IL-31-IL-31R interactions negatively regulate type 2 inflammation in the lung
Interleukin (IL) 31Ralpha (glycoprotein 130-like monocyte receptor and glycoprotein 130-like receptor) heterodimerizes with oncostatin M receptor beta to bind IL-31, a cytokine expressed preferentially by CD4(+) T helper type 2 (Th2) cells. However, the functions of IL-31-IL-31R signaling in immune...
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| Veröffentlicht in: | The Journal of experimental medicine 2007-03, Vol.204 (3), p.481-487 |
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| creator | Perrigoue, Jacqueline G Li, Ji Zaph, Colby Goldschmidt, Michael Scott, Phillip de Sauvage, Frederic J Pearce, Edward J Ghilardi, Nico Artis, David |
| description | Interleukin (IL) 31Ralpha (glycoprotein 130-like monocyte receptor and glycoprotein 130-like receptor) heterodimerizes with oncostatin M receptor beta to bind IL-31, a cytokine expressed preferentially by CD4(+) T helper type 2 (Th2) cells. However, the functions of IL-31-IL-31R signaling in immune regulation remain unknown. Here, we identify a novel role for IL-31R in limiting type 2 inflammation in the lung. After intravenous injection of Schistosoma mansoni eggs, IL-31Ralpha(-/-) mice developed severe pulmonary inflammation, characterized by an increase in the area of granulomatous inflammation, increased numbers of resistin-like molecule alpha(+) cells, and enhanced collagen deposition compared to WT counterparts. In vitro, macrophages generated from IL-31Ralpha(-/-) mice promoted enhanced ovalbumin-specific CD4(+) T cell proliferation and purified naive CD4(+) T cells from IL-31Ralpha(-/-) mice exhibited enhanced proliferation and expression of Th2 cytokines, identifying a T cell- and macrophage-intrinsic regulatory function for IL-31R signaling. In contrast, the generation of CD4(+) T cell-mediated Th1 responses were normal in IL-31Ralpha(-/-) mice, suggesting that the regulatory role of IL-31R signaling is limited to type 2 responses. Together, these data implicate IL-31R signaling as a novel negative regulatory pathway that specifically limits type 2 inflammation. |
| doi_str_mv | 10.1084/jem.20061791 |
| format | Article |
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However, the functions of IL-31-IL-31R signaling in immune regulation remain unknown. Here, we identify a novel role for IL-31R in limiting type 2 inflammation in the lung. After intravenous injection of Schistosoma mansoni eggs, IL-31Ralpha(-/-) mice developed severe pulmonary inflammation, characterized by an increase in the area of granulomatous inflammation, increased numbers of resistin-like molecule alpha(+) cells, and enhanced collagen deposition compared to WT counterparts. In vitro, macrophages generated from IL-31Ralpha(-/-) mice promoted enhanced ovalbumin-specific CD4(+) T cell proliferation and purified naive CD4(+) T cells from IL-31Ralpha(-/-) mice exhibited enhanced proliferation and expression of Th2 cytokines, identifying a T cell- and macrophage-intrinsic regulatory function for IL-31R signaling. In contrast, the generation of CD4(+) T cell-mediated Th1 responses were normal in IL-31Ralpha(-/-) mice, suggesting that the regulatory role of IL-31R signaling is limited to type 2 responses. Together, these data implicate IL-31R signaling as a novel negative regulatory pathway that specifically limits type 2 inflammation.</description><identifier>ISSN: 0022-1007</identifier><identifier>EISSN: 1540-9538</identifier><identifier>EISSN: 1892-1007</identifier><identifier>DOI: 10.1084/jem.20061791</identifier><identifier>PMID: 17353366</identifier><language>eng</language><publisher>United States: The Rockefeller University Press</publisher><subject>Acute Disease ; Animals ; Brief Definitive Reports ; Cells, Cultured ; Coculture Techniques ; Down-Regulation - genetics ; Down-Regulation - immunology ; Inflammation Mediators - metabolism ; Inflammation Mediators - physiology ; Interleukins - metabolism ; Lung Diseases, Parasitic - immunology ; Lung Diseases, Parasitic - pathology ; Lung Diseases, Parasitic - prevention & control ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Mice, Transgenic ; Receptors, Interleukin - genetics ; Receptors, Interleukin - metabolism ; Receptors, Interleukin - physiology ; Schistosoma mansoni ; Schistosomiasis mansoni - genetics ; Schistosomiasis mansoni - immunology ; Schistosomiasis mansoni - pathology ; Th2 Cells - immunology ; Th2 Cells - pathology</subject><ispartof>The Journal of experimental medicine, 2007-03, Vol.204 (3), p.481-487</ispartof><rights>Copyright © 2007, The Rockefeller University Press</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c479t-8e77c243f4fd767aa41553f0c9984e7180838094215d9e333fc7e8f440c5bd813</citedby><cites>FETCH-LOGICAL-c479t-8e77c243f4fd767aa41553f0c9984e7180838094215d9e333fc7e8f440c5bd813</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/17353366$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Perrigoue, Jacqueline G</creatorcontrib><creatorcontrib>Li, Ji</creatorcontrib><creatorcontrib>Zaph, Colby</creatorcontrib><creatorcontrib>Goldschmidt, Michael</creatorcontrib><creatorcontrib>Scott, Phillip</creatorcontrib><creatorcontrib>de Sauvage, Frederic J</creatorcontrib><creatorcontrib>Pearce, Edward J</creatorcontrib><creatorcontrib>Ghilardi, Nico</creatorcontrib><creatorcontrib>Artis, David</creatorcontrib><title>IL-31-IL-31R interactions negatively regulate type 2 inflammation in the lung</title><title>The Journal of experimental medicine</title><addtitle>J Exp Med</addtitle><description>Interleukin (IL) 31Ralpha (glycoprotein 130-like monocyte receptor and glycoprotein 130-like receptor) heterodimerizes with oncostatin M receptor beta to bind IL-31, a cytokine expressed preferentially by CD4(+) T helper type 2 (Th2) cells. However, the functions of IL-31-IL-31R signaling in immune regulation remain unknown. Here, we identify a novel role for IL-31R in limiting type 2 inflammation in the lung. After intravenous injection of Schistosoma mansoni eggs, IL-31Ralpha(-/-) mice developed severe pulmonary inflammation, characterized by an increase in the area of granulomatous inflammation, increased numbers of resistin-like molecule alpha(+) cells, and enhanced collagen deposition compared to WT counterparts. In vitro, macrophages generated from IL-31Ralpha(-/-) mice promoted enhanced ovalbumin-specific CD4(+) T cell proliferation and purified naive CD4(+) T cells from IL-31Ralpha(-/-) mice exhibited enhanced proliferation and expression of Th2 cytokines, identifying a T cell- and macrophage-intrinsic regulatory function for IL-31R signaling. In contrast, the generation of CD4(+) T cell-mediated Th1 responses were normal in IL-31Ralpha(-/-) mice, suggesting that the regulatory role of IL-31R signaling is limited to type 2 responses. Together, these data implicate IL-31R signaling as a novel negative regulatory pathway that specifically limits type 2 inflammation.</description><subject>Acute Disease</subject><subject>Animals</subject><subject>Brief Definitive Reports</subject><subject>Cells, Cultured</subject><subject>Coculture Techniques</subject><subject>Down-Regulation - genetics</subject><subject>Down-Regulation - immunology</subject><subject>Inflammation Mediators - metabolism</subject><subject>Inflammation Mediators - physiology</subject><subject>Interleukins - metabolism</subject><subject>Lung Diseases, Parasitic - immunology</subject><subject>Lung Diseases, Parasitic - pathology</subject><subject>Lung Diseases, Parasitic - prevention & control</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Knockout</subject><subject>Mice, Transgenic</subject><subject>Receptors, Interleukin - genetics</subject><subject>Receptors, Interleukin - metabolism</subject><subject>Receptors, Interleukin - physiology</subject><subject>Schistosoma mansoni</subject><subject>Schistosomiasis mansoni - genetics</subject><subject>Schistosomiasis mansoni - immunology</subject><subject>Schistosomiasis mansoni - pathology</subject><subject>Th2 Cells - immunology</subject><subject>Th2 Cells - pathology</subject><issn>0022-1007</issn><issn>1540-9538</issn><issn>1892-1007</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2007</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkU1rGzEQhkVpaRy3t57LnnrqOjP6WEmXQAhNYnAohPQsZHnW3rAfzkob8L_POnaT9NTLDMM8vMzwMPYNYYZg5NkDNTMOUKC2-IFNUEnIrRLmI5sAcJ4jgD5hpzE-AKCUqvjMTlALJURRTNjtfJELzF_qXVa1iXofUtW1MWtp7VP1RPUu62k91D5RlnZbyvjIlbVvGr8HxyFLG8rqoV1_YZ9KX0f6euxT9ufq1_3lTb74fT2_vFjkQWqbckNaBy5FKcuVLrT3EpUSJQRrjSSNBowwYCVHtbIkhCiDJlNKCUEtVwbFlJ0fcrfDsqFVoDb1vnbbvmp8v3Odr9y_m7bauHX35DgKbQHGgB_HgL57HCgm11QxUF37lrohOg3cGCXtf0G0BXDk-8SfBzD0XYw9la_XILi9KDeKcn9Fjfj39x-8wUcz4hmgq41P</recordid><startdate>20070319</startdate><enddate>20070319</enddate><creator>Perrigoue, Jacqueline G</creator><creator>Li, Ji</creator><creator>Zaph, Colby</creator><creator>Goldschmidt, Michael</creator><creator>Scott, Phillip</creator><creator>de Sauvage, Frederic J</creator><creator>Pearce, Edward J</creator><creator>Ghilardi, Nico</creator><creator>Artis, David</creator><general>The Rockefeller University Press</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>7T5</scope><scope>H94</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20070319</creationdate><title>IL-31-IL-31R interactions negatively regulate type 2 inflammation in the lung</title><author>Perrigoue, Jacqueline G ; Li, Ji ; Zaph, Colby ; Goldschmidt, Michael ; Scott, Phillip ; de Sauvage, Frederic J ; Pearce, Edward J ; Ghilardi, Nico ; Artis, David</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c479t-8e77c243f4fd767aa41553f0c9984e7180838094215d9e333fc7e8f440c5bd813</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2007</creationdate><topic>Acute Disease</topic><topic>Animals</topic><topic>Brief Definitive Reports</topic><topic>Cells, Cultured</topic><topic>Coculture Techniques</topic><topic>Down-Regulation - genetics</topic><topic>Down-Regulation - immunology</topic><topic>Inflammation Mediators - metabolism</topic><topic>Inflammation Mediators - physiology</topic><topic>Interleukins - metabolism</topic><topic>Lung Diseases, Parasitic - immunology</topic><topic>Lung Diseases, Parasitic - pathology</topic><topic>Lung Diseases, Parasitic - prevention & control</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Knockout</topic><topic>Mice, Transgenic</topic><topic>Receptors, Interleukin - genetics</topic><topic>Receptors, Interleukin - metabolism</topic><topic>Receptors, Interleukin - physiology</topic><topic>Schistosoma mansoni</topic><topic>Schistosomiasis mansoni - genetics</topic><topic>Schistosomiasis mansoni - immunology</topic><topic>Schistosomiasis mansoni - pathology</topic><topic>Th2 Cells - immunology</topic><topic>Th2 Cells - pathology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Perrigoue, Jacqueline G</creatorcontrib><creatorcontrib>Li, Ji</creatorcontrib><creatorcontrib>Zaph, Colby</creatorcontrib><creatorcontrib>Goldschmidt, Michael</creatorcontrib><creatorcontrib>Scott, Phillip</creatorcontrib><creatorcontrib>de Sauvage, Frederic J</creatorcontrib><creatorcontrib>Pearce, Edward J</creatorcontrib><creatorcontrib>Ghilardi, Nico</creatorcontrib><creatorcontrib>Artis, David</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Immunology Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of experimental medicine</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Perrigoue, Jacqueline G</au><au>Li, Ji</au><au>Zaph, Colby</au><au>Goldschmidt, Michael</au><au>Scott, Phillip</au><au>de Sauvage, Frederic J</au><au>Pearce, Edward J</au><au>Ghilardi, Nico</au><au>Artis, David</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>IL-31-IL-31R interactions negatively regulate type 2 inflammation in the lung</atitle><jtitle>The Journal of experimental medicine</jtitle><addtitle>J Exp Med</addtitle><date>2007-03-19</date><risdate>2007</risdate><volume>204</volume><issue>3</issue><spage>481</spage><epage>487</epage><pages>481-487</pages><issn>0022-1007</issn><eissn>1540-9538</eissn><eissn>1892-1007</eissn><abstract>Interleukin (IL) 31Ralpha (glycoprotein 130-like monocyte receptor and glycoprotein 130-like receptor) heterodimerizes with oncostatin M receptor beta to bind IL-31, a cytokine expressed preferentially by CD4(+) T helper type 2 (Th2) cells. However, the functions of IL-31-IL-31R signaling in immune regulation remain unknown. Here, we identify a novel role for IL-31R in limiting type 2 inflammation in the lung. After intravenous injection of Schistosoma mansoni eggs, IL-31Ralpha(-/-) mice developed severe pulmonary inflammation, characterized by an increase in the area of granulomatous inflammation, increased numbers of resistin-like molecule alpha(+) cells, and enhanced collagen deposition compared to WT counterparts. In vitro, macrophages generated from IL-31Ralpha(-/-) mice promoted enhanced ovalbumin-specific CD4(+) T cell proliferation and purified naive CD4(+) T cells from IL-31Ralpha(-/-) mice exhibited enhanced proliferation and expression of Th2 cytokines, identifying a T cell- and macrophage-intrinsic regulatory function for IL-31R signaling. In contrast, the generation of CD4(+) T cell-mediated Th1 responses were normal in IL-31Ralpha(-/-) mice, suggesting that the regulatory role of IL-31R signaling is limited to type 2 responses. Together, these data implicate IL-31R signaling as a novel negative regulatory pathway that specifically limits type 2 inflammation.</abstract><cop>United States</cop><pub>The Rockefeller University Press</pub><pmid>17353366</pmid><doi>10.1084/jem.20061791</doi><tpages>7</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Acute Disease Animals Brief Definitive Reports Cells, Cultured Coculture Techniques Down-Regulation - genetics Down-Regulation - immunology Inflammation Mediators - metabolism Inflammation Mediators - physiology Interleukins - metabolism Lung Diseases, Parasitic - immunology Lung Diseases, Parasitic - pathology Lung Diseases, Parasitic - prevention & control Mice Mice, Inbred C57BL Mice, Knockout Mice, Transgenic Receptors, Interleukin - genetics Receptors, Interleukin - metabolism Receptors, Interleukin - physiology Schistosoma mansoni Schistosomiasis mansoni - genetics Schistosomiasis mansoni - immunology Schistosomiasis mansoni - pathology Th2 Cells - immunology Th2 Cells - pathology |
| title | IL-31-IL-31R interactions negatively regulate type 2 inflammation in the lung |
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