TGF-β inhibits IL-2 production and promotes cell cycle arrest in TCR-activated effector/memory T cells in the presence of sustained TCR signal transduction

Journal of Immunology

Volumn 180, Issue 3, 2008, Pages 1490-1498

  Das, Lopamudra ^a   Levine, Alan D ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD45RA ANTIGEN; CYCLIN D1; DOCKING PROTEIN; INTERLEUKIN 2; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATASE; PHOSPHOLIPASE C GAMMA1; PHOSPHOTRANSFERASE; PROTEIN P21; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE SHP 1; PROTEIN TYROSINE PHOSPHATASE SHP 2; T LYMPHOCYTE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; TYROSINE; CALCIUM; CYTOKINE; LYMPHOCYTE ANTIGEN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PHOSPHOLIPASE C GAMMA; PROTEIN TYROSINE PHOSPHATASE;

ARTICLE; CALCIUM TRANSPORT; CELL ACTIVATION; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL FUNCTION; CELL PROLIFERATION; COMPARATIVE STUDY; CONTROLLED STUDY; EFFECTOR CELL; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; INHIBITION KINETICS; LIGATION; MEMORY T LYMPHOCYTE; NORMAL HUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOBLAST; CELL CULTURE; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; METABOLISM; T LYMPHOCYTE; UPREGULATION;

CALCIUM; CELL CYCLE; CELL PROLIFERATION; CELLS, CULTURED; CYTOKINES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; IMMUNOLOGIC MEMORY; INTERLEUKIN-2; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; PHOSPHOLIPASE C GAMMA; PROTEIN TYROSINE PHOSPHATASES; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRANSFORMING GROWTH FACTOR BETA; TYROSINE; UP-REGULATION;

EID: 40749107840     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.3.1490     Document Type: Article

References (63)

1. + regulatory T cell activity in both humans and mice. J. Immunol. 172: 834-842.
2. + regulatory T cells and TGF-β in oral tolerance. J. Leukocyte Biol. 77: 906-913.
3. Szczepanik, M., M. Tutaj, K. Bryniarski, and B. N. Dittel. 2005. Epicutaneously induced TGF-β-dependent tolerance inhibits experimental autoimmune encephalomyelitis. J. Neuroimmunol. 164: 105-114.
4. Racke, M. K., S. Dhib-Jalbut, B. Cannella, P. S. Albert, C. S. Raine, and D. E. McFarlin. 1991. Prevention and treatment of chronic relapsing experimental allergic encephalomyelitis by transforming growth factor-β1. J. Immunol. 146: 3012-3017.
5. + suppressor cells inhibit the function of effector cells of experimental autoimmune encephalomyelitis through a mechanism involving transforming growth factor-β. J. Immunol. 146: 1163-1168.
6. Santambrogio, L., G. M. Hochwald, B. Saxena, C. H. Leu, J. E. Martz, J. A. Carlino, N. H. Ruddle, M. A. Palladino, L. I. Gold, and G. J. Thorbecke. 1993. Studies on the mechanisms by which transforming growth factor-β (TGF-β) protects against allergic encephalomyelitis: antagonism between TGF-β and tumor necrosis factor. J. Immunol. 151: 1116-1127.
7. Brandes, M. E., J. B. Allen, Y. Ogawa, and S. M. Wahl. 1991. Transforming growth factor β1 suppresses acute and chronic arthritis in experimental animals. J. Clin. Invest. 87: 1108-1113.
8. Youn, J., S. H. Hwang, Z. Y. Ryoo, M. A. Lynes, D. J. Paik, H. S. Chung, and H. Y. Kim. 2002. Metallothionein suppresses collagen-induced arthritis via induction of TGF-β and down-regulation of proinflammatory mediators. Clin. Exp. Immunol. 129: 232-239.
9. R cells suppress innate immune pathology through cytokine-dependent mechanisms. J. Exp. Med. 197: 111-119.
10. Kehrl, J. H., L. M. Wakefield, A. B. Roberts, S. Jakowlew, M. Alvarez-Mon, R. Derynck, M. B. Sporn, and A. S. Fauci. 1986. Production of transforming growth factor β by human T lymphocytes and its potential role in the regulation of T cell growth. J. Exp. Med. 163: 1037-1050.
11. + T cell proliferation without modulating the cytokine response. Int. Immunol. 15: 1495-1504.
12. Choudhry, M. A., O. Sir, and M. M. Sayeed. 2001. TGF-β abrogates TCR-mediated signaling by upregulating tyrosine phosphatases in T cells. Shock 15: 193-199.
13. Siegenthaler, J. A., and M. W. Miller. 2005. Transforming growth factor β1 promotes cell cycle exit through the cyclin-dependent kinase inhibitor p21 in the developing cerebral cortex. J. Neurosci. 25: 8627-8636.
14. Bright, J. J., L. D. Kerr, and S. Sriram. 1997. TGF-β inhibits IL-2-induced tyrosine phosphorylation and activation of Jak-1 and Stat 5 in T lymphocytes. J. Immunol. 159: 175-183.
15. + T cell survival, division, and IL-2 production: a role for T cell intrinsic Smad3. J. Immunol. 174: 2071-2083.
16. 2+ influx, and NFATc translocation causing inhibition of T cell differentiation. J. Exp. Med. 197: 1689-1699.
17. Cantrell, D. 1996. T cell antigen receptor signal transduction pathways. Annu. Rev. Immunol. 14: 259-274.
18. Qian, D., and A. Weiss. 1997. T cell antigen receptor signal transduction. Curr. Opin. Cell Biol. 9: 205-212.
19. Clements, J. L., N. J. Boerth, J. R. Lee, and G. A. Koretzky. 1999. Integration of T cell receptor-dependent signaling pathways by adapter proteins. Annu. Rev. Immunol. 17: 89-108.
20. van Leeuwen, J. E., and L. E. Samelson. 1999. T cell antigen-receptor signal transduction. Curr. Opin. Immunol. 11: 242-248.
21. Zhang, W., J. Sloan-Lancaster, J. Kitchen, R. P. Trible, and L. E. Samelson. 1998. LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell 92: 83-92.
22. 2+ mobilization in Ehrlich ascites tumor cells. Arch. Biochem. Biophys. 245: 84-95.
23. Clark, J. A., A. R. Black, O. V. Leontieva, M. R. Frey, M. A. Pysz, L. Kunneva, A. Woloszynska-Read, D. Roy, and J. D. Black. 2004. Involvement of the ERK signaling cascade in protein kinase C-mediated cell cycle arrest in intestinal epithelial cells. J. Biol. Chem. 279: 9233-9247.
24. + suppressor T cell, NY4.2, in the prevention of autoimmune IDDM in NOD mice. J. Autoimmun. 10: 299-307.
25. Sturm, A., K. A. Krivacic, C. Fiocchi, and A. D. Levine. 2004. Dual function of the extracellular matrix: stimulatory for cell cycle progression of naive T cells and antiapoptotic for tissue-derived memory T cells. J. Immunol. 173: 3889-3900.
26. Mustelin, T., S. Rahmouni, N. Bottini, and A. Alonso. 2003. Role of protein tyrosine phosphatases in T cell activation. Immunol. Rev. 191: 139-147.
27. Kogkopoulou, O., E. Tzakos, G. Mavrothalassitis, C. T. Baldari, F. Paliogianni, H. A. Young, and G. Thyphronitis. 2006. Conditional up-regulation of IL-2 production by p38 MAPK inactivation is mediated by increased Erk1/2 activity. J. Leukocyte Biol. 79: 1052-1060.
28. Dubois, S., W. Shou, L. S. Haneline, S. Fleischer, T. A. Waldmann, and J. R. Muller. 2003. Distinct pathways involving the FK506-binding proteins 12 and 12.6 underlie IL-2-versus IL-15-mediated proliferation of T cells. Proc. Natl. Acad. Sci. USA 100: 14169-14174.
29. Kim, H. P., B. G. Kim, J. Letterio, and W. J. Leonard. 2005. Smad-dependent cooperative regulation of interleukin 2 receptor α chain gene expression by T cell receptor and transforming growth factor-β. J. Biol. Chem. 280: 34042-34047.
30. Chang, F., L. S. Steelman, J. G. Shelton, J. T. Lee, P. M. Navolanic, W. L. Blalock, R. Franklin, and J. A. McCubrey. 2003. Regulation of cell cycle progression and apoptosis by the Ras/Raf/MEK/ERK pathway (review). Int. J. Oncol. 22: 469-480.
31. Wafl/Cip1 by activating p53 and MEK/ERK1/2 MAPK pathways. J. Biol. Chem. 282: 11722-11731.
32. + regulatory T cells and immune tolerance. Autoimmunity 39: 269-276.
33. + natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol. Rev. 212: 8-27.
34. Kumar, V. 2004. Homeostatic control of immunity by TCR peptide-specific Tregs. J. Clin. Invest. 114: 1222-1226.
35. Dahan, S., F. Roth-Walter, P. Arnaboldi, S. Agarwal, and L. Mayer. 2007. Epithelia: lymphocyte interactions in the gut. Immunol. Rev. 215: 243-253.
36. Wahl, S. M., J. Wen, and N. Moutsopoulos. 2006. TGF-β: a mobile purveyor of immune privilege. Immunol. Rev. 213: 213-227.
37. Alard, P., S. L. Clark, and M. M. Kosiewicz. 2004. Mechanisms of tolerance induced by TGF β-treated APC: CD4 regulatory T cells prevent the induction of the immune response possibly through a mechanism involving TGF β. Eur. J. Immunol. 34: 1021-1030.
38. high regulatory T cells that mediate type V collagen-induced tolerance to lung allografts. J. Immunol. 171: 1140-1147.
39. Izcue, A., J. L. Coombes, and F. Powrie. 2006. Regulatory T cells suppress systemic and mucosal immune activation to control intestinal inflammation. Immunol. Rev. 212: 256-271.
40. Jump, R. L., and A. D. Levine. 2004. Mechanisms of natural tolerance in the intestine: implications for inflammatory bowel disease. Inflamm. Bowel Dis. 10: 462-478.
41. Dong, C., Z. Li, R. Alvarez, Jr., X. H. Feng, and P. J. Goldschmidt-Clermont. 2000. Microtubule binding to Smads may regulate TGF β activity. Mol. Cell 5: 27-34.
42. McKarns, S. C., R. H. Schwartz, and N. E. Kaminski. 2004. Smad3 is essential for TGF-β1 to suppress IL-2 production and TCR-induced proliferation, but not IL-2-induced proliferation. J. Immunol. 172: 4275-4284.
43. Hawrylowicz, C. M., and A. O'Garra. 2005. Potential role of interleukin-10-secreting regulatory T cells in allergy and asthma. Nat. Rev. Immunol 5: 271-283.
44. Holzer, U., M. Rieck, and J. H. Buckner. 2006. Lineage and signal strength determine the inhibitory effect of transforming growth factor β1 (TGF-β1) on human antigen-specific Th1 and Th2 memory cells. J. Autoimmun. 26: 241-251.
45. Carrier, Y., J. Yuan, V. K. Kuchroo, and H. L. Weiner. 2007. Th3 cells in peripheral tolerance. II. TGF-β-transgenic Th3 cells rescue IL-2-deficient mice from autoimmunity. J. Immunol. 178: 172-178.
46. - T cells by T cell receptor stimulation is TGFβ-dependent but does not confer a regulatory phenotype. Blood 110: 2983-2990.
47. + T lymphocytes. Int. Immunol. 6: 631-638.
48. Zhang, X., L. Giangreco, H. E. Broome, C. M. Dargan, and S. L. Swain. 1995. Control of CD4 effector fate: transforming growth factor β1 and interleukin 2 synergize to prevent apoptosis and promote effector expansion. J. Exp. Med. 182: 699-709.
49. Cerwenka, A., H. Kovar, O. Majdic, and W. Holter. 1996. Fas- and activation-induced apoptosis are reduced in human T cells preactivated in the presence of TGF-β1. J. Immunol. 156: 459-464.
50. + T cells, IL-2, and NK cell-derived TGF-β: contrasting effects of anti-CD2 and anti-CD3. J. Immunol. 160: 2248-2254.
51. Veldhoen, M., and B. Stockinger. 2006. TGFβ1, a "Jack of all trades": the link with pro-inflammatory IL-17-producing T cells. Trends Immunol. 27: 358-361.
52. Veldhoen, M., R. J. Hocking, R. A. Flavell, and B. Stockinger. 2006. Signals mediated by transforming growth factor-β initiate autoimmune encephalomyelitis, but chronic inflammation is needed to sustain disease. Nat. Immunol. 7: 1151-1156.
53. Qiao, L., G. Schurmann, M. Betzler, and S. C. Meuer. 1991. Activation and signaling status of human lamina propria T lymphocytes. Gastroenterology 101: 1529-1536.
54. Targan, S. R., R. L. Deem, M. Liu, S. Wang, and A. Nel. 1995. Definition of a lamina propria T cell responsive state: enhanced cytokine responsiveness of T cells stimulated through the CD2 pathway. J. Immunol. 154: 664-675.
55. Joseph, N. E., C. Fiocchi, and A. D. Levine. 1997. Chrohn's disease and ulcerative colitis mucosal T cells are stimulated by intestinal epithelial cells: implications for immunosuppressive therapy. Surgery 122: 809-814.
56. Faria, A. M., and H. L. Weiner. 2006. Oral tolerance and TGF-β-producing cells. Inflamm. Allergy Drug Targets 5: 179-190.
57. + lamina propria (LP) lymphokine secretion profiles in inflammatory bowel disease: Crohn's disease LP cells manifest increased secretion of IFN-γ, whereas ulcerative colitis LP cells manifest increased secretion of IL-5. J. Immunol. 157: 1261-1270.
58. Acuto, O., and F. Michel. 2003. CD28-mediated co-stimulation: a quantitative support for TCR signalling. Nat. Rev. Immunol. 3: 939-951.
59. Riley, J. L., M. Mao, S. Kobayashi, M. Biery, J. Burchard, G. Cavet, B. P. Gregson, C. H. June, and P. S. Linsley. 2002. Modulation of TCR-induced transcriptional profiles by ligation of CD28, ICOS, and CTLA-4 receptors. Proc. Natl. Acad. Sci. USA 99: 11790-11795.
60. Su, B., and M. Karin. 1996. Mitogen-activated protein kinase cascades and regulation of gene expression. Curr. Opin. Immunol. 8: 402-411.
61. Marshall, C. J. 1995. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80: 179-185.
62. Reyes, B. M., S. Danese, M. Sans, C. Fiocchi, and A. D. Levine. 2005. Redox equilibrium in mucosal T cells tunes the intestinal TCR signaling threshold. J. Immunol. 175: 2158-2166.
63. Greenwald, R. J., G. J. Freeman, and A. H. Sharpe. 2005. The B7 family revisited. Annu. Rev. Immunol. 23: 515-548.