Suppressor of cytokine signaling 3 regulates CD8 T-cell proliferation by inhibition of interleukins 6 and 27

Blood

Volumn 110, Issue 7, 2007, Pages 2528-2536

  Brender, Christine ^a   Tannahill, Gillian M ^a   Jenkins, Brendan J ^b   Fletcher, Joel ^a   Columbus, Ruth ^c   Saris, Christiaan J M ^d   Ernst, Matthias ^e   Nicola, Nicos A ^c   Hilton, Douglas J ^c   Alexander, Warren S ^c   Starr, Robyn ^a  

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

^b MONASH UNIVERSITY   (Australia)

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

^d AMGEN INC   (United States)

^e LUDWIG INSTITUTE FOR CANCER RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CD28 ANTIGEN; CD3 ANTIGEN; GLYCOPROTEIN GP 130; INTERLEUKIN 27; INTERLEUKIN 6; RECEPTOR; SUPPRESSOR OF CYTOKINE SIGNALING 3; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ARTICLE; BINDING SITE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; GENE OVEREXPRESSION; GENE TARGETING; IMMUNOREGULATION; LYMPHOCYTE PROLIFERATION; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; WILD TYPE;

ANIMALS; ANTIGENS, CD28; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CELLS, CULTURED; CYTOKINE RECEPTOR GP130; GENE DELETION; INTERLEUKIN-6; INTERLEUKINS; MICE; MICE, KNOCKOUT; MITOSIS; MUTATION; PHENOTYPE; RECEPTORS, ANTIGEN, T-CELL; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TYROSINE;

EID: 34948904840     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2006-08-041541     Document Type: Article

References (60)

1. Sadlack B, Merz H, Schorle H, Schimpl A, Feller AC, Horak I. Ulcerative colitis-like disease in mice with a disrupted interleukin-2 gene. Cell. 1993;75:253-261.
2. von Freeden-Jeffry U, Vieira P, Lucian LA, McNeil T, Burdach SE, Murray R. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J Exp Med. 1995;181:1519-1526.
3. + T cells. J Exp Med. 2001;193:219-231.
4. Kopf M, Le Gros G, Bachmann M, Lamers MC, Bluethmann H, Kohler G. Disruption of the murine IL-4 gene blocks Th2 cytokine responses. Nature. 1993;362:245-248.
5. Alexander WS, Hilton DJ. The role of suppressors of cytokine signaling (SOCS) proteins in regulation of the immune response. Annu Rev Immunol. 2004;22:503-529.
6. Egwuagu CE, Yu CR, Zhang M, Mahdi RM, Kim SJ, Gery I. Suppressors of cytokine signaling proteins are differentially expressed in Th1 and Th2 cells: implications for Th cell lineage commitment and maintenance. J Immunol. 2002;168:3181-3187.
7. Yu CR, Mahdi RM, Ebong S, Vistica BP, Gery I, Egwuagu CE. Suppressor of cytokine signaling 3 regulates proliferation and activation of T-helper cells. J Biol Chem. 2003;278:29752-29759.
8. + T cell differentiation. Immunity. 2003;18:475-487.
9. Cornish AL, Davey GM, Metcalf D, et al. Suppressor of cytokine signaling-1 has IFN-gamma-independent actions in T cell homeostasis. J Immunol. 2003;170:878-886.
10. Fletcher J, Starr R. The role of suppressors of cytokine signalling in thymopoiesis and T cell activation. Int J Biochem Cell Biol. 2005;37:1774-1786.
11. Ohya K, Kajigaya S, Yamashita Y, et al. SOCS-1/JAB/SSI-1 can bind to and suppress Tec proteintyrosine kinase. J Biol Chem. 1997;272:27178-27182.
12. Matsuda T, Yamamoto T, Kishi H, Yoshimura A, Muraguchi A. SOCS-1 can suppress CD3zeta- and Syk-mediated NF-AT activation in a non-lymphoid cell line. FEBS Lett. 2000;472:235-240.
13. Banerjee A, Banks AS, Nawijn MC, Chen XP, Rothman PB. Cutting edge: suppressor of cytokine signaling 3 inhibits activation of NFATp. J Immunol. 2002;168:4277-4281.
14. Starr R, Metcalf D, Elefanty AG, et al. Liver degeneration and lymphoid deficiencies in mice lacking suppressor of cytokine signaling-1. Proc Natl Acad Sci U S A. 1998;95:14395-14399.
15. Naka T, Matsumoto T, Narazaki M, et al. 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. 1998;95:15577-15582.
16. Alexander WS, Starr R, Fenner JE, et al. SOCS1 is a critical inhibitor of interferon gamma signaling and prevents the potentially fatal neonatal actions of this cytokine. Cell. 1999;98:597-608.
17. +CD44high memory T lymphocytes. J Immunol. 2003;171:2435-2445.
18. + T cells. J Exp Med. 2002;195:1533-1539.
19. Cornish AL, Chong MM, Davey GM, et al. 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. 2003;278:22755-22761.
20. Davey GM, Starr R, Cornish AL, et al. SOCS-1 regulates IL-15-driven homeostatic proliferation of antigen-naive CD8 T cells, limiting their autoimmune potential. J Exp Med. 2005;202:1099-1108.
21. Matsumoto A, Seki Y, Watanabe R, et al. A role of suppressor of cytokine signaling 3 (SOCS3/CIS3/SSI3) in CD28-mediated interleukin 2 production. J Exp Med. 2003;197:425-436.
22. Marine JC, McKay C, Wang D, et al. SOCS3 is essential in the regulation of fetal liver erythropoiesis. Cell. 1999;98:617-627.
23. Roberts AW, Robb L, Rakar S, et al. Placental defects and embryonic lethality in mice lacking suppressor of cytokine signaling 3. Proc Natl Acad Sci U S A. 2001;98:9324-9329.
24. Chen Z, Laurence A, Kanno Y, et al. Selective regulatory function of Socs3 in the formation of IL-17-secreting T cells. Proc Natl Acad Sci U S A. 2006;103:8137-8142.
25. Kinjyo I, Inoue H, Hamano S, et al. Loss of SOCS3 in T helper cells resulted in reduced immune responses and hyperproduction of interleukin 10 and transforming growth factor-beta 1. J Exp Med. 2006;203:1021-1031.
26. Stumhofer JS, Laurence A, Wilson EH, et al. Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system. Nat Immunol. 2006;7:937-945.
27. Croker BA, Krebs DL, Zhang JG, et al. SOCS3 negatively regulates IL-6 signaling in vivo. Nat Immunol. 2003;4:540-545.
28. Lang R, Pauleau AL, Parganas E, et al. SOCS3 regulates the plasticity of gp130 signaling. Nat Immunol. 2003;4:546-550.
29. Yasukawa H, Ohishi M, Mori H, et al. IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nat Immunol. 2003;4:551-556.
30. Nicholson SE, De Souza D, Fabri LJ, et al. Suppressor of cytokine signaling-3 preferentially binds to the SHP-2-binding site on the shared cytokine receptor subunit gp130. Proc Natl Acad Sci U S A. 2000;97:6493-6498.
31. Schmitz J, Weissenbach M, Haan S, Heinrich PC, Schaper F. SOCS3 exerts its inhibitory function on interleukin-6 signal transduction through the SHP2 recruitment site of gp130. J Biol Chem. 2000;275:12848-12856.
32. Takahashi Y, Carpino N, Cross JC, Torres M, Parganas E, Ihle JN. SOCS3: an essential regulator of LIF receptor signaling in trophoblast giant cell differentiation. EMBO J. 2003;22:372-384.
33. Robb L, Boyle K, Rakar S, et al. Genetic reduction of embryonic leukemia-inhibitory factor production rescues placentation in SOCS3-null embryos but does not prevent inflammatory disease. Proc Natl Acad Sci U S A. 2005;102:16333-16338.
34. Villarino AV, Huang E, Hunter CA. Understanding the pro- and anti-inflammatory properties of IL-27. J Immunol. 2004;173:715-720.
35. Hunter CA. New IL-12-family members: IL-23 and IL-27, cytokines with divergent functions. Nat Rev Immunol. 2005;5:521-531.
36. Batten M, Li J, Yi S, et al. Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells. Nat Immunol. 2006;7:929-936.
37. + T cells partially through STAT3-dependent mechanism. J Immunol. 2006;177:5377-5385.
38. Villarino AV, Stumhofer JS, Saris CJ, Kastelein RA, de Sauvage FJ, Hunter CA. IL-27 limits IL-2 production during Th1 differentiation. J Immunol. 2006;176:237-247.
39. Villarino AV, Tato CM, Stumhofer JS, et al. Helper T cell IL-2 production is limited by negative feedback and STAT-dependent cytokine signals. J Exp Med. 2007;204:65-71.
40. Owaki T, Asakawa M, Kamiya S, et al. IL-27 suppresses CD28-mediated [correction of medicated] IL-2 production through suppressor of cytokine signaling 3. J Immunol. 2006;176:2773-2780.
41. Orban PC, Chui D, Marth JD. Tissue- and site-specific DNA recombination in transgenic mice. Proc Natl Acad Sci U S A. 1992;89:6861-6865.
42. Jenkins BJ, Roberts AW, Najdovska M, Grail D, Ernst M. The threshold of gp130-dependent STAT3 signaling is critical for normal regulation of hematopoiesis. Blood. 2005;105:3512-3520.
43. Kopf M, Baumann H, Freer G, et al. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature. 1994;368:339-342.
44. Harding FA, McArthur JG, Gross JA, Raulet DH, Allison JP. CD28-mediated signalling co-stimulates murine T cells and prevents induction of anergy in T-cell clones. Nature. 1992;356:607-609.
45. Brysha M, Zhang JG, Bertolino P, et al. Suppressor of cytokine signaling-1 attenuates the duration of interferon gamma signal transduction in vitro and in vivo. J Biol Chem. 2001;276:22086-22089.
46. Tomita K, Saijo K, Yamasaki S, et al. Cytokine-independent Jak3 activation upon T cell receptor (TCR) stimulation through direct association of Jak3 and the TCR complex. J Biol Chem. 2001;276:25378-25385.
47. Cohney SJ, Sanden D, Cacalano NA, et al. SOCS-3 is tyrosine phosphorylated in response to interleukin-2 and suppresses STAT5 phosphorylation and lymphocyte proliferation. Mol Cell Biol. 1999;19:4980-4988.
48. Leung DT, Morefield S, Willerford DM. Regulation of lymphoid homeostasis by IL-2 receptor signals in vivo. J Immunol. 2000;164:3527-3534.
49. Schluns KS, Lefrancois L. Cytokine control of memory T-cell development and survival. Nat Rev Immunol. 2003;3:269-279.
50. Tebbutt NC, Giraud AS, Inglese M, et al. Reciprocal regulation of gastrointestinal homeostasis by SHP2 and STAT-mediated trefoil gene activation in gp130 mutant mice. Nat Med. 2002;8:1089-1097.
51. Atsumi T, Ishihara K, Kamimura D, et al. A point mutation of Tyr-759 in interleukin 6 family cytokine receptor subunit gp130 causes autoimmune arthritis. J Exp Med. 2002;196:979-990.
52. Vink A, Uyttenhove C, Wauters P, Van Snick J. Accessory factors involved in murine T cell activation: distinct roles of interleukin 6, interleukin 1 and tumor necrosis factor. Eur J Immunol. 1990;20:1-6.
53. + primary T helper cells: role of IL-1 and IL-6 in inducing IL-2 secretion and subsequent proliferation. Int Immunol. 1992;4:327-335.
54. Takeda K, Kaisho T, Yoshida N, Takeda J, Kishimoto T, Akira S. Stat3 activation is responsible for IL-6-dependent T cell proliferation through preventing apoptosis: generation and characterization of T cell-specific Stat3-deficient mice. J Immunol. 1998;161:4652-4660.
55. Sepulveda H, Cerwenka A, Morgan T, Dutton RW. CD28, IL-2-independent costimulatory pathways for CD8 T lymphocyte activation. J Immunol. 1999;163:1133-1142.
56. Pflanz S, Hibbert L, Mattson J, et al. WSX-1 and glycoprotein 130 constitute a signal-transducing receptor for IL-27. J Immunol. 2004;172:2225-2231.
57. + T cells. J Immunol. 2004;173:3871-3877.
58. Pflanz S, Timans JC, Cheung J, et al. IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4(+) T cells. Immunity. 2002;16:779-790.
59. + T cells leads to hyperproliferation and cytokine hyperproduction in response to TCR stimulation. Int Immunol. 2005;17:889-897.
60. Villarino A, Hibbert L, Lieberman L, et al. The IL-27R (WSX-1) is required to suppress T cell hyperactivity during infection. Immunity. 2003;19:645-655.