SOCS3 and its role in associated diseases

Human Immunology

Volumn 76, Issue 10, 2015, Pages 775-780

  Yin, Yanlin ^a   Liu, Weiwei ^a   Dai, Yalei ^a  

^a TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Cytokine; Immune homeostasis; JAK STAT signaling; SOCS3

Indexed keywords

CYTOKINE; CYTOKINE RECEPTOR; GLYCOPROTEIN; GROWTH FACTOR; JANUS KINASE; STAT PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; PROTEIN BINDING; SOCS3 PROTEIN, HUMAN; SUPPRESSOR OF CYTOKINE SIGNALING;

ALLERGY; AUTOIMMUNE DISEASE; CELL COMMUNICATION; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; INFLAMMATION; INFLAMMATORY BOWEL DISEASE; INSULIN RESISTANCE; KNOCKOUT MOUSE; MULTIPLE SCLEROSIS; NEOPLASM; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; REVIEW; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; TARGET CELL; ANIMAL; ASTHMA; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MOUSE; PATHOLOGY;

ANIMALS; ARTHRITIS, RHEUMATOID; ASTHMA; CELL COMMUNICATION; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATORY BOWEL DISEASES; JANUS KINASES; MICE; MICE, KNOCKOUT; MULTIPLE SCLEROSIS; NEOPLASMS; PROTEIN BINDING; RECEPTORS, CYTOKINE; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 84945919115     PISSN: 01988859     EISSN: 18791166     Source Type: Journal    
DOI: 10.1016/j.humimm.2015.09.037     Document Type: Review

References (77)

1. Lemmon M.A., Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2010, 141:1117-1134.
2. Ilangumaran S., Ramanathan S., Rottapel R. Regulation of the immune system by SOCS family adaptor proteins. Semin. Immunol. 2004, 16(6):351-365.
3. Croker B.A., Kiu H., Nicholson S.E. SOCS regulation of the JAK/STAT signalling pathway. Semin. Cell Dev. Biol. 2008, 19(4):414-422.
4. Piessevaux J., Lavens D., Peelman F., Tavernier J. The many faces of the SOCS box. Cytokine Growth Factor Rev. 2008, 19(5-6):371-381.
5. O'Sullivan L.A., Liongue C., Lewis R.S., Stephenson S.E.M., Ward A.C. Cytokine receptor signaling through the JAK-STAT-SOCS pathway in disease. Mol. Immunol. 2007, 44:2497-2506.
6. Babon J.J., Sabo J.K., Soetopo A., Yao S., Bailey M.F., Zhang J.G., et al. The SOCS box domain of SOCS3: structure and interaction with the elonginBC-cullin5 ubiquitin ligase. J. Mol. Biol. 2008, 381(4):928-940.
7. Shuai K., Liu B. Regulation of JAK-STAT signalling in the immune system. Nat. Rev. Immunol. 2003, 3(11):900-911.
8. Kershaw N.J., Murphy J.M., Liau N.P., Varghese L.N., Laktyushin A., Whitlock E.L., et al. SOCS3 binds specific receptor-JAK complexes to control cytokine signaling by direct kinase inhibition. Nat. Struct. Mol. Biol. 2013, 20(4):469-476.
9. Xiang S., Dong N.G., Liu J.P., Wang Y., Shi J.W., Wei Z.J., et al. Inhibitory effects of suppressor of cytokine signaling 3 on inflammatory cytokine expression and migration and proliferation of IL-6/IFN-γ-induced vascular smooth muscle cells. J. Huazhong Univ. Sci. Technolog Med. Sci. 2013, 33(5):615-622.
10. Qin H., Niyongere S.A., Lee S.J., Baker B.J., Benveniste E.N. Expression and functional significance of SOCS-1 and SOCS-3 in astrocytes. J. Immunol. 2008, 181:3167-3176.
11. Qin H., Wilson C.A., Roberts K.L., Baker B.J., Zhao X., Benveniste E.N. IL-10 inhibits lipopolysaccharide-induced CD40 gene expression through induction of suppressor of cytokine signaling-3. J. Immunol. 2006, 177:7761-7771.
12. Pauli E.K., Schmolke M., Wolff T., Viemann D., Roth J., Bode J.G., et al. Influenza A virus inhibits type I IFN signaling via NF-kappaB-dependent induction of SOCS-3 expression. PLoS Pathog. 2008, 4(11):e1000196.
13. Baetz A., Frey M., Heeg K., Dalpke A.H. Suppressor of cytokine signaling (SOCS) proteins indirectly regulate toll-like receptor signaling in innate immune cells. J. Biol. Chem. 2004, 279:54708-54715.
14. Bellezza I., Neuwirt H., Nemes C., Cavarretta I.T., Puhr M., Steiner H., et al. Suppressor of cytokine signaling-3 antagonizes cAMP effects on proliferation and apoptosis and is expressed in human prostate cancer. Am. J. Pathol. 2006, 169:2199-2208.
15. Chaves de Souza J.A., Nogueira A.V., Chaves de Souza P.P., Kim Y.J., Silva Lobo C., Lopes Pimentel, de Oliveira G.J., et al. SOCS3 expression correlates with severity of inflammation, expression of proinflammatory cytokines, and activation of STAT3 and p38 MAPK in LPS-induced inflammation in vivo. Mediators Inflamm. 2013, 10.1155/2013/650812.
16. Torun D., Nevruz O., Akyol M., Kozan S., Bahçe M., Güran S., et al. Methylation of SOCS3 in myeloproliferative neoplasms and secondary erythrocytosis/thrombocythemia. Turk. J. Haematol. 2013, 30(1):13-18.
17. Yan C., Cao J., Wu M., Zhang W., Jiang T., Yoshimura A., et al. Suppressor of cytokine signaling 3 inhibits LPS-induced IL-6 expression in osteoblasts by suppressing CCAAT/enhancer-binding protein {beta} activity. J. Biol. Chem. 2010, 285(48):37227-37239.
18. Barclay J.L., Anderson S.T., Waters M.J., Curlewis J.D. Regulation of suppressor of cytokine signaling 3 (SOC3) by growth hormone in pro-B cells. Mol. Endocrinol. 2007, 21(10):2503-2515.
19. Piao L., Park J., Li Y., Shin S., Shin S., Kong G., et al. SOCS3 and SOCS6 are required for the risperidone-mediated inhibition of insulin and leptin signaling in neuroblastoma cells. Int. J. Mol. Med. 2014, 33(5):1364-1370.
20. Sewell G.W., Marks D.J., Segal A.W. The immunopathogenesis of Crohn's disease: a three-stage model. Curr. Opin. Immunol. 2009, 21:506-513.
21. White G.E., Cotterill A., Addley M.R., Soilleux E.J., Greaves D.R. Suppressor of cytokine signalling protein SOCS3 expression is increased at sites of acute and chronic inflammation. J. Mol. Histol. 2010, 42:137-151.
22. Miyanaka Y., Ueno Y., Tanaka S., Yoshioka K., Hatakeyama T., Shimamoto M., et al. Clinical significance of mucosal suppressors of cytokine signaling 3 expression in ulcerative colitis. World J. Gastroenterol. 2007, 13:2939-2944.
23. Andoh A., Shioya M., Nishida A., Bamba S., Tsujikawa T., Kim-Mitsuyama S., et al. Expression of IL-24, an activator of the JAK1/STAT3/SOCS3 cascade, is enhanced in inflammatory bowel disease. J. Immunol. 2009, 183(1):687-695.
24. Rigby R.J., Simmons J.G., Greenhalgh C.J., Alexander W.S., Lund P.K. Suppressor of cytokine signaling 3 (SOCS3) limits damage-induced crypt hyper-proliferation and inflammation-associated tumorigenesis in the colon. Oncogene 2007, 26(33):4833-4841.
25. Hsu C.K., Lee I.T., Lin C.C., Hsiao L.D., Yang C.M. Nox2/ROS-dependent human antigen R translocation contributes to TNF-α-induced SOCS-3 expression in human tracheal smooth muscle cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2014, 306(6):L521-L533.
26. Niemand C., Nimmesgern A., Haan S., Fischer P., Schaper F., Rossaint R., et al. Activation of STAT3 by IL-6 and IL-10 in primary human macrophages is differentially modulated by suppressor of cytokine signaling 3. J. Immunol. 2003, 170:3263-3272.
27. Berlato C., Cassatella M.A., Kinjyo I., Gatto L., Yoshimura A., Bazzoni F. Involvement of suppressor of cytokine signaling-3 as a mediator of the inhibitory effects of IL-10 on lipopolysaccharide-induced macrophage activation. J. Immunol. 2002, 168:6404-6411.
28. Hu B., Elinav E., Huber S., Strowig T., Hao L., Hafemann A., et al. Microbiota-induced activation of epithelial IL-6 signaling links inflammasome-driven inflammation with transmissible cancer. Proc. Natl. Acad. Sci. U.S.A. 2013, 110(24):9862-9867.
29. Goldstein J.I., Kominsky D.J., Jacobson N., Bowers B., Regalia K., Austin G.L., et al. Defective leukocyte GM-CSF receptor (CD116) expression and function in inflammatory bowel disease. Gastroenterology 2011, 141(1):208-216.
30. Lovato P., Brender C., Agnholt J., Kelsen J., Kaltoft K., Svejgaard A., et al. Constitutive STAT3 activation in intestinal T cells from patients with Crohn's disease. J. Biol. Chem. 2003, 278:16777-16781.
31. Majithia V., Geraci S.A. Rheumatoid arthritis: diagnosis and management. Am. J. Med. 2007, 120(11):936-939.
32. Shouda T., Yoshida T., Hanada T., Wakioka T., Oishi M., Miyoshi K., et al. Induction of the cytokine signal regulator SOCS3/CIS3 as a therapeutic strategy for treating inflammatory arthritis. J. Clin. Invest. 2001, 108:1781-1788.
33. Wong P.K., Egan P.J., Croker B.A., O'Donnell K., Sims N.A., Drake S., et al. SOCS-3 negatively regulates innate and adaptive immune mechanisms in acute IL-1-dependent inflammatory arthritis. J. Clin. Invest. 2006, 116:1571-1581.
34. Sawa S., Kamimura D., Jin G.H., Morikawa H., Kamon H., Nishihara M., et al. Autoimmune arthritis associated with mutated interleukin(IL)-6 receptor gp130 is driven by STAT3/IL-7-dependent homeostatic proliferation of CD4+T cells. J. Exp. Med. 2006, 203(6):1459-1470.
35. Frisullo G., Angelucci F., Caggiula M., Nociti V., Iorio R., Patanella A.K., et al. PSTAT1, pSTAT3, and T-bet expression in peripheral blood mononuclear cells from relapsing-remitting multiple sclerosis patients correlates with disease activity. J. Neurosci. Res. 2006, 84:1027-1036.
36. Zhang X., Jin J., Peng X., Ramgolam V.S., Markovic-Plese S. Simvastatin inhibits IL-17 secretion by targeting multiple IL-17-regulatory cytokines and by inhibiting the expression of IL-17 transcription factor RORC in CD4+ lymphocytes. J. Immunol. 2008, 180:6988-6996.
37. Weber M.S., Zamvil S.S. Statins and demyelination. Curr. Top. Microbiol. Immunol. 2008, 318:313-324.
38. Li Y., Chu N., Rostami A., Zhang G.X. Dendritic cells transduced with SOCS-3 exhibit a tolerogenic/DC2 phenotype that directs type 2 Th cell differentiation in vitro and in vivo. J. Immunol. 2006, 177:1679-1688.
39. Seki Y., Inoue H., Nagata N., Hayashi K., Fukuyama S., Matsumoto K., et al. SOCS-3 regulates onset and maintenance of T(H)2-mediated allergic responses. Nat. Med. 2003, 9:1047-1054.
40. Arakawa S., Hatano Y., Katagiri K. Differential expression of mRNA for Th1 and Th2 cytokine-associated transcription factors and suppressors of cytokine signalling in peripheral blood mononuclear cells of patients with atopic dermatitis. Clin. Exp. Immunol. 2004, 135:505-510.
41. Moriwaki A., Inoue H., Nakano T., Matsunaga Y., Matsuno Y., Matsumoto T., et al. T cell treatment with small interfering RNA for suppressor of cytokine signaling 3 modulates allergic airway responses in a murine model of asthma. Am. J. Respir. Cell Mol. Biol. 2011, 44(4):448-455.
42. Zafra M.P., Mazzeo C., Gámez C., Rodriguez Marco A., de Zulueta A., Sanz V., et al. Gene silencing of SOCS3 by siRNA intranasal delivery inhibits asthma phenotype in mice. PLoS One 2014, 9(3):e91996.
43. Kinjyo I., Inoue H., Hamano S., Fukuyama S., Yoshimura T., Koga K., et al. Loss of SOCS3 in T helper cells resulted in reduced immune responses and hyperproduction of interleukin10 and transforming growth factor-beta1. J. Exp. Med. 2006, 203(4):1021-1031.
44. Ozaki A., Seki Y., Fukushima A., Kubo M. The control of allergic conjunctivitis by suppressor of cytokine signaling (SOCS) 3 and SOCS5. J. Immunol. 2005, 175:5489-5497.
45. Ortiz-Muñoz G., Martin-Ventura J.L., Hernandez-Vargas P., Mallavia B., Lopez-Parra V., Lopez-Franco O., et al. Suppressors of cytokine signaling modulate JAK/STAT-mediated cell responses during atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2009, 29:525-531.
46. Yin Y., Liu W., Ji G., Dai Y. The essential role of p38 MAPK in mediating the interplay of oxLDL and IL-10 in regulating endothelial cell apoptosis. Eur. J. Cell Biol. 2013, 92(4-5):150-159.
47. Taleb S., Romain M., Ramkhelawon B., Uyttenhove C., Pasterkamp G., Herbin O., et al. Loss of SOCS3 expression in T cells reveals a regulatory role for interleukin-17 in atherosclerosis. J. Exp. Med. 2009, 206:2067-2077.
48. Terrell A.M., Crisostomo P.R., Wairiuko G.M., Wang M., Morrell E.D., Meldrum D.R. Jak/STAT/SOCS signaling circuits and associated cytokine-mediated inflammation and hypertrophy in the heart. Shock 2006, 26:226-234.
49. Fahmi A., Smart N., Punn A., Jabr R., Marber M., Heads R. P42/p44-MAPK and PI3K are sufficient for IL-6 family cytokines/gp130 to signal to hypertrophy and survival in cardiomyocytes in the absence of JAK/STAT activation. Cell Signal. 2013, 25(4):898-909.
50. Jeppesen P.L., Christensen G.L., Schneider M., Nossent A.Y., Jensen H.B., Andersen D.C., et al. Angiotensin II type 1 receptor signalling regulates microRNA differentially in cardiac fibroblasts and myocytes. Br. J. Pharmacol. 2011, 164(2):394-404.
51. Calegari V.C., Bezerra R.M., Torsoni M.A., Torsoni A.S., Franchini K.G., Saad M.J., et al. Suppressor of cytokine signaling 3 is induced by angiotensin II in heart and isolated cardiomyocytes, and participates in desensitization. Endocrinology 2003, 144:4586-4696.
52. You J., Yu Y., Jiang L., Li W., Yu X., Gonzalez L., et al. Signaling through Tyr985 of lepfin receptor as an age/diet-dependent switch in the regulation of energy balance. Mol. Cell. Biol. 2010, 30:1650-1659.
53. Münzberg H., Flier J.S., Bjørbaek C. Region-specific leptin resistance within the hypothalamus of diet-induced obese mice. Endocrinology 2004, 145:4880-4889.
54. Wang Z.W., Pan W.T., Lee Y., Kakuma T., Zhou Y.T., Unger R.H. The role of leptin resistance in the lipid abnormalities of aging. FASEB J. 2001, 15:108-114.
55. Syed M., Cozart M., Haney A.C., Akhter N., Odle A.K., Allensworth-James M., et al. Ghrelin restoration of function in vitro in somatotropes from male mice lacking the Janus kinase (JAK)-binding site of the leptin receptor. Endocrinology 2013, 154(4):1565-1576.
56. Howard J.K., Cave B.J., Oksanen L.J., Tzameli I., Bjørbaek C., Flier J.S. Enhanced leptin sensitivity and attenuation of diet-induced obesity in mice with haploinsufficiency of Socs3. Nat. Med. 2004, 10:734-738.
57. Mori H., Hanada R., Hanada T., Aki D., Mashima R., Nishinakamura H., et al. Socs3 deficiency in the brain elevates leptin sensitivity and confers resistance to diet-induced obesity. Nat. Med. 2004, 10:739-743.
58. Kievit P., Howard J.K., Badman M.K., Balthasar N., Coppari R., Mori H., et al. Enhanced leptin sensitivity and improved glucose homeostasis in mice lacking suppressor of cytokine signaling-3 in POMC-expressing cells. Cell Metab. 2006, 2:123-132.
59. Olofsson L.E., Unger E.K., Cheung C.C., Xu A.W. Modulation of AgRP-neuronal function by SOCS3 as an initiating event in diet-induced hypothalamic leptin resistance. Proc. Natl. Acad. Sci. U.S.A. 2013, 110(8):E697-E706.
60. Yang Z., Hulver M., McMillan R.P., Cai L., Kershaw E.E., Yu L., et al. Regulation of insulin and leptin signaling by muscle suppressor of cytokine signaling 3 (SOCS3). PLoS One 2012, 7(10):e47493.
61. Shi H., Tzameli I., Bjørbaek C., Flier J.S. Suppressor of cytokine signaling-3 is a physiological regulator of adipocyte insulin signaling. J. Biol. Chem. 2004, 279:34733-34740.
62. Steppan C.M., Wang J., Whiteman E.L., Birnbaum M.J., Lazar M.A. Activation of SOCS-3 by resistin. Mol. Cell. Biol. 2005, 25:1569-1575.
63. Jorgensen S.B., O'Neill H.M., Sylow L., Honeyman J., Hewitt K.A., Palanivel R., et al. Deletion of skeletal muscle SOCS3 prevents insulin resistance in obesity. Diabetes 2013, 62(1):56-64.
64. Shi H., Cave B., Inouye K., Bjørbaek C., Flier J.S. Overexpression of suppressor of cytokine signaling 3 in adipose tissue causes local but not systemic insulin resistance. Diabetes 2006, 55:699-707.
65. Torisu T., Sato N., Yoshiga D., Kobayashi T., Yoshioka T., Mori H., et al. The dual function of hepatic SOCS3 in insulin resistance in vivo. Genes Cells 2007, 12:143-154.
66. Buzzelli M.D., Navaratnarajah M., Ahmed T., Nagarajan M., Shumate M.L., Lang C.H., et al. Nuclear factor kappaB mediates the inhibitory effects of interleukin-1 on growth hormone-inducible gene expression. J. Trauma 2008, 64(6):1427-1435.
67. Jenkins B.J., Grail D., Nheu T., Najdovska M., Wang B., Waring P., et al. Hyperactivation of Stat3 in gp130 mutant mice promotes gastric hyperproliferation and desensitizes TGF-beta signaling. Nat. Med. 2005, 11(8):845-852.
68. He B., You L., Uematsu K., Zang K., Xu Z., Lee A.Y., et al. SOCS-3 is frequently silenced by hypermethylation and suppresses cell growth in human lung cancer. Proc. Natl. Acad. Sci. U.S.A. 2003, 100(24):14133-14138.
69. Inagaki-Ohara K., Mayuzumi H., Kato S., Minokoshi Y., Otsubo T., Kawamura Y.I., et al. Enhancement of leptin receptor signaling by SOCS3 deficiency induces development of gastric tumors in mice. Oncogene 2014, 33(1):74-84.
70. Lesina M., Kurkowski M.U., Ludes K., Rose-John S., Treiber M., Klöppel G., et al. Stat3/Socs3 activation by IL-6 transsignaling promotes progression of pancreatic intraepithelial neoplasia and development of pancreatic cancer. Cancer Cell 2011, 19(4):456-469.
71. Puhr M., Santer F.R., Neuwirt H., Susani M., Nemeth J.A., Hobisch A., et al. Down-regulation of suppressor of cytokine signaling-3 causes prostate cancer cell death through activation of the extrinsic and intrinsic apoptosis pathways. Cancer Res. 2009, 69(18):7375-7384.
72. Hiwatashi K., Tamiya T., Hasegawa E., Fukaya T., Hashimoto M., Kakoi K., et al. Suppression of SOCS3 in macrophages prevents cancer metastasis by modifying macrophage phase and MCP2/CCL8 induction. Cancer Lett. 2011, 308(2):172-180.
73. Brender C., Lovato P., Sommer V.H., Woetmann A., Mathiesen A.M., Geisler C., et al. Constitutive SOCS-3 expression protects T-cell lymphoma against growth inhibition by IFNalpha. Leukemia 2005, 19(2):209-213.
74. Oguro T., Ishibashi K., Sugino T., Hashimoto K., Tomita S., Takahashi N., et al. Humanised antihuman IL-6R antibody with interferon inhibits renal cell carcinoma cell growth in vitro and in vivo through suppressed SOCS3 expression. Eur. J. Cancer 2013, 49(7):1715-1724.
75. Koeberlein B., zur Hausen A., Bektas N., Zentgraf H., Chin R., Nguyen L.T., et al. Hepatitis B virus overexpresses suppressor of cytokine signaling-3 (SOCS3) thereby contributing to severity of inflammation in the liver. Virus Res. 2010, 148:51-59.
76. Kamezaki K., Shimoda K., Numata A., Haro T., Kakumitsu H., Yoshie M., et al. Roles of Stat3 and ERK in G-CSF signaling. Stem Cells 2005, 23:252-263.
77. Uto-Konomi A., Miyauchi K., Ozaki N., Motomura Y., Suzuki Y., Yoshimura A., et al. Dysregulation of suppressor of cytokine signaling 3 in keratinocytes causes skin inflammation mediated by interleukin-20 receptor-related cytokines. PLoS One 2012, 7(7):e40343.