SOCS-1 binding to tyrosine 441 of IFN-γ receptor subunit 1 contributes to the attenuation of IFN-γ signaling in vivo

Journal of Immunology

Volumn 183, Issue 7, 2009, Pages 4537-4544

  Starr, Robyn ^a   Fuchsberger, Martina ^a   Lau, Lei Shong ^a   Uldrich, Adam P ^b   Goradia, Ankita ^a   Willson, Tracy A ^c   Verhagen, Anne M ^a   Alexander, Warren S ^c   Smyth, Mark J ^b  

^a ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b PETER MACCALLUM CANCER CENTRE   (Australia)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GALACTOSYLCERAMIDE; CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON RECEPTOR 1; INTERLEUKIN 12; STAT1 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 1; TYROSINE; GAMMA INTERFERON RECEPTOR; INTERFERON RECEPTOR; PROTEIN SUBUNIT; SOCS1 PROTEIN, MOUSE; SUPPRESSOR OF CYTOKINE SIGNALING;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTENUATION; BINDING SITE; CELL MUTANT; CONTROLLED STUDY; EMBRYO; IN VIVO STUDY; INNATE IMMUNITY; LUNG METASTASIS; MOUSE; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; TUMOR IMMUNITY; WILD TYPE; ANIMAL; C57BL MOUSE; CELL CULTURE; EXPERIMENTAL MELANOMA; GENE TARGETING; GENETICS; IMMUNOLOGY; LUNG TUMOR; METABOLISM; METASTASIS; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; CELLS, CULTURED; GENE KNOCK-IN TECHNIQUES; INTERFERON-GAMMA; LUNG NEOPLASMS; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PROTEIN BINDING; PROTEIN SUBUNITS; RECEPTORS, INTERFERON; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TYROSINE;

EID: 70449698533     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901010     Document Type: Article

References (41)

1. Ikeda, H., L. J. Old, and R. D. Schreiber. 2002. The roles of IFNγ in protection against tumor development and cancer immunoediting. Cytokine Growth Factor Rev. 13: 95-109.
2. Street, S. E., J. A. Trapani, D. MacGregor, and M. J. Smyth. 2002. Suppression of lymphoma and epithelial malignancies effected by interferon γ. J. Exp. Med. 196: 129-134.
3. Schroder, K., P. J. Hertzog, T. Ravasi, and D. A. Hume. 2004. Interferon-γ: an overview of signals, mechanisms and functions. J. Leukocyte Biol. 75: 163-189. (Pubitemid 38174573)
4. Dunn, G. P., C. M. Koebel, and R. D. Schreiber. 2006. Interferons, immunity and cancer immunoediting. Nat. Rev. Immunol. 6: 836-848.
5. Gresser, I., M. Aguet, L. Morel-Maroger, D. Woodrow, F. Puvion-Dutilleul, J. C. Guillon, and C. Maury. 1981. Electrophoretically pure mouse interferon inhibits growth, induces liver and kidney lesions, and kills suckling mice. Am. J. Pathol. 102: 396-402. (Pubitemid 11143433)
6. Toyonaga, T., O. Hino, S. Sugai, S. Wakasugi, K. Abe, M. Shichiri, and K. Yamamura. 1994. Chronic active hepatitis in transgenic mice expressing interferon-γ in the liver. Proc. Natl. Acad. Sci. USA 91: 614-618. (Pubitemid 24041452)
7. Alexander, W. S., R. Starr, J. E. Fenner, C. L. Scott, E. Handman, N. S. Sprigg, J. E. Corbin, A. L. Cornish, R. Darwiche, C. M. Owczarek, et al. 1999. SOCS1 is a critical inhibitor of interferon gamma signaling and prevents the potentially fatal neonatal actions of this cytokine. Cell 98: 597-608.
8. Alexander, W. S., and D. J. Hilton. 2004. The role of suppressors of cytokine signaling (SOCS) proteins in regulation of the immune response. Annu. Rev. Immunol. 22: 503-529.
9. Starr, R., D. Metcalf, A. G. Elefanty, M. Brysha, T. A. Willson, N. A. Nicola, D. J. Hilton, and W. S. Alexander. 1998. Liver degeneration and lymphoid deficiencies in mice lacking suppressor of cytokine signaling-1. Proc. Natl. Acad. Sci. USA 95: 14395-14399.
10. Endo, T. A., M. Masuhara, M. Yokouchi, R. Suzuki, H. Sakamoto, K. Mitsui, A. Matsumoto, S. Tanimura, M. Ohtsubo, H. Misawa, et al. 1997. A new protein containing an SH2 domain that inhibits JAK kinases. Nature 387: 921-924.
11. Nicholson, S. E., T. A. Willson, A. Farley, R. Starr, J.-G. Zhang, M. Baca, W. S. Alexander, D. Metcalf, D. J. Hilton, and N. A. Nicola. 1999. 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. 18: 375-385.
12. Yasukawa, H., H. Misawa, H. Sakamoto, M. Masuhara, A. Sasaki, T. Wakioka, S. Ohtsuka, T. Imaizumi, T. Matsuda, J. N. Ihle, and A. Yoshimura. 1999. The JAK-binding protein JAB inhibits Janus tyrosine kinase activity through binding in the activation loop. EMBO J. 18: 1309-1320.
13. Sporri, B., P. E. Kovanen, A. Sasaki, A. Yoshimura, and W. J. Leonard. 2001. JAB/SOCS1/SSI-1 is an interleukin-2-induced inhibitor of IL-2 signaling. Blood 97: 221-226.
14. Zhang, J. G., D. Metcalf, S. Rakar, M. Asimakis, C. J. Greenhalgh, T. A. Willson, R. Starr, S. E. Nicholson, W. Carter, W. S. Alexander, et al. 2001. The SOCS box of suppressor of cytokine signaling-1 is important for inhibition of cytokine action in vivo. Proc. Natl. Acad. Sci. USA 98: 13262-13265.
15. 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. 95: 13130-13134.
16. Sasaki, A., H. Yasukawa, A. Suzuki, S. Kamizono, T. Syoda, I. Kinjyo, M. Sasaki, J. A. Johnston, and A. Yoshimura. 1999. Cytokine-inducible SH2 protein-3 (CIS3/SOCS3) inhibits Janus tyrosine kinase by binding through the N-terminal kinase inhibitory region as well as SH2 domain. Genes Cells 4: 339-351.
17. Nicholson, S. E., D. De Souza, L. J. Fabri, J. Corbin, T. A. Willson, J.-G. Zhang, A. Silva, M. Asimakis, A. Farley, A. D. Nash, et al. 2000. Suppressor of cytokine signaling-3 preferentially binds to the SHP-2-binding site on the shared cytokine receptor subunit gp130. Proc. Natl. Acad. Sci. USA 97: 6493-6498.
18. Schmitz, J., M. Weissenbach, S. Haan, P. C. Heinrich, and F. Schaper. 2000. SOCS3 exerts its inhibitory function on interleukin-6 signal transduction through the SHP2 recruitment site of gp130. J. Biol. Chem. 275: 12848-12856.
19. Ohtani, T., K. Ishihara, T. Atsumi, K. Nishida, Y. Kaneko, T. Miyata, S. Itoh, M. Narimatsu, H. Maeda, T. Fukada, et al. 2000. Dissection of signaling cascades through gp130 in vivo: reciprocal roles for STAT3- and SHP2-mediated signals in immune responses. Immunity 12: 95-105.
20. Tebbutt, N. C., A. S. Giraud, M. Inglese, B. Jenkins, P. Waring, F. J. Clay, S. Malki, B. M. Alderman, D. Grail, F. Hollande, et al. 2002. Reciprocal regulation of gastrointestinal homeostasis by SHP2 and STAT-mediated trefoil gene activation in gp130 mutant mice. Nat. Med. 8: 1089-1097.
21. Fenner, J. E., R. Starr, A. L. Cornish, J. G. Zhang, D. Metcalf, R. D. Schreiber, K. Sheehan, D. J. Hilton, W. S. Alexander, and P. J. Hertzog. 2006. Suppressor of cytokine signaling 1 regulates the immune response to infection by a unique inhibition of type I interferon activity. Nat. Immunol. 7: 33-39.
22. Qing, Y., A. P. Costa-Pereira, D. Watling, and G. R. Stark. 2005. Role of tyrosine 441 of interferon-γ receptor subunit 1 in SOCS-1-mediated attenuation of STAT1 activation. J. Biol. Chem. 280: 1849-1853.
23. Kontgen, F., G. Suss, C. Stewart, M. Steinmetz, and H. Bluethmann. 1993. Targeted disruption of the MHC class II Aa gene in C57BL/6 mice. Int. Immunol. 5: 957-964. (Pubitemid 23241767)
24. Schwenk, F., U. Baron, and K. Rajewsky. 1995. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res. 23: 5080-5081. (Pubitemid 26012492)
25. Dalton, D. K., S. Pitts-Meek, S. Keshav, I. S. Figari, A. Bradley, and T. A. Stewart. 1993. Multiple defects of immune cell function in mice with disrupted interferon-γ genes. Science 259: 1739-1742.
26. Brysha, M., J. G. Zhang, P. Bertolino, J. E. Corbin, W. S. Alexander, N. A. Nicola, D. J. Hilton, and R. Starr. 2001. Suppressor of cytokine signaling-1 attenuates the duration of interferon γ signal transduction in vitro and in vivo. J. Biol. Chem. 276: 22086-22089. (Pubitemid 37410872)
27. + T cells and natural killer cells is essential for the antimetastatic effect of α-galactosylceramide. Blood 99: 1259-1266.
28. + T cell differentiation. Immunity 18: 475-487.
29. Smyth, M. J., M. Taniguchi, and S. E. Street. 2000. The anti-tumor activity of IL-12: mechanisms of innate immunity that are model and dose dependent. J. Immunol. 165: 2665-2670.
30. Newman, K. C., and E. M. Riley. 2007. Whatever turns you on: accessory-cell-dependent activation of NK cells by pathogens. Nat. Rev. Immunol. 7: 279-291.
31. Wendel, M., I. E. Galani, E. Suri-Payer, and A. Cerwenka. 2008. Natural killer cell accumulation in tumors is dependent on IFN-γ and CXCR3 ligands. Cancer Res. 68: 8437-8445.
32. Walser, T. C., X. Ma, N. Kundu, R. Dorsey, O. Goloubeva, and A. M. Fulton. 2007. Immune-mediated modulation of breast cancer growth and metastasis by the chemokine Mig (CXCL9) in a murine model. J. Immunother. 30: 490-498.
33. Starr, R., T. A. Willson, E. M. Viney, L. J. Murray, J. R. Rayner, B. J. Jenkins, T. J. Gonda, W. S. Alexander, D. Metcalf, N. A. Nicola, and D. J. Hilton. 1997. A family of cytokine-inducible inhibitors of signalling. Nature 387: 917-921.
34. Eyles, J. L., D. Metcalf, M. J. Grusby, D. J. Hilton, and R. Starr. 2002. Negative regulation of interleukin-12 signaling by suppressor of cytokine signaling-1. J. Biol. Chem. 277: 43735-43740.
35. c-dependent cytokines in peripheral T cells. J. Biol. Chem. 278: 22755-22761.
36. + thymocytes. Blood 102: 4115-4122.
37. Ramanathan, S., J. Gagnon, C. Leblanc, R. Rottapel, and S. Ilangumaran. 2006. Suppressor of cytokine signaling 1 stringently regulates distinct functions of IL-7 and IL-15 in vivo during T lymphocyte development and homeostasis. J. Immunol. 176: 4029-4041. (Pubitemid 44264381)
38. + T lymphocytes. Cell Signal. 19: 806-816.
39. Cornish, A. L., G. M. Davey, D. Metcalf, J. F. Purton, J. E. Corbin, C. J. Greenhalgh, R. Darwiche, L. Wu, N. A. Nicola, D. I. Godfrey, et al. 2003. Suppressor of cytokine signaling-1 has IFN-γ-independent actions in T cell homeostasis. J. Immunol. 170: 878-886.
40. Dupuis, S., R. Doffinger, C. Picard, C. Fieschi, F. Altare, E. Jouanguy, L. Abel, and J.-L. Casanova. 2000. Human interferon-γ-mediated immunity is a genetically controlled continuous trait that determines the outcome of mycobacterial invasion. Immunol. Rev. 178: 129-137.
41. Lio, D., V. Marino, A. Serauto, V. Gioia, L. Scola, A. Crivello, G. I. Forte, G. Colonna-Romano, G. Candore, and C. Caruso. 2002. Genotype frequencies of the +874T->A single nucleotide polymorphism in the first intron of the interferon-γ gene in a sample of Sicilian patients affected by tuberculosis. Eur. J. Immunogenet. 29: 371-374.