Pathogenic conversion of Foxp3+ T cells into TH17 cells in autoimmune arthritis
Regulatory T (T reg ) cells exhibit substantial phenotypic and functional plasticity. Hiroshi Takayanagi and his colleagues report that in autoimmune arthritis, a subset of T reg cells can lose Foxp3 expression and convert into T H 17 cells. This conversion is mediated by synovial fibroblast-derived...
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| Published in: | Nature medicine Vol. 20; no. 1; pp. 62 - 68 |
|---|---|
| Main Authors: | , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
New York
Nature Publishing Group US
01.01.2014
Nature Publishing Group |
| Subjects: | |
| ISSN: | 1078-8956, 1546-170X, 1546-170X |
| Online Access: | Get full text |
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| Abstract | Regulatory T (T
reg
) cells exhibit substantial phenotypic and functional plasticity. Hiroshi Takayanagi and his colleagues report that in autoimmune arthritis, a subset of T
reg
cells can lose Foxp3 expression and convert into T
H
17 cells. This conversion is mediated by synovial fibroblast-derived IL-6, and
in vivo
, these cells are osteoclastogenic and exacerbate arthritis. These findings suggest that a proportion of pathogenic T
H
17 cells in autoimmune disease may be derived from T
reg
cells.
Autoimmune diseases often result from an imbalance between regulatory T (T
reg
) cells and interleukin-17 (IL-17)-producing T helper (T
H
17) cells; the origin of the latter cells remains largely unknown. Foxp3 is indispensable for the suppressive function of T
reg
cells, but the stability of Foxp3 has been under debate. Here we show that T
H
17 cells originating from Foxp3
+
T cells have a key role in the pathogenesis of autoimmune arthritis. Under arthritic conditions, CD25
lo
Foxp3
+
CD4
+
T cells lose Foxp3 expression (herein called exFoxp3 cells) and undergo transdifferentiation into T
H
17 cells. Fate mapping analysis showed that IL-17–expressing exFoxp3 T (exFoxp3 T
H
17) cells accumulated in inflamed joints. The conversion of Foxp3
+
CD4
+
T cells to T
H
17 cells was mediated by synovial fibroblast-derived IL-6. These exFoxp3 T
H
17 cells were more potent osteoclastogenic T cells than were naive CD4
+
T cell–derived T
H
17 cells. Notably, exFoxp3 T
H
17 cells were characterized by the expression of Sox4, chemokine (C-C motif) receptor 6 (CCR6), chemokine (C-C motif) ligand 20 (CCL20), IL-23 receptor (IL-23R) and receptor activator of NF-κB ligand (RANKL, also called TNFSF11). Adoptive transfer of autoreactive, antigen-experienced CD25
lo
Foxp3
+
CD4
+
T cells into mice followed by secondary immunization with collagen accelerated the onset and increased the severity of arthritis and was associated with the loss of Foxp3 expression in the majority of transferred T cells. We observed IL-17
+
Foxp3
+
T cells in the synovium of subjects with active rheumatoid arthritis (RA), which suggests that plastic Foxp3
+
T cells contribute to the pathogenesis of RA. These findings establish the pathological importance of Foxp3 instability in the generation of pathogenic T
H
17 cells in autoimmunity. |
|---|---|
| AbstractList | Autoimmune diseases often result from an imbalance between regulatory T (Treg) cells and interleukin-17 (IL-17)-producing T helper (TH17) cells; the origin of the latter cells remains largely unknown. Foxp3 is indispensable for the suppressive function of Treg cells, but the stability of Foxp3 has been under debate. Here we show that TH17 cells originating from Foxp3(+) T cells have a key role in the pathogenesis of autoimmune arthritis. Under arthritic conditions, CD25(lo)Foxp3(+)CD4(+) T cells lose Foxp3 expression (herein called exFoxp3 cells) and undergo transdifferentiation into TH17 cells. Fate mapping analysis showed that IL-17-expressing exFoxp3 T (exFoxp3 TH17) cells accumulated in inflamed joints. The conversion of Foxp3(+)CD4(+) T cells to TH17 cells was mediated by synovial fibroblast-derived IL-6. These exFoxp3 TH17 cells were more potent osteoclastogenic T cells than were naive CD4(+) T cell-derived TH17 cells. Notably, exFoxp3 TH17 cells were characterized by the expression of Sox4, chemokine (C-C motif) receptor 6 (CCR6), chemokine (C-C motif) ligand 20 (CCL20), IL-23 receptor (IL-23R) and receptor activator of NF-κB ligand (RANKL, also called TNFSF11). Adoptive transfer of autoreactive, antigen-experienced CD25(lo)Foxp3(+)CD4(+) T cells into mice followed by secondary immunization with collagen accelerated the onset and increased the severity of arthritis and was associated with the loss of Foxp3 expression in the majority of transferred T cells. We observed IL-17(+)Foxp3(+) T cells in the synovium of subjects with active rheumatoid arthritis (RA), which suggests that plastic Foxp3(+) T cells contribute to the pathogenesis of RA. These findings establish the pathological importance of Foxp3 instability in the generation of pathogenic TH17 cells in autoimmunity. Autoimmune diseases often result from an imbalance between regulatory T (Treg) cells and interleukin-17 (IL-17)-producing T helper (TH17) cells; the origin of the latter cells remains largely unknown. Foxp3 is indispensable for the suppressive function of Treg cells, but the stability of Foxp3 has been under debate. Here we show that TH17 cells originating from Foxp3+ T cells have a key role in the pathogenesis of autoimmune arthritis. Under arthritic conditions, CD25loFoxp3+CD4+ T cells lose Foxp3 expression (herein called exFoxp3 cells) and undergo transdifferentiation into TH17 cells. Fate mapping analysis showed that IL-17–expressing exFoxp3 T (exFoxp3 TH17) cells accumulated in inflamed joints. The conversion of Foxp3+CD4+ T cells to TH17 cells was mediated by synovial fibroblast-derived IL-6. These exFoxp3 TH17 cells were more potent osteoclastogenic T cells than were naive CD4+ T cell–derived TH17 cells. Notably, exFoxp3 TH17 cells were characterized by the expression of Sox4, chemokine (C-C motif) receptor 6 (CCR6), chemokine (C-C motif) ligand 20 (CCL20), IL-23 receptor (IL-23R) and receptor activator of NF-κB ligand (RANKL, also called TNFSF11). Adoptive transfer of autoreactive, antigen-experienced CD25loFoxp3+CD4+ T cells into mice followed by secondary immunization with collagen accelerated the onset and increased the severity of arthritis and was associated with the loss of Foxp3 expression in the majority of transferred T cells. We observed IL-17+Foxp3+ T cells in the synovium of subjects with active rheumatoid arthritis (RA), which suggests that plastic Foxp3+ T cells contribute to the pathogenesis of RA. These findings establish the pathological importance of Foxp3 instability in the generation of pathogenic TH17 cells in autoimmunity. Autoimmune diseases often result from an imbalance between regulatory T (Treg) cells and interleukin-17 (IL-17)-producing T helper (TH17) cells; the origin of the latter cells remains largely unknown. Foxp3 is indispensable for the suppressive function of Treg cells, but the stability of Foxp3 has been under debate. Here we show that TH17 cells originating from Foxp3(+) T cells have a key role in the pathogenesis of autoimmune arthritis. Under arthritic conditions, CD25(lo)Foxp3(+)CD4(+) T cells lose Foxp3 expression (herein called exFoxp3 cells) and undergo transdifferentiation into TH17 cells. Fate mapping analysis showed that IL-17-expressing exFoxp3 T (exFoxp3 TH17) cells accumulated in inflamed joints. The conversion of Foxp3(+)CD4(+) T cells to TH17 cells was mediated by synovial fibroblast-derived IL-6. These exFoxp3 TH17 cells were more potent osteoclastogenic T cells than were naive CD4(+) T cell-derived TH17 cells. Notably, exFoxp3 TH17 cells were characterized by the expression of Sox4, chemokine (C-C motif) receptor 6 (CCR6), chemokine (C-C motif) ligand 20 (CCL20), IL-23 receptor (IL-23R) and receptor activator of NF-κB ligand (RANKL, also called TNFSF11). Adoptive transfer of autoreactive, antigen-experienced CD25(lo)Foxp3(+)CD4(+) T cells into mice followed by secondary immunization with collagen accelerated the onset and increased the severity of arthritis and was associated with the loss of Foxp3 expression in the majority of transferred T cells. We observed IL-17(+)Foxp3(+) T cells in the synovium of subjects with active rheumatoid arthritis (RA), which suggests that plastic Foxp3(+) T cells contribute to the pathogenesis of RA. These findings establish the pathological importance of Foxp3 instability in the generation of pathogenic TH17 cells in autoimmunity.Autoimmune diseases often result from an imbalance between regulatory T (Treg) cells and interleukin-17 (IL-17)-producing T helper (TH17) cells; the origin of the latter cells remains largely unknown. Foxp3 is indispensable for the suppressive function of Treg cells, but the stability of Foxp3 has been under debate. Here we show that TH17 cells originating from Foxp3(+) T cells have a key role in the pathogenesis of autoimmune arthritis. Under arthritic conditions, CD25(lo)Foxp3(+)CD4(+) T cells lose Foxp3 expression (herein called exFoxp3 cells) and undergo transdifferentiation into TH17 cells. Fate mapping analysis showed that IL-17-expressing exFoxp3 T (exFoxp3 TH17) cells accumulated in inflamed joints. The conversion of Foxp3(+)CD4(+) T cells to TH17 cells was mediated by synovial fibroblast-derived IL-6. These exFoxp3 TH17 cells were more potent osteoclastogenic T cells than were naive CD4(+) T cell-derived TH17 cells. Notably, exFoxp3 TH17 cells were characterized by the expression of Sox4, chemokine (C-C motif) receptor 6 (CCR6), chemokine (C-C motif) ligand 20 (CCL20), IL-23 receptor (IL-23R) and receptor activator of NF-κB ligand (RANKL, also called TNFSF11). Adoptive transfer of autoreactive, antigen-experienced CD25(lo)Foxp3(+)CD4(+) T cells into mice followed by secondary immunization with collagen accelerated the onset and increased the severity of arthritis and was associated with the loss of Foxp3 expression in the majority of transferred T cells. We observed IL-17(+)Foxp3(+) T cells in the synovium of subjects with active rheumatoid arthritis (RA), which suggests that plastic Foxp3(+) T cells contribute to the pathogenesis of RA. These findings establish the pathological importance of Foxp3 instability in the generation of pathogenic TH17 cells in autoimmunity. Autoimmune diseases often result from an imbalance between regulatory T (Treg) cells and interleukin-17 (IL-17)-producing T helper (TH17) cells; the origin of the latter cells remains largely unknown. Foxp3 is indispensable for the suppressive function of Treg cells, but the stability of Foxp3 has been under debate. Here we show that TH17 cells originating from Foxp3(+) T cells have a key role in the pathogenesis of autoimmune arthritis. Under arthritic conditions, CD25(lo)Foxp3(+)CD4(+) T cells lose Foxp3 expression (herein called exFoxp3 cells) and undergo transdifferentiation into TH17 cells. Fate mapping analysis showed that IL-17-expressing exFoxp3 T (exFoxp3 TH17) cells accumulated in inflamed joints. The conversion of Foxp3(+)CD4(+) T cells to TH17 cells was mediated by synovial fibroblast-derived IL-6. These exFoxp3 TH17 cells were more potent osteoclastogenic T cells than were naive CD4(+) T cell-derived TH17 cells. Notably, exFoxp3 TH17 cells were characterized by the expression of Sox4, chemokine (C-C motif) receptor 6 (CCR6), chemokine (C-C motif) ligand 20 (CCL20), IL-23 receptor (IL-23R) and receptor activator of NF-κB ligand (RANKL, also called TNFSF11). Adoptive transfer of autoreactive, antigen-experienced CD25(lo)Foxp3(+)CD4(+) T cells into mice followed by secondary immunization with collagen accelerated the onset and increased the severity of arthritis and was associated with the loss of Foxp3 expression in the majority of transferred T cells. We observed IL-17(+)Foxp3(+) T cells in the synovium of subjects with active rheumatoid arthritis (RA), which suggests that plastic Foxp3(+) T cells contribute to the pathogenesis of RA. These findings establish the pathological importance of Foxp3 instability in the generation of pathogenic TH17 cells in autoimmunity. [PUBLICATION ABSTRACT] Regulatory T (T reg ) cells exhibit substantial phenotypic and functional plasticity. Hiroshi Takayanagi and his colleagues report that in autoimmune arthritis, a subset of T reg cells can lose Foxp3 expression and convert into T H 17 cells. This conversion is mediated by synovial fibroblast-derived IL-6, and in vivo , these cells are osteoclastogenic and exacerbate arthritis. These findings suggest that a proportion of pathogenic T H 17 cells in autoimmune disease may be derived from T reg cells. Autoimmune diseases often result from an imbalance between regulatory T (T reg ) cells and interleukin-17 (IL-17)-producing T helper (T H 17) cells; the origin of the latter cells remains largely unknown. Foxp3 is indispensable for the suppressive function of T reg cells, but the stability of Foxp3 has been under debate. Here we show that T H 17 cells originating from Foxp3 + T cells have a key role in the pathogenesis of autoimmune arthritis. Under arthritic conditions, CD25 lo Foxp3 + CD4 + T cells lose Foxp3 expression (herein called exFoxp3 cells) and undergo transdifferentiation into T H 17 cells. Fate mapping analysis showed that IL-17–expressing exFoxp3 T (exFoxp3 T H 17) cells accumulated in inflamed joints. The conversion of Foxp3 + CD4 + T cells to T H 17 cells was mediated by synovial fibroblast-derived IL-6. These exFoxp3 T H 17 cells were more potent osteoclastogenic T cells than were naive CD4 + T cell–derived T H 17 cells. Notably, exFoxp3 T H 17 cells were characterized by the expression of Sox4, chemokine (C-C motif) receptor 6 (CCR6), chemokine (C-C motif) ligand 20 (CCL20), IL-23 receptor (IL-23R) and receptor activator of NF-κB ligand (RANKL, also called TNFSF11). Adoptive transfer of autoreactive, antigen-experienced CD25 lo Foxp3 + CD4 + T cells into mice followed by secondary immunization with collagen accelerated the onset and increased the severity of arthritis and was associated with the loss of Foxp3 expression in the majority of transferred T cells. We observed IL-17 + Foxp3 + T cells in the synovium of subjects with active rheumatoid arthritis (RA), which suggests that plastic Foxp3 + T cells contribute to the pathogenesis of RA. These findings establish the pathological importance of Foxp3 instability in the generation of pathogenic T H 17 cells in autoimmunity. |
| Author | Nakashima, Tomoki Takayanagi, Hiroshi Oh-hora, Masatsugu Okamoto, Kazuo Kodama, Tatsuhiko Komatsu, Noriko Tanaka, Sakae Bluestone, Jeffrey A Sawa, Shinichiro |
| Author_xml | – sequence: 1 givenname: Noriko surname: Komatsu fullname: Komatsu, Noriko organization: Department of Immunology, Graduate School of Medicine and Faculty of Medicine, The University of Tokyo, Bunkyo-ku, Japan Science and Technology Agency (JST), Exploratory Research for Advanced Technology (ERATO) Program, Takayanagi Osteonetwork Project, Bunkyo-ku – sequence: 2 givenname: Kazuo surname: Okamoto fullname: Okamoto, Kazuo organization: Department of Immunology, Graduate School of Medicine and Faculty of Medicine, The University of Tokyo, Bunkyo-ku, Japan Science and Technology Agency (JST), Exploratory Research for Advanced Technology (ERATO) Program, Takayanagi Osteonetwork Project, Bunkyo-ku – sequence: 3 givenname: Shinichiro surname: Sawa fullname: Sawa, Shinichiro organization: Department of Immunology, Graduate School of Medicine and Faculty of Medicine, The University of Tokyo, Bunkyo-ku, Japan Science and Technology Agency (JST), Exploratory Research for Advanced Technology (ERATO) Program, Takayanagi Osteonetwork Project, Bunkyo-ku – sequence: 4 givenname: Tomoki surname: Nakashima fullname: Nakashima, Tomoki organization: Japan Science and Technology Agency (JST), Exploratory Research for Advanced Technology (ERATO) Program, Takayanagi Osteonetwork Project, Bunkyo-ku, Department of Cell Signaling, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Bunkyo-ku, JST, Precursory Research for Embryonic Science and Technology Program, Bunkyo-ku – sequence: 5 givenname: Masatsugu surname: Oh-hora fullname: Oh-hora, Masatsugu organization: Department of Cell Signaling, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Bunkyo-ku, JST, Precursory Research for Embryonic Science and Technology Program, Bunkyo-ku, Global Center of Excellence (GCOE) Program, International Research Center for Molecular Science in Tooth and Bone Diseases, Bunkyo-ku – sequence: 6 givenname: Tatsuhiko surname: Kodama fullname: Kodama, Tatsuhiko organization: Laboratory for Systems Biology and Medicine, Research Center for Advanced Science and Technology, The University of Tokyo, Meguro-ku – sequence: 7 givenname: Sakae surname: Tanaka fullname: Tanaka, Sakae organization: Department of Orthopaedic Surgery, Faculty of Medicine, The University of Tokyo – sequence: 8 givenname: Jeffrey A surname: Bluestone fullname: Bluestone, Jeffrey A organization: Diabetes Center, University of California, San Francisco – sequence: 9 givenname: Hiroshi surname: Takayanagi fullname: Takayanagi, Hiroshi email: takayana@m.u-tokyo.ac.jp organization: Department of Immunology, Graduate School of Medicine and Faculty of Medicine, The University of Tokyo, Bunkyo-ku, Japan Science and Technology Agency (JST), Exploratory Research for Advanced Technology (ERATO) Program, Takayanagi Osteonetwork Project, Bunkyo-ku, Centre for Orthopaedic Research, School of Surgery, The University of Western Australia |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24362934$$D View this record in MEDLINE/PubMed |
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| Snippet | Regulatory T (T
reg
) cells exhibit substantial phenotypic and functional plasticity. Hiroshi Takayanagi and his colleagues report that in autoimmune... Autoimmune diseases often result from an imbalance between regulatory T (Treg) cells and interleukin-17 (IL-17)-producing T helper (TH17) cells; the origin of... |
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| SubjectTerms | 631/250/38 Adoptive Transfer Animals Antigens Arthritis Arthritis - immunology Autoimmune diseases Autoimmune Diseases - immunology Biomedical materials Biomedicine Cancer Research CCL20 protein CCR6 protein CD25 antigen CD4 antigen CD4-Positive T-Lymphocytes - cytology CD4-Positive T-Lymphocytes - metabolism Cell Differentiation - immunology Cell fate Chemokines Collagen Conversion Cytokines Fate maps Flow Cytometry Forkhead Transcription Factors - immunology Forkhead Transcription Factors - metabolism Foxp3 protein Gene Knock-In Techniques Helper cells Humans Immunization Infectious Diseases Inflammation Interleukin 17 Interleukin 23 Interleukin 6 Joint diseases Ligands Lymphocytes Lymphocytes T Mapping Metabolic Diseases Mice Mice, Inbred C57BL Molecular Medicine Neurosciences NF-κB protein Oligonucleotide Array Sequence Analysis Pathogenesis Rheumatoid arthritis Synovial Membrane - cytology Synovial Membrane - immunology Synovium T cell receptors Th17 Cells - cytology Th17 Cells - immunology TRANCE protein |
| Title | Pathogenic conversion of Foxp3+ T cells into TH17 cells in autoimmune arthritis |
| URI | https://link.springer.com/article/10.1038/nm.3432 https://www.ncbi.nlm.nih.gov/pubmed/24362934 https://www.proquest.com/docview/1474887624 https://www.proquest.com/docview/2320138124 https://www.proquest.com/docview/1490728887 |
| Volume | 20 |
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