Phosphorylation of FOXP3 controls regulatory T cell function and is inhibited by TNF-α in rheumatoid arthritis
TNF-α suppresses regulatory T (T reg ) cell function, however the mechanism remains unclear. Here Jingwu Z Zhang and colleagues find that in activated T cells, phosphorylation of FOXP3 promotes its transcriptional activity. TNF-α induces protein phosphatase 1 expression, leading to dephosphorylation...
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| Published in | Nature medicine Vol. 19; no. 3; pp. 322 - 328 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York
Nature Publishing Group US
01.03.2013
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | TNF-α suppresses regulatory T (T
reg
) cell function, however the mechanism remains unclear. Here Jingwu Z Zhang and colleagues find that in activated T cells, phosphorylation of FOXP3 promotes its transcriptional activity. TNF-α induces protein phosphatase 1 expression, leading to dephosphorylation of FOXP3 and inhibition of T
reg
cell function. In individuals with rheumatoid arthritis, TNF-α–specific antibody treatment restores T
reg
cell activity and FOXP3 phosphorylation, suggesting that post-translational modifications, including phosphorylation, regulate FOXP3 activity and T
reg
cell–mediated suppression.
Regulatory T (T
reg
) cells suppress autoimmune disease, and impaired T
reg
cell function is associated with rheumatoid arthritis. Here we demonstrate that forkhead box P3 (FOXP3) transcriptional activity and, consequently, T
reg
cell suppressive function are regulated by phosphorylation at Ser418 in the C-terminal DNA-binding domain. In rheumatoid arthritis–derived T
reg
cells, the Ser418 site was specifically dephosphorylated by protein phosphatase 1 (PP1), whose expression and enzymatic activity were induced in the inflamed synovium by tumor necrosis factor α (TNF-α), leading to impaired T
reg
cell function. Moreover, TNF-α–induced T
reg
cell dysfunction correlated with increased numbers of interleukin-17 (IL-17)
+
and interferon-γ (IFN-γ)
+
CD4
+
T cells within the inflamed synovium in rheumatoid arthritis. Treatment with a TNF-α–specific antibody restored T
reg
cell function in subjects with rheumatoid arthritis, which was associated with decreased PP1 expression and increased FOXP3 phosphorylation in T
reg
cells. Thus, TNF-α controls the balance between T
reg
cells and pathogenic T
H
17 and T
H
1 cells in the synovium of individuals with rheumatoid arthritis through FOXP3 dephosphorylation. |
|---|---|
| AbstractList | Regulatory T (Treg) cells suppress autoimmune disease, and impaired Treg cell function is associated with rheumatoid arthritis. Here we demonstrate that forkhead box P3 (FOXP3) transcriptional activity and, consequently, Treg cell suppressive function are regulated by phosphorylation at Ser418 in the C-terminal DNA-binding domain. In rheumatoid arthritis-derived Treg cells, the Ser418 site was specifically dephosphorylated by protein phosphatase 1 (PP1), whose expression and enzymatic activity were induced in the inflamed synovium by tumor necrosis factor α (TNF-α), leading to impaired Treg cell function. Moreover, TNF-α-induced Treg cell dysfunction correlated with increased numbers of interleukin-17 (IL-17)(+) and interferon-γ (IFN-γ)(+)CD4(+) T cells within the inflamed synovium in rheumatoid arthritis. Treatment with a TNF-α-specific antibody restored Treg cell function in subjects with rheumatoid arthritis, which was associated with decreased PP1 expression and increased FOXP3 phosphorylation in Treg cells. Thus, TNF-α controls the balance between Treg cells and pathogenic TH17 and TH1 cells in the synovium of individuals with rheumatoid arthritis through FOXP3 dephosphorylation. Regulatory T ([T.sub.reg]) cells suppress autoimmune disease, and impaired [T.sub.reg] cell function is associated with rheumatoid arthritis. Here we demonstrate that forkhead box P3 (FOXP3) transcriptional activity and, consequently, [T.sub.reg] cell suppressive function are regulated by phosphorylation at Ser418 in the C-terminal DNA-binding domain. In rheumatoid arthritis-derived [T.sub.reg] cells, the Ser418 site was specifically dephosphorylated by protein phosphatase 1 (PP1), whose expression and enzymatic activity were induced in the inflamed synovium by tumor necrosis factor α (TNF-α), leading to impaired [T.sub.reg] cell function. Moreover, TNF-α-induced [T.sub.reg] cell dysfunction correlated with increased numbers of interleukin-17 [(IL-17).sup.+] and interferon-γ [(IFN-γ).sup.+][CD4.sup.+] T cells within the inflamed synovium in rheumatoid arthritis. Treatment with a TNF-α-specific antibody restored [T.sub.reg] cell function in subjects with rheumatoid arthritis, which was associated with decreased PP1 expression and increased FOXP3 phosphorylation in [T.sub.reg] cells. Thus, TNF-α controls the balance between [T.sub.reg] cells and pathogenic [T.sub.H]17 and [T.sub.H]1 cells in the synovium of individuals with rheumatoid arthritis through FOXP3 dephosphorylation. Regulatory T (T sub(reg)) cells suppress autoimmune disease, and impaired T sub(reg) cell function is associated with rheumatoid arthritis. Here we demonstrate that forkhead box P3 (FOXP3) transcriptional activity and, consequently, T sub(reg) cell suppressive function are regulated by phosphorylation at Ser418 in the C-terminal DNA-binding domain. In rheumatoid arthritis-derived T sub(reg) cells, the Ser418 site was specifically dephosphorylated by protein phosphatase 1 (PP1), whose expression and enzymatic activity were induced in the inflamed synovium by tumor necrosis factor alpha (TNF- alpha ), leading to impaired T sub(reg) cell function. Moreover, TNF- alpha -induced T sub(reg) cell dysfunction correlated with increased numbers of interleukin-17 (IL-17) super(+) and interferon- gamma (IFN- gamma ) super(+)CD4 super(+) T cells within the inflamed synovium in rheumatoid arthritis. Treatment with a TNF- alpha -specific antibody restored T sub(reg) cell function in subjects with rheumatoid arthritis, which was associated with decreased PP1 expression and increased FOXP3 phosphorylation in T sub(reg) cells. Thus, TNF- alpha controls the balance between T sub(reg) cells and pathogenic T sub(H)17 and T sub(H)1 cells in the synovium of individuals with rheumatoid arthritis through FOXP3 dephosphorylation. Regulatory T (Treg) cells suppress autoimmune disease, and impaired Treg cell function is associated with rheumatoid arthritis. Here we demonstrate that forkhead box P3 (FOXP3) transcriptional activity and, consequently, Treg cell suppressive function are regulated by phosphorylation at Ser418 in the C-terminal DNA-binding domain. In rheumatoid arthritis-derived Treg cells, the Ser418 site was specifically dephosphorylated by protein phosphatase 1 (PP1), whose expression and enzymatic activity were induced in the inflamed synovium by tumor necrosis factor α (TNF-α), leading to impaired Treg cell function. Moreover, TNF-α-induced Treg cell dysfunction correlated with increased numbers of interleukin-17 (IL-17)(+) and interferon-γ (IFN-γ)(+)CD4(+) T cells within the inflamed synovium in rheumatoid arthritis. Treatment with a TNF-α-specific antibody restored Treg cell function in subjects with rheumatoid arthritis, which was associated with decreased PP1 expression and increased FOXP3 phosphorylation in Treg cells. Thus, TNF-α controls the balance between Treg cells and pathogenic TH17 and TH1 cells in the synovium of individuals with rheumatoid arthritis through FOXP3 dephosphorylation.Regulatory T (Treg) cells suppress autoimmune disease, and impaired Treg cell function is associated with rheumatoid arthritis. Here we demonstrate that forkhead box P3 (FOXP3) transcriptional activity and, consequently, Treg cell suppressive function are regulated by phosphorylation at Ser418 in the C-terminal DNA-binding domain. In rheumatoid arthritis-derived Treg cells, the Ser418 site was specifically dephosphorylated by protein phosphatase 1 (PP1), whose expression and enzymatic activity were induced in the inflamed synovium by tumor necrosis factor α (TNF-α), leading to impaired Treg cell function. Moreover, TNF-α-induced Treg cell dysfunction correlated with increased numbers of interleukin-17 (IL-17)(+) and interferon-γ (IFN-γ)(+)CD4(+) T cells within the inflamed synovium in rheumatoid arthritis. Treatment with a TNF-α-specific antibody restored Treg cell function in subjects with rheumatoid arthritis, which was associated with decreased PP1 expression and increased FOXP3 phosphorylation in Treg cells. Thus, TNF-α controls the balance between Treg cells and pathogenic TH17 and TH1 cells in the synovium of individuals with rheumatoid arthritis through FOXP3 dephosphorylation. TNF-α suppresses regulatory T (T reg ) cell function, however the mechanism remains unclear. Here Jingwu Z Zhang and colleagues find that in activated T cells, phosphorylation of FOXP3 promotes its transcriptional activity. TNF-α induces protein phosphatase 1 expression, leading to dephosphorylation of FOXP3 and inhibition of T reg cell function. In individuals with rheumatoid arthritis, TNF-α–specific antibody treatment restores T reg cell activity and FOXP3 phosphorylation, suggesting that post-translational modifications, including phosphorylation, regulate FOXP3 activity and T reg cell–mediated suppression. Regulatory T (T reg ) cells suppress autoimmune disease, and impaired T reg cell function is associated with rheumatoid arthritis. Here we demonstrate that forkhead box P3 (FOXP3) transcriptional activity and, consequently, T reg cell suppressive function are regulated by phosphorylation at Ser418 in the C-terminal DNA-binding domain. In rheumatoid arthritis–derived T reg cells, the Ser418 site was specifically dephosphorylated by protein phosphatase 1 (PP1), whose expression and enzymatic activity were induced in the inflamed synovium by tumor necrosis factor α (TNF-α), leading to impaired T reg cell function. Moreover, TNF-α–induced T reg cell dysfunction correlated with increased numbers of interleukin-17 (IL-17) + and interferon-γ (IFN-γ) + CD4 + T cells within the inflamed synovium in rheumatoid arthritis. Treatment with a TNF-α–specific antibody restored T reg cell function in subjects with rheumatoid arthritis, which was associated with decreased PP1 expression and increased FOXP3 phosphorylation in T reg cells. Thus, TNF-α controls the balance between T reg cells and pathogenic T H 17 and T H 1 cells in the synovium of individuals with rheumatoid arthritis through FOXP3 dephosphorylation. |
| Audience | Academic |
| Author | Wan, Bing Chen, Xi Li, Runsheng Xiao, Lianbo Zhang, Jingwu Z Guo, Taylor B He, Dongyi Zheng, Yingxia Nie, Hong Liu, Xuebin Fang, Lei Chin, Y Eugene |
| Author_xml | – sequence: 1 givenname: Hong surname: Nie fullname: Nie, Hong organization: Shanghai Institute of Immunology, Shanghai Jiao Tong University School of Medicine – sequence: 2 givenname: Yingxia surname: Zheng fullname: Zheng, Yingxia organization: Shanghai Institute of Immunology, Shanghai Jiao Tong University School of Medicine – sequence: 3 givenname: Runsheng surname: Li fullname: Li, Runsheng organization: Institute of Health Sciences, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences – sequence: 4 givenname: Taylor B surname: Guo fullname: Guo, Taylor B organization: Institute of Health Sciences, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences – sequence: 5 givenname: Dongyi surname: He fullname: He, Dongyi organization: Department of Medicine, Guanghua Rheumatology Hospital – sequence: 6 givenname: Lei surname: Fang fullname: Fang, Lei organization: Institute of Health Sciences, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences – sequence: 7 givenname: Xuebin surname: Liu fullname: Liu, Xuebin organization: GlaxoSmithKline Research and Development Center, Zhangjiang Hi-Tech Park, Pudong, Shanghai, China – sequence: 8 givenname: Lianbo surname: Xiao fullname: Xiao, Lianbo organization: Department of Surgery, Guanghua Rheumatology Hospital – sequence: 9 givenname: Xi surname: Chen fullname: Chen, Xi organization: Institute of Health Sciences, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences – sequence: 10 givenname: Bing surname: Wan fullname: Wan, Bing organization: Institute of Health Sciences, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences – sequence: 11 givenname: Y Eugene surname: Chin fullname: Chin, Y Eugene organization: Institute of Health Sciences, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences, Department of Surgery, Brown University School of Medicine-Rhode Island Hospital – sequence: 12 givenname: Jingwu Z surname: Zhang fullname: Zhang, Jingwu Z email: jingwu.z.zang@gsk.com organization: Shanghai Institute of Immunology, Shanghai Jiao Tong University School of Medicine, Institute of Health Sciences, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences, Present address: GlaxoSmithKline Research and Development Center, Zhangjiang Hi-Tech Park, Pudong, Shanghai, China |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23396208$$D View this record in MEDLINE/PubMed |
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| Snippet | TNF-α suppresses regulatory T (T
reg
) cell function, however the mechanism remains unclear. Here Jingwu Z Zhang and colleagues find that in activated T cells,... Regulatory T (Treg) cells suppress autoimmune disease, and impaired Treg cell function is associated with rheumatoid arthritis. Here we demonstrate that... Regulatory T ([T.sub.reg]) cells suppress autoimmune disease, and impaired [T.sub.reg] cell function is associated with rheumatoid arthritis. Here we... Regulatory T (T sub(reg)) cells suppress autoimmune disease, and impaired T sub(reg) cell function is associated with rheumatoid arthritis. Here we demonstrate... |
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| SubjectTerms | 631/250/127/1220 631/250/1619/554/1898/1271 631/250/249/1313/498 631/250/516 Arthritis, Rheumatoid - immunology Arthritis, Rheumatoid - metabolism Biomedicine Cancer Research Cells, Cultured DNA-Binding Proteins - metabolism Forkhead Transcription Factors - chemistry Forkhead Transcription Factors - metabolism Genetic aspects Health aspects Humans Infectious Diseases Interferon-gamma - biosynthesis Interleukin-17 - biosynthesis Interleukin-2 Receptor alpha Subunit - biosynthesis Interleukin-7 Receptor alpha Subunit - biosynthesis Metabolic Diseases Molecular Medicine Neurosciences Phosphorylation Physiological aspects Protein Phosphatase 1 - metabolism Rheumatoid arthritis Risk factors RNA Interference RNA, Small Interfering Synovial Membrane - immunology Synovial Membrane - metabolism T cells T-Lymphocytes, Regulatory - immunology T-Lymphocytes, Regulatory - metabolism Th1 Cells - immunology Th1 Cells - metabolism Th17 Cells - immunology Th17 Cells - metabolism Tumor necrosis factor Tumor Necrosis Factor-alpha - immunology Tumor Necrosis Factor-alpha - metabolism |
| Title | Phosphorylation of FOXP3 controls regulatory T cell function and is inhibited by TNF-α in rheumatoid arthritis |
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