BRG1 attenuates colonic inflammation and tumorigenesis through autophagy-dependent oxidative stress sequestration
Identifieur interne : 000147 ( Pmc/Curation ); précédent : 000146; suivant : 000148BRG1 attenuates colonic inflammation and tumorigenesis through autophagy-dependent oxidative stress sequestration
Auteurs : Min Liu [République populaire de Chine] ; Tongyu Sun [République populaire de Chine] ; Ni Li [République populaire de Chine] ; Junjie Peng [République populaire de Chine] ; Da Fu [République populaire de Chine] ; Wei Li [République populaire de Chine] ; Li Li [République populaire de Chine] ; Wei-Qiang Gao [République populaire de Chine]Source :
- Nature Communications [ 2041-1723 ] ; 2019.
Abstract
Autophagy is a central component of integrated stress responses that influences many inflammatory diseases, including inflammatory bowel disease (IBD) and colorectal cancer (CRC). While the core machinery is known, the molecular basis of the epigenetic regulation of autophagy and its role in colon inflammation remain largely undefined. Here, we report that BRG1, an ATPase subunit of the SWI/SNF chromatin remodeling complex, is required for the homeostatic maintenance of intestinal epithelial cells (IECs) to prevent the inflammation and tumorigenesis. BRG1 emerges as a key regulator that directly governs the transcription of
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DOI: 10.1038/s41467-019-12573-z
PubMed: 31601814
PubMed Central: 6787222
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Key Laboratory of Oncogenes and Related Genes, Renji-Med X Clinical Stem Cell Research Center, Ren Ji Hospital, School of Medicine and School of Biomedical Engineering,</institution><institution>Shanghai Jiao Tong University,</institution></institution-wrap>Shanghai, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0368 8293</institution-id><institution-id institution-id-type="GRID">grid.16821.3c</institution-id><institution>Med-X Research Institute,</institution><institution>Shanghai Jiao Tong University,</institution></institution-wrap>Shanghai, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai</wicri:regionArea></affiliation></author></analytic><series><title level="j">Nature Communications</title><idno type="eISSN">2041-1723</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p id="Par1">Autophagy is a central component of integrated stress responses that influences many inflammatory diseases, including inflammatory bowel disease (IBD) and colorectal cancer (CRC). While the core machinery is known, the molecular basis of the epigenetic regulation of autophagy and its role in colon inflammation remain largely undefined. Here, we report that BRG1, an ATPase subunit of the SWI/SNF chromatin remodeling complex, is required for the homeostatic maintenance of intestinal epithelial cells (IECs) to prevent the inflammation and tumorigenesis. BRG1 emerges as a key regulator that directly governs the transcription of <italic>Atg16l1</italic>, <italic>Ambra1</italic>, <italic>Atg7</italic> and <italic>Wipi2</italic>, which are important for autophagosome biogenesis. Defective autophagy in BRG1-deficient IECs results in excess reactive oxygen species (ROS), which leads to the defects in barrier integrity. Together, our results establish that BRG1 may represent an autophagy checkpoint that is pathogenetically linked to colitis and is therefore likely a potential therapeutic target for disease intervention.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Ekbom, A" uniqKey="Ekbom A">A Ekbom</name></author><author><name sortKey="Helmick, C" uniqKey="Helmick C">C Helmick</name></author><author><name sortKey="Zack, M" uniqKey="Zack M">M Zack</name></author><author><name sortKey="Adami, Ho" uniqKey="Adami H">HO Adami</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Grivennikov, Si" uniqKey="Grivennikov S">SI Grivennikov</name></author><author><name sortKey="Greten, Fr" uniqKey="Greten F">FR Greten</name></author><author><name sortKey="Karin, M" uniqKey="Karin M">M Karin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Turner, Jr" uniqKey="Turner J">JR 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article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Nat Commun</journal-id><journal-id journal-id-type="iso-abbrev">Nat Commun</journal-id><journal-title-group><journal-title>Nature Communications</journal-title></journal-title-group><issn pub-type="epub">2041-1723</issn><publisher><publisher-name>Nature Publishing Group UK</publisher-name><publisher-loc>London</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31601814</article-id><article-id pub-id-type="pmc">6787222</article-id><article-id pub-id-type="publisher-id">12573</article-id><article-id pub-id-type="doi">10.1038/s41467-019-12573-z</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>BRG1 attenuates colonic inflammation and tumorigenesis through autophagy-dependent oxidative stress sequestration</article-title></title-group><contrib-group><contrib contrib-type="author" equal-contrib="yes"><name><surname>Liu</surname><given-names>Min</given-names></name><xref ref-type="aff" rid="Aff1">1</xref><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author" equal-contrib="yes"><name><surname>Sun</surname><given-names>Tongyu</given-names></name><xref ref-type="aff" rid="Aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Li</surname><given-names>Ni</given-names></name><xref ref-type="aff" rid="Aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Peng</surname><given-names>Junjie</given-names></name><xref ref-type="aff" rid="Aff4">4</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0002-0878-2575</contrib-id><name><surname>Fu</surname><given-names>Da</given-names></name><xref ref-type="aff" rid="Aff5">5</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0001-7864-404X</contrib-id><name><surname>Li</surname><given-names>Wei</given-names></name><xref ref-type="aff" rid="Aff6">6</xref></contrib><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0003-2342-3658</contrib-id><name><surname>Li</surname><given-names>Li</given-names></name><address><email>lil@sjtu.edu.cn</email></address><xref ref-type="aff" rid="Aff1">1</xref><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author" corresp="yes"><name><surname>Gao</surname><given-names>Wei-Qiang</given-names></name><address><email>gao.weiqiang@sjtu.edu.cn</email></address><xref ref-type="aff" rid="Aff1">1</xref><xref ref-type="aff" rid="Aff2">2</xref></contrib><aff id="Aff1"><label>1</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0368 8293</institution-id><institution-id institution-id-type="GRID">grid.16821.3c</institution-id><institution>State Key Laboratory of Oncogenes and Related Genes, Renji-Med X Clinical Stem Cell Research Center, Ren Ji Hospital, School of Medicine and School of Biomedical Engineering,</institution><institution>Shanghai Jiao Tong University,</institution></institution-wrap>Shanghai, China</aff><aff id="Aff2"><label>2</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0368 8293</institution-id><institution-id institution-id-type="GRID">grid.16821.3c</institution-id><institution>Med-X Research Institute,</institution><institution>Shanghai Jiao Tong University,</institution></institution-wrap>Shanghai, China</aff><aff id="Aff3"><label>3</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1797 8419</institution-id><institution-id institution-id-type="GRID">grid.410726.6</institution-id><institution>CAS Key Laboratory of Tissue Microenvironment and Tumor, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Nutrition and Health, Shanghai Institutes for Biological Sciences,</institution><institution>University of Chinese Academy of Sciences, Chinese Academy of Sciences,</institution></institution-wrap>Shanghai, China</aff><aff id="Aff4"><label>4</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1808 0942</institution-id><institution-id institution-id-type="GRID">grid.452404.3</institution-id><institution>Department of Colorectal Surgery,</institution><institution>Fudan University Shanghai Cancer Center,</institution></institution-wrap>Shanghai, China</aff><aff id="Aff5"><label>5</label><institution-wrap><institution-id institution-id-type="ISNI">0000000123704535</institution-id><institution-id institution-id-type="GRID">grid.24516.34</institution-id><institution>Central Laboratory for Medical Research, Shanghai Tenth People’s Hospital,</institution><institution>Tongji University School of Medicine,</institution></institution-wrap>Shanghai, China</aff><aff id="Aff6"><label>6</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1792 6416</institution-id><institution-id institution-id-type="GRID">grid.458458.0</institution-id><institution>State Key Laboratory of Stem Cell and Reproductive Biology,</institution><institution>Institute of Zoology, Chinese Academy of Sciences,</institution></institution-wrap>Beijing, China</aff></contrib-group><pub-date pub-type="epub"><day>10</day><month>10</month><year>2019</year></pub-date><pub-date pub-type="pmc-release"><day>10</day><month>10</month><year>2019</year></pub-date><pub-date pub-type="collection"><year>2019</year></pub-date><volume>10</volume><elocation-id>4614</elocation-id><history><date date-type="received"><day>22</day><month>11</month><year>2018</year></date><date date-type="accepted"><day>11</day><month>9</month><year>2019</year></date></history><permissions><copyright-statement>© The Author(s) 2019</copyright-statement><license license-type="OpenAccess"><license-p><bold>Open Access</bold> This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>.</license-p></license></permissions><abstract id="Abs1"><p id="Par1">Autophagy is a central component of integrated stress responses that influences many inflammatory diseases, including inflammatory bowel disease (IBD) and colorectal cancer (CRC). While the core machinery is known, the molecular basis of the epigenetic regulation of autophagy and its role in colon inflammation remain largely undefined. Here, we report that BRG1, an ATPase subunit of the SWI/SNF chromatin remodeling complex, is required for the homeostatic maintenance of intestinal epithelial cells (IECs) to prevent the inflammation and tumorigenesis. BRG1 emerges as a key regulator that directly governs the transcription of <italic>Atg16l1</italic>, <italic>Ambra1</italic>, <italic>Atg7</italic> and <italic>Wipi2</italic>, which are important for autophagosome biogenesis. Defective autophagy in BRG1-deficient IECs results in excess reactive oxygen species (ROS), which leads to the defects in barrier integrity. Together, our results establish that BRG1 may represent an autophagy checkpoint that is pathogenetically linked to colitis and is therefore likely a potential therapeutic target for disease intervention.</p></abstract><abstract id="Abs2" abstract-type="web-summary"><p id="Par2">Dysfunctional autophagy induces inflammation that contributes to tumorigenesis. Here, the authors show that loss of BRG1 impairs autophagy and enhances reactive oxygen species production to disrupt intestinal barrier integrity, leading to spontaneous colitis and subsequent colorectal cancer development.</p></abstract><kwd-group kwd-group-type="npg-subject"><title>Subject terms</title><kwd>Cancer</kwd><kwd>Gastroenterology</kwd></kwd-group><funding-group><award-group><funding-source><institution>Ministry of Science and Technology of the People’s Republic of China (2017YFA0102900 to WQG), National Natural Science Foundation of China (81872406 and 81630073 to WQG, 81772938 to L. Li), State Key Laboratory of Oncogenes and Related Genes (KF01801 to L. Li), Science and Technology Commission of Shanghai Municipality (16JC1405700 to WQG, 18140902700 and 19140905500 to L. Li),</institution></funding-source></award-group></funding-group><custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name><meta-value>© The Author(s) 2019</meta-value></custom-meta></custom-meta-group></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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