Decoding the temporal nature of brain GR activity in the NFκB signal transition leading to depressive-like behavior.
Identifieur interne : 000084 ( Main/Exploration ); précédent : 000083; suivant : 000085Decoding the temporal nature of brain GR activity in the NFκB signal transition leading to depressive-like behavior.
Auteurs : Young-Min Han [Corée du Sud] ; Min Sun Kim [Corée du Sud] ; Juyeong Jo [Corée du Sud] ; Daiha Shin [Corée du Sud] ; Seung-Hae Kwon [Corée du Sud] ; Jong Bok Seo [Corée du Sud] ; Dongmin Kang [Corée du Sud] ; Byoung Dae Lee [Corée du Sud] ; Hoon Ryu [Corée du Sud] ; Eun Mi Hwang [Corée du Sud] ; Jae-Min Kim [Corée du Sud] ; Paresh D. Patel [États-Unis] ; David M. Lyons [États-Unis] ; Alan F. Schatzberg [États-Unis] ; Song Her [Corée du Sud]Source :
- Molecular psychiatry [ 1476-5578 ] ; 2021.
Abstract
The fine-tuning of neuroinflammation is crucial for brain homeostasis as well as its immune response. The transcription factor, nuclear factor-κ-B (NFκB) is a key inflammatory player that is antagonized via anti-inflammatory actions exerted by the glucocorticoid receptor (GR). However, technical limitations have restricted our understanding of how GR is involved in the dynamics of NFκB in vivo. In this study, we used an improved lentiviral-based reporter to elucidate the time course of NFκB and GR activities during behavioral changes from sickness to depression induced by a systemic lipopolysaccharide challenge. The trajectory of NFκB activity established a behavioral basis for the NFκB signal transition involved in three phases, sickness-early-phase, normal-middle-phase, and depressive-like-late-phase. The temporal shift in brain GR activity was differentially involved in the transition of NFκB signals during the normal and depressive-like phases. The middle-phase GR effectively inhibited NFκB in a glucocorticoid-dependent manner, but the late-phase GR had no inhibitory action. Furthermore, we revealed the cryptic role of basal GR activity in the early NFκB signal transition, as evidenced by the fact that blocking GR activity with RU486 led to early depressive-like episodes through the emergence of the brain NFκB activity. These results highlight the inhibitory action of GR on NFκB by the basal and activated hypothalamic-pituitary-adrenal (HPA)-axis during body-to-brain inflammatory spread, providing clues about molecular mechanisms underlying systemic inflammation caused by such as COVID-19 infection, leading to depression.
DOI: 10.1038/s41380-021-01016-1
PubMed: 33483691
PubMed Central: PMC7821461
Affiliations:
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Sud</country><wicri:regionArea>Department of Psychiatry, Chonnam National University Medical School, Seoul</wicri:regionArea><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><author><name sortKey="Patel, Paresh D" sort="Patel, Paresh D" uniqKey="Patel P" first="Paresh D" last="Patel">Paresh D. Patel</name><affiliation wicri:level="2"><nlm:affiliation>Department of Psychiatry, Molecular and Behavioral Neuroscience Institute, University of Michigan Medical Centre, Ann Arbor, MI, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Psychiatry, Molecular and Behavioral Neuroscience Institute, University of Michigan Medical Centre, Ann Arbor, MI</wicri:regionArea><placeName><region type="state">Michigan</region></placeName></affiliation></author><author><name sortKey="Lyons, David M" sort="Lyons, David M" uniqKey="Lyons D" first="David M" last="Lyons">David M. 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Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Seoul Centre, Korea Basic Science Institute, Seoul</wicri:regionArea><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><author><name sortKey="Kim, Min Sun" sort="Kim, Min Sun" uniqKey="Kim M" first="Min Sun" last="Kim">Min Sun Kim</name><affiliation wicri:level="3"><nlm:affiliation>Seoul Centre, Korea Basic Science Institute, Seoul, South Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Seoul Centre, Korea Basic Science Institute, Seoul</wicri:regionArea><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><author><name sortKey="Jo, Juyeong" sort="Jo, Juyeong" uniqKey="Jo J" first="Juyeong" last="Jo">Juyeong Jo</name><affiliation wicri:level="3"><nlm:affiliation>Seoul Centre, Korea Basic Science Institute, Seoul, South Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Seoul Centre, Korea Basic Science Institute, Seoul</wicri:regionArea><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><author><name sortKey="Shin, Daiha" sort="Shin, Daiha" uniqKey="Shin D" first="Daiha" last="Shin">Daiha Shin</name><affiliation wicri:level="3"><nlm:affiliation>Seoul Centre, Korea Basic Science Institute, Seoul, South Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Seoul Centre, Korea Basic Science Institute, Seoul</wicri:regionArea><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><author><name sortKey="Kwon, Seung Hae" sort="Kwon, Seung Hae" uniqKey="Kwon S" first="Seung-Hae" last="Kwon">Seung-Hae Kwon</name><affiliation wicri:level="3"><nlm:affiliation>Seoul Centre, Korea Basic Science Institute, Seoul, South Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Seoul Centre, Korea Basic Science Institute, Seoul</wicri:regionArea><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><author><name sortKey="Seo, Jong Bok" sort="Seo, Jong Bok" uniqKey="Seo J" first="Jong Bok" last="Seo">Jong Bok Seo</name><affiliation wicri:level="3"><nlm:affiliation>Seoul Centre, Korea Basic Science Institute, Seoul, South Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Seoul Centre, Korea Basic Science Institute, Seoul</wicri:regionArea><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><author><name sortKey="Kang, Dongmin" sort="Kang, Dongmin" uniqKey="Kang D" first="Dongmin" last="Kang">Dongmin Kang</name><affiliation wicri:level="3"><nlm:affiliation>Department of Life Science, Ewha Womans University, Seoul, South Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Life Science, Ewha Womans University, Seoul</wicri:regionArea><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><author><name sortKey="Lee, Byoung Dae" sort="Lee, Byoung Dae" uniqKey="Lee B" first="Byoung Dae" last="Lee">Byoung Dae Lee</name><affiliation wicri:level="3"><nlm:affiliation>Department of Physiology, School of Medicine, Kyung Hee University, Seoul, South Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Physiology, School of Medicine, Kyung Hee University, Seoul</wicri:regionArea><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><author><name sortKey="Ryu, Hoon" sort="Ryu, Hoon" uniqKey="Ryu H" first="Hoon" last="Ryu">Hoon Ryu</name><affiliation wicri:level="3"><nlm:affiliation>Neuroscience Centre, Korea Institute of Science and Technology, Seoul, South Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Neuroscience Centre, Korea Institute of Science and Technology, Seoul</wicri:regionArea><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><author><name sortKey="Hwang, Eun Mi" sort="Hwang, Eun Mi" uniqKey="Hwang E" first="Eun Mi" last="Hwang">Eun Mi Hwang</name><affiliation wicri:level="3"><nlm:affiliation>Center for Functional Connectomics, Korea Institute of Science and Technology, Seoul, South Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Center for Functional Connectomics, Korea Institute of Science and Technology, Seoul</wicri:regionArea><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><author><name sortKey="Kim, Jae Min" sort="Kim, Jae Min" uniqKey="Kim J" first="Jae-Min" last="Kim">Jae-Min Kim</name><affiliation wicri:level="3"><nlm:affiliation>Department of Psychiatry, Chonnam National University Medical School, Seoul, South Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Psychiatry, Chonnam National University Medical School, Seoul</wicri:regionArea><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><author><name sortKey="Patel, Paresh D" sort="Patel, Paresh D" uniqKey="Patel P" first="Paresh D" last="Patel">Paresh D. Patel</name><affiliation wicri:level="2"><nlm:affiliation>Department of Psychiatry, Molecular and Behavioral Neuroscience Institute, University of Michigan Medical Centre, Ann Arbor, MI, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Psychiatry, Molecular and Behavioral Neuroscience Institute, University of Michigan Medical Centre, Ann Arbor, MI</wicri:regionArea><placeName><region type="state">Michigan</region></placeName></affiliation></author><author><name sortKey="Lyons, David M" sort="Lyons, David M" uniqKey="Lyons D" first="David M" last="Lyons">David M. Lyons</name><affiliation wicri:level="2"><nlm:affiliation>Departments of Psychiatry, Stanford University Medical Centre, Stanford, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Departments of Psychiatry, Stanford University Medical Centre, Stanford, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Schatzberg, Alan F" sort="Schatzberg, Alan F" uniqKey="Schatzberg A" first="Alan F" last="Schatzberg">Alan F. Schatzberg</name><affiliation wicri:level="2"><nlm:affiliation>Departments of Psychiatry, Stanford University Medical Centre, Stanford, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Departments of Psychiatry, Stanford University Medical Centre, Stanford, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Her, Song" sort="Her, Song" uniqKey="Her S" first="Song" last="Her">Song Her</name><affiliation wicri:level="3"><nlm:affiliation>Seoul Centre, Korea Basic Science Institute, Seoul, South Korea. swher@kbsi.re.kr.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Seoul Centre, Korea Basic Science Institute, Seoul</wicri:regionArea><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author></analytic><series><title level="j">Molecular psychiatry</title><idno type="eISSN">1476-5578</idno><imprint><date when="2021" type="published">2021</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The fine-tuning of neuroinflammation is crucial for brain homeostasis as well as its immune response. The transcription factor, nuclear factor-κ-B (NFκB) is a key inflammatory player that is antagonized via anti-inflammatory actions exerted by the glucocorticoid receptor (GR). However, technical limitations have restricted our understanding of how GR is involved in the dynamics of NFκB in vivo. In this study, we used an improved lentiviral-based reporter to elucidate the time course of NFκB and GR activities during behavioral changes from sickness to depression induced by a systemic lipopolysaccharide challenge. The trajectory of NFκB activity established a behavioral basis for the NFκB signal transition involved in three phases, sickness-early-phase, normal-middle-phase, and depressive-like-late-phase. The temporal shift in brain GR activity was differentially involved in the transition of NFκB signals during the normal and depressive-like phases. The middle-phase GR effectively inhibited NFκB in a glucocorticoid-dependent manner, but the late-phase GR had no inhibitory action. Furthermore, we revealed the cryptic role of basal GR activity in the early NFκB signal transition, as evidenced by the fact that blocking GR activity with RU486 led to early depressive-like episodes through the emergence of the brain NFκB activity. These results highlight the inhibitory action of GR on NFκB by the basal and activated hypothalamic-pituitary-adrenal (HPA)-axis during body-to-brain inflammatory spread, providing clues about molecular mechanisms underlying systemic inflammation caused by such as COVID-19 infection, leading to depression.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">33483691</PMID><DateRevised><Year>2021</Year><Month>01</Month><Day>25</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1476-5578</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2021</Year><Month>Jan</Month><Day>22</Day></PubDate></JournalIssue><Title>Molecular psychiatry</Title><ISOAbbreviation>Mol Psychiatry</ISOAbbreviation></Journal><ArticleTitle>Decoding the temporal nature of brain GR activity in the NFκB signal transition leading to depressive-like behavior.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.1038/s41380-021-01016-1</ELocationID><Abstract><AbstractText>The fine-tuning of neuroinflammation is crucial for brain homeostasis as well as its immune response. The transcription factor, nuclear factor-κ-B (NFκB) is a key inflammatory player that is antagonized via anti-inflammatory actions exerted by the glucocorticoid receptor (GR). However, technical limitations have restricted our understanding of how GR is involved in the dynamics of NFκB in vivo. In this study, we used an improved lentiviral-based reporter to elucidate the time course of NFκB and GR activities during behavioral changes from sickness to depression induced by a systemic lipopolysaccharide challenge. The trajectory of NFκB activity established a behavioral basis for the NFκB signal transition involved in three phases, sickness-early-phase, normal-middle-phase, and depressive-like-late-phase. The temporal shift in brain GR activity was differentially involved in the transition of NFκB signals during the normal and depressive-like phases. The middle-phase GR effectively inhibited NFκB in a glucocorticoid-dependent manner, but the late-phase GR had no inhibitory action. Furthermore, we revealed the cryptic role of basal GR activity in the early NFκB signal transition, as evidenced by the fact that blocking GR activity with RU486 led to early depressive-like episodes through the emergence of the brain NFκB activity. These results highlight the inhibitory action of GR on NFκB by the basal and activated hypothalamic-pituitary-adrenal (HPA)-axis during body-to-brain inflammatory spread, providing clues about molecular mechanisms underlying systemic inflammation caused by such as COVID-19 infection, leading to depression.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Han</LastName><ForeName>Young-Min</ForeName><Initials>YM</Initials><AffiliationInfo><Affiliation>Seoul Centre, Korea Basic Science Institute, Seoul, South Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kim</LastName><ForeName>Min Sun</ForeName><Initials>MS</Initials><AffiliationInfo><Affiliation>Seoul Centre, Korea Basic Science Institute, Seoul, South Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jo</LastName><ForeName>Juyeong</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Seoul Centre, Korea Basic Science Institute, Seoul, South Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Shin</LastName><ForeName>Daiha</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Seoul Centre, Korea Basic Science Institute, Seoul, South Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kwon</LastName><ForeName>Seung-Hae</ForeName><Initials>SH</Initials><AffiliationInfo><Affiliation>Seoul Centre, Korea Basic Science Institute, Seoul, South Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Seo</LastName><ForeName>Jong Bok</ForeName><Initials>JB</Initials><AffiliationInfo><Affiliation>Seoul Centre, Korea Basic Science Institute, Seoul, South Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kang</LastName><ForeName>Dongmin</ForeName><Initials>D</Initials><Identifier Source="ORCID">http://orcid.org/0000-0001-5997-625X</Identifier><AffiliationInfo><Affiliation>Department of Life Science, Ewha Womans University, Seoul, South Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lee</LastName><ForeName>Byoung Dae</ForeName><Initials>BD</Initials><AffiliationInfo><Affiliation>Department of Physiology, School of Medicine, Kyung Hee University, Seoul, South Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ryu</LastName><ForeName>Hoon</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Neuroscience Centre, Korea Institute of Science and Technology, Seoul, South Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hwang</LastName><ForeName>Eun Mi</ForeName><Initials>EM</Initials><AffiliationInfo><Affiliation>Center for Functional Connectomics, Korea Institute of Science and Technology, Seoul, South Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kim</LastName><ForeName>Jae-Min</ForeName><Initials>JM</Initials><AffiliationInfo><Affiliation>Department of Psychiatry, Chonnam National University Medical School, Seoul, South Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Patel</LastName><ForeName>Paresh D</ForeName><Initials>PD</Initials><AffiliationInfo><Affiliation>Department of Psychiatry, Molecular and Behavioral Neuroscience Institute, University of Michigan Medical Centre, Ann Arbor, MI, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lyons</LastName><ForeName>David M</ForeName><Initials>DM</Initials><AffiliationInfo><Affiliation>Departments of Psychiatry, Stanford University Medical Centre, Stanford, CA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Schatzberg</LastName><ForeName>Alan F</ForeName><Initials>AF</Initials><AffiliationInfo><Affiliation>Departments of Psychiatry, Stanford University Medical Centre, Stanford, CA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Her</LastName><ForeName>Song</ForeName><Initials>S</Initials><Identifier Source="ORCID">http://orcid.org/0000-0001-9678-3203</Identifier><AffiliationInfo><Affiliation>Seoul Centre, Korea Basic Science Institute, Seoul, South Korea. swher@kbsi.re.kr.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>NRF-2016M3C7A1904362</GrantID><Agency>National Research Foundation of Korea (NRF)</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2021</Year><Month>01</Month><Day>22</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Mol Psychiatry</MedlineTA><NlmUniqueID>9607835</NlmUniqueID><ISSNLinking>1359-4184</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>01</Month><Day>03</Day></PubMedPubDate><PubMedPubDate 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