Protein Kinase Cδ Selectively Regulates Protein Kinase D-Dependent Activation of NF-κB in Oxidative Stress Signaling

Molecular and Cellular Biology

Volumn 24, Issue 7, 2004, Pages 2614-2626

  Storz, Peter ^a   Döppler, Heike ^a   Toker, Alex ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN KINASE C DELTA; PROTEIN KINASE C EPSILON; PROTEIN KINASE C ZETA; PROTEIN KINASE D; SERINE; TYROSINE; ENZYME INHIBITOR; ISOENZYME; PRKCD PROTEIN, HUMAN; PROTEIN KINASE C; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE;

ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME INDUCTION; FEMALE; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; GENETICS; HELA CELL; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; REPORTER GENE; RNA INTERFERENCE;

ENZYME ACTIVATION; ENZYME INHIBITORS; GENES, REPORTER; HELA CELLS; HUMANS; ISOENZYMES; NF-KAPPA B; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN KINASE C-DELTA; PROTO-ONCOGENE PROTEINS C-ABL; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

EID: 1642379541     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.7.2614-2626.2004     Document Type: Article

References (58)

1. Aruoma, O. I., B. Halliwell, B. M. Hoey, and J. Butler. 1989. The antioxidant action of N-acetylcysteine: its reaction with hydrogen peroxide, hydroxyl radical, superoxide, and hypochlorous acid. Free Radic. Biol. Med. 6:593-597.
2. Bauer, B., N. Krumbock, F. Fresser, F. Hochholdinger, M. Spitaler, A. Simm, F. Uberall, B. Schraven, and G. Baier. 2001. Complex formation and cooperation of protein kinase Cθ and Akt1/protein kinase Bα in the NF-κB transactivation cascade in Jurkat T cells. J. Biol. Chem. 276:31627-31634.
3. Brandlin, I., S. Hubner, T. Eiseler, M. Martinez-Moya, A. Horschinek, A. Hausser, G. Link, S. Rupp, P. Storz, K. Pfizenmaier, and F. J. Johannes. 2002. Protein kinasc C (PKC)η-mediated PKCμ activation modulates ERK and JNK signal pathways. J. Biol. Chem. 277:6490-6496.
4. Brodie, C., and P. M. Blumberg. 2003. Regulation of cell apoptosis by protein kinase Cδ. Apoptosis 8:19-27.
5. Brummelkamp, T. R., R. Bernards, and R. Agami. 2002. A system for stable expression of short interfering RNAs in mammalian cells. Science 296:550-553.
6. Cenni, V., H. Doppler, E. D. Sonnenburg, N. Maraldi, A. C. Newton, and A. Toker. 2002. Regulation of novel protein kinase Cε by phosphorylation. Biochem. J. 363:537-545.
7. Chou, M. M., W. Hou, J. Johnson, L. K. Graham, M. H. Lee, C. S. Chen, A. C. Newton, B. S. Schaffhausen, and A. Toker. 1998. Regulation of protein kinase Cζ by PI 3-kinase and PDK-1. Curr. Biol. 8:1069-1077.
8. Coudronniere, N., M. Villalba, N. Englund, and A. Altman. 2000. NF-κB activation induced by T cell receptor/CD28 costimulation is mediated by protein kinase C-θ. Proc. Natl. Acad. Sci. USA 97:3394-3399.
9. Davies, S. P., H. Reddy, M. Caivano, and P. Cohen. 2000. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351:95-105.
10. Duran, A., M. T. Diaz-Meco, and J. Moscat. 2003. Essential role of RelA Ser311 phosphorylation by ζPKC in NF-κB transcriptional activation. EMBO J. 22:3910-3918.
11. Englert, R. P., and E. Shacter. 2002. Distinct modes of cell death induced by different reactive oxygen species: amino acyl chloramines mediate hypochlorous acid-induced apoptosis. J. Biol. Chem. 277:20518-20526.
12. Fan, C., Q. Li, D. Ross, and J. F. Engelhardt. 2003. Tyrosine phosphorylation of IκBα activates NFκB through a redox-regulated and c-Src-dependent mechanism following hypoxia/reoxygenation. J. Biol. Chem. 278:2072-2080.
13. Finkel, T. 2003. Oxidant signals and oxidative stress. Curr. Opin. Cell Biol. 15:247-254.
14. Gschwendt, M., H. J. Muller, K. Kielbassa, R. Zang, W. Kittstein, G. Rincke, and F. Marks. 1994. Rottlerin, a novel protein kinase inhibitor. Biochem. Biophys. Res. Commun. 199:93-98.
15. Hausser, A., G. Link, L. Bamberg, A. Burzlaff, S. Lutz, K. Pfizenmaier, and F. J. Johannes. 2002. Structural requirements for localization and activation of protein kinase Cμ (PKCμ) at the Golgi compartment. J. Cell Biol. 156: 65-74.
16. Hayakawa, M., H. Miyashita, I. Sakamoto, M. Kitagawa, H. Tanaka, H. Yasuda, M. Karin, and K. Kikugawa. 2003. Evidence that reactive oxygen species do not mediate NF-KB activation. EMBO J. 22:3356-3366.
17. Hirano, M., S. Hirai, K. Mizuno, S. Osada, M. Hosaka, and S. Ohno. 1995. A protein kinase C isozyme, nPKCε, is involved in the activation of NF-κB by 12-O-tetradecanoylphorbol-13-acetate (TPA) in rat 3Y1 fibroblasts. Biochem. Biophys. Res. Commun. 206:429-436.
18. Iglesias, T., and E. Rozengurt. 1998. Protein kinase D activation by mutations within its pleckstrin homology domain. J. Biol. Chem. 273:410-416.
19. Iglesias, T., R. T. Waldron, and E. Rozengurt. 1998. Identification of in vivo phosphorylation sites required for protein kinase D activation. J. Biol. Chem. 273:27662-27667.
20. Karin, M. 1999. How NF-κB is activated: the role of the IκB kinase (IKK) complex. Oncogene 18:6867-6874.
21. Karin, M., T. Takahashi, P. Kapahi, M. Delhase, Y. Chen, C. Makris, D. Rothwarf, V. Baud, G. Natoli, F. Guido, and N. Li. 2001. Oxidative stress and gene expression: the AP-1 and NF-κB connections. Biofactors 15:87-89.
22. Kilpatrick, L. E., J. Y. Lee, K. M. Haines, D. E. Campbell, K. E. Sullivan, and H. M. Korchak. 2002. A role for PKC-δ and PI 3-kinase in TNF-α-mediated antiapoptotic signaling in the human neutrophil. Am. J. Physiol. Cell Physiol. 283:C48-C57.
23. 2. Proc. Natl. Acad. Sci. USA 94:11233-11237.
24. 2-treated cells and its activation by tyrosine kinase in vitro. Proc. Natl. Acad. Sci. USA 98:6587-6592.
25. Krappmann, D., A. Patke, V. Heissmeyer, and C. Scheidereit. 2001. B-cell receptor- and phorbol ester-induced NF-κB and c-Jun N-terminal kinase activation in B cells requires novel protein kinase C's. Mol. Cell. Biol. 21:6640-6650.
26. Kronfeld, I., G. Kazimirsky, P. S. Lorenzo, S. H. Garfield, P. M. Blumberg, and C. Brodie. 2000. Phosphorylation of protein kinase Cδ on distinct tyrosine residues regulates specific cellular functions. J. Biol. Chem. 275: 35491-35498.
27. Le Good, J. A., W. H. Ziegler, D. B. Parekh, D. R. Alessi, P. Cohen, and P. J. Parker. 1998. Protein kinase C isotypes controlled by phosphoinositide 3-kinase through the protein kinase PDK1. Science 281:2042-2045.
28. Leitges, M., L. Sanz, P. Martin, A. Duran, U. Braun, J. F. Garcia, F. Camacho, M. T. Diaz-Meco, P. D. Rennert, and J. Moscat. 2001. Targeted disruption of the ζPKC gene results in the impairment of the NF-κB pathway. Mol. Cell 8:771-780.
29. Li, N., and M. Karin. 1999. Is NF-κB the sensor of oxidative stress? FASEB J. 13:1137-1143.
30. Li, W., H. Mischak, J. C. Yu, L. M. Wang, J. F. Mushinski, M. A. Heidaran, and J. H. Pierce. 1994. Tyrosine phosphorylation of protein kinase C-δ in response to its activation. J. Biol. Chem. 269:2349-2352.
31. Lin, X., A. O'Mahony, Y. Mu, R. Geleziunas, and W. C. Greene. 2000. Protein kinase C-θ participates in NF-κB activation induced by CD3-CD28 costimulation through selective activation of IκB kinase β. Mol. Cell. Biol. 20:2933-2940.
32. Manning, G., D. B. Whyte, R. Martinez, T. Hunter, and S. Sudarsanam. 2002. The protein kinase complement of the human genome. Science 298: 1912-1934.
33. Meister, A., and M. E. Anderson. 1983. Glutathione. Annu. Rev. Biochem. 52:711-760.
34. Mercurio, F., and A. M. Manning. 1999. NF-κB as a primary regulator of the stress response. Oncogene 18:6163-6171.
35. Prasad, N., R. S. Topping, D. Zhou, and S. J. Decker. 2000. Oxidative stress and vanadate induce tyrosine phosphorylation of phosphoinositide-dependent kinase 1 (PDK1). Biochemistry 39:6929-6935.
36. Roebuck, K. A. 1999. Oxidant stress regulation of IL-8 and ICAM-1 gene expression: differential activation and binding of the transcription factors AP-1 and NF-κB (review). Int. J. Mol. Med. 4:223-230.
37. Rykx, A., L. De Kimpe, S. Mikhalap, T. Vantus, T. Seufferlein, J. R. Vandenheede, and J. Van Lint. 2003. Protein kinase D: a family affair. FEBS Lett. 546:81-86.
38. Saijo, K., I. Mecklenbrauker, A. Santana, M. Leitger, C. Schmedt, and A. Tarakhovsky. 2002. Protein kinase Cβ controls nuclear factor κB activation in B cells through selective regulation of the IκB kinase α. J. Exp. Med. 195:1647-1652.
39. Soltoff, S. P. 2001. Rottlerin is a mitochondrial uncoupler that decreases cellular ATP levels and indirectly blocks protein kinase Cδ tyrosine phosphorylation. J. Biol. Chem. 276:37986-37992.
40. Storz, P., H. Doppler, F. J. Johannes, and A. Toker. 2003. Tyrosine phosphorylation of protein kinase D in the pleckstrin homology domain leads to activation. J. Biol. Chem. 278:17969-17976.
41. Storz, P., and A. Toker. 2003. NF-κB signaling - an alternate pathway for oxidative stress responses. Cell Cycle 2:9-10.
42. Storz, P., and A. Toker. 2003. Protein kinase D mediates a stress-induced NF-κB activation and survival pathway. EMBO J. 22:109-120.
43. Su, T. T., B. Guo, Y. Kawakami, K. Sommer, K. Chae, L. A. Humphries, R. M. Kato, S. Kang, L. Patrone, R. Wall, M. Teitell, M. Leitges, T. Kawakami, and D. J. Rawlings. 2002. PKC-β controls IκB kinase lipid raft recruitment and activation in response to BCR signaling. Nat. Immunol. 3:780-786.
44. Sun, X., F. Wu, R. Datta, S. Kharbanda, and D. Kufe. 2000. Interaction between protein kinase Cδ and the c-Abl tyrosine kinase in the cellular response to oxidative stress. J. Biol. Chem. 275:7470-7473.
45. Sun, Z., C. W. Arendt, W. Ellmeier, E. M. Schaeffer, M. J. Sunshine, L. Gandhi, J. Annes, D. Petrzilka, A. Kupfer, P. L. Schwartzberg, and D. R. Littman. 2000. PKC-θ is required for TCR-induced NF-κB activation in mature but not immature T lymphocytes. Nature 404:402-407.
46. Tan, S., Y. Sagara, Y. Liu, P. Maher, and D. Schubert. 1998. The regulation of reactive oxygen species production during programmed cell death. J. Cell Biol. 141:1423-1432.
47. Tapia, J. A., L. J. Garcia-Marin, and R. T. Jensen. 2003. Cholecystokinin-stimulated protein kinase C-δ kinase activation, tyrosine phosphorylation and translocation is mediated by Src tyrosine kinases in pancreatic acinar cells. J. Biol. Chem. 278:35220-35230.
48. Vancurova, I., V. Miskolci, and D. Davidson. 2001. NF-κB activation in tumor necrosis factor alpha-stimulated neutrophils is mediated by protein kinase Cδ. Correlation to nuclear IκB. J. Biol. Chem. 276:19746-19752.
49. van den Berg, R., G. R. Haenen, H. van den Berg, and A. Bast. 2001. Transcription factor NF-κB as a potential biomarker for oxidative stress. Br. J. Nutr. 86:(Suppl. 1):S121-S127.
50. Van Lint, J., Y. Ni, M. Valius, W. Merlevede, and J. R. Vandenheede. 1998. Platelet-derived growth factor stimulates protein kinase D through the activation of phospholipase Cγ and protein kinase C. J. Biol. Chem. 273:7038-7043.
51. Van Lint, J., A. Rykx, Y. Maeda, T. Vantus, S. Sturany, V. Malhotra, J. R. Vandenheede, and T. Seufferlein. 2002. Protein kinase D: an intracellular traffic regulator on the move. Trends Cell Biol. 12:193-200.
52. Waldron, R. T., T. Iglesias, and E. Rozengurt. 1999. The pleckstrin homology domain of protein kinase D interacts preferentially with the η isoform of protein kinase C. J. Biol. Chem. 274:9224-9230.
53. Waldron, R. T., O. Rey, T. Iglesias, T. Tugal, D. Cantrell, and E. Rozengurt. 2001. Activation loop Ser744 and Ser748 in protein kinase D are transphosphorylated in vivo. J. Biol. Chem. 276:32606-32615.
54. 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.
55. Yuan, J., D. Bae, D. Cantrell, A. E. Nel, and E. Rozengurt. 2002. Protein kinase D is a downstream target of protein kinase Cθo. Biochem. Biophys. Res. Commun. 291:444-452.
56. Yuan, Z. M., T. Utsugisawa, T. Ishiko, S. Nakada, Y. Huang, S. Kharbanda, R. Weichselbaum, and D. Kufe. 1998. Activation of protein kinase Cδ by the c-Abl tyrosine kinase in response to ionizing radiation. Oncogene 16:1643-1648.
57. Zang, Q., P. Frankel, and D. A. Foster. 1995. Selective activation of protein kinase C isoforms by v-Src. Cell Growth Differ. 6:1367-1373.
58. Zugaza, J. L., J. Sinnett-Smith, J. Van Lint, and E. Rozengurt. 1996. Protein kinase D (PKD) activation in intact cells through a protein kinase C-dependent signal transduction pathway. EMBO J. 15:6220-6230.