Intestinal IFN-γ–producing type 1 regulatory T cells coexpress CCR5 and programmed cell death protein 1 and downregulate IL-10 in the inflamed guts of patients with inflammatory bowel disease
IL-10 is an anti-inflammatory cytokine required for intestinal immune homeostasis. It mediates suppression of T-cell responses by type 1 regulatory T (TR1) cells but is also produced by CD25+ regulatory T (Treg) cells. We aimed to identify and characterize human intestinal TR1 cells and to investiga...
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| Veröffentlicht in: | Journal of allergy and clinical immunology Jg. 142; H. 5; S. 1537 - 1547.e8 |
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| Format: | Journal Article |
| Sprache: | Englisch |
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United States
Elsevier Inc
01.11.2018
Elsevier Limited |
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| ISSN: | 0091-6749, 1097-6825, 1097-6825 |
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| Abstract | IL-10 is an anti-inflammatory cytokine required for intestinal immune homeostasis. It mediates suppression of T-cell responses by type 1 regulatory T (TR1) cells but is also produced by CD25+ regulatory T (Treg) cells.
We aimed to identify and characterize human intestinal TR1 cells and to investigate whether they are a relevant cellular source of IL-10 in patients with inflammatory bowel diseases (IBDs).
CD4+ T cells isolated from the intestinal lamina propria of human subjects and mice were analyzed for phenotype, cytokine production, and suppressive capacities. Intracellular IL-10 expression by CD4+ T-cell subsets in the inflamed guts of patients with IBD (Crohn disease or ulcerative colitis) was compared with that in cells from noninflamed control subjects. Finally, the effects of proinflammatory cytokines on T-cell IL-10 expression were analyzed, and IL-1β and IL-23 responsiveness was assessed.
Intestinal TR1 cells could be identified by coexpression of CCR5 and programmed cell death protein 1 (PD-1) in human subjects and mice. CCR5+PD-1+ TR1 cells expressed IFN-γ and efficiently suppressed T-cell proliferation and transfer colitis. Intestinal IFN-γ+ TR1 cells, but not IL-7 receptor–positive TH cells or CD25+ Treg cells, showed lower IL-10 expression in patients with IBDs. TR1 cells were responsive to IL-23, and IFN-γ+ TR1 cells downregulated IL-10 with IL-1β and IL-23. Conversely, CD25+ Treg cells expressed higher levels of IL-1 receptor but showed stable IL-10 expression.
We provide the first ex vivo characterization of human intestinal TR1 cells. Selective downregulation of IL-10 by IFN-γ+ TR1 cells in response to proinflammatory cytokines is likely to drive excessive intestinal inflammation in patients with IBDs.
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| AbstractList | BackgroundIL-10 is an anti-inflammatory cytokine required for intestinal immune homeostasis. It mediates suppression of T-cell responses by type 1 regulatory T (TR1) cells but is also produced by CD25+ regulatory T (Treg) cells.ObjectiveWe aimed to identify and characterize human intestinal TR1 cells and to investigate whether they are a relevant cellular source of IL-10 in patients with inflammatory bowel diseases (IBDs).MethodsCD4+ T cells isolated from the intestinal lamina propria of human subjects and mice were analyzed for phenotype, cytokine production, and suppressive capacities. Intracellular IL-10 expression by CD4+ T-cell subsets in the inflamed guts of patients with IBD (Crohn disease or ulcerative colitis) was compared with that in cells from noninflamed control subjects. Finally, the effects of proinflammatory cytokines on T-cell IL-10 expression were analyzed, and IL-1β and IL-23 responsiveness was assessed.ResultsIntestinal TR1 cells could be identified by coexpression of CCR5 and programmed cell death protein 1 (PD-1) in human subjects and mice. CCR5+PD-1+ TR1 cells expressed IFN-γ and efficiently suppressed T-cell proliferation and transfer colitis. Intestinal IFN-γ+ TR1 cells, but not IL-7 receptor–positive TH cells or CD25+ Treg cells, showed lower IL-10 expression in patients with IBDs. TR1 cells were responsive to IL-23, and IFN-γ+ TR1 cells downregulated IL-10 with IL-1β and IL-23. Conversely, CD25+ Treg cells expressed higher levels of IL-1 receptor but showed stable IL-10 expression.ConclusionsWe provide the first ex vivo characterization of human intestinal TR1 cells. Selective downregulation of IL-10 by IFN-γ+ TR1 cells in response to proinflammatory cytokines is likely to drive excessive intestinal inflammation in patients with IBDs. IL-10 is an anti-inflammatory cytokine required for intestinal immune homeostasis. It mediates suppression of T-cell responses by type 1 regulatory T (TR1) cells but is also produced by CD25+ regulatory T (Treg) cells. We aimed to identify and characterize human intestinal TR1 cells and to investigate whether they are a relevant cellular source of IL-10 in patients with inflammatory bowel diseases (IBDs). CD4+ T cells isolated from the intestinal lamina propria of human subjects and mice were analyzed for phenotype, cytokine production, and suppressive capacities. Intracellular IL-10 expression by CD4+ T-cell subsets in the inflamed guts of patients with IBD (Crohn disease or ulcerative colitis) was compared with that in cells from noninflamed control subjects. Finally, the effects of proinflammatory cytokines on T-cell IL-10 expression were analyzed, and IL-1β and IL-23 responsiveness was assessed. Intestinal TR1 cells could be identified by coexpression of CCR5 and programmed cell death protein 1 (PD-1) in human subjects and mice. CCR5+PD-1+ TR1 cells expressed IFN-γ and efficiently suppressed T-cell proliferation and transfer colitis. Intestinal IFN-γ+ TR1 cells, but not IL-7 receptor–positive TH cells or CD25+ Treg cells, showed lower IL-10 expression in patients with IBDs. TR1 cells were responsive to IL-23, and IFN-γ+ TR1 cells downregulated IL-10 with IL-1β and IL-23. Conversely, CD25+ Treg cells expressed higher levels of IL-1 receptor but showed stable IL-10 expression. We provide the first ex vivo characterization of human intestinal TR1 cells. Selective downregulation of IL-10 by IFN-γ+ TR1 cells in response to proinflammatory cytokines is likely to drive excessive intestinal inflammation in patients with IBDs. [Display omitted] IL-10 is an anti-inflammatory cytokine required for intestinal immune homeostasis. It mediates suppression of T-cell responses by type 1 regulatory T (TR1) cells but is also produced by CD25+ regulatory T (Treg) cells.BACKGROUNDIL-10 is an anti-inflammatory cytokine required for intestinal immune homeostasis. It mediates suppression of T-cell responses by type 1 regulatory T (TR1) cells but is also produced by CD25+ regulatory T (Treg) cells.We aimed to identify and characterize human intestinal TR1 cells and to investigate whether they are a relevant cellular source of IL-10 in patients with inflammatory bowel diseases (IBDs).OBJECTIVEWe aimed to identify and characterize human intestinal TR1 cells and to investigate whether they are a relevant cellular source of IL-10 in patients with inflammatory bowel diseases (IBDs).CD4+ T cells isolated from the intestinal lamina propria of human subjects and mice were analyzed for phenotype, cytokine production, and suppressive capacities. Intracellular IL-10 expression by CD4+ T-cell subsets in the inflamed guts of patients with IBD (Crohn disease or ulcerative colitis) was compared with that in cells from noninflamed control subjects. Finally, the effects of proinflammatory cytokines on T-cell IL-10 expression were analyzed, and IL-1β and IL-23 responsiveness was assessed.METHODSCD4+ T cells isolated from the intestinal lamina propria of human subjects and mice were analyzed for phenotype, cytokine production, and suppressive capacities. Intracellular IL-10 expression by CD4+ T-cell subsets in the inflamed guts of patients with IBD (Crohn disease or ulcerative colitis) was compared with that in cells from noninflamed control subjects. Finally, the effects of proinflammatory cytokines on T-cell IL-10 expression were analyzed, and IL-1β and IL-23 responsiveness was assessed.Intestinal TR1 cells could be identified by coexpression of CCR5 and programmed cell death protein 1 (PD-1) in human subjects and mice. CCR5+PD-1+ TR1 cells expressed IFN-γ and efficiently suppressed T-cell proliferation and transfer colitis. Intestinal IFN-γ+ TR1 cells, but not IL-7 receptor-positive TH cells or CD25+ Treg cells, showed lower IL-10 expression in patients with IBDs. TR1 cells were responsive to IL-23, and IFN-γ+ TR1 cells downregulated IL-10 with IL-1β and IL-23. Conversely, CD25+ Treg cells expressed higher levels of IL-1 receptor but showed stable IL-10 expression.RESULTSIntestinal TR1 cells could be identified by coexpression of CCR5 and programmed cell death protein 1 (PD-1) in human subjects and mice. CCR5+PD-1+ TR1 cells expressed IFN-γ and efficiently suppressed T-cell proliferation and transfer colitis. Intestinal IFN-γ+ TR1 cells, but not IL-7 receptor-positive TH cells or CD25+ Treg cells, showed lower IL-10 expression in patients with IBDs. TR1 cells were responsive to IL-23, and IFN-γ+ TR1 cells downregulated IL-10 with IL-1β and IL-23. Conversely, CD25+ Treg cells expressed higher levels of IL-1 receptor but showed stable IL-10 expression.We provide the first ex vivo characterization of human intestinal TR1 cells. Selective downregulation of IL-10 by IFN-γ+ TR1 cells in response to proinflammatory cytokines is likely to drive excessive intestinal inflammation in patients with IBDs.CONCLUSIONSWe provide the first ex vivo characterization of human intestinal TR1 cells. Selective downregulation of IL-10 by IFN-γ+ TR1 cells in response to proinflammatory cytokines is likely to drive excessive intestinal inflammation in patients with IBDs. IL-10 is an anti-inflammatory cytokine required for intestinal immune homeostasis. It mediates suppression of T-cell responses by type 1 regulatory T (T 1) cells but is also produced by CD25 regulatory T (Treg) cells. We aimed to identify and characterize human intestinal T 1 cells and to investigate whether they are a relevant cellular source of IL-10 in patients with inflammatory bowel diseases (IBDs). CD4 T cells isolated from the intestinal lamina propria of human subjects and mice were analyzed for phenotype, cytokine production, and suppressive capacities. Intracellular IL-10 expression by CD4 T-cell subsets in the inflamed guts of patients with IBD (Crohn disease or ulcerative colitis) was compared with that in cells from noninflamed control subjects. Finally, the effects of proinflammatory cytokines on T-cell IL-10 expression were analyzed, and IL-1β and IL-23 responsiveness was assessed. Intestinal T 1 cells could be identified by coexpression of CCR5 and programmed cell death protein 1 (PD-1) in human subjects and mice. CCR5 PD-1 T 1 cells expressed IFN-γ and efficiently suppressed T-cell proliferation and transfer colitis. Intestinal IFN-γ T 1 cells, but not IL-7 receptor-positive T cells or CD25 Treg cells, showed lower IL-10 expression in patients with IBDs. T 1 cells were responsive to IL-23, and IFN-γ T 1 cells downregulated IL-10 with IL-1β and IL-23. Conversely, CD25 Treg cells expressed higher levels of IL-1 receptor but showed stable IL-10 expression. We provide the first ex vivo characterization of human intestinal T 1 cells. Selective downregulation of IL-10 by IFN-γ T 1 cells in response to proinflammatory cytokines is likely to drive excessive intestinal inflammation in patients with IBDs. |
| Author | Maglie, Stefano Gruarin, Paola Abrignani, Sergio Flavell, Richard A. Moro, Monica Ranzani, Valeria Gagliani, Nicola Alfen, Johanna Sophie Paroni, Moira Iseppon, Andrea Caprioli, Flavio Bosotti, Roberto Crosti, Maria Cristina Geginat, Jens Pagani, Massimiliano Larghi, Paola Vasco, Chiara Maria Frusteri, Cristina Facciotti, Federica Gatti, Stefano |
| Author_xml | – sequence: 1 givenname: Johanna Sophie surname: Alfen fullname: Alfen, Johanna Sophie organization: INGM–National Institute of Molecular Genetics “Romeo ed Enrica Invernizzi” Milan, Milan, Italy – sequence: 2 givenname: Paola surname: Larghi fullname: Larghi, Paola organization: INGM–National Institute of Molecular Genetics “Romeo ed Enrica Invernizzi” Milan, Milan, Italy – sequence: 3 givenname: Federica surname: Facciotti fullname: Facciotti, Federica organization: INGM–National Institute of Molecular Genetics “Romeo ed Enrica Invernizzi” Milan, Milan, Italy – sequence: 4 givenname: Nicola surname: Gagliani fullname: Gagliani, Nicola organization: Department of Medicine & Department of General, Visceral and Thoracic Surgery, University Medical Center Hamburg–Eppendorf, Hamburg, Germany – sequence: 5 givenname: Roberto surname: Bosotti fullname: Bosotti, Roberto organization: INGM–National Institute of Molecular Genetics “Romeo ed Enrica Invernizzi” Milan, Milan, Italy – sequence: 6 givenname: Moira surname: Paroni fullname: Paroni, Moira organization: INGM–National Institute of Molecular Genetics “Romeo ed Enrica Invernizzi” Milan, Milan, Italy – sequence: 7 givenname: Stefano surname: Maglie fullname: Maglie, Stefano organization: INGM–National Institute of Molecular Genetics “Romeo ed Enrica Invernizzi” Milan, Milan, Italy – sequence: 8 givenname: Paola surname: Gruarin fullname: Gruarin, Paola organization: INGM–National Institute of Molecular Genetics “Romeo ed Enrica Invernizzi” Milan, Milan, Italy – sequence: 9 givenname: Chiara Maria surname: Vasco fullname: Vasco, Chiara Maria organization: INGM–National Institute of Molecular Genetics “Romeo ed Enrica Invernizzi” Milan, Milan, Italy – sequence: 10 givenname: Valeria surname: Ranzani fullname: Ranzani, Valeria organization: INGM–National Institute of Molecular Genetics “Romeo ed Enrica Invernizzi” Milan, Milan, Italy – sequence: 11 givenname: Cristina surname: Frusteri fullname: Frusteri, Cristina organization: Unità Operativa di Gastroenterologia ed Endoscopia, Fondazione Ca' Granda Ospedale Maggiore Policlinico, Milan, Italy – sequence: 12 givenname: Andrea surname: Iseppon fullname: Iseppon, Andrea organization: Department of Immunobiology, School of Medicine, Yale University, New Haven, Conn – sequence: 13 givenname: Monica surname: Moro fullname: Moro, Monica organization: INGM–National Institute of Molecular Genetics “Romeo ed Enrica Invernizzi” Milan, Milan, Italy – sequence: 14 givenname: Maria Cristina surname: Crosti fullname: Crosti, Maria Cristina organization: INGM–National Institute of Molecular Genetics “Romeo ed Enrica Invernizzi” Milan, Milan, Italy – sequence: 15 givenname: Stefano surname: Gatti fullname: Gatti, Stefano organization: Centro Ricerche Precliniche, Fondazione Ca' Granda Ospedale Maggiore Policlinico, Milan, Italy – sequence: 16 givenname: Massimiliano surname: Pagani fullname: Pagani, Massimiliano organization: INGM–National Institute of Molecular Genetics “Romeo ed Enrica Invernizzi” Milan, Milan, Italy – sequence: 17 givenname: Flavio surname: Caprioli fullname: Caprioli, Flavio organization: Department of Pathophysiology and Transplantation (DEPT), University of Milan, Milan, Italy – sequence: 18 givenname: Sergio surname: Abrignani fullname: Abrignani, Sergio organization: INGM–National Institute of Molecular Genetics “Romeo ed Enrica Invernizzi” Milan, Milan, Italy – sequence: 19 givenname: Richard A. surname: Flavell fullname: Flavell, Richard A. organization: Department of Immunobiology, School of Medicine, Yale University, New Haven, Conn – sequence: 20 givenname: Jens orcidid: 0000-0003-4813-0384 surname: Geginat fullname: Geginat, Jens email: geginat@ingm.org organization: INGM–National Institute of Molecular Genetics “Romeo ed Enrica Invernizzi” Milan, Milan, Italy |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29369775$$D View this record in MEDLINE/PubMed |
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| Keywords | CD IL-7R LAG3 PMA Treg IBD FACS IL-23 IL-1R IL-10 UC Inflammatory bowel disease regulatory T cells IL-23R STAT TR1 CRC Foxp3 PD-1 DC |
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| Snippet | IL-10 is an anti-inflammatory cytokine required for intestinal immune homeostasis. It mediates suppression of T-cell responses by type 1 regulatory T (TR1)... IL-10 is an anti-inflammatory cytokine required for intestinal immune homeostasis. It mediates suppression of T-cell responses by type 1 regulatory T (T 1)... BackgroundIL-10 is an anti-inflammatory cytokine required for intestinal immune homeostasis. It mediates suppression of T-cell responses by type 1 regulatory T... |
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| SubjectTerms | Apoptosis Biopsy CCR5 protein CD25 antigen CD4 antigen Cell death Cell proliferation Cytokines Disease Flow cytometry Helper cells Homeostasis Human subjects IL-10 IL-1β IL-23 Immunoregulation Inflammatory bowel disease Inflammatory bowel diseases Interleukin 1 Interleukin 1 receptors Interleukin 10 Interleukin 23 Interleukin 7 Intestine Laboratories Lamina propria Lymphocytes Lymphocytes T PD-1 protein Phenotypes regulatory T cells Rodents Ulcerative colitis γ-Interferon |
| Title | Intestinal IFN-γ–producing type 1 regulatory T cells coexpress CCR5 and programmed cell death protein 1 and downregulate IL-10 in the inflamed guts of patients with inflammatory bowel disease |
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