SOCS6 is a selective suppressor of receptor tyrosine kinase signaling

Tumor Biology

Volumn 35, Issue 11, 2014, Pages 10581-10589

  Kabir, Nuzhat N ^a   Sun, Jianmin ^b,c   Rönnstrand, Lars ^b,c   Kazi, Julhash U ^a,b,c  

^a KN Biomedical Research Institute   (Bangladesh)

^b LUND UNIVERSITY   (Sweden)

^c LUND UNIVERSITY   (Sweden)

Author keywords

FL; FLT3; INSR; Insulin; KIT; SCF; SOCS

Indexed keywords

CD135 ANTIGEN; INSULIN RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE KINASE; STEM CELL FACTOR RECEPTOR; SUPPRESSOR OF CYTOKINE SIGNALING; SUPPRESSOR OF CYTOKINE SIGNALING 6; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; SOCS6 PROTEIN, HUMAN; SOCS6 PROTEIN, MOUSE;

APOPTOSIS; CANCER SURVIVAL; CELLULAR DISTRIBUTION; DISEASE ASSOCIATION; ENZYME BINDING; GENE ACTIVITY; GENE FUNCTION; HUMAN; INSULIN BINDING; KNOCKOUT MOUSE; NEGATIVE FEEDBACK; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING 6 GENE; TISSUE DIFFERENTIATION; TRANSGENIC MOUSE; TUMOR SUPPRESSOR GENE; AMINO ACID SEQUENCE; ANIMAL; ANTAGONISTS AND INHIBITORS; GENE EXPRESSION REGULATION; METABOLISM; MOLECULAR GENETICS; NEOPLASM; PATHOLOGY; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; GENE EXPRESSION REGULATION; HUMANS; MOLECULAR SEQUENCE DATA; NEOPLASMS; RECEPTOR PROTEIN-TYROSINE KINASES; SEQUENCE HOMOLOGY, AMINO ACID; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 84920938375     PISSN: 10104283     EISSN: 14230380     Source Type: Journal    
DOI: 10.1007/s13277-014-2542-4     Document Type: Review

References (57)

1. Kazi JU, Kabir NN, Flores-Morales A, Rönnstrand L. SOCS proteins in regulation of receptor tyrosine kinase signaling. Cell Mol Life Sci. 2014;71:3297–310.
2. Kazi JU, Rönnstrand L. Suppressor of cytokine signaling 2 (SOCS2) associates with FLT3 and negatively regulates downstream signaling. Mol Oncol. 2013;7:693–703.
3. Kazi JU, Sun J, Phung B, Zadjali F, Flores-Morales A, Rönnstrand L. Suppressor of cytokine signaling 6 (SOCS6) negatively regulates Flt3 signal transduction through direct binding to phosphorylated tyrosines 591 and 919 of Flt3. J Biol Chem. 2012;287:36509–17.
4. Zadjali F, Pike AC, Vesterlund M, Sun J, Wu C, Li SS, et al. Structural basis for c-Kit inhibition by the suppressor of cytokine signaling 6 (SOCS6) ubiquitin ligase. J Biol Chem. 2011;286:480–90.
5. Bayle J, Letard S, Frank R, Dubreuil P, De Sepulveda P. Suppressor of cytokine signaling 6 associates with Kit and regulates Kit receptor signaling. J Biol Chem. 2004;279:12249–59.
6. Matuoka K, Miki H, Takahashi K, Takenawa T. A novel ligand for an SH3 domain of the adaptor protein Nck bears an SH2 domain and nuclear signaling motifs. Biochem Biophys Res Commun. 1997;239:488–92.
7. Martens N, Wery M, Wang P, Braet F, Gertler A, Hooghe R, et al. The suppressor of cytokine signaling (SOCS)-7 interacts with the actin cytoskeleton through vinexin. Exp Cell Res. 2004;298:239–48.
8. De Sepulveda P, Okkenhaug K, Rose JL, Hawley RG, Dubreuil P, Rottapel R. Socs1 binds to multiple signalling proteins and suppresses steel factor-dependent proliferation. EMBO J. 1999;18:904–15.
9. Rui L, Yuan M, Frantz D, Shoelson S, White MF. SOCS-1 and SOCS-3 block insulin signaling by ubiquitin-mediated degradation of IRS1 and IRS2. J Biol Chem. 2002;277:42394–8.
10. Gui Y, Yeganeh M, Ramanathan S, Leblanc C, Pomerleau V, Ferbeyre G, et al. SOCS1 controls liver regeneration by regulating HGF signaling in hepatocytes. J Hepatol. 2011;55:1300–8.
11. Hafizi S, Alindri F, Karlsson R, Dahlbäck B. Interaction of Axl receptor tyrosine kinase with C1-TEN, a novel C1 domain-containing protein with homology to tensin. Biochem Biophys Res Commun. 2002;299:793–800.
12. Dey BR, Spence SL, Nissley P, Furlanetto RW. Interaction of human suppressor of cytokine signaling (SOCS)-2 with the insulin-like growth factor-I receptor. J Biol Chem. 1998;273:24095–101.
13. Xia L, Wang L, Chung AS, Ivanov SS, Ling MY, Dragoi AM, et al. Identification of both positive and negative domains within the epidermal growth factor receptor COOH-terminal region for signal transducer and activator of transcription (STAT) activation. J Biol Chem. 2002;277:30716–23.
14. Ben-Zvi T, Yayon A, Gertler A, Monsonego-Ornan E. Suppressors of cytokine signaling (SOCS) 1 and SOCS3 interact with and modulate fibroblast growth factor receptor signaling. J Cell Sci. 2006;119:380–7.
15. Sasi W, Jiang WG, Sharma A, Mokbel K. Higher expression levels of SOCS 1,3,4,7 are associated with earlier tumour stage and better clinical outcome in human breast cancer. BMC Cancer. 2010;10:178.
16. Kile BT, Alexander WS. The suppressors of cytokine signalling (SOCS). Cell Mol Life Sci. 2001;58:1627–35.
17. Li L, Gronning LM, Anderson PO, Li S, Edvardsen K, Johnston J, et al. Insulin induces SOCS-6 expression and its binding to the p85 monomer of phosphoinositide 3-kinase, resulting in improvement in glucose metabolism. J Biol Chem. 2004;279:34107–14.
18. Lai RH, Hsiao YW, Wang MJ, Lin HY, Wu CW, Chi CW, et al. SOCS6, down-regulated in gastric cancer, inhibits cell proliferation and colony formation. Cancer Lett. 2010;288:75–85.
19. Lin HY, Lai RH, Lin ST, Lin RC, Wang MJ, Lin CC, et al. Suppressor of cytokine signaling 6 (SOCS6) promotes mitochondrial fission via regulating DRP1 translocation. Cell Death Differ. 2013;20:139–53.
20. Masuhara M, Sakamoto H, Matsumoto A, Suzuki R, Yasukawa H, Mitsui K, et al. Cloning and characterization of novel CIS family genes. Biochem Biophys Res Commun. 1997;239:439–46.
21. Ram PA, Waxman DJ. SOCS/CIS protein inhibition of growth hormone-stimulated STAT5 signaling by multiple mechanisms. J Biol Chem. 1999;274:35553–61.
22. Helman D, Sandowski Y, Cohen Y, Matsumoto A, Yoshimura A, Merchav S, et al. Cytokine-inducible SH2 protein (CIS3) and JAK2 binding protein (JAB) abolish prolactin receptor-mediated STAT5 signaling. FEBS Lett. 1998;441:287–91.
23. Nicholson SE, Willson TA, Farley A, Starr R, Zhang JG, Baca M, et al. Mutational analyses of the SOCS proteins suggest a dual domain requirement but distinct mechanisms for inhibition of LIF and IL-6 signal transduction. EMBO J. 1999;18:375–85.
24. Lai RH, Wang MJ, Yang SH, Chen JY. Genomic organization and functional characterization of the promoter for the human suppressor of cytokine signaling 6 gene. Gene. 2009;448:64–73.
25. Dowton SB, Hing AV, Sheen-Kaniecki V, Watson MS. Chromosome 18q22.2 → qter deletion and a congenital anomaly syndrome with multiple vertebral segmentation defects. J Med Genet. 1997;34:414–7.
26. Yoon S, Yi YS, Kim SS, Kim JH, Park WS, Nam SW. SOCS5 and SOCS6 have similar expression patterns in normal and cancer tissues. Tumour Biol J Int Soc Oncodevelopmental Biol Med. 2012;33:215–21.
27. Hwang MN, Ha TH, Park J, Shim J, Lee H, Kim YN, et al. Increased SOCS6 stability with PMA requires its N-terminal region and the Erk pathway via PKC delta activation. Biochem Biophys Res Commun. 2007;354:184–9.
28. Kazi JU, Kabir NN, Rönnstrand L. Protein kinase C (PKC) as a drug target in chronic lymphocytic leukemia. Med Oncol. 2013;30:757.
29. Kazi JU. The mechanism of protein kinase C regulation. Front Biol. 2011;6:328–36.
30. Kazi JU, Kim CR, Soh JW. Subcellular localization of diacylglycerol-responsive protein kinase C isoforms in HeLa cells. Bull Kor Chem Soc. 2009;30:1981–4.
31. Kazi JU, Soh JW. Role of regulatory domain mutants of PKC isoforms in c-fos induction. Bull Kor Chem Soc. 2008;29:252–4.
32. Kazi JU, Soh JW. Induction of the nuclear proto-oncogene c-fos by the phorbol ester TPA and v-H-Ras. Mol Cells. 2008;26:462–7.
33. 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;33:1364–70.
34. Storojeva I, Boulay JL, Ballabeni P, Buess M, Terracciano L, Laffer U, et al. Prognostic and predictive relevance of DNAM-1, SOCS6 and CADH-7 genes on chromosome 18q in colorectal cancer. Oncology. 2005;68:246–55.
35. Sriram KB, Larsen JE, Savarimuthu Francis SM, Wright CM, Clarke BE, Duhig EE, et al. Array-comparative genomic hybridization reveals loss of SOCS6 is associated with poor prognosis in primary lung squamous cell carcinoma. PLoS One. 2012;7:e30398.
36. Qiu X, Zheng J, Guo X, Gao X, Liu H, Tu Y, et al. Reduced expression of SOCS2 and SOCS6 in hepatocellular carcinoma correlates with aggressive tumor progression and poor prognosis. Mol Cell Biochem. 2013;378:99–106.
37. Wu K, Hu G, He X, Zhou P, Li J, He B, et al. MicroRNA-424-5p suppresses the expression of SOCS6 in pancreatic cancer. Pathol Oncol Res POR. 2013;19:739–48.
38. Tanaka T, Arai M, Jiang X, Sugaya S, Kanda T, Fujii K, et al. Downregulation of microRNA-431 by human interferon-beta inhibits viability of medulloblastoma and glioblastoma cells via upregulation of SOCS6. Int J Oncol. 2014;44:1685–90.
39. Wu Q, Luo G, Yang Z, Zhu F, An Y, Shi Y, et al. Mir-17-5p promotes proliferation by targeting SOCS6 in gastric cancer cells. FEBS Lett. 2014;588:2055–62.
40. Mooney RA, Senn J, Cameron S, Inamdar N, Boivin LM, Shang Y, et al. Suppressors of cytokine signaling-1 and -6 associate with and inhibit the insulin receptor. A potential mechanism for cytokine-mediated insulin resistance. J Biol Chem. 2001;276:25889–93.
41. Guo S. Insulin signaling, resistance, and the metabolic syndrome: insights from mouse models into disease mechanisms. J Endocrinol. 2014;220:T1–23.
42. Krebs DL, Uren RT, Metcalf D, Rakar S, Zhang JG, Starr R, et al. SOCS-6 binds to insulin receptor substrate 4, and mice lacking the SOCS-6 gene exhibit mild growth retardation. Mol Cell Biol. 2002;22:4567–78.
43. Banks AS, Li J, McKeag L, Hribal ML, Kashiwada M, Accili D, et al. Deletion of SOCS7 leads to enhanced insulin action and enlarged islets of Langerhans. J Clin Invest. 2005;115:2462–71.
44. Ueki K, Fruman DA, Yballe CM, Fasshauer M, Klein J, Asano T, et al. Positive and negative roles of p85 alpha and p85 beta regulatory subunits of phosphoinositide 3-kinase in insulin signaling. J Biol Chem. 2003;278:48453–66.
45. Ueki K, Fruman DA, Brachmann SM, Tseng YH, Cantley LC, Kahn CR. Molecular balance between the regulatory and catalytic subunits of phosphoinositide 3-kinase regulates cell signaling and survival. Mol Cell Biol. 2002;22:965–77.
46. Kabir NN, Kazi JU. Grb10 is a dual regulator of receptor tyrosine kinase signaling. Mol Biol Rep. 2014;41:1985–92.
47. Sattler M, Salgia R, Shrikhande G, Verma S, Pisick E, Prasad KV, et al. Steel factor induces tyrosine phosphorylation of CRKL and binding of CRKL to a complex containing c-Kit, phosphatidylinositol 3-kinase, and p120(CBL). J Biol Chem. 1997;272:10248–53.
48. Fang D, Wang HY, Fang N, Altman Y, Elly C, Liu YC. Cbl-b, a RING-type E3 ubiquitin ligase, targets phosphatidylinositol 3-kinase for ubiquitination in T cells. J Biol Chem. 2001;276:4872–8.
49. Lennartsson J, Rönnstrand L. Stem cell factor receptor/c-Kit: from basic science to clinical implications. Physiol Rev. 2012;92:1619–49.
50. Kazi JU, Agarwal S, Sun J, Bracco E, Rönnstrand L. Src-like-adaptor protein (SLAP) differentially regulates normal and oncogenic c-Kit signaling. J Cell Sci. 2014;127:653–62.
51. Sun J, Mohlin S, Lundby A, Kazi JU, Hellman U, Påhlman S, et al. The PI3-kinase isoform p110delta is essential for cell transformation induced by the D816V mutant of c-Kit in a lipid-kinase-independent manner. Oncogene. 2013. doi:10.1038/onc.2013.479.
52. Kazi JU, Vaapil M, Agarwal S, Bracco E, Påhlman S, Rönnstrand L. The tyrosine kinase CSK associates with FLT3 and c-Kit receptors and regulates downstream signaling. Cell Signal. 2013;25:1852–60.
53. Kazi JU, Kabir NN, Soh JW. Bioinformatic prediction and analysis of eukaryotic protein kinases in the rat genome. Gene. 2008;410:147–53.
54. Kabir NN, Rönnstrand L, Kazi JU. Flt3 mutations in patients with childhood acute lymphoblastic leukemia (ALL). Med Oncol. 2013;30:462.
55. Ben-Yair L, Slaaby R, Herman A, Cohen Y, Biener E, Moran N, et al. Preparation and expression of biologically active prolactin and growth hormone receptors and suppressor of cytokine signaling proteins 1, 2, 3, and 6 tagged with cyan and yellow fluorescent proteins. Protein Expr Purif. 2002;25:456–64.
56. Hwang MN, Min CH, Kim HS, Lee H, Yoon KA, Park SY, et al. The nuclear localization of SOCS6 requires the N-terminal region and negatively regulates Stat3 protein levels. Biochem Biophys Res Commun. 2007;360:333–8.
57. Bayle J, Lopez S, Iwai K, Dubreuil P, De Sepulveda P. The E3 ubiquitin ligase HOIL-1 induces the polyubiquitination and degradation of SOCS6 associated proteins. FEBS Lett. 2006;580:2609–14.