Microbiota metabolites modulate the T helper 17 to regulatory T cell (Th17/Treg) imbalance promoting resilience to stress-induced anxiety- and depressive-like behaviors.
Identifieur interne : 000114 ( Main/Exploration ); précédent : 000113; suivant : 000115Microbiota metabolites modulate the T helper 17 to regulatory T cell (Th17/Treg) imbalance promoting resilience to stress-induced anxiety- and depressive-like behaviors.
Auteurs : Susan Westfall [États-Unis] ; Francesca Caracci [États-Unis] ; Danyue Zhao [États-Unis] ; Qing-Li Wu [États-Unis] ; Tal Frolinger [États-Unis] ; James Simon [États-Unis] ; Giulio Maria Pasinetti [États-Unis]Source :
- Brain, behavior, and immunity [ 1090-2139 ] ; 2020.
Abstract
Chronic stress disrupts immune homeostasis while gut microbiota-derived metabolites attenuate inflammation, thus promoting resilience to stress-induced immune and behavioral abnormalities. There are both peripheral and brain region-specific maladaptations of the immune response to chronic stress that produce interrelated mechanistic considerations required for the design of novel therapeutic strategies for prevention of stress-induced psychological impairment. This study shows that a combination of probiotics and polyphenol-rich prebiotics, a synbiotic, attenuates the chronic-stress induced inflammatory responses in the ileum and the prefrontal cortex promoting resilience to the consequent depressive- and anxiety-like behaviors in male mice. Pharmacokinetic studies revealed that this effect may be attributed to specific synbiotic-produced metabolites including 4-hydroxyphenylpropionic, 4-hydroxyphenylacetic acid and caffeic acid. Using a model of chronic unpredictable stress, behavioral abnormalities were associated to strong immune cell activation and recruitment in the ileum while inflammasome pathways were implicated in the prefrontal cortex and hippocampus. Chronic stress also upregulated the ratio of activated proinflammatory T helper 17 (Th17) to regulatory T cells (Treg) in the liver and ileum and it was predicted with ingenuity pathway analysis that the aryl hydrocarbon receptor (AHR) could be driving the synbiotic's effect on the ileum's inflammatory response to stress. Synbiotic treatment indiscriminately attenuated the stress-induced immune and behavioral aberrations in both the ileum and the brain while in a gut-immune co-culture model, the synbiotic-specific metabolites promoted anti-inflammatory activity through the AHR. Overall, this study characterizes a novel synbiotic treatment for chronic-stress induced behavioral impairments while defining a putative mechanism of gut-microbiota host interaction for modulating the peripheral and brain immune systems.
DOI: 10.1016/j.bbi.2020.10.013
PubMed: 33096252
Affiliations:
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Peters Veterans Affairs Medical Center, Bronx, New York, USA. Electronic address: giulio.pasinetti@mssm.edu.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Icahn School of Medicine at Mount Sinai, Department of Neurology, New York, NY, USA; Geriatric Research, Education and Clinical Center, James J. Peters Veterans Affairs Medical Center, Bronx, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author></analytic><series><title level="j">Brain, behavior, and immunity</title><idno type="eISSN">1090-2139</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">Chronic stress disrupts immune homeostasis while gut microbiota-derived metabolites attenuate inflammation, thus promoting resilience to stress-induced immune and behavioral abnormalities. There are both peripheral and brain region-specific maladaptations of the immune response to chronic stress that produce interrelated mechanistic considerations required for the design of novel therapeutic strategies for prevention of stress-induced psychological impairment. This study shows that a combination of probiotics and polyphenol-rich prebiotics, a synbiotic, attenuates the chronic-stress induced inflammatory responses in the ileum and the prefrontal cortex promoting resilience to the consequent depressive- and anxiety-like behaviors in male mice. Pharmacokinetic studies revealed that this effect may be attributed to specific synbiotic-produced metabolites including 4-hydroxyphenylpropionic, 4-hydroxyphenylacetic acid and caffeic acid. Using a model of chronic unpredictable stress, behavioral abnormalities were associated to strong immune cell activation and recruitment in the ileum while inflammasome pathways were implicated in the prefrontal cortex and hippocampus. Chronic stress also upregulated the ratio of activated proinflammatory T helper 17 (Th17) to regulatory T cells (Treg) in the liver and ileum and it was predicted with ingenuity pathway analysis that the aryl hydrocarbon receptor (AHR) could be driving the synbiotic's effect on the ileum's inflammatory response to stress. Synbiotic treatment indiscriminately attenuated the stress-induced immune and behavioral aberrations in both the ileum and the brain while in a gut-immune co-culture model, the synbiotic-specific metabolites promoted anti-inflammatory activity through the AHR. Overall, this study characterizes a novel synbiotic treatment for chronic-stress induced behavioral impairments while defining a putative mechanism of gut-microbiota host interaction for modulating the peripheral and brain immune systems.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">33096252</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>23</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1090-2139</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2020</Year><Month>Oct</Month><Day>20</Day></PubDate></JournalIssue><Title>Brain, behavior, and immunity</Title><ISOAbbreviation>Brain Behav Immun</ISOAbbreviation></Journal><ArticleTitle>Microbiota metabolites modulate the T helper 17 to regulatory T cell (Th17/Treg) imbalance promoting resilience to stress-induced anxiety- and depressive-like behaviors.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">S0889-1591(20)32363-1</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1016/j.bbi.2020.10.013</ELocationID><Abstract><AbstractText>Chronic stress disrupts immune homeostasis while gut microbiota-derived metabolites attenuate inflammation, thus promoting resilience to stress-induced immune and behavioral abnormalities. There are both peripheral and brain region-specific maladaptations of the immune response to chronic stress that produce interrelated mechanistic considerations required for the design of novel therapeutic strategies for prevention of stress-induced psychological impairment. This study shows that a combination of probiotics and polyphenol-rich prebiotics, a synbiotic, attenuates the chronic-stress induced inflammatory responses in the ileum and the prefrontal cortex promoting resilience to the consequent depressive- and anxiety-like behaviors in male mice. Pharmacokinetic studies revealed that this effect may be attributed to specific synbiotic-produced metabolites including 4-hydroxyphenylpropionic, 4-hydroxyphenylacetic acid and caffeic acid. Using a model of chronic unpredictable stress, behavioral abnormalities were associated to strong immune cell activation and recruitment in the ileum while inflammasome pathways were implicated in the prefrontal cortex and hippocampus. Chronic stress also upregulated the ratio of activated proinflammatory T helper 17 (Th17) to regulatory T cells (Treg) in the liver and ileum and it was predicted with ingenuity pathway analysis that the aryl hydrocarbon receptor (AHR) could be driving the synbiotic's effect on the ileum's inflammatory response to stress. Synbiotic treatment indiscriminately attenuated the stress-induced immune and behavioral aberrations in both the ileum and the brain while in a gut-immune co-culture model, the synbiotic-specific metabolites promoted anti-inflammatory activity through the AHR. Overall, this study characterizes a novel synbiotic treatment for chronic-stress induced behavioral impairments while defining a putative mechanism of gut-microbiota host interaction for modulating the peripheral and brain immune systems.</AbstractText><CopyrightInformation>Copyright © 2020. Published by Elsevier Inc.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Westfall</LastName><ForeName>Susan</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Icahn School of Medicine at Mount Sinai, Department of Neurology, New York, NY, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Caracci</LastName><ForeName>Francesca</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Icahn School of Medicine at Mount Sinai, Department of Neurology, New York, NY, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhao</LastName><ForeName>Danyue</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Department of Plant Biology, Rutgers University, New Brunswick, NJ, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wu</LastName><ForeName>Qing-Li</ForeName><Initials>QL</Initials><AffiliationInfo><Affiliation>Department of Plant Biology, Rutgers University, New Brunswick, NJ, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Frolinger</LastName><ForeName>Tal</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>Icahn School of Medicine at Mount Sinai, Department of Neurology, New York, NY, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Simon</LastName><ForeName>James</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Plant Biology, Rutgers University, New Brunswick, NJ, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Maria Pasinetti</LastName><ForeName>Giulio</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Icahn School of Medicine at Mount Sinai, Department of Neurology, New York, NY, USA; Geriatric Research, Education and Clinical Center, James J. Peters Veterans Affairs Medical Center, Bronx, New York, USA. Electronic address: giulio.pasinetti@mssm.edu.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>10</Month><Day>20</Day></ArticleDate></Article><MedlineJournalInfo><Country>Netherlands</Country><MedlineTA>Brain Behav Immun</MedlineTA><NlmUniqueID>8800478</NlmUniqueID><ISSNLinking>0889-1591</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Adaptive Immunity</Keyword><Keyword MajorTopicYN="N">Aryl Hydrocarbon Receptor</Keyword><Keyword MajorTopicYN="N">Gut Microbiota</Keyword><Keyword MajorTopicYN="N">Gut-Brain-Axis</Keyword><Keyword MajorTopicYN="N">Metabolome</Keyword><Keyword MajorTopicYN="N">Neuroinflammation</Keyword><Keyword MajorTopicYN="N">Polyphenols</Keyword><Keyword MajorTopicYN="N">Psychiatric Disorders</Keyword><Keyword MajorTopicYN="N">Regulatory T Cells</Keyword><Keyword MajorTopicYN="N">Th17 Cells</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>07</Month><Day>22</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>10</Month><Day>07</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>10</Month><Day>10</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>10</Month><Day>23</Day><Hour>20</Hour><Minute>11</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>10</Month><Day>24</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>10</Month><Day>24</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">33096252</ArticleId><ArticleId IdType="pii">S0889-1591(20)32363-1</ArticleId><ArticleId IdType="doi">10.1016/j.bbi.2020.10.013</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>États-Unis</li></country><region><li>New Jersey</li><li>État de New York</li></region><settlement><li>New Brunswick (New Jersey)</li></settlement><orgName><li>Université Rutgers</li></orgName></list><tree><country name="États-Unis"><region name="État de New York"><name sortKey="Westfall, Susan" sort="Westfall, Susan" uniqKey="Westfall S" first="Susan" last="Westfall">Susan Westfall</name></region><name sortKey="Caracci, Francesca" sort="Caracci, Francesca" uniqKey="Caracci F" first="Francesca" last="Caracci">Francesca Caracci</name><name sortKey="Frolinger, Tal" sort="Frolinger, Tal" uniqKey="Frolinger T" first="Tal" last="Frolinger">Tal Frolinger</name><name sortKey="Maria Pasinetti, Giulio" sort="Maria Pasinetti, Giulio" uniqKey="Maria Pasinetti G" first="Giulio" last="Maria Pasinetti">Giulio Maria Pasinetti</name><name sortKey="Simon, James" sort="Simon, James" uniqKey="Simon J" first="James" last="Simon">James Simon</name><name sortKey="Wu, Qing Li" sort="Wu, Qing Li" uniqKey="Wu Q" first="Qing-Li" last="Wu">Qing-Li Wu</name><name sortKey="Zhao, Danyue" sort="Zhao, Danyue" uniqKey="Zhao D" first="Danyue" last="Zhao">Danyue Zhao</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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