Brg1 restrains the pro-inflammatory properties of ILC3s and modulates intestinal immunity
Group 3 innate lymphoid cells (ILC3s), a subset of the innate lymphoid cells, are abundantly present in the intestine and are crucial regulators of intestinal inflammation. Brg1 (Brahma-related gene 1), a catalytic subunit of the mammalian SWI-SNF-like chromatin-remodeling BAF complex, regulates the...
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| Veröffentlicht in: | Mucosal immunology 2021-01, Vol.14 (1), p.38-52 |
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| creator | Qi, Xinyi Qiu, Jinxin Chang, Jiali Ji, Yan Yang, Qi Cui, Guoliang Sun, Liming Chai, Qian Qin, Jun Qiu, Ju |
| description | Group 3 innate lymphoid cells (ILC3s), a subset of the innate lymphoid cells, are abundantly present in the intestine and are crucial regulators of intestinal inflammation. Brg1 (Brahma-related gene 1), a catalytic subunit of the mammalian SWI-SNF-like chromatin-remodeling BAF complex, regulates the development and function of various immune cells. Here, by genetic deletion of Brg1 in ILC3s (
Smarca4
ΔILC3
), we prove that Brg1 supports the differentiation of NKp46
+
ILC3s by promoting the T-bet expression in NKp46
−
ILC3s, which facilitates the conversion of NKp46
−
ILC3s to NKp46
+
ILC3s. Strikingly,
Smarca4
ΔILC3
mice of the
Rag1
−/−
background develop spontaneous colitis accompanied with increased GM-CSF production in ILC3s. By construction of a mixed bone marrow chimeric system, we demonstrate that Brg1 enhances T-bet and inhibits GM-CSF expression in ILC3s through a cell-intrinsic manner. Blockade of GM-CSF ameliorates colitis in
Rag1
−/−
Smarca4
ΔILC3
mice, suggesting that the suppression of GM-CSF production from ILC3s by Brg1 serves as a critical mechanism for Brg1 to restrain intestinal inflammation. We have further demonstrated that Brg1 binds to the
Tbx21
and
Csf2
gene locus in ILC3s, and favors the active and repressive histones modifications on gene locus of
Tbx21
and
Csf2
respectively. Our work reveals the essential role of Brg1 in intestinal immunity by regulating ILC3s. |
| doi_str_mv | 10.1038/s41385-020-0317-3 |
| format | Article |
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Smarca4
ΔILC3
), we prove that Brg1 supports the differentiation of NKp46
+
ILC3s by promoting the T-bet expression in NKp46
−
ILC3s, which facilitates the conversion of NKp46
−
ILC3s to NKp46
+
ILC3s. Strikingly,
Smarca4
ΔILC3
mice of the
Rag1
−/−
background develop spontaneous colitis accompanied with increased GM-CSF production in ILC3s. By construction of a mixed bone marrow chimeric system, we demonstrate that Brg1 enhances T-bet and inhibits GM-CSF expression in ILC3s through a cell-intrinsic manner. Blockade of GM-CSF ameliorates colitis in
Rag1
−/−
Smarca4
ΔILC3
mice, suggesting that the suppression of GM-CSF production from ILC3s by Brg1 serves as a critical mechanism for Brg1 to restrain intestinal inflammation. We have further demonstrated that Brg1 binds to the
Tbx21
and
Csf2
gene locus in ILC3s, and favors the active and repressive histones modifications on gene locus of
Tbx21
and
Csf2
respectively. Our work reveals the essential role of Brg1 in intestinal immunity by regulating ILC3s.</description><identifier>ISSN: 1933-0219</identifier><identifier>EISSN: 1935-3456</identifier><identifier>DOI: 10.1038/s41385-020-0317-3</identifier><identifier>PMID: 32612160</identifier><language>eng</language><publisher>New York: Nature Publishing Group US</publisher><subject>Allergology ; Animals ; Antibodies ; Antigens, Ly ; Biomedical and Life Sciences ; Biomedicine ; Bone marrow ; Brahma-related gene ; BRG1 protein ; Chromatin remodeling ; Colitis ; DNA Helicases - genetics ; DNA Helicases - metabolism ; Gastroenterology ; Granulocyte-macrophage colony-stimulating factor ; Histones ; Homeostasis ; Immunity ; Immunity, Innate ; Immunity, Mucosal ; Immunology ; Immunomodulation ; Inflammation ; Inflammatory bowel disease ; Intestinal Mucosa - immunology ; Intestinal Mucosa - metabolism ; Intestinal Mucosa - pathology ; Intestine ; Intestines - immunology ; Lymphocyte Subsets - immunology ; Lymphocyte Subsets - metabolism ; Lymphoid cells ; Mice ; Natural Cytotoxicity Triggering Receptor 1 ; Nuclear Proteins - genetics ; Nuclear Proteins - metabolism ; RAG1 protein ; T-Box Domain Proteins - immunology ; T-Box Domain Proteins - metabolism ; Transcription Factors - genetics ; Transcription Factors - metabolism</subject><ispartof>Mucosal immunology, 2021-01, Vol.14 (1), p.38-52</ispartof><rights>The Author(s) 2020</rights><rights>The Author(s) 2020. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c470t-815687e8ccffe80d74b69b8747f783f73939ddbc69c663f8580f3f0b63bd58693</citedby><cites>FETCH-LOGICAL-c470t-815687e8ccffe80d74b69b8747f783f73939ddbc69c663f8580f3f0b63bd58693</cites><orcidid>0000-0002-1543-5678</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32612160$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Qi, Xinyi</creatorcontrib><creatorcontrib>Qiu, Jinxin</creatorcontrib><creatorcontrib>Chang, Jiali</creatorcontrib><creatorcontrib>Ji, Yan</creatorcontrib><creatorcontrib>Yang, Qi</creatorcontrib><creatorcontrib>Cui, Guoliang</creatorcontrib><creatorcontrib>Sun, Liming</creatorcontrib><creatorcontrib>Chai, Qian</creatorcontrib><creatorcontrib>Qin, Jun</creatorcontrib><creatorcontrib>Qiu, Ju</creatorcontrib><title>Brg1 restrains the pro-inflammatory properties of ILC3s and modulates intestinal immunity</title><title>Mucosal immunology</title><addtitle>Mucosal Immunol</addtitle><addtitle>Mucosal Immunol</addtitle><description>Group 3 innate lymphoid cells (ILC3s), a subset of the innate lymphoid cells, are abundantly present in the intestine and are crucial regulators of intestinal inflammation. Brg1 (Brahma-related gene 1), a catalytic subunit of the mammalian SWI-SNF-like chromatin-remodeling BAF complex, regulates the development and function of various immune cells. Here, by genetic deletion of Brg1 in ILC3s (
Smarca4
ΔILC3
), we prove that Brg1 supports the differentiation of NKp46
+
ILC3s by promoting the T-bet expression in NKp46
−
ILC3s, which facilitates the conversion of NKp46
−
ILC3s to NKp46
+
ILC3s. Strikingly,
Smarca4
ΔILC3
mice of the
Rag1
−/−
background develop spontaneous colitis accompanied with increased GM-CSF production in ILC3s. By construction of a mixed bone marrow chimeric system, we demonstrate that Brg1 enhances T-bet and inhibits GM-CSF expression in ILC3s through a cell-intrinsic manner. Blockade of GM-CSF ameliorates colitis in
Rag1
−/−
Smarca4
ΔILC3
mice, suggesting that the suppression of GM-CSF production from ILC3s by Brg1 serves as a critical mechanism for Brg1 to restrain intestinal inflammation. We have further demonstrated that Brg1 binds to the
Tbx21
and
Csf2
gene locus in ILC3s, and favors the active and repressive histones modifications on gene locus of
Tbx21
and
Csf2
respectively. Our work reveals the essential role of Brg1 in intestinal immunity by regulating ILC3s.</description><subject>Allergology</subject><subject>Animals</subject><subject>Antibodies</subject><subject>Antigens, Ly</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Bone marrow</subject><subject>Brahma-related gene</subject><subject>BRG1 protein</subject><subject>Chromatin remodeling</subject><subject>Colitis</subject><subject>DNA Helicases - genetics</subject><subject>DNA Helicases - metabolism</subject><subject>Gastroenterology</subject><subject>Granulocyte-macrophage colony-stimulating factor</subject><subject>Histones</subject><subject>Homeostasis</subject><subject>Immunity</subject><subject>Immunity, Innate</subject><subject>Immunity, Mucosal</subject><subject>Immunology</subject><subject>Immunomodulation</subject><subject>Inflammation</subject><subject>Inflammatory bowel disease</subject><subject>Intestinal Mucosa - immunology</subject><subject>Intestinal Mucosa - metabolism</subject><subject>Intestinal Mucosa - pathology</subject><subject>Intestine</subject><subject>Intestines - immunology</subject><subject>Lymphocyte Subsets - immunology</subject><subject>Lymphocyte Subsets - metabolism</subject><subject>Lymphoid cells</subject><subject>Mice</subject><subject>Natural Cytotoxicity Triggering Receptor 1</subject><subject>Nuclear Proteins - genetics</subject><subject>Nuclear Proteins - metabolism</subject><subject>RAG1 protein</subject><subject>T-Box Domain Proteins - immunology</subject><subject>T-Box Domain Proteins - metabolism</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><issn>1933-0219</issn><issn>1935-3456</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNp1kUtr3DAUhUVJyav5Ad0UQzbZuL3ytV6bQDo0bWCgm3bRlZBtaaJgS1PJLsy_j6aTpg_oQg_u_e6RDoeQ1xTeUkD5LrcUJauhgRqQihpfkFOqkNXYMn70846lS9UJOcv5AYADMDwmJ9hw2lAOp-Tb-7ShVbJ5TsaHXM33ttqmWPvgRjNNZo5pty9sbZq9zVV01d16hbkyYaimOCyjmUvZh7LPPpix8tO0BD_vXpGXzozZXjyd5-Tr7Ycvq0_1-vPHu9XNuu5bAXMtKeNSWNn3zlkJg2g7rjopWuGERCdQoRqGrueq5xydZBIcOug4dgOTXOE5uT7obpduskNvQ7Ey6m3yk0k7HY3Xf3eCv9eb-EMLoUAwWgSungRS_L4UG3ryubfjaIKNS9ZNS5WgDYOmoJf_oA9xScX1nhIcylK8UPRA9SnmnKx7_gwFvQ9OH4LTJTi9D05jmXnzp4vniV9JFaA5ALm0wsam30__X_URduSkSA</recordid><startdate>20210101</startdate><enddate>20210101</enddate><creator>Qi, Xinyi</creator><creator>Qiu, Jinxin</creator><creator>Chang, Jiali</creator><creator>Ji, Yan</creator><creator>Yang, Qi</creator><creator>Cui, Guoliang</creator><creator>Sun, Liming</creator><creator>Chai, Qian</creator><creator>Qin, Jun</creator><creator>Qiu, Ju</creator><general>Nature Publishing Group US</general><general>Elsevier Limited</general><scope>C6C</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7T5</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-1543-5678</orcidid></search><sort><creationdate>20210101</creationdate><title>Brg1 restrains the pro-inflammatory properties of ILC3s and modulates intestinal immunity</title><author>Qi, Xinyi ; Qiu, Jinxin ; Chang, Jiali ; Ji, Yan ; Yang, Qi ; Cui, Guoliang ; Sun, Liming ; Chai, Qian ; Qin, Jun ; Qiu, Ju</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c470t-815687e8ccffe80d74b69b8747f783f73939ddbc69c663f8580f3f0b63bd58693</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Allergology</topic><topic>Animals</topic><topic>Antibodies</topic><topic>Antigens, Ly</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Bone marrow</topic><topic>Brahma-related gene</topic><topic>BRG1 protein</topic><topic>Chromatin remodeling</topic><topic>Colitis</topic><topic>DNA Helicases - genetics</topic><topic>DNA Helicases - metabolism</topic><topic>Gastroenterology</topic><topic>Granulocyte-macrophage colony-stimulating factor</topic><topic>Histones</topic><topic>Homeostasis</topic><topic>Immunity</topic><topic>Immunity, Innate</topic><topic>Immunity, Mucosal</topic><topic>Immunology</topic><topic>Immunomodulation</topic><topic>Inflammation</topic><topic>Inflammatory bowel disease</topic><topic>Intestinal Mucosa - immunology</topic><topic>Intestinal Mucosa - metabolism</topic><topic>Intestinal Mucosa - pathology</topic><topic>Intestine</topic><topic>Intestines - immunology</topic><topic>Lymphocyte Subsets - immunology</topic><topic>Lymphocyte Subsets - metabolism</topic><topic>Lymphoid cells</topic><topic>Mice</topic><topic>Natural Cytotoxicity Triggering Receptor 1</topic><topic>Nuclear Proteins - genetics</topic><topic>Nuclear Proteins - metabolism</topic><topic>RAG1 protein</topic><topic>T-Box Domain Proteins - immunology</topic><topic>T-Box Domain Proteins - metabolism</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Qi, Xinyi</creatorcontrib><creatorcontrib>Qiu, Jinxin</creatorcontrib><creatorcontrib>Chang, Jiali</creatorcontrib><creatorcontrib>Ji, Yan</creatorcontrib><creatorcontrib>Yang, Qi</creatorcontrib><creatorcontrib>Cui, Guoliang</creatorcontrib><creatorcontrib>Sun, Liming</creatorcontrib><creatorcontrib>Chai, Qian</creatorcontrib><creatorcontrib>Qin, Jun</creatorcontrib><creatorcontrib>Qiu, Ju</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Immunology Abstracts</collection><collection>ProQuest Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biological Sciences</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>Biological Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Mucosal immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Qi, Xinyi</au><au>Qiu, Jinxin</au><au>Chang, Jiali</au><au>Ji, Yan</au><au>Yang, Qi</au><au>Cui, Guoliang</au><au>Sun, Liming</au><au>Chai, Qian</au><au>Qin, Jun</au><au>Qiu, Ju</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Brg1 restrains the pro-inflammatory properties of ILC3s and modulates intestinal immunity</atitle><jtitle>Mucosal immunology</jtitle><stitle>Mucosal Immunol</stitle><addtitle>Mucosal Immunol</addtitle><date>2021-01-01</date><risdate>2021</risdate><volume>14</volume><issue>1</issue><spage>38</spage><epage>52</epage><pages>38-52</pages><issn>1933-0219</issn><eissn>1935-3456</eissn><abstract>Group 3 innate lymphoid cells (ILC3s), a subset of the innate lymphoid cells, are abundantly present in the intestine and are crucial regulators of intestinal inflammation. Brg1 (Brahma-related gene 1), a catalytic subunit of the mammalian SWI-SNF-like chromatin-remodeling BAF complex, regulates the development and function of various immune cells. Here, by genetic deletion of Brg1 in ILC3s (
Smarca4
ΔILC3
), we prove that Brg1 supports the differentiation of NKp46
+
ILC3s by promoting the T-bet expression in NKp46
−
ILC3s, which facilitates the conversion of NKp46
−
ILC3s to NKp46
+
ILC3s. Strikingly,
Smarca4
ΔILC3
mice of the
Rag1
−/−
background develop spontaneous colitis accompanied with increased GM-CSF production in ILC3s. By construction of a mixed bone marrow chimeric system, we demonstrate that Brg1 enhances T-bet and inhibits GM-CSF expression in ILC3s through a cell-intrinsic manner. Blockade of GM-CSF ameliorates colitis in
Rag1
−/−
Smarca4
ΔILC3
mice, suggesting that the suppression of GM-CSF production from ILC3s by Brg1 serves as a critical mechanism for Brg1 to restrain intestinal inflammation. We have further demonstrated that Brg1 binds to the
Tbx21
and
Csf2
gene locus in ILC3s, and favors the active and repressive histones modifications on gene locus of
Tbx21
and
Csf2
respectively. Our work reveals the essential role of Brg1 in intestinal immunity by regulating ILC3s.</abstract><cop>New York</cop><pub>Nature Publishing Group US</pub><pmid>32612160</pmid><doi>10.1038/s41385-020-0317-3</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-1543-5678</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
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| ispartof | Mucosal immunology, 2021-01, Vol.14 (1), p.38-52 |
| issn | 1933-0219 1935-3456 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7790751 |
| source | MEDLINE; Alma/SFX Local Collection; EZB Electronic Journals Library |
| subjects | Allergology Animals Antibodies Antigens, Ly Biomedical and Life Sciences Biomedicine Bone marrow Brahma-related gene BRG1 protein Chromatin remodeling Colitis DNA Helicases - genetics DNA Helicases - metabolism Gastroenterology Granulocyte-macrophage colony-stimulating factor Histones Homeostasis Immunity Immunity, Innate Immunity, Mucosal Immunology Immunomodulation Inflammation Inflammatory bowel disease Intestinal Mucosa - immunology Intestinal Mucosa - metabolism Intestinal Mucosa - pathology Intestine Intestines - immunology Lymphocyte Subsets - immunology Lymphocyte Subsets - metabolism Lymphoid cells Mice Natural Cytotoxicity Triggering Receptor 1 Nuclear Proteins - genetics Nuclear Proteins - metabolism RAG1 protein T-Box Domain Proteins - immunology T-Box Domain Proteins - metabolism Transcription Factors - genetics Transcription Factors - metabolism |
| title | Brg1 restrains the pro-inflammatory properties of ILC3s and modulates intestinal immunity |
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