Protein kinase D orchestrates the activation of DRAK2 in response to TCR-induced Ca2+ influx and mitochondrial reactive oxygen generation

Journal of Immunology

Volumn 186, Issue 2, 2011, Pages 940-950

  Newton, Ryan H ^a,b   Leverrier, Sabrina ^a   Srikanth, Sonal ^c   Gwack, Yousang ^c   Cahalan, Michael D ^a   Walsh, Craig M ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

12 (2 CYANOETHYL) 6,7,12,13 TETRAHYDRO 13 METHYL 5 OXOINDOLO[2,3 A]PYRROLO[3,4 C]CARBAZOLE; CALCIUM CHANNEL; CALCIUM ION; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; DRAK2 PROTEIN; PROTEIN KINASE D; PROTEIN SERINE THREONINE KINASE; REACTIVE OXYGEN METABOLITE; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM HOMEOSTASIS; CALCIUM MOBILIZATION; CALCIUM TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; EXTRACELLULAR CALCIUM; HUMAN; HUMAN CELL; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; CALCIUM SIGNALING; CLONE CELLS; ENZYME ACTIVATION; HOMEOSTASIS; HUMANS; JURKAT CELLS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MITOCHONDRIA; PROTEIN KINASE C; PROTEIN-SERINE-THREONINE KINASES; REACTIVE OXYGEN SPECIES; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES;

EID: 79251534056     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1000942     Document Type: Article

References (52)

1. McGargill, M. A., B. G. Wen, C. M. Walsh, and S. M. Hedrick. 2004. A deficiency in Drak2 results in a T cell hypersensitivity and an unexpected resistance to autoimmunity. Immunity 21: 781-791.
2. Friedrich, M. L., B. G. Wen, G. Bain, B. L. Kee, C. Katayama, C. Murre, S. M. Hedrick, and C. M. Walsh. 2005. DRAK2, a lymphoid-enriched DAP kinase, regulates the TCR activation threshold during thymocyte selection. Int. Immunol. 17: 1379-1390.
3. Ramos, S. J., J. B. Hernandez, M. Gatzka, and C. M. Walsh. 2008. Enhanced T cell apoptosis within Drak2-deficient mice promotes resistance to autoimmunity. J. Immunol. 181: 7606-7616.
4. McGargill, M. A., C. Choy, B. G. Wen, and S. M. Hedrick. 2008. Drak2 regulates the survival of activated T cells and is required for organ-specific autoimmune disease. J. Immunol. 181: 7593-7605.
5. Kögel, D., J. H. Prehn, and K. H. Scheidtmann. 2001. The DAP kinase family of pro-apoptotic proteins: novel players in the apoptotic game. Bioessays 23: 352-358.
6. Kuwahara, H., N. Nakamura, and H. Kanazawa. 2006. Nuclear localization of the serine/threonine kinase DRAK2 is involved in UV-induced apoptosis. Biol. Pharm. Bull. 29: 225-233.
7. Kuwahara, H., M. Nishizaki, and H. Kanazawa. 2008. Nuclear localization signal and phosphorylation of serine350 specify intracellular localization of DRAK2. J. Biochem. 143: 349-358.
8. Friedrich, M. L., M. Cui, J. B. Hernandez, B. M. Weist, H. M. Andersen, X. Zhang, L. Huang, and C. M. Walsh. 2007. Modulation of DRAK2 autophosphorylation by antigen receptor signaling in primary lymphocytes. J. Biol. Chem. 282: 4573-4584.
9. Rozengurt, E., O. Rey, and R. T. Waldron. 2005. Protein kinase D signaling. J. Biol. Chem. 280: 13205-13208.
10. Irie, A., K. Harada, H. Tsukamoto, J. R. Kim, N. Araki, and Y. Nishimura. 2006. Protein kinase D2 contributes to either IL-2 promoter regulation or induction of cell death upon TCR stimulation depending on its activity in Jurkat cells. Int. Immunol. 18: 1737-1747.
11. Matthews, S. A., E. Rozengurt, and D. Cantrell. 2000. Protein kinase D: a selective target for antigen receptors and a downstream target for protein kinase C in lymphocytes. J. Exp. Med. 191: 2075-2082.
12. Marklund, U., K. Lightfoot, and D. Cantrell. 2003. Intracellular location and cell context-dependent function of protein kinase D. Immunity 19: 491-501.
13. Matthews, S. A., T. Iglesias, E. Rozengurt, and D. Cantrell. 2000. Spatial and temporal regulation of protein kinase D (PKD). EMBO J. 19: 2935-2945. (Pubitemid 30386765)
14. Waldron, R. T., and E. Rozengurt. 2003. Protein kinase C phosphorylates protein kinase D activation loop Ser744 and Ser748 and releases autoinhibition by the pleckstrin homology domain. J. Biol. Chem. 278: 154-163.
15. Sinnett-Smith, J., R. Jacamo, R. Kui, Y. M. Wang, S. H. Young, O. Rey, R. T. Waldron, and E. Rozengurt. 2009. Protein kinase D mediates mitogenic signaling by Gq-coupled receptors through protein kinase C-independent regulation of activation loop Ser744 and Ser748 phosphorylation. J. Biol. Chem. 284: 13434-13445.
16. Zhang, W., S. Zheng, P. Storz, and W. Min. 2005. Protein kinase D specifically mediates apoptosis signal-regulating kinase 1-JNK signaling induced by H2O2 but not tumor necrosis factor. J. Biol. Chem. 280: 19036-19044.
17. Storz, P., H. Döppler, and A. Toker. 2005. Protein kinase D mediates mitochondrion-to-nucleus signaling and detoxification from mitochondrial reactive oxygen species. Mol. Cell. Biol. 25: 8520-8530.
18. Kunkel, M. T., A. Toker, R. Y. Tsien, and A. C. Newton. 2007. Calcium-dependent regulation of protein kinase D revealed by a genetically encoded kinase activity reporter. J. Biol. Chem. 282: 6733-6742.
19. Koncz, P., G. Szanda, L. Fülöp, A. Rajki, and A. Spät. 2009. Mitochondrial Ca2+ uptake is inhibited by a concerted action of p38 MAPK and protein kinase D. Cell Calcium 46: 122-129.
20. Cahalan, M. D., and K. G. Chandy. 2009. The functional network of ion channels in T lymphocytes. Immunol. Rev. 231: 59-87.
21. Crabtree, G. R., and E. N. Olson. 2002. NFAT signaling: choreographing the social lives of cells. Cell 109: S67-S79.
22. Dower, N. A., S. L. Stang, D. A. Bottorff, J. O. Ebinu, P. Dickie, H. L. Ostergaard, and J. C. Stone. 2000. RasGRP is essential for mouse thymocyte differentiation and TCR signaling. Nat. Immunol. 1: 317-321.
23. 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.
24. Feske, S. 2007. Calcium signalling in lymphocyte activation and disease. Nat. Rev. Immunol. 7: 690-702.
25. Gwack, Y., S. Feske, S. Srikanth, P. G. Hogan, and A. Rao. 2007. Signalling to transcription: store-operated Ca2+ entry and NFAT activation in lymphocytes. Cell Calcium 42: 145-156.
26. Gatzka, M., R. H. Newton, and C. M. Walsh. 2009. Altered thymic selection and increased autoimmunity caused by ectopic expression of DRAK2 during T cell development. J. Immunol. 183: 285-297.
27. Gschwendt, M., S. Dieterich, J. Rennecke, W. Kittstein, H. J. Mueller, and F. J. Johannes. 1996. Inhibition of protein kinase C mu by various inhibitors: differentiation from protein kinase C isoenzymes. FEBS Lett. 392: 77-80.
28. Kaye, J., S. Porcelli, J. Tite, B. Jones, and C. A. Janeway, Jr. 1983. Both a monoclonal antibody and antisera specific for determinants unique to individual cloned helper T cell lines can substitute for antigen and antigen-presenting cells in the activation of T cells. J. Exp. Med. 158: 836-856.
29. Kerschbaum, H. H., and M. D. Cahalan. 1999. Single-channel recording of a store-operated Ca2+ channel in Jurkat T lymphocytes. Science 283: 836-839.
30. Cahalan, M. D. 2009. STIMulating store-operated Ca(2+) entry. Nat. Cell Biol. 11: 669-677.
31. Gwack, Y., S. Srikanth, M. Oh-Hora, P. G. Hogan, E. D. Lamperti, M. Yamashita, C. Gelinas, D. S. Neems, Y. Sasaki, S. Feske, et al. 2008. Hair loss and defective T- and B-cell function in mice lacking ORAI1. Mol. Cell. Biol. 28: 5209-5222.
32. Sanjo, H., T. Kawai, and S. Akira. 1998. DRAKs, novel serine/threonine kinases related to death-associated protein kinase that trigger apoptosis. J. Biol. Chem. 273: 29066-29071.
33. Nolen, B., S. Taylor, and G. Ghosh. 2004. Regulation of protein kinases; controlling activity through activation segment conformation. Mol. Cell 15: 661-675.
34. Singh, D. K., D. Kumar, Z. Siddiqui, S. K. Basu, V. Kumar, and K. V. Rao. 2005. The strength of receptor signaling is centrally controlled through a cooperative loop between Ca2+ and an oxidant signal. Cell 121: 281-293.
35. Lee, K., and W. J. Esselman. 2002. Inhibition of PTPs by H(2)O(2) regulates the activation of distinct MAPK pathways. Free Radic. Biol. Med. 33: 1121-1132.
36. Hildeman, D. A., T. Mitchell, T. K. Teague, P. Henson, B. J. Day, J. Kappler, and P. C. Marrack. 1999. Reactive oxygen species regulate activation-induced T cell apoptosis. Immunity 10: 735-744.
37. Tonks, N. K. 2005. Redox redux: revisiting PTPs and the control of cell signaling. Cell 121: 667-670.
38. Reth, M. 2002. Hydrogen peroxide as second messenger in lymphocyte activation. Nat. Immunol. 3: 1129-1134.
39. Capasso, M., M. K. Bhamrah, T. Henley, R. S. Boyd, C. Langlais, K. Cain, D. Dinsdale, K. Pulford, M. Khan, B. Musset, et al. 2010. HVCN1 modulates BCR signal strength via regulation of BCR-dependent generation of reactive oxygen species. Nat. Immunol. 11: 265-272.
40. Döppler, H., and P. Storz. 2007. A novel tyrosine phosphorylation site in protein kinase D contributes to oxidative stress-mediated activation. J. Biol. Chem. 282: 31873-31881.
41. Waldron, R. T., and E. Rozengurt. 2000. Oxidative stress induces protein kinase D activation in intact cells: involvement of Src and dependence on protein kinase C. J. Biol. Chem. 275: 17114-17121.
42. Eisenberg-Lerner, A., and A. Kimchi. 2007. DAP kinase regulates JNK signaling by binding and activating protein kinase D under oxidative stress. Cell Death Differ. 14: 1908-1915. (Pubitemid 350011666)
43. Cowell, C. F., H. Döppler, I. K. Yan, A. Hausser, Y. Umezawa, and P. Storz. 2009. Mitochondrial diacylglycerol initiates protein-kinase D1-mediated ROS signaling. J. Cell Sci. 122: 919-928.
44. Chang, W. K., K. D. Yang, H. Chuang, J. T. Jan, and M. F. Shaio. 2002. Glutamine protects activated human T cells from apoptosis by up-regulating glutathione and Bcl-2 levels. Clin. Immunol. 104: 151-160.
45. Williams, M. S., and J. Kwon. 2004. T cell receptor stimulation, reactive oxygen species, and cell signaling. Free Radic. Biol. Med. 37: 1144-1151.
46. Cárdenas, C., R. A. Miller, I. Smith, T. Bui, J. Molgó, M. Müller, H. Vais, K. H. Cheung, J. Yang, I. Parker, et al. 2010. Essential regulation of cell bioenergetics by constitutive InsP3 receptor Ca2+ transfer to mitochondria. Cell 142: 270-283.
47. Hoth, M., C. M. Fanger, and R. S. Lewis. 1997. Mitochondrial regulation of store-operated calcium signaling in T lymphocytes. J. Cell Biol. 137: 633-648.
48. Quintana, A., C. Schwindling, A. S. Wenning, U. Becherer, J. Rettig, E. C. Schwarz, and M. Hoth. 2007. T cell activation requires mitochondrial translocation to the immunological synapse. Proc. Natl. Acad. Sci. USA 104: 14418-14423.
49. Jones, R. G., T. Bui, C. White, M. Madesh, C. M. Krawczyk, T. Lindsten, B. J. Hawkins, S. Kubek, K. A. Frauwirth, Y. L. Wang, et al. 2007. The proapoptotic factors Bax and Bak regulate T cell proliferation through control of endoplasmic reticulum Ca(2+) homeostasis. Immunity 27: 268-280.
50. Jones, R. G., and C. B. Thompson. 2007. Revving the engine: signal transduction fuels T cell activation. Immunity 27: 173-178.
51. Ramos, S. J., J. L. Hardison, L. N. Stiles, T. E. Lane, and C. M. Walsh. 2007. Anti-viral effector T cell responses and trafficking are not dependent upon DRAK2 signaling following viral infection of the central nervous system. Autoimmunity 40: 54-65.
52. Kerschbaum, H. H., P. A. Negulescu, and M. D. Cahalan. 1997. Ion channels, Ca2+ signaling, and reporter gene expression in antigen-specific mouse T cells. J. Immunol. 159: 1628-1638.