Positive feedback of protein kinase C proteolytic activation during apoptosis

Biochemical Journal

Volumn 368, Issue 3, 2002, Pages 905-913

  Leverrier, Sabrina ^a   Vallentin, Alice ^b   Joubert, Dominique ^b  

^a INSERM   (France)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Calpain; Caspase; Cysteine protease; Pituitary; Programmed cell death

Indexed keywords

ENZYME KINETICS; GENES; PROTEINS;

PRO-APOPTOTIC FUNCTIONS;

BIOCHEMISTRY;

CALPAIN; CASPASE; CASPASE 3; CYTOCHROME C; ISOENZYME; PROTEIN KINASE C;

ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INDUCTION; ENZYME LOCALIZATION; ENZYME RELEASE; GENOTOXICITY; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; RAT;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CALPAIN; CATALYTIC DOMAIN; CELL SURVIVAL; CULTURE MEDIA, SERUM-FREE; CYSTEINE ENDOPEPTIDASES; CYTOCHROME C GROUP; DNA FRAGMENTATION; IMMUNOHISTOCHEMISTRY; ISOENZYMES; PITUITARY GLAND; PLASMIDS; PROTEIN KINASE C; PROTEIN KINASE C-ALPHA; PROTEIN KINASE C-DELTA; PROTEIN KINASE C-EPSILON; PROTEIN STRUCTURE, TERTIARY; RATS; SUBCELLULAR FRACTIONS; TIME FACTORS; TRANSFECTION; TUMOR CELLS, CULTURED; ULTRAVIOLET RAYS;

ANIMALIA;

EID: 0037115731     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20021253     Document Type: Article

References (47)

1. Arends, M. J. and Wyllie, A. H. (1991) Apoptosis: Mechanisms and roles in pathology. Int. Rev. Exp. Pathol. 32, 223-254
2. Takahashi, A. and Earnshaw, W. C. (1996) ICE-related proteases in apoptosis. Curr. Opin. Genet. Dev. 6, 50-55
3. Cohen, G. M. (1997) Caspases: The executioners of apoptosis. Biochem. J. 326, 1-16
4. Thornberry, N. A. and Lazebnik, Y. (1998) Caspases: Enemies within. Science 281, 1312-1316
5. Wang, K. K. (2000) Calpain and caspase: Can you tell the difference? Trends Neurosci. 23, 20-26
6. Kishimoto, A., Mikawa, K., Hashimoto, K., Yasuda, I., Tanaka, S., Tominaga, M., Kuroda, T. and Nishizuka, Y. (1989) Limited proteolysis of protein kinase C subspecies by calcium-dependent neutral protease (calpain). J. Biol. Chem. 264, 4088-4092
7. Touyarot, K., Poussard, S., Verret, C., Aragon, B., Cottin, P., Nogues, X. and Micheau, J. (2000) Calpain-PKC inter-relations in mouse hippocampus: A biochemical approach. Neurochem. Res. 25, 781-790
8. Datta, R., Kojima, H., Yoshida, K. and Kufe, D. (1997) Caspase-3-mediated cleavage of protein kinase C theta in induction of apoptosis. J. Biol. Chem. 272, 20317-20320
9. Reyland, M. E., Anderson, S. M., Matassa, A. A., Barzen, K. A. and Quissell, D. O. (1999) Protein kinase C delta is essential for etoposide-induced apoptosis in salivary gland acinar cells. J. Biol. Chem. 274, 19115-19123
10. Emoto, Y., Manome, Y., Meinhardt, G., Kisaki, H., Kharbanda, S., Robertson, M., Ghayur, T., Wong, W. W., Kamen, R., Weichselbaum, R. et al. (1995) Proteolytic activation of protein kinase C delta by an ICE-like protease in apoptotic cells. EMBO J. 14, 6148-6156
11. Frutos, S., Moscat, J. and Diaz-Meco, M. T. (1999) Cleavage of zetaPKC but not lambda/iotaPKC by caspase-3 during UV-induoed apoptosis. J. Biol. Chem. 214, 10765-10770
12. Denning, M. F., Wang, Y., Nickololf, B. J. and Wrone-Smith, T. (1998) Protein kinase Cdelta is activated by caspase-dependent proteolysis during ultraviolet radiation-induced apoptosis of human keratinocytes. J. Biol. Chem. 273, 29995-30002
13. Villalba, M. (1998) A possible role for PKC delta in cerebellar granule cells apoptosis. NeuroReport 9, 2381-2385
14. Brachat. A., Pierrat, B., Brungger, A. and Helm, J. (2000) Comparative microarray analysis of gene expression during apoptosis-induction by growth factor deprivation or protein kinase C inhibition. Oncogene 19, 5073-5082
15. Fujii, T., Garcia-Bermejo, M. L., Bernaba, J. L., Caamano, J., Ohba, M., Kuroki, T., Li, L., Yuspa, S. H. and Kazanietz, M. G. (2000) Involvement of protein kinase C delta (PKCdelta) in phorbol ester-induced apoptosis in LNCaP prostate cancer cells. Lack of proteolytic cleavage of PKCdelta. J. Biol. Chem. 275, 7574-7582
16. Zhong, M., Lu, Z. and Foster, D. A. (2002) Downregulating PKC delta provides a P13K/Akt-independent survival signal that overcomes apoptotic signals generated by c-Src overexpression. Oncogene 21, 1071-1078
17. Majumder, P. K., Pandey, P., Sun, X., Cheng, K., Datta, R., Saxena, S., Kharbanda, S. and Kule, D. (2000) Mitochondrial translocation of protein kinase C delta in phorbol ester-induced cytochrome c release and apoptosis. J. Biol. Chem. 275, 21793-21796
18. Shao, R. G., Cap, C. X. and Pommier, Y. (1997) Activation of PKCalpha downstream from caspases during apoptosis induced by 7-hydroxystaurosporine or the topoisomerase inhibitors, camptothecin and etoposide, in human myeloid leukemia HL60 cells. J. Biol. Chem. 272, 31321-31325
19. Mizuno, K., Noda, K., Araki, T., Imaoka, T., Kobayashi, Y., Akita, Y., Shimonaka, M., Kishi, S. and Ohno, S. (1997) The proteolytic cleavage of protein kinase C isotypes, which generates kinase and regulatory fragments, correlates with Fas-mediated and 12-O-tetradecanoyl-phorbol-13-acetate-induced apoptosis. Eur. J. Biochem. 256, 7-18
20. Gubina, E., Rinaudo, M. S., Szallasi, Z., Blumberg, P. M. and Mufson, R. A. (1998) Overexpression of protein kinase C isoform epsilon but not delta in human interleukin-3-dependent cells suppresses apoptosis and induces bcl-2 expression. Blood 91, 823-829
21. Ghayur, T., Hugunin, M., Talanian, R. V., Ratnofsky, S., Quinlan, C., Emoto, Y., Pandey, P., Datta, R., Huang, Y., Kharbanda, S. 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
22. Dooley, N. P., Baltuch, G. H., Groome, N., Villemure, J. G. and Yong, V. W. (1998) Apoptosis is induced in glioma cells by antisense oligonucleotides to protein kinase C alpha and is enhanced by cycloheximide. NeuroReport 9, 1727-1733
23. Whelan, R. D. and Parker, P. J. (1998) Loss of protein kinase C function induces an apoptotic response. Oncogene 16, 1939-1944
24. Lee, J. Y., Hannun, Y. A. and Obeid, L. M. (2000) Functional dichotomy of protein kinase C (PKC) in tumor necrosis factor-alpha (TNF-alpha) signal transduction in L929 cells. Translocation and inactivation of PKC by TNF-alpha. J. Biol. Chem. 275, 29290-29298
25. Vallentin, A., Prevostel, C., Fauquier, T., Bonnefont, X. and Joubert, D. (2000) Membrane targeting and cytoplasmic sequestration in the spatiotemporal localization of human protein kinase C alpha. J. Biol. Chem. 275, 6014-6021
26. Germain, M., Affar, E. B., D'Amours, D., Dixit, V. M., Salvesen, G. S. and Poirier, G. G. (1999) Cleavage of automodified poly(ADP-ribose) polymerase during apoptosis. Evidence for involvement of caspase-7. J. Biol. Chem. 274, 28379-28384
27. Pears, C. J., Kour, G., House, C., Kemp, B. E. and Parker, P. J. (1990) Mutagenesis of the pseudosubstrate site of protein kinase C leads to activation. Eur. J. Biochem. 194, 89-94
28. Eto, A., Akita, Y., Saido, T. C., Suzuki, K. and Kawashima, S. (1995) The role of the calpain-calpastatin system in thyrotropin-releasing hormone-induced selective downregulation of a protein kinase C isozyme, nPKC epsilon, in rat pituitary GH4C1 cells. J. Biol. Chem. 276, 25115-25120
29. Nath, R., Raser, K. J., McGinnis, K., Nadimpalli, R., Stafford, D. and Wang, K. K. (1996) Effects of ICE-like protease and calpain inhibitors on neuronal apoptosis. NeuroReport 8, 249-255
30. Squier, M. K., Miller, A. C., Malkinson, A. M. and Cohen, J. J. (1994) Calpain activation in apoptosis. J. Cell. Physiol. 169, 229-237
31. Squier, M. K., Sehnert, A. J., Sellins, K. S., Malkinson, A. M., Takano, E. and Cohen, J. J. (1999) Calpain and calpastatin regulate neutrophil apoptosis. J. Cell. Physiol. 178, 311-319
32. Couly, G. F. and Le Douarin, N. M. (1985) Mapping of the early neural primordium in quail-chick chimeras. I. Developmental relationships between placodes, facial ectoderm, and prosencephalon. Dev. Biol. 110, 422-439
33. Couly, G. F. and Le Douarin, N. M. (1987) Mapping of the early neural primordium in quail-chick chimeras. II. The prosencephalic neural plate and neural folds: Implications for the genesis of cephalic human congenital abnormalities. Dev. Biol. 120, 198-214
34. Brunet-de Carvalho, N., Picart, R., Van de Moortele, S., Tougard, C. and Tixier-Vidal, A. (1989) Laminin induces formation of neurite-like processes and potentiates prolactin secretion by GH3 rat pituitary cells. Differentiation 40, 106-118
35. Wang, K. K., Posmantur, R., Nadimpalli, R., Nath, R., Mohan, P., Nixon, R. A., Tafanian, R. V., Keegan, M., Herzog, L. and Allen, H. (1998) Caspase-mediated fragmentation of calpain inhibitor protein calpastatin during apoptosis. Arch. Biochem. Biophys. 356, 187-196
36. Kato, M., Nonaka, T., Maki, M., Kikuchi, H. and Imajoh-Ohmi, S. (2000) Caspases cleave the amino-terminal calpain inhibitory unit of calpastatin during apoptosis in human Jurkat T cells. J. Biochem. (Tokyo) 127, 297-305
37. Porn-Ares, M. I., Samali, A. and Orrenius, S. (1998) Cleavage of the calpain inhibitor, calpastatin, during apoptosis. Cell Death Differ. 5, 1028-1033
38. Shi, Y. Melnikov, V. Y., Schrier, R. W. and Edelstein, C. L. (2000) Downregulation of the calpain inhibitor protein calpastatin by caspases during renal ischemiareperfusion. Am. J. Physiol. Renal Physiol. 279, F509-F517
39. Chen, N., Ma, W., Huang, C. and Dong, Z. (1999) Translocation of protein kinase Cepsilon and protein kinase Cdelta to membrane is required for ultraviolet B-induced activation of mitogen-activated protein kinases and apoptosis. J. Biol. Chem. 274, 15389-15394
40. Scheel-Toellner, D., Pilling, D., Akbar, A. N., Hardie, D., Lombardi, G., Salmon, M. and Lord, J. M. (1999) Inhibition of T cell apeptosis by IFN-beta rapidly reverses nuclear translocation of protein kinase C-delta. Eur. J. Immunol. 29, 2603-2612
41. Hong, D. H., Huan, J., Ou, B. R., Yeh, J. Y., Saido, T. C., Cheeke, P. R. and Forsberg, N. E. (1995) Protein kinase C isoforms in muscle cells and their regulation by phorbol ester and calpain. Biochim. Biophys. Acta 1267, 45-54
42. Ruvolo, P. P., Deng, X., Carr, B. K. and May, W. S. (1998) A functional role for mitochondrial protein kinase Calpha in Bcl2 phosphorylation and suppression of apoptosis. J. Biol. Chem. 273, 25435-25442
43. Basu, A. and Akkaraju, G. R. (1999) Regulation of caspase activation and cisdiamminedichloroplatinum(ll)-induced cell death by protein kinase C. Biochemistry 38, 4245-4251
44. Matassa, A. A., Carpenter, L., Biden, T. J., Humphries, M. J. and Reyland, M. E. (2001) PKCdelta is required for mitochondrial-dependent apoptosis in salivary epithelial cells. J. Biol. Chem. 276, 29719-29728
45. Cardone, M. H., Salvesen, G. S., Widmann, C., Johnson, G. and Frisch, S. M. (1997) The regulation of anoikis: MEKK-1 activation requires cleavage by caspases. Cell 90, 315-323
46. Denning, M. F., Wang, Y., Tibudan, S., Alkan, S., Nickoloff, B. J. and Qin, J. Z. (2002) Caspase activation and disruption of mitochondrial membrane potential during UV radiation-induced apoptosis of human keratinocytes requires activation of protein kinase C. Cell Death Differ. 9, 40-52
47. Goerke, A., Sakai, N., Gutjahr, E., Schlapkohl, W. A., Mushinski, J. F., Hailer, H., Kolch, W., Saito, N. and Mischak, H. (2002) Induction of apoptosis by protein kinase C delta is independent of its kinase activity. J. Biol. Chem. 277, 32054-32062