The suppressors of cytokine signalling E3 ligases behave as tumour suppressors

Biochemical Society Transactions

Volumn 36, Issue 3, 2008, Pages 464-468

  Elliott, Joanne ^a   Hookham, Michelle B ^a   Johnston, James A ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

Cancer; Cytokine signalling; E3 ubiquitin ligase; Suppressor of cytokine signalling (SOCS); Tumorigenesis; Tumour suppressor

Indexed keywords

CYTOKINE; JANUS KINASE; JANUS KINASE 2; SUPPRESSOR OF CYTOKINE SIGNALING; SUPPRESSOR OF CYTOKINE SIGNALING 1; SUPPRESSOR OF CYTOKINE SIGNALING 2; SUPPRESSOR OF CYTOKINE SIGNALING 3; UBIQUITIN PROTEIN LIGASE E3;

CONFERENCE PAPER; ENZYME PHOSPHORYLATION; ENZYME REGULATION; ENZYME REPRESSION; GENE MUTATION; METHYLATION; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR SUPPRESSOR GENE;

ANIMALS; HUMANS; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN-PROTEIN LIGASES;

EID: 45249103554     PISSN: 03005127     EISSN: None     Source Type: Journal    
DOI: 10.1042/BST0360464     Document Type: Conference Paper

References (72)

1. Shuai, K. and Liu, B. (2003) Regulation of JAK-STAT signalling in the immune system. Nat. Rev. Immunol. 3, 900-911
2. Yoshimura, A., Naka, T. and Kubo, M. (2007) SOCS proteins, cytokine signalling and immune regulation. Nat. Rev. Immunol. 7, 454-465
3. Elliott, J. and Johnston, J.A. (2004) SOCS: role in inflammation, allergy and homeostasis. Trends Immunol. 25, 434-440
4. Hilton, D.J., Richardson, R.T., Alexander, W.S., Viney, E.M., Willson, T.A., Sprigg, N.S., Starr, R., Nicholson, S.E., Metcalf, D. and Nicola, N.A. (1998) Twenty proteins containing a C-terminal SOCS box form five structural classes. Proc. Natl. Acad. Sci. U.S.A. 95, 114-119
5. Narazaki, M., Fujimoto, M., Matsumoto, T., Morita, Y., Saito, H., Kajita, T., Yoshizaki, K., Naka, T. and Kishimoto, T. (1998) Three distinct domains of SSI-1/SOCS-1/JAB protein are required for its suppression of interleukin 6 signaling. Proc. Natl. Acad. Sci. U.S.A. 95, 13130-13134
6. Yasukawa, H., Misawa, H., Sakamoto, H., Masuhara, M., Sasaki, A., Wakioka, T., Ohtsuka, S., Imaizumi, T., Matsuda, T., Ihle, J.N. and Yoshimura, A. (1999) The JAK-binding protein JAB inhibits Janus tyrosine kinase activity through binding in the activation loop. EMBO J. 18, 1309-1320
7. Kamura, T., Sato, S., Haque, D., Liu, L., Kaelin, Jr, W.G., Conaway, R.C. and Conaway, J.W. (1998) The elongin · BC complex interacts with the conserved SOCS-box motif present in members of the SOCS, ras, WD-40 repeat, and ankyrin repeat families. Genes Dev. 12, 3872-3881
8. Naka, T., Matsumoto, T., Narazaki, M., Fujimoto, M., Morita, Y., Ohsawa, Y., Saito, H., Nagasawa, T., Uchiyama, Y. and Kishimoto, T. (1998) Accelerated apoptosis of lymphocytes by augmented induction of bax in SSI-1 (STAT-induced STAT inhibitor-1) deficient mice. Proc. Natl. Acad. Sci. U.S.A. 95, 15577-15582
9. Starr, R., Metcalf, D., Elefanty, A.G., Brysha, M., Willson, T.A., Nicola, N.A., Hilton, D.J. and Alexander, W.S. (1998) Liver degeneration and lymphoid deficiencies in mice lacking suppressor of cytokine signaling-1. Proc. Natl. Acad. Sci. U.S.A. 95, 14395-14399
10. Metcalf, D., Mifsud, S., Di Rago, L., Nicola, N.A., Hilton, D.J. and Alexander, W.S. (2002) Polycystic kidneys and chronic inflammatory lesions are the delayed consequences of loss of the suppressor of cytokine signaling-1 (SOCS-1). Proc. Natl. Acad. Sci. U.S.A. 99, 943-948
11. Metcalf, D., Greenhalgh, C.J., Viney, E., Willson, T.A., Starr, R., Nicola, N.A., Hilton, D.J. and Alexander, W.S. (2000) Gigantism in mice lacking suppressor of cytokine signalling-2. Nature 405, 1069-1073
12. Greenhalgh, C.J., Bertolino, P., Asa, S.L., Metcalf, D., Corbin, J.E., Adams, T.E., Davey, H.W., Nicola, N.A., Hilton, D.J. and Alexander, W.S. (2002) 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, 1394-1406
13. Greenhalgh, C.J., Metcalf, D., Thaus, A.L., Corbin, J.E., Uren, R., Morgan, P.O., Fabri, L.J., Zhang, J.G., Martin, H.M., Willson, T.A. 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
14. Tannahill, G.M., Elliott, J., Barry, A.C., Hibbert, L., Cacalano, N.A. and Johnston, J.A. (2005) SOCS2 can enhance interleukin-2 (IL-2) and IL-3 signaling by accelerating SOCS3 degradation. Mol. Cell. Biol. 25, 9115-9126
15. Rico-Bautista, E., Flores-Morales, A. and Fernández-Pérez, L. (2006) Suppressor of cytokine signaling (SOCS) 2, a protein with multiple functions. Cytokine Growth Factor Rev. 17, 431-439
16. Lehmann, U., Schmitz, J., Weissenbach, M., Sobota, R.M., Hortner, M., Friederichs, K., Behrmann, I., Tsiaris, W., Sasaki, A., Schneider-Mergener, J. et al. (2003) SHP2 and SOCS3 contribute to Tyr-759-dependent attenuation of interleukin-6 signaling through gp130. J. Biol. Chem. 278, 661-671
17. 985. J. Biol. Chem. 275, 40649-40657
18. Sasaki, A., Yasukawa, H., Shouda, T., Kitamura, T., Dikic, I. and Yoshimura, A. (2000) CIS3/SOCS-3 suppresses erythropoietin (EPO) signaling by binding the EPO receptor and JAK2. J. Biol. Chem. 275, 29338-29347
19. Roberts, A.W., Robb, L., Rakar, S., Hartley, L., Cluse, L., Nicola, N.A., Metcalf, D., Hilton, D.J. and Alexander, W.S. (2001) Placental defects and embryonic lethality in mice lacking suppressor of cytokine signaling 3. Proc. Natl. Acad. Sci. U.S.A. 98, 9324-9329
20. Takahashi, Y., Carpino, N., Cross, J.C., Torres, M., Parganas, E. and Ihle, J.N. (2003) SOCS3: An essential regulator of LIF receptor signaling in trophoblast giant cell differentiation. EMBO J. 22, 372-384
21. 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
22. Suzuki, A., Hanada, T., Mitsuyama, K., Yoshida, T., Kamizono, S., Hoshino, T., Kubo, M., Yamashita, A., Okabe, M., Takeda, K. et al. (2001) CIS3/SOCS3/SSI3 plays a negative regulatory role in STAT3 activation and intestinal inflammation. J. Exp. Med. 193, 471-481
23. 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 regulator SOCS3/CIS3 as a therapeutic strategy for treating inflammatory arthritis. J. Clin. Invest. 108, 1781-1788
24. H2-mediated allergic responses. Nat. Med. 9, 1047-1054
25. Ozaki, A., Seki, Y., Fukushima, A. and Kubo, M. (2005) The control of allergic conjunctivitis by suppressor of cytokine signaling (SOCS)3 and SOCS5 in a murine model. J. Immunol. 175, 5489-5497
26. Yoshimura, A., Naka, T. and Kubo, M. (2007) SOCS proteins, cytokine signalling and immune regulation. Nat. Rev. Immunol. 7, 454-465
27. Kishimoto, T. and Kikutani, H. (2001) Knocking the SOCS off a tumor suppressor. Nat. Genet. 28, 4-5
28. Ventura, A., Kirsch, D.G., McLaughlin, M.E., Tuveson, D.A., Grimm, J., Lintault, L., Newman, J., Reczek, E.E., Weissleder, R. and Jacks, T. (2007) Restoration of p53 function leads to tumour regression in vivo. Nature 445, 661-665
29. Hanahan, D. and Weinberg, R.A. (2000) The hallmarks of cancer. Cell 100, 57-70
30. Sotillo, R., Hernando, E., Diaz-Rodriguez, E., Teruya-Feldstein, J., Cordon-Cardo, C., Lowe, S.W. and Benezra, R. (2007) Mad2 overexpression promotes aneuploidy and tumorigenesis in mice. Cancer Cell 11, 9-23
31. Zheng, L. and Lee, W.H. (2002) Retinoblastoma tumor suppressor and genome stability. Adv. Cancer Res. 85, 13-50
32. Mazoyer, S. (2005) Genomic rearrangements in the BRCA1 and BRCA2 genes. Hum. Mutat. 25, 415-422
33. Barth, T.F., Melzner, I., Wegener, S., Bucur, A.J., Bruderlein, S., Dorsch, K., Hasel, C., Leithauser, F. and Moller, P. (2005) Biallelic mutation of SOCS-1 impairs JAK2 degradation and sustains phospho-JAK2 action in MedB-1 mediastinal lymphoma line. Verh. Dtsch. Ges. Pathol. 89, 234-244
34. Melzner, I., Weniger, M.A., Bucur, A.J., Bruderlein, S., Dorsch, K., Hasel, C., Leithauser, F., Ritz, O., Dyer, M.J., Barth, T.F. and Moller, P. (2006) Biallelic deletion within 16p13.13 including SOCS-1 in Karpas1106P mediastinal B-cell lymphoma line is associated with delayed degradation of JAK2 protein. Int. J. Cancer 118, 1941-1944
35. Weniger, M.A., Melzner, I., Menz, C.K., Wegener, S., Bucur, A.J., Dorsch, K., Mattfeldt, T., Barth, T.F. and Moller, P. (2006) Mutations of the tumor suppressor gene SOCS-1 in classical Hodgkin lymphoma are frequent and associated with nuclear phospho-STAT5 accumulation. Oncogene 25, 2679-2684
36. Ungureanu, D., Saharinen, P., Junttila, I., Hilton, D.J. and Silvennoinen, O. (2002) Regulation of Jak2 through the ubiquitin-proteasome pathway involves phosphorylation of Jak2 on Y1007 and interaction with SOCS-1. Mol. Cell. Biol. 22, 3316-3326
37. Esteller, M. (2007) Epigenetics provides a new generation of oncogenes and tumour-suppressor genes. Br. J. Cancer 96, (Suppl.), R26-R30
38. Peng, B., Hodge, D.R., Thomas, S.B., Cherry, J.M., Munroe, D.J., Pompeia, C., Xiao, W. and Farrar, W.L. (2005) Epigenetic silencing of the human nucleotide excision repair gene, hHR23B, in interleukin-6-responsive multiple myeloma KAS-6/1 cells. J. Biol. Chem. 280, 4182-4187
39. Wehbe, H., Henson, R., Meng, F., Mize-Berge, J. and Patel, T. (2006) Interleukin-6 contributes to growth in cholangiocarcinoma cells by aberrant promoter methylation and gene expression. Cancer Res. 66, 10517-10524
40. Oshimo, Y., Kuraoka, K., Nakayama, H., Kitadai, Y., Yoshida, K., Chayama, K. and Yasui, W. (2004) Epigenetic inactivation of SOCS-1 by CpG island hypermethylation in human gastric carcinoma. Int. J. Cancer 112, 1003-1009
41. Yang, B., Guo, M., Herman, J.G. and Clark, D.P. (2003) Aberrant promoter methylation profiles of tumor suppressor genes in hepatocellular carcinoma. Am. J. Pathol. 163, 1101-1107
42. Brakensiek, K., Langer, F., Schlegelberger, B., Kreipe, H. and Lehmann, U. (2005) Hypermethylation of the suppressor of cytokine signalling-1 (SOCS-1) in myelodysplastic syndrome. Br. J. Haematol. 130, 209-217
43. Fukushima, N., Sato, N., Sahin, F., Su, G.H., Hruban, R.H. and Goggins, M. (2003) Aberrant methylation of suppressor of cytokine signalling-1 (SOCS-1) gene in pancreatic ductal neoplasms. Br. J. Cancer 89, 338-343
44. Sutherland, K.D., Lindeman, G.J., Choong, D.Y., Wittlin, S., Brentzell, L., Phillips, W., Campbell, I.G. and Visvader, J.E. (2004) Differential hypermethylation of SOCS genes in ovarian and breast carcinomas. Oncogene 23, 7726-7733
45. Yoshida, T., Ogata, H., Kamio, M., Joo, A., Shiraishi, H., Tokunaga, Y., Sata, M., Nagai, H. and Yoshimura, A. (2004) SOCS1 is a suppressor of liver fibrosis and hepatitis-induced carcinogenesis. J. Exp. Med. 199, 1701-1707
46. Miyoshi, H., Fujie, H., Shintani, Y., Tsutsumi, T., Shinzawa, S., Makuuchi, M., Kokudo, N., Matsuura, Y., Suzuki, T., Miyamura, T. et al. (2005) Hepatitis C virus core protein exerts an inhibitory effect on suppressor of cytokine signaling (SOCS)-1 gene expression. J. Hepatol. 43, 757-763
47. Weber, A., Hengge, U.R., Bardenheuer, W., Tischoff, I., Sommerer, F., Markwarth, A., Dietz, A., Wittekind, C. and Tannapfel, A. (2005) SOCS-3 is frequently methylated in head and neck squamous cell carcinoma and its precursor lesions and causes growth inhibition. Oncogene 24, 6699-6708
48. Niwa, Y., Kanda, H., Shikauchi, Y., Saiura, A., Matsubara, K., Kitagawa, T., Yamamoto, J., Kubo, T. and Yoshikawa, H. (2005) Methylation silencing of SOCS-3 promotes cell growth and migration by enhancing JAK/STAT and FAK signalings in human hepatocellular carcinoma. Oncogene 24, 6406-6417
49. He, B., You, L., Xu, Z., Mazieres, J., Lee, A.Y. and Jablons, D.M. (2004) Activity of the suppressor of cytokine signaling-3 promoter in human non-small-cell lung cancer. Clin. Lung Cancer 5, 366-370
50. Li, Z., Metze, D., Nashan, D., Muller-Tidow, C., Serve, H. L., Poremba, C., Luger, T.A. and Bohm, M. (2004) Expression of SOCS-1, suppressor of cytokine signalling-1, in human melanoma. J. Invest. Dermatol. 123, 737-745
51. Roman-Gomez, J., Jimenez-Velasco, A., Castillejo, J.A., Cervantes, F., Barrios, M., Colomer, D., Heiniger, A. and Torres, A. (2004) The suppressor of cytokine signaling-1 is constitutively expressed in chronic myeloid leukemia and correlates with poor cytogenetic response to interferon-α. Haematologica 89, 42-48
52. Raccurt, M., Tam, S.P., Lau, P., Mertani, H.C., Lambert, A., Garcia-Caballero, T., Li, H., Brown, R.J., McGuckin, M.A., Morel, G. and Waters, M.J. (2003) Suppressor of cytokine signalling gene expression is elevated in breast carcinoma. Br. J. Cancer 89, 524-532
53. Komyod, W., Bohm, M., Metze, D., Heinrich, P.C. and Behrmann, I. (2007) Constitutive suppressor of cytokine signaling 3 expression confers a growth advantage to a human melanoma cell line. Mol. Cancer Res. 5, 271-281
54. Zhang, J.G., Farley, A., Nicholson, S.E., Willson, T.A., Zugaro, L.M., Simpson, R.J., Moritz, R.L., Cary, D., Richardson, R., Hausmann, G. et al. (1999) The conserved SOCS box motif in suppressors of cytokine signaling binds to elongins B and C and may couple bound proteins to proteasomal degradation. Proc. Natl. Acad. Sci. U.S.A. 96, 2071-2076
55. Limnander, A., Danial, N.N. and Rothman, P.B. (2004) v-Abl signaling disrupts SOCS-1 function in transformed pre-B cells. Mol. Cell 15, 329-341
56. White, E. (2003) The pims and outs of survival signaling: role for the Pim-2 protein kinase in the suppression of apoptosis by cytokines. Genes Dev. 17, 1813-1816
57. Mikkers, H., Nawijn, M., Allen, J., Brouwers, C., Verhoeven, E., Jonkers, J. and Berns, A. (2004) Mice deficient for all PIM kinases display reduced body size and impaired responses to hematopoietic growth factors. Mol. Cell. Biol. 24, 6104-6115
58. Amaravadi, R. and Thompson, C.B. (2005) The survival kinases Akt and Pim as potential pharmacological targets. J. Clin. Invest. 115, 2618-2624
59. Chen, X.P., Losman, J.A., Cowan, S., Donahue, E., Fay, S., Vuong, B.Q., Nawijn, M.C., Capece, D., Cohan, V.L. and Rothman, P. (2002) Pim serine/threonine kinases regulate the stability of Socs-1 protein. Proc. Natl. Acad. Sci. U.S.A. 99, 2175-2180
60. Adam, M., Pogacic, V., Bendit, M., Chappuis, R., Nawijn, M.C., Duyster, J., Fox, C.J., Thompson, C.B., Cools, J. and Schwaller, J. (2006) Targeting PIM kinases impairs survival of hematopoietic cells transformed by kinase inhibitor-sensitive and kinase inhibitor-resistant forms of Fms-like tyrosine kinase 3 and BCR/ABL. Cancer Res. 66, 3828-3835
61. Chen, J.L., Limnander, A. and Rothman, P.B. (2007) Pim-1 and Pim-2 kinases are required for efficient pre-B cell transformation by v-Abl oncogene. Blood 111, 1677-1685
62. Haan, S., Ferguson, P., Sommer, U., Hiremath, M., McVicar, D.W., Heinrich, P.C., Johnston, J.A. and Cacalano, N.A. (2003) Tyrosine phosphorylation disrupts elongin interaction and accelerates SOCS3 degradation. J. Biol. Chem. 278, 31972-31979
63. Cacalano, N.A., Sanden, D. and Johnston, J.A. (2001) Tyrosine- phosphorylated SOCS-3 inhibits STAT activation but binds to p120 RasGAP and activates Ras. Nat. Cell Biol. 3, 460-465
64. Hookham, M.B., Elliott, J., Suessmuth, Y., Staerk, J., Ward, A.C., Vainchenker, W., Percy, M.J., McMullin, M.F., Constantinescu, S.N. and Johnston, J.A. (2007) The myeloproliferative disorder-associated JAK2 V617F mutant escapes negative regulation by suppressor of cytokine signaling 3. Blood 109, 4924-4929
65. Baxter, E.J., Scott, L.M., Campbell, P.J., East, C., Fourouclas, N., Swanton, S., Vassiliou, G.S., Bench, A.J., Boyd, E.M., Curtin, N. et al. (2005) Acquired mutation of the tyrosine kinase JAK2 in human myeloproliferative disorders. Lancet 365, 1054-1061
66. Kralovics, R., Passamonti, F., Buser, A.S., Teo, S.S., Tiedt, R., Passweg, J.R., Tichelli, A., Cazzola, M. and Skoda, R.C. (2005) A gain-of-function mutation of JAK2 in myeloproliferative disorders. N. Engl. J. Med. 352, 1779-1790
67. Levine, R.L., Wadleigh, M., Cools, J., Ebert, B.L., Wernig, G., Huntly, B.J., Boggon, T.J., Wlodarska, I., Clark, J.J., Moore, S. et al. (2005) Activating mutation in the tyrosine kinase JAK2 in polycythemia vera, essential thrombocythemia, and myeloid metaplasia with myelofibrosis. Cancer Cell 7, 387-397
68. James, C., Ugo, V., Le Couedic, J.P., Staerk, J., Delhommeau, F., Lacout, C., Garcon, L., Raslova, H., Berger, R., Bennaceur-Griscelli, A. et al. (2005) A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera. Nature 434, 1144-1148
69. Zhao, R., Xing, S., Li, Z., Fu, X., Li, Q., Krantz, S.B. and Zhao, Z.J. (2005) Identification of an acquired JAK2 mutation in polycythemia vera. J. Biol. Chem. 280, 22788-22792
70. Hortner, M., Nielsch, U., Mayr, L.M., Heinrich, P.C. and Haan, S. (2002) A new high affinity binding site for suppressor of cytokine signaling-3 on the erythropoietin receptor. Eur. J. Biochem. 269, 2516-2526
71. Schultheis, B., Carapeti-Marootian, M., Hochhaus, A., Weisser, A., Goldman, J.M. and Melo, J.V. (2002) Overexpression of SOCS-2 in advanced stages of chronic myeloid leukemia: possible inadequacy of a negative feedback mechanism. Blood 99, 1766-1775
72. Roman-Gomez, J., Jimenez-Velasco, A., Castillejo, J.A., Cervantes, F., Barrios, M., Colomer, D., Heiniger, A. and Torres, A. (2004) The suppressor of cytokine signaling-1 is constitutively expressed in chronic myeloid leukemia and correlates with poor cytogenetic response to interferon-α. Haematologica 89, 42-48