Presence of a pre-apoptotic complex of pro-caspase-3, Hsp60 and Hsp10 in the mitochondrial fraction of Jurkat cells

EMBO Journal

Volumn 18, Issue 8, 1999, Pages 2040-2048

  Samali, Afshin ^a   Cai, Jiyang ^a,b   Zhivotovsky, Boris ^a   Jones, Dean P ^a,b   Orrenius, Sten ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis caspase; Chaperone; Hsp; Mitochondrial transmembrane potential

Indexed keywords

ADENYLATE KINASE; CASPASE; CHAPERONE; CYTOCHROME C; DEOXYADENOSINE TRIPHOSPHATE; ENZYME PRECURSOR; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 60; MEMBRANE PROTEIN; RECOMBINANT PROTEIN; STAUROSPORINE;

APOPTOSIS; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; PRIORITY JOURNAL;

EID: 0033561295     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.8.2040     Document Type: Article

References (63)

1. Adachi, S., Gottlieb, R.A. and Babior, B.M. (1998) Lack of release of cytochrome c from mitochondria into cytosol early in the course of Fas-mediated apoptosis of Jurkat cells. J. Biol. Chem., 273, 19892-19894.
2. Alnemri, E.S., Livingston, D.J., Nicholson, D.W., Salvesen, G., Thornberry, N.A., Wong, W.W. and Yuan, J. (1996) Human ICE/CED-3 protease nomenclature. Cell, 87, 171.
3. Arrigo, A.P. (1998) Small stress proteins: chaperones that act as regulators of intracellular redox state and programmed cell death. Biol. Chem., 379, 19-26.
4. Bossy-Wetzel, E., Newmeyer, D.D. and Green, D.R. (1997) Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J., 17, 37-49.
5. Bukau, B. and Horwich, A.L. (1998) The Hsp70 and Hsp60 chaperone machines. Cell, 92, 351-366.
6. Casciola-Rosen, L., Nicholson, D.W., Chong, T., Rowan, K.R., Thornberry, N.A., Miller, D.K. and Rosen, A. (1996) Apopain/CPP32 cleaves proteins that are essential for cellular repair: a fundamental principle of apoptotic cell death. J. Exp. Med, 183, 1957-1964.
7. Emoto, Y. et al. (1995) Proteolytic activation of protein kinase C by an ICE-like protease in apoptotic cells. EMBO J., 14, 6148-6156.
8. 2+ from the endoplasmic reticulum is not the mechanism for bile acid-induced cholestasis and hepatotoxicity in the intact rat liver J. Clin. Invest., 85, 1255-1259.
9. Gabai, V.L., Meriin, A.B., Mosser, D.D., Caron, A.W., Rits, S., Shifrin, V.I. and Sherman, M.Y. (1997) Hsp70 prevents activation of stress kinases. A novel pathway of cellular thermotolerance. J. Biol Chem., 272, 18033-18037.
10. Galea-Lauri, J., Richardson, A.J., Latchman, D.S. and Katz, D.R. (1996) Increased heat shock protein 90 (hsp90) expression leads to increased apoptosis in the monoblastoid cell line U937 following induction with TNF-α and cycloheximide: a possible role in immunopathology. J. Immunol., 157, 4109-4118.
11. Goldberg, Y.P. et al. (1996) Cleavage of huntingtin by apopain, a proapoptotic cysteine protease, is modulated by the polyglutamine tract. Nature Genet., 13, 442-449.
12. Gorman, A.M., Heavey, B., Creagh, E., Cotter, T.G. and Samali, A. (1999) Antioxidant-mediated inhibition of the heat shock response leads to apoptosis. FEBS Lett., 445, 98-102.
13. Hampton, M.B., Zhivotovsky, B., Slater, A.F., Burgess, D.H. and Orrenius, S. (1998) Importance of the redox state of cytochrome c during caspase activation in cytosolic extracts. Biochem. J., 329, 95-99.
14. Jäättelä, M., Wissing, D., Kokholm, K., Kallunki, T. and Egeblad, M. (1998) Hsp70 exerts its anti-apoptotic function downstream of caspase-3-like proteases. EMBO J., 17, 6124-6134.
15. Jacobson, M.D., Weil, M. and Raff, M.C. (1997) Programmed cell death in animal development. Cell, 88, 347-354.
16. Kerr, J.F.R. (1971) Shrinkage necrosis: a distinct mode of cell death. J. Pathol., 105, 13-20.
17. Kim, C.N., Yang, J., Jemmerson, R. and Wang, X. (1996) Induction of the apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell, 86, 147-157.
18. L inhibits ara-C-induced mitochondrial loss of cytochrome c and other pertubations that activate the molecular cascade of apoptosis. Cancer Res., 57, 3115-3120.
19. Kluck, R.M., Bossy-Wetzel, E., Green, D.R. and Newmeyer, D.D. (1997a) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science, 275, 1132-1136.
20. Kluck, R.M., Martin, S.J., Hoffman, B.M., Zhou, J.S., Green, D.R. and Newmeyer, D.D. (1997b) Cytochrome c activation of CPP32-like proteolysis plays a critical role in a Xenopus cell-free apoptosis system. EMBO J., 16, 4639-4649.
21. Köhler, C., Gahm, A., Noma, T., Nakazawa, A., Orrenius, S. and Zhivotovsky, B. (1999) Release of adenylate kinase 2 from the mitochondrial intermembrane space during apoptosis. FEBS Lett., 447, 10-12.
22. Kroemer, G., Zamzami, N. and Susin, S.A. (1997) Mitochondrial control of apoptosis. Immunol. Today, 18, 44-51.
23. Kroemer, G., Dallaporta, B. and Resche-Rigon, M. (1998) The mitochondrial death/life regulator in apoptosis and necrosis. Annu. Rev. Physiol., 60, 619-642.
24. L has activity independent of cytochrome c release. J. Biol. Chem., 272, 30299-30305.
25. Li, H., Zhu, H., Xu, C.J. and Yuan, J. (1998) Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell, 94, 491-501.
26. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S.M., Ahmad, M., Alnemri, E.S. and Wang, X. (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell, 91, 479-489.
27. Lindquist, S. and Craig, E.A. (1988) The heat shock proteins. Annu. Rev. Genet., 22, 631-677.
28. Liu, X., Kim, N.C., Yang, J., Jemmerson, R. and Wang, X. (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell, 86, 147-157.
29. Liu, X., Zou, H., Slaughter, C. and Wang, X. (1997) DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell, 89, 175-184.
30. Lund, P.A. (1995) The roles of molecular chaperones in vivo. Essays Biochem., 29, 113-123.
31. Luo, X., Budihardjo, I., Zou, H., Slaughter, C. and Wang, X. (1998) Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell, 94, 481-490.
32. Mancini, M., Nicholson, D.W., Roy, S., Thornberry, N.A., Peterson, E.P., Casciola-Rosen, L.A. and Rosen, A. (1998) The caspase-3 precursor has a cytosolic and mitochondrial distribution: implications for apoptotic signaling. J. Cell Biol, 140, 1485-1495.
33. L. FEBS Lett., 415, 29-32.
34. Mehlen, R., Schulze-Osthoff, K. and Arrigo, A.P. (1996) Small stress proteins as novel regulators of apoptosis. Heat shock protein 27 blocks Fas/APO-1-and staurosporine-induced cell death. J. Biol. Chem., 271, 16510-16514.
35. Mosser, D.D., Caron, A.W., Bourget, L., Denis-Larose, C. and Massie, B. (1997) Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis. Mol. Cell. Biol., 17, 5317-5327.
36. Nicholson, D.W. and Thornberry, N.A. (1997) Caspases: killer proteases. Trends Biochem. Sci., 22, 299-306.
37. Nicholson, D.W. et al. (1995) Identification and inhibition of the ICE/ CED-3 protease necessary for mammalian apoptosis. Nature, 376, 37-43.
38. Nilsson, O. and Dallner, G. (1975) Distribution of constitutive enzymes and phospholipids in microsomal membranes of rat liver. FEBS Lett., 58, 190-193.
39. Pörn-Ares, M.I., Samali, A. and Orrenius, S. (1998) Cleavage of the calpain inhibitor, calpastatin, during apoptosis. Cell Death Differ., 5, 1028-1033.
40. Reed, J.C. (1997) Cytochrome c: can't live with it - can't live without it. Cell, 91, 559-562.
41. Rosse, T., Olivier, R., Monney, L., Rager, M., Conus, S., Fellay, I., Jansen, B. and Borner, C. (1998) Bcl-2 prolongs cell survival after Bax-induced release of cytochrome c. Nature, 391, 496-499.
42. Ryan, M.T., Naylor, D.J., Hoj, P.B., Clark, M.S. and Hoogenraad, N.J. (1997) The role of molecular chaperones in mitochondrial protein import and folding. Int. Rev. Cytol., 174, 127-193.
43. Samali, A. and Cotter, T.G. (1996) Heat shock proteins increase resistance to apoptosis. Exp. Cell Res., 223, 163-170.
44. Samali, A. and Orrenius, S. (1998) Heat shock proteins: regulators of stress response and apoptosis. Cell Stress Chap., 3, 228-236.
45. Samali, A., Zhivotovsky, B., Jones, D.P. and Orrenius, S. (1998) Detection of pro-caspase-3 in cytosol and mitochondria of various tissues. FEBS Lett., 431, 167-170.
46. Scarlett, J.L. and Murphy, M.P. (1997) Release of apoptogenic proteins from the mitochondrial intermembrane space during the mitochondrial permeability transition. FEBS Lett., 418, 282-286.
47. Single, B., Leist, M. and Nicotera, P. (1998) Simultaneous release of adenylate kinase and cytochrome c in cell death. Cell Death Differ., 5, 1001-1003.
48. Soltys, B.J. and Gupta, R.S. (1996) Immunoelectron microscopic localization of the 60-kDa heat shock chaperonin protein (Hsp60) in mammalian cells. Exp. Cell Res., 222, 16-27.
49. Sottocasa, G.L., Kuylenstierna, B., Bergstrand, A. and Ernster, L. (1967) An electron-transport system associated with the outer membrane of liver mitochondria. A biochemical and morphological study. J. Cell Biol., 32, 415-438.
50. Susin, S.A., Lorenzo, H.K., Zamzami, N., Marzo, I., Brenner, C., Larochette, N., Prevost, M.C, Alzari, P.M. and Kroemer, G. (1999) Mitochondrial release of caspase-2 and -9 during the apoptotic process. J. Exp. Med., 189, 381-394.
51. Tewari, M. et al. (1995) Yama/Cpp32, a mammalian homologue of CED-3, is a crmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell, 81, 801-809.
52. Thompson, C.B. (1995) Apoptosis in the pathogenesis and treatment of disease. Science, 267, 1456-1462.
53. Thornberry, N.A. and Lazebnik, Y. (1998) Caspases: enemies within. Science, 28, 1312-1316.
54. L regulates the membrane potential and volume homeostasis of mitochondria. Cell, 91, 627-637.
55. Volker, U., Mach, H., Schmid, R. and Hecker, M. (1992) Stress proteins and cross-protection by heat shock and salt stress in Bacillus subtilis. J. Gen. Microbiol., 138, 2125-2135.
56. Wang, K.K. et al. (1998) Caspase-mediated fragmentation of calpain inhibitor protein calpastatin during apoptosis. Arch. Biochem. Biophys., 356, 187-196.
57. Wang, X., Zelenski, N.G., Yang, J., Sakai, J., Brown, M.S. and Goldstein, J.L. (1996) Cleavage of sterol regulatory element binding proteins (SREBPs) by CPP32 during apoptosis. EMBO J., 15, 1012-1020.
58. White, E. (1996) Life, death and the pursuit of apoptosis. Genes Dev., 10, 1-15.
59. Wyllie, A.H., Kerr, J.F.R. and Currie, A.R. (1980) Cell death: the significance of apoptosis. Int. Dev. Cyltol., 68, 251-306.
60. Xanthoudakis, S., Roy, S., Rasper, D., Hennessey, T., Cassady, R., Tawa, P., Ruel, R., Rosen, A. and Nicholson, D.W. (1999) Hsp60 accelerates the maturation of pro-caspase-3 by upstream activator proteases during apoptosis. EMBO J., 18, 2049-2056.
61. Yang, J., Liu, X., Bhalla, K., Kim, C.N., Ibrado, A.M., Cai, J., Peng, T.I., Jones, D.P. and Wang, X. (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science, 275, 1129-1132.
62. Zhivotovsky, B., Orrenius, S., Brustugun, O.T. and Doskeland, S.O. (1998) Injected cytochrome c induces apoptosis. Nature, 391, 449-450.
63. Zhou, H., Henze, W.J., Liu, X., Lutschg, A. and Wang, X. (1997) Apaf-1, a human protein homologous to C.elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell, 90, 405-413.