Innate lymphoid cells regulate intestinal epithelial cell glycosylation
Fucosylation of intestinal epithelial cells, catalyzed by fucosyltransferase 2 (Fut2), is a major glycosylation mechanism of host-microbiota symbiosis. Commensal bacteria induce epithelial fucosylation, and epithelial fucose is used as a dietary carbohydrate by many of these bacteria. However, the m...
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| Veröffentlicht in: | Science (American Association for the Advancement of Science) 2014-09, Vol.345 (6202), p.1310-1310 |
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| creator | Goto, Yoshiyuki Obata, Takashi Kunisawa, Jun Sato, Shintaro Ivanov, Ivaylo I. Lamichhane, Aayam Takeyama, Natsumi Kamioka, Mariko Sakamoto, Mitsuo Matsuki, Takahiro Setoyama, Hiromi Imaoka, Akemi Uematsu, Satoshi Akira, Shizuo Domino, Steven E. Kulig, Paulina Becher, Burkhard Renauld, Jean-Christophe Sasakawa, Chihiro Umesaki, Yoshinori Benno, Yoshimi Kiyono, Hiroshi |
| description | Fucosylation of intestinal epithelial cells, catalyzed by fucosyltransferase 2 (Fut2), is a major glycosylation mechanism of host-microbiota symbiosis. Commensal bacteria induce epithelial fucosylation, and epithelial fucose is used as a dietary carbohydrate by many of these bacteria. However, the molecular and cellular mechanisms that regulate the induction of epithelial fucosylation are unknown. Here, we show that type 3 innate lymphoid cells (ILC3) induced intestinal epithelial Fut2 expression and fucosylation in mice. This induction required the cytokines interleukin-22 and lymphotoxin in a commensal bacteria-dependent and -independent manner, respectively. Disruption of intestinal fucosylation led to increased susceptibility to infection by Salmonella typhimurium. Our data reveal a role for ILC3 in shaping the gut microenvironment through the regulation of epithelial glycosylation. |
| doi_str_mv | 10.1126/science.1254009 |
| format | Article |
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Commensal bacteria induce epithelial fucosylation, and epithelial fucose is used as a dietary carbohydrate by many of these bacteria. However, the molecular and cellular mechanisms that regulate the induction of epithelial fucosylation are unknown. Here, we show that type 3 innate lymphoid cells (ILC3) induced intestinal epithelial Fut2 expression and fucosylation in mice. This induction required the cytokines interleukin-22 and lymphotoxin in a commensal bacteria-dependent and -independent manner, respectively. Disruption of intestinal fucosylation led to increased susceptibility to infection by Salmonella typhimurium. Our data reveal a role for ILC3 in shaping the gut microenvironment through the regulation of epithelial glycosylation.</description><identifier>ISSN: 0036-8075</identifier><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.1254009</identifier><identifier>PMID: 25214634</identifier><identifier>CODEN: SCIEAS</identifier><language>eng</language><publisher>United States: American Association for the Advancement of Science</publisher><subject>Animals ; Base Sequence ; Biotechnology ; Carbohydrates ; Cellular biology ; Cytokines ; Digestive system ; Disease Models, Animal ; epithelial cells ; Fucose ; Fucose - metabolism ; Fucosyltransferases - genetics ; Fucosyltransferases - metabolism ; Galactoside 2-alpha-L-fucosyltransferase ; Germ-Free Life ; Glycosylation ; Goblet Cells - enzymology ; Goblet Cells - immunology ; Goblet Cells - microbiology ; Ileum - enzymology ; Ileum - immunology ; Ileum - microbiology ; Immune system ; Immune systems ; Immunity, Innate ; Interleukin-22 ; Interleukins - immunology ; intestinal microorganisms ; intestinal mucosa ; Intestinal Mucosa - enzymology ; Intestinal Mucosa - immunology ; Intestinal Mucosa - microbiology ; Logical Thinking ; Lymphocytes - immunology ; lymphotoxin ; membrane proteins ; Mice ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Mice, Mutant Strains ; Microbiota - immunology ; Microorganisms ; Molecular Sequence Data ; Paneth Cells - enzymology ; Paneth Cells - immunology ; Paneth Cells - microbiology ; Proteins ; RESEARCH ARTICLE SUMMARY ; Salmonella Infections - immunology ; Salmonella Infections - microbiology ; Salmonella typhimurium ; Signal processing</subject><ispartof>Science (American Association for the Advancement of Science), 2014-09, Vol.345 (6202), p.1310-1310</ispartof><rights>Copyright © 2014 American Association for the Advancement of Science</rights><rights>Copyright © 2014, American Association for the Advancement of Science.</rights><rights>Copyright © 2014, American Association for the Advancement of Science</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c691t-4a22420b839dccaf35a9bf448c3df5c0e68957638129a982fe3696368ef0c65e3</citedby><cites>FETCH-LOGICAL-c691t-4a22420b839dccaf35a9bf448c3df5c0e68957638129a982fe3696368ef0c65e3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/24917596$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/24917596$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,776,780,799,881,2871,2872,27901,27902,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25214634$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Goto, Yoshiyuki</creatorcontrib><creatorcontrib>Obata, Takashi</creatorcontrib><creatorcontrib>Kunisawa, Jun</creatorcontrib><creatorcontrib>Sato, Shintaro</creatorcontrib><creatorcontrib>Ivanov, Ivaylo I.</creatorcontrib><creatorcontrib>Lamichhane, Aayam</creatorcontrib><creatorcontrib>Takeyama, Natsumi</creatorcontrib><creatorcontrib>Kamioka, Mariko</creatorcontrib><creatorcontrib>Sakamoto, Mitsuo</creatorcontrib><creatorcontrib>Matsuki, Takahiro</creatorcontrib><creatorcontrib>Setoyama, Hiromi</creatorcontrib><creatorcontrib>Imaoka, Akemi</creatorcontrib><creatorcontrib>Uematsu, Satoshi</creatorcontrib><creatorcontrib>Akira, Shizuo</creatorcontrib><creatorcontrib>Domino, Steven E.</creatorcontrib><creatorcontrib>Kulig, Paulina</creatorcontrib><creatorcontrib>Becher, Burkhard</creatorcontrib><creatorcontrib>Renauld, Jean-Christophe</creatorcontrib><creatorcontrib>Sasakawa, Chihiro</creatorcontrib><creatorcontrib>Umesaki, Yoshinori</creatorcontrib><creatorcontrib>Benno, Yoshimi</creatorcontrib><creatorcontrib>Kiyono, Hiroshi</creatorcontrib><title>Innate lymphoid cells regulate intestinal epithelial cell glycosylation</title><title>Science (American Association for the Advancement of Science)</title><addtitle>Science</addtitle><description>Fucosylation of intestinal epithelial cells, catalyzed by fucosyltransferase 2 (Fut2), is a major glycosylation mechanism of host-microbiota symbiosis. Commensal bacteria induce epithelial fucosylation, and epithelial fucose is used as a dietary carbohydrate by many of these bacteria. However, the molecular and cellular mechanisms that regulate the induction of epithelial fucosylation are unknown. Here, we show that type 3 innate lymphoid cells (ILC3) induced intestinal epithelial Fut2 expression and fucosylation in mice. This induction required the cytokines interleukin-22 and lymphotoxin in a commensal bacteria-dependent and -independent manner, respectively. Disruption of intestinal fucosylation led to increased susceptibility to infection by Salmonella typhimurium. Our data reveal a role for ILC3 in shaping the gut microenvironment through the regulation of epithelial glycosylation.</description><subject>Animals</subject><subject>Base Sequence</subject><subject>Biotechnology</subject><subject>Carbohydrates</subject><subject>Cellular biology</subject><subject>Cytokines</subject><subject>Digestive system</subject><subject>Disease Models, Animal</subject><subject>epithelial cells</subject><subject>Fucose</subject><subject>Fucose - metabolism</subject><subject>Fucosyltransferases - genetics</subject><subject>Fucosyltransferases - metabolism</subject><subject>Galactoside 2-alpha-L-fucosyltransferase</subject><subject>Germ-Free Life</subject><subject>Glycosylation</subject><subject>Goblet Cells - enzymology</subject><subject>Goblet Cells - immunology</subject><subject>Goblet Cells - microbiology</subject><subject>Ileum - enzymology</subject><subject>Ileum - immunology</subject><subject>Ileum - microbiology</subject><subject>Immune system</subject><subject>Immune systems</subject><subject>Immunity, Innate</subject><subject>Interleukin-22</subject><subject>Interleukins - immunology</subject><subject>intestinal microorganisms</subject><subject>intestinal mucosa</subject><subject>Intestinal Mucosa - enzymology</subject><subject>Intestinal Mucosa - immunology</subject><subject>Intestinal Mucosa - microbiology</subject><subject>Logical Thinking</subject><subject>Lymphocytes - immunology</subject><subject>lymphotoxin</subject><subject>membrane proteins</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Mutant Strains</subject><subject>Microbiota - immunology</subject><subject>Microorganisms</subject><subject>Molecular Sequence Data</subject><subject>Paneth Cells - enzymology</subject><subject>Paneth Cells - immunology</subject><subject>Paneth Cells - microbiology</subject><subject>Proteins</subject><subject>RESEARCH ARTICLE SUMMARY</subject><subject>Salmonella Infections - immunology</subject><subject>Salmonella Infections - microbiology</subject><subject>Salmonella typhimurium</subject><subject>Signal processing</subject><issn>0036-8075</issn><issn>1095-9203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkUtPGzEUha2qVQnQdVetRmLDZsBvjzeVEAKKhNRNWVuOcydx5NipPYOUf4-nCfSxYWXL9_O5Oucg9JngC0KovCzOQ3RwQajgGOt3aEawFq2mmL1HM4yZbDusxBE6LmWNKyE0-4iOqKCES8Zn6O4-RjtAE3ab7Sr5ReMghNJkWI5hevdxgDL4aEMDWz-sIPh6naBmGXYulV3FfIqn6ENvQ4FPh_MEPd7e_Lz-3j78uLu_vnpondRkaLmllFM875heOGd7Jqye95x3ji164TDITgslWUeotrqjPTCpJZMd9NhJAewEfdvrbsf5BhYO4pBtMNvsNzbvTLLe_DuJfmWW6clwpXjVrgLnB4Gcfo3Vm9n4MvmxEdJYDK0pMcWJwm-iRGNOmegEeRsVkmjFhOIVPfsPXacx14B_U0JgTti0-3JPuZxKydC_WiTYTNWbQ_XmUH398fXvZF75l64r8GUPrMuQ8p8510SJGvIzI0a0xw</recordid><startdate>20140912</startdate><enddate>20140912</enddate><creator>Goto, Yoshiyuki</creator><creator>Obata, Takashi</creator><creator>Kunisawa, Jun</creator><creator>Sato, Shintaro</creator><creator>Ivanov, Ivaylo I.</creator><creator>Lamichhane, Aayam</creator><creator>Takeyama, Natsumi</creator><creator>Kamioka, Mariko</creator><creator>Sakamoto, Mitsuo</creator><creator>Matsuki, Takahiro</creator><creator>Setoyama, Hiromi</creator><creator>Imaoka, Akemi</creator><creator>Uematsu, Satoshi</creator><creator>Akira, Shizuo</creator><creator>Domino, Steven E.</creator><creator>Kulig, Paulina</creator><creator>Becher, Burkhard</creator><creator>Renauld, Jean-Christophe</creator><creator>Sasakawa, Chihiro</creator><creator>Umesaki, Yoshinori</creator><creator>Benno, Yoshimi</creator><creator>Kiyono, Hiroshi</creator><general>American Association for the Advancement of Science</general><general>The American Association for the Advancement of Science</general><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>7QF</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QQ</scope><scope>7QR</scope><scope>7SC</scope><scope>7SE</scope><scope>7SN</scope><scope>7SP</scope><scope>7SR</scope><scope>7SS</scope><scope>7T7</scope><scope>7TA</scope><scope>7TB</scope><scope>7TK</scope><scope>7TM</scope><scope>7U5</scope><scope>7U9</scope><scope>8BQ</scope><scope>8FD</scope><scope>C1K</scope><scope>F28</scope><scope>FR3</scope><scope>H8D</scope><scope>H8G</scope><scope>H94</scope><scope>JG9</scope><scope>JQ2</scope><scope>K9.</scope><scope>KR7</scope><scope>L7M</scope><scope>L~C</scope><scope>L~D</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope></search><sort><creationdate>20140912</creationdate><title>Innate lymphoid cells regulate intestinal epithelial cell glycosylation</title><author>Goto, Yoshiyuki ; Obata, Takashi ; Kunisawa, Jun ; Sato, Shintaro ; Ivanov, Ivaylo I. ; Lamichhane, Aayam ; Takeyama, Natsumi ; Kamioka, Mariko ; Sakamoto, Mitsuo ; Matsuki, Takahiro ; Setoyama, Hiromi ; Imaoka, Akemi ; Uematsu, Satoshi ; Akira, Shizuo ; Domino, Steven E. ; Kulig, Paulina ; Becher, Burkhard ; Renauld, Jean-Christophe ; Sasakawa, Chihiro ; Umesaki, Yoshinori ; Benno, Yoshimi ; Kiyono, Hiroshi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c691t-4a22420b839dccaf35a9bf448c3df5c0e68957638129a982fe3696368ef0c65e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Animals</topic><topic>Base Sequence</topic><topic>Biotechnology</topic><topic>Carbohydrates</topic><topic>Cellular biology</topic><topic>Cytokines</topic><topic>Digestive system</topic><topic>Disease Models, Animal</topic><topic>epithelial cells</topic><topic>Fucose</topic><topic>Fucose - metabolism</topic><topic>Fucosyltransferases - genetics</topic><topic>Fucosyltransferases - metabolism</topic><topic>Galactoside 2-alpha-L-fucosyltransferase</topic><topic>Germ-Free Life</topic><topic>Glycosylation</topic><topic>Goblet Cells - enzymology</topic><topic>Goblet Cells - immunology</topic><topic>Goblet Cells - microbiology</topic><topic>Ileum - enzymology</topic><topic>Ileum - immunology</topic><topic>Ileum - microbiology</topic><topic>Immune system</topic><topic>Immune systems</topic><topic>Immunity, Innate</topic><topic>Interleukin-22</topic><topic>Interleukins - immunology</topic><topic>intestinal microorganisms</topic><topic>intestinal mucosa</topic><topic>Intestinal Mucosa - enzymology</topic><topic>Intestinal Mucosa - immunology</topic><topic>Intestinal Mucosa - microbiology</topic><topic>Logical Thinking</topic><topic>Lymphocytes - immunology</topic><topic>lymphotoxin</topic><topic>membrane proteins</topic><topic>Mice</topic><topic>Mice, Inbred BALB C</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Mutant Strains</topic><topic>Microbiota - 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Commensal bacteria induce epithelial fucosylation, and epithelial fucose is used as a dietary carbohydrate by many of these bacteria. However, the molecular and cellular mechanisms that regulate the induction of epithelial fucosylation are unknown. Here, we show that type 3 innate lymphoid cells (ILC3) induced intestinal epithelial Fut2 expression and fucosylation in mice. This induction required the cytokines interleukin-22 and lymphotoxin in a commensal bacteria-dependent and -independent manner, respectively. Disruption of intestinal fucosylation led to increased susceptibility to infection by Salmonella typhimurium. Our data reveal a role for ILC3 in shaping the gut microenvironment through the regulation of epithelial glycosylation.</abstract><cop>United States</cop><pub>American Association for the Advancement of Science</pub><pmid>25214634</pmid><doi>10.1126/science.1254009</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0036-8075 |
| ispartof | Science (American Association for the Advancement of Science), 2014-09, Vol.345 (6202), p.1310-1310 |
| issn | 0036-8075 1095-9203 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4774895 |
| source | American Association for the Advancement of Science; Jstor Complete Legacy; MEDLINE |
| subjects | Animals Base Sequence Biotechnology Carbohydrates Cellular biology Cytokines Digestive system Disease Models, Animal epithelial cells Fucose Fucose - metabolism Fucosyltransferases - genetics Fucosyltransferases - metabolism Galactoside 2-alpha-L-fucosyltransferase Germ-Free Life Glycosylation Goblet Cells - enzymology Goblet Cells - immunology Goblet Cells - microbiology Ileum - enzymology Ileum - immunology Ileum - microbiology Immune system Immune systems Immunity, Innate Interleukin-22 Interleukins - immunology intestinal microorganisms intestinal mucosa Intestinal Mucosa - enzymology Intestinal Mucosa - immunology Intestinal Mucosa - microbiology Logical Thinking Lymphocytes - immunology lymphotoxin membrane proteins Mice Mice, Inbred BALB C Mice, Inbred C57BL Mice, Mutant Strains Microbiota - immunology Microorganisms Molecular Sequence Data Paneth Cells - enzymology Paneth Cells - immunology Paneth Cells - microbiology Proteins RESEARCH ARTICLE SUMMARY Salmonella Infections - immunology Salmonella Infections - microbiology Salmonella typhimurium Signal processing |
| title | Innate lymphoid cells regulate intestinal epithelial cell glycosylation |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-31T11%3A53%3A09IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-jstor_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Innate%20lymphoid%20cells%20regulate%20intestinal%20epithelial%20cell%20glycosylation&rft.jtitle=Science%20(American%20Association%20for%20the%20Advancement%20of%20Science)&rft.au=Goto,%20Yoshiyuki&rft.date=2014-09-12&rft.volume=345&rft.issue=6202&rft.spage=1310&rft.epage=1310&rft.pages=1310-1310&rft.issn=0036-8075&rft.eissn=1095-9203&rft.coden=SCIEAS&rft_id=info:doi/10.1126/science.1254009&rft_dat=%3Cjstor_pubme%3E24917596%3C/jstor_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1565504130&rft_id=info:pmid/25214634&rft_jstor_id=24917596&rfr_iscdi=true |