SOCS-1 regulates IL-15-driven homeostatic proliferation of antigen-naive CD8 T cells, limiting their autoimmune potential

Journal of Experimental Medicine

Volumn 202, Issue 8, 2005, Pages 1099-1108

  Davey, Gayle M ^a   Starr, Robyn ^a,d   Cornish, Ann L ^a   Burghardt, J Theodore ^b   Alexander, Warren S ^a   Carbone, Francis R ^c   Surh, Charles D ^b   Heath, William R ^a  

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

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF MELBOURNE   (Australia)

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

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; HERMES ANTIGEN; INTERLEUKIN 15; POLYCLONAL ANTIBODY; SUPPRESSOR OF CYTOKINE SIGNALING 1; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY SPECIFICITY; ARTICLE; AUTOIMMUNITY; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HOMEOSTASIS; IMMUNE DEFICIENCY; IMMUNOREGULATION; LIGAND BINDING; LYMPHOCYTE DEPLETION; LYMPHOCYTE PROLIFERATION; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; PHENOTYPE; POLYCLONAL ACTIVATION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION;

ADOPTIVE TRANSFER; ANIMALS; AUTOIMMUNITY; BONE MARROW TRANSPLANTATION; CARRIER PROTEINS; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; FLOW CYTOMETRY; IMMUNE TOLERANCE; INTERLEUKIN-15; LYMPHOCYTE ACTIVATION; MICE; MICE, KNOCKOUT; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TRANSPLANTATION CHIMERA;

EID: 26844492214     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20050003     Document Type: Article

References (49)

1. Naka, T., M. Narazaki, M. Hirata, T. Matsumoto, S. Minamoto, A. Aono, N. Nishimoto, T. Kajita, T. Taga, K. Yoshizaki, et al. 1997. Structure and function of a new STAT-induced STAT inhibitor. Nature. 387:924-929.
2. 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.
3. 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.
4. 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.
5. Kamura, T., S. Sato, D. Haque, L. Liu, W.G. Kaelin Jr., R.C. Conaway, and J.W. Conaway. 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.
6. Zhang, J.G., A. Farley, S.E. Nicholson, T.A. Willson, L.M. Zugaro, R.J. Simpson, R.L. Moritz, D. Cary, R. Richardson, G. Hausmann, 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. USA. 96:2071-2076.
7. Alexander, W.S. 2002. Suppressors of cytokine signalling (SOCS) in the immune system. Nat. Rev. Immunol. 2:410-416.
8. Fujimoto, M., and T. Naka. 2003. Regulation of cytokine signaling by SOCS family molecules. Trends Immunol. 24:659-666.
9. Ilangumaran, S., S. Ramanathan, T. Ning, J. La Rose, B. Reinhart, P. Poussier, and R. Rottapel. 2003. Suppressor of cytokine signaling 1 attenuates IL-15 receptor signaling in CD8+ thymocytes. Blood. 102:4115-4122.
10. Cornish, A.L., M.M. Chong, G.M. Davey, R. Darwiche, N.A. Nicola, D.J. Hilton, T.W. Kay, R. Starr, and W.S. Alexander. 2003. Suppressor of cytokine signaling-1 regulates signaling in response to interleukin-2 and other gamma c-dependent cytokines in peripheral T cells. J. Biol. Chem. 278:22755-22761.
11. high memory T lymphocytes. J. Immunol. 171:2435-2445.
12. 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.
13. + T cell differentiation. Immunity. 18:475-487.
14. Naka, T., T. Matsumoto, M. Narazaki, M. Fujimoto, Y. Morita, Y. Ohsawa, H. Saito, T. Nagasawa, Y. Uchiyama, and T. Kishimoto. 1998. Accelerated apoptosis of lymphocytes by augmented induction of Bax in SSI-1 (STAT-induced STAT inhibitor-1) deficient mice. Proc. Natl. Acad. Sci. USA. 95:15577-15582.
15. 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.
16. -/- mice prevents fatty degeneration of the liver but not subsequent fatal inflammatory disease. Immunology. 104:92-98.
17. Marine, J.C., D.J. Topham, C. McKay, D. Wang, E. Parganas, D. Stravopodis, A. Yoshimura, and J.N. Ihle. 1999. SOCS1 deficiency causes a lymphocyte-dependent perinatal lethality. Cell. 98:609-616.
18. Metcalf, D., S. Mifsud, L. Di Rago, N.A. Nicola, D.J. Hilton, and W.S. Alexander. 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. USA. 99:943-948.
19. Naka, T., H. Tsutsui, M. Fujimoto, Y. Kawazoe, H. Kohzaki, Y. Morita, R. Nakagawa, M. Narazaki, K. Adachi, T. Yoshimoto, et al. 2001. SOCS-1/SSI-1-deficient NKT cells participate in severe hepatitis through dysregulated cross-talk inhibition of IFN-gamma and IL-4 signaling in vivo. Immunity. 14:535-545.
20. 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.
21. 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-gamma-independent actions in T cell homeostasis. J. Immunol. 170:878-886.
22. Hanada, T., H. Yoshida, S. Kato, K. Tanaka, K. Masutani, J. Tsukada, Y. Nomura, H. Mimata, M. Kubo, and A. Yoshimura. 2003. Suppressor of cytokine signaling-1 is essential for suppressing dendritic cell activation and systemic autoimmunity. Immunity. 19:437-450.
23. + T cells in lymphopenic hosts. Immunity. 11:183-190.
24. Ernst, B., D.S. Lee, J.M. Chang, J. Sprent, and C.D. Surh. 1999. The peptide ligands mediating positive selection in the thymus control T cell survival and homeostatic proliferation in the periphery. Immunity. 11:173-181.
25. Kieper, W.C., and S.C. Jameson. 1999. Homeostatic expansion and phenotypic conversion of naive T cells in response to self peptide/MHC ligands. Proc. Natl. Acad. Sci. USA. 96:13306-13311.
26. Rocha, B., and H. von Boehmer. 1991. Peripheral selection of the T cell repertoire. Science. 251:1225-1228.
27. Tanchot, C., F.A. Lemonnier, B. Perarnau, A.A. Freitas, and B. Rocha. 1997. Differential requirements for survival and proliferation of CD8 naive or memory T cells. Science. 276:2057-2062.
28. + cells. J. Exp. Med. 195:1523-1532.
29. Goldrath, A.W., P.V. Sivakumar, M. Glaccum, M.K. Kennedy, M.J. Bevan, C. Benoist, D. Mathis, and E.A. Butz. 2002. Cytokine requirements for acute and basal homeostatic proliferation of naive and memory CD8+ T cells. J. Exp. Med. 195:1515-1522.
30. Heath, W.R., and F.R. Carbone. 2001. Cross-presentation in viral immunity and self-tolerance. Nat. Rev. Immunol. 1:126-134.
31. + T cell ignorance or tolerance to islet antigens depends on antigen dose. Proc. Natl. Acad. Sci. USA. 96:12703-12707.
32. Kurts, C., H. Kosaka, F.R. Carbone, J.F. Miller, and W.R. Heath. 1997. Class I-restricted cross-presentation of exogenous self-antigens leads to deletion of autoreactive CD8(+) T cells. J. Exp. Med. 186:239-245.
33. Davey, G.M., C. Kurts, J.F. Miller, P. Bouillet, A. Strasser, A.G. Brooks, F.R. Carbone, and W.R. Heath. 2002. Peripheral deletion of autoreactive CD8 T cells by cross presentation of self-antigen occurs by a Bcl-2-inhibitable pathway mediated by Bim. J. Exp. Med. 196:947-955.
34. Belz, G.T., G.M. Behrens, C.M. Smith, J.F. Miller, C. Jones, K. Lejon, C.G. Fathman, S.N. Mueller, K. Shortman, F.R. Carbone, and W.R. Heath. 2002. The CD8alpha(+) dendritic cell is responsible for inducing peripheral self-tolerance to tissue-associated antigens. J. Exp. Med. 196:1099-1104.
35. Kurts, C., J.F. Miller, R.M. Subramaniam, F.R. Carbone, and W.R. Heath. 1998. Major histocompatibility complex class I-restricted cross-presentation is biased towards high dose antigens and those released during cellular destruction. J. Exp. Med. 188:409-414.
36. Kurts, C., W.R. Heath, F.R. Carbone, J. Allison, J.F. Miller, and H. Kosaka. 1996. Constitutive class I-restricted exogenous presentation of self antigens in vivo. J. Exp. Med. 184:923-930.
37. Kurts, C., F.R. Carbone, M.F. Krummel, K.M. Koch, J.F. Miller, and W.R. Heath. 1999. Signalling through CD30 protects against autoimmune diabetes mediated by CD8 T cells. Nature. 398:341-344.
38. Tan, J.T., E. Dudl, E. LeRoy, R. Murray, J. Sprent, K.I. Weinberg, and C.D. Surh. 2001. IL-7 is critical for homeostatic proliferation and survival of naive T cells. Proc. Natl. Acad. Sci. USA. 98:8732-8737.
39. Vivien, L., C. Benoist, and D. Mathis. 2001. T lymphocytes need IL-7 but not IL-4 or IL-6 to survive in vivo. Int. Immunol. 13:763-768.
40. Berard, M., K. Brandt, S. Bulfone-Paus, and D.F. Tough. 2003. IL-15 promotes the survival of naive and memory phenotype CD8+ T cells. J. Immunol. 170:5018-5026.
41. Oldstone, M.B., M. Nerenberg, P. Southern, J. Price, and H. Lewicki. 1991. Virus infection triggers insulin-dependent diabetes mellitus in a transgenic model: role of anti-self (virus) immune response. Cell. 65:319-331.
42. Ohashi, P.S., S. Oehen, K. Buerki, H. Pircher, C.T. Ohashi, B. Odermatt, B. Malissen, R.M. Zinkernagel, and H. Hengartner. 1991. Ablation of "tolerance" and induction of diabetes by virus infection in viral antigen transgenic mice. Cell. 65:305-317.
43. Hogquist, K.A., S.C. Jameson, W.R. Heath, J.L. Howard, M.J. Bevan, and F.R. Carbone. 1994. T cell receptor antagonist peptides induce positive selection. Cell. 76:17-27.
44. Bluthmann, H., P. Kisielow, Y. Uematsu, M. Malissen, P. Krimpenfort, A. Berns, H. von Boehmer, and M. Steinmetz. 1988. T-cell-specific deletion of T-cell receptor transgenes allows functional rearrangement of endogenous alpha- and beta-genes. Nature. 334:156-159.
45. Spanopoulou, E., C.A. Roman, L.M. Corcoran, M.S. Schlissel, D.P. Silver, D. Nemazee, M.C. Nussenzweig, S.A. Shinton, R.R. Hardy, and D. Baltimore. 1994. Functional immunoglobulin transgenes guide ordered B-cell differentiation in Rag-1-deficient mice. Genes Dev. 8:1030-1042.
46. Kennedy, M.K., M. Glaccum, S.N. Brown, E.A. Butz, J.L. Viney, M. Embers, N. Matsuki, K. Charrier, L. Sedger, C.R. Willis, et al. 2000. Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J. Exp. Med. 191:771-780.
47. von Freeden-Jeffry, U., P. Vieira, L.A. Lucian, T. McNeil, S.E. Burdach, and R. Murray. 1995. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J. Exp. Med. 181:1519-1526.
48. + T cells. Cell. 71:1205-1214.
49. Aldrich, C.J., H.G. Ljunggren, L. Van Kaer, P.G. Ashton-Rickardt, S. Tonegawa, and J. Forman. 1994. Positive selection of self- and alloreactive CD8+ T cells in Tap-1 mutant mice. Proc. Natl. Acad. Sci. USA. 91:6525-6528.