Suppressor of cytokine signaling (SOCS) 2, a protein with multiple functions

Cytokine and Growth Factor Reviews

Volumn 17, Issue 6, 2006, Pages 431-439

  Rico Bautista, Elizabeth ^a   Flores Morales, Amilcar ^a   Fernández Pérez, Leandro ^b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF LAS PALMAS DE GRAN CANARIA   (Spain)

Author keywords

Cytokine signaling; GH; SOCS2

Indexed keywords

CYTOKINE; HORMONE; SUPPRESSOR OF CYTOKINE SIGNALING 2;

CARCINOGENESIS; CENTRAL NERVOUS SYSTEM; CYTOKINE RELEASE; DIMERIZATION; DOWN REGULATION; ENZYME ACTIVATION; GENE EXPRESSION; GENE TARGETING; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; INSULIN RESISTANCE; MAMMARY GLAND; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SHORT SURVEY; SIGNAL TRANSDUCTION;

ANIMALS; BONE DEVELOPMENT; CYTOKINES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MICE; MODELS, BIOLOGICAL; NEOPLASMS; NERVOUS SYSTEM; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 33751212182     PISSN: 13596101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cytogfr.2006.09.008     Document Type: Short Survey

References (84)

1. Rawlings J.S., Rosler K.M., and Harrison D.A. The JAK/STAT signaling pathway. J Cell Sci 117 (2004) 1281-1283
2. Rakesh K., and Agrawal D.K. Controlling cytokine signaling by constitutive inhibitors. Biochem Pharmacol 70 (2005) 649-657
3. Flores-Morales A., Greenhalgh C.J., Norstedt G., and Rico-Bautista E. Negative regulation of GH receptor signaling. Mol Endocrinol 20 (2006) 241-253
4. Starr R., Willson T.A., Viney E.M., Murray L.J., Rayner J.R., Jenkins B.J., et al. A family of cytokine-inducible inhibitors of signalling. Nature 387 (1997) 917-921
5. Naka T., Narazaki M., Hirata M., Matsumoto T., Minamoto S., Aono A., et al. Structure and function of a new STAT-induced STAT inhibitor. Nature 387 (1997) 924-929
6. Endo T.A., Masuhara M., Yokouchi M., Suzuki R., Sakamoto H., Mitsui K., et al. A new protein containing an SH2 domain that inhibits JAK kinases. Nature 387 (1997) 921-924
7. Minamoto S., Ikegame K., Ueno K., Narazaki M., Naka T., Yamamoto H., et al. Cloning and functional analysis of new members of STAT induced STAT inhibitor (SSI) family: SSI-2 and SSI-3. Biochem Biophys Res Commun 237 (1997) 79-83
8. Fujimoto M., and Naka T. Regulation of cytokine signaling by SOCS family molecules. Trends Immunol 24 (2003) 659-666
9. Kile B.T., Schulman B.A., Alexander W.S., Nicola N.A., Martin H.M., and Hilton D.J. The SOCS box: a tale of destruction and degradation. Trends Biochem Sci 27 (2002) 235-241
10. Greenhalgh C.J., and Hilton D.J. Negative regulation of cytokine signaling. J Leukoc Biol 70 (2001) 348-356
11. Song M.M., and Shuai K. The suppressor of cytokine signaling (SOCS) 1 and SOCS3 but not SOCS2 proteins inhibit interferon-mediated antiviral and antiproliferative activities. J Biol Chem 273 (1998) 35056-35062
12. Greenhalgh C.J., and Alexander W.S. Suppressors of cytokine signalling and regulation of growth hormone action. Growth Horm IGF Res 14 (2004) 200-206
13. Elliott J., and Johnston J.A. SOCS: role in inflammation, allergy and homeostasis. Trends Immunol 25 (2004) 434-440
14. Yoshimura A., Nishinakamura H., Matsumura Y., and Hanada T. Negative regulation of cytokine signaling and immune responses by SOCS proteins. Arthritis Res Ther 7 (2005) 100-110
15. Metcalf D., Greenhalgh C.J., Viney E., Willson T.A., Starr R., Nicola N.A., et al. Gigantism in mice lacking suppressor of cytokine signalling-2. Nature 405 (2000) 1069-1073
16. Kopchick J.J., Bellush L.L., and Coschigano K.T. Transgenic models of growth hormone action. Annu Rev Nutr 19 (1999) 437-461
17. Colao A., Merola B., Ferone D., and Lombardi G. Acromegaly. J Clin Endocrinol Metab 82 (1997) 2777-2781
18. Bradford G.E., and Famula T.R. Evidence for a major gene for rapid postweaning growth in mice. Genet Res 44 (1984) 293-308
19. Horvat S., and Medrano J.F. Lack of Socs2 expression causes the high-growth phenotype in mice. Genomics 72 (2001) 209-212
20. Wong M.L., Islas-Trejo A., and Medrano J.F. Structural characterization of the mouse high growth deletion and discovery of a novel fusion transcript between suppressor of cytokine signaling-2 (Socs-2) and viral encoded semaphorin receptor (Plexin C1). Gene 299 (2002) 153-163
21. Rico-Bautista E., Greenhalgh C.J., Tollet-Egnell P., Hilton D.J., Alexander W.S., Norstedt G., et al. Suppressor of cytokine signaling-2 deficiency induces molecular and metabolic changes that partially overlap with growth hormone-dependent effects. Mol Endocrinol 19 (2005) 781-793
22. Greenhalgh C.J., Bertolino P., Asa S.L., Metcalf D., Corbin J.E., Adams T.E., et al. Growth enhancement in suppressor of cytokine signaling 2 (SOCS-2)-deficient mice is dependent on signal transducer and activator of transcription 5b (STAT5b). Mol Endocrinol 16 (2002) 1394-1406
23. Greenhalgh C.J., Rico-Bautista E., Lorentzon M., Thaus A.L., Morgan P.O., Willson T.A., et al. SOCS2 negatively regulates growth hormone action in vitro and in vivo. J Clin Invest 115 (2005) 397-406
24. Boverhof D.R., Tam E., Harney A.S., Crawford R.B., Kaminski N.E., and Zacharewski T.R. 2,3,7,8-Tetrachlorodibenzo-p-dioxin induces suppressor of cytokine signaling 2 in murine B cells. Mol Pharmacol 66 (2004) 1662-1670
25. Davey H.W., McLachlan M.J., Wilkins R.J., Hilton D.J., and Adams T.E. STAT5b mediates the GH-induced expression of SOCS-2 and SOCS-3 mRNA in the liver. Mol Cell Endocrinol 158 (1999) 111-116
26. Woelfle J., and Rotwein P. In vivo regulation of growth hormone-stimulated gene transcription by STAT5b. Am J Physiol Endocrinol Metab 286 (2004) E393-E401
27. Vidal OM, Merino R, Rico-Bautista E, Fernandez-Perez L, Chia DJ, Woelfle J, Ono M, Lenhard B, Norstedt G, Rotwein P, et al. In vivo transcript profiling and phylogenetic analysis identifies SOCS2 as a direct STAT5b target in liver. Mol Endocrinol; 2006.
28. Tollet-Egnell P., Flores-Morales A., Stavreus-Evers A., Sahlin L., and Norstedt G. Growth hormone regulation of SOCS-2, SOCS-3, and CIS messenger ribonucleic acid expression in the rat. Endocrinology 140 (1999) 3693-3704
29. Adams T.E., Hansen J.A., Starr R., Nicola N.A., Hilton D.J., and Billestrup N. Growth hormone preferentially induces the rapid, transient expression of SOCS-3, a novel inhibitor of cytokine receptor signaling. J Biol Chem 273 (1998) 1285-1287
30. Paul C., Seiliez I., Thissen J.P., and Le Cam A. Regulation of expression of the rat SOCS-3 gene in hepatocytes by growth hormone, interleukin-6 and glucocorticoids mRNA analysis and promoter characterization. Eur J Biochem 267 (2000) 5849-5857
31. Rico-Bautista E., Negrin-Martinez C., Novoa-Mogollon J., Fernandez-Perez L., and Flores-Morales A. Downregulation of the growth hormone-induced Janus kinase 2/signal transducer and activator of transcription 5 signaling pathway requires an intact actin cytoskeleton. Exp Cell Res 294 (2004) 269-280
32. Flores-Morales A., Fernandez L., Rico-Bautista E., Umana A., Negrin C., Zhang J.G., et al. Endoplasmic reticulum stress prolongs GH-induced Janus kinase (JAK2)/signal transducer and activator of transcription (STAT5) signaling pathway. Mol Endocrinol 15 (2001) 1471-1483
33. Favre H., Benhamou A., Finidori J., Kelly P.A., and Edery M. Dual effects of suppressor of cytokine signaling (SOCS-2) on growth hormone signal transduction. FEBS Lett 453 (1999) 63-66
34. Greenhalgh C.J., Metcalf D., Thaus A.L., Corbin J.E., Uren R., Morgan P.O., et al. Biological evidence that SOCS-2 can act either as an enhancer or suppressor of growth hormone signaling. J Biol Chem 277 (2002) 40181-40184
35. Miller M.E., Michaylira C.Z., Simmons J.G., Ney D.M., Dahly E.M., Heath J.K., et al. Suppressor of cytokine signaling-2: a growth hormone-inducible inhibitor of intestinal epithelial cell proliferation. Gastroenterology 127 (2004) 570-581
36. Leung K.C., Doyle N., Ballesteros M., Sjogren K., Watts C.K., Low T.H., et al. Estrogen inhibits GH signaling by suppressing GH-induced JAK2 phosphorylation, an effect mediated by SOCS-2. Proc Natl Acad Sci USA 100 (2003) 1016-1021
37. Turnley A.M. Role of SOCS2 in growth hormone actions. Trends Endocrinol Metab 16 (2005) 53-58
38. Bullock A.N., Debreczeni J.E., Edwards A.M., Sundstrom M., and Knapp S. Crystal structure of the SOCS2-Elongin C-Elongin B complex defines a prototypical SOCS box ubiquitin ligase. Proc Natl Acad Sci USA 103 (2006) 7637-7642
39. Smit L.S., Meyer D.J., Billestrup N., Norstedt G., Schwartz J., and Carter-Su C. The role of the growth hormone (GH) receptor and JAK1 and JAK2 kinases in the activation of Stats 1, 3 and 5 by GH. Mol Endocrinol 10 (1996) 519-533
40. Ram P.A., and Waxman D.J. SOCS/CIS protein inhibition of growth hormone-stimulated STAT5 signaling by multiple mechanisms. J Biol Chem 274 (1999) 35553-35561
41. Dey B.R., Spence S.L., Nissley P., and Furlanetto R.W. Interaction of human suppressor of cytokine signaling (SOCS)-2 with the insulin-like growth factor-I receptor. J Biol Chem 273 (1998) 24095-24101
42. Zong C.S., Chan J., Levy D.E., Horvath C., Sadowski H.B., and Wang L.H. Mechanism of STAT3 activation by insulin-like growth factor I receptor. J Biol Chem 275 (2000) 15099-15105
43. Fruchtman S., Simmons J.G., Michaylira C.Z., Miller M.E., Greenhalgh C.J., Ney D.M., et al. Suppressor of cytokine signaling-2 modulates the fibrogenic actions of Gh and Igf-I in intestinal mesenchymal cells. Am J Physiol Gastrointest Liver Physiol 289 (2005) G342-G350
44. Pezet A., Favre H., Kelly P.A., and Edery M. Inhibition and restoration of prolactin signal transduction by suppressors of cytokine signaling. J Biol Chem 274 (1999) 24497-24502
45. Lindeman G.J., Wittlin S., Lada H., Naylor M.J., Santamaria M., Zhang J.G., et al. SOCS1 deficiency results in accelerated mammary gland development and rescues lactation in prolactin receptor-deficient mice. Genes Dev 15 (2001) 1631-1636
46. Harris J., Stanford P.M., Sutherland K., Oakes S.R., Naylor M.J., Robertson F.G., et al. Socs2 and elf5 mediate prolactin-induced mammary gland development. Mol Endocrinol 20 (2006) 1177-1187
47. Dif F., Saunier E., Demeneix B., Kelly P.A., and Edery M. Cytokine-inducible SH2-containing protein suppresses PRL signaling by binding the PRL receptor. Endocrinology 142 (2001) 5286-5293
48. Tannahill G.M., Elliott J., Barry A.C., Hibbert L., Cacalano N.A., and Johnston J.A. SOCS2 can enhance interleukin-2 (IL-2) and IL-3 signaling by accelerating SOCS3 degradation. Mol Cell Biol 25 (2005) 9115-9126
49. Jegalian A.G., and Wu H. Differential roles of SOCS family members in EpoR signal transduction. J Interferon Cytokine Res 22 (2002) 853-860
50. Goldshmit Y., Walters C.E., Scott H.J., Greenhalgh C.J., and Turnley A.M. SOCS2 induces neurite outgrowth by regulation of epidermal growth factor receptor activation. J Biol Chem 279 (2004) 16349-16355
51. Eyckerman S., Verhee A., der Heyden J.V., Lemmens I., Ostade X.V., Vandekerckhove J., et al. Design and application of a cytokine-receptor-based interaction trap. Nat Cell Biol 3 (2001) 1114-1119
52. Shen X., Hong F., Nguyen V.A., and Gao B. IL-10 attenuates IFN-alpha-activated STAT1 in the liver: involvement of SOCS2 and SOCS3. FEBS Lett 480 (2000) 132-136
53. Lavens D, Montoye T, Piessevaux J, Zabeau L, Vandekerckhove J, Gevaert K, et al., A complex interaction pattern of CIS and SOCS2 with the leptin receptor. J Cell Sci; 2006.
54. Machado FS, Johndrow JE, Esper L, Dias A, Bafica A, Serhan CN, et al., Anti-inflammatory actions of lipoxin A(4) and aspirin-triggered lipoxin are SOCS-2 dependent. Nat Med; 2006.
55. Corva P.M., and Medrano J.F. Diet effects on weight gain and body composition in high growth (hg/hg) mice. Physiol Genomics 3 (2000) 17-23
56. Kato H, Nomura K, Osabe D, Shinohara S, Mizumori O, Katashima R, et al., Association of single-nucleotide polymorphisms in the suppressor of cytokine signaling 2 (SOCS2) gene with type 2 diabetes in the Japanese. Genomics; 2006.
57. Lorentzon M., Greenhalgh C.J., Mohan S., Alexander W.S., and Ohlsson C. Reduced bone mineral density in SOCS-2-deficient mice. Pediatr Res 57 (2005) 223-226
58. Ouyang X, Fujimoto M, Nakagawa R, Serada S, Tanaka T, Nomura S, et al. SOCS-2 interferes with myotube formation and potentiates osteoblast differentiation through upregulation of JunB in C2C12 cells. J Cell Physiol; 2006.
59. Polizzotto M.N., Bartlett P.F., and Turnley A.M. Expression of "suppressor of cytokine signalling" (SOCS) genes in the developing and adult mouse nervous system. J Comp Neurol 423 (2000) 348-358
60. Campbell I.L. Cytokine-mediated inflammation, tumorigenesis, and disease-associated JAK/STAT/SOCS signaling circuits in the CNS. Brain Res Brain Res Rev 48 (2005) 166-177
61. Turnley A.M., Faux C.H., Rietze R.L., Coonan J.R., and Bartlett P.F. Suppressor of cytokine signaling 2 regulates neuronal differentiation by inhibiting growth hormone signaling. Nat Neurosci 5 (2002) 1155-1162
62. Ransome M.I., Goldshmit Y., Bartlett P.F., Waters M.J., and Turnley A.M. Comparative analysis of CNS populations in knockout mice with altered growth hormone responsiveness. Eur J Neurosci 19 (2004) 2069-2079
63. Goldshmit Y., Greenhalgh C.J., and Turnley A.M. Suppressor of cytokine signalling-2 and epidermal growth factor regulate neurite outgrowth of cortical neurons. Eur J Neurosci 20 (2004) 2260-2266
64. Wang L., Zhang Z., Zhang R., Hafner M.S., Wong H.K., Jiao Z., et al. Erythropoietin up-regulates SOCS2 in neuronal progenitor cells derived from SVZ of adult rat. Neuroreport 15 (2004) 1225-1229
65. Naka T., Fujimoto M., Tsutsui H., and Yoshimura A. Negative regulation of cytokine and TLR signalings by SOCS and others. Adv Immunol 87 (2005) 61-122
66. Dogusan Z., Hooghe-Peters E.L., Berus D., Velkeniers B., and Hooghe R. Expression of SOCS genes in normal and leukemic human leukocytes stimulated by prolactin, growth hormone and cytokines. J Neuroimmunol 109 (2000) 34-39
67. Schultheis B., Carapeti-Marootian M., Hochhaus A., Weisser A., Goldman J.M., and Melo J.V. Overexpression of SOCS-2 in advanced stages of chronic myeloid leukemia: possible inadequacy of a negative feedback mechanism. Blood 99 (2002) 1766-1775
68. Faderl S., Harris D., Van Q., Kantarjian H.M., Talpaz M., and Estrov Z. Granulocyte-macrophage colony-stimulating factor (GM-CSF) induces antiapoptotic and proapoptotic signals in acute myeloid leukemia. Blood 102 (2003) 630-637
69. Arany I., Muldrow M., and Tyring S.K. The endogenous interferon system in anal squamous epithelial lesions with different grades from HIV-positive individuals. Int J STD AIDS 12 (2001) 229-233
70. Wikman H., Kettunen E., Seppanen J.K., Karjalainen A., Hollmen J., Anttila S., et al. Identification of differentially expressed genes in pulmonary adenocarcinoma by using cDNA array. Oncogene 21 (2002) 5804-5813
71. Sutherland K.D., Lindeman G.J., Choong D.Y., Wittlin S., Brentzell L., Phillips W., et al. Differential hypermethylation of SOCS genes in ovarian and breast carcinomas. Oncogene 23 (2004) 7726-7733
72. Hendriksen P.J., Dits N.F., Kokame K., Veldhoven A., van Weerden W.M., Bangma C.H., Trapman J., and Jenster G. Evolution of the androgen receptor pathway during progression of prostate cancer. Cancer Res 66 (2006) 5012-5020
73. Ling C., and Billig H. PRL receptor-mediated effects in female mouse adipocytes: PRL induces suppressors of cytokine signaling expression and suppresses insulin-induced leptin production in adipocytes in vitro. Endocrinology 142 (2001) 4880-4890
74. Tam S.P., Lau P., Djiane J., Hilton D.J., and Waters M.J. Tissue-specific induction of SOCS gene expression by PRL. Endocrinology 142 (2001) 5015-5026
75. Sadowski C.L., Choi T.S., Le M., Wheeler T.T., Wang L.H., and Sadowski H.B. Insulin induction of SOCS-2 and SOCS-3 mRNA expression in C2C12 skeletal muscle cells is mediated by Stat5*. J Biol Chem 276 (2001) 20703-20710
76. Jelinsky S.A., Harris H.A., Brown E.L., Flanagan K., Zhang X., Tunkey C., et al. Global transcription profiling of estrogen activity: estrogen receptor alpha regulates gene expression in the kidney. Endocrinology 144 (2003) 701-710
77. Kovanen P.E., Young L., Al-Shami A., Rovella V., Pise-Masison C.A., Radonovich M.F., et al. Global analysis of IL-2 target genes: identification of chromosomal clusters of expressed genes. Int Immunol 17 (2005) 1009-1021
78. Santangelo C., Scipioni A., Marselli L., Marchetti P., and Dotta F. Suppressor of cytokine signaling gene expression in human pancreatic islets: modulation by cytokines. Eur J Endocrinol 152 (2005) 485-489
79. Lejeune D., Demoulin J.B., and Renauld J.C. Interleukin 9 induces expression of three cytokine signal inhibitors: cytokine-inducible SH2-containing protein, suppressor of cytokine signalling (SOCS)-2 and SOCS-3, but only SOCS-3 overexpression suppresses interleukin 9 signalling. Biochem J 353 (2001) 109-116
80. Brender C., Nielsen M., Ropke C., Nissen M.H., Svejgaard A., Billestrup N., et al. Interferon-alpha induces transient suppressors of cytokine signalling expression in human T cells. Exp Clin Immunogenet 18 (2001) 80-85
81. Federici M., Giustizieri M.L., Scarponi C., Girolomoni G., and Albanesi C. Impaired IFN-gamma-dependent inflammatory responses in human keratinocytes overexpressing the suppressor of cytokine signaling 1. J Immunol 169 (2002) 434-442
82. Tone E., Kunisada K., Kumanogoh A., Negoro S., Funamoto M., Osugi T., et al. gp130-Dependent signalling pathway is not enhanced in gp130 transgenic heart after LIF stimulation. Cytokine 12 (2000) 1512-1518
83. Bjorbaek C., Elmquist J.K., El-Haschimi K., Kelly J., Ahima R.S., Hileman S., et al. Activation of SOCS-3 messenger ribonucleic acid in the hypothalamus by ciliary neurotrophic factor. Endocrinology 140 (1999) 2035-2043
84. Ziotopoulou M., Erani D.M., Hileman S.M., Bjorbaek C., and Mantzoros C.S. Unlike leptin, ciliary neurotrophic factor does not reverse the starvation-induced changes of serum corticosterone and hypothalamic neuropeptide levels but induces expression of hypothalamic inhibitors of leptin signaling. Diabetes 49 (2000) 1890-1896