The isoform-specific regulation of apoptosis by protein kinase C

Cellular and Molecular Life Sciences

Volumn 60, Issue 6, 2003, Pages 1061-1070

  Gutcher, I ^a   Webb, P R ^a   Anderson, N G ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Bcl 2; Caspase; Cell death; Diacylglycerol; Mitochondria; Phorbol ester; Phosphorylation

Indexed keywords

CASPASE; DIACYLGLYCEROL; DNA; ISOENZYME; PHORBOL ESTER; PROTEIN BCL 2; PROTEIN KINASE C;

ANIMAL CELL; APOPTOSIS; CELL DEATH; CELL LINE; CELL SURVIVAL; DNA DAMAGE; ENZYME ANALYSIS; ENZYME PHOSPHORYLATION; ENZYME REGULATION; HUMAN; HUMAN CELL; MITOCHONDRION; NONHUMAN; REVIEW; TISSUE DISTRIBUTION;

ANIMALIA;

EID: 0037710311     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00018-003-2281-y     Document Type: Review

References (86)

1. Meier P., Finch A. and Evan G. (2000) Apoptosis in development. Nature 407: 796-801
2. Antonsson B. and Martinou J.-C. (2000) The Bcl-2 protein family. Exp. Cell Res. 256: 50-57
3. Karran L. and Dyer M. J. (2001) Proteolytic cleavage of molecules involved in cell death or survival pathways: a role in the control ofapoptosis? Crit. Rev. Eukaryot. Gene Expr. 11: 269-277
4. Shi Y. (2002) Mechanisms of caspase activation and inhibition during apoptosis. Mol. Cell 9: 459-470
5. Vaughan A. T., Betti C. J. and Villalobos M. J. (2002) Surviving apoptosis. Apoptosis 7: 173-177
6. Dempsey E. C., Newton A. C., Mochley-Rosen D., Fields A. P., Reyland M. E., Insel P. A. et al. (2000). Protein kinase C isozymes and the regulation of diverse cell responses. Am. J. Physiol. Lung Cell Mol. Physiol. 279: L429-L438
7. Ventura C. and Maioli M. (2001) Protein kinase C control of gene expression. Crit. Rev. Eukaryot. Gene Expr. 11: 243-267
8. Newton A. C. (2001) Protein kinase C: structural and spatial regulation by phosphorylation, cofactors and macromolecular interactions. Chem. Rev. 101: 2353-2364
9. Nagata S. (2000) Apoptotic DNA fragmentation. Exp. Cell Res. 256: 12-18
10. Wajant H. (2002) The Fas signaling pathway: more than a paradigm. Science 296: 1635-1636
11. Gross A., McDonnell J. M. and Korsmeyer S. J. (1999) BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 13: 1899-1911
12. Hayashi A., Seki N., Hattori A., Kozuma S. and Saito T. (1999) PKCnu, a new member of the protein kinase C family, composes a fourth subfamily with PKCmu. Biochem. Biophys. Acta 1450: 99-106
13. Soderling T. R. (1990) Protein kinases. Regulation by autoinhibitory domains. J. Biol. Chem. 265: 1823-1826
14. Liu W. S. and Heckman C. A. (1998) The sevenfold way of PKC regulation. Cell Signal. 10: 529-542
15. Schechtman D. and Mochly-Rosen D. (2001) Adaptor proteins in protein kinase C-mediated signal transduction. Oncogene 20: 6339-6347
16. Parekh D. B., Ziegler W. and Parker P. J. (2000) Multiple pathways control protein kinase C phosphorylation. EMBO J. 19: 496-503
17. McConkey D. J., Hartzell P., Jondal M. and Orrenius S. (1989) Inhibition of DNA fragmentation in thymocytes and isolated thymocyte nuclei by agents that stimulate protein kinase C. J. Biol. Chem. 264: 13399-13402
18. Azuma Y., Onishi Y., Sato Y. and Kizaki H. (1993). Induction of mouse thymocyte apoptosis by inhibitors of tyrosine kinases is associated with dephosphorylation of nuclear proteins. Cell Immunol. 152: 271-278
19. Cross T. G., Scheel-Toellner D., Henriquez N. V., Deacon E., Salmon M. and Lord J. M. (2000a). Serine/threonine protein kinases and apoptosis. Exp. Cell Res. 256: 34-41
20. Haimovitz-Friedman A., Balaban N., McLoughlin M., Ehleiter D., Michaeli J., Vlodavsky I. et al. (1994) Protein kinase C mediates basic fibroblast growth factor protection of endothelial cells against radiation-induced apoptosis. Cancer Res. 54: 2591-2597
21. Ahmad S., Mineta T., Martuza R. L. and Glazer R. I. (1994). Antisense expression of protein kinase C alpha inhibits the growth and tumorigenicity of human glioblastoma cells. Neurosurgery 35: 904-908
22. Dooley N. P., Baltuch G. H., Groome N., Villemure J. G. and Yong V. W. (1998) Apoptosis is induced in glioma cells by anti-sense oligonucleotides to protein kinase C alpha and is enhanced by cycloheximide. Neuroreports 9: 1727-1733
23. Whelan R. D. H. and Parker P. J. (1998) Loss of protein kinase C function induces an apoptotic response. Oncogene 16: 1939-1944
24. Matassa A. A., Carpenter L., Biden T. J., Humphries M. J. and Reyland M. E. (2001) PKCδ is required for the mitochondrial-dependent apoptosis in salivary epithelial cells. J. Biol. Chem. 276: 29719-28728
25. Powell C. T., Brittis N. J., Stec D., Hug H., Heston W. D. and Fair W. R. (1996) Persistant membrane translocation of protein kinase C alpha during 12-O-tetradecanoylphorbol-13-acetate induced apoptosis of LNCaP human prostate cancer cells. Cell Growth Differ. 7: 419-428
26. Knox K. A., Johnson G. D. and Gordon J. (1993) A study of protein kinase C isozyme distribution in relation to Bcl-2 expression during apoptosis of epithelial cells in vivo. Exp. Cell Res. 207: 68-73
27. Nowak G (2002) PKC-alpha and ERK1/2 mediate mitochondrial dysfunction, decreases in active Na+ transport, and cisplatin-induced apoptosis in renal cells. J. Biol. Chem. 277: 43377-43388
28. Meinhardt G., Roth J. and Totok G. (2000) Protein kinase C activation modulates pro- and anti-apoptotic signaling pathways. Eur. J. Cell Biol. 79: 824-833
29. Ruvolo P. P., Deng X., Carr B. K. and May W. S. (1998) A functional role for mitochondrial protein kinase C alpha in Bcl2 phosphorylation and suppression of apoptosis. J. Biol. Chem. 273: 25436-25442
30. Majewski M., Niebrowska-Skorsa M., Salomoni P., Slupianek A., Reiss K., Trotta R. et al. (1999) Activation of mitochondrial Raf-1 is involved in the antiapoptotic effects of Akt. Cancer Res. 59: 2815-2819
31. Kolch W., Heidecker G., Kochs G., Hummel R., Vahidi H., Mischak H. et al. (1993) Protein kinase Ca activates Raf-1 by direct phosphorylation. Nature 364: 249-252
32. Cai H., Smola U., Wixler V., Eisenmann-Tappe I., Diaz-Meco M. T., Moscat J. et al. (1997). Role of diacylglycerol-regulated protein kinase C isotypes in growth factor activation of the Raf-1 protein kinase. Mol. Cell. Biol. 17: 732-741
33. Ueda Y., Hirai S., Osada S., Suzuki A., Mizuno K. and Ohno S. (1996) Protein kinase C activates the MEK-ERK pathway in a manner independent of Ras and dependent on Raf. J. Biol. Chem. 38: 23512-23519
34. Gomez-Angelats M. and Cidlowski J. A. (2001) Protein kinase C regulates FADD recruitment and death-inducing signaling complex formation in FAS/CD95-induced apoptosis. J. Biol. Chem. 276: 44944-44952
35. Pongracz J., Tuffley W., Johnson J. D., Deacon E. M., Burnett D., Stockley R. A. et al. (1995) Changes in protein kinase C expression associated with apoptosis in U937 myelomonocytic cells. Exp. Cell. Res. 218: 430-438
36. Yuan Z. M., Utsugisawa T., Ishiko T., Nakada S., Huang Y., Kharbanda S. et al. (1998) Activation of protein kinase C-δ by the c-abl tyrosine kinase in response to ionizing radiation. Oncogene 16: 1643-1648
37. Evans C. A., Lord J. M., Owen-Lynch P. J., Johnson G., Dive C. and Whetton A. D. (1995) Suppression of apoptosis by v-Ab1 protein kinase is associated with nuclear translocation and activation of protein kinase C in an interleukin-3-dependent haemopoietic cell line. J. Cell Sci. 108: 2591-2598
38. 11 protein kinase C as a mitotic lamin kinase. J. Biol. Chem. 269: 19074-19080
39. Chiarini A., Whitfield J. F., Armato U. and Dal Pra I. (2002) Protein kinase C-beta II Is an apoptotic lamin kinase in polyomavirus-transformed, etoposide-treated pyF111 rat fibroblasts. J. Biol. Chem. 277: 18827-18839
40. Whitman S. P., Civoli F. and Daniel L. W. (1997) Protein kinase CbetaII activation by 1-beta-D-arabinofuranosylcytosine is antagonistic to stimulation of apoptosis and Bcl-2alpha down-regulation. J. Biol. Chem. 272: 23481-23484
41. Su T. T., Guo B., Kawakami Y., Sommer K., Chae K., Humphries L. A. et al. (2002) PKC-beta controls I kappa B kinase lipid raft recruitment and activation in response to BCR signalling. Nat. Immunol. 3: 780-786
42. MacFarlane D. E. and Manzel L. (1994) Activation of beta-isozyme of protein kinase C (PKC beta) is necessary and sufficient for phorbol ester-induced differentiation of HL-60 promyelocytes. Studies with PKC beta-defective PET mutant. J. Biol. Chem. 269: 4327-4331
43. Ito Y., Mishra N. C., Yoshida K., Kharbanda S., Saxena S. and Kufe D. (2001) Mitochondrial targeting of JNK/SAPK in the phorbol ester response of myeloid leukemia cells. Cell Death Differ. 8: 794-800
44. Bertolotto C., Maulon L., Filippa N., Baier G. and Auberger P. (2000) Protein kinase C theta and epsilon promote T-cell survival by a rsk-dependent phosphorylation and inactivation of BAD. J. Biol. Chem. 275: 37246-37250
45. Ding L., Wang H., Lang W. and Xiao L. (2002) Protein kinase C-epsilon promotes survival of lung cancer cells by suppressing apoptosis through dysregulation of the mitochondrial caspase pathway. J. Biol. Chem. 277: 35305-35313
46. Murray N. R. and Fields A. P. (1997) Atypical protein kinase C ι protects human leukaemia cells against drug-induced apoptosis. J. Biol. Chem. 272: 27521-27524
47. Jamieson L., Carpenter L., Biden T. J. and Fields A. P. (1999) Protein kinase Cι activity is necessary for Bcr-Ab1-mediated resistance to drug-induced apoptosis. J. Biol. Chem. 274: 3927-3930
48. Diaz-Meco M. T., Municio M. M., Frutos S., Sanchez P., Lozano J., Sanz L. et al. (1996). The product of Par-4, a gene induced during apoptosis, interacts selectively with the atypical isoforms of protein kinase C. Cell 86: 777-786
49. Smith L., Chen L., Reyland M. E., DeVries T. A., Talanian R. V., Omura S. et al. (2000) Activation of atypical protein kinase C zeta by caspase processing and degradation by the ubiquitin-proteasome system. J. Biol. Chem. 275: 40620-40627
50. Plo I., Hernandez H., Kohlhagen G., Lautier D., Pommier Y. and Laurent G. (2002) Overexpression of the atypical protein kinase C zeta reduces topoisomerase II catalytic activity, cleavable complexes formation and drug-induced cytotoxicity in monocytic U937 leukemia cells. J. Biol. Chem. 277: 31407-31415
51. Leitges M., Sanz L., Martin P., Duran A., Braun U., Garcia J. F. et al. (2001) Targeted disruption of the zetaPKC gene results in the impairment of the NF-kappaB pathway. Mol. Cell 8: 771-780
52. Martin P., Duran A., Minguet S., Gaspar M. L., Diaz-Meco M. T, Rennert P. et al. (2002) Role of zeta PKC in B-cell signaling and function. EMBO J. 21: 4049-4057
53. Doornbos R. P., Theelen M., van der Hoeven P. C. J., van Blitterswijk W. J., Verkleij A. J. and Henegouwen P. (1999) Protein kinase C zeta is a negative regulator of protein kinase B activity. J. Biol. Chem. 274: 8589-8596
54. Mao M., Fang X., Lu Y., Lapushin R., Bast R. C. and Mills G. B. (2000) Inhibition of growth-factor-induced phosphorylation and activation of protein kinase B/Akt by atypical protein kinase C in breast cancer cells. Biochem J. 352: 475-482
55. Mizuno K, Noda K., Araki T., Imaoka T., Kobayashi Y., Akita Y. et al. (1997) The proteolytic cleavage of PKC isotypes, which generates kinase and regulatory fragments, correlates with Fas-mediated and 12-O-tetradecanoyl-phorbol-13-acetate-induced apoptosis. Eur. J. Biochem 250: 7-18
56. Denning M. F., Wang Y., Nickoloff B. J. and Wrone-Smith T. (1998). Protein kinase Cδ is activated by caspase-dependent proteolysis during ultraviolet radiation-induced apoptosis of human keratinocytes. J. Biol. Chem. 273: 29995-30002
57. Reyland M., Anderson S., Matassa A. A., Barzen K. A. and Quissell D. O. (1999) Protein kinase C δ is essential for etoposide-induced apoptosis in salivary acinar cells. J. Biol. Chem. 274: 19115-19123
58. Lu Z., Hornia A., Jiang Y. W., Zang Q., Ohno S. and Foster D. A. (1997) Tumour promotion by depleting cells of protein kinase Cδ. Mol. Cell. Biol. 17: 3418-3428
59. Emoto Y., Manome Y., Meinhardt G, Kisaki H., Kharbanda S., Robertson M. et al. (1995) Proteolytic activation of protein kinase C δ by an ICE-like protease in apoptotic cells. EMBO J. 14: 6148-6156
60. Ghayur T., Hugunin M., Talanian R. V., Ratnofsky S., Quinlan C., Emoto Y. et al. (1996) Proteolytic activation of protein kinase C delta by an ICE/CED 3-like protease induces characteristics of apoptosis. J. Exp. Med. 184: 2399-2404
61. Cross T, Griffiths G., Deacon E., Sallis R., Gough M., Watters D. et al. (2000). PKC-δ is an apoptotic lamin kinase. Oncogene 19: 2331-2337
62. Scheel-Toellner D., Pilling D., Akbar A. N., Hardie D., Lombardi G., Salmon M. et al. (1999) Inhibition of T cell death apoptosis by IFN-β rapidly reverses nuclear translocation of protein kinase C-δ. Eur. J. Immunol. 29: 2603-2612
63. Lord J. M., Garronne B., Griffiths G. and Watters D. (1995) Apoptosis induced by bistratene A in HL-60 cells involves the selective activation of PKC-delta and its association with nuclear lamins at DNA replication sites. J. Cell. Biochem. S19B: 275
64. Bharti A., Kraeft S.-K., Gounder M., Pandey P., Jin S., Yuan Z.-M. et al. (1998). Inactivation of DNA-dependent protein kinase by protein kinase Cδ: implications for apoptosis. Mol. Cell. Biol. 18: 6719-6728
65. Ren J., Datta R., Shioya H., Li Y, Oki E., Biedermann V. et al. (2002) p73β is regulated by protein kinase Cδ catalytic fragment generated in the apoptotic response to DNA damage. J. Biol. Chem. 277: 33758-33765
66. Gschwendt M. (1999) Protein kinase Cδ. Eur. J. Biochem. 259: 555-564
67. Owen P. J., Johnson G. D. and Lord J. M. (1996) Protein kinase C-delta associates with vimentin intermediate filaments in differentiated HL60 cells. Exp. Cell Res. 225: 366-373
68. Basu A., Woolard M. D. and Johnson C. L. (2001). Involvement of protein kinase C-delta in DNA damage-induced apoptosis. Cell Death Differ. 8: 899-908
69. Leverrier S., Vallentin A. and Joubert D. Y. (2002) Positive feedback of Protein kinase C proteolytic activation during apoptosis. Biochem. J., in press
70. Basu A., Lu D., Sun B., Moor A. N., Akkaraju G. R. and Huang J. (2002a) Proteolytic activation of protein kinase C-epsilon by caspase-mediated processing and transduction of anti-apoptotic signals. J. Biol. Chem. 277: 41850-41856
71. Fujii T, Garcia-Bermejo M. L., Bernabo J .L., Caamano J., Ohba M., Kuroki T. et al. (2000) Involvement of PKC-δ (PKC δ) in phorbol ester-induced apoptosis in LNCaP prostate cancer cells. Lack of proteolytic cleavage of PKC δ. J. Biol. Chem. 275: 7574-7582
72. Ohmori T. and Artega C. L. (1998) Protein kinase C epsilon translocation and phosphorylation by cis-diamminedichloro-platinum(II) (CDDP): potential role in CDDP-mediated cytotoxicity. Cell Growth Differ. 9: 345-353
73. Li L., Lorenzo P. S., Bogi K., Blumberg P. M. and Yuspa S. H. (1999) Protein kinase Cδ targets mitochondria, alters mitochondrial membrane potential and induces apoptosis in normal and neoplastic keratinocytes when overexpressed by an adenoviral vector. Mol. Cell. Biol. 19: 8547-8558
74. Majumder P. K., Pandey P., Sun X., Cheng K., Datta R., Saxena S. et al. (2000) Mitochondrial translocation of protein kinase C δ in phorbol ester-induced cytochrome c release and apoptosis. J. Biol. Chem. 275: 21793-21796
75. Garcia-Bermejo M. L., Coluccio Leskow F., Fujii T., Wang Q., Blumberg P. M., Ohba M. et al. (2001) DAG-lactones, a new class of PKC agonists, induce apoptosis in LNCaP prostate cancer cells by selective activation of PKCα. J. Biol. Chem. 277: 645-655
76. Davies S. P., Reddy H., Caivano M. and Cohen P. (2000). Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J. 351: 95-105
77. Soltoff S. P. (2001) Rottlerin is a mitochondrial uncoupler that decreases cellular ATP levels and indirectly blocks protein kinase cdelta tyrosine phosphorylation. J. Biol. Chem. 276: 37986-37992
78. Basu A., Johnson D. E. and Woolard M. D. (2002b) Potentiation of tumor necrosis factor-alpha-induced cell death by rottlerin through a cytochrome-C-independent pathway. Exp. Cell Res. 278: 209-214
79. Sakurai Y., Onishi Y., Tanimoto Y. and Kizaki H. (2001) Novel protein kinase C delta isoform insensitive to caspase-3. Biol. Pharm. Bull. 24: 973-977
80. Villalba M, Bushway P. and Altman A. (2001) Protein kinase C-θ mediates a selective T cell survival signal via phosphorylation of BAD. J. Immunol. 166: 5955-5963
81. Osada S., Mizuno K., Saido T. C., Suzuki K., Kuroki T. and Ohno S. (1992) A new member of the protein kinase C family, nPKCθ, predominantly expressed in skeletal muscle. Mol. Cell. Biol. 12: 3930-3938
82. O'Brian C. A., Vogel V. G., Singletary S. E. and Ward N. E. (1989) Elevated protein kinase C expression in human breast tumor biopsies relative to normal breast tissue. Cancer Res. 49: 3215-3217
83. Hatada S., Sakanoue Y., Kusunoki M., Kobayashi A. and Utsonomiya J. (1992) Protein kinase C activity in human thyroid carcinoma and adenoma. Cancer 70: 2918-2922
84. Parker P. J. (1999) Inhibition of protein kinase C - do we can we, and should we? Pharmacol. Ther. 82: 263-267
85. O'Brian C. A., Ward N. E., Stewart J. R. and Chu F. (2001) Prospects for targeting protein kinase C isozymes in the therapy of drug-resistant cancer - an evolving story. Cancer Metastasis Rev. 20: 95-100
86. Ma D. (2001) Recent advances in the discovery of protein kinase C modulators based on the structures of natural protein kinase C activators. Curr. Med. Chem. 8: 191-202