Negative regulation of cytokine signaling in immunity

Cold Spring Harbor Perspectives in Biology

Volumn 10, Issue 7, 2018, Pages

  Yoshimura, Akihiko ^a   Ito, Minako ^a   Chikuma, Shunsuke ^a   Akanuma, Takashi ^a   Nakatsukasa, Hiroko ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE;

ANIMAL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; CYTOKINES; GENE EXPRESSION REGULATION; HUMANS; SIGNAL TRANSDUCTION;

EID: 85045874920     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a028571     Document Type: Article

References (116)

1. Ahmed CM, Larkin J IIII, Johnson HM. 2015. SOCS1 mimetics and antagonists: A complementary approach to positive and negative regulation of immune function. Front Immunol 6: 183.
2. Al Muftah WA, Al-Shafai M, Zaghlool SB, Visconti A, Tsai PC, Kumar P, Spector T, Bell J, Falchi M, Suhre K. 2016. Epigenetic associations of type 2 diabetes and BMI in an Arab population. Clin Epigenetics 8: 13.
3. Aman MJ, Migone TS, Sasaki A, Ascherman DP, Zhu M, Soldaini E, Imada K, Miyajima A, Yoshimura A, Leonard WJ. 1999. CIS associates with the interleukin-2 receptor β chain and inhibits interleukin-2-dependent signaling. J Biol Chem 274: 30266–30272.
4. Asselbergs FW, Guo YR, van Iperen EPA, Sivapalaratnam S, Tragante V, Lanktree MB, Lange LA, Almoguera B, Appel-man YE, Barnard J, et al. 2012. Large-scale gene-centric meta-analysis across 32 studies identifies multiple lipid loci. Am J Hum Genet 91: 823–838.
5. Babon JJ, Kershaw NJ, Murphy JM, Varghese LN, Laktyushin A, Young SN, Lucet IS, Norton RS, Nicola NA. 2012. Suppression of cytokine signaling by SOCS3: Characterization of the mode of inhibition and the basis of its specificity. Immunity 36: 239–250.
6. Bettelli E, Korn T, Kuchroo VK. 2007. Th17: The third member of the effector T cell trilogy. Curr Opin Immunol 19: 652–657.
7. Bouamar H, Jiang DF, Wang L, Lin AP, Ortega M, Aguiar RCT. 2015. MicroRNA 155 control of p53 activity is context dependent and mediated by Aicda and Socs1. Mol Cell Biol 35: 1329–1340.
8. Bourdonnay E, Zaslona Z, Penke LRK, Speth JM, Schneider DJ, Przybranowski S, Swanson JA, Mancuso P, Freeman CM, Curtis JL, et al. 2015. Transcellular delivery of vesic-ular SOCS proteins from macrophages to epithelial cells blunts inflammatory signaling. J Exp Med 212: 729–742.
9. + T cells. Nat Immunol 6: 715–721.
10. Chambers JC, Loh M, Lehne B, Drong A, Kriebel J, Motta V, Wahl S, Elliott HR, Rota F, Scott WR, et al. 2015. Epige-nome-wide association of DNA methylation markers in peripheral blood from Indian Asians and Europeans with incident type 2 diabetes: A nested case-control study. Lancet Diabetes Endo 3: 526–534.
11. Chang JH, Xiao YC, Hu HB, Jin J, Yu JY, Zhou XF, Wu XF, Johnson HM, Akira SZ, Pasparakis M, et al. 2012. Ubc13 maintains the suppressive function of regulatory T cells and prevents their conversion into effector-like T cells. Nat Immunol 13: 481–U484.
12. Chen S, Anderson PO, Li L, Sjogren HO, Wang P, Li SL. 2003. Functional association of cytokine-induced SH2 protein and protein kinase C in activated T cells. Int Immunol 15: 403–409.
13. Chen Z, Laurence A, Kanno Y, Pacher-Zavisin M, Zhu BM, Tato C, Yoshimura A, Hennighausen L, O’Shea JJ. 2006. Selective regulatory function of Socs3 in the formation of IL-17-secreting T cells. Proc Natl Acad Sci 103: 8137– 8142.
14. Chen SQ, Wang L, Fan J, Ye C, Dominguez D, Zhang Y, Curiel TJ, Fang DY, Kuzel TM, Zhang B. 2015. Host miR155 promotes tumor growth through a myeloid-de-rived suppressor cell-dependent mechanism. Cancer Res 75: 519–531.
15. Chikuma S, Kanamori M, Mise-Omata S, Yoshimura A. 2017. Suppressors of cytokine signaling: Potential immune checkpoint molecules for cancerimmunotherapy. Cancer Sci 108: 574–580.
16. Choi YB, Son M, Park M, Shin J, Yun Y. 2010. SOCS-6 negatively regulates T cell activation through targeting p56(lck) to proteasomal degradation. J Biol Chem 285: 7271–7280.
17. de Lapuente AL, Pinto-Medel MJ, Astobiza I, Alloza I, Comabella M, Malhotra S, Montalban X, Zettl UK, Rodriguez-Antiguedad A, Fernandez O, et al. 2015. Cell-specific effects in different immune subsets associated with SOCS1 genotypes in multiple sclerosis. Mult Scler 21: 1498–1512.
18. Delconte RB, Kolesnik TB, Dagley LF, Rautela J, Shi W, Putz EM, Stannard K, Zhang JG, Teh C, Firth M, et al. 2016. CIS is a potent checkpoint in NK cell-mediated tumor immunity. Nat Immunol 17: 816.
19. Disanto G, Sandve GK, Ricigliano VAG, Pakpoor J, Ber-langa-Taylor AJ, Handel AE, Kuhle J, Holden L, Watson CT, Giovannoni G, et al. 2014. DNase hypersensitive sites and association with multiple sclerosis. Hum Mol Genet 23: 942–948.
20. Dong M, Li JX, Tang RQ, Zhu P, Qiu F, Wang C, Qiu J, Wang L, Dai YP, Xu P, et al. 2015. Multiple genetic variants associated with primary biliary cirrhosis in a Han Chinese population. Clin Rev Allerg Immunol 48: 316–321.
21. Dubois PCA, Trynka G, Franke L, Hunt KA, Romanos J, Curtotti A, Zhernakova A, Heap GAR, Adany R, Aromaa A, et al. 2010. Multiple common variants for celiac disease influencing immune gene expression. Nat Genet 42: 295–302.
22. + T cell responses to virus infection and cancer. Immunity 38: 742–753.
23. Ellinghaus D, Ellinghaus E, Nair RP, Stuart PE, Esko T, Met-spalu A, Debrus S, Raelson JV, Tejasvi T, Belouchi M, et al. 2012. Combined analysis of genome-wide association studies for Crohn disease and psoriasis identifies seven shared susceptibility loci. Am J Hum Genet 90: 636–647.
24. Endo TA, Masuhara M, Yokouchi M, Suzuki R, Sakamoto H, Mitsui K, Matsumoto A, Tanimura S, Ohtsubo M, Misawa H, et al. 1997. A new protein containing an SH2 domain that inhibits JAK kinases. Nature 387: 921–924.
25. Endo T, Sasaki A, Minoguchi M, Joo A, Yoshimura A. 2003. CIS1 interacts with the Y532 of the prolactin receptor and suppresses prolactin-dependent STAT5 activation. J Biochem 133: 109–113.
26. Feng Y, Arvey A, Chinen T, van der Veeken J, Gasteiger G, Rudensky AY. 2014. Control of the inheritance of regulatory T cell identity by a cis element in the Foxp3 locus. Cell 158: 749–763.
27. + T lymphocytes. Cell Signal 19: 806–816.
28. Greenhalgh CJ, Metcalf D, Thaus AL, Corbin JE, Uren R, Morgan PO, Fabri LJ, Zhang JG, Martin HM, Willson TA, et al. 2002. Biological evidence that SOCS-2 can act either as an enhancer or suppressor of growth hormone signaling. J Biol Chem 277: 40181–40184.
29. Grigoryev DN, Cheranova DI, Chaudhary S, Heruth DP, Zhang LQ, Ye SQ. 2015. Identification of new biomarkers for acute respiratory distress syndrome by expression-based genome-wide association study. BMC Pulm Med 15: 95.
30. Gui Y, Yeganeh M, Donates YC, Tobelaim WS, Chababi W, Mayhue M, Yoshimura A, Ramanathan S, Saucier C, Ilangumaran S. 2015. Regulation of MET receptor tyrosine kinase signaling by suppressor of cytokine signaling 1 in hepatocellular carcinoma. Oncogene 34: 5718–5728.
31. Guschin D, Rogers N, Briscoe J, Witthuhn B, Watling D, Horn F, Pellegrini S, Yasukawa K, Heinrich P, Stark GR, et al. 1995. A major role for the protein tyrosine kinase JAK1 in the JAK/STAT signal transduction pathway in response to interleukin-6. EMBO J 14: 1421–1429.
32. Hanada T, Yoshida T, Kinjyo I, Minoguchi S, Yasukawa H, Kato S, Mimata H, Nomura Y, Seki Y, Kubo M, et al. 2001. A mutant form of JAB/SOCS1 augments the cytokine-induced JAK/STAT pathway by accelerating degradation of wild-type JAB/CIS family proteins through the SOCS-box. J Biol Chem 276: 40746–40754.
33. Hanada T, Tanaka K, Matsumura Y, Yamauchi M, Nishina-kamura H, Aburatani H, Mashima R, Kubo M, Kobayashi T, Yoshimura A. 2005. Induction of hyper Th1 cell-type immune responses by dendritic cells lacking the suppressor of cytokine signaling-1 gene. J Immunol 174: 4325– 4332.
34. Hanada T, Kobayashi T, Chinen T, Saeki K, Takaki H, Koga K, Minoda Y, Sanada T, Yoshioka T, Mimata H, et al. 2006. IFNγ-dependent, spontaneous development of colorectal carcinomas in SOCS1-deficient mice. J Exp Med 203: 1391–1397.
35. Hao K, Bosse Y, Nickle DC, Pare PD, Postma DS, Laviolette M, Sandford A, Hackett TL, Daley D, Hogg JC, et al. 2012. Lung eQTLs to help reveal the molecular underpinnings of asthma. PloS Genet 8: e1003029.
36. Hashimoto M, Ayada T, Kinjyo I, Hiwatashi K, Yoshida H, Okada Y, Kobayashi T, Yoshimura A. 2009. Silencing of SOCS1 in macrophages suppresses tumor development by enhancing antitumor inflammation. Cancer Sci 100: 730–736.
37. Hilton DJ, Richardson RT, Alexander WS, Viney EM, Willson TA, Sprigg NS, Starr R, Nicholson SE, Metcalf D, Nicola NA. 1998. Twenty proteins containing a C-terminal SOCS box form five structural classes. Proc Natl Acad Sci 95: 114–119.
38. Hirata Y, Brems H, Suzuki M, Kanamori M, Okada M, Morita R, Llano-Rivas I, Ose T, Messiaen L, Legius E, et al. 2016. Interaction between a domain of the negative regulator of the Ras-ERK pathway, SPRED1 protein, and the GTPase-activating protein-related domain of neurofi-bromin is implicated in Legius syndrome and neurofi-bromatosis type 1. J Biol Chem 291: 3124–3134.
39. Hu Z, Yang J, Wu Y, Xiong G, Wang Y, Yang J, Deng L. 2014. Polymorphisms in CISH gene are associated with persistent hepatitis B virus infection in Han Chinese population. PloS ONE 9: e100826.
40. Inagaki-Ohara K, Kondo T, Ito M, Yoshimura A. 2013. SOCS, inflammation, and cancer. JAKSTAT 2: e24053.
41. Inagaki-Ohara K, Mayuzumi H, Kato S, Minokoshi Y, Ot-subo T, Kawamura YI, Dohi T, Matsuzaki G, Yoshimura A. 2014. Enhancement of leptin receptor signaling by SOCS3 deficiency induces development of gastric tumors in mice. Oncogene 33: 74–84.
42. Jenkins BJ, Grail D, Nheu T, Najdovska M, Wang B, Waring P, Inglese M, McLoughlin RM, Jones SA, Topley N, et al. 2005. Hyperactivation of Stat3 in gp130 mutant mice promotes gastric hyperproliferation and desensitizes TGF-β signaling. Nat Med 11: 845–852.
43. Judd LM, Bredin K, Kalantzis A, Jenkins BJ, Ernst M, Giraud AS. 2006. STAT3 activation regulates growth, inflammation, and vascularization in a mouse model of gastric tumorigenesis. Gastroenterology 131: 1073–1085.
44. Kamio M, Yoshida T, Ogata H, Douchi T, Nagata Y, Inoue M, Hasegawa M, Yonemitsu Y, Yoshimura A. 2004. SOC1 inhibits HPV-E7-mediated transformation by inducing degradation of E7 protein. Oncogene 23: 3107–3115.
45. Kamizono S, Hanada T, Yasukawa H, Minoguchi S, Kato R, Minoguchi M, Hattori K, Hatakeyama S, Yada M, Morita S, et al. 2001. The SOCS box of SOCS-1 accelerates ubiq-uitin-dependent proteolysis of TEL-JAK2. J Biol Chem 276: 12530–12538.
46. Kamura T, Maenaka K, Kotoshiba S, Matsumoto M, Kohda D, Conaway RC, Conaway JW, Nakayama KI. 2004. VHL-box and SOCS-box domains determine binding specificity for Cul2-Rbx1 and Cul5-Rbx2 modules of ubiquitin ligases. Genes Dev 18: 3055–3065.
47. Karabulut R, Turkyilmaz Z, Sonmez K, Kumas G, Ergun SG, Ergun MA, Basaklar AC. 2013. Twenty-four genes are upregulated in patients with hypospadias. J Med Genet 16: 39–43.
48. Kershaw NJ, Murphy JM, Liau NP, Varghese LN, Laktyushin A, Whitlock EL, Lucet IS, Nicola NA, Babon JJ. 2013. SOCS3 binds specific receptor-JAK complexes to control cytokine signaling by direct kinase inhibition. Nat Struct Mol Biol 20: 469–476.
49. Khor CC, Vannberg FO, Chapman SJ, Guo H, Wong SH, Walley AJ, Vukcevic D, Rautanen A, Mills TC, Chang KC, et al. 2010. CISH and susceptibility to infectious diseases. N Engl J Med 362: 2092–2101.
50. Kinjyo I, Inoue H, Hamano S, Fukuyama S, Yoshimura T, Koga K, Takaki H, Himeno K, Takaesu G, Kobayashi T, et al. 2006. Loss of SOCS3 in T helper cells resulted in reduced immune responses and hyperproduction of interleukin 10 and transforming growth factor-β1. J Exp Med 203: 1021–1031.
51. Lan F, Zhang N, Zhang J, Krysko O, Zhang QB, Xian JM, Derycke L, Qi YY, Li K, Liu SX, et al. 2013. Forkhead box protein 3 in human nasal polyp regulatory T cells is regulated by the protein suppressor of cytokine signaling 3. J Allergy Clin Immun 132: 1314.
52. Le Y, Zhu BM, Harley B, Park SY, Kobayashi T, Manis JP, Luo HR, Yoshimura A, Hennighausen L, Silberstein LE. 2007. SOCS3 protein developmentally regulates the chemokine receptor CXCR4-FAK signaling pathway during B lym-phopoiesis. Immunity 27: 811–823.
53. Lee SH, Yun S, Piao ZH, Jeong M, Kim DO, Jung H, Lee J, Kim MJ, Kim MS, Chung JW, et al. 2010. Suppressor of cytokine signaling 2 regulates IL-15-primed human NK cell function via control of phosphorylated Pyk2. J Immunol 185: 917–928.
54. + T cells. PloS ONE 10: e0132957.
55. Lennerz JK, Hoffmann K, Bubolz AM, Lessel D, Welke C, Ruther N, Viardot A, Moller P. 2015. Suppressor of cytokine signaling 1 gene mutation status as a prognostic biomarker in classical Hodgkin lymphoma. Oncotarget 6: 29097–29110.
56. Lesina M, Kurkowski MU, Ludes K, Rose-John S, Treiber M, Kloppel G, Yoshimura A, Reindl W, Sipos B, Akira S, et al. 2011. Stat3/Socs3 activation by IL-6 transsignaling promotes progression of pancreatic intraepithelial neoplasia and development of pancreatic cancer. Cancer Cell 19: 456–469.
57. Lewis RS, Noor SM, Fraser FW, Sertori R, Liongue C, Ward AC. 2014. Regulation of embryonic hematopoiesis by a cytokine-inducible SH2 domain homolog in zebrafish. J Immunol 92: 5739–5748.
58. Li S, Chen S, Xu X, Sundstedt A, Paulsson KM, Anderson P, Karlsson S, Sjogren HO, Wang P. 2000. Cytokine-induced Src homology 2 protein (CIS) promotes T cell receptor-mediated proliferation and prolongs survival of activated T cells. J Exp Med 191: 985–994.
59. Liu H, Irwanto A, Fu X, Yu GQ, Yu YX, Sun YH, Wang C, Wang ZZ, Okada Y, Low HQ, et al. 2015. Discovery of six new susceptibility loci and analysis of pleiotropic effects in leprosy. Nat Genet 47: 267.
60. Lu LF, Thai TH, Calado DP, Chaudhry A, Kubo M, Tanaka K, Loeb GB, Lee H, Yoshimura A, Rajewsky K, et al. 2009. Foxp3-dependent microRNA155 confers competitive fitness to regulatory T cells by targeting SOCS1 protein. Immunity 30: 80–91.
61. Lu LF, Boldin MP, Chaudhry A, Lin LL, Taganov KD, Hanada T, Yoshimura A, Baltimore D, Rudensky AY. 2010. Function of miR-146a in controlling Treg cell-mediated regulation of Th1 responses. Cell 142: 914–929.
62. Lu LF, Gasteiger G, Yu IS, Chaudhry A, Hsin JP, Lu YH, Bos PD, Lin LL, Zawislak CL, Cho SL, et al. 2015. A single miRNA-mRNA interaction affects the immune response in a context-and cell-type-specific manner. Immunity 43: 52–64.
63. + lineage fate by inducing the SOCS suppressors of cytokine signaling. Nat Immunol 15: 638–645.
64. Mallette FA, Calabrese V, Ilangumaran S, Ferbeyre G. 2010. SOCS1, a novel interaction partner of p53 controlling oncogene-induced senescence. Aging (Albany NY) 2: 445–452.
65. Mansell A, Smith R, Doyle SL, Gray P, Fenner JE, Crack PJ, Nicholson SE, Hilton DJ, O’Neill LA, Hertzog PJ. 2006. Suppressor of cytokine signaling 1 negatively regulates Toll-like receptor signaling by mediating Mal degradation. Nat Immunol 7: 148–155.
66. Matsumoto A, Masuhara M, Mitsui K, Yokouchi M, Ohtsubo M, Misawa H, Miyajima A, Yoshimura A. 1997. CIS, a cytokine inducible SH2 protein, is a target of the JAK-STAT5 pathway and modulates STAT5 activation. Blood 89: 3148–3154.
67. Matsumura Y, Kobayashi T, Ichiyama K, Yoshida R, Hashimoto M, Takimoto T, Tanaka K, Chinen T, Shichita T, Wyss-Coray T, et al. 2007. Selective expansion of Foxp3-positive regulatory T cells and immunosuppression by suppressors of cytokine signaling 3-deficient dendritic cells. J Immunol 179: 2170–2179.
68. Mostecki J, Cassel SL, Klimecki WT, Stern DA, Knisz J, Iwa-shita S, Graves P, Miller RL, van Peer M, Halonen M, et al. 2011. A SOCS-1 promoter variant is associated with total serum IgE levels. J Immunol 187: 2794–2802.
69. Nonami A, Kato R, Harada M, Yoshimura A. 2003. Spred-1 negatively regulates cytokine-induced MAP kinase activation in hematopoietic cells. Blood 102: 833A–833A.
70. Ogata H, Kobayashi T, Chinen T, Takaki H, Sanada T, Minoda Y, Koga K, Takaesu G, Maehara Y, Iida M, et al. 2006. Deletion of the SOCS3 gene in liver parenchymal cells promotes hepatitis-induced hepatocarcinogenesis. Gastroenterology 131: 179–193.
71. Okabe S, Tauchi T, Morita H, Ohashi H, Yoshimura A, Ohyashiki K. 1999. Thrombopoietin induces an SH2-containing protein, CIS1, which binds to Mpl: Involvement of the ubiquitin proteosome pathway. Exp Hematol 27: 1542–1547.
72. O’Shea JJ, Gadina M, Schreiber RD. 2002. Cytokine signaling in 2002: New surprises in the Jak/Stat pathway. Cell 109: S121–S131.
73. + T cells to maintain tumor tolerance. J Exp Med 212: 2095–2113.
74. Ram PA, Waxman DJ. 2000. Role of the cytokine-inducible SH2 protein CIS in desensitization of STAT5b signaling by continuous growth hormone. J Biol Chem 275: 39487–39496.
75. Ramanathan S, Dubois S, Gagnon J, Leblanc C, Mariathasan S, Ferbeyre G, Rottapel R, Ohashi PS, Ilangumaran S. 2010. Regulation of cytokine-driven functional differentiation of CD8 T cells by suppressor of cytokine signaling 1 controls autoimmunity and preserves their proliferative capacity toward foreign antigens. J Immunol 185: 357– 366.
76. Romain M, Taleb S, Dalloz M, Ponnuswamy P, Esposito B, Perez N, Wang Y, Yoshimura A, Tedgui A, Mallat Z. 2013. Overexpression of SOCS3 in T lymphocytes leads to impaired interleukin-17 production and severe aortic aneurysm formation in mice-brief report. Arterioscler Thromb Vasc Biol 33: 581–584.
77. Schif B, Lennerz JK, Kohler CW, Bentink S, Kreuz M, Melz-ner I, Ritz O, Trumper L, Loeffler M, Spang R, et al. 2013. SOCS1 mutation subtypes predict divergent outcomes in diffuse large B-cell lymphoma (DLBCL) patients. Oncotarget 4: 35–47.
78. H2-mediated allergic responses. Nat Med 9: 1047–1054.
79. Sekiya T, Nakatsukasa H, Lu Q, Yoshimura A. 2016. Roles of transcription factors and epigenetic modifications in differentiation and maintenance of regulatory T cells. Microbes Infect 18: 378–386.
80. Sharma M, Mitnala S, Vishnubhotla RK, Mukherjee R, Reddy DN, Rao PN. 2015. The riddle of nonalcoholic fatty liver disease: Progression from nonalcoholic fatty liver to nonalcoholic steatohepatitis. J Clin Exp Hepatol 5: 147–158.
81. Shembade N, Harhaj EW. 2012. Regulation of NF-κB signaling by the A20 deubiquitinase. Cell Mol Immunol 9: 123–130.
82. Shen L, Evel-Kabler K, Strube R, Chen SY. 2004. Silencing of SOCS1 enhances antigen presentation by dendritic cells and antigen-specific anti-tumor immunity. Nat Biotechnol 22: 1546–1553.
83. Shi H, Tzameli I, Bjorbaek C, Flier JS. 2004. Suppressor of cytokine signaling 3 is a physiological regulator of adipo-cyte insulin signaling. J Biol Chem 279: 34733–34740.
84. Shouda T, Yoshida T, Hanada T, Wakioka T, Oishi M, Miyoshi K, Komiya S, Kosai K, Hanakawa Y, Hashimoto K, et al. 2001. Induction of the cytokine signal regulatorSOCS3/CIS3 as a therapeutic strategy for treating inflammatory arthritis. J Clin Invest 108: 1781–1788.
85. Shouda T, Hiraoka K, Komiya S, Hamada T, Zenmyo M, Iwasaki H, Isayama T, Fukushima N, Nagata K, Yoshimura A. 2006. Suppression of IL-6 production and proliferation by blocking STAT3 activation in malignant soft tissue tumor cells. Cancer Lett 231: 176–184.
86. Song G, Rao H, Feng B, Wei L. 2014. Association between CISH polymorphisms and spontaneous clearance of hepatitis B virus in hepatitis B extracellular antigen-positive patients during immune active phase. Chin Med J (Engl) 127: 1691–1695.
87. F136L) cannot regulate erythropoietin responses. Brit J Haematol 147: 450–458.
88. cip1: Regulation by SOCS3. Biochem Biophys Res Commun 338: 1943–1949.
89. Sun L, Jin YQ, Shen C, Qi H, Chu P, Yin QQ, Li JQ, Tian JL, Jiao WW, Xiao J, et al. 2014. Genetic contribution of CISH promoter polymorphisms to susceptibility to tuberculosis in Chinese children. PloS ONE 9: e92020.
90. Tagami-Nagata N, Serada S, Fujimoto M, Tanemura A, Nakatsuka R, Ohkawara T, Murota H, Kishimoto T, Katayama I, Naka T. 2015. Suppressor of cytokine signal-ling-1 induces significant preclinical antitumor effect in malignant melanoma cells. Exp Dermatol 24: 864–871.
91. Takahashi R, Yoshimura A. 2014. SOCS1 and regulation of regulatory T cells plasticity. J Immunol Res 2014: 943149.
92. Takahashi R, Nishimoto S, Muto G, Sekiya T, Tamiya T, Kimura A, Morita R, Asakawa M, Chinen T, Yoshimura A. 2011. SOCS1 is essential for regulatory T cell functions by preventing loss of Foxp3 expression as well as IFN-γ and IL-17A production. J Exp Med 208: 2055–2067.
93. Takimoto T, Wakabayashi Y, Sekiya T, Inoue N, Morita R, Ichiyama K, Takahashi R, Asakawa M, Muto G, Mori T, et al. 2010. Smad2 and Smad3 are redundantly essential for the TGF-β-mediated regulation of regulatory T plasticity and Th1 development. J Immunol 185: 842–855.
94. Taleb S, Romain M, Ramkhelawon B, Uyttenhove C, Paster-kamp G, Herbin O, Esposito B, Perez N, Yasukawa H, Van Snick J, et al. 2009. Loss of SOCS3 expression in T cells reveals a regulatory role for interleukin-17 in atherosclerosis. J Exp Med 206: 2067–2077.
95. Tamiya T, Kashiwagi I, Takahashi R, Yasukawa H, Yoshimura A. 2011. Suppressors of cytokine signaling (SOCS) proteins and JAK/STAT pathways: Regulation of T-cell inflammation by SOCS1 and SOCS3. Arterioscler Thromb Vasc Biol 31: 980–985.
96. Tamiya T, Ichiyama K, Kotani H, Fukaya T, Sekiya T, Shichita T, Honma K, Yui K, Matsuyama T, Nakao T, et al. 2013. Smad2/3 and IRF4 play a cooperative role in IL-9-pro-ducing T cell induction. J Immunol 191: 2360–2371.
97. Tanaka K, Ichiyama K, Hashimoto M, Yoshida H, Takimoto T, Takaesu G, Torisu T, Hanada T, Yasukawa H, Fukuyama S, et al. 2008. Loss of suppressor of cytokine signaling 1 in helper T cells leads to defective Th17 differentiation by enhancing antagonistic effects of IFN-γ on STAT3 and Smads. J Immunol 180: 3746–3756.
98. Tang B, Wang ZR, Qi GY, Yuan SG, Yu SP, Li B, Wei YC, Huang Q, Zhai R, He SQ. 2015. MicroRNA-155 deficiency attenuates ischemia-reperfusion injury after liver transplantation in mice. Transpl Int 28: 751–760.
99. Tokumaru S, Sayama K, Yamasaki K, Shirakata Y, Hanakawa Y, Yahata Y, Dai XJ, Tohyama M, Yang LJ, Yoshimura A, et al. 2005. SOCS3/CIS3 negative regulation of STAT3 in HGF-induced keratinocyte migration. Biochem Biophys Res Commun 327: 100–105.
100. Tong HV, Toan NL, Song le H, Kremsner PG, Kun JF, Tp V. 2012. Association of CISH-292A/T genetic variant with hepatitis B virus infection. Immunogenetics 64: 261–265.
101. Torisu T, Sato N, Yoshiga D, Kobayashi T, Yoshioka T, Mori H, Iida M, Yoshimura A. 2007. The dual function of hepatic SOCS3 in insulin resistance in vivo. Genes Cells 12: 143–154.
102. Vogelzang A, McGuire HM, Yu D, Sprent J, Mackay CR, King C. 2008. A fundamental role for interleukin-21 in the generation of T follicular helper cells. Immunity 29: 127–137.
103. Wakioka T, Sasaki A, Kato R, Shouda T, Matsumoto A, Miyoshi K, Tsuneoka M, Komiya S, Baron R, Yoshimura A. 2001. Spred is a Sprouty-related suppressor of Ras signalling. Nature 412: 647–651.
104. Wang X, Li T, Li M, Cao N, Han J. 2016. The functional SOCS3 RS115785973 variant regulated by MiR-4308 promotes gastric cancer development in Chinese population. Cell Physiol Biochem 38: 1796–1802.
105. Weber-Nordt RM, Riley JK, Greenlund AC, Moore KW, Darnell JE, Schreiber RD. 1996. Stat3 recruitment by two distinct ligand-induced, tyrosine-phosphorylated docking sites in the interleukin-10 receptor intracellular domain. J Biol Chem 271: 27954–27961.
106. Yamamoto K, Yamaguchi M, Miyasaka N, Miura O. 2003. SOCS-3 inhibits IL-12-induced STAT4 activation by binding through its SH2 domain to the STAT4 docking site in the IL-12 receptor β2 subunit. Biochem Biophys Res Commun 310: 1188–1193.
107. Yang XXO, Zhang HY, Kim BS, Niu XY, Peng J, Chen YH, Kerketta R, Lee YH, Chang SH, Corry DB, et al. 2013. The signaling suppressor CIS controls proallergic T cell development and allergic airway inflammation. Nat Immunol 14: 732.
108. Yasukawa H, Misawa H, Sakamoto H, Masuhara M, Sasaki A, Wakioka T, Ohtsuka S, Imaizumi T, Matsuda T, Ihle JN, et al. 1999. The JAK-binding protein JAB inhibits Janus tyrosine kinase activity through binding in the activation loop. EMBO J 18: 1309–1320.
109. Yasukawa H, Ohishi M, Mori H, Murakami M, Chinen T, Aki D, Hanada T, Takeda K, Akira S, Hoshijima M, et al. 2003. IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nat Immunol 4: 551– 556.
110. Yeganeh M, Gui Y, Kandhi R, Bobbala D, Tobelaim WS, Saucier C, Yoshimura A, Ferbeyre G, Ramanathan S, Ilangumaran S. 2016. Suppressor of cytokine signaling 1-de-pendent regulation of the expression and oncogenic functions of p21 in the liver. Oncogene 35: 4200–4211.
111. Yoshida T, Ogata H, Kamio M, Joo A, Shiraishi H, Tokunaga Y, Sata M, Nagai H, Yoshimura A. 2004. SOCS1 is a suppressor of liver fibrosis and hepatitis-induced carcinogenesis. J Exp Med 199: 1701–1707.
112. Yoshida T, Hisamoto T, Akiba J, Koga H, Nakamura K, Tokunaga Y, Hanada S, Kumemura H, Maeyama M, Harada M, et al. 2006. Spreds, inhibitors of the Ras/ERK signal transduction, are dysregulated in human hepatocellular carcinoma and linked to the malignant phenotype of tumors. Oncogene 25: 6056–6066.
113. Yoshikawa H, Matsubara K, Qian GS, Jackson P, Groopman JD, Manning JE, Harris CC, Herman JG. 2001. SOCS-1, a negative regulator of the JAK/STAT pathway, is silenced by methylation in human hepatocellular carcinoma and shows growth-suppression activity. Nat Genet 28: 29–35.
114. Yoshimura A, Ohkubo T, Kiguchi T, Jenkins NA, Gilbert DJ, Copeland NG, Hara T, Miyajima A. 1995. A novel cytokine-inducible gene CIS encodes an SH2-containing protein that binds to tyrosine-phosphorylated interleukin 3 and erythropoietin receptors. EMBO J 14: 2816–2826.
115. Yoshimura A, Naka T, Kubo M. 2007. SOCS proteins, cytokine signalling and immune regulation. Nat Rev Immunol 7: 454–465.
116. Yoshimura A, Suzuki M, Sakaguchi R, Hanada T, Yasukawa H. 2012. SOCS, inflammation, and autoimmunity. Front Immunol 3: 20.