Influenza a virus-triggered autophagy decreases the pluripotency of human-induced pluripotent stem cells.
Identifieur interne : 000317 ( Main/Exploration ); précédent : 000316; suivant : 000318Influenza a virus-triggered autophagy decreases the pluripotency of human-induced pluripotent stem cells.
Auteurs : Ali Zahedi-Amiri [Canada] ; Glen L. Sequiera [Canada] ; Sanjiv Dhingra [Canada] ; Kevin M. Coombs [Canada]Source :
- Cell death & disease [ 2041-4889 ] ; 2019.
Descripteurs français
- KwdFr :
- Autophagie (effets des médicaments et des substances chimiques), Cellules A549 (MeSH), Cellules souches pluripotentes induites (cytologie), Cellules souches pluripotentes induites (métabolisme), Cellules souches pluripotentes induites (virologie), Différenciation cellulaire (MeSH), Développement embryonnaire (MeSH), Facteurs de transcription SOX-B1 (métabolisme), Humains (MeSH), Macrolides (pharmacologie), Protéine homéotique Nanog (métabolisme), Protéome (analyse), Protéomique (MeSH), Réplication virale (MeSH), Sirolimus (pharmacologie), Virus de la grippe A (physiologie), Voies et réseaux métaboliques (MeSH).
- MESH :
- analyse : Protéome.
- cytologie : Cellules souches pluripotentes induites.
- effets des médicaments et des substances chimiques : Autophagie.
- métabolisme : Cellules souches pluripotentes induites, Facteurs de transcription SOX-B1, Protéine homéotique Nanog.
- pharmacologie : Macrolides, Sirolimus.
- physiologie : Virus de la grippe A.
- virologie : Cellules souches pluripotentes induites.
- Cellules A549, Différenciation cellulaire, Développement embryonnaire, Humains, Protéomique, Réplication virale, Voies et réseaux métaboliques.
English descriptors
- KwdEn :
- A549 Cells (MeSH), Autophagy (drug effects), Cell Differentiation (MeSH), Embryonic Development (MeSH), Humans (MeSH), Induced Pluripotent Stem Cells (cytology), Induced Pluripotent Stem Cells (metabolism), Induced Pluripotent Stem Cells (virology), Influenza A virus (physiology), Macrolides (pharmacology), Metabolic Networks and Pathways (MeSH), Nanog Homeobox Protein (metabolism), Proteome (analysis), Proteomics (MeSH), SOXB1 Transcription Factors (metabolism), Sirolimus (pharmacology), Virus Replication (MeSH).
- MESH :
- chemical , analysis : Proteome.
- chemical , metabolism : Nanog Homeobox Protein, SOXB1 Transcription Factors.
- chemical , pharmacology : Macrolides, Sirolimus.
- cytology : Induced Pluripotent Stem Cells.
- drug effects : Autophagy.
- metabolism : Induced Pluripotent Stem Cells.
- physiology : Influenza A virus.
- virology : Induced Pluripotent Stem Cells.
- A549 Cells, Cell Differentiation, Embryonic Development, Humans, Metabolic Networks and Pathways, Proteomics, Virus Replication.
Abstract
Maternal influenza infection during pregnancy was reported multiple times as the possible cause of many defects and congenital anomalies. Apart from several cases of influenza-related miscarriage during various trimesters of pregnancy, some epidemiological data suggest a link between maternal influenza infection and genetic abnormalities in offspring. However, there are no reports yet describing how maternal influenza alters cellular pathways at early stages of development to result in congenital defects in the fetus. In the present study, using proteomic approaches, we utilized human-induced pluripotent stem cells (hiPSCs) for modeling intrablastocyst infection with influenza virus to not only investigate the vulnerability and responses of pluripotent stem cells to this virus but also to determine the possible impacts of influenza on pluripotency and signaling pathways controlling differentiation and embryogenesis. Our data indicated viral protein production in influenza A virus (IAV)-infected hiPSCs. However, viral replication was restricted in these cells, but cell viability and pluripotency were negatively affected. These events occurred simultaneously with an excessive level of IAV-induced autophagy as well as cytopathic effects. Quantitative SOMAscan screening also indicated that changes in the proteome of hiPSCs corresponded to abnormal differentiation in these cells. Taken together, our results showed that IAV-modulated reduction in hiPSC pluripotency is associated with significant activation of autophagy. Further investigations are required to explore the role of IAV-induced autophagy in leading pluripotent stem cells toward abnormal differentiation and impaired development in early stages of embryogenesis.
DOI: 10.1038/s41419-019-1567-4
PubMed: 31000695
PubMed Central: PMC6472374
Affiliations:
Links toward previous steps (curation, corpus...)
Le document en format XML
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Sequiera</name><affiliation wicri:level="4"><nlm:affiliation>Department of Physiology and Pathophysiology, University of Manitoba, Winnipeg, MB, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Department of Physiology and Pathophysiology, University of Manitoba, Winnipeg, MB</wicri:regionArea><orgName type="university">Université du Manitoba</orgName><placeName><settlement type="city">Winnipeg</settlement><region type="state">Manitoba</region></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Institute of Cardiovascular Sciences, Albrechtsen Research Centre, St. Boniface Hospital, Winnipeg, MB, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Institute of Cardiovascular Sciences, Albrechtsen Research Centre, St. Boniface Hospital, Winnipeg, MB</wicri:regionArea><wicri:noRegion>MB</wicri:noRegion></affiliation></author><author><name sortKey="Dhingra, Sanjiv" sort="Dhingra, Sanjiv" uniqKey="Dhingra S" first="Sanjiv" last="Dhingra">Sanjiv Dhingra</name><affiliation wicri:level="4"><nlm:affiliation>Department of Physiology and Pathophysiology, University of Manitoba, Winnipeg, MB, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Department of Physiology and Pathophysiology, University of Manitoba, Winnipeg, MB</wicri:regionArea><orgName type="university">Université du Manitoba</orgName><placeName><settlement type="city">Winnipeg</settlement><region type="state">Manitoba</region></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Institute of Cardiovascular Sciences, Albrechtsen Research Centre, St. Boniface Hospital, Winnipeg, MB, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Institute of Cardiovascular Sciences, Albrechtsen Research Centre, St. Boniface Hospital, Winnipeg, MB</wicri:regionArea><wicri:noRegion>MB</wicri:noRegion></affiliation></author><author><name sortKey="Coombs, Kevin M" sort="Coombs, Kevin M" uniqKey="Coombs K" first="Kevin M" last="Coombs">Kevin M. Coombs</name><affiliation wicri:level="4"><nlm:affiliation>Department of Medical Microbiology and Infectious Diseases, University of Manitoba, Winnipeg, MB, Canada. kevin.coombs@umanitoba.ca.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Department of Medical Microbiology and Infectious Diseases, University of Manitoba, Winnipeg, MB</wicri:regionArea><orgName type="university">Université du Manitoba</orgName><placeName><settlement type="city">Winnipeg</settlement><region type="state">Manitoba</region></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Manitoba Centre for Proteomics and Systems Biology, Winnipeg, MB, Canada. kevin.coombs@umanitoba.ca.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Manitoba Centre for Proteomics and Systems Biology, Winnipeg, MB</wicri:regionArea><wicri:noRegion>MB</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Children's Hospital Research Institute of Manitoba, Winnipeg, MB, Canada. kevin.coombs@umanitoba.ca.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Children's Hospital Research Institute of Manitoba, Winnipeg, MB</wicri:regionArea><wicri:noRegion>MB</wicri:noRegion></affiliation></author></analytic><series><title level="j">Cell death & disease</title><idno type="eISSN">2041-4889</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>A549 Cells (MeSH)</term><term>Autophagy (drug effects)</term><term>Cell Differentiation (MeSH)</term><term>Embryonic Development (MeSH)</term><term>Humans (MeSH)</term><term>Induced Pluripotent Stem Cells (cytology)</term><term>Induced Pluripotent Stem Cells (metabolism)</term><term>Induced Pluripotent Stem Cells (virology)</term><term>Influenza A virus (physiology)</term><term>Macrolides (pharmacology)</term><term>Metabolic Networks and Pathways (MeSH)</term><term>Nanog Homeobox Protein (metabolism)</term><term>Proteome (analysis)</term><term>Proteomics (MeSH)</term><term>SOXB1 Transcription Factors (metabolism)</term><term>Sirolimus (pharmacology)</term><term>Virus Replication (MeSH)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Autophagie (effets des médicaments et des substances chimiques)</term><term>Cellules A549 (MeSH)</term><term>Cellules souches pluripotentes induites (cytologie)</term><term>Cellules souches pluripotentes induites (métabolisme)</term><term>Cellules souches pluripotentes induites (virologie)</term><term>Différenciation cellulaire (MeSH)</term><term>Développement embryonnaire (MeSH)</term><term>Facteurs de transcription SOX-B1 (métabolisme)</term><term>Humains (MeSH)</term><term>Macrolides (pharmacologie)</term><term>Protéine homéotique Nanog (métabolisme)</term><term>Protéome (analyse)</term><term>Protéomique (MeSH)</term><term>Réplication virale (MeSH)</term><term>Sirolimus (pharmacologie)</term><term>Virus de la grippe A (physiologie)</term><term>Voies et réseaux métaboliques (MeSH)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="analysis" xml:lang="en"><term>Proteome</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Nanog Homeobox Protein</term><term>SOXB1 Transcription Factors</term></keywords><keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en"><term>Macrolides</term><term>Sirolimus</term></keywords><keywords scheme="MESH" qualifier="analyse" xml:lang="fr"><term>Protéome</term></keywords><keywords scheme="MESH" qualifier="cytologie" xml:lang="fr"><term>Cellules souches pluripotentes induites</term></keywords><keywords scheme="MESH" qualifier="cytology" xml:lang="en"><term>Induced Pluripotent Stem Cells</term></keywords><keywords scheme="MESH" qualifier="drug effects" xml:lang="en"><term>Autophagy</term></keywords><keywords scheme="MESH" qualifier="effets des médicaments et des substances chimiques" xml:lang="fr"><term>Autophagie</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Induced Pluripotent Stem Cells</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Cellules souches pluripotentes induites</term><term>Facteurs de transcription SOX-B1</term><term>Protéine homéotique Nanog</term></keywords><keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr"><term>Macrolides</term><term>Sirolimus</term></keywords><keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Virus de la grippe A</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Influenza A virus</term></keywords><keywords scheme="MESH" qualifier="virologie" xml:lang="fr"><term>Cellules souches pluripotentes induites</term></keywords><keywords scheme="MESH" qualifier="virology" xml:lang="en"><term>Induced Pluripotent Stem Cells</term></keywords><keywords scheme="MESH" xml:lang="en"><term>A549 Cells</term><term>Cell Differentiation</term><term>Embryonic Development</term><term>Humans</term><term>Metabolic Networks and Pathways</term><term>Proteomics</term><term>Virus Replication</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Cellules A549</term><term>Différenciation cellulaire</term><term>Développement embryonnaire</term><term>Humains</term><term>Protéomique</term><term>Réplication virale</term><term>Voies et réseaux métaboliques</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Maternal influenza infection during pregnancy was reported multiple times as the possible cause of many defects and congenital anomalies. Apart from several cases of influenza-related miscarriage during various trimesters of pregnancy, some epidemiological data suggest a link between maternal influenza infection and genetic abnormalities in offspring. However, there are no reports yet describing how maternal influenza alters cellular pathways at early stages of development to result in congenital defects in the fetus. In the present study, using proteomic approaches, we utilized human-induced pluripotent stem cells (hiPSCs) for modeling intrablastocyst infection with influenza virus to not only investigate the vulnerability and responses of pluripotent stem cells to this virus but also to determine the possible impacts of influenza on pluripotency and signaling pathways controlling differentiation and embryogenesis. Our data indicated viral protein production in influenza A virus (IAV)-infected hiPSCs. However, viral replication was restricted in these cells, but cell viability and pluripotency were negatively affected. These events occurred simultaneously with an excessive level of IAV-induced autophagy as well as cytopathic effects. Quantitative SOMAscan screening also indicated that changes in the proteome of hiPSCs corresponded to abnormal differentiation in these cells. Taken together, our results showed that IAV-modulated reduction in hiPSC pluripotency is associated with significant activation of autophagy. Further investigations are required to explore the role of IAV-induced autophagy in leading pluripotent stem cells toward abnormal differentiation and impaired development in early stages of embryogenesis.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">31000695</PMID><DateCompleted><Year>2020</Year><Month>05</Month><Day>19</Day></DateCompleted><DateRevised><Year>2020</Year><Month>05</Month><Day>19</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2041-4889</ISSN><JournalIssue CitedMedium="Internet"><Volume>10</Volume><Issue>5</Issue><PubDate><Year>2019</Year><Month>04</Month><Day>18</Day></PubDate></JournalIssue><Title>Cell death & disease</Title><ISOAbbreviation>Cell Death Dis</ISOAbbreviation></Journal><ArticleTitle>Influenza a virus-triggered autophagy decreases the pluripotency of human-induced pluripotent stem cells.</ArticleTitle><Pagination><MedlinePgn>337</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1038/s41419-019-1567-4</ELocationID><Abstract><AbstractText>Maternal influenza infection during pregnancy was reported multiple times as the possible cause of many defects and congenital anomalies. Apart from several cases of influenza-related miscarriage during various trimesters of pregnancy, some epidemiological data suggest a link between maternal influenza infection and genetic abnormalities in offspring. However, there are no reports yet describing how maternal influenza alters cellular pathways at early stages of development to result in congenital defects in the fetus. In the present study, using proteomic approaches, we utilized human-induced pluripotent stem cells (hiPSCs) for modeling intrablastocyst infection with influenza virus to not only investigate the vulnerability and responses of pluripotent stem cells to this virus but also to determine the possible impacts of influenza on pluripotency and signaling pathways controlling differentiation and embryogenesis. Our data indicated viral protein production in influenza A virus (IAV)-infected hiPSCs. However, viral replication was restricted in these cells, but cell viability and pluripotency were negatively affected. These events occurred simultaneously with an excessive level of IAV-induced autophagy as well as cytopathic effects. Quantitative SOMAscan screening also indicated that changes in the proteome of hiPSCs corresponded to abnormal differentiation in these cells. Taken together, our results showed that IAV-modulated reduction in hiPSC pluripotency is associated with significant activation of autophagy. Further investigations are required to explore the role of IAV-induced autophagy in leading pluripotent stem cells toward abnormal differentiation and impaired development in early stages of embryogenesis.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Zahedi-Amiri</LastName><ForeName>Ali</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Medical Microbiology and Infectious Diseases, University of Manitoba, Winnipeg, MB, Canada.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Manitoba Centre for Proteomics and Systems Biology, Winnipeg, MB, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sequiera</LastName><ForeName>Glen L</ForeName><Initials>GL</Initials><AffiliationInfo><Affiliation>Department of Physiology and Pathophysiology, University of Manitoba, Winnipeg, MB, Canada.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Institute of Cardiovascular Sciences, Albrechtsen Research Centre, St. Boniface Hospital, Winnipeg, MB, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dhingra</LastName><ForeName>Sanjiv</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Department of Physiology and Pathophysiology, University of Manitoba, Winnipeg, MB, Canada.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Institute of Cardiovascular Sciences, Albrechtsen Research Centre, St. Boniface Hospital, Winnipeg, MB, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Coombs</LastName><ForeName>Kevin M</ForeName><Initials>KM</Initials><AffiliationInfo><Affiliation>Department of Medical Microbiology and Infectious Diseases, University of Manitoba, Winnipeg, MB, Canada. kevin.coombs@umanitoba.ca.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Manitoba Centre for Proteomics and Systems Biology, Winnipeg, MB, Canada. kevin.coombs@umanitoba.ca.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Children's Hospital Research Institute of Manitoba, Winnipeg, MB, Canada. kevin.coombs@umanitoba.ca.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>MOP-106713</GrantID><Agency>CIHR</Agency><Country>Canada</Country></Grant><Grant><GrantID>MOP-142265</GrantID><Agency>CIHR</Agency><Country>Canada</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>04</Month><Day>18</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Cell Death Dis</MedlineTA><NlmUniqueID>101524092</NlmUniqueID></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D018942">Macrolides</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D000071317">Nanog Homeobox Protein</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D020543">Proteome</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D055748">SOXB1 Transcription Factors</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="C527783">Sox2 protein, mouse</NameOfSubstance></Chemical><Chemical><RegistryNumber>88899-55-2</RegistryNumber><NameOfSubstance UI="C040929">bafilomycin A1</NameOfSubstance></Chemical><Chemical><RegistryNumber>W36ZG6FT64</RegistryNumber><NameOfSubstance UI="D020123">Sirolimus</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000072283" MajorTopicYN="N">A549 Cells</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D001343" MajorTopicYN="Y">Autophagy</DescriptorName><QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D002454" MajorTopicYN="N">Cell Differentiation</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D047108" MajorTopicYN="N">Embryonic Development</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D057026" MajorTopicYN="N">Induced Pluripotent Stem Cells</DescriptorName><QualifierName UI="Q000166" MajorTopicYN="N">cytology</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName><QualifierName UI="Q000821" MajorTopicYN="N">virology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D009980" MajorTopicYN="N">Influenza A virus</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D018942" MajorTopicYN="N">Macrolides</DescriptorName><QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D053858" MajorTopicYN="N">Metabolic Networks and Pathways</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D000071317" MajorTopicYN="N">Nanog Homeobox Protein</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D020543" MajorTopicYN="N">Proteome</DescriptorName><QualifierName UI="Q000032" MajorTopicYN="N">analysis</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D040901" MajorTopicYN="N">Proteomics</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D055748" MajorTopicYN="N">SOXB1 Transcription Factors</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D020123" MajorTopicYN="N">Sirolimus</DescriptorName><QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D014779" MajorTopicYN="N">Virus Replication</DescriptorName></MeshHeading></MeshHeadingList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year><Month>10</Month><Day>01</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>04</Month><Day>04</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2019</Year><Month>03</Month><Day>26</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>4</Month><Day>20</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2019</Year><Month>4</Month><Day>20</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>5</Month><Day>20</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">31000695</ArticleId><ArticleId IdType="doi">10.1038/s41419-019-1567-4</ArticleId><ArticleId IdType="pii">10.1038/s41419-019-1567-4</ArticleId><ArticleId IdType="pmc">PMC6472374</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Canada</li></country><region><li>Manitoba</li></region><settlement><li>Winnipeg</li></settlement><orgName><li>Université du Manitoba</li></orgName></list><tree><country name="Canada"><region name="Manitoba"><name sortKey="Zahedi Amiri, Ali" sort="Zahedi Amiri, Ali" uniqKey="Zahedi Amiri A" first="Ali" last="Zahedi-Amiri">Ali Zahedi-Amiri</name></region><name sortKey="Coombs, Kevin M" sort="Coombs, Kevin M" uniqKey="Coombs K" first="Kevin M" last="Coombs">Kevin M. Coombs</name><name sortKey="Coombs, Kevin M" sort="Coombs, Kevin M" uniqKey="Coombs K" first="Kevin M" last="Coombs">Kevin M. Coombs</name><name sortKey="Coombs, Kevin M" sort="Coombs, Kevin M" uniqKey="Coombs K" first="Kevin M" last="Coombs">Kevin M. Coombs</name><name sortKey="Dhingra, Sanjiv" sort="Dhingra, Sanjiv" uniqKey="Dhingra S" first="Sanjiv" last="Dhingra">Sanjiv Dhingra</name><name sortKey="Dhingra, Sanjiv" sort="Dhingra, Sanjiv" uniqKey="Dhingra S" first="Sanjiv" last="Dhingra">Sanjiv Dhingra</name><name sortKey="Sequiera, Glen L" sort="Sequiera, Glen L" uniqKey="Sequiera G" first="Glen L" last="Sequiera">Glen L. Sequiera</name><name sortKey="Sequiera, Glen L" sort="Sequiera, Glen L" uniqKey="Sequiera G" first="Glen L" last="Sequiera">Glen L. Sequiera</name><name sortKey="Zahedi Amiri, Ali" sort="Zahedi Amiri, Ali" uniqKey="Zahedi Amiri A" first="Ali" last="Zahedi-Amiri">Ali Zahedi-Amiri</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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{{Explor lien
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|area= RapamycinFungusV1
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