IL-6 activates STAT5 in T cells

Cytokine

Volumn 60, Issue 2, 2012, Pages 575-582

  Tormo, Aurélie Jeanne ^a   Letellier, Marie Claude ^a   Sharma, Mukut ^b   Elson, Greg ^c   Crabé, Sandrine ^a,d   Gauchat, Jean François ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b KCVA Medical Center   (United States)

^c NOVIMMUNE SA   (Switzerland)

^d Wittycell   (France)

Author keywords

CD4 T cells; Interleukin 6; STAT3; STAT5; Th17

Indexed keywords

INTERLEUKIN 6; MESSENGER RNA; STAT1 PROTEIN; STAT3 PROTEIN; STAT5 PROTEIN;

ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; FLOW CYTOMETRY; GENE CONTROL; LYMPHOCYTE DIFFERENTIATION; MONONUCLEAR CELL; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; UPREGULATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; FEMALE; INTERLEUKIN-6; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; PHOSPHORYLATION; STAT1 TRANSCRIPTION FACTOR; STAT3 TRANSCRIPTION FACTOR; STAT5 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; T-LYMPHOCYTES;

EID: 84866763565     PISSN: 10434666     EISSN: 10960023     Source Type: Journal    
DOI: 10.1016/j.cyto.2012.07.002     Document Type: Article

References (86)

1. Hirano T., Yasukawa K., Harada H., Taga T., Watanabe Y., Matsuda T., et al. Complementary DNA for a novel human interleukin (BSF-2) that induces B lymphocytes to produce immunoglobulin. Nature 1986, 324:73-76.
2. Andus T., Geiger T., Hirano T., Northoff H., Ganter U., Bauer J., et al. Recombinant human B cell stimulatory factor 2 (BSF-2/IFN-beta 2) regulates beta-fibrinogen and albumin mRNA levels in Fao-9 cells. FEBS Lett 1987, 221:18-22.
3. Gauldie J., Richards C., Harnish D., Lansdorp P., Baumann H. Interferon beta 2/B-cell stimulatory factor type 2 shares identity with monocyte-derived hepatocyte-stimulating factor and regulates the major acute phase protein response in liver cells. Proc Natl Acad Sci USA 1987, 84:7251-7255.
4. Kopf M., Baumann H., Freer G., Freudenberg M., Lamers M., Kishimoto T., et al. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 1994, 368:339-342.
5. Hurst S.M., Wilkinson T.S., McLoughlin R.M., Jones S., Horiuchi S., Yamamoto N., et al. Il-6 and its soluble receptor orchestrate a temporal switch in the pattern of leukocyte recruitment seen during acute inflammation. Immunity 2001, 14:705-714.
6. Bettelli E., Carrier Y., Gao W., Korn T., Strom T.B., Oukka M., et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006, 441:235-238.
7. Bettelli E., Oukka M., Kuchroo V.K. T(H)-17 cells in the circle of immunity and autoimmunity. Nat Immunol 2007, 8:345-350.
8. McGeachy M.J., Bak-Jensen K.S., Chen Y., Tato C.M., Blumenschein W., McClanahan T., et al. TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat Immunol 2007, 8:1390-1397.
9. Veldhoen M., Hocking R.J., Atkins C.J., Locksley R.M., Stockinger B. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 2006, 24:179-189.
10. Mangan P.R., Harrington L.E., O'Quinn D.B., Helms W.S., Bullard D.C., Elson C.O., et al. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 2006, 441:231-234.
11. Eto D., Lao C., DiToro D., Barnett B., Escobar T.C., Kageyama R., et al. IL-21 and IL-6 are critical for different aspects of B cell immunity and redundantly induce optimal follicular helper CD4 T cell (Tfh) differentiation. PLoS One 2011, 6:e17739.
12. Nurieva R.I., Chung Y., Hwang D., Yang X.O., Kang H.S., Ma L., et al. Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity 2008, 29:138-149.
13. Diehl S., Anguita J., Hoffmeyer A., Zapton T., Ihle J.N., Fikrig E., et al. Inhibition of Th1 differentiation by IL-6 is mediated by SOCS1. Immunity 2000, 13:805-815.
14. Pasare C., Medzhitov R. Toll pathway-dependent blockade of CD4+CD25+T cell-mediated suppression by dendritic cells. Science 2003, 299:1033-1036.
15. Tesmer L.A., Lundy S.K., Sarkar S., Fox D.A. Th17 cells in human disease. Immunol Rev 2008, 223:87-113.
16. Ziegler S.F. FOXP3: of mice and men. Annu Rev Immunol 2006, 24:209-226.
17. Sakaguchi S., Ono M., Setoguchi R., Yagi H., Hori S., Fehervari Z., et al. Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev 2006, 212:8-27.
18. Naugler W.E., Karin M. The wolf in sheep's clothing: the role of interleukin-6 in immunity, inflammation and cancer. Trend Mol Med 2008, 14:109-119.
19. Ishihara K., Hirano T. IL-6 in autoimmune disease and chronic inflammatory proliferative disease. Cytokine Growth Factor Rev 2002, 13:357-368.
20. Rose-John S., Scheller J., Elson G., Jones S.A. Interleukin-6 biology is coordinated by membrane-bound and soluble receptors: role in inflammation and cancer. J Leukoc Biol 2006, 80:227-236.
21. Melton L., Coombs A. Actemra poised to launch IL-6 inhibitors. Nat Biotechnol 2008, 26:957-959.
22. Sebba A. Tocilizumab: the first interleukin-6-receptor inhibitor. Am J Health Syst Pharm 2008, 65:1413-1418.
23. Scheinecker C., Smolen J., Yasothan U., Stoll J., Kirkpatrick P. Tocilizumab. Nat Rev Drug Discov 2009, 8:273-274.
24. Nishimoto N., Kanakura Y., Aozasa K., Johkoh T., Nakamura M., Nakano S., et al. Humanized anti-interleukin-6 receptor antibody treatment of multicentric Castleman disease. Blood 2005, 106:2627-2632.
25. Smolen J.S., Beaulieu A., Rubbert-Roth A., Ramos-Remus C., Rovensky J., Alecock E., et al. Effect of interleukin-6 receptor inhibition with tocilizumab in patients with rheumatoid arthritis (OPTION study): a double-blind, placebo-controlled, randomised trial. Lancet 2008, 371:987-997.
26. Nishimoto N., Yoshizaki K., Miyasaka N., Yamamoto K., Kawai S., Takeuchi T., et al. Treatment of rheumatoid arthritis with humanized anti-interleukin-6 receptor antibody: a multicenter, double-blind, placebo-controlled trial. Arthritis Rheum 2004, 50:1761-1769.
27. Nishimoto N, Miyasaka N, Yamamoto K, Kawai S, Takeuchi T, Azuma J. Long-term safety and efficacy of tocilizumab, an anti-interleukin-6 receptor monoclonal antibody. In: Monotherapy, in patients with rheumatoid arthritis (the STREAM study): evidence of safety and efficacy in a 5-year extension study. Annals of the rheumatic diseases; 2008.
28. Yokota S., Imagawa T., Mori M., Miyamae T., Aihara Y., Takei S., et al. Efficacy and safety of tocilizumab in patients with systemic-onset juvenile idiopathic arthritis: a randomised, double-blind, placebo-controlled, withdrawal phase III trial. Lancet 2008, 371:998-1006.
29. Ito H., Takazoe M., Fukuda Y., Hibi T., Kusugami K., Andoh A., et al. A pilot randomized trial of a human anti-interleukin-6 receptor monoclonal antibody in active Crohn's disease. Gastroenterology 2004, 126:989-996. [discussion 47].
30. Murakami M., Nishimoto N. The value of blocking IL-6 outside of rheumatoid arthritis: current perspective. Curr Opin Rheumatol 2011, 23:273-277.
31. Heinrich P.C., Behrmann I., Haan S., Hermanns H.M., Muller-Newen G., Schaper F. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J 2003, 374:1-20.
32. Mathur A.N., Chang H.C., Zisoulis D.G., Stritesky G.L., Yu Q., O'Malley J.T., et al. Stat3 and Stat4 direct development of IL-17-secreting Th cells. J Immunol 2007, 178:4901-4907.
33. Yang X.O., Panopoulos A.D., Nurieva R., Chang S.H., Wang D., Watowich S.S., et al. STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J Biol Chem 2007, 282:9358-9363.
34. Harris T.J., Grosso J.F., Yen H.R., Xin H., Kortylewski M., Albesiano E., et al. Cutting edge: an in vivo requirement for STAT3 signaling in TH17 development and TH17-dependent autoimmunity. J Immunol 2007, 179:4313-4317.
35. Lutticken C., Wegenka U.M., Yuan J., Buschmann J., Schindler C., Ziemiecki A., et al. Association of transcription factor APRF and protein kinase Jak1 with the interleukin-6 signal transducer gp130. Science 1994, 263:89-92.
36. Grivennikov S., Karin E., Terzic J., Mucida D., Yu G.Y., Vallabhapurapu S., et al. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 2009, 15:103-113.
37. Bollrath J., Phesse T.J., von Burstin V.A., Putoczki T., Bennecke M., Bateman T., et al. Gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis. Cancer Cell 2009, 15:91-102.
38. Atreya R., Mudter J., Finotto S., Mullberg J., Jostock T., Wirtz S., et al. Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in crohn disease and experimental colitis in vivo. Nat Med 2000, 6:583-588.
39. Liu X., Lee Y.S., Yu C.R., Egwuagu C.E. Loss of STAT3 in CD4+ T cells prevents development of experimental autoimmune diseases. J Immunol 2008, 180:6070-6076.
40. Murakami M., Kamimura D., Hirano T. New IL-6 (gp130) family cytokine members, CLC/NNT1/BSF3 and IL-27. Growth Factors 2004, 22:75-77.
41. Collison L.W., Delgoffe G.M., Guy C.S., Vignali K.M., Chaturvedi V., Fairweather D., et al. The composition and signaling of the IL-35 receptor are unconventional. Nat Immunol 2012, 13:290-299.
42. Schuster B., Kovaleva M., Sun Y., Regenhard P., Matthews V., Grotzinger J., et al. Signaling of human ciliary neurotrophic factor (CNTF) revisited. The interleukin-6 receptor can serve as an alpha-receptor for CTNF. J Biol Chem 2003, 278:9528-9535.
43. Lust J.A., Donovan K.A., Kline M.P., Greipp P.R., Kyle R.A., Maihle N.J. Isolation of an mRNA encoding a soluble form of the human interleukin-6 receptor. Cytokine 1992, 4:96-100.
44. Matthews V., Schuster B., Schutze S., Bussmeyer I., Ludwig A., Hundhausen C., et al. Cellular cholesterol depletion triggers shedding of the human interleukin-6 receptor by ADAM10 and ADAM17 (TACE). J Biol Chem 2003, 278:38829-38839.
45. Lissilaa R., Buatois V., Magistrelli G., Williams A.S., Jones G.W., Herren S., et al. Although IL-6 trans-signaling is sufficient to drive local immune responses, classical IL-6 signaling is obligate for the induction of T cell-mediated autoimmunity. J Immunol 2010, 185:5512-5521.
46. Laurence A., Tato C.M., Davidson T.S., Kanno Y., Chen Z., Yao Z., et al. Interleukin-2 signaling via STAT5 constrains T helper 17 cell generation. Immunity 2007, 26:371-381.
47. Johnston R.J., Choi Y.S., Diamond J.A., Yang J.A., Crotty S. STAT5 is a potent negative regulator of TFH cell differentiation. J Exp Med 2012, 209:243-250.
48. Yang X.P., Ghoreschi K., Steward-Tharp S.M., Rodriguez-Canales J., Zhu J., Grainger J.R., et al. Opposing regulation of the locus encoding IL-17 through direct, reciprocal actions of STAT3 and STAT5. Nat Immunol 2011, 12:247-254.
49. Wei L., Laurence A., O'Shea J.J. New insights into the roles of Stat5a/b and Stat3 in T cell development and differentiation. Semin Cell Dev Biol 2008, 19:394-400.
50. Crabe S., Guay-Giroux A., Tormo A.J., Duluc D., Lissilaa R., Guilhot F., et al. The IL-27 p28 subunit binds cytokine-like factor 1 to form a cytokine regulating NK and T cell activities requiring IL-6R for signaling. J Immunol 2009, 183:7692-7702.
51. Cognet I., Guilhot F., Chevalier S., Guay-Giroux A., Bert A., Elson G.C., et al. Expression of biologically active mouse ciliary neutrophic factor (CNTF) and soluble CNTFRalpha in Escherichia coli and characterization of their functional specificities. Eur Cytokine Netw 2004, 15:255-262.
52. Kimmel A.R., Berger S.L. Preparation of cDNA and the generation of cDNA libraries: overview. Methods Enzymol 1987, 152:307-316.
53. Baron C., Somogyi R., Greller L.D., Rineau V., Wilkinson P., Cho C.R., et al. Prediction of graft-versus-host disease in humans by donor gene-expression profiling. PLoS Med 2007, 4:e23.
54. Kamimura D., Ishihara K., Hirano T. IL-6 signal transduction and its physiological roles: the signal orchestration model. Rev Physiol Biochem Pharmacol 2003, 149:1-38.
55. Lucas S., Ghilardi N., Li J., de Sauvage F.J. IL-27 regulates IL-12 responsiveness of naive CD4+ T cells through Stat1-dependent and -independent mechanisms. Proc Natl Acad Sci USA 2003, 100:15047-15052.
56. Nurieva R.I., Podd A., Chen Y., Alekseev A.M., Yu M., Qi X., et al. STAT5 negatively regulates T follicular helper (Tfh) cell generation and function. J Biol Chem 2012.
57. Damas P., Ledoux D., Nys M., Vrindts Y., De Groote D., Franchimont P., et al. Cytokine serum level during severe sepsis in human IL-6 as a marker of severity. Ann Surg 1992, 215:356-362.
58. Hack C.E., De Groot E.R., Felt-Bersma R.J., Nuijens J.H., Strack Van Schijndel R.J., Eerenberg-Belmer A.J., et al. Increased plasma levels of interleukin-6 in sepsis. Blood 1989, 74:1704-1710.
59. Pinsky M.R., Vincent J.L., Deviere J., Alegre M., Kahn R.J., Dupont E. Serum cytokine levels in human septic shock. Relation to multiple-system organ failure and mortality. Chest 1993, 103:565-575.
60. Waage A., Brandtzaeg P., Halstensen A., Kierulf P., Espevik T. The complex pattern of cytokines in serum from patients with meningococcal septic shock. Association between interleukin 6, interleukin 1, and fatal outcome. J Exp Med 1989, 169:333-338.
61. Haan S., Keller J.F., Behrmann I., Heinrich P.C., Haan C. Multiple reasons for an inefficient STAT1 response upon IL-6-type cytokine stimulation. Cell Signal 2005, 17:1542-1550.
62. Feldman G.M., Rosenthal L.A., Liu X., Hayes M.P., Wynshaw-Boris A., Leonard W.J., et al. STAT5A-deficient mice demonstrate a defect in granulocyte-macrophage colony-stimulating factor-induced proliferation and gene expression. Blood 1997, 90:1768-1776.
63. Matsumoto A., Masuhara M., Mitsui K., Yokouchi M., Ohtsubo M., Misawa H., et al. CIS, a cytokine inducible SH2 protein, is a target of the JAK-STAT5 pathway and modulates STAT5 activation. Blood 1997, 89:3148-3154.
64. Yoshimura A., Ohkubo T., Kiguchi T., Jenkins N.A., Gilbert D.J., Copeland N.G., et al. A novel cytokine-inducible gene CIS encodes an SH2-containing protein that binds to tyrosine-phosphorylated interleukin 3 and erythropoietin receptors. EMBO J 1995, 14:2816-2826.
65. Lin J.X., Migone T.S., Tsang M., Friedmann M., Weatherbee J.A., Zhou L., et al. The role of shared receptor motifs and common Stat proteins in the generation of cytokine pleiotropy and redundancy by IL-2, IL-4, IL-7, IL-13, and IL-15. Immunity 1995, 2:331-339.
66. Pflanz S., Timans J.C., Cheung J., Rosales R., Kanzler H., Gilbert 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.
67. Kotake S., Sato K., Kim K.J., Takahashi N., Udagawa N., Nakamura I., et al. Interleukin-6 and soluble interleukin-6 receptors in the synovial fluids from rheumatoid arthritis patients are responsible for osteoclast-like cell formation. J Bone Miner Res 1996, 11:88-95.
68. Yoshizaki K., Matsuda T., Nishimoto N., Kuritani T., Taeho L., Aozasa K., et al. Pathogenic significance of interleukin-6 (IL-6/BSF-2) in Castleman's disease. Blood 1989, 74:1360-1367.
69. Nakajima H., Liu X.W., Wynshaw-Boris A., Rosenthal L.A., Imada K., Finbloom D.S., et al. An indirect effect of Stat5a in IL-2-induced proliferation: a critical role for Stat5a in IL-2-mediated IL-2 receptor alpha chain induction. Immunity 1997, 7:691-701.
70. Yao Z., Kanno Y., Kerenyi M., Stephens G., Durant L., Watford W.T., et al. Nonredundant roles for Stat5a/b in directly regulating Foxp3. Blood 2007, 109:4368-4375.
71. Hosui A., Kimura A., Yamaji D., Zhu B.M., Na R., Hennighausen L. Loss of STAT5 causes liver fibrosis and cancer development through increased TGF-{beta} and STAT3 activation. J Exp Med 2009, 206:819-831.
72. Li M.O., Wan Y.Y., Flavell R.A. T cell-produced transforming growth factor-beta1 controls T cell tolerance and regulates Th1- and Th17-cell differentiation. Immunity 2007, 26:579-591.
73. Pesu M., Watford W.T., Wei L., Xu L., Fuss I., Strober W., et al. T-cell-expressed proprotein convertase furin is essential for maintenance of peripheral immune tolerance. Nature 2008, 455:246-250.
74. Classen S., Zander T., Eggle D., Chemnitz J.M., Brors B., Buchmann I., et al. Human resting CD4+ T cells are constitutively inhibited by TGF beta under steady-state conditions. J Immunol 2007, 178:6931-6940.
75. Mitsuyama K., Matsumoto S., Rose-John S., Suzuki A., Hara T., Tomiyasu N., et al. STAT3 activation via interleukin 6 trans-signalling contributes to ileitis in SAMP1/Yit mice. Gut 2006, 55:1263-1269.
76. Nowell M.A., Richards P.J., Horiuchi S., Yamamoto N., Rose-John S., Topley N., et al. Soluble IL-6 receptor governs IL-6 activity in experimental arthritis: blockade of arthritis severity by soluble glycoprotein 130. J Immunol 2003, 171:3202-3209.
77. Richards P.J., Nowell M.A., Horiuchi S., McLoughlin R.M., Fielding C.A., Grau S., et al. Functional characterization of a soluble gp130 isoform and its therapeutic capacity in an experimental model of inflammatory arthritis. Arthritis Rheum 2006, 54:1662-1672.
78. Nowell M.A., Williams A.S., Carty S.A., Scheller J., Hayes A.J., Jones G.W., et al. Therapeutic targeting of IL-6 trans signaling counteracts STAT3 control of experimental inflammatory arthritis. J Immunol 2009, 182:613-622.
79. Becker C., Fantini M.C., Schramm C., Lehr H.A., Wirtz S., Nikolaev A., et al. TGF-beta suppresses tumor progression in colon cancer by inhibition of IL-6 trans-signaling. Immunity 2004, 21:491-501.
80. Fujitani Y., Hibi M., Fukada T., Takahashi-Tezuka M., Yoshida H., Yamaguchi T., et al. An alternative pathway for STAT activation that is mediated by the direct interaction between JAK and STAT. Oncogene 1997, 14:751-761.
81. Lai C.F., Ripperger J., Morella K.K., Wang Y., Gearing D.P., Horseman N.D., et al. STAT3 and STAT5B are targets of two different signal pathways activated by hematopoietin receptors and control transcription via separate cytokine response elements. J Biol Chem 1995, 270:23254-23257.
82. Ripperger J.A., Fritz S., Richter K., Hocke G.M., Lottspeich F., Fey G.H. Transcription factors Stat3 and Stat5b are present in rat liver nuclei late in an acute phase response and bind interleukin-6 response elements. J Biol Chem 1995, 270:29998-30006.
83. Haftchenary S., Avadisian M., Gunning P.T. Inhibiting aberrant Stat3 function with molecular therapeutics: a progress report. Anticancer Drugs 2011, 22:115-127.
84. Lavecchia A., Di Giovanni C., Novellino E. STAT-3 inhibitors: state of the art and new horizons for cancer treatment. Curr Med Chem 2011, 18:2359-2375.
85. Veeriah S., Brennan C., Meng S., Singh B., Fagin J.A., Solit D.B., et al. The tyrosine phosphatase PTPRD is a tumor suppressor that is frequently inactivated and mutated in glioblastoma and other human cancers. Proc Natl Acad Sci USA 2009, 106:9435-9440.
86. Zhang X., Guo A., Yu J., Possemato A., Chen Y., Zheng W., et al. Identification of STAT3 as a substrate of receptor protein tyrosine phosphatase T. Proc Natl Acad Sci USA 2007, 104:4060-4064.