-type="bibr" rid="CR169">169</xref>]. Three new triterpenoid saponins, maesargentoside I, III, IV (<bold>283</bold>–<bold>285</bold>) from the leaf extract of <italic>Maesa argentea</italic> (Myrsinaceae) have displayed non-selective antiplasmodial activity against K1 <italic>P. falciparum</italic> [<xref ref-type="bibr" rid="CR170">170</xref>]. The medicinal mushroom <italic>Ganoderma boninense</italic> produced a new nortriterpenoid with a 3,4-seco-27-norlanostane rearranged skeleton. The metabolite ganoboninketal C (<bold>286</bold>) inhibited <italic>P. falciparum</italic> 3D7 strain with low cytotoxicity against A549 cells [<xref ref-type="bibr" rid="CR171">171</xref>]. The antiplasmodial activity of squalene (<bold>287</bold>), isolated from <italic>Uapaca paludosa</italic> (Euphorbiaceae) trunk bark extract, was reported for the first time. However, it was also cytotoxic against KB and Vero cells [<xref ref-type="bibr" rid="CR172">172</xref>].<fig id="Fig36"><label>Fig. 36</label><caption><p>Structures of other triterpenes</p></caption><graphic xlink:href="12936_2019_3026_Fig36_HTML" id="MO36"></graphic></fig></p><p id="Par87">The ethyl acetate extract of the soil fungus <italic>Neosartorya tatenoi</italic> KKU-2NK23 exhibited antiplasmodial activity (IC<sub>50</sub> = 3.09 µg/mL). A chemical investigation of the fungal material yielded the known meroterpenoid aszonapyrone A (<bold>288</bold>) (Fig. <xref rid="Fig36" ref-type="fig">36</xref>). The compound was active against the K1 strain with low cytotoxicity against KB cells (IC<sub>50</sub> = 48.18 µg/mL). However, the compound was cytotoxic against cancerous NCI-H187 cells, suggesting some level of selectivity in the toxicity to cells. An analogue of <bold>288</bold>, which had a free hydroxy group at C-3 instead of the acetoxy in <bold>288</bold>, was inactive, suggesting a SAR role at this position and indicating that acetylation of the free hydroxy is beneficial to activity [<xref ref-type="bibr" rid="CR173">173</xref>].</p></sec><sec id="Sec19"><title>Steroids</title><p id="Par88">An analysis of 65,000 small molecules using the in silico similarity ensemble approach (SEA), predicted antiplasmodial activity for selected physalins. Physalins B, D, F, and G were then isolated from <italic>Physalis angulata</italic> (Solanaceae) and evaluated for in vitro and in vivo anti-malarial activity. Physalins B (<bold>289</bold>) and F (<bold>290</bold>) (Fig. <xref rid="Fig37" ref-type="fig">37</xref>) had in vitro activity against W2 parasite but were also cytotoxic (SI = 12 and 6, respectively). Interestingly, all the mice treated with <bold>290</bold> died from an exacerbated infection due to the increase in parasitaemia that was attributed to an immunosuppressive effect of the compound. However, physalin D (<bold>291</bold>), without the immunosuppressive effect, decreased parasitaemia in <italic>P. berghei</italic> infected mice by 65% at 100 mg/kg [<xref ref-type="bibr" rid="CR174">174</xref>]. The <italic>n</italic>-butanol fraction of <italic>Caesalpinia volkensii</italic> (Fabaceae) methanol stem bark extract inhibited <italic>P. falciparum</italic> D6 and W2 strains (IC<sub>50</sub> = 4.5 and 1.3 µg/mL, respectively) better than the less polar fractions. Bioassay-guided purification led to the isolation of the new steroid glycoside 3-<italic>O</italic>-[β-glucopyranosy-(1 → 2)-<italic>O</italic>-β-xylopyranosyl]stigmasterol (<bold>292</bold>) with antiplasmodial activity against the D6 and W2 strains. Crucially, the aglycone, which was isolated from the chloroform fraction, was inactive, suggesting that the two sugars potentiate antiplasmodial activity [<xref ref-type="bibr" rid="CR175">175</xref>]. The marine red alga <italic>Halymenia floresii</italic> has produced a new steroid, halymeniaol (<bold>293</bold>), which inhibited 3D7 <italic>P. falciparum</italic> and was not cytotoxic [<xref ref-type="bibr" rid="CR176">176</xref>]. Chemical reinvestigation of the Caribbean sponge <italic>Pandaros acanthifolium</italic> has yielded two new steroid glycosides, pandaroside G (<bold>294</bold>) and pandaroside G methyl ester (<bold>295</bold>). The two compounds were active against the K1 strain as well as cytotoxic against L6 cells, indicating non-selective toxicity. The compounds did not inhibit recombinant <italic>P. falciparum</italic> fatty acid biosynthesis enzymes at the highest tested concentration (20 µg/mL) [<xref ref-type="bibr" rid="CR177">177</xref>].<fig id="Fig37"><label>Fig. 37</label><caption><p>Structures of steroids</p></caption><graphic xlink:href="12936_2019_3026_Fig37_HTML" id="MO37"></graphic></fig></p></sec><sec id="Sec20"><title>Limonoids</title><p id="Par89">African great apes such as Chimpanzees have been observed to ingest the non-nutritional bitter bark and sap of <italic>Khaya anthotheca</italic> (Meliaceae) in the wild, and it has been proposed that this unusual feeding is for medicinal purposes [<xref ref-type="bibr" rid="CR178">178</xref>, <xref ref-type="bibr" rid="CR179">179</xref>]. In an effort to identify bioactive constituents from this plant, the seed petroleum ether extract was tested against <italic>P. falciparum</italic> and showed good activity (IC<sub>50</sub> = 0.96 µg/mL). Bioassay-guided purification of the extract yielded the known limonoids grandifolione (<bold>296</bold>) and 7-deacetylkhivorin (<bold>297</bold>) (Fig. <xref rid="Fig38" ref-type="fig">38</xref>) as the active antiplasmodial constituents. The compounds inhibited the K1 strain, and <bold>296</bold> was less toxic towards L6 cells than <bold>297</bold>, SI = 64 and 11, respectively [<xref ref-type="bibr" rid="CR180">180</xref>]. Two new antiplasmodial limonoids, kostchyienones A (<bold>298</bold>) and B (<bold>299</bold>), were isolated from the root extract of <italic>Pseudocedrela kostchyi</italic> (Meliaceae). Previous investigations indicated that the extract inhibited <italic>P. falciparum</italic> schizont development [<xref ref-type="bibr" rid="CR181">181</xref>]. Antiplasmodial activity of the new compounds against 3D7 and <italic>Pf</italic>INDO strains was selective, and the compounds were not toxic to HEK239T cells (IC<sub>50</sub> > 200 µg/mL). The antiplasmodial activity of limonoids has been attributed to the presence of the α, β-unsaturated carbonyl moiety in the structures, which may be involved in Michael-type addition reactions [<xref ref-type="bibr" rid="CR182">182</xref>].<fig id="Fig38"><label>Fig. 38</label><caption><p>Structures of limonoids</p></caption><graphic xlink:href="12936_2019_3026_Fig38_HTML" id="MO38"></graphic></fig></p></sec><sec id="Sec21"><title>Quassinoids</title><p id="Par90">The leaf of the tropical Amazonian medicinal plant <italic>Quassia amara</italic> (Simaroubaceae) is used traditionally by people in French Guinea for the preparation of popular anti-malarial remedies, alone or in combination with other plants [<xref ref-type="bibr" rid="CR183">183</xref>]. The plant leaf extract was prepared according to traditional instructions and found to be active against <italic>P. falciparum</italic> in vitro and in vivo, without signs of general toxicity [<xref ref-type="bibr" rid="CR184">184</xref>]. The known quassinoid simalikalactone D (<bold>300</bold>) (Fig. <xref rid="Fig39" ref-type="fig">39</xref>), identified as the main antiplasmodial component of <italic>Quassia amara</italic>, had an IC<sub>50</sub> of 10 nM against the FcB1 parasite and showed in vivo efficacy (oral) [<xref ref-type="bibr" rid="CR185">185</xref>]. The known cytotoxicity of quassinoids prompted investigations into the toxicity of <bold>300</bold>. The compound displayed antiproliferative activity against cancerous KB cells (IC<sub>50</sub> = 6.3 nM) but was less cytotoxic against HeLa and noncancerous Vero cells (IC<sub>50</sub> = 2 and 10 µM, respectively). Similarly, Raji B cells mitotic activity was inhibited at concentrations larger than 45 nM, but no apoptosis or necrosis was observed at a concentration of up to 200 µM of <bold>300</bold>. The compound did not inhibit heme crystallization or parasite-induced host erythrocyte membrane permeability. Moreover, <bold>300</bold> showed a stage-specific activity by inhibiting DNA replication in mature trophozoites. An additive effect was observed in combination studies with <bold>300</bold> and the traditional anti-malarials chloroquine, artemisinin, and analogues. Interestingly, a synergistic effect was observed with atovaquone, opening the possibility of combination therapy to combat drug resistance and mitigate toxicity [<xref ref-type="bibr" rid="CR186">186</xref>]. Two more quassinoid metabolites of <italic>Quassia amara</italic>, quassin (<bold>301</bold>) and neo-quassin (<bold>302</bold>), isolated from the stem bark, inhibited the MRC-pf-20 and MRC-pf-303 strains. However, the two compounds and the control (artesunate) were less active than the crude stem bark extract (IC<sub>50</sub> = 0.0025 µg/mL), and the extract was not toxic to mice. A combination treatment with artesunate and <bold>301</bold> or <bold>302</bold> showed synergism at a ratio of 1:2 and additive interaction at a 2:1 ratio; a similar result was obtained when <bold>301</bold> and <bold>302</bold> were combined [<xref ref-type="bibr" rid="CR187">187</xref>]. These findings suggest that other metabolites in the stem bark extract might potentiate the antiplasmodial activity of these two compounds. The frequent ethnomedicinal usage, superior activity, and general lack of toxicity of <italic>Quassia amara</italic> extract make it an attractive herbal anti-malarial remedy worthy of further development. The acetone stem extract of <italic>Brucea javanica</italic> (Simaroubaceae) produced the antiplasmodial quassinoids bruceine D (<bold>303</bold>), and H (<bold>304</bold>) (Fig. <xref rid="Fig39" ref-type="fig">39</xref>). Bruceine D (<bold>303</bold>) was also isolated from the roots of the plant. Both compounds inhibited <italic>P. falciparum</italic> K1 strain, but <bold>303</bold> was also cytotoxic against cancerous human KB and NCI-H187 cells [<xref ref-type="bibr" rid="CR188">188</xref>, <xref ref-type="bibr" rid="CR189">189</xref>]. <italic>Eurycoma longifolia</italic> (Simaroubaceae) root extract yielded the new 18-dehydro-6α-hydroxyeurycomalactone (<bold>305</bold>), alongside known eurycomanone (<bold>306</bold>) and eurycomanol (<bold>307</bold>), with nanomolar antiplasmodial activity [<xref ref-type="bibr" rid="CR86">86</xref>]. The bioactivity of quassinoids has been correlated with the presence of an α,β-unsaturated ketone in ring A. Quassinoids possessing an oxymethylene bridge joining C-8 and C-13 have also shown pronounced activity [<xref ref-type="bibr" rid="CR188">188</xref>]. These two structural features are considered essential for potent antiplasmodial activity but might also be responsible for the cytotoxicity of the compounds. Furthermore, hydroxy groups at C-11 and C-12 have been implicated in the cytotoxicity of quassinoids [<xref ref-type="bibr" rid="CR189">189</xref>]. Thus, medicinal chemistry approaches could be employed to optimize the antiplasmodial activity and reduce cytotoxicity of this class of compounds, especially since there might be a different mechanism of action from the traditional anti-malarials.<fig id="Fig39"><label>Fig. 39</label><caption><p>Structures of quassinoids</p></caption><graphic xlink:href="12936_2019_3026_Fig39_HTML" id="MO39"></graphic></fig></p></sec></sec><sec id="Sec22"><title>Polyphenols</title><p id="Par91">Among the 447 isolated natural products with IC<sub>50</sub> ≤ 3.0 µM reported in this review, 17.4% are polyphenols.</p><sec id="Sec23"><title>Biflavonoids</title><p id="Par92">Traditional healers in Congo-Kinshasa claim that the chewing of <italic>Garcinia kola</italic> (Clusiaceae) nuts in small quantities daily can ward off malaria. This ethnomedicinal use was validated by the activity of seed extracts against <italic>P. falciparum</italic> in vitro and <italic>P. berghei</italic> in vivo [<xref ref-type="bibr" rid="CR190">190</xref>, <xref ref-type="bibr" rid="CR191">191</xref>]. Moreover, 5 µg/mL of a 70% ethanolic extract of the seed inhibited <italic>P. falciparum</italic> by 87%. Subsequent bioassay-guided fractionation led to the isolation of three biflavanones GB1a (<bold>308</bold>), GB1 (<bold>309</bold>), and GB2 (<bold>310</bold>) (Fig. <xref rid="Fig40" ref-type="fig">40</xref>), as the antiplasmodial principles. All three compounds exhibited sub-micromolar antiplasmodial activity against the FCR3 strain with low cytotoxicity against cancerous KB3-1 cells (SI = 77 to 900). In vivo treatment of <italic>P. berghei</italic>-infected mice with 100 mg/kg of the principal and most active constituent, <bold>309</bold>, led to 52% suppression of parasites. The compound was orally active, which is crucial for an anti-malarial lead, and no visible signs of toxicity were observed in the treated mice [<xref ref-type="bibr" rid="CR192">192</xref>]. Another biflavonoid, volkensiflavone (<bold>311</bold>), with antiplasmodial activity against the F32 and FcM29 <italic>P. falciparum</italic> strains, was isolated from <italic>Allanblackia floribunda</italic> (Clusiaceae). Two structural analogues of <bold>311</bold> with an additional hydroxy at C-3′ on the lower flavone unit were > 10 times less active, suggesting a SAR that could be further exploited [<xref ref-type="bibr" rid="CR193">193</xref>].<fig id="Fig40"><label>Fig. 40</label><caption><p>Structures of biflavonoids</p></caption><graphic xlink:href="12936_2019_3026_Fig40_HTML" id="MO40"></graphic></fig></p></sec><sec id="Sec24"><title>Prenylated flavonoids</title><p id="Par93">The ethyl acetate extract of <italic>Artocarpus styracifolius</italic> (Moraceae) stem bark (10 µg/mL) inhibited FcB1 <italic>P. falciparum</italic> by 87%. A phytochemical investigation of this extract yielded prenylated flavonoids, the new styracifolin B (<bold>312</bold>), together with known artonin B (<bold>313</bold>), artonin F (<bold>314</bold>), heterophyllin (<bold>315</bold>) and artoheterophyllin B (<bold>316</bold>) (Fig. <xref rid="Fig41" ref-type="fig">41</xref>) [<xref ref-type="bibr" rid="CR194">194</xref>]. The compounds displayed antiplasmodial activity against FcB1 parasites with varying degrees of cytotoxicity against KB and MRC-5 cells (IC<sub>50</sub> = 4.7–97 µM). An assessment of the structural features of the flavonoids shows that the two most cytotoxic compounds <bold>312</bold> and <bold>315</bold> had a prenyl chain at C-3. The C-3 prenyl side chain was transformed into a furan ring that was fused to flavonoid ring B in the most selective analogue (<bold>314</bold>) [<xref ref-type="bibr" rid="CR194">194</xref>]. A crude extract from <italic>Macaranga triloba</italic> (Euphorbiaceae) inflorescence showed antiplasmodial activity against the 3D7 strain with an IC<sub>50</sub> of 2.01 µg/mL [<xref ref-type="bibr" rid="CR195">195</xref>]. The prenylated flavonoids nymphaeol C (<bold>317</bold>) and 6-farnesyl-3′,4′,5,7-tetrahydroxyflavanone (<bold>318</bold>) were isolated from this extract and inhibited the 3D7 parasites. The compounds also displayed varying levels of cytotoxicity to cancerous HL-60, MCF-7, and HeLa cells (IC<sub>50</sub> = 1.3–23 µg/mL), suggesting some degree of selectivity in the toxicity to cellular components [<xref ref-type="bibr" rid="CR195">195</xref>]. The antiplasmodial activity of <italic>Tephrosia purpurea</italic> (Fabaceae), a widely distributed medicinal plant, was validated in vitro against the D6 and W2 strains [<xref ref-type="bibr" rid="CR196">196</xref>, <xref ref-type="bibr" rid="CR197">197</xref>]. A phytochemical investigation of <italic>Tephrosia purpurea</italic> subsp. <italic>leptostachya</italic> afforded a new antiplasmodial prenylflavone, (<italic>E</italic>)-5-hydroxytephrostachin (<bold>319</bold>) (Fig. <xref rid="Fig41" ref-type="fig">41</xref>). It was not cytotoxic to cancerous HepG2 cells at 100 µM while being moderately cytotoxic against non-cancerous human cells, indicating selectivity against D6 parasites [<xref ref-type="bibr" rid="CR198">198</xref>]. The aerial parts of the related <italic>Tephrosia subtriflora</italic> were also active against <italic>P. falciparum</italic> 3D7, D6, and KSM 009 field isolate (IC<sub>50</sub> = 4.5–11.4 µg/mL [<xref ref-type="bibr" rid="CR199">199</xref>]. The prenylated flavonoid MS-II (<bold>320</bold>) was subsequently isolated from the active extract and inhibited the 3D7, KSM 009, and artemisinin-sensitive F32-TEM strains. The compound was not cytotoxic against Hep2 and Vero cells at 247.5 µM, suggesting a selective antiplasmodial activity [<xref ref-type="bibr" rid="CR199">199</xref>]. Furthermore, the root extract of <italic>Tephrosia aequilata</italic>, which inhibited 3D7 <italic>P. falciparum</italic> by 100% at 10 µg/mL, produced the new aequichalcone C (<bold>321</bold>). It inhibited the 3D7 strain without being cytotoxic against HEK-293 cells up to 40 µM, indicating selectivity [<xref ref-type="bibr" rid="CR200">200</xref>]. Another prenylated flavonoid, carpachromene (<bold>322</bold>), was isolated from <italic>Flindersia pimenteliana</italic> (Rutaceae) as one of the antiplasmodial principles, and it was not cytotoxic against HEK-293 cells at 40 µM [<xref ref-type="bibr" rid="CR71">71</xref>].<fig id="Fig41"><label>Fig. 41</label><caption><p>Structures of prenylated flavonoids</p></caption><graphic xlink:href="12936_2019_3026_Fig41_HTML" id="MO41"></graphic></fig></p><p id="Par94">Although many prenylated flavonoids are active against the malaria parasite, many of these compounds are also cytotoxic, and selectivity is a problem. Fröhlich et al. reported that prenylated chalcones isolated from hops (<italic>Humulus lupulus</italic>, Cannabaceae) interfere with haem degradation in <italic>P. falciparum</italic>, suggesting a possible mechanism of action [<xref ref-type="bibr" rid="CR201">201</xref>].</p></sec><sec id="Sec25"><title>Other flavonoids</title><p id="Par95">Methanol supercritical fluid extraction yielded four kaempferol 3-<italic>O</italic>-rhamnosides (<bold>323</bold>–<bold>326</bold>) from <italic>Platanus occidentalis</italic> (Platanaceae) and three kaempferol 3-<italic>O</italic>-glucosides (<bold>327</bold>–<bold>330</bold>) from <italic>Quercus laceyi</italic> (Fagaceae) (Fig. <xref rid="Fig42" ref-type="fig">42</xref>) [<xref ref-type="bibr" rid="CR158">158</xref>]. The glycoside esters exhibited activity against HB3 parasites but were 2–11 times less active against a multidrug-resistant NHP1337 clone. The glucosides <bold>327</bold>–<bold>330</bold> were also cytotoxic against HeLa cells, while rhamnosides <bold>323</bold>–<bold>326</bold> were more selective against HB3 parasites (SI = 6–34) [<xref ref-type="bibr" rid="CR158">158</xref>]. An ethnobotanical survey of medicinal plants used by the people in the Comoros Islands indicated that a decoction of <italic>Flacourtia indica</italic> (Salicaceae) stem and leaves is used against malaria. But, extracts prepared from the aerial parts of this plant displayed only weak activity against K1 parasites (IC<sub>50</sub> = 49 µg/mL) for dichloromethane and > 50 µg/mL for polar extracts [<xref ref-type="bibr" rid="CR202">202</xref>]. However, in support of the ethnomedical use of the plant, a 95% ethanol extract of <italic>Flacourtia indica</italic> inhibited the 3D7 strain (IC<sub>50</sub> = 0.5 µg/mL), but was inactive against K1 at the highest tested concentration (10 µg/mL). Chemical investigation of the active extract afforded six phenolic compounds (Fig. <xref rid="Fig42" ref-type="fig">42</xref>) of which the flavonolignans, mururin A (<bold>331</bold>), and catechin-[5,6-e]-4β-(3,4-dihydroxyphenyl)dihydro-2(3<italic>H</italic>)-pyranone (<bold>332</bold>) exhibited selective antiplasmodial activity. Compound <bold>331</bold> inhibited 3D7 and K1 <italic>P. falciparum</italic>, while <bold>332</bold> was active only against the 3D7 strain. Both compounds also inhibited β-haematin formation similar to chloroquine and H<sub>2</sub>O<sub>2</sub>-mediated heme degradation, suggesting a possible mechanism of action [<xref ref-type="bibr" rid="CR203">203</xref>]. The known flavonoid, 3′,4′,7-trihydroxyflavone (<bold>333</bold>), isolated from <italic>Albizia zygia</italic> (Fabaceae) extract, inhibited K1 <italic>P. falciparum</italic> but was also cytotoxic against L6 cells [<xref ref-type="bibr" rid="CR204">204</xref>]. (−)-Epigallocatechin-3-gallate (EGCG) (<bold>334</bold>), the major polyphenol in green tea (<italic>Camellia sinensis</italic>, Theaceae), displayed antiplasmodial activity against 3D7 <italic>P. falciparum</italic>. EGCG also inhibited chaperone and ATPase functions by targeting <italic>Pf</italic>Hsp70-1 and <italic>Pf</italic>Hsp70-z [<xref ref-type="bibr" rid="CR205">205</xref>]. A previous study had shown that EGCG did not interfere with the parasite folate pathway. Moreover, the antiplasmodial activity of green tea and <bold>334</bold> was demonstrated previously, and EGCG was shown to have an additive effect in combination with artemisinin [<xref ref-type="bibr" rid="CR206">206</xref>]. However, a higher IC<sub>50</sub> value (37.2 µM) for EGCG against 3D7 parasites was reported in that study, even though comparable assay methods were used to evaluate the activity. The availability, low cost, and lack of toxicity of green tea coupled with the potentiating effect on the antiplasmodial activity of artemisinin could be exploited to design new artemisinin combination therapies [<xref ref-type="bibr" rid="CR206">206</xref>].<fig id="Fig42"><label>Fig. 42</label><caption><p>Structures of other flavonoids</p></caption><graphic xlink:href="12936_2019_3026_Fig42_HTML" id="MO42"></graphic></fig></p></sec><sec id="Sec26"><title>Coumarins and lactones</title><p id="Par96">Bioassay-guided fractionation of the rhizome extract of the Korean medicinal plant, <italic>Angelica purpuraefolia</italic> (Apiaceae) led to the isolation of the pyranocoumarins 3′-decanoyl-<italic>cis</italic>-khellactone (<bold>335</bold>) and 4′-decanoyl-<italic>cis</italic>-khellactone (<bold>336</bold>) as the main antiplasmodial compounds (Fig. <xref rid="Fig43" ref-type="fig">43</xref>). Both compounds inhibited D10 parasite strains without cytotoxicity against cancerous SK-OV-3 cells, suggesting selectivity towards the parasite [<xref ref-type="bibr" rid="CR207">207</xref>]. The known metabolite 6-acetyl-2-isopropenyl-8-methoxy-1,3-benzodioxin-4-one (<bold>337</bold>), with an additional oxygen atom in the lactone ring, was also isolated as the main antiplasmodial constituent from a <italic>Carpesium divaricatum</italic> (Asteraceae) extract [<xref ref-type="bibr" rid="CR208">208</xref>]. The dichloromethane extract of <italic>Malleastrum</italic> sp. (Meliaceae) showed antiplasmodial activity against the Dd2 strain with IC<sub>50</sub> = 1.3 µg/mL. A new butanolide lactone, malleastrumolide A (<bold>338</bold>), was subsequently isolated from the active extract and was found to inhibit Dd2 parasites, but it was also cytotoxic against A2780 cancer cells [<xref ref-type="bibr" rid="CR209">209</xref>].<fig id="Fig43"><label>Fig. 43</label><caption><p>Structures of coumarins and lactones</p></caption><graphic xlink:href="12936_2019_3026_Fig43_HTML" id="MO43"></graphic></fig></p></sec><sec id="Sec27"><title>Phenolic acids, phenylethanoids, phenylpropanoids, and other shikimic acid-derived metabolites</title><p id="Par97">The leaf extract of <italic>Dacryodes edulis</italic> (Burseraceae), a West African traditional medicinal plant, exhibited antiplasmodial activity against 3D7 and Dd2 parasites (IC<sub>50</sub> = 6.45 and 8.62 µg/mL, respectively) [<xref ref-type="bibr" rid="CR210">210</xref>]. Antiplasmodial screening of the stem bark extract showed that it was also active with an IC<sub>50</sub> of 4.34 and 6.43 µg/mL against 3D7 and Dd2 strains, respectively. Chemical investigations of the stem bark extract afforded methyl gallate (<bold>339</bold>) (Fig. <xref rid="Fig44" ref-type="fig">44</xref>) as the most active compound against the same parasite strains without cytotoxicity against LLC-MK2 cells. Preliminary investigations showed that <bold>339</bold> acts on late-stage parasite trophozoites and schizonts. Compound <bold>339</bold> also acts in synergism with quinine but had an additive effect with artemether [<xref ref-type="bibr" rid="CR211">211</xref>]. A new gallic acid ester, 2,3,4-trihydroxy-2-methylbutyl gallate (<bold>340</bold>), with activity against D6 and W2 <italic>P. falciparum</italic>, was isolated from the aerial parts of <italic>Limonium leptophyllum</italic> (Plumbaginaceae). The compound was almost twice as active against the chloroquine-resistant W2 strain as against the chloroquine-sensitive D6 strain [<xref ref-type="bibr" rid="CR212">212</xref>]. Likewise, a galloylated norbegenin derivative, 4-<italic>O</italic>-(3′-methylgalloyl)norbergenin (<bold>341</bold>), was obtained as the most active antiplasmodial constituent of <italic>Diospyros sanza</italic>-<italic>minika</italic> (Ebenaceae) stem bark extract. Norbegenin, which was also isolated from the same extract, was 32 times less active (40.15 µM), indicating that the additional galloyl group is beneficial to the antiplasmodial activity [<xref ref-type="bibr" rid="CR213">213</xref>]. Antiplasmodial activity was demonstrated for <italic>Anogeissus leiocarpus</italic> (Combretaceae) methanol bark extract (IC<sub>50</sub> = 18.8 µg/mL), and ellagic acid (<bold>342</bold>) was isolated as the most active antiplasmodial metabolite of the extract against 3D7 <italic>P. falciparum</italic> [<xref ref-type="bibr" rid="CR214">214</xref>]. The in vitro and in vivo anti-malarial activity of ellagic acid was previously demonstrated with little cytotoxicity. It also has a synergistic effect in combination with chloroquine and artesunate [<xref ref-type="bibr" rid="CR215">215</xref>].<fig id="Fig44"><label>Fig. 44</label><caption><p>Structures of esters and lactones</p></caption><graphic xlink:href="12936_2019_3026_Fig44_HTML" id="MO44"></graphic></fig></p><p id="Par98">The leaf extract of South American folkloric medicinal plant <italic>Jacaranda glabra</italic> (Bignoniaceae) exhibited antiplasmodial activity against the K1 strain. Bioassay-guided purification was subsequently used to isolate the phenylethanoid glucosides jacaglabrosides A–D (<bold>343</bold>–<bold>346</bold>) (Fig. <xref rid="Fig45" ref-type="fig">45</xref>). All four jacaranone-based glucosides (<bold>343</bold>–<bold>346</bold>) inhibited <italic>P. falciparum</italic> K1 strain. Compound <bold>344</bold>–<bold>346</bold> were not cytotoxic, but <bold>343</bold> showed cytotoxicity against L6 cells [<xref ref-type="bibr" rid="CR216">216</xref>].<fig id="Fig45"><label>Fig. 45</label><caption><p>Structures of phenylethanoids and phenylpropanoids</p></caption><graphic xlink:href="12936_2019_3026_Fig45_HTML" id="MO45"></graphic></fig></p><p id="Par99">The ethyl acetate fraction of <italic>Magnolia grandiflora</italic> (Magnoliaceae) fruit and twig extracts inhibited Dd2 <italic>P. falciparum</italic> (IC<sub>50</sub> = 10 µg/mL). The known 4′-<italic>O</italic>-methyl honokiol (<bold>347</bold>) was the most active among the isolated bioactive neolignans against the Dd2 strain. The position and number of substituents on the neolignan aromatic rings affected the bioactivity. Honokiol, which is structurally similar to <bold>347</bold> but is not methoxylated, was six times less active (IC<sub>50</sub> = 16.5 µM). However, magnolol, which is isomeric to honokiol, was only slightly less active (IC<sub>50</sub> = 3.4 µM) than <bold>347</bold>, while an additional methoxy group on magnolol (3-methoxymagnolol) resulted in a 30 fold decrease in activity [<xref ref-type="bibr" rid="CR217">217</xref>]. More SAR studies are needed to fully understand the effect of substituents on the antiplasmodial activity of simple neolignans. A new dihydrobenzofuranoid neolignan, ococymosin (<bold>348</bold>), was obtained from the antiplasmodial hexane stem extract (IC<sub>50</sub> = 1.25 µg/mL) of <italic>Ocotea cymosa</italic> (Lauraceae) as the most active metabolite against the Dd2 strain [<xref ref-type="bibr" rid="CR218">218</xref>]. The antiplasmodial screening of a library of marine- and plant-derived extracts showed that <italic>Grevillea</italic> (Poorinda Queen, Proteaceae) leaf and twigs extract displayed antiplasmodial activity. Subsequent bioassay-guided purification of the active extract yielded the hemiquinone-containing phenylpropanoid glycosides robustasides D (<bold>349</bold>) and G (<bold>350</bold>) (Fig. <xref rid="Fig45" ref-type="fig">45</xref>) as the main antiplasmodial constituents. Both compounds were more active against chloroquine-resistant <italic>P. falciparum</italic> than to chloroquine-sensitive strains. Compound <bold>350</bold> was more active against the Dd2 and K1 strains, whereas <bold>349</bold> was more active against the multidrug-resistant TM93-C1088 and TM90-C2B strains. Treatment of <italic>P. berghei</italic> infected mice with 32 mg/kg dose of <bold>350</bold> twice a day for 4 days suppressed parasitaemia by 95% without evidence of toxicity [<xref ref-type="bibr" rid="CR219">219</xref>]. The phenylpropanoid glycoside vanicoside F (<bold>351</bold>), isolated as a major constituent of <italic>Polygonum hydropiper</italic> (Polygonaceae) aerial parts, also inhibited <italic>P. falciparum</italic> D6 and W2 strains without cytotoxicity against Vero cells [<xref ref-type="bibr" rid="CR220">220</xref>].</p><p id="Par100">The culture broth of the <italic>Penicillium</italic> sp. FKI-4410 (<italic>Penicillium viticola</italic> sp. nov) fungus afforded some tropolones, among which puberulic acid (<bold>352</bold>) and a new derivative viticolin B (<bold>353</bold>) (Fig. <xref rid="Fig46" ref-type="fig">46</xref>) showed activity. Compound <bold>352</bold> showed potent nM activity against K1 and FCR3 parasites and was not cytotoxic against MCR-5 cells, whereas <bold>353</bold> was less active and selective. Treatment of <italic>P. berghei</italic>-infected mice with 2 mg/kg of <bold>352</bold> for 3 days suppressed parasitaemia by 69%, comparable to chloroquine and artesunate. A preliminary SAR of the tropone compounds suggests that a hydroxy group at C-7 and a methoxy group at C-2 are important for activity while a carboxylic acid function at C-4 improves selectivity [<xref ref-type="bibr" rid="CR221">221</xref>].<fig id="Fig46"><label>Fig. 46</label><caption><p>Structures of tropones</p></caption><graphic xlink:href="12936_2019_3026_Fig46_HTML" id="MO46"></graphic></fig></p><p id="Par101">A phytochemical reinvestigation of <italic>Cleistochlamys kirkii</italic> (Annonaceae) leaf extract led to the isolation of new polyoxygenated cyclohexenones cleistodienediol (<bold>354</bold>), cleistodienol B (<bold>355</bold>), and the known cleistodienol A (<bold>356</bold>) (Fig. <xref rid="Fig47" ref-type="fig">47</xref>). The configuration of the exocyclic double bond in <bold>356</bold> was revised based on the similarity of the nuclear magnetic resonance spectroscopic and specific rotation data with those of <bold>354</bold>. The absolute configuration of <bold>354</bold> was established by X-ray diffraction analysis, which showed that it adopts a half-chair conformation. All three compounds inhibited 3D7 and Dd2 <italic>P. falciparum</italic> strains but were also cytotoxic against noncancerous HEK-293 and cancerous MDA-MB-231 cells. The additional acetylation of compound <bold>356</bold> led to a decrease in activity and selectivity, suggesting a SAR role that could be further explored [<xref ref-type="bibr" rid="CR222">222</xref>].<fig id="Fig47"><label>Fig. 47</label><caption><p>Structures of oxygenated cylcohexenones</p></caption><graphic xlink:href="12936_2019_3026_Fig47_HTML" id="MO47"></graphic></fig></p><p id="Par102">The strobilurins are used commercially in agriculture as fungicides. An investigation of the extracts from the fungus <italic>Favolaschia tonkinensis</italic> led to the isolation of the β-methoxyacrylate derivatives, 9-methoxystrobilurins A, B, and G (<bold>357</bold>–<bold>359</bold>), and oudemansin B (<bold>360</bold>) (Fig. <xref rid="Fig48" ref-type="fig">48</xref>). The compounds were active against K1 <italic>P. falciparum</italic> strain and weakly cytotoxic against Vero cells [<xref ref-type="bibr" rid="CR223">223</xref>].<fig id="Fig48"><label>Fig. 48</label><caption><p>Structures of strobilurins</p></caption><graphic xlink:href="12936_2019_3026_Fig48_HTML" id="MO48"></graphic></fig></p></sec><sec id="Sec28"><title>Xanthones</title><p id="Par103">The extract from fruit pericarp of <italic>Pentadesma butyracea</italic> (Clusiaceae) exhibited antiplasmodial activity against W2 parasites with IC<sub>50</sub> = 1.8 µg/mL. Bioassay-guided purification of the extract yielded the new prenylxanthone pentadexanthone (<bold>361</bold>), together with the known cratoxylone (<bold>362</bold>), garcinone E (<bold>363</bold>) and α-mangostin (<bold>364</bold>) (Fig. <xref rid="Fig49" ref-type="fig">49</xref>). All four xanthones were active against <italic>P. falciparum</italic> W2 strain [<xref ref-type="bibr" rid="CR224">224</xref>]. The antiplasmodial activity of <bold>363</bold> from the same plant against FcB1 was previously reported, but it was also cytotoxic against MCF-7 cells [<xref ref-type="bibr" rid="CR225">225</xref>]. Xanthone <bold>364</bold> was isolated from <italic>Garcinia mangostana</italic> (mangosteen, Clusiaceae) husk and it inhibited FCR3 <italic>P. falciparum</italic> but, surprisingly, it was much less active against the 3D7 strain. Intraperitoneal treatment of <italic>P. berghei</italic> infected mice with <bold>364</bold> at 100 mg/kg suppressed parasitaemia by 80%. Oral treatment produced only 27% suppression. The compound was not cytotoxic to U-937 cells (LC<sub>50</sub> = 130.6 µM), but caused haemolysis of red blood cells at 69.7 µM [<xref ref-type="bibr" rid="CR226">226</xref>]. Another prenylated xanthone, macluraxanthone (<bold>365</bold>), was isolated from an antiplasmodial extract of <italic>Allanblackia floribunda</italic> (Clusiaceae) and had activity against the F32 and FcM29 parasites [<xref ref-type="bibr" rid="CR193">193</xref>]. <italic>Hypericum lanceolatum</italic> (Hypericaceae) is a multipurpose medicinal plant that is used by the people in the southwest province of Cameroon to treat fever [<xref ref-type="bibr" rid="CR227">227</xref>]. In an effort to rationalize this ethnomedicinal use scientifically, the stem bark ethyl acetate fraction was assayed and antiplasmodial activity was observed against the W2mef parasite, IC<sub>50</sub> = 5.02 µg/mL. A bioassay-guided purification of the extract afforded 5-hydroxy-3-methoxyxanthone (<bold>366</bold>) as the most active compound. It inhibited <italic>P. falciparum</italic> SHF4 field isolate but was slightly less active against the W2mef strain. The compound was not cytotoxic against LLC-MK2 cells at the highest concentration tested (100 µg/mL). Interestingly, the 3-hydroxy-5-methoxy isomer of <bold>366</bold> was inactive, suggesting that substitution pattern of the xanthone skeleton play a crucial role in the bioactivity [<xref ref-type="bibr" rid="CR228">228</xref>]. <italic>Garcinia</italic> species produce a unique group of metabolites called caged <italic>Garcinia</italic> xanthones (CGXs) in which the C-ring of the xanthone skeleton has a prenyl substituent that has been transformed to form a tricyclic ring. It was observed that these compounds with interesting bioactivities tend to localize in cell mitochondria and cause damage to it [<xref ref-type="bibr" rid="CR229">229</xref>]. Gambogic acid (<bold>367</bold>) (Fig. <xref rid="Fig49" ref-type="fig">49</xref>), the representative CGX, was isolated from <italic>Garcinia</italic> (Gamboge) resin and exhibited antiplasmodial activity against Dd2 parasites with a sub-micromolar IC<sub>50</sub> value. Chemically modified analogues <bold>368</bold> and <bold>369</bold> that incorporated a triphenylphosphonium group into the CGX skeleton displayed low nanomolar activity against parasite trophozoites and schizonts, whereas replacement of the CGX scaffold with a planar xanthone structure led to a reduction in activity. These observations indicate the beneficial effect of conjugating a triphenylphosphonium moiety to the CGXs and the vital role of the CGX scaffold in the activity of these compounds. The CGXs caused mitochondrial fragmentation and morphological changes within the parasite but did not affect the mitochondrial electron transport chain. This suggests a different mechanism of action from other anti-malarial drugs, such as atovaquone, that target parasite mitochondria. The cytotoxicity of the compounds against HEK293 cells was in the µM range, making them selectively toxic to the parasite at the active concentration (SI > 100) [<xref ref-type="bibr" rid="CR230">230</xref>]. A tetrahydroxanthone dimer, dicerandrol D (<bold>370</bold>), from the endophytic fungus <italic>Diaporthe</italic> sp. (CY-5188) also inhibited <italic>P. falciparum</italic> with a sub-micromolar IC<sub>50</sub> value and moderate cytotoxicity. The bioactivity is influenced by the configuration, and the C-12 epimer, dicerandrol B, was inactive [<xref ref-type="bibr" rid="CR231">231</xref>].<fig id="Fig49"><label>Fig. 49</label><caption><p>Structures of xanthones</p></caption><graphic xlink:href="12936_2019_3026_Fig49_HTML" id="MO49"></graphic></fig></p></sec><sec id="Sec29"><title>Phloroglucinol derivatives</title><p id="Par104">Two new dimeric phloroglucinols, mallotojaponins B (<bold>371</bold>) and C (<bold>372</bold>) (Fig. <xref rid="Fig50" ref-type="fig">50</xref>), were obtained from <italic>Mallotus oppositifolius</italic> (Euphorbiaceae) leaf and inflorescence ethanol extract. Both compounds were active against the Dd2 parasite and cytotoxic against cancerous A2780 cells. Also, the compounds displayed cytocidal activity against the HB3 (LD<sub>50</sub> 14.6 and 0.81 µM for <bold>371</bold> and <bold>372</bold>, respectively) and Dd2 strains (LD<sub>50</sub> = 6.7 and 0.8 µM for <bold>371</bold> and <bold>372</bold>, respectively). Mallotophenone, isolated from the same plant, lacked the prenyl chain of the mallotojaponins and was inactive. Also, <bold>372</bold>, with two prenyl chains, was more active than the monoprenylated <bold>371</bold>, suggesting that prenylation is essential for the antiplasmodial activity of these compounds [<xref ref-type="bibr" rid="CR232">232</xref>]. The synthesis of mallotojaponin C (<bold>372</bold>) was demonstrated in a three-step procedure [<xref ref-type="bibr" rid="CR233">233</xref>]. Seven new polycyclic polyprenylated acylphloroglucinols (PPAPs), symphonones A (<bold>373</bold>), C–E (<bold>374</bold>–<bold>376</bold>), G (<bold>377</bold>), H (<bold>378</bold>), and 14-deoxy-7-epi-isogarcinol (<bold>379</bold>) have been isolated from <italic>Symphonia globulifera</italic> (Clusiaceae) root bark extract. It was previously observed that the extract inhibited <italic>P. falciparum</italic> by 97% at a concentration of 10 µg/mL. These benzophenone derivatives were active against FcB1 <italic>P. falciparum</italic> but were also cytotoxic against MRC-5 cells [<xref ref-type="bibr" rid="CR234">234</xref>].<fig id="Fig50"><label>Fig. 50</label><caption><p>Structures of phloroglucinol derivatives</p></caption><graphic xlink:href="12936_2019_3026_Fig50_HTML" id="MO50"></graphic></fig></p></sec><sec id="Sec30"><title>β-Triketones</title><p id="Par105">This interesting antiplasmodial scaffold is present in compounds isolated from plants of the Myrtaceae. These compounds have been isolated as adducts of phloroglucinol and terpenes, as well as simple acylated syncarpic acid derivatives. A new phloroglucinol β-triketone rhodomyrtosone F (<bold>380</bold>) (Fig. <xref rid="Fig51" ref-type="fig">51</xref>) from <italic>Syncarpia glomulifera</italic> (Myrtaceae) stem bark extract, displayed sub-micromolar inhibition of Dd2 <italic>P. falciparum</italic> and only inhibited HEK293 cells by 58% at 50 µM, suggesting selective toxicity to parasites [<xref ref-type="bibr" rid="CR235">235</xref>]. Likewise, rhodomyrtone (<bold>381</bold>), from the flower extract of <italic>Angophora woodsiana</italic> (Myrtaceae), was active against 3D7 and Dd2 parasites but moderately cytotoxic [<xref ref-type="bibr" rid="CR236">236</xref>]. Tomentosone A (<bold>382</bold>), with a novel hexacyclic ring system that features a bisfurano moiety, was isolated from the dichloromethane extract of <italic>Rhodomyrtus tomentosa</italic> leaves (Myrtaceae). The compound inhibited 3D7 and Dd2 parasites without being cytotoxic against HEK293 cells at 40 µM [<xref ref-type="bibr" rid="CR237">237</xref>]. Watsonianones B (<bold>383</bold>) and C (<bold>384</bold>), from the flowers of <italic>Corymbia watsoniana</italic> (Myrtaceae), have also shown antiplasmodial activity [<xref ref-type="bibr" rid="CR238">238</xref>]. Watsonianone C is the first 4,4a,9,9a-tetrahydro-2<italic>H</italic>-xanthene-1,3,5,7(6<italic>H</italic>,8<italic>H</italic>)-tetraone to be reported while watsonianone B possesses the rare bisfurano moiety present in <bold>382</bold> and is only the fourth fused bisfurano-β-triketone to be reported. Compounds <bold>383</bold> and <bold>384</bold> exerted antiplasmodial activity on the parasite ring stage, with <bold>383</bold> acting predominantly on early ring stage trophozoites. Tomentosone A (<bold>382</bold>), with an additional syncarpic acid moiety and an isobutyl instead of the ethylphenyl group, was less active than <bold>383</bold>. The beneficial role of the ethylphenyl over the isobutyl chain was further demonstrated by the activity of rhodomyrtosone A, which was 50 times less than that of <bold>383</bold> [<xref ref-type="bibr" rid="CR238">238</xref>]. Woodsianone B (<bold>385</bold>), a simple acylated syncarpic acid derivative with an epoxide-containing isopentyl side chain, was also obtained from <italic>Angophora woodsiana</italic> and inhibited the 3D7 and Dd2 parasites [<xref ref-type="bibr" rid="CR236">236</xref>]. Unfortunately, the terpene-β-triketone adducts demonstrated only weak antiplasmodial activity, and this was attributed to poor water solubility of the compounds. Indeed, the more water-soluble analogues have shown better activity. It is plausible that improving the water solubility might lead to more active compounds. The β-triketone pharmacophore can be considered as a novel antiplasmodial scaffold [<xref ref-type="bibr" rid="CR236">236</xref>].<fig id="Fig51"><label>Fig. 51</label><caption><p>Structures of β-triketones</p></caption><graphic xlink:href="12936_2019_3026_Fig51_HTML" id="MO51"></graphic></fig></p></sec><sec id="Sec31"><title>Other polyphenols</title><p id="Par106">Atranorin (<bold>386</bold>) (Fig. <xref rid="Fig52" ref-type="fig">52</xref>) was isolated from the antiplasmodial <italic>Kigelia africana</italic> (Bignoniaceae) bark extract and inhibited the CAM10, SHF4, and W2 parasite strains. The polyphenolic depside <bold>386</bold> also inhibited W2mef parasites and showed synergism in combination with artemether [<xref ref-type="bibr" rid="CR117">117</xref>, <xref ref-type="bibr" rid="CR118">118</xref>].<fig id="Fig52"><label>Fig. 52</label><caption><p>Structure of atranorin</p></caption><graphic xlink:href="12936_2019_3026_Fig52_HTML" id="MO52"></graphic></fig></p></sec></sec><sec id="Sec32"><title>Quinones and polyketides</title><sec id="Sec33"><title>Anthraquinones</title><p id="Par107">An antiplasmodial screening of 6900 extracts identified <italic>Kniphofia ensifolia</italic> (Asphodelaceae) dichloromethane extract as active against Dd2 parasites (IC<sub>50</sub> = 6 µg/mL) [<xref ref-type="bibr" rid="CR239">239</xref>]. Bioassay-guided fractionation afforded the bisanthraquinones chryslandicin (<bold>387</bold>) and 10-(chrysophanol-7-yl)-10-hydroxy-chrysophanol anthrone (<bold>388</bold>), and the phenylanthraquinone, knipholone (<bold>389</bold>) as active principles (Fig. <xref rid="Fig53" ref-type="fig">53</xref>). The compounds displayed activity against Dd2 <italic>P. falciparum</italic> but were also moderately cytotoxic to cancerous A2780 cells [<xref ref-type="bibr" rid="CR239">239</xref>]. Inhibition of the 3D7 strain was previously reported for all the three compounds, but <bold>387</bold> and <bold>388</bold> were not cytotoxic against KB cells [<xref ref-type="bibr" rid="CR240">240</xref>]. Aloe-emodin, which was also isolated from <italic>Kniphofia ensifolia</italic>, was less active against the Dd2 parasites (IC<sub>50</sub> = 58 µM) and did not exhibit antiproliferative activity against A2780 cells. However, a semi-synthetic derivative of aloe-emodin, the 3,4-di-<italic>O</italic>-methylcaffeoyl ester <bold>390</bold>, potently inhibited <italic>P. falciparum</italic> without being cytotoxic [<xref ref-type="bibr" rid="CR239">239</xref>]. The crude extract of <italic>Kniphofia foliosa</italic> root also inhibited <italic>P. falciparum</italic> W2 and D6 strains with IC<sub>50</sub> = 11.29 and 8.92 µg/mL, respectively. A reinvestigation of the extract yielded a new bisanthraquinone, 10-(chrysophanol-7-yl)-10-methoxy-chrysophanol anthrone (<bold>391</bold>), and the compound was more active against the chloroquine-resistant W2 strain than against the D6 strain [<xref ref-type="bibr" rid="CR241">241</xref>]. The leafhopper pathogenic fungus <italic>Torrubiella sp.</italic> BCC 28517 also produced a dimeric anthraquinone, torrubiellin B (<bold>392</bold>), with activity against K1 <italic>P. falciparum</italic>. The new compound, which had rare C-4–C-5′ and C-11–C-10a′ linkages, was cytotoxic against cancerous human KB, NCI-H187, and MCF-7 cells. The structural analogue torrubiellin A, with two less hydroxy groups (C-6 and C-7), was ten times less active against parasites [<xref ref-type="bibr" rid="CR242">242</xref>]. Antiplasmodial screening of crude extracts of marine actinomycetes from Thailand identified <italic>Streptomyces sp.</italic> BCC45596 to have potent activity with IC<sub>50</sub> = 1.45–3.56 µg/mL. Bioassay-guided purification of the extracts led to the isolation of two new <italic>C</italic>-glycosylated benz[α]anthraquinones, urdamycinone E (<bold>393</bold>) and G (<bold>394</bold>), and the known urdamycin E (<bold>395</bold>). Sub-micromolar antiplasmodial activity was obtained for these compounds against the K1 strain. However, the compounds also showed antiproliferative activity against cancerous KB, MCF-7, and NCI-H187 cells, but were less cytotoxic against non-cancerous Vero cells [<xref ref-type="bibr" rid="CR243">243</xref>]. The antiplasmodial activity of four more anthraquinones (<bold>396</bold>–<bold>399</bold>) from an active root extract of <italic>Rennellia elliptica</italic> (Rubiaceae) was demonstrated [<xref ref-type="bibr" rid="CR244">244</xref>].<fig id="Fig53"><label>Fig. 53</label><caption><p>Structures of anthraquinones</p></caption><graphic xlink:href="12936_2019_3026_Fig53_HTML" id="MO53"></graphic></fig></p></sec><sec id="Sec34"><title>Naphthoquinones</title><p id="Par108">The leaf extract of <italic>Pentas longiflora</italic> (Rubiaceae), which is used in Kenyan folk medicine to treat malaria, was active against <italic>P. falciparum</italic> [<xref ref-type="bibr" rid="CR245">245</xref>]. Antiplasmodial investigation of the root extract showed a better activity against the W2 and D6 parasites than the leaf extract (IC<sub>50</sub> = 0.93 and 0.99 µg/mL, respectively). Phytochemical investigation yielded the pyranonaphthoquinones pentalongin (<bold>400</bold>) and psychorubrin (<bold>401</bold>) (Fig. <xref rid="Fig54" ref-type="fig">54</xref>) with antiplasmodial activity against W2 and D6 strains. However, both compounds were also cytotoxic [<xref ref-type="bibr" rid="CR246">246</xref>]. The ethyl acetate extract of <italic>Markhamia tomentosa</italic> (Bignoniaceae) stem bark showed activity against the W2 and K1 strains (IC<sub>50</sub> = 1.46 and 2.81 µg/mL, respectively). Two furanonaphthoquinones (<bold>402</bold> and <bold>403</bold>) were isolated from the extract and inhibited the W2 and K1 parasites. However, <bold>402</bold> and <bold>403</bold> were also cytotoxic against L6 cells [<xref ref-type="bibr" rid="CR247">247</xref>]. Plumbagin (<bold>404</bold>) is the major phytochemical in the extracts of several <italic>Plumbago</italic> species (Plumbaginaceae), including <italic>Plumbago indica</italic> and <italic>Plumbago zeylanica</italic>, with anti-malarial activity [<xref ref-type="bibr" rid="CR248">248</xref>, <xref ref-type="bibr" rid="CR249">249</xref>]. Plumbagin (<bold>404</bold>) inhibited 3D7 and K1 <italic>P. falciparum</italic> strains and suppressed parasitaemia in <italic>P. berghei</italic>-infected mice by 41% after treatment (25 mg/kg body weight). Acute and subacute toxicity was observed in mice after oral administration of <bold>404</bold> above 100 and 25 mg/kg body weight, respectively. The relatively poor in vivo anti-malarial activity of <bold>404</bold> might be due to low bioavailability in living cells [<xref ref-type="bibr" rid="CR250">250</xref>].<fig id="Fig54"><label>Fig. 54</label><caption><p>Structures of other quinones</p></caption><graphic xlink:href="12936_2019_3026_Fig54_HTML" id="MO54"></graphic></fig></p></sec><sec id="Sec35"><title>Perylenequinones</title><p id="Par109">The perylenequinones cercosporin (<bold>405</bold>), 14-<italic>O</italic>-acetylcercosporin (<bold>406</bold>), and di-<italic>O</italic>-acetylcercosporin (<bold>407</bold>) (Fig. <xref rid="Fig54" ref-type="fig">54</xref>) were isolated from the culture medium of the plant pathogenic fungus, <italic>Septoria pistaciarum</italic>. Compound <bold>405</bold> was also obtained from an extract of the endophytic fungus <italic>Mycosphaerella</italic> sp. F2140. The phytotoxins <bold>405</bold>–<bold>407</bold> inhibited <italic>P. falciparum</italic> D6 and W2 strain but were also cytotoxic against MCF-7 and Vero cells. Interestingly, a new cercosporin analogue with a hydroxy and a methoxy group instead of the methylenedioxy bridge in <bold>405</bold>–<bold>407</bold> was inactive. This suggests a SAR role at these two positions that could be exploited for optimized antiparasitic activity [<xref ref-type="bibr" rid="CR251">251</xref>, <xref ref-type="bibr" rid="CR252">252</xref>].</p></sec><sec id="Sec36"><title>Other polyketides</title><p id="Par110">The Solomon Island-sourced marine sponge <italic>Xestospongia testudinaria</italic> produced a halenaquinone-type polyketide 3-ketoadociaquinone A (<bold>408</bold>) (Fig. <xref rid="Fig55" ref-type="fig">55</xref>), which selectively inhibited the FcB1 and 3D7 strains. Halenaquinone, which differs from <bold>408</bold> only in the absence of the dioxothiazine ring, was inactive, indicating that a dioxothiazine ring is necessary for the antiplasmodial activity of the compound [<xref ref-type="bibr" rid="CR253">253</xref>]. The crude extract of terrestrial <italic>Streptomyces</italic> sp. BCC71188 from Thailand inhibited <italic>P. falciparum</italic> (IC<sub>50</sub> = 0.19 µg/mL). Two benzoquinone polyketides, geldanamycin (<bold>409</bold>) and 17-demethoxyreblastatin (<bold>410</bold>), were isolated from the extract and showed antiplasmodial activity against the K1 strain. The quinone moiety in <bold>409</bold> appears to contribute to the cytotoxicity since the structural analogue <bold>410</bold> with a phenol group instead of the quinone was more selective against the parasite [<xref ref-type="bibr" rid="CR254">254</xref>]. Two new antiplasmodial azaphilones, longirostrerone A (<bold>411</bold>) and C (<bold>412</bold>), were isolated from the ethyl acetate extract of the Thailand soil fungus <italic>Chaetomium longirostre</italic>. Both compounds inhibited K1 <italic>P. falciparum</italic> but were also cytotoxic against cancerous KB cells. Compound <bold>411</bold> was also cytotoxic against NCIH-187 and MCF-7 cancer cells, whereas <bold>412</bold> was inactive, indicating selective cytotoxicity [<xref ref-type="bibr" rid="CR255">255</xref>]. Longirostrerone D, which differs from <bold>411</bold> in the configuration of the isochromeno-lactone ring junction and a double bond in the butyrolactone ring, was inactive. Likewise, longirostrerone B, which lacks the lactone moiety, was less active. These observations suggest that the nature of the six-membered ring attached to isochromene, the lactone ring, and the configuration of the compounds play a role in the activity, and further modifications might produce analogues that are more selective.<fig id="Fig55"><label>Fig. 55</label><caption><p>Structures of other polyketides</p></caption><graphic xlink:href="12936_2019_3026_Fig55_HTML" id="MO55"></graphic></fig></p><p id="Par111">Three other new cyclohexenones, poupartones A–C (<bold>413</bold>–<bold>415</bold>) were isolated from the ethyl acetate leaf extract of <italic>Poupartia borbonica</italic> (Anacardiaceae) by bioassay-guided fractionation [<xref ref-type="bibr" rid="CR256">256</xref>]. The extract was previously shown to inhibit the 3D7 strain of <italic>P. falciparum</italic> with IC<sub>50</sub> = 3.28 µg/mL. The compounds were active against W2 and 3D7 parasites but were also cytotoxic against HeLa and WI38 cells. No haemolytic activity was observed with the compounds, indicating that the antiplasmodial activity was due to direct action on the parasites. Treatment of <italic>P. berghei</italic>-infected mice with <bold>413</bold> (15 mg/kg/day for 4 days) led to 69.5% parasite suppression, but it was also toxic to the mice. A toxicity assay of <bold>413</bold> using the zebrafish embryo model indicated that the compound might be cardiotoxic [<xref ref-type="bibr" rid="CR256">256</xref>].</p><p id="Par112">The Senegalese marine sponge <italic>Axinyssa djiferi</italic> produced an antiplasmodial mixture containing three glycosphingolipids axidjiferosides A–C (<bold>416</bold>–<bold>418</bold>) (Fig. <xref rid="Fig55" ref-type="fig">55</xref>). The mixture represented 2.16% of the dried sponge lipid content, while axidjiferoside A (<bold>416</bold>) constituted 60% of the mixture. The compounds were identified as homologs of β-galactopyranosylceramide, containing a 2-amino-1,3,4-trihydroxy-octadecene sphingoid base. Moreover, the fatty acid methyl ester of the major compound (<bold>416</bold>) was identified as 2-hydroxytetracosanoic acid. The mixture exhibited antiplasmodial activity against the FcB1 strain (IC<sub>50</sub> = 0.53 µM) and was not cytotoxic against a panel of cancerous cells. The activity also appeared to be parasite selective because <italic>Leishmania donovani</italic> and <italic>Trypanosoma brucei</italic> were not susceptible to the mixture [<xref ref-type="bibr" rid="CR257">257</xref>]. The endophytic fungus <italic>Diaporthe miriciae</italic> produced epoxycytochalasin H (<bold>419</bold>) with potent antiplasmodial activity against D6 and W2 parasite strains. The compound was not cytotoxic against Vero cells, indicating that the toxicity to the parasite is selective [<xref ref-type="bibr" rid="CR258">258</xref>].</p></sec></sec><sec id="Sec37"><title>Macrocycles</title><sec id="Sec38"><title>Macrolides</title><p id="Par113">The bromophycolides are diterpene-benzoate macrolides that were isolated from the Fijian marine red alga <italic>Callophycus serratus</italic> and had antiplasmodial activity [<xref ref-type="bibr" rid="CR259">259</xref>]. A reinvestigation of <italic>Callophycus serratus</italic> afforded bromophycolides R (<bold>420</bold>), S (<bold>421</bold>), and U (<bold>422</bold>) (Fig. <xref rid="Fig56" ref-type="fig">56</xref>) with antiplasmodial activity and moderate cytotoxicity against cancerous cells [<xref ref-type="bibr" rid="CR260">260</xref>]. Bromophycolides with 15- and 16-membered rings have shown potent antiplasmodial activity. No significant influence of the lactone ring size on activity was observed between 15- and 16-membered lactone rings. The macrolide ring appears to improve bioactivity, considering that non-macrocyclic diterpene-benzoic acids and diterpene-phenols were less active. Furthermore, isolation of the less active 14-membered ring callophycolide A (IC<sub>50</sub> = 5.4 µM), which lacked the bromine atoms and a cyclohexane ring, showed that these features are not essential but improve the potency [<xref ref-type="bibr" rid="CR259">259</xref>, <xref ref-type="bibr" rid="CR261">261</xref>]. Some bromophycolides target haem crystallization, suggesting that the mechanism of action involves the inhibition of haemozoin formation [<xref ref-type="bibr" rid="CR262">262</xref>]. Bastimolide A (<bold>423</bold>), a 40-membered ring polyhydroxy macrolide with 10 stereocentres and a rare <italic>tert</italic>-butyl terminus, was isolated from marine cyanobacterium, <italic>Okeania hirsuta</italic> (PAB-19MAY11-4) [<xref ref-type="bibr" rid="CR242">242</xref>]. The planar structure and absolute configuration of the macrocyclic lactone, which consist of a 1,3-diol, one 1,3,5-triol, and six 1,5-diols, were established by X-ray crystallography. It was hypothesized that the rare <italic>tert</italic>-butyl group near the lactone ester in the bastimolide structure protects the lactone ring against hydrolysis. The compound inhibited multidrug-resistant strains TM90-C2A, TM90-C2A, TM91-C235, and W2 with nanomolar IC<sub>50</sub> values. Surprisingly, the chloroquine-sensitive HB3 strain was less susceptible to <bold>423</bold> (IC<sub>50</sub> in µM). Additionally, the semi-synthetic (2<italic>E</italic>)-isomer was more active against the HB3 strain than the (2<italic>Z</italic>) natural product. Further investigation of <italic>Okeania hirsuta</italic> yielded bastimolide B, in which lactonization produced a 24-membered ring and a highly oxidized side chain that terminated in a <italic>tert</italic>-butyl group. Bastimolide B was not as active as <bold>423</bold>, suggesting that the lactone ring size affects the potency [<xref ref-type="bibr" rid="CR263">263</xref>, <xref ref-type="bibr" rid="CR264">264</xref>]. The Thailand marine sponge <italic>Pachastrissa nux</italic> exhibited antiplasmodial activity against K1 <italic>P. falciparum</italic> (IC<sub>50</sub> = 0.7 µg/mL). The 25-membered ring trisoxazole macrolides kabiramides B (<bold>424</bold>), D (<bold>425</bold>), and J–L (<bold>426</bold>–<bold>428</bold>) (Fig. <xref rid="Fig56" ref-type="fig">56</xref>) were subsequently isolated from the extract and were shown to inhibit K1 parasites. However, the compounds were also cytotoxic against cancerous MCF-7 cells and normal human fibroblasts [<xref ref-type="bibr" rid="CR265">265</xref>, <xref ref-type="bibr" rid="CR266">266</xref>]. Likewise, the crude extract of terrestrial <italic>Streptomyces</italic> sp. BCC71188 afforded the macrolides monoglycosylelaiolide (<bold>429</bold>), azalomycin B (<bold>430</bold>), and 11,11′-<italic>O</italic>-dimethylelaiophylin (<bold>431</bold>) as active metabolite against the K1 strain, but these compounds were also cytotoxic against cancerous and Vero cells [<xref ref-type="bibr" rid="CR254">254</xref>]. <italic>Streptomyces</italic> sp. BCC72023, isolated from rice stems, produced the macrolide efomycin G (<bold>432</bold>) and 29-<italic>O</italic>-methylabierixin (<bold>433</bold>), with activity against K1 <italic>P. falciparum</italic> [<xref ref-type="bibr" rid="CR267">267</xref>].<fig id="Fig56"><label>Fig. 56</label><caption><p>Structures of macrolides</p></caption><graphic xlink:href="12936_2019_3026_Fig56_HTML" id="MO56"></graphic></fig></p></sec><sec id="Sec39"><title>Resorcylic acid lactones</title><p id="Par114">The mycelial culture of the filamentous fungus, <italic>Paecilomyces</italic> sp. SC0924 produced the new 14-membered ring β-resorcylic acid lactones (RALs, Fig. <xref rid="Fig57" ref-type="fig">57</xref>) paecilomycins A (<bold>434</bold>), E (<bold>435</bold>), F (<bold>436</bold>), together with aigilomycin B (<bold>437</bold>) and aigialomycin F (<bold>438</bold>), all with potent antiplasmodial activity. Paecilomycin E (<bold>435</bold>) and aigialomycin F (<bold>438</bold>) showed sub-micromolar inhibition of 3D7 parasites, with all the compounds more potent against the 3D7 than the Dd2 strain, suggesting resistance by the Dd2 strain. The compounds were not cytotoxic against Vero cells at 50 µM [<xref ref-type="bibr" rid="CR268">268</xref>]. Cochliomycins A–F are structural analogues of the paecilomycins and were initially isolated from the culture broth of <italic>Cochliobolus lunatus</italic> in trace quantities [<xref ref-type="bibr" rid="CR269">269</xref>, <xref ref-type="bibr" rid="CR270">270</xref>]. Two cochliomycin analogues were subsequently isolated in larger amounts from an optimized fermentation broth, and the natural cochliomycins and some derivatives were obtained by semi-synthesis. In contrast to the paecilomycins, the cochliomycins generally showed poor antiplasmodial activity. However, semi-synthetic acetonide derivative <bold>439</bold> inhibited <italic>P. falciparum</italic> (SI = 184) selectively, whereas the hydroxylated parent was inactive. Also, cochliomycin C, the chlorinated derivative of paecilomycin F (<bold>436</bold>), was inactive. SAR deductions from the RAL structures indicate that the presence of acetyl and acetonide groups on the lactone ring hydroxy groups improve activity, with the acetonide derivative having a superior activity. A chlorine atom on the aromatic C-5 decreases activity, while the C-2 phenolic group is important for selective activity. The presence of an enone moiety in the lactone macrocycle contributes to cytotoxicity, whereas the configuration of the 1,2,3-triol or 1,2-diol stereocentres had a negligible effect on the activity [<xref ref-type="bibr" rid="CR271">271</xref>].<fig id="Fig57"><label>Fig. 57</label><caption><p>Structures of resorcyclic acid lactones</p></caption><graphic xlink:href="12936_2019_3026_Fig57_HTML" id="MO57"></graphic></fig></p></sec><sec id="Sec40"><title>Cyclodepsipeptides and other peptides</title><p id="Par115">The cyclodepsipeptides lagunamides A–C (<bold>440</bold>–<bold>442</bold>) (Fig. <xref rid="Fig58" ref-type="fig">58</xref>) were obtained from the marine cyanobacterium, <italic>Lyngbya majuscula.</italic> The planar lagunamide macrocyclic scaffold consists of peptide and polyketide substructures, and the main differences are in the polyketide part. Lagunamides A and B are 26-membered macrocycles, whereas lagumanide C has an additional methylene carbon in the polyketide structure. The compounds exhibited potent antiplasmodial activity against NF54 <italic>P. falciparum</italic> strain and were also cytotoxic against cancerous cells [<xref ref-type="bibr" rid="CR272">272</xref>, <xref ref-type="bibr" rid="CR273">273</xref>]. The double bond in the side chain of <bold>441</bold> might be responsible for the lower activity. Mollemycin A (<bold>443</bold>), a glyco-hexadepsipeptide with a polyketide residue, was isolated from an Australian <italic>Streptomyces</italic> sp. CMBM0244 and had a potent nanomolar antiplasmodial activity. It was equally active against the 3D7 and Dd2 strains and only slightly cytotoxic against human fibroblast cells (SI > 20), suggesting selectivity against the parasites [<xref ref-type="bibr" rid="CR274">274</xref>]. Two other antiplasmodial octacyclodepsipeptides, octaminomycins A (<bold>444</bold>) and B (<bold>445</bold>), were isolated from Indonesian soil <italic>Streptomyces</italic> sp. RK85-270. The octaminomycin amino acid sequence was established as cyclo-(Pro-<italic>N</italic>-MeTyr-Leu-Pro-Val-Leu-Phe-Thr). Furthermore, the only structural difference is the presence of propionyl and acetyl chains on the threonine nitrogen in <bold>444</bold> and <bold>445</bold>, respectively. Both compounds were active against 3D7, Dd2, and K1 strains, and were not cytotoxic at 30 µM [<xref ref-type="bibr" rid="CR275">275</xref>]. A new cyclodepsipeptide incorporating a 3-hydroxy-4-methylpentadecanoic acid moiety, fusaripeptide A (<bold>446</bold>), was obtained from <italic>Mentha longifolia</italic> (Lamiaceae) root endophytic fungus, <italic>Fusarium</italic> sp. from Saudi Arabia. The amino acid sequence was established as cyclo-(Ala-Ala-Thr-Ile-Tyr-Glu). Compound <bold>446</bold> exhibited antiplasmodial activity against D6 <italic>P. falciparum</italic> and was moderately cytotoxic against cancerous L5178Y and PC12 cells [<xref ref-type="bibr" rid="CR276">276</xref>].<fig id="Fig58"><label>Fig. 58</label><caption><p>Structures of cyclodepsipeptides</p></caption><graphic xlink:href="12936_2019_3026_Fig58_HTML" id="MO58"></graphic></fig></p><p id="Par116">Carmaphycin B (<bold>447</bold>) (Fig. <xref rid="Fig59" ref-type="fig">59</xref>), with an amino acid sequence of <sc>l</sc>-Val-<sc>l</sc>-Met sulfone-<sc>l</sc>-Leu, was isolated from the cyanobacterium, <italic>Symploca</italic> sp. The tripeptide with hexanoyl and an α,β-epoxyketone groups on the <italic>N</italic> and carboxyl ends, respectively, had potent nM in vitro and in vivo antiplasmodial activity, but it was also cytotoxic against HepG2 cells. The synthetically modified analogue <bold>448</bold> with a <sc>d</sc>-Val-<sc>l</sc>-Nle-<sc>l</sc>-Leu amino acid sequence showed improved antiplasmodial activity and selectivity (SI = 379). The peptides act in synergy with artemisinin and kill the parasite by targeting the β5 subunit of <italic>Plasmodium</italic> proteasome [<xref ref-type="bibr" rid="CR277">277</xref>]. A marine actinobacteria from Papua New Guinea, <italic>Streptomyces bangulaensis</italic>, produced the antiplasmodial tetrapeptide, actinoramide A (<bold>449</bold>). The compound displayed sub-micromolar antiplasmodial activity against <italic>P. falciparum</italic> Dd2, HB3, 7G8, GB4, and cp250 strains, and no cytotoxicity. The 25-epimer of <bold>449</bold>, 25-<italic>epi</italic>-actinoramide A was about 20-fold less active, suggesting an influence of the configuration on activity. Actinoramide F, which is structurally similar to <bold>449</bold> but has a 5-amino-5,6-dihydrouracil terminus instead of the cyclic 2-amino-4-ureidobutanoic acid of <bold>449,</bold> was inactive. This suggests that the terminal substructure of the actinoramides is crucial for antiplasmodial activity [<xref ref-type="bibr" rid="CR278">278</xref>]. A new antiplasmodial cyclic tetrapeptide, apicidin F (<bold>450</bold>), was isolated from the rice fungus pathogen, <italic>Fusarium fujikuroi</italic>, and the amino acid composition was established to be <sc>l</sc>-tryptophan, <sc>d</sc>-pipecolic acid, <sc>l</sc>-phenylalanine, and <sc>l</sc>-2-aminooctanedioic acid [<xref ref-type="bibr" rid="CR279">279</xref>].<fig id="Fig59"><label>Fig. 59</label><caption><p>Structures of other peptides</p></caption><graphic xlink:href="12936_2019_3026_Fig59_HTML" id="MO59"></graphic></fig></p><p id="Par117">Cyclopeptide alkaloids are 13, 14, or 15-membered ring polyamides with a styrylamine unit, a β-hydroxy amino acid and other common amino acid forming the macrocycle. The macrocyclic polyamide has an attached side chain, which could be basic or neutral. Spinanine B (<bold>451</bold>) (Fig. <xref rid="Fig59" ref-type="fig">59</xref>), a cyclopeptide alkaloid from the stem bark of <italic>Ziziphus spina</italic>-<italic>christi</italic> (Rhamnaceae), inhibited the K1 strain of <italic>P. falciparum</italic> without cytotoxicity to MRC-5 cells at 64 µM [<xref ref-type="bibr" rid="CR280">280</xref>]. Evaluation of the antiplasmodial activity of 19 cyclopeptide alkaloids facilitated some SAR conclusions. Preliminary SAR studies indicated that the 13-membered ring cyclopeptide alkaloids were generally more active than the 14 and 15 membered analogues. Also, a methoxy group on the styrylamine moiety was more favourable for antiplasmodial activity than a hydroxy group [<xref ref-type="bibr" rid="CR281">281</xref>, <xref ref-type="bibr" rid="CR282">282</xref>].</p></sec></sec><sec id="Sec41"><title>Cyclic phosphotriesters</title><p id="Par118">A marine actinobacterium, <italic>Salinospora</italic> sp., produced a new class of antiplasmodial scaffold based on a bicyclic phosphotriester core, substituted with alkyl chains. Among the new compounds, salinipostins A-D, F-G, and I (<bold>452</bold>–<bold>458</bold>) (Fig. <xref rid="Fig60" ref-type="fig">60</xref>) potently inhibited W2 <italic>P. falciparum</italic> without cytotoxicity. Preliminary SAR findings indicated that an increase in alkyl chain length attached to the phosphoester oxygen (R<sup>2</sup>) and vinyl carbon (R<sup>1</sup>) led to increased activity while branching of the R<sup>1</sup> alkyl causes a slight reduction in activity. The most active <bold>452</bold> had sub-micromolar IC<sub>50</sub> values and stage-specific activity on early stage parasite ring forms, but parasite trophozoites were less susceptible. The compound did not affect parasite schizonts, indicating that it acts by disrupting the processes required for the establishment or growth of intracellular parasites. Salinispostin A (<bold>452</bold>) did not inhibit haemozoin formation but appears to cause cellular disorganization and disintegration of internal structures. Moreover, experiments for resistance selection under three different conditions failed to identify mutant resistant strains, suggesting that the compound may be less susceptible to resistance development. These compounds represent a new class of antiplasmodial agents, and further biological studies on them are warranted [<xref ref-type="bibr" rid="CR283">283</xref>].<fig id="Fig60"><label>Fig. 60</label><caption><p>Structures of cyclic phosphotriesters</p></caption><graphic xlink:href="12936_2019_3026_Fig60_HTML" id="MO60"></graphic></fig></p></sec><sec id="Sec42"><title>Mechanism of action of antiplasmodial natural products: <italic>Plasmodium</italic> cellular targets identified for natural products</title><p id="Par119">Understanding the mechanism of action of bioactive molecules facilitates the development of leads into improved therapeutic compounds and aids in the understanding of resistance evolution. Natural products have proven to be a prolific source of drug leads, but limited knowledge about the mechanism of action often impedes further development [<xref ref-type="bibr" rid="CR284">284</xref>]. In order to understand the mechanism of action of anti-malarial natural products, it is necessary to identify the molecular targets in the parasite. The anti-malarial drugs in current use are based on pharmacophores acting on a small number of targets as their mechanism of action. The use of these compounds as monotherapy resulted in the emergence of multidrug-resistant parasites [<xref ref-type="bibr" rid="CR285">285</xref>, <xref ref-type="bibr" rid="CR286">286</xref>]. Many of the candidates currently in the anti-malarial drug pipeline are based on chemical modifications to overcome the handicaps of the traditional anti-malarials [<xref ref-type="bibr" rid="CR287">287</xref>]. Eventual development of resistance to these new therapies when they become clinically useful is inevitable. Therefore, it is imperative to discover new therapeutics with novel targets and mechanisms of action. The increased understanding of the <italic>Plasmodium</italic> parasite biology following the sequencing of its genome has led to the identification of novel potential drug targets that are thought to be essential for parasite survival [<xref ref-type="bibr" rid="CR288">288</xref>].</p><p id="Par120">Crucial enzymes and macromolecules in the parasite fatty acid, haemoglobin, protein, Ca<sup>2+</sup> metabolism, glyoxalase detoxification system, and protein folding pathways have been inhibited by natural products. Reports on natural products as inhibitors of potential and proven antiplasmodial targets together with the mechanism of action are summarized in Table <xref rid="Tab1" ref-type="table">1</xref>. Natural products have also modulated their parasite killing effect by disrupting the haem detoxification systems as well as induction of oxidative stress and lipid peroxidation in the parasite (Table <xref rid="Tab1" ref-type="table">1</xref>). Some natural products have also been reported to mediate antiplasmodial activity by inducing morphological and ultrastructural changes that are detrimental to parasite viability [<xref ref-type="bibr" rid="CR230">230</xref>, <xref ref-type="bibr" rid="CR289">289</xref>].<table-wrap id="Tab1"><label>Table 1</label><caption><p>Mechanism of action of antiplasmodial natural products</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left">Pathway</th><th align="left">Mechanism of action</th><th align="left">Target</th><th align="left">Compound</th><th align="left">Compound class</th><th align="left">References</th></tr></thead><tbody><tr><td align="left">Fatty acid metabolism</td><td align="left">Inhibitionof type II fatty acid synthase (FAS II) enzymes</td><td align="left"><italic>Plasmodium falciparum</italic> enoyl-ACP reductase (<italic>Pf</italic>FabI)</td><td align="left">Oroidin</td><td align="left">Bromopyrrole alkaloid</td><td align="left">[<xref ref-type="bibr" rid="CR290">290</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Luteolin 7-<italic>O</italic>-β<sc>-d-</sc>glucopyranoside</td><td align="left">Flavonoid glycoside</td><td align="left">[<xref ref-type="bibr" rid="CR291">291</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Anthecularin</td><td align="left">Sesquiterpene lactone</td><td align="left">[<xref ref-type="bibr" rid="CR292">292</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">4-Hydroxyanthecotulide</td><td align="left">Sesquiterpene lactone</td><td align="left">[<xref ref-type="bibr" rid="CR293">293</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">4-Acetoxyanthecotulide</td><td align="left">Sesquiterpene lactone</td><td align="left">[<xref ref-type="bibr" rid="CR293">293</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Mucusisoflavone C</td><td align="left">Flavonoid</td><td align="left">[<xref ref-type="bibr" rid="CR294">294</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">3-<italic>O</italic>-Methylquercetin</td><td align="left">Flavonoid</td><td align="left">[<xref ref-type="bibr" rid="CR294">294</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Isowighteone</td><td align="left">Flavonoid</td><td align="left">[<xref ref-type="bibr" rid="CR294">294</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Evernic acid</td><td align="left">Phenolic acid</td><td align="left">[<xref ref-type="bibr" rid="CR295">295</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Psoromic acid</td><td align="left">Phenolic acid</td><td align="left">[<xref ref-type="bibr" rid="CR295">295</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Methylenebissantin</td><td align="left">Flavonoid</td><td align="left">[<xref ref-type="bibr" rid="CR296">296</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"><italic>Plasmodium falciparum</italic> β-ketoacyl-ACP reductase (<italic>Pf</italic>FabG)</td><td align="left">Anthecularin</td><td align="left">Sesquiterpene lactone</td><td align="left">[<xref ref-type="bibr" rid="CR292">292</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">4-Hydroxyanthecotulide</td><td align="left">Sesquiterpene lactone</td><td align="left">[<xref ref-type="bibr" rid="CR293">293</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">4-Acetoxyanthecotulide</td><td align="left">Sesquiterpene lactone</td><td align="left">[<xref ref-type="bibr" rid="CR293">293</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Psoromic acid</td><td align="left">Phenolic acid</td><td align="left">[<xref ref-type="bibr" rid="CR295">295</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"><italic>Plasmodium falciparum</italic> β-hydroxyacyl-ACP dehydratase (<italic>Pf</italic> FabZ)</td><td align="left">Evernic acid</td><td align="left">Phenolic acid</td><td align="left">[<xref ref-type="bibr" rid="CR295">295</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Vulpic acid</td><td align="left">Phenolic acid</td><td align="left">[<xref ref-type="bibr" rid="CR295">295</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Psoromic acid</td><td align="left">Phenolic acid</td><td align="left">[<xref ref-type="bibr" rid="CR295">295</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Catechin gallate</td><td align="left">Catechin</td><td align="left">[<xref ref-type="bibr" rid="CR297">297</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Bromopyrrolohomoarginin</td><td align="left">Bromopyrrole alkaloid</td><td align="left">[<xref ref-type="bibr" rid="CR93">93</xref>]</td></tr><tr><td align="left">Detoxification of haem</td><td align="left">Inhibition of β-haematin formation</td><td align="left">Haem crystallization</td><td align="left">Bromophycolide A</td><td align="left">Macrocyclic meroditerpene</td><td align="left">[<xref ref-type="bibr" rid="CR262">262</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Bergenin</td><td align="left">Phenolic glycoside</td><td align="left">[<xref ref-type="bibr" rid="CR298">298</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Fraxetin</td><td align="left">Coumarin</td><td align="left">[<xref ref-type="bibr" rid="CR299">299</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">1,3,6-Trihydroxy-2-(3-methyl but-dienyl)-7-methoxy-8-(3- methyl but-2-enyl)xanthen-9-one</td><td align="left">Xanthone</td><td align="left">[<xref ref-type="bibr" rid="CR300">300</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">2-(6-<italic>O</italic>-Benzoyl-β<sc>-d-</sc>glucopyranosyloxy)-7-(1α, 2α, 6α-trihydroxy-3-oxocyclohex-4-enoyl)-5-hydroxybenzyl alcohol</td><td align="left">Phenolic glycoside</td><td align="left">[<xref ref-type="bibr" rid="CR301">301</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Dimethylisoborreverine</td><td align="left">Indole alkaloid</td><td align="left">[<xref ref-type="bibr" rid="CR46">46</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Nitidine</td><td align="left">Benzophenanthridine alkaloid</td><td align="left">[<xref ref-type="bibr" rid="CR62">62</xref>]</td></tr><tr><td align="left"></td><td align="left">Inhibition of β-haematin formation, inhibition of H<sub>2</sub>O<sub>2</sub> and glutathione mediated hemin degradation</td><td align="left"></td><td align="left">Axisonitrile-3</td><td align="left">Sesquiterpene isonitrile</td><td align="left">[<xref ref-type="bibr" rid="CR154">154</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Diisocyanoadociane</td><td align="left">Diterpene isonitrile</td><td align="left">[<xref ref-type="bibr" rid="CR154">154</xref>]</td></tr><tr><td align="left"></td><td align="left">Inhibition of β-haematin formation, inhibition of H<sub>2</sub>O<sub>2</sub> mediated haemin degradation</td><td align="left"></td><td align="left">Catechin-[5,6-e]-4β-(3,4-dihydroxyphenyl) dihydro-2(3H)-pyranone</td><td align="left">Phenylpropanoid catechin</td><td align="left">[<xref ref-type="bibr" rid="CR203">203</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Mururin A</td><td align="left">Phenylpropanoid catechin</td><td align="left">[<xref ref-type="bibr" rid="CR203">203</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"><italic>Plasmodium falciparum</italic> glutathione transferase (<italic>Pf</italic>GST)</td><td align="left">JB42C</td><td align="left">Sesquiterpene lactone</td><td align="left">[<xref ref-type="bibr" rid="CR302">302</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Tral-1</td><td align="left">Coumarin catechin</td><td align="left">[<xref ref-type="bibr" rid="CR302">302</xref>]</td></tr><tr><td align="left">Oxidative stress</td><td align="left">Production of ROS and lipid peroxidation product</td><td align="left">Trafficking, transmembrane and vesicular transport parasite proteins</td><td align="left">Plakortin</td><td align="left">Polyketide endoperoxide</td><td align="left">[<xref ref-type="bibr" rid="CR303">303</xref>]</td></tr><tr><td align="left">Haemoglobin degradation</td><td align="left">Inhibition of food vacuole falcipains</td><td align="left">Falcipain 2</td><td align="left">2,3,6-Trihydroxy benzoic acid</td><td align="left">Phenolic acid</td><td align="left">[<xref ref-type="bibr" rid="CR304">304</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">2,3,6-Trihydroxy methyl benzoate</td><td align="left">Phenolic ester</td><td align="left">[<xref ref-type="bibr" rid="CR304">304</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Symplostatin 4</td><td align="left">Depsipeptide</td><td align="left">[<xref ref-type="bibr" rid="CR284">284</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left">Falcipain 2′ and 3</td><td align="left">Symplostatin 4</td><td align="left">Depsipeptide</td><td align="left">[<xref ref-type="bibr" rid="CR284">284</xref>]</td></tr><tr><td align="left">Glyoxalase detoxification system</td><td align="left">Inhibition of <italic>Plasmodium falciparum</italic> glyoxalase I (PfGLOI)</td><td align="left">(<italic>Pf</italic>GLOI)</td><td align="left">Puberulic acid</td><td align="left">Tropone</td><td align="left">[<xref ref-type="bibr" rid="CR305">305</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Hinokitiol</td><td align="left">Tropone</td><td align="left">[<xref ref-type="bibr" rid="CR305">305</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Tropolone</td><td align="left">Tropone</td><td align="left">[<xref ref-type="bibr" rid="CR305">305</xref>]</td></tr><tr><td align="left">Protein folding</td><td align="left">Inhibition of <italic>Plasmodium falciparum</italic> Hsp70-1 (PfHsp70-1) chaperone function</td><td align="left">(<italic>Pf</italic>Hsp70-1)</td><td align="left">Malonganenone A</td><td align="left">Purine alkaloid</td><td align="left">[<xref ref-type="bibr" rid="CR306">306</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Malonganenone B</td><td align="left">Purine alkaloid</td><td align="left">[<xref ref-type="bibr" rid="CR306">306</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Malonganenone C</td><td align="left">Alkaloid</td><td align="left">[<xref ref-type="bibr" rid="CR306">306</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">Lapachol</td><td align="left">Naphthoquinone</td><td align="left">[<xref ref-type="bibr" rid="CR306">306</xref>]</td></tr><tr><td align="left"></td><td align="left">Inhibition of chaperone and ATPase functions</td><td align="left">PfHsp70-1, PfHsp70-z</td><td align="left">Epigallocatechin 3-gallate</td><td align="left">Catechin</td><td align="left">[<xref ref-type="bibr" rid="CR205">205</xref>]</td></tr><tr><td align="left">Protein degradation</td><td align="left">inhibition of Pf20S proteasome</td><td align="left">β5 subunit</td><td align="left">Carmaphycin B</td><td align="left">Tripeptide</td><td align="left">[<xref ref-type="bibr" rid="CR277">277</xref>]</td></tr><tr><td align="left">Ca<sup>2+</sup> metabolism</td><td align="left">Inhibition of SERCA-type Ca<sup>2+</sup>-ATPase</td><td align="left">PfATP6</td><td align="left">Artemisinins</td><td align="left">Sesquiterpene endoperoxide</td><td align="left">[<xref ref-type="bibr" rid="CR307">307</xref>]</td></tr><tr><td align="left">Protein biosynthesis</td><td align="left">Inhibition of cytoplasmic lysyl-tRNA synthetase</td><td align="left"><italic>Pf</italic> lysyl-tRNA synthetase</td><td align="left">Cladosporin</td><td align="left">Isocoumarin</td><td align="left">[<xref ref-type="bibr" rid="CR308">308</xref>]</td></tr></tbody></table></table-wrap></p></sec><sec id="Sec43"><title>Natural products with transmission-blocking potentials</title><p id="Par121">Malaria chemotherapy has focused mainly on controlling the disease. Thus, most anti-malarial drugs act on asexual blood stage parasites that are responsible for the clinical manifestations of the disease. However, there has been a shift in focus towards malaria elimination strategies. In this regard, compounds with activity against asymptomatic gametocytes and liver stage parasites, including hypnozoites (prophylaxis), are crucial to the eradication agenda. As yet, artesunate, artemether, methylene blue, and primaquine are the known gametocidal agents, with primaquine being the only approved prophylactic and gametocytocidal drug [<xref ref-type="bibr" rid="CR309">309</xref>]. Some natural products have shown transmission blocking potential by exhibiting activity against one or more of these parasite life cycle stages. These natural products are summarized in Table <xref rid="Tab2" ref-type="table">2</xref>. Similarly, extracts from <italic>Zanthoxylum heitzii</italic>, <italic>Vernonia amygdalina</italic>, <italic>Artemisia afra</italic>, <italic>Trichilia emetica</italic>, <italic>Turraea floribunda</italic>, and <italic>Leonotis leonurus</italic> have shown gametocidal activity [<xref ref-type="bibr" rid="CR65">65</xref>, <xref ref-type="bibr" rid="CR310">310</xref>, <xref ref-type="bibr" rid="CR311">311</xref>]. The standardized commercial preparation NeemAzal<sup>®</sup>, an azadirachtin-enriched neem extract, has also demonstrated potent transmission-blocking activity ex vivo and in vivo [<xref ref-type="bibr" rid="CR312">312</xref>, <xref ref-type="bibr" rid="CR313">313</xref>]. The targeting of gametocytes is indeed of great importance in the fight against malaria. The limited information available in the literature on drugs with this activity may be a reflection of the difficulty of assaying gametocidal activity.<table-wrap id="Tab2"><label>Table 2</label><caption><p>Natural products with transmission-blocking potential</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left">Compound</th><th align="left">Parasite</th><th align="left">Active on</th><th align="left">Activity</th><th align="left">IC<sub>50</sub></th><th align="left">References</th></tr></thead><tbody><tr><td align="left">Dihydronitidine</td><td align="left"><italic>Plasmodium berghei</italic></td><td align="left">Early mosquito stage</td><td align="left">Inhibition of ookinete formation</td><td align="left">1.7 µM</td><td align="left">[<xref ref-type="bibr" rid="CR65">65</xref>]</td></tr><tr><td align="left">Heitziquinone</td><td align="left"><italic>P. berghei</italic></td><td align="left">Early mosquito stage</td><td align="left">Inhibition of ookinete formation</td><td align="left">17 µM</td><td align="left">[<xref ref-type="bibr" rid="CR65">65</xref>]</td></tr><tr><td align="left">Mallotojaponin C</td><td align="left"><italic>P. falciparum</italic> NF54</td><td align="left">Stage V gametocytes</td><td align="left">Gametocytocidal</td><td align="left">3.6 µM</td><td align="left">[<xref ref-type="bibr" rid="CR232">232</xref>]</td></tr><tr><td align="left">Carmaphycin B</td><td align="left"><italic>P. falciparum</italic> NF54</td><td align="left">Stage V gametocytes</td><td align="left">Gametocytocidal</td><td align="left">160 nM</td><td align="left">[<xref ref-type="bibr" rid="CR277">277</xref>]</td></tr><tr><td align="left">Carmaphycin B</td><td align="left"><italic>P. berghei</italic></td><td align="left">Liver stage</td><td align="left"></td><td align="left">61.6 nM</td><td align="left"></td></tr><tr><td align="left">Parthenine</td><td align="left"><italic>P. falciparum</italic> NF54</td><td align="left">Stage V gametocytes</td><td align="left">Gametocytocidal. Inhibition of microgamete exflagellation. Prevent oocysts development in mosquito at 3.84 µM</td><td align="left"></td><td align="left">[<xref ref-type="bibr" rid="CR314">314</xref>]</td></tr><tr><td align="left"></td><td align="left"></td><td align="left">Early mosquito stage</td><td align="left">Inhibition of ookinete formation</td><td align="left">100% inhibition at 191 µM</td><td align="left">[<xref ref-type="bibr" rid="CR314">314</xref>]</td></tr><tr><td align="left">Parthenolide</td><td align="left"><italic>P. falciparum</italic> NF54</td><td align="left">stage V gametocytes</td><td align="left">Gametocytocidal. Inhibition of microgamete exflagellation. prevent oocysts development in mosquito at 4 µM</td><td align="left"></td><td align="left">[<xref ref-type="bibr" rid="CR314">314</xref>]</td></tr><tr><td align="left">Deacetylnimbin</td><td align="left"><italic>P. berghei</italic></td><td align="left">Early mosquito stage</td><td align="left">Inhibition of ookinete formation</td><td align="left">100% inhibition at 100 µM</td><td align="left">[<xref ref-type="bibr" rid="CR315">315</xref>]</td></tr><tr><td align="left">Azadirachtin</td><td align="left"><italic>P. falciparum</italic> NF54</td><td align="left">Stage V gametocytes</td><td align="left">100% inhibition of microgamete exflagellation</td><td align="left"></td><td align="left">[<xref ref-type="bibr" rid="CR316">316</xref>]</td></tr><tr><td align="left"></td><td align="left"><italic>P. berghei</italic></td><td align="left">Stage V gametocytes</td><td align="left">Gametocytocidal. Inhibition of microgamete exflagellation</td><td align="left">3.25 µM</td><td align="left">[<xref ref-type="bibr" rid="CR316">316</xref>]</td></tr><tr><td align="left">Vernodalol</td><td align="left"><italic>P. berghei</italic></td><td align="left">Early mosquito stage</td><td align="left">Inhibition of early sporogenic stages development</td><td align="left">18.7 µM</td><td align="left">[<xref ref-type="bibr" rid="CR310">310</xref>]</td></tr><tr><td align="left">Vernolide</td><td align="left"><italic>P. berghei</italic></td><td align="left">Early mosquito stage</td><td align="left">9–33% inhibition of early sporogenic stages development at 50 µM</td><td align="left"></td><td align="left">[<xref ref-type="bibr" rid="CR310">310</xref>]</td></tr><tr><td align="left">Usnic acid</td><td align="left"><italic>P. berghei</italic></td><td align="left">Liver stage</td><td align="left"></td><td align="left">2.3 µM</td><td align="left">[<xref ref-type="bibr" rid="CR295">295</xref>]</td></tr><tr><td align="left">Vulpic acid</td><td align="left"><italic>P. berghei</italic></td><td align="left">Liver stage</td><td align="left"></td><td align="left">10.2 µM</td><td align="left">[<xref ref-type="bibr" rid="CR295">295</xref>]</td></tr><tr><td align="left">Psoromic acid</td><td align="left"><italic>P. berghei</italic></td><td align="left">Liver stage</td><td align="left"></td><td align="left">31.6 µM</td><td align="left">[<xref ref-type="bibr" rid="CR295">295</xref>]</td></tr><tr><td align="left">Evernic acid</td><td align="left"><italic>P. berghei</italic></td><td align="left">Liver stage</td><td align="left"></td><td align="left">77.3 µM</td><td align="left">[<xref ref-type="bibr" rid="CR295">295</xref>]</td></tr><tr><td align="left">Balsaminol F</td><td align="left"><italic>P. berghei</italic></td><td align="left">Liver stage</td><td align="left">Inhibition of intracellular development</td><td align="left">> 95% inhibition at 15 µM</td><td align="left">[<xref ref-type="bibr" rid="CR163">163</xref>]</td></tr><tr><td align="left">BalsaminosideB</td><td align="left"><italic>P. berghei</italic></td><td align="left">Liver stage</td><td align="left">Inhibition of intracellular development</td><td align="left">> 95% inhibition at 15 µM</td><td align="left">[<xref ref-type="bibr" rid="CR163">163</xref>]</td></tr><tr><td align="left">Triacetylbalsaminol F</td><td align="left"><italic>P. berghei</italic></td><td align="left">Liver stage</td><td align="left">Inhibition of intracellular development</td><td align="left">> 95% inhibition at 15 µM</td><td align="left">[<xref ref-type="bibr" rid="CR163">163</xref>]</td></tr><tr><td align="left">6-Deoxy-8-<italic>O</italic>-methylrabelomycin</td><td align="left"><italic>P. berghei</italic></td><td align="left">Liver stage</td><td align="left"></td><td align="left">18.5 µM</td><td align="left">[<xref ref-type="bibr" rid="CR317">317</xref>]</td></tr><tr><td align="left">X-14881 E</td><td align="left"><italic>P. berghei</italic></td><td align="left">Liver stage</td><td align="left"></td><td align="left">3.0 µM</td><td align="left">[<xref ref-type="bibr" rid="CR317">317</xref>]</td></tr><tr><td align="left">Marilone A</td><td align="left"><italic>P. berghei</italic></td><td align="left">Liver stage</td><td align="left">Inhibition of liver cell infection</td><td align="left">12.1 µM</td><td align="left">[<xref ref-type="bibr" rid="CR318">318</xref>]</td></tr></tbody></table></table-wrap></p></sec><sec id="Sec44" sec-type="conclusion"><title>Conclusions</title><p id="Par122">The present review covered the antiplasmodial natural products reported between 2010 and 2017. A breakdown of the statistics of compounds and the biological source reported per year is given in Fig. <xref rid="Fig61" ref-type="fig">61</xref>.<fig id="Fig61"><label>Fig. 61</label><caption><p>Summary of biological sources from which antiplasmodial natural products were isolated between 2010 and 2017</p></caption><graphic xlink:href="12936_2019_3026_Fig61_HTML" id="MO61"></graphic></fig></p><p id="Par123">A total of 447 compounds derived from plant, microrganisms, and marine organisms were found to have IC<sub>50</sub> ≤ 3.0 µM against at least one strain of asexual blood-stage <italic>P. falciparum</italic>. Some of these compounds showed potent selective activity against parasites. However, others were equally cytotoxic against cancerous and/or noncancerous cells. Notwithstanding the cytotoxicity, we have considered these compounds to be promising anti-malarial hits of which the cytotoxicity could be mitigated by medicinal chemistry approaches, as was demonstrated, for example, with ferruginol (<bold>230</bold>) and carmaphycin B (<bold>447</bold>) [<xref ref-type="bibr" rid="CR149">149</xref>, <xref ref-type="bibr" rid="CR277">277</xref>]. Also, some of these compounds could serve as templates for designing novel antiplasmodial pharmacophores using the strategy of diversity-oriented synthesis. More than half of the compounds belong to three major chemical classes comprising alkaloids (31.9%), terpenoids (30.8%), and polyphenols (17.4%). This is consistent with the phytochemical distribution of antiplasmodial compounds from earlier reviews [<xref ref-type="bibr" rid="CR12">12</xref>, <xref ref-type="bibr" rid="CR13">13</xref>]. This review also discussed compounds with potent selective antiplasmodial activities that belong to classes from which antiplasmodial activity has not been previously reported. Such novel antiplasmodial scaffolds, e.g. the tropolones and cyclic phosphotriesters, are important in the battle against malaria because these compounds might possess a novel mechanism of action and expand the therapeutic arsenal against the disease.</p><p id="Par124">Many of the plants were investigated based on the ethnobotanical history of use against malaria, while the non-plant materials were mostly investigated because of their chemical profiles. This underscores the need to employ the dual approach of ethnobotanical reputation and chemical profiling in the search for anti-malarial natural products. Although fewer marine and microorganisms have been screened for antiplasmodial compounds compared to plants, the diverse nature of metabolites produced by these alternative sources presents a compelling case for intensive exploration. Only a small number of in vivo studies to validate the in vitro efficacy of these compounds have been conducted. This is not surprising considering that natural products are usually isolated in small amounts, which is barely sufficient for in vitro testing. Nevertheless, the need for in vivo confirmation of observed in vitro potency could not be overemphasized. Therefore, efficient total synthesis of the most promising compounds identified in this review should be prioritized.</p><p id="Par125">It is now accepted that the <italic>Plasmodium</italic> parasite transmission from an infected host to uninfected mosquitoes should be blocked to curtail the spread of malaria. Compounds with activity against sexual and liver stage parasites are therefore crucial to the malaria eradication agenda. Sadly, only a few chemical compounds have a proven ability to kill liver and sexual stage parasites. In spite of the fruitful relationship between malaria chemotherapy and natural products, only a few natural products have been evaluated for activity against the parasite gametocytes and liver forms. As this review has shown, the few investigated natural products have shown promise. Therefore, the exploration of natural products in this regard cannot be overemphasized. The compounds covered in this review will be a good starting point, since natural products, unlike the synthetic counterparts, might have multi-stage activity. Priority should be given to compounds of which the mode of action does not involve the inhibition of haemozoin formation since stage V gametes, which are the transmissible form of the parasite, do not digest haemoglobin. Standardized assay methods for evaluating late stage gametocidal and liver stage activities have been developed that will aid in the high-throughput screening of natural products [<xref ref-type="bibr" rid="CR319">319</xref>, <xref ref-type="bibr" rid="CR320">320</xref>].</p></sec><sec sec-type="supplementary-material"><title>Supplementary information</title><sec id="Sec45"><p><supplementary-material content-type="local-data" id="MOESM1"><media xlink:href="12936_2019_3026_MOESM1_ESM.docx"><caption><p><bold>Additional file 1.</bold> Antiplasmodial activity reported (2010–2017) for all natural products, irrespective of level of activity (no cutoff value for activity).</p></caption></media></supplementary-material></p></sec></sec></body><back><glossary><title>Abbreviations</title><def-list><def-item><term>ACT</term><def><p id="Par4">artemisinin-based combination therapy</p></def></def-item><def-item><term>ATPase</term><def><p id="Par5">adenosine triphosphatase</p></def></def-item><def-item><term>CGX</term><def><p id="Par6">Garcinia xanthones</p></def></def-item><def-item><term>DDT</term><def><p id="Par7">dichlorodiphenyltrichloroethane</p></def></def-item><def-item><term>DGAT</term><def><p id="Par8">diacylglycerol <italic>O</italic>-acyltransferase</p></def></def-item><def-item><term>DNA</term><def><p id="Par9">deoxyribonucleic acid</p></def></def-item><def-item><term>EGCG</term><def><p id="Par10">epigallocatechin-3-gallate</p></def></def-item><def-item><term>ELISA</term><def><p id="Par11">enzyme-linked immunosorbent assays</p></def></def-item><def-item><term>Glu</term><def><p id="Par12">glutamic acid</p></def></def-item><def-item><term>HRP2</term><def><p id="Par13">histidine-rich protein 2</p></def></def-item><def-item><term>Ile</term><def><p id="Par14">isoleucine</p></def></def-item><def-item><term>LC-MS</term><def><p id="Par15">liquid chromatography-mass spectrometry</p></def></def-item><def-item><term>Leu</term><def><p id="Par16">leucine</p></def></def-item><def-item><term>Met</term><def><p id="Par17">methionine</p></def></def-item><def-item><term>MeTyr</term><def><p id="Par18">methyl tyrosine</p></def></def-item><def-item><term>Nle</term><def><p id="Par19">norleucine</p></def></def-item><def-item><term>µM</term><def><p id="Par20">micromolar</p></def></def-item><def-item><term>nM</term><def><p id="Par21">nanomolar</p></def></def-item><def-item><term>NMR</term><def><p id="Par22">nuclear magnetic resonance spectroscopy</p></def></def-item><def-item><term>PfDGAT</term><def><p id="Par23"><italic>Plasmodium falciparum</italic> diacylglycerol <italic>O</italic>-acyltransferase</p></def></def-item><def-item><term>PfHsp</term><def><p id="Par24"><italic>Plasmodium falciparum</italic> heat shock protein</p></def></def-item><def-item><term>Phe</term><def><p id="Par25">phenylalanine</p></def></def-item><def-item><term>pLDH</term><def><p id="Par26">Plasmodium lactate dehydrogenase protein</p></def></def-item><def-item><term>PPAP</term><def><p id="Par27">polyprenylated acylphloroglucinol</p></def></def-item><def-item><term>Pro</term><def><p id="Par28">proline</p></def></def-item><def-item><term>ROS</term><def><p id="Par29">recactive oxygen species</p></def></def-item><def-item><term>SAR</term><def><p id="Par30">structure–activity relationship</p></def></def-item><def-item><term>SI</term><def><p id="Par31">selectivity index</p></def></def-item><def-item><term>Thr</term><def><p id="Par32">threonine</p></def></def-item><def-item><term>USA</term><def><p id="Par33">United States of America</p></def></def-item><def-item><term>Val</term><def><p id="Par34">valine</p></def></def-item><def-item><term>WHO</term><def><p id="Par35">World Health Organization</p></def></def-item></def-list></glossary><fn-group><fn><p><bold>Publisher's Note</bold></p><p>Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.</p></fn></fn-group><sec><title>Supplementary information</title><p><bold>Supplementary information</bold> accompanies this paper at 10.1186/s12936-019-3026-1.</p></sec><notes notes-type="author-contribution"><title>Authors’ contributions</title><p>The two authors have equally contributed to the concept and writing of the review. Both authors read and approved the final manuscript.</p></notes><notes notes-type="funding-information"><title>Funding</title><p>Financial support by the University of KwaZulu-Natal and the National Research Foundation of South Africa (NRF) (Grant No: 98345, 2016–2020) is acknowledged.</p></notes><notes notes-type="data-availability"><title>Availability of data and materials</title><p>Not applicable.</p></notes><notes><title>Ethics approval and consent to participate</title><p id="Par126">Not applicable.</p></notes><notes><title>Consent for publication</title><p id="Par127">Not applicable.</p></notes><notes notes-type="COI-statement"><title>Competing interests</title><p id="Par128">The authors declare that they have no competing interests.</p></notes><ref-list id="Bib1"><title>References</title><ref id="CR1"><label>1.</label><element-citation publication-type="book"><person-group person-group-type="author"><collab>WHO</collab></person-group><source>World Malaria Report 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