Protein kinase Cε regulates proliferation and cell sensitivity to TGF-1β of CD4 + T lymphocytes: Implications for Hashimoto thyroiditis

Journal of Immunology

Volumn 187, Issue 9, 2011, Pages 4721-4732

  Mirandola, Prisco ^a   Gobbi, Giuliana ^a   Masselli, Elena ^a   Micheloni, Cristina ^a   Di Marcantonio, Daniela ^a   Queirolo, Valeria ^a   Chiodera, Paolo ^a   Meschi, Tiziana ^a   Vitale, Marco ^a  

^a UNIVERSITY OF PARMA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 2 RECEPTOR; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 2 RECEPTOR BETA; INTERLEUKIN 2 RECEPTOR GAMMA; MONOCLONAL ANTIBODY CD28; MONOCLONAL ANTIBODY CD3; PROTEIN KINASE C EPSILON; TRANSFORMING GROWTH FACTOR BETA1;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CELL COUNT; CELL DEATH; CELL STIMULATION; CELL SURVIVAL; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; HASHIMOTO DISEASE; HUMAN; HUMAN CELL; IMMUNOPATHOGENESIS; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; MALE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

ADULT; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CELLS, CULTURED; FEMALE; HASHIMOTO DISEASE; HUMANS; JURKAT CELLS; LYMPHOCYTE ACTIVATION; MALE; MICE; MIDDLE AGED; PROTEIN KINASE C-EPSILON; TRANSFORMING GROWTH FACTOR BETA1;

EID: 80555154815     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1003258     Document Type: Article

References (58)

1. Basu, A., and U. Sivaprasad. 2007. Protein kinase Cepsilon makes the life and death decision. Cell. Signal. 19: 1633-1642. (Pubitemid 46935437)
2. Altman, A., N. Isakov, and G. Baier. 2000. Protein kinase Ctheta: a new essential superstar on the T-cell stage. Immunol. Today 21: 567-573.
3. Isakov, N., and A. Altman. 2002. Protein kinase C(theta) in T cell activation. Annu. Rev. Immunol. 20: 761-794. (Pubitemid 34293439)
4. Keenan, C., Y. Volkov, D. Kelleher, and A. Long. 1997. Subcellular localization and translocation of protein kinase C isoforms zeta and epsilon in human peripheral blood lymphocytes. Int. Immunol. 9: 1431-1439. (Pubitemid 27434675)
5. Genot, E. M., P. J. Parker, and D. A. Cantrell. 1995. Analysis of the role of protein kinase C-alpha, -epsilon, and -zeta in T cell activation. J. Biol. Chem. 270: 9833-9839.
6. Szamel, M., A. Appel, R. Schwinzer, and K. Resch. 1998. Different protein kinase C isoenzymes regulate IL-2 receptor expression or IL-2 synthesis in human lymphocytes stimulated via the TCR. J. Immunol. 160: 2207-2214. (Pubitemid 28119900)
7. Castrillo, A., D. J. Pennington, F. Otto, P. J. Parker, M. J. Owen, and L. Boscá. 2001. Protein kinase Cepsilon is required for macrophage activation and defense against bacterial infection. J. Exp. Med. 194: 1231-1242. (Pubitemid 33055042)
8. Roncarolo, M. G., S. Gregori, M. Battaglia, R. Bacchetta, K. Fleischhauer, and M. K. Levings. 2006. Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunol. Rev. 212: 28-50. (Pubitemid 44116698)
9. Sitkovsky, M. V. 2009. T regulatory cells: hypoxia-adenosinergic suppression and re-direction of the immune response. Trends Immunol. 30: 102-108.
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 beta by human T lymphocytes and its potential role in the regulation of T cell growth. J. Exp. Med. 163: 1037-1050. (Pubitemid 16000407)
11. Wolfraim, L. A., T. M. Walz, Z. James, T. Fernandez, and J. J. Letterio. 2004. p21Cip1 and p27Kip1 act in synergy to alter the sensitivity of naive T cells to TGF-beta-mediated G1 arrest through modulation of IL-2 responsiveness. J. Immunol. 173: 3093-3102. (Pubitemid 39142015)
12. Rubtsov, Y. P., and A. Y. Rudensky. 2007. TGFbeta signalling in control of T-cell-mediated self-reactivity. Nat. Rev. Immunol. 7: 443-453. (Pubitemid 46834850)
13. Li, M. O., Y. Y. Wan, S. Sanjabi, A. K. Robertson, and R. A. Flavell. 2006. Transforming growth factor-beta regulation of immune responses. Annu. Rev. Immunol. 24: 99-146.
14. Gorelik, L., and R. A. Flavell. 2000. Abrogation of TGFbeta signaling in T cells leads to spontaneous T cell differentiation and autoimmune disease. Immunity 12: 171-181. (Pubitemid 30398631)
15. Kulkarni, A. B., C. G. Huh, D. Becker, A. Geiser, M. Lyght, K. C. Flanders, A. B. Roberts, M. B. Sporn, J. M. Ward, and S. Karlsson. 1993. Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death. Proc. Natl. Acad. Sci. USA 90: 770-774. (Pubitemid 23028947)
16. Selvaraj, R. K., and T. L. Geiger. 2007. A kinetic and dynamic analysis of Foxp3 induced in T cells by TGF-beta. J. Immunol. 178: 7667-7677. (Pubitemid 46898037)
17. Fontenot, J. D., J. P. Rasmussen, L. M. Williams, J. L. Dooley, A. G. Farr, and A. Y. Rudensky. 2005. Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity 22: 329-341. (Pubitemid 40387475)
18. Deaglio, S., K. M. Dwyer, W. Gao, D. Friedman, A. Usheva, A. Erat, J. F. Chen, K. Enjyoji, J. Linden, M. Oukka, et al. 2007. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J. Exp. Med. 204: 1257-1265. (Pubitemid 46919862)
19. Nakamura, K., A. Kitani, and W. Strober. 2001. Cell contact-dependent immunosuppression by CD4(+)CD25(+) regulatory T cells is mediated by cell surfacebound transforming growth factor beta. J. Exp. Med. 194: 629-644. (Pubitemid 32844773)
20. Sakaguchi, S., N. Sakaguchi, M. Asano, M. Itoh, and M. Toda. 1995. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155: 1151-1164.
21. McHugh, R. S., and E. M. Shevach. 2002. Cutting edge: depletion of CD4+ CD25+ regulatory T cells is necessary, but not sufficient, for induction of organspecific autoimmune disease. J. Immunol. 168: 5979-5983. (Pubitemid 34620008)
22. Morris, G. P., Y. Yan, C. S. David, and Y. C. Kong. 2005. H2A- and H2E-derived CD4+CD25+ regulatory T cells: a potential role in reciprocal inhibition by class II genes in autoimmune thyroiditis. J. Immunol. 174: 3111-3116. (Pubitemid 40279734)
23. Wang, S. H., and J. R. Baker. 2007. The role of apoptosis in thyroid autoimmunity. Thyroid 17: 975-979. (Pubitemid 350071601)
24. Stassi, G., and R. De Maria. 2002. Autoimmune thyroid disease: new models of cell death in autoimmunity. Nat. Rev. Immunol. 2: 195-204. (Pubitemid 37328766)
25. Vural, P., S. Degirmencioglu, S. Erden, and A. Gelincik. 2009. The relationship between transforming growth factor-beta1, vascular endothelial growth factor, nitric oxide and Hashimoto's thyroiditis. Int. Immunopharmacol. 9: 212-215.
26. Marazuela, M., M. A. García-López, N. Figueroa-Vega, H. de la Fuente, B. Alvarado-Sánchez, A. Monsiváis-Urenda, F. Sánchez-Madrid, and R. González-Amaro. 2006. Regulatory T cells in human autoimmune thyroid disease. J. Clin. Endocrinol. Metab. 91: 3639-3646. (Pubitemid 44402149)
27. Secchiero, P., P. Mirandola, D. Zella, C. Celeghini, A. Gonelli, M. Vitale, S. Capitani, and G. Zauli. 2001. Human herpesvirus 7 induces the functional upregulation of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) coupled to TRAIL-R1 down-modulation in CD4(+) T cells. Blood 98: 2474- 2481.
28. Secchiero, P., D. Zella, S. Curreli, P. Mirandola, S. Capitani, R. C. Gallo, and G. Zauli. 2000. Engagement of CD28 modulates CXC chemokine receptor 4 surface expression in both resting and CD3-stimulated CD4+ T cells. J. Immunol. 164: 4018-4024. (Pubitemid 30215055)
29. Secchiero, P., D. Zella, S. Curreli, P. Mirandola, S. Capitani, R. C. Gallo, and G. Zauli. 2000. Pivotal role of cyclic nucleoside phosphodiesterase 4 in Tatmediated CD4+ T cell hyperactivation and HIV type 1 replication. Proc. Natl. Acad. Sci. USA 97: 14620-14625. (Pubitemid 32016625)
30. Mirandola, P., G. Gobbi, I. Sponzilli, M. Pambianco, C. Malinverno, A. Cacchioli, G. De Panfilis, and M. Vitale. 2007. Exogenous hydrogen sulfide induces functional inhibition and cell death of cytotoxic lymphocytes subsets. J. Cell. Physiol. 213: 826-833. (Pubitemid 350058277)
31. Classen, S., T. Zander, D. Eggle, J. M. Chemnitz, B. Brors, I. Büchmann, A. Popov, M. Beyer, R. Eils, S. Debey, and J. L. Schultze. 2007. Human resting CD4+ T cells are constitutively inhibited by TGF beta under steady-state conditions. J. Immunol. 178: 6931-6940. (Pubitemid 46847419)
32. Mirandola, P., G. Gobbi, C. Ponti, I. Sponzilli, L. Cocco, and M. Vitale. 2006. PKCepsilon controls protection against TRAIL in erythroid progenitors. Blood 107: 508-513. (Pubitemid 43076372)
33. Gobbi, G., P. Mirandola, I. Sponzilli, C. Micheloni, C. Malinverno, L. Cocco, and M. Vitale. 2007. Timing and expression level of protein kinase C epsilon regulate the megakaryocytic differentiation of human CD34 cells. Stem Cells 25: 2322-2329. (Pubitemid 47480491)
34. Ivaska, J., R. D. Whelan, R. Watson, and P. J. Parker. 2002. PKC epsilon controls the traffic of beta1 integrins in motile cells. EMBO J. 21: 3608-3619. (Pubitemid 34787035)
35. Hughes-Fulford, M., E. Sugano, T. Schopper, C. F. Li, J. B. Boonyaratanakornkit and A. Cogoli. 2005. Early immune response and regulation of IL-2 receptor subunits. Cell. Signal. 17: 1111-1124. (Pubitemid 40933531)
36. Lipscomb, M. W., L. Chen, J. L. Taylor, C. Goldbach, S. C. Watkins, P. Kalinski, L. H. Butterfield, A. K. Wesa, and W. J. Storkus. 2009. Ectopic T-bet expression licenses dendritic cells for IL-12-independent priming of type 1 T cells in vitro. J. Immunol. 183: 7250-7258.
37. Cenni, V., H. Döppler, E. D. Sonnenburg, N. Maraldi, A. C. Newton, and A. Toker. 2002. Regulation of novel protein kinase C epsilon by phosphorylation. Biochem. J. 363: 537-545. (Pubitemid 34526374)
38. Karin, M., and A. Lin. 2002. NF-kappaB at the crossroads of life and death. Nat. Immunol. 3: 221-227.
39. Perkins, N. D. 2007. Integrating cell-signalling pathways with NF-kappaB and IKK function. Nat. Rev. Mol. Cell Biol. 8: 49-62. (Pubitemid 46012014)
40. Lan, R. Y., C. Selmi, and M. E. Gershwin. 2008. The regulatory, inflammatory, and T cell programming roles of interleukin-2 (IL-2). J. Autoimmun. 31: 7-12.
41. Kim, H. P., J. Imbert, and W. J. Leonard. 2006. Both integrated and differential regulation of components of the IL-2/IL-2 receptor system. Cytokine Growth Factor Rev. 17: 349-366. (Pubitemid 44604346)
42. Giroux, M., J. S. Delisle, A. O'Brien, M. J. Hébert, and C. Perreault. 2010. T cell activation leads to protein kinase C theta-dependent inhibition of TGF-beta signaling. J. Immunol. 185: 1568-1576.
43. McKarns, S. C., R. H. Schwartz, and N. E. Kaminski. 2004. Smad3 is essential for TGF-beta 1 to suppress IL-2 production and TCR-induced proliferation, but not IL-2-induced proliferation. J. Immunol. 172: 4275-4284. (Pubitemid 38375241)
44. Elyaman, W., E. M. Bradshaw, C. Uyttenhove, V. Dardalhon, A. Awasthi, J. Imitola, E. Bettelli, M. Oukka, J. van Snick, J. C. Renauld, et al. 2009. IL-9 induces differentiation of TH17 cells and enhances function of FoxP3+ natural regulatory T cells. Proc. Natl. Acad. Sci. USA 106: 12885-12890.
45. Hucho, T. B., O. A. Dina, and J. D. Levine. 2005. Epac mediates a cAMP-to- PKC signaling in inflammatory pain: an isolectin B4(+) neuron-specific mechanism. J. Neurosci. 25: 6119-6126. (Pubitemid 40923478)
46. Aksoy, E., M. Goldman, and F. Willems. 2004. Protein kinase C epsilon: a new target to control inflammation and immune-mediated disorders. Int. J. Biochem. Cell Biol. 36: 183-188. (Pubitemid 37487754)
47. Koyanagi, T., K. Noguchi, A. Ootani, K. Inagaki, R. C. Robbins, and D. Mochly- Rosen. 2007. Pharmacological inhibition of epsilon PKC suppresses chronic inflammation in murine cardiac transplantation model. J. Mol. Cell. Cardiol. 43: 517-522. (Pubitemid 47451418)
48. Gruber, T., N. Thuille, N. Hermann-Kleiter, M. Leitges, and G. Baier. 2005. Protein kinase Cepsilon is dispensable for TCR/CD3-signaling. Mol. Immunol. 42: 305-310. (Pubitemid 39626762)
49. Durgan, J., A. J. Cameron, A. T. Saurin, S. Hanrahan, N. Totty, R. O. Messing, and P. J. Parker. 2008. The identification and characterization of novel PKCepsilon phosphorylation sites provide evidence for functional cross-talk within the PKC superfamily. Biochem. J. 411: 319-331. (Pubitemid 351580184)
50. Saurin, A. T., J. Durgan, A. J. Cameron, A. Faisal, M. S. Marber, and P. J. Parker. 2008. The regulated assembly of a PKCepsilon complex controls the completion of cytokinesis. Nat. Cell Biol. 10: 891-901.
51. Karin, M., and Y. Ben-Neriah. 2000. Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu. Rev. Immunol. 18: 621-663. (Pubitemid 30365393)
52. Baldwin, A. S., Jr. 1996. The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu. Rev. Immunol. 14: 649-683.
53. Finco, T. S., and A. S. Baldwin. 1995. Mechanistic aspects of NF-kappa B regulation: the emerging role of phosphorylation and proteolysis. Immunity 3: 263-272.
54. Pears, C. J., K. Thornber, J. M. Auger, C. E. Hughes, B. Grygielska, M. B. Protty, A. C. Pearce, and S. P. Watson. 2008. Differential roles of the PKC novel isoforms, PKCdelta and PKCepsilon, in mouse and human platelets. PLoS ONE 3: e3793.
55. Gray, M. O., H. Z. Zhou, I. Schafhalter-Zoppoth, P. Zhu, D. Mochly-Rosen, and R. O. Messing. 2004. Preservation of base-line hemodynamic function and loss of inducible cardioprotection in adult mice lacking protein kinase C epsilon. J. Biol. Chem. 279: 3596-3604. (Pubitemid 38140600)
56. Ways, D. K., C. A. Kukoly, J. deVente, J. L. Hooker, W. O. Bryant, K. J. Posekany, D. J. Fletcher, P. P. Cook, and P. J. Parker. 1995. MCF-7 breast cancer cells transfected with protein kinase C-alpha exhibit altered expression of other protein kinase C isoforms and display a more aggressive neoplastic phenotype. J. Clin. Invest. 95: 1906-1915.
57. Pass, J. M., J. Gao, W. K. Jones, W. B. Wead, X. Wu, J. Zhang, C. P. Baines, R. Bolli, Y. T. Zheng, I. G. Joshua, and P. Ping. 2001. Enhanced PKC beta II translocation and PKC beta II-RACK1 interactions in PKC epsilon-induced heart failure: a role for RACK1. Am. J. Physiol. Heart. Circ. Physiol. 281: H2500-H2510.
58. Takimoto, T., Y. Wakabayashi, T. Sekiya, N. Inoue, R. Morita, K. Ichiyama, R. Takahashi, M. Asakawa, G. Muto, T. Mori, et al. 2010. Smad2 and Smad3 are redundantly essential for the TGF-beta-mediated regulation of regulatory T plasticity and Th1 development. [Published erratum appears in 2011 J. Immunol. 186: 632]. J. Immunol. 185: 842-855.