A food-responsive switch modulates TFEB and autophagy, and determines susceptibility to coxsackievirus infection and pancreatitis.
Identifieur interne : 000158 ( Main/Exploration ); précédent : 000157; suivant : 000159A food-responsive switch modulates TFEB and autophagy, and determines susceptibility to coxsackievirus infection and pancreatitis.
Auteurs : Mehrdad Alirezaei [États-Unis] ; Claudia T. Flynn [États-Unis] ; Selma D. Garcia [États-Unis] ; Taishi Kimura [États-Unis] ; J Lindsay Whitton [États-Unis]Source :
- Autophagy [ 1554-8635 ] ; 2020.
Abstract
Almost a billion people worldwide are chronically undernourished. Herein, using a mouse model of coxsackievirus B3 (CVB3) infection, we report that a single day of food restriction (FR) markedly increases susceptibility to attenuated enterovirus infection, replication, and disease. These "pro-viral" effects, which are rapidly-reversed by the restoration of food, are mediated by several genes whose expression is altered by FR, and which support CVB3 replication. Central to this is TFEB, a protein whose expression and activation status are rapidly increased by FR. TFEB, which regulates the transcription of >100 genes involved in macroautophagy/autophagy and lysosomal biogenesis, responds similarly to both FR and CVB3 infection and plays a pivotal role in determining host susceptibility to CVB3. We propose that, by upregulating TFEB, FR generates an intracellular environment that is more hospitable to the incoming virus, facilitating its replication. This interplay between nutritional status and enterovirus replication has implications for human health and, perhaps, for the evolution of these viruses.Abbreviations: Atg/ATG: autophagy-related; CAR: Coxsackievirus and adenovirus receptor; Cas9: CRISPR associated protein 9; Cre: recombinase that causes recombination; CRISPR: clustered regularly interspaced short palindromic repeats; Ctsb/CTSB: cathepsin B; CVB3: coxsackievirus B3; DsRedCVB3: a recombinant CVB3 that encodes the Discosoma red fluorescent protein; EL: elastase; FR: food restriction; GFP: green fluorescent protein; gRNA: guide RNA; HBSS: Hanks Buffered Salt Solution; LYNUS: lysosomal nutrient sensing machinery; MAP1LC3/LC3: microtubule-associated protein 1 light chain 3; MFI: mean fluorescence intensity; MOI: multiplicity of infection; MTOR: mechanistic target of rapamycin kinase; Nluc: nanoluciferase; NlucCVB3: a recombinant CVB3 encoding nanoluciferase; pfu: plaque-forming unit(s); p.i.: post infection; rCVB: recombinant coxsackievirus B3; RPS6KB/p70S6K: ribosomal protein S6 kinase; RT: room temperature; siRNA: small interfering RNA; TFEB: transcription factor EB; tg: transgenic; TUBB: β-tubulin; UNINF: uninfected; wrt: with respect to; WT: wild type.
DOI: 10.1080/15548627.2020.1720425
PubMed: 32019403
Affiliations:
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Flynn</name><affiliation wicri:level="2"><nlm:affiliation>Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Garcia, Selma D" sort="Garcia, Selma D" uniqKey="Garcia S" first="Selma D" last="Garcia">Selma D. Garcia</name><affiliation wicri:level="2"><nlm:affiliation>Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Kimura, Taishi" sort="Kimura, Taishi" uniqKey="Kimura T" first="Taishi" last="Kimura">Taishi Kimura</name><affiliation wicri:level="2"><nlm:affiliation>Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Whitton, J Lindsay" sort="Whitton, J Lindsay" uniqKey="Whitton J" first="J Lindsay" last="Whitton">J Lindsay Whitton</name><affiliation wicri:level="2"><nlm:affiliation>Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author></analytic><series><title level="j">Autophagy</title><idno type="eISSN">1554-8635</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Almost a billion people worldwide are chronically undernourished. Herein, using a mouse model of coxsackievirus B3 (CVB3) infection, we report that a single day of food restriction (FR) markedly increases susceptibility to attenuated enterovirus infection, replication, and disease. These "pro-viral" effects, which are rapidly-reversed by the restoration of food, are mediated by several genes whose expression is altered by FR, and which support CVB3 replication. Central to this is TFEB, a protein whose expression and activation status are rapidly increased by FR. TFEB, which regulates the transcription of >100 genes involved in macroautophagy/autophagy and lysosomal biogenesis, responds similarly to both FR and CVB3 infection and plays a pivotal role in determining host susceptibility to CVB3. We propose that, by upregulating TFEB, FR generates an intracellular environment that is more hospitable to the incoming virus, facilitating its replication. This interplay between nutritional status and enterovirus replication has implications for human health and, perhaps, for the evolution of these viruses.<b>Abbreviations:</b> Atg/ATG: autophagy-related; CAR: Coxsackievirus and adenovirus receptor; Cas9: CRISPR associated protein 9; Cre: recombinase that causes recombination; CRISPR: clustered regularly interspaced short palindromic repeats; <i>Ctsb</i>/CTSB: cathepsin B; CVB3: coxsackievirus B3; DsRedCVB3: a recombinant CVB3 that encodes the Discosoma red fluorescent protein; EL: elastase; FR: food restriction; GFP: green fluorescent protein; gRNA: guide RNA; HBSS: Hanks Buffered Salt Solution; LYNUS: lysosomal nutrient sensing machinery; MAP1LC3/LC3: microtubule-associated protein 1 light chain 3; MFI: mean fluorescence intensity; MOI: multiplicity of infection; MTOR: mechanistic target of rapamycin kinase; Nluc: nanoluciferase; NlucCVB3: a recombinant CVB3 encoding nanoluciferase; pfu: plaque-forming unit(s); p.i.: post infection; rCVB: recombinant coxsackievirus B3; RPS6KB/p70S6K: ribosomal protein S6 kinase; RT: room temperature; siRNA: small interfering RNA; TFEB: transcription factor EB; tg: transgenic; TUBB: β-tubulin; UNINF: uninfected; wrt: with respect to; WT: wild type.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">32019403</PMID><DateRevised><Year>2020</Year><Month>02</Month><Day>05</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1554-8635</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2020</Year><Month>Feb</Month><Day>04</Day></PubDate></JournalIssue><Title>Autophagy</Title><ISOAbbreviation>Autophagy</ISOAbbreviation></Journal><ArticleTitle>A food-responsive switch modulates TFEB and autophagy, and determines susceptibility to coxsackievirus infection and pancreatitis.</ArticleTitle><Pagination><MedlinePgn>1-18</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1080/15548627.2020.1720425</ELocationID><Abstract><AbstractText>Almost a billion people worldwide are chronically undernourished. Herein, using a mouse model of coxsackievirus B3 (CVB3) infection, we report that a single day of food restriction (FR) markedly increases susceptibility to attenuated enterovirus infection, replication, and disease. These "pro-viral" effects, which are rapidly-reversed by the restoration of food, are mediated by several genes whose expression is altered by FR, and which support CVB3 replication. Central to this is TFEB, a protein whose expression and activation status are rapidly increased by FR. TFEB, which regulates the transcription of >100 genes involved in macroautophagy/autophagy and lysosomal biogenesis, responds similarly to both FR and CVB3 infection and plays a pivotal role in determining host susceptibility to CVB3. We propose that, by upregulating TFEB, FR generates an intracellular environment that is more hospitable to the incoming virus, facilitating its replication. This interplay between nutritional status and enterovirus replication has implications for human health and, perhaps, for the evolution of these viruses.<b>Abbreviations:</b> Atg/ATG: autophagy-related; CAR: Coxsackievirus and adenovirus receptor; Cas9: CRISPR associated protein 9; Cre: recombinase that causes recombination; CRISPR: clustered regularly interspaced short palindromic repeats; <i>Ctsb</i>/CTSB: cathepsin B; CVB3: coxsackievirus B3; DsRedCVB3: a recombinant CVB3 that encodes the Discosoma red fluorescent protein; EL: elastase; FR: food restriction; GFP: green fluorescent protein; gRNA: guide RNA; HBSS: Hanks Buffered Salt Solution; LYNUS: lysosomal nutrient sensing machinery; MAP1LC3/LC3: microtubule-associated protein 1 light chain 3; MFI: mean fluorescence intensity; MOI: multiplicity of infection; MTOR: mechanistic target of rapamycin kinase; Nluc: nanoluciferase; NlucCVB3: a recombinant CVB3 encoding nanoluciferase; pfu: plaque-forming unit(s); p.i.: post infection; rCVB: recombinant coxsackievirus B3; RPS6KB/p70S6K: ribosomal protein S6 kinase; RT: room temperature; siRNA: small interfering RNA; TFEB: transcription factor EB; tg: transgenic; TUBB: β-tubulin; UNINF: uninfected; wrt: with respect to; WT: wild type.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Alirezaei</LastName><ForeName>Mehrdad</ForeName><Initials>M</Initials><Identifier Source="ORCID">https://orcid.org/0000-0003-2154-0789</Identifier><AffiliationInfo><Affiliation>Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Flynn</LastName><ForeName>Claudia T</ForeName><Initials>CT</Initials><AffiliationInfo><Affiliation>Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Garcia</LastName><ForeName>Selma D</ForeName><Initials>SD</Initials><AffiliationInfo><Affiliation>Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kimura</LastName><ForeName>Taishi</ForeName><Initials>T</Initials><Identifier Source="ORCID">https://orcid.org/0000-0003-1360-5431</Identifier><AffiliationInfo><Affiliation>Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Whitton</LastName><ForeName>J Lindsay</ForeName><Initials>JL</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-8218-551X</Identifier><AffiliationInfo><Affiliation>Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA, USA.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>02</Month><Day>04</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Autophagy</MedlineTA><NlmUniqueID>101265188</NlmUniqueID><ISSNLinking>1554-8627</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">ATG5</Keyword><Keyword MajorTopicYN="N">CVB3</Keyword><Keyword MajorTopicYN="N">MTOR</Keyword><Keyword MajorTopicYN="N">RNA virus</Keyword><Keyword MajorTopicYN="N">TFEB</Keyword><Keyword MajorTopicYN="N">autophagy</Keyword><Keyword MajorTopicYN="N">coxsackievirus</Keyword><Keyword MajorTopicYN="N">enterovirus</Keyword><Keyword MajorTopicYN="N">food restriction</Keyword><Keyword MajorTopicYN="N">starvation</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>2</Month><Day>6</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>2</Month><Day>6</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>2</Month><Day>6</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32019403</ArticleId><ArticleId IdType="doi">10.1080/15548627.2020.1720425</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>États-Unis</li></country><region><li>Californie</li></region></list><tree><country name="États-Unis"><region name="Californie"><name sortKey="Alirezaei, Mehrdad" sort="Alirezaei, Mehrdad" uniqKey="Alirezaei M" first="Mehrdad" last="Alirezaei">Mehrdad Alirezaei</name></region><name sortKey="Flynn, Claudia T" sort="Flynn, Claudia T" uniqKey="Flynn C" first="Claudia T" last="Flynn">Claudia T. Flynn</name><name sortKey="Garcia, Selma D" sort="Garcia, Selma D" uniqKey="Garcia S" first="Selma D" last="Garcia">Selma D. Garcia</name><name sortKey="Kimura, Taishi" sort="Kimura, Taishi" uniqKey="Kimura T" first="Taishi" last="Kimura">Taishi Kimura</name><name sortKey="Whitton, J Lindsay" sort="Whitton, J Lindsay" uniqKey="Whitton J" first="J Lindsay" last="Whitton">J Lindsay Whitton</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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