Peptide from thaumatin plant protein exhibits selective anticandidal activity by inducing apoptosis via membrane receptor.
Identifieur interne : 000033 ( Main/Exploration ); précédent : 000032; suivant : 000034Peptide from thaumatin plant protein exhibits selective anticandidal activity by inducing apoptosis via membrane receptor.
Auteurs : Francisco E S. Lopes [Brésil] ; Helen P S. Da Costa [Brésil] ; Pedro F N. Souza [États-Unis] ; João P B. Oliveira [Brésil] ; Márcio V. Ramos [Brésil] ; José E C. Freire [Brésil] ; Thiago L. Jucá [Brésil] ; Cleverson D T. Freitas [Brésil]Source :
- Phytochemistry [ 1873-3700 ] ; 2019.
Descripteurs français
- KwdFr :
- Antifongiques (composition chimique), Antifongiques (pharmacologie), Apoptose (effets des médicaments et des substances chimiques), Bases de données de protéines (MeSH), Candida albicans (croissance et développement), Candida albicans (effets des médicaments et des substances chimiques), Candida albicans (métabolisme), Découverte de médicament (MeSH), Espèces réactives de l'oxygène (métabolisme), Membrane cellulaire (effets des médicaments et des substances chimiques), Paroi cellulaire (effets des médicaments et des substances chimiques), Peptides (composition chimique), Peptides (métabolisme), Peptides (pharmacologie), Plantes (composition chimique), Protéines végétales (composition chimique), Récepteurs de surface cellulaire (effets des médicaments et des substances chimiques), Saccharomyces cerevisiae (croissance et développement), Saccharomyces cerevisiae (effets des médicaments et des substances chimiques), Saccharomyces cerevisiae (métabolisme), Simulation de docking moléculaire (MeSH), Séquence d'acides aminés (MeSH), Tests de sensibilité microbienne (MeSH).
- MESH :
- composition chimique : Antifongiques, Peptides, Plantes, Protéines végétales.
- croissance et développement : Candida albicans, Saccharomyces cerevisiae.
- effets des médicaments et des substances chimiques : Apoptose, Candida albicans, Membrane cellulaire, Paroi cellulaire, Récepteurs de surface cellulaire, Saccharomyces cerevisiae.
- métabolisme : Candida albicans, Espèces réactives de l'oxygène, Peptides, Saccharomyces cerevisiae.
- pharmacologie : Antifongiques, Peptides.
- Bases de données de protéines, Découverte de médicament, Simulation de docking moléculaire, Séquence d'acides aminés, Tests de sensibilité microbienne.
English descriptors
- KwdEn :
- Amino Acid Sequence (MeSH), Antifungal Agents (chemistry), Antifungal Agents (pharmacology), Apoptosis (drug effects), Candida albicans (drug effects), Candida albicans (growth & development), Candida albicans (metabolism), Cell Membrane (drug effects), Cell Wall (drug effects), Databases, Protein (MeSH), Drug Discovery (MeSH), Microbial Sensitivity Tests (MeSH), Molecular Docking Simulation (MeSH), Peptides (chemistry), Peptides (metabolism), Peptides (pharmacology), Plant Proteins (chemistry), Plants (chemistry), Reactive Oxygen Species (metabolism), Receptors, Cell Surface (drug effects), Saccharomyces cerevisiae (drug effects), Saccharomyces cerevisiae (growth & development), Saccharomyces cerevisiae (metabolism).
- MESH :
- chemical , chemistry : Antifungal Agents, Peptides, Plant Proteins.
- chemical , drug effects : Receptors, Cell Surface.
- chemical , metabolism : Peptides, Reactive Oxygen Species.
- chemical , pharmacology : Antifungal Agents, Peptides.
- chemistry : Plants.
- drug effects : Apoptosis, Candida albicans, Cell Membrane, Cell Wall, Saccharomyces cerevisiae.
- growth & development : Candida albicans, Saccharomyces cerevisiae.
- metabolism : Candida albicans, Saccharomyces cerevisiae.
- Amino Acid Sequence, Databases, Protein, Drug Discovery, Microbial Sensitivity Tests, Molecular Docking Simulation.
Abstract
Osmotin- and thaumatin-like proteins (OLPs and TLPs) have been associated with plant defense responses to different biotic stresses. In the present work, several in silico sequences from OLPs and TLPs were investigated by means of bioinformatics tools aiming to prospect for antimicrobial peptides. The peptide sequences chosen were further synthesized and characterized, and their activities and action mechanisms were assayed against some phytopathogenic fungi, bacteria and yeasts of clinical importance. From this survey approach, four peptide sequences (GDCKATSC, CPRALKVPGGCN, IVGQCPAKLKA, and CAADIVGQCPAKLK) were selected considering some chemical parameters commonly attributed to antimicrobial peptides. Antimicrobial assays showed that these peptides were unable to inhibit mycelial growth of phytopathogenic fungi and they did not affect bacterial cell growth. Nevertheless, significant inhibitory activity was found for CPRALKVPGGCN and CAADIVGQCPAKLK against Candida albicans and Saccharomyces cerevisiae. Fluorescence and scanning electron microscopy assays suggested that CAADIVGQCPAKLK did not damage the overall cell structure, or its activity was negligible on yeast membrane and cell wall integrity. However, it induced the production of reactive oxygen species (ROS) and apoptosis. Molecular docking analysis showed that CAADIVGQCPAKLK had strong affinity to interact with specific plasma membrane receptors of C. albicans and S. cerevisiae, which have been described as promoting the induction of apoptosis. The results indicate that CAADIVGQCPAKLK can be a valuable target for the development of a desired antimicrobial agent against the pathogen C. albicans.
DOI: 10.1016/j.phytochem.2018.12.006
PubMed: 30577001
Affiliations:
Links toward previous steps (curation, corpus...)
Le document en format XML
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<profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Amino Acid Sequence (MeSH)</term>
<term>Antifungal Agents (chemistry)</term>
<term>Antifungal Agents (pharmacology)</term>
<term>Apoptosis (drug effects)</term>
<term>Candida albicans (drug effects)</term>
<term>Candida albicans (growth & development)</term>
<term>Candida albicans (metabolism)</term>
<term>Cell Membrane (drug effects)</term>
<term>Cell Wall (drug effects)</term>
<term>Databases, Protein (MeSH)</term>
<term>Drug Discovery (MeSH)</term>
<term>Microbial Sensitivity Tests (MeSH)</term>
<term>Molecular Docking Simulation (MeSH)</term>
<term>Peptides (chemistry)</term>
<term>Peptides (metabolism)</term>
<term>Peptides (pharmacology)</term>
<term>Plant Proteins (chemistry)</term>
<term>Plants (chemistry)</term>
<term>Reactive Oxygen Species (metabolism)</term>
<term>Receptors, Cell Surface (drug effects)</term>
<term>Saccharomyces cerevisiae (drug effects)</term>
<term>Saccharomyces cerevisiae (growth & development)</term>
<term>Saccharomyces cerevisiae (metabolism)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr"><term>Antifongiques (composition chimique)</term>
<term>Antifongiques (pharmacologie)</term>
<term>Apoptose (effets des médicaments et des substances chimiques)</term>
<term>Bases de données de protéines (MeSH)</term>
<term>Candida albicans (croissance et développement)</term>
<term>Candida albicans (effets des médicaments et des substances chimiques)</term>
<term>Candida albicans (métabolisme)</term>
<term>Découverte de médicament (MeSH)</term>
<term>Espèces réactives de l'oxygène (métabolisme)</term>
<term>Membrane cellulaire (effets des médicaments et des substances chimiques)</term>
<term>Paroi cellulaire (effets des médicaments et des substances chimiques)</term>
<term>Peptides (composition chimique)</term>
<term>Peptides (métabolisme)</term>
<term>Peptides (pharmacologie)</term>
<term>Plantes (composition chimique)</term>
<term>Protéines végétales (composition chimique)</term>
<term>Récepteurs de surface cellulaire (effets des médicaments et des substances chimiques)</term>
<term>Saccharomyces cerevisiae (croissance et développement)</term>
<term>Saccharomyces cerevisiae (effets des médicaments et des substances chimiques)</term>
<term>Saccharomyces cerevisiae (métabolisme)</term>
<term>Simulation de docking moléculaire (MeSH)</term>
<term>Séquence d'acides aminés (MeSH)</term>
<term>Tests de sensibilité microbienne (MeSH)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>Antifungal Agents</term>
<term>Peptides</term>
<term>Plant Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="drug effects" xml:lang="en"><term>Receptors, Cell Surface</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Peptides</term>
<term>Reactive Oxygen Species</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en"><term>Antifungal Agents</term>
<term>Peptides</term>
</keywords>
<keywords scheme="MESH" qualifier="chemistry" xml:lang="en"><term>Plants</term>
</keywords>
<keywords scheme="MESH" qualifier="composition chimique" xml:lang="fr"><term>Antifongiques</term>
<term>Peptides</term>
<term>Plantes</term>
<term>Protéines végétales</term>
</keywords>
<keywords scheme="MESH" qualifier="croissance et développement" xml:lang="fr"><term>Candida albicans</term>
<term>Saccharomyces cerevisiae</term>
</keywords>
<keywords scheme="MESH" qualifier="drug effects" xml:lang="en"><term>Apoptosis</term>
<term>Candida albicans</term>
<term>Cell Membrane</term>
<term>Cell Wall</term>
<term>Saccharomyces cerevisiae</term>
</keywords>
<keywords scheme="MESH" qualifier="effets des médicaments et des substances chimiques" xml:lang="fr"><term>Apoptose</term>
<term>Candida albicans</term>
<term>Membrane cellulaire</term>
<term>Paroi cellulaire</term>
<term>Récepteurs de surface cellulaire</term>
<term>Saccharomyces cerevisiae</term>
</keywords>
<keywords scheme="MESH" qualifier="growth & development" xml:lang="en"><term>Candida albicans</term>
<term>Saccharomyces cerevisiae</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Candida albicans</term>
<term>Saccharomyces cerevisiae</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Candida albicans</term>
<term>Espèces réactives de l'oxygène</term>
<term>Peptides</term>
<term>Saccharomyces cerevisiae</term>
</keywords>
<keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr"><term>Antifongiques</term>
<term>Peptides</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Amino Acid Sequence</term>
<term>Databases, Protein</term>
<term>Drug Discovery</term>
<term>Microbial Sensitivity Tests</term>
<term>Molecular Docking Simulation</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr"><term>Bases de données de protéines</term>
<term>Découverte de médicament</term>
<term>Simulation de docking moléculaire</term>
<term>Séquence d'acides aminés</term>
<term>Tests de sensibilité microbienne</term>
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<front><div type="abstract" xml:lang="en">Osmotin- and thaumatin-like proteins (OLPs and TLPs) have been associated with plant defense responses to different biotic stresses. In the present work, several in silico sequences from OLPs and TLPs were investigated by means of bioinformatics tools aiming to prospect for antimicrobial peptides. The peptide sequences chosen were further synthesized and characterized, and their activities and action mechanisms were assayed against some phytopathogenic fungi, bacteria and yeasts of clinical importance. From this survey approach, four peptide sequences (GDCKATSC, CPRALKVPGGCN, IVGQCPAKLKA, and CAADIVGQCPAKLK) were selected considering some chemical parameters commonly attributed to antimicrobial peptides. Antimicrobial assays showed that these peptides were unable to inhibit mycelial growth of phytopathogenic fungi and they did not affect bacterial cell growth. Nevertheless, significant inhibitory activity was found for CPRALKVPGGCN and CAADIVGQCPAKLK against Candida albicans and Saccharomyces cerevisiae. Fluorescence and scanning electron microscopy assays suggested that CAADIVGQCPAKLK did not damage the overall cell structure, or its activity was negligible on yeast membrane and cell wall integrity. However, it induced the production of reactive oxygen species (ROS) and apoptosis. Molecular docking analysis showed that CAADIVGQCPAKLK had strong affinity to interact with specific plasma membrane receptors of C. albicans and S. cerevisiae, which have been described as promoting the induction of apoptosis. The results indicate that CAADIVGQCPAKLK can be a valuable target for the development of a desired antimicrobial agent against the pathogen C. albicans.</div>
</front>
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<Month>03</Month>
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<Month>03</Month>
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<Month>Mar</Month>
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<Title>Phytochemistry</Title>
<ISOAbbreviation>Phytochemistry</ISOAbbreviation>
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<ArticleTitle>Peptide from thaumatin plant protein exhibits selective anticandidal activity by inducing apoptosis via membrane receptor.</ArticleTitle>
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<ELocationID EIdType="pii" ValidYN="Y">S0031-9422(18)30194-8</ELocationID>
<ELocationID EIdType="doi" ValidYN="Y">10.1016/j.phytochem.2018.12.006</ELocationID>
<Abstract><AbstractText>Osmotin- and thaumatin-like proteins (OLPs and TLPs) have been associated with plant defense responses to different biotic stresses. In the present work, several in silico sequences from OLPs and TLPs were investigated by means of bioinformatics tools aiming to prospect for antimicrobial peptides. The peptide sequences chosen were further synthesized and characterized, and their activities and action mechanisms were assayed against some phytopathogenic fungi, bacteria and yeasts of clinical importance. From this survey approach, four peptide sequences (GDCKATSC, CPRALKVPGGCN, IVGQCPAKLKA, and CAADIVGQCPAKLK) were selected considering some chemical parameters commonly attributed to antimicrobial peptides. Antimicrobial assays showed that these peptides were unable to inhibit mycelial growth of phytopathogenic fungi and they did not affect bacterial cell growth. Nevertheless, significant inhibitory activity was found for CPRALKVPGGCN and CAADIVGQCPAKLK against Candida albicans and Saccharomyces cerevisiae. Fluorescence and scanning electron microscopy assays suggested that CAADIVGQCPAKLK did not damage the overall cell structure, or its activity was negligible on yeast membrane and cell wall integrity. However, it induced the production of reactive oxygen species (ROS) and apoptosis. Molecular docking analysis showed that CAADIVGQCPAKLK had strong affinity to interact with specific plasma membrane receptors of C. albicans and S. cerevisiae, which have been described as promoting the induction of apoptosis. The results indicate that CAADIVGQCPAKLK can be a valuable target for the development of a desired antimicrobial agent against the pathogen C. albicans.</AbstractText>
<CopyrightInformation>Copyright © 2018. Published by Elsevier Ltd.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Lopes</LastName>
<ForeName>Francisco E S</ForeName>
<Initials>FES</Initials>
<AffiliationInfo><Affiliation>Universidade Federal do Ceará, Departamento de Bioquímica e Biologia Molecular, CEP 60.440-970, Fortaleza, Ceará, Brazil.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>da Costa</LastName>
<ForeName>Helen P S</ForeName>
<Initials>HPS</Initials>
<AffiliationInfo><Affiliation>Universidade Federal do Ceará, Departamento de Bioquímica e Biologia Molecular, CEP 60.440-970, Fortaleza, Ceará, Brazil.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Souza</LastName>
<ForeName>Pedro F N</ForeName>
<Initials>PFN</Initials>
<AffiliationInfo><Affiliation>Nebraska Center for Virology, University of Nebraska-Lincoln, Lincoln, NE, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Oliveira</LastName>
<ForeName>João P B</ForeName>
<Initials>JPB</Initials>
<AffiliationInfo><Affiliation>Universidade Federal do Ceará, Departamento de Bioquímica e Biologia Molecular, CEP 60.440-970, Fortaleza, Ceará, Brazil.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Ramos</LastName>
<ForeName>Márcio V</ForeName>
<Initials>MV</Initials>
<AffiliationInfo><Affiliation>Universidade Federal do Ceará, Departamento de Bioquímica e Biologia Molecular, CEP 60.440-970, Fortaleza, Ceará, Brazil.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Freire</LastName>
<ForeName>José E C</ForeName>
<Initials>JEC</Initials>
<AffiliationInfo><Affiliation>Faculdade UniNassau, Campus Parangaba, Av. Dr. Silas Munguba, 403-433, Parangaba, Fortaleza, Ceará, Brazil.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Jucá</LastName>
<ForeName>Thiago L</ForeName>
<Initials>TL</Initials>
<AffiliationInfo><Affiliation>Refinaria de Lubrificantes e Derivados do Nordeste (Lubnor), Petrobras, Fortaleza, Ceará, Brazil.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Freitas</LastName>
<ForeName>Cleverson D T</ForeName>
<Initials>CDT</Initials>
<AffiliationInfo><Affiliation>Universidade Federal do Ceará, Departamento de Bioquímica e Biologia Molecular, CEP 60.440-970, Fortaleza, Ceará, Brazil. Electronic address: cleversondiniz@hotmail.com.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic"><Year>2018</Year>
<Month>12</Month>
<Day>19</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo><Country>England</Country>
<MedlineTA>Phytochemistry</MedlineTA>
<NlmUniqueID>0151434</NlmUniqueID>
<ISSNLinking>0031-9422</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList><Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D000935">Antifungal Agents</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010455">Peptides</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D017382">Reactive Oxygen Species</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D011956">Receptors, Cell Surface</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>53850-34-3</RegistryNumber>
<NameOfSubstance UI="C003427">thaumatin protein, plant</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList><MeshHeading><DescriptorName UI="D000595" MajorTopicYN="N">Amino Acid Sequence</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D000935" MajorTopicYN="N">Antifungal Agents</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000494" MajorTopicYN="Y">pharmacology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D017209" MajorTopicYN="N">Apoptosis</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="Y">drug effects</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D002176" MajorTopicYN="N">Candida albicans</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="Y">drug effects</QualifierName>
<QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D002462" MajorTopicYN="N">Cell Membrane</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D002473" MajorTopicYN="N">Cell Wall</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D030562" MajorTopicYN="N">Databases, Protein</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D055808" MajorTopicYN="N">Drug Discovery</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D008826" MajorTopicYN="N">Microbial Sensitivity Tests</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D062105" MajorTopicYN="N">Molecular Docking Simulation</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D010455" MajorTopicYN="N">Peptides</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000494" MajorTopicYN="Y">pharmacology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="Y">chemistry</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D010944" MajorTopicYN="N">Plants</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="Y">chemistry</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D017382" MajorTopicYN="N">Reactive Oxygen Species</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D011956" MajorTopicYN="N">Receptors, Cell Surface</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="Y">drug effects</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D012441" MajorTopicYN="N">Saccharomyces cerevisiae</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
<QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Candida</Keyword>
<Keyword MajorTopicYN="N">Saccharomyces</Keyword>
<Keyword MajorTopicYN="N">Yeast</Keyword>
<Keyword MajorTopicYN="N">human pathogens</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year>
<Month>06</Month>
<Day>06</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="revised"><Year>2018</Year>
<Month>12</Month>
<Day>10</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted"><Year>2018</Year>
<Month>12</Month>
<Day>11</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="pubmed"><Year>2018</Year>
<Month>12</Month>
<Day>24</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline"><Year>2019</Year>
<Month>3</Month>
<Day>16</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez"><Year>2018</Year>
<Month>12</Month>
<Day>22</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList><ArticleId IdType="pubmed">30577001</ArticleId>
<ArticleId IdType="pii">S0031-9422(18)30194-8</ArticleId>
<ArticleId IdType="doi">10.1016/j.phytochem.2018.12.006</ArticleId>
</ArticleIdList>
</PubmedData>
</pubmed>
<affiliations><list><country><li>Brésil</li>
<li>États-Unis</li>
</country>
<region><li>Ceará</li>
<li>Nebraska</li>
</region>
</list>
<tree><country name="Brésil"><region name="Ceará"><name sortKey="Lopes, Francisco E S" sort="Lopes, Francisco E S" uniqKey="Lopes F" first="Francisco E S" last="Lopes">Francisco E S. Lopes</name>
</region>
<name sortKey="Da Costa, Helen P S" sort="Da Costa, Helen P S" uniqKey="Da Costa H" first="Helen P S" last="Da Costa">Helen P S. Da Costa</name>
<name sortKey="Freire, Jose E C" sort="Freire, Jose E C" uniqKey="Freire J" first="José E C" last="Freire">José E C. Freire</name>
<name sortKey="Freitas, Cleverson D T" sort="Freitas, Cleverson D T" uniqKey="Freitas C" first="Cleverson D T" last="Freitas">Cleverson D T. Freitas</name>
<name sortKey="Juca, Thiago L" sort="Juca, Thiago L" uniqKey="Juca T" first="Thiago L" last="Jucá">Thiago L. Jucá</name>
<name sortKey="Oliveira, Joao P B" sort="Oliveira, Joao P B" uniqKey="Oliveira J" first="João P B" last="Oliveira">João P B. Oliveira</name>
<name sortKey="Ramos, Marcio V" sort="Ramos, Marcio V" uniqKey="Ramos M" first="Márcio V" last="Ramos">Márcio V. Ramos</name>
</country>
<country name="États-Unis"><region name="Nebraska"><name sortKey="Souza, Pedro F N" sort="Souza, Pedro F N" uniqKey="Souza P" first="Pedro F N" last="Souza">Pedro F N. Souza</name>
</region>
</country>
</tree>
</affiliations>
</record>
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