SOCS1 is a critical inhibitor of interferon γ signaling and prevents the potentially fatal neonatal actions of this cytokine

Cell

Volumn 98, Issue 5, 1999, Pages 597-608

  Alexander, Warren S ^a   Starr, Robyn ^a   Fenner, Jennifer E ^b   Scott, Clare L ^a   Handman, Emanuela ^a   Sprigg, Naomi S ^a   Corbin, Jason E ^a   Cornish, Ann L ^a   Darwiche, Rima ^a   Owczarek, Catherine M ^b   Kay, Thomas W H ^a   Nicola, Nicos A ^a   Hertzog, Paul J ^b   Metcalf, Donald ^a   Hilton, Douglas J ^a  

^a ROYAL MELBOURNE HOSPITAL   (Australia)

^b MONASH MEDICAL CENTRE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GAMMA INTERFERON;

ANIMAL EXPERIMENT; ARTICLE; HEMATOPOIESIS; INFECTION PREVENTION; INHIBITION KINETICS; LEISHMANIA MAJOR; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; VIRUS INFECTION;

ANIMALIA; LEISHMANIA MAJOR;

EID: 0033520326     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)80047-1     Document Type: Article

References (66)

1. Adams, T.E., Hansen, J.A., Starr, R., Nicola, N.A., Hilton, D.J., and Billestrup, N. (1998). Growth hormone preferentially induces the rapid, transient expression of SOCS-3, a novel inhibitor of cytokine receptor signaling. J. Biol. Chem. 273, 1285-1287.
2. Alexander, W.S., Metcalf, D., and Dunn, A.R. (1995). Point mutations within a dimer interface homology domain of c-mpl induce constitutive receptor activity and tumorogenesis. EMBO J. 14, 5569-5578.
3. Ando, K., Moriyama, T., Guidotti, LG., Wirth, S., Schreiber, R.D., Schlicht, H.J., Huang, S.N., and Chisari, F.V. (1993). Mechanisms of class I restricted immunopathology. A transgenic mouse model of fulminant hepatitis. J. Exp. Med. 178, 1541-1554.
4. Auernhammer, C.J., Chesnokova, V., Bousquet, C., and Melmed, S. (1998). Pituitary corticotroph SOCS-3: novel intracellular regulation of leukemia-inhibitory factor-mediated proopiomelanocortin gene expression and adrenocorticotropin secretion. Mol. Endocrinol. 12, 954-961.
5. Bach, E.A., Aguet, M., and Schreiber, R.D. (1997). The IFN gamma receptor: a paradigm for cytokine receptor signaling. Annu. Rev. Immunol. 15, 563-591.
6. Billiau, A. (1996). Interferon-gamma: biology and role in pathogenesis. Adv. Immunol. 62, 61-130.
7. Billiau, A., and Vandekerckhove, F. (1991). Cytokines and their interactions with other inflammatory mediators in the pathogenesis of sepsis and septic shock. Eur. J. Clin. Inv. 21, 559-573.
8. Bjorbaek, C., Elmquist, J.K., Frantz, J.D., Shoelson, S.E., and Flier, U.S. (1998). Identification of SOCS-3 as a potential mediator of central leptin resistance. Mol. Cell 1, 619-625.
9. Boehm, U., Klamp, T., Groot, M., and Howard, J.C. (1997). Cellular responses to interferon-gamma. Annu. Rev. Immunol. 15, 749-795.
10. Dalton, D.K., Pitts-Meek, S., Keshav, S., Figari, I.S., Bradley, A., and Stewart, T. A. (1993). Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 259, 1739-1742.
11. Darnell, J.E., Jr. (1997). STATs and gene regulation. Science 277, 1630-1635.
12. Darnell, J.E., Jr., Kerr, I.M., and Stark, G.R. (1994). Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264, 1415-1421.
13. De Maeyer, E., and De Maeyer-Guignard, S. (1998). Interferons. In The Cytokine Handbook, A. Thomson, ed. (San Diego, CA: Academic Press), pp. 491-516.
14. De Sepulveda, P., Okkenhaug, K., La Rose, J., Hawley, R.G., Dubreuil, P., and Rottapel, R. (1999). Socs1 binds to multiple signaling proteins and suppresses Steel factor dependent proliferation. EMBO J. 18, 904-915.
15. Durbin, J.E., Hackenmiller, R., Simon, M.C., and Levy, D.E. (1996). Targeted disruption of the mouse Stal1 gene results in compromised innate immunity to viral disease. Cell 84, 443-450.
16. Endo, T.A., 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.
17. Greenlund, A.C., Farrar, M.A., Viviano, B.L., and Schreiber, R.D. (1994). Ligand-induced IFN gamma receptor tyrosine phosphorylation couples the receptor to its signal transduction system (p91). EMBO J. 13, 1591-1600.
18. Gresser, I. (1982). Can Interferon induce disease? Interferon 4, 95-127.
19. Gresser, I., Aguet, M., Morel-Maroger, L, Woodrow, D., Puvion-Dutilleul, F., Guillon, J.C., and Maury, C. (1981). Electrophoretically pure mouse interferon inhibits growth, induces liver and kidney lesions, and kills suckling mice. Am. J. Pathol. 102, 396-402.
20. Gresser, I., Woodrow, D., Moss, J., Maury, C., Tavernier, J., and Fiers, W. (1987). Toxic effects of recombinant tumor necrosis factor in suckling mice. Comparisons with interferon alpha/beta. Am. J. Pathol. 128, 13-18.
21. Handman, E. (1983). Association of serum proteins with cultured Leishmania: a warning note. Parasite Immunol. 5, 109-112.
22. Heim, M.H., Kerr, I.M., Stark, G.R., and Darnell, J.E., Jr. (1995). Contribution of STAT SH2 groups to specific interferon signaling by the Jak-STAT pathway. Science 267, 1347-1349.
23. Hemmi, S., Bohni, R., Stark, G., Di Marco, F., and Aguet, M. (1994). A novel member of the interferon receptor family complements functionality of the murine interferon gamma receptor in human cells. Cell 76, 803-810.
24. Hertzog, P.J., Wright, A., Harris, G., Linnane A.W., and Mackay, I.R. (1991). Intermittent interferonemia and interferon responses in multiple sclerosis. Clin. Immunol. Immunopathol. 58, 18-32.
25. 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. USA 95, 114-119.
26. Huang, S., Hendriks, W., Althage, A., Hemmi, S., Bluethmann, H., Kamijo, R., Vilcek, J., Zinkernagel, R.M., and Aguet, M. (1993). Immune response in mice that lack the interferon-gamma receptor. Science 259, 1742-1745.
27. Igarashi, K., Garotta, G., Ozmen, L., Ziemiecki, A., Wilks, A.F., Harpur, A.G., Larner, A.C., and Finbloom, D.S. (1994). Interferon-gamma induces tyrosine phosphorylation of interferon-gamma receptor and regulated association of protein tyrosine kinases, Jak1 and Jak2, with its receptor. J. Biol. Chem. 269, 14333-14336.
28. Ihle, J.N., Witthuhn, B.A., Quelle, F.W., Yamamoto, K., Thierfelder, W.E., Kreider, B., and Silvennoinen, O. (1994). Signaling by the cytokine receptor superfamily: JAKs and STATs. Trends Biochem. Sci. 19, 222-227.
29. Ito, S., Ansari, P., Sakatsume, M., Dickensheets, H., Vasquez, N., Donnelly, R.P., Larner, A.C., and Finbloom, D.S. (1999). Interleukin-10 inhibits expression of both interferonα- and interferon γ-induced genes by suppressing tyrosine phosphorylation of STAT1. Blood 93, 1-9.
30. Kamijo, R., Harada, H., Matsuyama, T., Bosland, M., Gerecitano, J., Shapiro, D., Le, J., Koh, S.I., Kimura, T., Green, S.J., et al. (1994). Requirement for transcription factor IRF-1 in NO synthase induction in macrophages. Science 263, 1612-1615.
31. Leonard, W.J., and O'Shea, J.J. (1998). Jaks and STATs: biological implications. Annu. Rev. Immunol. 16, 293-322.
32. Liu, Z., Simpson, R.J., and Cheers, C. (1995). Role of interleukin-6 in T-cell activation during primary and secondary infection with Listeria monocytogenes. Infect. Immun. 63, 2790-2792.
33. Lu, B., Ebensperger, C., Dembic, Z., Wang, Y., Kvatyuk, M., Lu, T., Coffman, R.L., Pestka, S., and Rothman, P.B. (1998). Targeted disruption of the interferon-gamma receptor 2 gene results in severe immune defects in mice. Proc. Natl. Acad. Sci. USA 95, 8233-8238.
34. MacMicking, J.D., Nathan, C., Hom, G., Chartrain, N., Fletcher, D.S., Trumbauer, M., Stevens, K., Xie, Q.W., Sokol, K., Hutchinson, N., et al. (1995). Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell 81, 641-650.
35. Massa, P.T., and Wu, C. (1996). The role of protein tyrosine phosphatase SHP-1 in the regulation of IFN-gamma signaling in neural cells. J. Immunol. 157, 5139-5144.
36. Matsumoto, A., Masuhara, M., Mitsui, K., Yokouchi, M., Ohtsubo, M., Misawa, H., Miyajima, A., and Yoshimura, A. (1997). CIS, a cytokine inducible SH2 protein, is a target of the JAK-STAT5 pathway and modulates STATS activation. Blood 89, 3148-3154.
37. Matsuyama, T., Kimura, T., Kitagawa, M., Pfeffer, K., Kawakami, T., Watanabe, N., Kundig, T.M., Amakawa, R., Kishihara, K., Wakeham, A., et al. (1993). Targeted disruption of IRF-1 or IRF-2 results in abnormal type IIFN gene induction and aberrant lymphocyte development. Cell 75, 83-97.
38. Matthys, P., Mitera, T., Heremans, H., Van Damme, J., and Billau, A. (1995). Anti-IFN-γ and anti-IL-6 antibodies affect staphylococcal enterotoxin B-induced weight loss, hypoglycemia and cytokine release in D-galactosamine sensitized and unsensititized mice. Infect. Immun. 63, 1158-1164.
39. Meraz, M.A., White, J.M., Sheehan, K.C., Bach, E.A., Rodig, S.J., Dighe, A.S., Kaplan, D.H., Riley, J.K., Greenlund, A.C., Campbell, D., et al. (1996). Targeted disruption of the Stal1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 84, 431-442.
40. Metcalf, D., Alexander, W.S., Elefanty, A.G., Nicola, N.A., Hilton, D.J., Starr, R., Mifsud, S., and Di Rago, L. (1999). Aberrant hematopoiesis in mice with inactivation of the gene encoding SOCS-1. Leukemia 13, 926-934.
41. Moore, K.W., O'Garra, A., de Waal Malefyt, R., Vieira, P., and Mosmann, T.R. (1993). Interleukin-10. Annu. Rev. Immunol. 11, 165-190.
42. Muller, M., Briscoe, J., Laxton, C., Guschin, D., Ziemiecki, A., Silvennoinen, O., Harpur, A.G., Barbieri, G., Witthuhn, B.A., Schindler, C., et al. (1993a). The protein tyrosine kinase JAK1 complements defects in interferon-alpha/beta and -gamma signal transduction. Nature 366, 129-135.
43. Muller, M., Laxton, C., Briscoe, J., Schindler, C., Improta, T., Darnell, J.E., Jr., Stark, G.R., and Kerr, I.M. (1993b). Complementation of a mutant cell line: central role of the 91 kDa polypeptide of ISGF3 in the interferon-alpha and -gamma signal transduction pathways. EMBO J. 12, 4221-4228.
44. Naka, T., Narazaki, M., Hirata, M., Matsumoto, T., Minamoto, S., Aono, A., Nishimoto, N., Kajita, T., Taga, T., Yoshizaki, K., et al. (1997). Structure and function of a new STAT-induced STAT inhibitor. Nature 387, 924-929.
45. Newport, M.J., Huxley, C.M., Huston, S., Hawrylowicz, C.M., Oostra, B.A., Williamson, R., and Levin, M. (1996). A mutation in the interferon-gamma-receptor gene and susceptibility to mycobacterial infection. N. Eng. J. Med. 335, 1941-1949.
46. Nicholson, S.E., Willson, T.A., Starr, R., Zhang, J.-G., Baca, M., Alexander, W.S., Metcalf, D., Nicola, N.A. and Hilton, D.U. (1999). Mutational analyses of the SOCS proteins suggest a dual domain requirement but distinct mechanisms for inhibiton of LIF and IL-6 signal transduction. EMBO J. 18, 375-385.
47. Novak, U., Harpur, A.G., Paradiso, L., Kanagasundaram, V., Jaworowski, A., Wilks, A.F., and Hamilton, J.A. (1995). Colony-stimulating factor 1-induced STAT1 and STAT3 activation is accompanied by phosphorylation of Tyk2 in macrophages and Tyk2 and JAK1 in fibroblasts. Blood 86, 2948-2956.
48. Novick, D., Cohen, B., and Rubinstein, M. (1994). The human Interferon alpha/beta receptor: characterization and molecular cloning. Cell 77, 391-400.
49. Ozato, K., Mayer, N.M., and Sachs, D.H. (1982). Monoclonal antibodies to mouse major histocompatability complex antigens. Transplantation 34, 113-120.
50. Paul, W.E. (1991). Interleukin-4: a prototypic immunoregulatory lymphokine. Blood 77, 1859-1870.
51. Proudfoot, L., Schneider, P., Ferguson, M.A., and McConville, M.J. (1995). Biosynthesis of the glycolipid anchor of lipophosphoglycan and the structurally related glycoinositolphospholipids from Leishmania major. Biochem J. 15, 45-55.
52. Ruff-Jamison, S., Chen, K., and Cohen, S. (1993). Induction by EGF and interferon-gamma of tyrosine phosphorylated DNA binding proteins in mouse liver nuclei. Science 261, 1733-1736.
53. Sakamoto, H., Yasukawa, H., Masuhara, M., Tanimura, S., Sasaki, A., Yuge, K., Ohtsubo, M., Ohtsuka, A., Fujita, T., Ohta, T., et al. (1998). A Janus kinase inhibitor, JAB, is an interferon-gamma-inducible gene and confers resistance to interferons. Blood 92, 1668-1676.
54. Schindler, C., and Darnell, J.E., Jr. (1995). Transcriptional responses to polypeptide ligands: the JAK-STAT pathway. Annu. Rev. Biochem. 64, 621-651.
55. Shuai, K., Schindler, C., Prezioso, V.R., and Darnell, J.E., Jr. (1992). Activation of transcription by IFN-gamma: tyrosine phosphorylation of a 91-kD DNA binding protein. Science 258, 1808-1812.
56. Shuai, K., Horvath, C.M., Huang, L.H., Qureshi, S.A., Cowburn, D., and Darnell, J.E., Jr. (1994). Interferon activation of the transcription factor Stat91 involves dimerization through SH2-phosphotyrosyl peptide interactions. Cell 76, 821-828.
57. Song, M.M., and Shuai, K. (1998). The suppressor of cytokine signaling (SOCS) 1 and SOCS3 but not SOCS2 or CIS proteins inhbit interferon-mediated antiviral and antiproliferative activities. J. Biol. Chem. 273, 35056-35062.
58. Starr, R., Willson, T.A., Viney, E.M., Murray, L.J., Rayner, J.R., Jenkins, B.J., Gonda, T.J., Alexander, W.S., Metcalf, D., Nicola, N.A., and Hilton, D.J. (1997). A family of cytokine-inducible inhibitors of signaling. Nature 387, 917-921.
59. Starr, R., Metcalf, D., Elefanty, A.G., Brysha, M., Willson, T.A., Nicola, N.A., Hilton, D.J., and Alexander, W.A. (1998). Liver degeneration and lymphoid deficiencies in mice lacking suppressor of cytokine signaling-1. Proc. Natl. Acad. Sci. USA 95, 14395-14399.
60. Strasser, A., Harris, A.W., and Cory, S. (1991 ). Bcl-2 transgene inhibits T cell death and perturbs thymic self-censorship. Cell 67, 889-899.
61. Tatake, R.J., and Zeff, R.A. (1993). Regulated expression of the major histocompatibility complex class I genes. Proc. Soc. Exp. Biol. Med. 203, 405-417.
62. Thomas, H.E., Parker, J.L., Schreiber, R.D., and Kay, T.W.H. (1998). IFN-γ action on pancreatic beta cells causes class I MHC upregulation but not diabetes. J. Clin. Invest. 702, 1249-1257.
63. Toyonaga, T., Hino, O., Sugai, S., Wakasugi, S., Abe, K., Shichiri, M., and Yamamura, K. (1994). Chronic active hepatitis in transgenic mice expressing interferon-gamma in the liver. Proc. Natl. Acad. Sci. USA 91, 614-618.
64. Wang, D., Stravopodis, D., Teglund, S., Kitazawa, J., and Ihle, J.N. (1996). Naturally occurring dominant negative variants of Stat5. Mol. Cell. Biol. 16, 6141-6148.
65. Watling, D., Guschin, D., Muller, M., Silvennoinen, O., Witthuhn, B.A., Quelle, F.W., Rogers, N.C., Schindler, C., Stark, G.R., Ihle, J.N., and Kerr, I.M. (1993). Complementation by the protein tyrosine kinase JAK2 of a mutant cell line defective in the interferon-gamma signal transduction pathway. Nature 366, 166-170.
66. Zurawski, G., and de Vries, J.E. (1994). Interleukin 13, an interleukin 4-like cytokine that acts on monocytes and B cells, but not on T cells. Immunol. Today 15, 19-26.