IL‐34‐ and M‐CSF‐induced macrophages switch memory T cells into Th17 cells via membrane IL‐1α
Macrophages orchestrate the immune response via the polarization of CD4+ T helper (Th) cells. Different subsets of macrophages with distinct phenotypes, and sometimes opposite functions, have been described. M‐CSF and IL‐34 induce the differentiation of monocytes into IL‐10high IL‐12low immunoregula...
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| Veröffentlicht in: | European journal of immunology 2015-04, Vol.45 (4), p.1092-1102 |
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| creator | Foucher, Etienne D. Blanchard, Simon Preisser, Laurence Descamps, Philippe Ifrah, Norbert Delneste, Yves Jeannin, Pascale |
| description | Macrophages orchestrate the immune response via the polarization of CD4+ T helper (Th) cells. Different subsets of macrophages with distinct phenotypes, and sometimes opposite functions, have been described. M‐CSF and IL‐34 induce the differentiation of monocytes into IL‐10high IL‐12low immunoregulatory macrophages, which are similar to tumor‐associated macrophages (TAMs) in ovarian cancer. In this study, we evaluated the capacity of human macrophages induced in the presence of M‐CSF (M‐CSF macrophages) or IL‐34 (IL‐34 macrophages) and ovarian cancer TAMs to modulate the phenotype of human CD4+ T cells. Taken together, our results show that M‐CSF‐, IL‐34 macrophages, and TAMs switch non‐Th17 committed memory CD4+ T cells into conventional CCR4+ CCR6+ CD161+ Th17 cells, expressing or not IFN‐gamma. Contrary, the pro‐inflammatory GM‐CSF macrophages promote Th1 cells. The polarization of memory T cells into Th17 cells is mediated via membrane IL‐1α (mIL‐1α), which is constitutively expressed by M‐CSF‐, IL‐34 macrophages, and TAMs. This study elucidates a new mechanism that allows macrophages to maintain locally restrained and smoldering inflammation, which is required in angiogenesis and metastasis. |
| doi_str_mv | 10.1002/eji.201444606 |
| format | Article |
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Different subsets of macrophages with distinct phenotypes, and sometimes opposite functions, have been described. M‐CSF and IL‐34 induce the differentiation of monocytes into IL‐10high IL‐12low immunoregulatory macrophages, which are similar to tumor‐associated macrophages (TAMs) in ovarian cancer. In this study, we evaluated the capacity of human macrophages induced in the presence of M‐CSF (M‐CSF macrophages) or IL‐34 (IL‐34 macrophages) and ovarian cancer TAMs to modulate the phenotype of human CD4+ T cells. Taken together, our results show that M‐CSF‐, IL‐34 macrophages, and TAMs switch non‐Th17 committed memory CD4+ T cells into conventional CCR4+ CCR6+ CD161+ Th17 cells, expressing or not IFN‐gamma. Contrary, the pro‐inflammatory GM‐CSF macrophages promote Th1 cells. The polarization of memory T cells into Th17 cells is mediated via membrane IL‐1α (mIL‐1α), which is constitutively expressed by M‐CSF‐, IL‐34 macrophages, and TAMs. This study elucidates a new mechanism that allows macrophages to maintain locally restrained and smoldering inflammation, which is required in angiogenesis and metastasis.</description><identifier>ISSN: 0014-2980</identifier><identifier>EISSN: 1521-4141</identifier><identifier>DOI: 10.1002/eji.201444606</identifier><identifier>PMID: 25545357</identifier><language>eng</language><publisher>Germany: Wiley-VCH Verlag</publisher><subject>Adaptive immunology ; Cell Differentiation - immunology ; Cells, Cultured ; Coculture Techniques ; Dendritic Cells - immunology ; Female ; Granulocyte-Macrophage Colony-Stimulating Factor - pharmacology ; Humans ; IL‐1α ; IL‐34 ; Immunologic Memory - immunology ; Immunology ; Inflammation ; Innate immunity ; Interferon-gamma - biosynthesis ; Interleukin-10 - metabolism ; Interleukin-12 Subunit p35 - metabolism ; Interleukin-17 - biosynthesis ; Interleukin-1alpha - immunology ; Interleukins - immunology ; Interleukins - pharmacology ; Life Sciences ; Macrophage Colony-Stimulating Factor - immunology ; Macrophage Colony-Stimulating Factor - pharmacology ; Macrophages ; Macrophages - immunology ; Monocytes - immunology ; M‐CSF ; NK Cell Lectin-Like Receptor Subfamily B - metabolism ; Ovarian Neoplasms - immunology ; Receptors, CCR4 - metabolism ; Receptors, CCR6 - metabolism ; Th17 cells ; Th17 Cells - cytology ; Th17 Cells - immunology</subject><ispartof>European journal of immunology, 2015-04, Vol.45 (4), p.1092-1102</ispartof><rights>2014 WILEY‐VCH Verlag GmbH & Co. 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Different subsets of macrophages with distinct phenotypes, and sometimes opposite functions, have been described. M‐CSF and IL‐34 induce the differentiation of monocytes into IL‐10high IL‐12low immunoregulatory macrophages, which are similar to tumor‐associated macrophages (TAMs) in ovarian cancer. In this study, we evaluated the capacity of human macrophages induced in the presence of M‐CSF (M‐CSF macrophages) or IL‐34 (IL‐34 macrophages) and ovarian cancer TAMs to modulate the phenotype of human CD4+ T cells. Taken together, our results show that M‐CSF‐, IL‐34 macrophages, and TAMs switch non‐Th17 committed memory CD4+ T cells into conventional CCR4+ CCR6+ CD161+ Th17 cells, expressing or not IFN‐gamma. Contrary, the pro‐inflammatory GM‐CSF macrophages promote Th1 cells. The polarization of memory T cells into Th17 cells is mediated via membrane IL‐1α (mIL‐1α), which is constitutively expressed by M‐CSF‐, IL‐34 macrophages, and TAMs. This study elucidates a new mechanism that allows macrophages to maintain locally restrained and smoldering inflammation, which is required in angiogenesis and metastasis.</description><subject>Adaptive immunology</subject><subject>Cell Differentiation - immunology</subject><subject>Cells, Cultured</subject><subject>Coculture Techniques</subject><subject>Dendritic Cells - immunology</subject><subject>Female</subject><subject>Granulocyte-Macrophage Colony-Stimulating Factor - pharmacology</subject><subject>Humans</subject><subject>IL‐1α</subject><subject>IL‐34</subject><subject>Immunologic Memory - immunology</subject><subject>Immunology</subject><subject>Inflammation</subject><subject>Innate immunity</subject><subject>Interferon-gamma - biosynthesis</subject><subject>Interleukin-10 - metabolism</subject><subject>Interleukin-12 Subunit p35 - metabolism</subject><subject>Interleukin-17 - biosynthesis</subject><subject>Interleukin-1alpha - immunology</subject><subject>Interleukins - immunology</subject><subject>Interleukins - pharmacology</subject><subject>Life Sciences</subject><subject>Macrophage Colony-Stimulating Factor - immunology</subject><subject>Macrophage Colony-Stimulating Factor - pharmacology</subject><subject>Macrophages</subject><subject>Macrophages - immunology</subject><subject>Monocytes - immunology</subject><subject>M‐CSF</subject><subject>NK Cell Lectin-Like Receptor Subfamily B - metabolism</subject><subject>Ovarian Neoplasms - immunology</subject><subject>Receptors, CCR4 - metabolism</subject><subject>Receptors, CCR6 - metabolism</subject><subject>Th17 cells</subject><subject>Th17 Cells - cytology</subject><subject>Th17 Cells - immunology</subject><issn>0014-2980</issn><issn>1521-4141</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkc1O20AQx1eoVQnQY6_VHtuDYWY_vUcUQQkK6qHhvFrba7zIjlNvAsqtj9BX4UV4CJ6EDQk5Vr3Ml376a2b-hHxBOEUAdubvwykDFEIoUAdkhJJhJlDgBzKCNM-YyeGQHMV4DwBGSfOJHDIpheRSj0gzmb78-ctFCtTNK3qTivGvyxTDvFqVvqKdK4d-0bg7H2l8DMuyoZ3v-mFNZ7T0bRtpmC97OmtQ7_qH4DZIMbi5p2_6-Px0Qj7Wro3-8y4fk9vLi9n4Kpv-_DEZn0-zUiKDjDutnahrX6kaCkQtDJYVGFFIlRdGp6TrUukcjZAmz12uCmkwL0Ei1NzxY_J9q9u41i6G0LlhbXsX7NX51G5mgNwwJvABE_ttyy6G_vfKx6XtQtzckBbvV9Gi0orLXBr9PyhTCEqJhGZbNP0txsHX-zUQ7MYzmzyze88S_3UnvSo6X-3pd5MSwLbAY2j9-t9q9uJ6wpkA_gqE7KIZ</recordid><startdate>201504</startdate><enddate>201504</enddate><creator>Foucher, Etienne D.</creator><creator>Blanchard, Simon</creator><creator>Preisser, Laurence</creator><creator>Descamps, Philippe</creator><creator>Ifrah, Norbert</creator><creator>Delneste, Yves</creator><creator>Jeannin, Pascale</creator><general>Wiley-VCH Verlag</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>7X8</scope><scope>7T5</scope><scope>H94</scope><scope>1XC</scope><scope>VOOES</scope><orcidid>https://orcid.org/0000-0002-2142-596X</orcidid><orcidid>https://orcid.org/0000-0002-9788-8581</orcidid><orcidid>https://orcid.org/0000-0002-7953-0455</orcidid></search><sort><creationdate>201504</creationdate><title>IL‐34‐ and M‐CSF‐induced macrophages switch memory T cells into Th17 cells via membrane IL‐1α</title><author>Foucher, Etienne D. ; Blanchard, Simon ; Preisser, Laurence ; Descamps, Philippe ; Ifrah, Norbert ; Delneste, Yves ; Jeannin, Pascale</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5120-3a77a4ffed6f0b117491cd094b568b97b567fc6781945988a86b5918c0510f3a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Adaptive immunology</topic><topic>Cell Differentiation - immunology</topic><topic>Cells, Cultured</topic><topic>Coculture Techniques</topic><topic>Dendritic Cells - immunology</topic><topic>Female</topic><topic>Granulocyte-Macrophage Colony-Stimulating Factor - pharmacology</topic><topic>Humans</topic><topic>IL‐1α</topic><topic>IL‐34</topic><topic>Immunologic Memory - immunology</topic><topic>Immunology</topic><topic>Inflammation</topic><topic>Innate immunity</topic><topic>Interferon-gamma - biosynthesis</topic><topic>Interleukin-10 - metabolism</topic><topic>Interleukin-12 Subunit p35 - metabolism</topic><topic>Interleukin-17 - biosynthesis</topic><topic>Interleukin-1alpha - immunology</topic><topic>Interleukins - immunology</topic><topic>Interleukins - pharmacology</topic><topic>Life Sciences</topic><topic>Macrophage Colony-Stimulating Factor - immunology</topic><topic>Macrophage Colony-Stimulating Factor - pharmacology</topic><topic>Macrophages</topic><topic>Macrophages - immunology</topic><topic>Monocytes - immunology</topic><topic>M‐CSF</topic><topic>NK Cell Lectin-Like Receptor Subfamily B - metabolism</topic><topic>Ovarian Neoplasms - immunology</topic><topic>Receptors, CCR4 - metabolism</topic><topic>Receptors, CCR6 - metabolism</topic><topic>Th17 cells</topic><topic>Th17 Cells - cytology</topic><topic>Th17 Cells - immunology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Foucher, Etienne D.</creatorcontrib><creatorcontrib>Blanchard, Simon</creatorcontrib><creatorcontrib>Preisser, Laurence</creatorcontrib><creatorcontrib>Descamps, Philippe</creatorcontrib><creatorcontrib>Ifrah, Norbert</creatorcontrib><creatorcontrib>Delneste, Yves</creatorcontrib><creatorcontrib>Jeannin, Pascale</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Immunology Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>European journal of immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Foucher, Etienne D.</au><au>Blanchard, Simon</au><au>Preisser, Laurence</au><au>Descamps, Philippe</au><au>Ifrah, Norbert</au><au>Delneste, Yves</au><au>Jeannin, Pascale</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>IL‐34‐ and M‐CSF‐induced macrophages switch memory T cells into Th17 cells via membrane IL‐1α</atitle><jtitle>European journal of immunology</jtitle><addtitle>Eur J Immunol</addtitle><date>2015-04</date><risdate>2015</risdate><volume>45</volume><issue>4</issue><spage>1092</spage><epage>1102</epage><pages>1092-1102</pages><issn>0014-2980</issn><eissn>1521-4141</eissn><abstract>Macrophages orchestrate the immune response via the polarization of CD4+ T helper (Th) cells. Different subsets of macrophages with distinct phenotypes, and sometimes opposite functions, have been described. M‐CSF and IL‐34 induce the differentiation of monocytes into IL‐10high IL‐12low immunoregulatory macrophages, which are similar to tumor‐associated macrophages (TAMs) in ovarian cancer. In this study, we evaluated the capacity of human macrophages induced in the presence of M‐CSF (M‐CSF macrophages) or IL‐34 (IL‐34 macrophages) and ovarian cancer TAMs to modulate the phenotype of human CD4+ T cells. Taken together, our results show that M‐CSF‐, IL‐34 macrophages, and TAMs switch non‐Th17 committed memory CD4+ T cells into conventional CCR4+ CCR6+ CD161+ Th17 cells, expressing or not IFN‐gamma. Contrary, the pro‐inflammatory GM‐CSF macrophages promote Th1 cells. The polarization of memory T cells into Th17 cells is mediated via membrane IL‐1α (mIL‐1α), which is constitutively expressed by M‐CSF‐, IL‐34 macrophages, and TAMs. This study elucidates a new mechanism that allows macrophages to maintain locally restrained and smoldering inflammation, which is required in angiogenesis and metastasis.</abstract><cop>Germany</cop><pub>Wiley-VCH Verlag</pub><pmid>25545357</pmid><doi>10.1002/eji.201444606</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0002-2142-596X</orcidid><orcidid>https://orcid.org/0000-0002-9788-8581</orcidid><orcidid>https://orcid.org/0000-0002-7953-0455</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | European journal of immunology, 2015-04, Vol.45 (4), p.1092-1102 |
| issn | 0014-2980 1521-4141 |
| language | eng |
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| source | MEDLINE; Wiley Online Library Journals Frontfile Complete; Wiley Online Library Free Content; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals |
| subjects | Adaptive immunology Cell Differentiation - immunology Cells, Cultured Coculture Techniques Dendritic Cells - immunology Female Granulocyte-Macrophage Colony-Stimulating Factor - pharmacology Humans IL‐1α IL‐34 Immunologic Memory - immunology Immunology Inflammation Innate immunity Interferon-gamma - biosynthesis Interleukin-10 - metabolism Interleukin-12 Subunit p35 - metabolism Interleukin-17 - biosynthesis Interleukin-1alpha - immunology Interleukins - immunology Interleukins - pharmacology Life Sciences Macrophage Colony-Stimulating Factor - immunology Macrophage Colony-Stimulating Factor - pharmacology Macrophages Macrophages - immunology Monocytes - immunology M‐CSF NK Cell Lectin-Like Receptor Subfamily B - metabolism Ovarian Neoplasms - immunology Receptors, CCR4 - metabolism Receptors, CCR6 - metabolism Th17 cells Th17 Cells - cytology Th17 Cells - immunology |
| title | IL‐34‐ and M‐CSF‐induced macrophages switch memory T cells into Th17 cells via membrane IL‐1α |
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