Annona coriacea Mart. Fractions Promote Cell Cycle Arrest and Inhibit Autophagic Flux in Human Cervical Cancer Cell Lines
Identifieur interne : 000B70 ( Ncbi/Merge ); précédent : 000B69; suivant : 000B71Annona coriacea Mart. Fractions Promote Cell Cycle Arrest and Inhibit Autophagic Flux in Human Cervical Cancer Cell Lines
Auteurs : Izabela N. Faria Gomes ; Renato J. Silva-Oliveira ; Viviane A. Oliveira Silva ; Marcela N. Rosa ; Patrik S. Vital ; Maria Cristina S. Barbosa ; Fábio Vieira Dos Santos ; João Gabriel M. Junqueira ; Vanessa G. P. Severino ; Bruno G. Oliveira ; Wanderson Romão ; Rui Manuel Reis [Portugal] ; Rosy Iara Maciel De Azambuja RibeiroSource :
- Molecules [ 1420-3049 ] ; 2019.
Abstract
Plant-based compounds are an option to explore and perhaps overcome the limitations of current antitumor treatments.
Url:
DOI: 10.3390/molecules24213963
PubMed: 31683835
PubMed Central: 6864525
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en"><italic>Annona coriacea</italic> Mart. Fractions Promote Cell Cycle Arrest and Inhibit Autophagic Flux in Human Cervical Cancer Cell Lines</title><author><name sortKey="Gomes, Izabela N Faria" sort="Gomes, Izabela N Faria" uniqKey="Gomes I" first="Izabela N. Faria" last="Gomes">Izabela N. Faria Gomes</name><affiliation><nlm:aff id="af1-molecules-24-03963">Experimental Pathology Laboratory, Federal University of São João del Rei—CCO/UFSJ, Divinópolis 35501-296, Brazil;<email>izabela.faria.tk@hotmail.com</email> (I.N.F.G.);<email>patrikdasilvavital@gmail.com</email> (P.S.V.)</nlm:aff></affiliation><affiliation><nlm:aff id="af2-molecules-24-03963">Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos 14784-400, Brazil;<email>renatokjso@gmail.com</email> (R.J.S.-O.);<email>vivianeaos@gmail.com</email> (V.A.O.S.);<email>nr.marcela@gmail.com</email> (M.N.R.)</nlm:aff></affiliation></author><author><name sortKey="Silva Oliveira, Renato J" sort="Silva Oliveira, Renato J" uniqKey="Silva Oliveira R" first="Renato J." last="Silva-Oliveira">Renato J. Silva-Oliveira</name><affiliation><nlm:aff id="af2-molecules-24-03963">Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos 14784-400, Brazil;<email>renatokjso@gmail.com</email> (R.J.S.-O.);<email>vivianeaos@gmail.com</email> (V.A.O.S.);<email>nr.marcela@gmail.com</email> (M.N.R.)</nlm:aff></affiliation></author><author><name sortKey="Oliveira Silva, Viviane A" sort="Oliveira Silva, Viviane A" uniqKey="Oliveira Silva V" first="Viviane A." last="Oliveira Silva">Viviane A. Oliveira Silva</name><affiliation><nlm:aff id="af2-molecules-24-03963">Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos 14784-400, Brazil;<email>renatokjso@gmail.com</email> (R.J.S.-O.);<email>vivianeaos@gmail.com</email> (V.A.O.S.);<email>nr.marcela@gmail.com</email> (M.N.R.)</nlm:aff></affiliation></author><author><name sortKey="Rosa, Marcela N" sort="Rosa, Marcela N" uniqKey="Rosa M" first="Marcela N." last="Rosa">Marcela N. Rosa</name><affiliation><nlm:aff id="af2-molecules-24-03963">Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos 14784-400, Brazil;<email>renatokjso@gmail.com</email> (R.J.S.-O.);<email>vivianeaos@gmail.com</email> (V.A.O.S.);<email>nr.marcela@gmail.com</email> (M.N.R.)</nlm:aff></affiliation></author><author><name sortKey="Vital, Patrik S" sort="Vital, Patrik S" uniqKey="Vital P" first="Patrik S." last="Vital">Patrik S. Vital</name><affiliation><nlm:aff id="af1-molecules-24-03963">Experimental Pathology Laboratory, Federal University of São João del Rei—CCO/UFSJ, Divinópolis 35501-296, Brazil;<email>izabela.faria.tk@hotmail.com</email> (I.N.F.G.);<email>patrikdasilvavital@gmail.com</email> (P.S.V.)</nlm:aff></affiliation></author><author><name sortKey="Barbosa, Maria Cristina S" sort="Barbosa, Maria Cristina S" uniqKey="Barbosa M" first="Maria Cristina S." last="Barbosa">Maria Cristina S. Barbosa</name><affiliation><nlm:aff id="af3-molecules-24-03963">Laboratory of Cell Biology and Mutagenesis, Federal University of São João del Rei—CCO/UFSJ, Divinópolis 35501-296, Brazil;<email>mariacristina@ufsj.edu.br</email> (M.C.S.B.);<email>fabiosantos@ufsj.edu.br</email> (F.V.d.S.)</nlm:aff></affiliation></author><author><name sortKey="Dos Santos, Fabio Vieira" sort="Dos Santos, Fabio Vieira" uniqKey="Dos Santos F" first="Fábio Vieira" last="Dos Santos">Fábio Vieira Dos Santos</name><affiliation><nlm:aff id="af3-molecules-24-03963">Laboratory of Cell Biology and Mutagenesis, Federal University of São João del Rei—CCO/UFSJ, Divinópolis 35501-296, Brazil;<email>mariacristina@ufsj.edu.br</email> (M.C.S.B.);<email>fabiosantos@ufsj.edu.br</email> (F.V.d.S.)</nlm:aff></affiliation></author><author><name sortKey="Junqueira, Joao Gabriel M" sort="Junqueira, Joao Gabriel M" uniqKey="Junqueira J" first="João Gabriel M." last="Junqueira">João Gabriel M. Junqueira</name><affiliation><nlm:aff id="af4-molecules-24-03963">Special Academic Unit of Physics and Chemistry, Federal University of Goiás, Catalão 75704-020, Brazil;<email>jgmjunqueira@gmail.com</email> (J.G.M.J.);<email>vanessa.pasqualotto@gmail.com</email> (V.G.P.S.)</nlm:aff></affiliation></author><author><name sortKey="Severino, Vanessa G P" sort="Severino, Vanessa G P" uniqKey="Severino V" first="Vanessa G. P." last="Severino">Vanessa G. P. Severino</name><affiliation><nlm:aff id="af4-molecules-24-03963">Special Academic Unit of Physics and Chemistry, Federal University of Goiás, Catalão 75704-020, Brazil;<email>jgmjunqueira@gmail.com</email> (J.G.M.J.);<email>vanessa.pasqualotto@gmail.com</email> (V.G.P.S.)</nlm:aff></affiliation></author><author><name sortKey="Oliveira, Bruno G" sort="Oliveira, Bruno G" uniqKey="Oliveira B" first="Bruno G" last="Oliveira">Bruno G. Oliveira</name><affiliation><nlm:aff id="af5-molecules-24-03963">Petroleomic and forensic chemistry laboratory, Department of Chemistry, Federal Institute of Espirito Santo, Vitória, ES 29075-910, Brazil;<email>brunoliveir_ra20@msn.com</email> (B.G.O.);<email>wandersonromao@gmail.com</email> (W.R.)</nlm:aff></affiliation></author><author><name sortKey="Romao, Wanderson" sort="Romao, Wanderson" uniqKey="Romao W" first="Wanderson" last="Romão">Wanderson Romão</name><affiliation><nlm:aff id="af5-molecules-24-03963">Petroleomic and forensic chemistry laboratory, Department of Chemistry, Federal Institute of Espirito Santo, Vitória, ES 29075-910, Brazil;<email>brunoliveir_ra20@msn.com</email> (B.G.O.);<email>wandersonromao@gmail.com</email> (W.R.)</nlm:aff></affiliation></author><author><name sortKey="Reis, Rui Manuel" sort="Reis, Rui Manuel" uniqKey="Reis R" first="Rui Manuel" last="Reis">Rui Manuel Reis</name><affiliation><nlm:aff id="af2-molecules-24-03963">Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos 14784-400, Brazil;<email>renatokjso@gmail.com</email> (R.J.S.-O.);<email>vivianeaos@gmail.com</email> (V.A.O.S.);<email>nr.marcela@gmail.com</email> (M.N.R.)</nlm:aff></affiliation><affiliation wicri:level="4"><nlm:aff id="af6-molecules-24-03963">Life and Health Sciences Research Institute (ICVS), Medical School, University of Minho, 4710-057 Braga, Portugal</nlm:aff><country xml:lang="fr">Portugal</country><wicri:regionArea>Life and Health Sciences Research Institute (ICVS), Medical School, University of Minho, 4710-057 Braga</wicri:regionArea><orgName type="university">Université du Minho</orgName><placeName><settlement type="city">Braga</settlement><region>Région Nord (Portugal)</region></placeName></affiliation><affiliation wicri:level="1"><nlm:aff id="af7-molecules-24-03963">3ICVS/3B’s-PT Government Associate Laboratory, 4710-057 Braga, Portugal</nlm:aff><country xml:lang="fr">Portugal</country><wicri:regionArea>3ICVS/3B’s-PT Government Associate Laboratory, 4710-057 Braga</wicri:regionArea><wicri:noRegion>4710-057 Braga</wicri:noRegion></affiliation></author><author><name sortKey="Ribeiro, Rosy Iara Maciel De Azambuja" sort="Ribeiro, Rosy Iara Maciel De Azambuja" uniqKey="Ribeiro R" first="Rosy Iara Maciel De Azambuja" last="Ribeiro">Rosy Iara Maciel De Azambuja Ribeiro</name><affiliation><nlm:aff id="af1-molecules-24-03963">Experimental Pathology Laboratory, Federal University of São João del Rei—CCO/UFSJ, Divinópolis 35501-296, Brazil;<email>izabela.faria.tk@hotmail.com</email> (I.N.F.G.);<email>patrikdasilvavital@gmail.com</email> (P.S.V.)</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">31683835</idno><idno type="pmc">6864525</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6864525</idno><idno type="RBID">PMC:6864525</idno><idno type="doi">10.3390/molecules24213963</idno><date when="2019">2019</date><idno type="wicri:Area/Pmc/Corpus">000721</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000721</idno><idno type="wicri:Area/Pmc/Curation">000721</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000721</idno><idno type="wicri:Area/Pmc/Checkpoint">000A91</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000A91</idno><idno type="wicri:Area/Ncbi/Merge">000B70</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main"><italic>Annona coriacea</italic> Mart. Fractions Promote Cell Cycle Arrest and Inhibit Autophagic Flux in Human Cervical Cancer Cell Lines</title><author><name sortKey="Gomes, Izabela N Faria" sort="Gomes, Izabela N Faria" uniqKey="Gomes I" first="Izabela N. Faria" last="Gomes">Izabela N. Faria Gomes</name><affiliation><nlm:aff id="af1-molecules-24-03963">Experimental Pathology Laboratory, Federal University of São João del Rei—CCO/UFSJ, Divinópolis 35501-296, Brazil;<email>izabela.faria.tk@hotmail.com</email> (I.N.F.G.);<email>patrikdasilvavital@gmail.com</email> (P.S.V.)</nlm:aff></affiliation><affiliation><nlm:aff id="af2-molecules-24-03963">Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos 14784-400, Brazil;<email>renatokjso@gmail.com</email> (R.J.S.-O.);<email>vivianeaos@gmail.com</email> (V.A.O.S.);<email>nr.marcela@gmail.com</email> (M.N.R.)</nlm:aff></affiliation></author><author><name sortKey="Silva Oliveira, Renato J" sort="Silva Oliveira, Renato J" uniqKey="Silva Oliveira R" first="Renato J." last="Silva-Oliveira">Renato J. Silva-Oliveira</name><affiliation><nlm:aff id="af2-molecules-24-03963">Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos 14784-400, Brazil;<email>renatokjso@gmail.com</email> (R.J.S.-O.);<email>vivianeaos@gmail.com</email> (V.A.O.S.);<email>nr.marcela@gmail.com</email> (M.N.R.)</nlm:aff></affiliation></author><author><name sortKey="Oliveira Silva, Viviane A" sort="Oliveira Silva, Viviane A" uniqKey="Oliveira Silva V" first="Viviane A." last="Oliveira Silva">Viviane A. Oliveira Silva</name><affiliation><nlm:aff id="af2-molecules-24-03963">Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos 14784-400, Brazil;<email>renatokjso@gmail.com</email> (R.J.S.-O.);<email>vivianeaos@gmail.com</email> (V.A.O.S.);<email>nr.marcela@gmail.com</email> (M.N.R.)</nlm:aff></affiliation></author><author><name sortKey="Rosa, Marcela N" sort="Rosa, Marcela N" uniqKey="Rosa M" first="Marcela N." last="Rosa">Marcela N. Rosa</name><affiliation><nlm:aff id="af2-molecules-24-03963">Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos 14784-400, Brazil;<email>renatokjso@gmail.com</email> (R.J.S.-O.);<email>vivianeaos@gmail.com</email> (V.A.O.S.);<email>nr.marcela@gmail.com</email> (M.N.R.)</nlm:aff></affiliation></author><author><name sortKey="Vital, Patrik S" sort="Vital, Patrik S" uniqKey="Vital P" first="Patrik S." last="Vital">Patrik S. Vital</name><affiliation><nlm:aff id="af1-molecules-24-03963">Experimental Pathology Laboratory, Federal University of São João del Rei—CCO/UFSJ, Divinópolis 35501-296, Brazil;<email>izabela.faria.tk@hotmail.com</email> (I.N.F.G.);<email>patrikdasilvavital@gmail.com</email> (P.S.V.)</nlm:aff></affiliation></author><author><name sortKey="Barbosa, Maria Cristina S" sort="Barbosa, Maria Cristina S" uniqKey="Barbosa M" first="Maria Cristina S." last="Barbosa">Maria Cristina S. Barbosa</name><affiliation><nlm:aff id="af3-molecules-24-03963">Laboratory of Cell Biology and Mutagenesis, Federal University of São João del Rei—CCO/UFSJ, Divinópolis 35501-296, Brazil;<email>mariacristina@ufsj.edu.br</email> (M.C.S.B.);<email>fabiosantos@ufsj.edu.br</email> (F.V.d.S.)</nlm:aff></affiliation></author><author><name sortKey="Dos Santos, Fabio Vieira" sort="Dos Santos, Fabio Vieira" uniqKey="Dos Santos F" first="Fábio Vieira" last="Dos Santos">Fábio Vieira Dos Santos</name><affiliation><nlm:aff id="af3-molecules-24-03963">Laboratory of Cell Biology and Mutagenesis, Federal University of São João del Rei—CCO/UFSJ, Divinópolis 35501-296, Brazil;<email>mariacristina@ufsj.edu.br</email> (M.C.S.B.);<email>fabiosantos@ufsj.edu.br</email> (F.V.d.S.)</nlm:aff></affiliation></author><author><name sortKey="Junqueira, Joao Gabriel M" sort="Junqueira, Joao Gabriel M" uniqKey="Junqueira J" first="João Gabriel M." last="Junqueira">João Gabriel M. Junqueira</name><affiliation><nlm:aff id="af4-molecules-24-03963">Special Academic Unit of Physics and Chemistry, Federal University of Goiás, Catalão 75704-020, Brazil;<email>jgmjunqueira@gmail.com</email> (J.G.M.J.);<email>vanessa.pasqualotto@gmail.com</email> (V.G.P.S.)</nlm:aff></affiliation></author><author><name sortKey="Severino, Vanessa G P" sort="Severino, Vanessa G P" uniqKey="Severino V" first="Vanessa G. P." last="Severino">Vanessa G. P. Severino</name><affiliation><nlm:aff id="af4-molecules-24-03963">Special Academic Unit of Physics and Chemistry, Federal University of Goiás, Catalão 75704-020, Brazil;<email>jgmjunqueira@gmail.com</email> (J.G.M.J.);<email>vanessa.pasqualotto@gmail.com</email> (V.G.P.S.)</nlm:aff></affiliation></author><author><name sortKey="Oliveira, Bruno G" sort="Oliveira, Bruno G" uniqKey="Oliveira B" first="Bruno G" last="Oliveira">Bruno G. Oliveira</name><affiliation><nlm:aff id="af5-molecules-24-03963">Petroleomic and forensic chemistry laboratory, Department of Chemistry, Federal Institute of Espirito Santo, Vitória, ES 29075-910, Brazil;<email>brunoliveir_ra20@msn.com</email> (B.G.O.);<email>wandersonromao@gmail.com</email> (W.R.)</nlm:aff></affiliation></author><author><name sortKey="Romao, Wanderson" sort="Romao, Wanderson" uniqKey="Romao W" first="Wanderson" last="Romão">Wanderson Romão</name><affiliation><nlm:aff id="af5-molecules-24-03963">Petroleomic and forensic chemistry laboratory, Department of Chemistry, Federal Institute of Espirito Santo, Vitória, ES 29075-910, Brazil;<email>brunoliveir_ra20@msn.com</email> (B.G.O.);<email>wandersonromao@gmail.com</email> (W.R.)</nlm:aff></affiliation></author><author><name sortKey="Reis, Rui Manuel" sort="Reis, Rui Manuel" uniqKey="Reis R" first="Rui Manuel" last="Reis">Rui Manuel Reis</name><affiliation><nlm:aff id="af2-molecules-24-03963">Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos 14784-400, Brazil;<email>renatokjso@gmail.com</email> (R.J.S.-O.);<email>vivianeaos@gmail.com</email> (V.A.O.S.);<email>nr.marcela@gmail.com</email> (M.N.R.)</nlm:aff></affiliation><affiliation wicri:level="4"><nlm:aff id="af6-molecules-24-03963">Life and Health Sciences Research Institute (ICVS), Medical School, University of Minho, 4710-057 Braga, Portugal</nlm:aff><country xml:lang="fr">Portugal</country><wicri:regionArea>Life and Health Sciences Research Institute (ICVS), Medical School, University of Minho, 4710-057 Braga</wicri:regionArea><orgName type="university">Université du Minho</orgName><placeName><settlement type="city">Braga</settlement><region>Région Nord (Portugal)</region></placeName></affiliation><affiliation wicri:level="1"><nlm:aff id="af7-molecules-24-03963">3ICVS/3B’s-PT Government Associate Laboratory, 4710-057 Braga, Portugal</nlm:aff><country xml:lang="fr">Portugal</country><wicri:regionArea>3ICVS/3B’s-PT Government Associate Laboratory, 4710-057 Braga</wicri:regionArea><wicri:noRegion>4710-057 Braga</wicri:noRegion></affiliation></author><author><name sortKey="Ribeiro, Rosy Iara Maciel De Azambuja" sort="Ribeiro, Rosy Iara Maciel De Azambuja" uniqKey="Ribeiro R" first="Rosy Iara Maciel De Azambuja" last="Ribeiro">Rosy Iara Maciel De Azambuja Ribeiro</name><affiliation><nlm:aff id="af1-molecules-24-03963">Experimental Pathology Laboratory, Federal University of São João del Rei—CCO/UFSJ, Divinópolis 35501-296, Brazil;<email>izabela.faria.tk@hotmail.com</email> (I.N.F.G.);<email>patrikdasilvavital@gmail.com</email> (P.S.V.)</nlm:aff></affiliation></author></analytic><series><title level="j">Molecules</title><idno type="eISSN">1420-3049</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Plant-based compounds are an option to explore and perhaps overcome the limitations of current antitumor treatments. <italic>Annona coriacea</italic> Mart. is a plant with a broad spectrum of biological activities, but its antitumor activity is still unclear. The purpose of our study was to determine the effects of <italic>A. coriacea</italic> fractions on a panel of cervical cancer cell lines and a normal keratinocyte cell line. The antitumor effect was investigated in vitro by viability assays, cell cycle, apoptosis, migration, and invasion assays. Intracellular signaling was assessed by Western blot, and major compounds were identified by mass spectrometry. All fractions exhibited a cytotoxic effect on cisplatin-resistant cell lines, SiHa and HeLa. C3 and C5 were significantly more cytotoxic and selective than cisplatin in SiHa and Hela cells. However, in CaSki, a cisplatin-sensitive cell line, the compounds did not demonstrate higher cytotoxicity when compared with cisplatin. Alkaloids and acetogenins were the main compounds identified in the fractions. These fractions also markedly decreased cell proliferation with p21 increase and cell cycle arrest in G2/M. These effects were accompanied by an increase of H2AX phosphorylation levels and DNA damage index. In addition, fractions C3 and C5 promoted p62 accumulation and decrease of LC3II, as well as acid vesicle levels, indicating the inhibition of autophagic flow. These findings suggest that <italic>A. coriacea</italic> fractions may become effective antineoplastic drugs and highlight the autophagy inhibition properties of these fractions in sensitizing cervical cancer cells to treatment.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Bray, F" uniqKey="Bray F">F. Bray</name></author><author><name sortKey="Ferlay, J" uniqKey="Ferlay J">J. Ferlay</name></author><author><name sortKey="Soerjomataram, I" uniqKey="Soerjomataram I">I. Soerjomataram</name></author><author><name sortKey="Siegel, R L" uniqKey="Siegel R">R.L. Siegel</name></author><author><name sortKey="Torre, L A" uniqKey="Torre L">L.A. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Molecules</journal-id><journal-id journal-id-type="iso-abbrev">Molecules</journal-id><journal-id journal-id-type="publisher-id">molecules</journal-id><journal-title-group><journal-title>Molecules</journal-title></journal-title-group><issn pub-type="epub">1420-3049</issn><publisher><publisher-name>MDPI</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31683835</article-id><article-id pub-id-type="pmc">6864525</article-id><article-id pub-id-type="doi">10.3390/molecules24213963</article-id><article-id pub-id-type="publisher-id">molecules-24-03963</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title><italic>Annona coriacea</italic> Mart. Fractions Promote Cell Cycle Arrest and Inhibit Autophagic Flux in Human Cervical Cancer Cell Lines</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Gomes</surname><given-names>Izabela N. Faria</given-names></name><xref ref-type="aff" rid="af1-molecules-24-03963">1</xref><xref ref-type="aff" rid="af2-molecules-24-03963">2</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0001-6500-4190</contrib-id><name><surname>Silva-Oliveira</surname><given-names>Renato J.</given-names></name><xref ref-type="aff" rid="af2-molecules-24-03963">2</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0001-5919-5242</contrib-id><name><surname>Oliveira Silva</surname><given-names>Viviane A.</given-names></name><xref ref-type="aff" rid="af2-molecules-24-03963">2</xref></contrib><contrib contrib-type="author"><name><surname>Rosa</surname><given-names>Marcela N.</given-names></name><xref ref-type="aff" rid="af2-molecules-24-03963">2</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0001-8390-6980</contrib-id><name><surname>Vital</surname><given-names>Patrik S.</given-names></name><xref ref-type="aff" rid="af1-molecules-24-03963">1</xref></contrib><contrib contrib-type="author"><name><surname>Barbosa</surname><given-names>Maria Cristina S.</given-names></name><xref ref-type="aff" rid="af3-molecules-24-03963">3</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0003-0389-1737</contrib-id><name><surname>dos Santos</surname><given-names>Fábio Vieira</given-names></name><xref ref-type="aff" rid="af3-molecules-24-03963">3</xref></contrib><contrib contrib-type="author"><name><surname>Junqueira</surname><given-names>João Gabriel M.</given-names></name><xref ref-type="aff" rid="af4-molecules-24-03963">4</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0001-5384-6657</contrib-id><name><surname>Severino</surname><given-names>Vanessa G. P.</given-names></name><xref ref-type="aff" rid="af4-molecules-24-03963">4</xref></contrib><contrib contrib-type="author"><name><surname>Oliveira</surname><given-names>Bruno G</given-names></name><xref ref-type="aff" rid="af5-molecules-24-03963">5</xref></contrib><contrib contrib-type="author"><name><surname>Romão</surname><given-names>Wanderson</given-names></name><xref ref-type="aff" rid="af5-molecules-24-03963">5</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0002-9639-7940</contrib-id><name><surname>Reis</surname><given-names>Rui Manuel</given-names></name><xref ref-type="aff" rid="af2-molecules-24-03963">2</xref><xref ref-type="aff" rid="af6-molecules-24-03963">6</xref><xref ref-type="aff" rid="af7-molecules-24-03963">7</xref><xref rid="c1-molecules-24-03963" ref-type="corresp">*</xref></contrib><contrib contrib-type="author"><name><surname>Ribeiro</surname><given-names>Rosy Iara Maciel de Azambuja</given-names></name><xref ref-type="aff" rid="af1-molecules-24-03963">1</xref><xref rid="c1-molecules-24-03963" ref-type="corresp">*</xref></contrib></contrib-group><aff id="af1-molecules-24-03963"><label>1</label>Experimental Pathology Laboratory, Federal University of São João del Rei—CCO/UFSJ, Divinópolis 35501-296, Brazil;<email>izabela.faria.tk@hotmail.com</email> (I.N.F.G.);<email>patrikdasilvavital@gmail.com</email> (P.S.V.)</aff><aff id="af2-molecules-24-03963"><label>2</label>Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos 14784-400, Brazil;<email>renatokjso@gmail.com</email> (R.J.S.-O.);<email>vivianeaos@gmail.com</email> (V.A.O.S.);<email>nr.marcela@gmail.com</email> (M.N.R.)</aff><aff id="af3-molecules-24-03963"><label>3</label>Laboratory of Cell Biology and Mutagenesis, Federal University of São João del Rei—CCO/UFSJ, Divinópolis 35501-296, Brazil;<email>mariacristina@ufsj.edu.br</email> (M.C.S.B.);<email>fabiosantos@ufsj.edu.br</email> (F.V.d.S.)</aff><aff id="af4-molecules-24-03963"><label>4</label>Special Academic Unit of Physics and Chemistry, Federal University of Goiás, Catalão 75704-020, Brazil;<email>jgmjunqueira@gmail.com</email> (J.G.M.J.);<email>vanessa.pasqualotto@gmail.com</email> (V.G.P.S.)</aff><aff id="af5-molecules-24-03963"><label>5</label>Petroleomic and forensic chemistry laboratory, Department of Chemistry, Federal Institute of Espirito Santo, Vitória, ES 29075-910, Brazil;<email>brunoliveir_ra20@msn.com</email> (B.G.O.);<email>wandersonromao@gmail.com</email> (W.R.)</aff><aff id="af6-molecules-24-03963"><label>6</label>Life and Health Sciences Research Institute (ICVS), Medical School, University of Minho, 4710-057 Braga, Portugal</aff><aff id="af7-molecules-24-03963"><label>7</label>3ICVS/3B’s-PT Government Associate Laboratory, 4710-057 Braga, Portugal</aff><author-notes><corresp id="c1-molecules-24-03963"><label>*</label>Correspondence: <email>ruireis.hcb@gmail.com</email> (R.M.R.); <email>rosy@ufsj.edu.br</email> (R.I.M.d.A.R.); Tel.: +55-173-321-6600 (R.M.R.); +55-3736-904-484 or +55-3799-1619-155 (R.I.M.d.A.R.)</corresp></author-notes><pub-date pub-type="epub"><day>01</day><month>11</month><year>2019</year></pub-date><pub-date pub-type="collection"><month>11</month><year>2019</year></pub-date><volume>24</volume><issue>21</issue><elocation-id>3963</elocation-id><history><date date-type="received"><day>25</day><month>9</month><year>2019</year></date><date date-type="accepted"><day>29</day><month>10</month><year>2019</year></date></history><permissions><copyright-statement>© 2019 by the authors.</copyright-statement><copyright-year>2019</copyright-year><license license-type="open-access"><license-p>Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) 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>).</license-p></license></permissions><abstract><p>Plant-based compounds are an option to explore and perhaps overcome the limitations of current antitumor treatments. <italic>Annona coriacea</italic> Mart. is a plant with a broad spectrum of biological activities, but its antitumor activity is still unclear. The purpose of our study was to determine the effects of <italic>A. coriacea</italic> fractions on a panel of cervical cancer cell lines and a normal keratinocyte cell line. The antitumor effect was investigated in vitro by viability assays, cell cycle, apoptosis, migration, and invasion assays. Intracellular signaling was assessed by Western blot, and major compounds were identified by mass spectrometry. All fractions exhibited a cytotoxic effect on cisplatin-resistant cell lines, SiHa and HeLa. C3 and C5 were significantly more cytotoxic and selective than cisplatin in SiHa and Hela cells. However, in CaSki, a cisplatin-sensitive cell line, the compounds did not demonstrate higher cytotoxicity when compared with cisplatin. Alkaloids and acetogenins were the main compounds identified in the fractions. These fractions also markedly decreased cell proliferation with p21 increase and cell cycle arrest in G2/M. These effects were accompanied by an increase of H2AX phosphorylation levels and DNA damage index. In addition, fractions C3 and C5 promoted p62 accumulation and decrease of LC3II, as well as acid vesicle levels, indicating the inhibition of autophagic flow. These findings suggest that <italic>A. coriacea</italic> fractions may become effective antineoplastic drugs and highlight the autophagy inhibition properties of these fractions in sensitizing cervical cancer cells to treatment.</p></abstract><kwd-group><kwd>natural compounds</kwd><kwd>cervical cancer</kwd><kwd>autophagy</kwd><kwd>cell cycle arrest</kwd></kwd-group></article-meta></front><floats-group><fig id="molecules-24-03963-f001" orientation="portrait" position="float"><label>Figure 1</label><caption><p>Cytotoxicity in SiHa cells. (<bold>A</bold>) Cell viability measured after 24 h of exposure in SiHa cells. (<bold>B</bold>) Cell cytotoxicity measured after 24 h of exposure in SiHa cells. There was an increase in cytotoxicity and a decrease in viability in a dose-dependent manner (<italic>p</italic> < 0.0001). C3: Ethyl acetate fraction; C5: Fraction enriched in acetogenin; Cis: cisplatin. *** Indicates a statistical difference between groups. UFR: Relative unit of fluorescence.</p></caption><graphic xlink:href="molecules-24-03963-g001"></graphic></fig><fig id="molecules-24-03963-f002" orientation="portrait" position="float"><label>Figure 2</label><caption><p>Cell proliferation and invasion upon C3 and C5 treatment (5µg/mL) in SiHa cells (<bold>A</bold>) Western blotting of phospho-AKT (protein kinase B) upon C3 and C5 treatment. (<bold>B</bold>) Number of colonies in the soft agar assay performed for 45 days. (<bold>C</bold>) BrdU incorporation after C3 and C5 treatment (<italic>p</italic> < 0.0001) in SiHa cells. (<bold>D</bold>) Densitometry of p-AKT. (<bold>E</bold>) Invasion inhibition through C3 and C5 treatments in SiHa cells. (<bold>F</bold>) Percentage of invasion cells in SiHa cells (*** <italic>p</italic> < 0.0001; * <italic>p</italic> < 0.05). * Indicates statistical difference between the treatments). C3: Ethyl acetate fraction; C5: Fraction enriched in acetogenin; Cis: cisplatin.</p></caption><graphic xlink:href="molecules-24-03963-g002"></graphic></fig><fig id="molecules-24-03963-f003" orientation="portrait" position="float"><label>Figure 3</label><caption><p>Cell cycle alterations in SiHa cells after exposure to C3 and C5 compounds (<bold>A</bold>) Western blot of p21 in SiHa cells upon C3, C5, and cisplatin treatments. (<bold>B</bold>) Densitometry of p21. (<bold>C</bold>) Cell cycle profile in SiHa cells. (<bold>D</bold>) Cell cycle phase distribution after treatment with C3 and C5. (*** <italic>p</italic> < 0.0001; * <italic>p</italic> < 0.05). C3: Ethyl acetate fraction; C5: Fraction enriched in acetogenin; Cis: cisplatin; DMSO: dimethylsulfoxide.</p></caption><graphic xlink:href="molecules-24-03963-g003"></graphic></fig><fig id="molecules-24-03963-f004" orientation="portrait" position="float"><label>Figure 4</label><caption><p>Apoptosis evaluation in SiHa cells upon C3 and C5 compounds. (<bold>A</bold>) Western blot of PARP (Poly (ADP-ribose) polymerase), caspase 3, and H2AX (H2A histone family member X) proteins (<bold>B</bold>) Flow cytometry for SiHa cells. (<bold>C</bold>) Comparison of apoptotic cells upon C3 and C5 treatment. There was a significant increase for cells in apoptosis only for cisplatin (CIS) * <italic>p</italic> = 0.0282 (<bold>D</bold>) Depolarization of the mitochondrial membrane after treatment with C3 and C5 and cisplatin in the SiHa cell line. C3: Ethyl acetate fraction; C5: Fraction enriched in acetogenin; Cis: cisplatin; DMM: Depolarized mitochondrial membrane; PMM: Polarized mitochondrial membrane. <italic>p</italic> < 0.05). C3: Ethyl acetate fraction; C5: Fraction enriched in acetogenin; Cis: cisplatin.</p></caption><graphic xlink:href="molecules-24-03963-g004"></graphic></fig><fig id="molecules-24-03963-f005" orientation="portrait" position="float"><label>Figure 5</label><caption><p>DNA damage evaluation in HeLa cells upon C3 and C5 compounds. (<bold>A</bold>) Genotoxic damage induced by C3. (<bold>B</bold>) Genotoxic damage induced by C5. Data are representative of three experiments. Error bars represent SD. C3: Ethyl acetate fraction; C5: Fraction enriched in acetogenin; Cis: cisplatin; C3: Ethyl acetate fraction; C5: Fraction enriched in acetogenin; Cis: cisplatin; MMS: Methyl methane sulphonate, DMSO: dimethylsulfoxide. *** <italic>p</italic> < 0.0001; ** <italic>p</italic> < 0.01, * <italic>p</italic> < 0.05).</p></caption><graphic xlink:href="molecules-24-03963-g005"></graphic></fig><fig id="molecules-24-03963-f006" orientation="portrait" position="float"><label>Figure 6</label><caption><p>Analysis of the involvement of <italic>A. coriacea</italic> fractions in autophagy. (<bold>A</bold>) Analysis of the expression of proteins involved in the autophagic flux in SiHa cells. (<bold>B</bold>) Densitometry of p62. (<bold>C</bold>) Densitometry of LC3 B/A (Microtubule-associated protein 1A/1B-light chain 3). (<bold>D</bold>) Acridine orange staining in SiHa cells. There was a reduction in the percentage of formation of acid vesicles, evidenced by a reduction of the fluorescent green signal after treatment with the fractions (<italic>p</italic> < 0.05). HBSS: Hank’s balanced salt solution; EBSS: Earle’s balanced salt solution; C3: Ethyl acetate fraction; C5: Fraction enriched in acetogenin; Cis: cisplatin. BAF: Bafilomycin.</p></caption><graphic xlink:href="molecules-24-03963-g006"></graphic></fig><table-wrap id="molecules-24-03963-t001" orientation="portrait" position="float"><object-id pub-id-type="pii">molecules-24-03963-t001_Table 1</object-id><label>Table 1</label><caption><p>Proposed structures by ESI (-) FT-ICR MS for the main molecules in C3 and C5 fractions from <italic>Annona coriacea.</italic></p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1"><italic>Measured m/z</italic></th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1"><italic>Theoretical m/z</italic></th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Error (ppm)</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">DBE</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">[M-H]<sup>−</sup></th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Proposed Compound</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Reference</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">255.2332</td><td align="center" valign="middle" rowspan="1" colspan="1">255.23324</td><td align="center" valign="middle" rowspan="1" colspan="1">−1.12</td><td align="center" valign="middle" rowspan="1" colspan="1">1</td><td align="center" valign="middle" rowspan="1" colspan="1">[C<sub>16</sub>H<sub>32</sub>O<sub>2</sub>–H<sup>+</sup>]<sup>−</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">palmitic acid</td><td align="center" valign="middle" rowspan="1" colspan="1">Chen et al., 2016</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">281.24881</td><td align="center" valign="middle" rowspan="1" colspan="1">281.24886</td><td align="center" valign="middle" rowspan="1" colspan="1">0.92</td><td align="center" valign="middle" rowspan="1" colspan="1">2</td><td align="center" valign="middle" rowspan="1" colspan="1">[C<sub>18</sub>H<sub>34</sub>O<sub>2</sub>–H<sup>+</sup>]<sup>−</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">oleic acid</td><td align="center" valign="middle" rowspan="1" colspan="1">Chen et al., 2016</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">595.45815</td><td align="center" valign="middle" rowspan="1" colspan="1">595.45822</td><td align="center" valign="middle" rowspan="1" colspan="1">−0.49</td><td align="center" valign="middle" rowspan="1" colspan="1">4</td><td align="center" valign="middle" rowspan="1" colspan="1">[C<sub>35</sub>H<sub>64</sub>O<sub>7</sub>–H<sup>+</sup>]<sup>−</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">asitrocinone</td><td align="center" valign="middle" rowspan="1" colspan="1">Adewole e Ojewole et al., 2008</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">595.45838</td><td align="center" valign="middle" rowspan="1" colspan="1">595.45845</td><td align="center" valign="middle" rowspan="1" colspan="1">−0.87</td><td align="center" valign="middle" rowspan="1" colspan="1">4</td><td align="center" valign="middle" rowspan="1" colspan="1">[C<sub>35</sub>H<sub>64</sub>O<sub>7</sub>–H<sup>+</sup>]<sup>−</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">annonacin</td><td align="center" valign="middle" rowspan="1" colspan="1">Alkofahi et al., 1988</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">609.43885</td><td align="center" valign="middle" rowspan="1" colspan="1">609.43893</td><td align="center" valign="middle" rowspan="1" colspan="1">−2.85</td><td align="center" valign="middle" rowspan="1" colspan="1">5</td><td align="center" valign="middle" rowspan="1" colspan="1">[C<sub>35</sub>H<sub>62</sub>O<sub>8</sub>–H<sup>+</sup>]<sup>−</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">trilobalicin</td><td align="center" valign="middle" rowspan="1" colspan="1">He et al., 1997</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">611.45312</td><td align="center" valign="middle" rowspan="1" colspan="1">611.45314</td><td align="center" valign="middle" rowspan="1" colspan="1">−0.49</td><td align="center" valign="middle" rowspan="1" colspan="1">4</td><td align="center" valign="middle" rowspan="1" colspan="1">[C<sub>35</sub>H<sub>64</sub>O<sub>8</sub>–H<sup>+</sup>]<sup>−</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">annomuricin E</td><td align="center" valign="middle" rowspan="1" colspan="1">Kim et al., 1998</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">621.4742</td><td align="center" valign="middle" rowspan="1" colspan="1">621.4743</td><td align="center" valign="middle" rowspan="1" colspan="1">−1.17</td><td align="center" valign="middle" rowspan="1" colspan="1">5</td><td align="center" valign="middle" rowspan="1" colspan="1">[C<sub>37</sub>H<sub>66</sub>O<sub>7</sub>–H<sup>+</sup>]<sup>−</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">asimicin</td><td align="center" valign="middle" rowspan="1" colspan="1">Ye et al., 1996</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">621.47413</td><td align="center" valign="middle" rowspan="1" colspan="1">621.47418</td><td align="center" valign="middle" rowspan="1" colspan="1">−0.96</td><td align="center" valign="middle" rowspan="1" colspan="1">5</td><td align="center" valign="middle" rowspan="1" colspan="1">[C<sub>37</sub>H<sub>66</sub>O<sub>7</sub>–H<sup>+</sup>]<sup>−</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">bullatacin</td><td align="center" valign="middle" rowspan="1" colspan="1">Morre et al., 1995</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">627.4483</td><td align="center" valign="middle" rowspan="1" colspan="1">627.44832</td><td align="center" valign="middle" rowspan="1" colspan="1">−0.9</td><td align="center" valign="middle" rowspan="1" colspan="1">4</td><td align="center" valign="middle" rowspan="1" colspan="1">[C<sub>35</sub>H<sub>64</sub>O<sub>9</sub>–H<sup>+</sup>]<sup>−</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">annohexocin</td><td align="center" valign="middle" rowspan="1" colspan="1">Moghadamtousi et al., 2015</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">627.44823</td><td align="center" valign="middle" rowspan="1" colspan="1">627.44828</td><td align="center" valign="middle" rowspan="1" colspan="1">−0.83</td><td align="center" valign="middle" rowspan="1" colspan="1">4</td><td align="center" valign="middle" rowspan="1" colspan="1">[C<sub>35</sub>H<sub>64</sub>O<sub>9</sub>–H<sup>+</sup>]<sup>−</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">murihexocin</td><td align="center" valign="middle" rowspan="1" colspan="1">Kim et al., 1998</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">635.4540</td><td align="center" valign="middle" rowspan="1" colspan="1">635.4542</td><td align="center" valign="middle" rowspan="1" colspan="1">−2.14</td><td align="center" valign="middle" rowspan="1" colspan="1">6</td><td align="center" valign="middle" rowspan="1" colspan="1">[C<sub>37</sub>H<sub>64</sub>O<sub>8</sub>–H<sup>+</sup>]<sup>−</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">goniotriocin</td><td align="center" valign="middle" rowspan="1" colspan="1">Alali et al., 1999</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">637.46921</td><td align="center" valign="middle" rowspan="1" colspan="1">637.46927</td><td align="center" valign="middle" rowspan="1" colspan="1">−1.22</td><td align="center" valign="middle" rowspan="1" colspan="1">5</td><td align="center" valign="middle" rowspan="1" colspan="1">[C<sub>37</sub>H<sub>66</sub>O<sub>8</sub>–H<sup>+</sup>]<sup>−</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">bullatalicinone</td><td align="center" valign="middle" rowspan="1" colspan="1">Hui et al., 1991</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">637.46905</td><td align="center" valign="middle" rowspan="1" colspan="1">637.46914</td><td align="center" valign="middle" rowspan="1" colspan="1">−1.02</td><td align="center" valign="middle" rowspan="1" colspan="1">5</td><td align="center" valign="middle" rowspan="1" colspan="1">[C<sub>37</sub>H<sub>66</sub>O<sub>8</sub>–H<sup>+</sup>]<sup>−</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">annoglaucin</td><td align="center" valign="middle" rowspan="1" colspan="1">Bermejo et al., 2005</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">641.42889</td><td align="center" valign="middle" rowspan="1" colspan="1">641.42895</td><td align="center" valign="middle" rowspan="1" colspan="1">−1.34</td><td align="center" valign="middle" rowspan="1" colspan="1">4</td><td align="center" valign="middle" rowspan="1" colspan="1">[C<sub>35</sub>H<sub>64</sub>O<sub>10</sub>–H<sup>+</sup>]<sup>−</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">coriaheptocin B/A</td><td align="center" valign="middle" rowspan="1" colspan="1">Formagio et al., 2015</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">651.44943</td><td align="center" valign="middle" rowspan="1" colspan="1">651.44949</td><td align="center" valign="middle" rowspan="1" colspan="1">−2.65</td><td align="center" valign="middle" rowspan="1" colspan="1">6</td><td align="center" valign="middle" rowspan="1" colspan="1">[C<sub>35</sub>H<sub>64</sub>O<sub>10</sub>–H<sup>+</sup>]<sup>−</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">ginsenoside Rh5</td><td align="center" valign="middle" rowspan="1" colspan="1">Vamanu, 2014</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">653.46442</td><td align="center" valign="middle" rowspan="1" colspan="1">653.46444</td><td align="center" valign="middle" rowspan="1" colspan="1">−1.58</td><td align="center" valign="middle" rowspan="1" colspan="1">5</td><td align="center" valign="middle" rowspan="1" colspan="1">[C<sub>37</sub>H<sub>66</sub>O<sub>9</sub>–H<sup>+</sup>]<sup>−</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">salzmanolin</td><td align="center" valign="middle" rowspan="1" colspan="1">Queiroz et al., 2003</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">669.46005</td><td align="center" valign="middle" rowspan="1" colspan="1">669.4601</td><td align="center" valign="middle" rowspan="1" colspan="1">−1.22</td><td align="center" valign="middle" rowspan="1" colspan="1">6</td><td align="center" valign="middle" rowspan="1" colspan="1">[C<sub>37</sub>H<sub>68</sub>O<sub>10</sub>–H<sup>+</sup>]<sup>−</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">annoheptocin A</td><td align="center" valign="middle" rowspan="1" colspan="1">Meneses Da Silva et al., 1998</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">671.47569</td><td align="center" valign="middle" rowspan="1" colspan="1">671.47575</td><td align="center" valign="middle" rowspan="1" colspan="1">−1</td><td align="center" valign="middle" rowspan="1" colspan="1">6</td><td align="center" valign="middle" rowspan="1" colspan="1">[C<sub>37</sub>H<sub>68</sub>O<sub>10</sub>–H<sup>+</sup>]<sup>−</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">annoheptocin B</td><td align="center" valign="middle" rowspan="1" colspan="1">Meneses Da Silva et al., 1998</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">763.47932</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">763.47939</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">−0.83</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">12</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[C<sub>39</sub>H<sub>70</sub>O<sub>5</sub>–H]<sup>−</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">squamocin glycosilated</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Jamkhande e Wattamwar, 2015</td></tr></tbody></table><table-wrap-foot><fn><p>DBE: Double bond equivalent; m/z: mass-to-charge ratio.</p></fn></table-wrap-foot></table-wrap><table-wrap id="molecules-24-03963-t002" orientation="portrait" position="float"><object-id pub-id-type="pii">molecules-24-03963-t002_Table 2</object-id><label>Table 2</label><caption><p>IC<sub>50</sub> values for <italic>A. coriacea</italic> compounds and cisplatin in cervical cancer cell lines.</p></caption><table frame="hsides" rules="groups"><thead><tr><th colspan="9" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1">IC<sub>50</sub> Value (Mean ± SD) µg/mL</th></tr><tr><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cell Line</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">C1</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">C2</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">C3</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">C4</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">C5</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">C6</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">C7</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cisplatin</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">CaSki</td><td align="center" valign="middle" rowspan="1" colspan="1">17.8 ± 2.8</td><td align="center" valign="middle" rowspan="1" colspan="1">ND</td><td align="center" valign="middle" rowspan="1" colspan="1">6.5 ± 1.8</td><td align="center" valign="middle" rowspan="1" colspan="1">ND</td><td align="center" valign="middle" rowspan="1" colspan="1">3.6 ± 0.9</td><td align="center" valign="top" rowspan="1" colspan="1">11.7 ± 2.2</td><td align="center" valign="top" rowspan="1" colspan="1">21.4 ± 3.3</td><td align="center" valign="middle" rowspan="1" colspan="1">1.05 ± 1.2</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">HeLa</td><td align="center" valign="middle" rowspan="1" colspan="1">12.2 ± 1.5</td><td align="center" valign="middle" rowspan="1" colspan="1">ND</td><td align="center" valign="middle" rowspan="1" colspan="1">6.6 ± 1.2</td><td align="center" valign="middle" rowspan="1" colspan="1">ND</td><td align="center" valign="middle" rowspan="1" colspan="1">4.1 ± 0.4</td><td align="center" valign="middle" rowspan="1" colspan="1">12.9 ± 1.9</td><td align="center" valign="middle" rowspan="1" colspan="1">12.3 ± 0.83</td><td align="center" valign="middle" rowspan="1" colspan="1">13.6 ± 0.44</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SiHa</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">16.1 ± 2.7</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ND</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">8.7 ± 1.3</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ND</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">5.1 ± 0.6</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">12.6 ± 1.6</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">12.7 ± 1.3</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">15.5 ± 0.93</td></tr></tbody></table><table-wrap-foot><fn><p>ND: Not determined; C1: Ethanolic extract; C2: Hexane fraction; C3: Ethyl acetate fraction; C4: Hidroalcoholic fraction; C5: Fraction enriched in acetogenin; C6: Neutral dichloromethane fraction obtained from acid-base extraction; C7: Dichloromethane fraction enriched in alkaloids.</p></fn></table-wrap-foot></table-wrap><table-wrap id="molecules-24-03963-t003" orientation="portrait" position="float"><object-id pub-id-type="pii">molecules-24-03963-t003_Table 3</object-id><label>Table 3</label><caption><p>IC<sub>50</sub> values and selectivity index for the C3 and C5 fractions of cisplatin to tumor cells as compared with HaCaT.</p></caption><table frame="hsides" rules="groups"><thead><tr><th colspan="7" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1">IC50 Value (Mean ± SD) µg/mL and SI ª</th></tr><tr><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cell Line</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">C3</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">C5</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cisplatin</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SIC3</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SIC5</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SI Cisplatin</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">CaSki</td><td align="center" valign="middle" rowspan="1" colspan="1">6.5 ± 1.8</td><td align="center" valign="middle" rowspan="1" colspan="1">3.6 ± 0.9</td><td align="center" valign="middle" rowspan="1" colspan="1">1.05 ± 1.2</td><td align="center" valign="middle" rowspan="1" colspan="1">1.57</td><td align="center" valign="middle" rowspan="1" colspan="1">3.72</td><td align="center" valign="middle" rowspan="1" colspan="1">4.57</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">HeLa</td><td align="center" valign="middle" rowspan="1" colspan="1">6.6 ± 1.2</td><td align="center" valign="middle" rowspan="1" colspan="1">4.1 ± 0.4</td><td align="center" valign="middle" rowspan="1" colspan="1">13.6 ± 0.44</td><td align="center" valign="middle" rowspan="1" colspan="1">1.55</td><td align="center" valign="middle" rowspan="1" colspan="1">3.27</td><td align="center" valign="middle" rowspan="1" colspan="1">0.35</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">SiHa</td><td align="center" valign="middle" rowspan="1" colspan="1">8.7 ± 1.3</td><td align="center" valign="middle" rowspan="1" colspan="1">5.1 ± 0.6</td><td align="center" valign="middle" rowspan="1" colspan="1">15.5 ±0.93</td><td align="center" valign="middle" rowspan="1" colspan="1">1.17</td><td align="center" valign="middle" rowspan="1" colspan="1">2.63</td><td align="center" valign="middle" rowspan="1" colspan="1">0.31</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HaCat</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">10.2 ± 2.4</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">13.4 ± 1.0</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">4.8 ± 1.3</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">R</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">R</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">R</td></tr></tbody></table><table-wrap-foot><fn><p><sup>a</sup> Selectivity index is the ratio of the IC<sub>50</sub> values of the treatments on HaCaT cells to those in the cancer cell lines. SI: Selectivity index; C3: Ethyl acetate fraction; C5: Fraction enriched in acetogenin; R: Reference cell line.</p></fn></table-wrap-foot></table-wrap></floats-group></pmc><affiliations><list><country><li>Portugal</li></country><region><li>Région Nord (Portugal)</li></region><settlement><li>Braga</li></settlement><orgName><li>Université du Minho</li></orgName></list><tree><noCountry><name sortKey="Barbosa, Maria Cristina S" sort="Barbosa, Maria Cristina S" uniqKey="Barbosa M" first="Maria Cristina S." last="Barbosa">Maria Cristina S. Barbosa</name><name sortKey="Dos Santos, Fabio Vieira" sort="Dos Santos, Fabio Vieira" uniqKey="Dos Santos F" first="Fábio Vieira" last="Dos Santos">Fábio Vieira Dos Santos</name><name sortKey="Gomes, Izabela N Faria" sort="Gomes, Izabela N Faria" uniqKey="Gomes I" first="Izabela N. Faria" last="Gomes">Izabela N. Faria Gomes</name><name sortKey="Junqueira, Joao Gabriel M" sort="Junqueira, Joao Gabriel M" uniqKey="Junqueira J" first="João Gabriel M." last="Junqueira">João Gabriel M. Junqueira</name><name sortKey="Oliveira Silva, Viviane A" sort="Oliveira Silva, Viviane A" uniqKey="Oliveira Silva V" first="Viviane A." last="Oliveira Silva">Viviane A. Oliveira Silva</name><name sortKey="Oliveira, Bruno G" sort="Oliveira, Bruno G" uniqKey="Oliveira B" first="Bruno G" last="Oliveira">Bruno G. Oliveira</name><name sortKey="Ribeiro, Rosy Iara Maciel De Azambuja" sort="Ribeiro, Rosy Iara Maciel De Azambuja" uniqKey="Ribeiro R" first="Rosy Iara Maciel De Azambuja" last="Ribeiro">Rosy Iara Maciel De Azambuja Ribeiro</name><name sortKey="Romao, Wanderson" sort="Romao, Wanderson" uniqKey="Romao W" first="Wanderson" last="Romão">Wanderson Romão</name><name sortKey="Rosa, Marcela N" sort="Rosa, Marcela N" uniqKey="Rosa M" first="Marcela N." last="Rosa">Marcela N. Rosa</name><name sortKey="Severino, Vanessa G P" sort="Severino, Vanessa G P" uniqKey="Severino V" first="Vanessa G. P." last="Severino">Vanessa G. P. Severino</name><name sortKey="Silva Oliveira, Renato J" sort="Silva Oliveira, Renato J" uniqKey="Silva Oliveira R" first="Renato J." last="Silva-Oliveira">Renato J. Silva-Oliveira</name><name sortKey="Vital, Patrik S" sort="Vital, Patrik S" uniqKey="Vital P" first="Patrik S." last="Vital">Patrik S. Vital</name></noCountry><country name="Portugal"><region name="Région Nord (Portugal)"><name sortKey="Reis, Rui Manuel" sort="Reis, Rui Manuel" uniqKey="Reis R" first="Rui Manuel" last="Reis">Rui Manuel Reis</name></region><name sortKey="Reis, Rui Manuel" sort="Reis, Rui Manuel" uniqKey="Reis R" first="Rui Manuel" last="Reis">Rui Manuel Reis</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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