Potent antiviral activity of carbohydrate-specific algal and leguminous lectins from the Brazilian biodiversity.
Identifieur interne : 000C36 ( PubMed/Checkpoint ); précédent : 000C35; suivant : 000C37Potent antiviral activity of carbohydrate-specific algal and leguminous lectins from the Brazilian biodiversity.
Auteurs : Ana C S. Gondim [Oman] ; Suzete Roberta Da Silva [Brésil] ; Leen Mathys [Belgique] ; Sam Noppen [Belgique] ; Sandra Liekens [Belgique] ; Alexandre Holanda Sampaio [Brésil] ; Celso S. Nagano [Brésil] ; Cintia Renata Costa Rocha [Brésil] ; Kyria S. Nascimento [Oman] ; Benildo S. Cavada [Oman] ; Peter J. Sadler [Royaume-Uni] ; Jan Balzarini [Belgique]Source :
- MedChemComm [ 2040-2511 ] ; 2019.
Abstract
Brazil has one of the largest biodiversities in the world. The search for new natural products extracted from the Brazilian flora may lead to the discovery of novel drugs with potential to treat infectious and other diseases. Here, we have investigated 9 lectins extracted and purified from the Northeastern Brazilian flora, from both leguminous species: Canavalia brasiliensis (ConBr), C. maritima (ConM), Dioclea lasiocarpa (DLasiL) and D. sclerocarpa (DSclerL), and algae Amansia multifida (AML), Bryothamniom seaforthii (BSL), Hypnea musciformis (HML), Meristiella echinocarpa (MEL) and Solieria filiformis (SfL). They were exposed to a panel of 18 different viruses, including HIV and influenza viruses. Several lectins showed highly potent antiviral activity, often within the low nanomolar range. DSclerL and DLasiL exhibited EC50 values (effective concentration of lectin required to inhibit virus-induced cytopathicity by 50%) of 9 nM to 46 nM for HIV-1 and respiratory syncytial virus (RSV), respectively, DLasiL also inhibited feline corona virus at an EC50 of 5 nM, and DSclerL, ConBr and ConM showed remarkably low EC50 values ranging from 0.4 to 6 nM against influenza A virus strain H3N2 and influenza B virus. For HIV, evidence pointed to the blockage of entry of the virus into its target cells as the underlying mechanism of antiviral action of these lectins. Overall, the most promising lectins based on their EC50 values were DLasiL, DSclerL, ConBr, ConM, SfL and HML. These novel findings indicate that lectins from the Brazilian flora may provide novel antiviral compounds with therapeutic potential.
DOI: 10.1039/c8md00508g
PubMed: 30996857
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Potent antiviral activity of carbohydrate-specific algal and leguminous lectins from the Brazilian biodiversity.</title><author><name sortKey="Gondim, Ana C S" sort="Gondim, Ana C S" uniqKey="Gondim A" first="Ana C S" last="Gondim">Ana C S. Gondim</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biochemistry and Molecular Biology , Federal University of Ceará , 60455-760 , Fortaleza , Ceará , Brazil . Email: bscavada@gmail.com.</nlm:affiliation><country wicri:rule="url">Oman</country></affiliation></author><author><name sortKey="Roberta Da Silva, Suzete" sort="Roberta Da Silva, Suzete" uniqKey="Roberta Da Silva S" first="Suzete" last="Roberta Da Silva">Suzete Roberta Da Silva</name><affiliation wicri:level="1"><nlm:affiliation>Department of Fishing and Engineering , Federal University of Ceará , 60455-900 , Fortaleza , Ceará , Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Department of Fishing and Engineering , Federal University of Ceará , 60455-900 , Fortaleza , Ceará </wicri:regionArea><wicri:noRegion>Ceará </wicri:noRegion></affiliation></author><author><name sortKey="Mathys, Leen" sort="Mathys, Leen" uniqKey="Mathys L" first="Leen" last="Mathys">Leen Mathys</name><affiliation wicri:level="1"><nlm:affiliation>Rega Institute for Medical Research , Department of Microbiology and Immunology , KU Leuven , 3000 Leuven , Belgium . Email: jan.balzarini@kuleuven.be.</nlm:affiliation><country wicri:rule="url">Belgique</country></affiliation></author><author><name sortKey="Noppen, Sam" sort="Noppen, Sam" uniqKey="Noppen S" first="Sam" last="Noppen">Sam Noppen</name><affiliation wicri:level="1"><nlm:affiliation>Rega Institute for Medical Research , Department of Microbiology and Immunology , KU Leuven , 3000 Leuven , Belgium . Email: jan.balzarini@kuleuven.be.</nlm:affiliation><country wicri:rule="url">Belgique</country></affiliation></author><author><name sortKey="Liekens, Sandra" sort="Liekens, Sandra" uniqKey="Liekens S" first="Sandra" last="Liekens">Sandra Liekens</name><affiliation wicri:level="1"><nlm:affiliation>Rega Institute for Medical Research , Department of Microbiology and Immunology , KU Leuven , 3000 Leuven , Belgium . 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Nagano</name><affiliation wicri:level="1"><nlm:affiliation>Department of Fishing and Engineering , Federal University of Ceará , 60455-900 , Fortaleza , Ceará , Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Department of Fishing and Engineering , Federal University of Ceará , 60455-900 , Fortaleza , Ceará </wicri:regionArea><wicri:noRegion>Ceará </wicri:noRegion></affiliation></author><author><name sortKey="Renata Costa Rocha, Cintia" sort="Renata Costa Rocha, Cintia" uniqKey="Renata Costa Rocha C" first="Cintia" last="Renata Costa Rocha">Cintia Renata Costa Rocha</name><affiliation wicri:level="1"><nlm:affiliation>Biochemistry Department , LINKA/UFPE , CEP 50670-901 , Recife , Pernambuco , Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Biochemistry Department , LINKA/UFPE , CEP 50670-901 , Recife , Pernambuco </wicri:regionArea><wicri:noRegion>Pernambuco </wicri:noRegion></affiliation></author><author><name sortKey="Nascimento, Kyria S" sort="Nascimento, Kyria S" uniqKey="Nascimento K" first="Kyria S" last="Nascimento">Kyria S. Nascimento</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biochemistry and Molecular Biology , Federal University of Ceará , 60455-760 , Fortaleza , Ceará , Brazil . Email: bscavada@gmail.com.</nlm:affiliation><country wicri:rule="url">Oman</country></affiliation></author><author><name sortKey="Cavada, Benildo S" sort="Cavada, Benildo S" uniqKey="Cavada B" first="Benildo S" last="Cavada">Benildo S. Cavada</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biochemistry and Molecular Biology , Federal University of Ceará , 60455-760 , Fortaleza , Ceará , Brazil . Email: bscavada@gmail.com.</nlm:affiliation><country wicri:rule="url">Oman</country></affiliation></author><author><name sortKey="Sadler, Peter J" sort="Sadler, Peter J" uniqKey="Sadler P" first="Peter J" last="Sadler">Peter J. Sadler</name><affiliation wicri:level="1"><nlm:affiliation>Department of Chemistry , University of Warwick , Coventry CV4 7AL , UK . Email: P.J.Sadler@warwick.ac.uk.</nlm:affiliation><country>Royaume-Uni</country><wicri:regionArea>Department of Chemistry , University of Warwick , Coventry CV4 7AL </wicri:regionArea><wicri:noRegion>Coventry CV4 7AL </wicri:noRegion></affiliation></author><author><name sortKey="Balzarini, Jan" sort="Balzarini, Jan" uniqKey="Balzarini J" first="Jan" last="Balzarini">Jan Balzarini</name><affiliation wicri:level="1"><nlm:affiliation>Rega Institute for Medical Research , Department of Microbiology and Immunology , KU Leuven , 3000 Leuven , Belgium . 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Gondim</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biochemistry and Molecular Biology , Federal University of Ceará , 60455-760 , Fortaleza , Ceará , Brazil . Email: bscavada@gmail.com.</nlm:affiliation><country wicri:rule="url">Oman</country></affiliation></author><author><name sortKey="Roberta Da Silva, Suzete" sort="Roberta Da Silva, Suzete" uniqKey="Roberta Da Silva S" first="Suzete" last="Roberta Da Silva">Suzete Roberta Da Silva</name><affiliation wicri:level="1"><nlm:affiliation>Department of Fishing and Engineering , Federal University of Ceará , 60455-900 , Fortaleza , Ceará , Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Department of Fishing and Engineering , Federal University of Ceará , 60455-900 , Fortaleza , Ceará </wicri:regionArea><wicri:noRegion>Ceará </wicri:noRegion></affiliation></author><author><name sortKey="Mathys, Leen" sort="Mathys, Leen" uniqKey="Mathys L" first="Leen" last="Mathys">Leen Mathys</name><affiliation wicri:level="1"><nlm:affiliation>Rega Institute for Medical Research , Department of Microbiology and Immunology , KU Leuven , 3000 Leuven , Belgium . Email: jan.balzarini@kuleuven.be.</nlm:affiliation><country wicri:rule="url">Belgique</country></affiliation></author><author><name sortKey="Noppen, Sam" sort="Noppen, Sam" uniqKey="Noppen S" first="Sam" last="Noppen">Sam Noppen</name><affiliation wicri:level="1"><nlm:affiliation>Rega Institute for Medical Research , Department of Microbiology and Immunology , KU Leuven , 3000 Leuven , Belgium . Email: jan.balzarini@kuleuven.be.</nlm:affiliation><country wicri:rule="url">Belgique</country></affiliation></author><author><name sortKey="Liekens, Sandra" sort="Liekens, Sandra" uniqKey="Liekens S" first="Sandra" last="Liekens">Sandra Liekens</name><affiliation wicri:level="1"><nlm:affiliation>Rega Institute for Medical Research , Department of Microbiology and Immunology , KU Leuven , 3000 Leuven , Belgium . Email: jan.balzarini@kuleuven.be.</nlm:affiliation><country wicri:rule="url">Belgique</country></affiliation></author><author><name sortKey="Holanda Sampaio, Alexandre" sort="Holanda Sampaio, Alexandre" uniqKey="Holanda Sampaio A" first="Alexandre" last="Holanda Sampaio">Alexandre Holanda Sampaio</name><affiliation wicri:level="1"><nlm:affiliation>Department of Fishing and Engineering , Federal University of Ceará , 60455-900 , Fortaleza , Ceará , Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Department of Fishing and Engineering , Federal University of Ceará , 60455-900 , Fortaleza , Ceará </wicri:regionArea><wicri:noRegion>Ceará </wicri:noRegion></affiliation></author><author><name sortKey="Nagano, Celso S" sort="Nagano, Celso S" uniqKey="Nagano C" first="Celso S" last="Nagano">Celso S. Nagano</name><affiliation wicri:level="1"><nlm:affiliation>Department of Fishing and Engineering , Federal University of Ceará , 60455-900 , Fortaleza , Ceará , Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Department of Fishing and Engineering , Federal University of Ceará , 60455-900 , Fortaleza , Ceará </wicri:regionArea><wicri:noRegion>Ceará </wicri:noRegion></affiliation></author><author><name sortKey="Renata Costa Rocha, Cintia" sort="Renata Costa Rocha, Cintia" uniqKey="Renata Costa Rocha C" first="Cintia" last="Renata Costa Rocha">Cintia Renata Costa Rocha</name><affiliation wicri:level="1"><nlm:affiliation>Biochemistry Department , LINKA/UFPE , CEP 50670-901 , Recife , Pernambuco , Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Biochemistry Department , LINKA/UFPE , CEP 50670-901 , Recife , Pernambuco </wicri:regionArea><wicri:noRegion>Pernambuco </wicri:noRegion></affiliation></author><author><name sortKey="Nascimento, Kyria S" sort="Nascimento, Kyria S" uniqKey="Nascimento K" first="Kyria S" last="Nascimento">Kyria S. Nascimento</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biochemistry and Molecular Biology , Federal University of Ceará , 60455-760 , Fortaleza , Ceará , Brazil . Email: bscavada@gmail.com.</nlm:affiliation><country wicri:rule="url">Oman</country></affiliation></author><author><name sortKey="Cavada, Benildo S" sort="Cavada, Benildo S" uniqKey="Cavada B" first="Benildo S" last="Cavada">Benildo S. Cavada</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biochemistry and Molecular Biology , Federal University of Ceará , 60455-760 , Fortaleza , Ceará , Brazil . Email: bscavada@gmail.com.</nlm:affiliation><country wicri:rule="url">Oman</country></affiliation></author><author><name sortKey="Sadler, Peter J" sort="Sadler, Peter J" uniqKey="Sadler P" first="Peter J" last="Sadler">Peter J. Sadler</name><affiliation wicri:level="1"><nlm:affiliation>Department of Chemistry , University of Warwick , Coventry CV4 7AL , UK . Email: P.J.Sadler@warwick.ac.uk.</nlm:affiliation><country>Royaume-Uni</country><wicri:regionArea>Department of Chemistry , University of Warwick , Coventry CV4 7AL </wicri:regionArea><wicri:noRegion>Coventry CV4 7AL </wicri:noRegion></affiliation></author><author><name sortKey="Balzarini, Jan" sort="Balzarini, Jan" uniqKey="Balzarini J" first="Jan" last="Balzarini">Jan Balzarini</name><affiliation wicri:level="1"><nlm:affiliation>Rega Institute for Medical Research , Department of Microbiology and Immunology , KU Leuven , 3000 Leuven , Belgium . Email: jan.balzarini@kuleuven.be.</nlm:affiliation><country wicri:rule="url">Belgique</country></affiliation></author></analytic><series><title level="j">MedChemComm</title><idno type="eISSN">2040-2511</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Brazil has one of the largest biodiversities in the world. The search for new natural products extracted from the Brazilian flora may lead to the discovery of novel drugs with potential to treat infectious and other diseases. Here, we have investigated 9 lectins extracted and purified from the Northeastern Brazilian flora, from both leguminous species: <i>Canavalia brasiliensis</i> (ConBr), <i>C. maritima</i> (ConM), <i>Dioclea lasiocarpa</i> (DLasiL) and <i>D. sclerocarpa</i> (DSclerL), and algae <i>Amansia multifida</i> (AML), <i>Bryothamniom seaforthii</i> (BSL), <i>Hypnea musciformis</i> (HML), <i>Meristiella echinocarpa</i> (MEL) and <i>Solieria filiformis</i> (SfL). They were exposed to a panel of 18 different viruses, including HIV and influenza viruses. Several lectins showed highly potent antiviral activity, often within the low nanomolar range. DSclerL and DLasiL exhibited EC<sub>50</sub> values (effective concentration of lectin required to inhibit virus-induced cytopathicity by 50%) of 9 nM to 46 nM for HIV-1 and respiratory syncytial virus (RSV), respectively, DLasiL also inhibited feline corona virus at an EC<sub>50</sub> of 5 nM, and DSclerL, ConBr and ConM showed remarkably low EC<sub>50</sub> values ranging from 0.4 to 6 nM against influenza A virus strain H3N2 and influenza B virus. For HIV, evidence pointed to the blockage of entry of the virus into its target cells as the underlying mechanism of antiviral action of these lectins. Overall, the most promising lectins based on their EC<sub>50</sub> values were DLasiL, DSclerL, ConBr, ConM, SfL and HML. These novel findings indicate that lectins from the Brazilian flora may provide novel antiviral compounds with therapeutic potential.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">30996857</PMID><DateRevised><Year>2020</Year><Month>02</Month><Day>25</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Electronic">2040-2511</ISSN><JournalIssue CitedMedium="Internet"><Volume>10</Volume><Issue>3</Issue><PubDate><Year>2019</Year><Month>Mar</Month><Day>01</Day></PubDate></JournalIssue><Title>MedChemComm</Title><ISOAbbreviation>Medchemcomm</ISOAbbreviation></Journal><ArticleTitle>Potent antiviral activity of carbohydrate-specific algal and leguminous lectins from the Brazilian biodiversity.</ArticleTitle><Pagination><MedlinePgn>390-398</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1039/c8md00508g</ELocationID><Abstract><AbstractText>Brazil has one of the largest biodiversities in the world. The search for new natural products extracted from the Brazilian flora may lead to the discovery of novel drugs with potential to treat infectious and other diseases. Here, we have investigated 9 lectins extracted and purified from the Northeastern Brazilian flora, from both leguminous species: <i>Canavalia brasiliensis</i> (ConBr), <i>C. maritima</i> (ConM), <i>Dioclea lasiocarpa</i> (DLasiL) and <i>D. sclerocarpa</i> (DSclerL), and algae <i>Amansia multifida</i> (AML), <i>Bryothamniom seaforthii</i> (BSL), <i>Hypnea musciformis</i> (HML), <i>Meristiella echinocarpa</i> (MEL) and <i>Solieria filiformis</i> (SfL). They were exposed to a panel of 18 different viruses, including HIV and influenza viruses. Several lectins showed highly potent antiviral activity, often within the low nanomolar range. DSclerL and DLasiL exhibited EC<sub>50</sub> values (effective concentration of lectin required to inhibit virus-induced cytopathicity by 50%) of 9 nM to 46 nM for HIV-1 and respiratory syncytial virus (RSV), respectively, DLasiL also inhibited feline corona virus at an EC<sub>50</sub> of 5 nM, and DSclerL, ConBr and ConM showed remarkably low EC<sub>50</sub> values ranging from 0.4 to 6 nM against influenza A virus strain H3N2 and influenza B virus. For HIV, evidence pointed to the blockage of entry of the virus into its target cells as the underlying mechanism of antiviral action of these lectins. Overall, the most promising lectins based on their EC<sub>50</sub> values were DLasiL, DSclerL, ConBr, ConM, SfL and HML. These novel findings indicate that lectins from the Brazilian flora may provide novel antiviral compounds with therapeutic potential.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Gondim</LastName><ForeName>Ana C S</ForeName><Initials>ACS</Initials><Identifier Source="ORCID">0000-0003-3526-1203</Identifier><AffiliationInfo><Affiliation>Department of Biochemistry and Molecular Biology , Federal University of Ceará , 60455-760 , Fortaleza , Ceará , Brazil . Email: bscavada@gmail.com.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Chemistry , University of Warwick , Coventry CV4 7AL , UK . Email: P.J.Sadler@warwick.ac.uk.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Organic and Inorganic Chemistry , Federal University of Ceará , 60455-900 , Fortaleza , Ceará , Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Roberta da Silva</LastName><ForeName>Suzete</ForeName><Initials>S</Initials><Identifier Source="ORCID">0000-0002-6254-1975</Identifier><AffiliationInfo><Affiliation>Department of Fishing and Engineering , Federal University of Ceará , 60455-900 , Fortaleza , Ceará , Brazil.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Para West Federal University , 68220-000 , Monte Alegre , Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mathys</LastName><ForeName>Leen</ForeName><Initials>L</Initials><Identifier Source="ORCID">0000-0002-5123-8751</Identifier><AffiliationInfo><Affiliation>Rega Institute for Medical Research , Department of Microbiology and Immunology , KU Leuven , 3000 Leuven , Belgium . Email: jan.balzarini@kuleuven.be.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Noppen</LastName><ForeName>Sam</ForeName><Initials>S</Initials><Identifier Source="ORCID">0000-0002-2831-5042</Identifier><AffiliationInfo><Affiliation>Rega Institute for Medical Research , Department of Microbiology and Immunology , KU Leuven , 3000 Leuven , Belgium . Email: jan.balzarini@kuleuven.be.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liekens</LastName><ForeName>Sandra</ForeName><Initials>S</Initials><Identifier Source="ORCID">0000-0002-3529-8121</Identifier><AffiliationInfo><Affiliation>Rega Institute for Medical Research , Department of Microbiology and Immunology , KU Leuven , 3000 Leuven , Belgium . Email: jan.balzarini@kuleuven.be.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Holanda Sampaio</LastName><ForeName>Alexandre</ForeName><Initials>A</Initials><Identifier Source="ORCID">0000-0003-3871-0502</Identifier><AffiliationInfo><Affiliation>Department of Fishing and Engineering , Federal University of Ceará , 60455-900 , Fortaleza , Ceará , Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nagano</LastName><ForeName>Celso S</ForeName><Initials>CS</Initials><Identifier Source="ORCID">0000-0001-5988-5868</Identifier><AffiliationInfo><Affiliation>Department of Fishing and Engineering , Federal University of Ceará , 60455-900 , Fortaleza , Ceará , Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Renata Costa Rocha</LastName><ForeName>Cintia</ForeName><Initials>C</Initials><Identifier Source="ORCID">0000-0002-3366-3615</Identifier><AffiliationInfo><Affiliation>Biochemistry Department , LINKA/UFPE , CEP 50670-901 , Recife , Pernambuco , Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nascimento</LastName><ForeName>Kyria S</ForeName><Initials>KS</Initials><Identifier Source="ORCID">0000-0002-2220-4552</Identifier><AffiliationInfo><Affiliation>Department of Biochemistry and Molecular Biology , Federal University of Ceará , 60455-760 , Fortaleza , Ceará , Brazil . Email: bscavada@gmail.com.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Cavada</LastName><ForeName>Benildo S</ForeName><Initials>BS</Initials><Identifier Source="ORCID">0000-0002-5791-6170</Identifier><AffiliationInfo><Affiliation>Department of Biochemistry and Molecular Biology , Federal University of Ceará , 60455-760 , Fortaleza , Ceará , Brazil . Email: bscavada@gmail.com.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sadler</LastName><ForeName>Peter J</ForeName><Initials>PJ</Initials><Identifier Source="ORCID">0000-0001-9160-1941</Identifier><AffiliationInfo><Affiliation>Department of Chemistry , University of Warwick , Coventry CV4 7AL , UK . Email: P.J.Sadler@warwick.ac.uk.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Balzarini</LastName><ForeName>Jan</ForeName><Initials>J</Initials><Identifier Source="ORCID">0000-0003-1144-1808</Identifier><AffiliationInfo><Affiliation>Rega Institute for Medical Research , Department of Microbiology and Immunology , KU Leuven , 3000 Leuven , Belgium . Email: jan.balzarini@kuleuven.be.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>01</Month><Day>14</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Medchemcomm</MedlineTA><NlmUniqueID>101531525</NlmUniqueID><ISSNLinking>2040-2503</ISSNLinking></MedlineJournalInfo></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year><Month>10</Month><Day>08</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2018</Year><Month>12</Month><Day>11</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>4</Month><Day>19</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate 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