The caspase-3 precursor has a cytosolic and mitochondrial distribution: Implications for apoptotic signaling

Journal of Cell Biology

Volumn 140, Issue 6, 1998, Pages 1485-1495

  Mancini, Marie ^a   Nicholson, Donald W ^b   Roy, Sophie ^b   Thornberry, Nancy A ^c   Peterson, Erin P ^c   Casciola Rosen, Livia A ^a   Rosen, Antony ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MERCK FROSST CENTRE FOR THERAPEUTIC RESEARCH   (Canada)

^c MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CYTOCHROME C; CYTOSKELETON PROTEIN; ENZYME PRECURSOR; MITOCHONDRIAL ENZYME; PROTEIN BCL 2; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVATION; HUMAN; HUMAN CELL; LIVER MITOCHONDRION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

EID: 0032559799     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.140.6.1485     Document Type: Article

References (72)

1. Alnemri, E.S., D.J. Livingston, D.W. Nicholson, G. Salvesen, N.A. Thornberry, W.W. Wong, and J.Y. Yuan. 1996. Human ICE/CED-3 protease nomenclature. Cell. 87: 171.
2. Balch, W.E., and J.E. Rothman. 1985. Characterization of protein transport between successive compartments of the Golgi: asymmetric properties of donor and acceptor activities in a cell-free system. Arch. Biochem. Biophys. 240:413-425.
3. Berryman, M.A., W.R. Porter, R.D. Rodewald, and A.L. Hubhard. 1992. Effects of tannic acid on antigenicity and membrane contrast in ultrastruclural immunocytochemistry. J. Histochem. Cytochem. 10:845-857.
4. Boldin, M.P., E.E. Varfolomeev, Z. Pancer, I.E. Mett, J.H. Camonis. and D. Wallach. 1995. A novel protein that interacts with the death domain of Fas/APO-1 contains a sequence motif related to the death domain. J. Biol. Chem. 270:7795-7798.
5. Boldin, M.P., T.M. Goncharov, Y.V. Goltsev, and D. Wallach. 1996. Involvement of MACH, a novel MORT1/FADD-interacting protease. in Fas/APO-1- and TNF receptor-induced cell death. Cell. 85:803-815.
6. Casciola-Rosen, L.A., G. Anhalt, and A. Rosen. 1994a. Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J. Exp. Med. 179:1317-1330.
7. Casciola-Rosen. L.A., D.K. Miller, G.J. Anhalt, and A. Rosen. 1994b. Specific cleavage of the 70-kD protein component of the U1 small nuclear ribonucleoprotein is a characteristic biochemical feature of apoptotic cell death. J. Biol. Chem. 269:30757-30760.
8. Casciola-Rosen. E.A., G.J. Anhalt, and A. Rosen. 1995. DNA-dependent protein kinase is one of a subset of autoantigens specifically cleaved early during apoptosis. J. Exp. Med. 182:1625-1634.
9. Casciola-Rosen, E.A., D.W. Nicholson, T. Chong, K.R. Rowan, N.A. Thornberry, D.K. Miller, and A. Rosen. 1996. Apopain/CPP32 cleaves proteins that are essential for cellular repair: a fundamental principle of apoplotic death. J. Exp. Med. 183:1957-1964.
10. Castedo, M., A. Macho, N. Zamzami, T. Hirsch. P. Marchetti, J. Uriel, and G. Kroemer. 1995. Mitochondrial perturbations define Iymphocytes undergoing apoptotic depletion in vivo. Eur. J. Immunol. 25:3277-3284.
11. Chinnaiyan, A.M., and V.M. Dixit. 1996. The cell-death machine. Curr. Biol. 6:555-562.
12. Chinnaiyan, A.M., K. O'Rourke, M. Tewari, and V.M. Dixit. 1995. FADD, a novel death domain-containing protein, interacts with the death domain of Fas and iniliates apopiosis. Cell. 81:505-512.
13. Chinnaiyan, A.M., W.E. Hanna, K. Orth, H.J. Duan, G.G. Poirier, C.J. Froelich, and V.M. Dixit. 1996a. Cytotoxic T-cell-derived granxyme B activates the apoptotic protease ICE-LAP3. Curr. Biol. 6:897-899.
14. Chinnaiyan, A.M., K. Orth, K. O'Rourke, H.J. Duan, G.G. Poirier, and V.M. Dixit. 1996b. Molecular ordering of the cell death pathway: Bcl-2 and Bcl-xL function upstream of the Ced-3-like apoptotic proteases. J. Biol. Chem. 271: 4573-4576.
15. Chinnaiyan, A.M., K. O'Rourfce, B.R. Lane, and V.M. Dixit. 1997. Interaction of CED-4 with CED-3 and CED-9: a molecular framework for cell death. Science. 275:1122-1126.
16. Cossarizza, A., C. Franceschi, D. Monti, S. Salvioli, E. Bellesia, R. Rivabene, L. Biondo, G. Rainaldi, A. Tinari, and W. Malorni. 1995. Protective effect of N-acetyl-cysteine in tumor necrosis factor-α-induced apoptosis in U937 cells: the role of mitochondria. Exp. Cell Res. 220:232-240.
17. Darmon, A.J., D.W. Nicholson, and R.C. Bleackley. 1995. Activation of the apoptotic protease CPP32 by cytotoxic T-cell-derived granzyme B. Nature. 377:446-448.
18. Deckwerth, T.L., and E.M. Johnson. 1993. Temporal analysis of events associated with programmed cell death (apoptosis) of sympathetic neurons deprived of nerve growth factor. J. Cell Biol. 123:1207-1222.
19. Duan, H., K. Orth, A.M. Chinnaiyan, G.G. Poirier, C.J. Froclich, W.-W. He, and V.M. Dixit. 1999. ICE-LAP6, a novel member of the ICE/Ced-3 gene-family, is activated by the cytotoxic T cell protease granzyme B. J. Biol. Chem. 271:16720-16724.
20. L. J. Biol. Chem. 271:17601-17604.
21. Gu, Y., C. Sarnecki, M.A. Fleming, J.A. Lippke, R.C. Bleakley, and M.S.S. Su. 1996. Processing and activation of CMH-1 by aranzyme B. J. Biol. Chem. 271:10816-10820.
22. Haimowitz-Friedman, A., C.-C. Kan, D. Ehleiter, R.S. Persaud, M. McLoughlin. Z. Fuks, and R.N. Kolesnick. 1994. Ionizing radiation acts on cellular membranes to generate ceramide and initiate apoptosis. J. Exp. Med. 180: 525-535.
23. Hanna, W.L., X. Zhang, J. Turhov, U. Winkler, D. Hudig, and C.J. Froelich. 1993. Rapid purification of cationic granule proteases: application to human granzymes. Prot. Expr. Purif. 3:398-404.
24. Henkart, P.A., and S. Grinstein. 1996. Apoptosis: mitochondria resurrected? J. Exp. Med. 183:1293-1295.
25. Ihrke, G., E.B. Neufeld, T. Meads, M.R. Shanks, D. Cassio, M. Laurent, T.A. Schroer, R.E. Pagano, and A.L. Hubbard. 1993. WIF-B cells: an in vitro model for studies of hepatocyle polarity. J. Cell Biol. 123:1761-1775.
26. Jacobson, M.D., M. Weil, and M.C. Raff. 1996. Role of Ced3/ICE-family proteases in staurosporine-induced programmed cell death. J. Cell Biol. 133: 1041-1051.
27. Jacobson, M.D., M. Weil, and M.C. Raff. 1997. Programmed cell death in animal development. Cell. 88:347-354.
28. Kluck, R.M., E. Bossy-Wetzel, D.R. Green, and D.D. Newmeyer. 1997. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science. 275:1132-1136.
29. Krajewski, S., S. Tanaka, S. Takayama, M.J. Schihler, W. Fenton, and J.C. Reed. 1993. Investigation of the subcellular distribution of the Bcl-2 oncoprotein: residence in the nuclear envelope, endoplasmic reticulum, and outer mitochondrial membranes. Cancer Res. 53:4701-1714.
30. Kroemer, G., N. Zamzami, and S.A. Susin. 1997. Mitochondrial control of apoptosis. Immunol. Today. 44:44-51.
31. Li, P., D. Nijhawan, I. Budihardjo, S.M. Srinivasula, M. Ahmad, E.S. Alnemri, and X. Wang. 1997. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 91:479-489.
32. Liu, X., C.N. Kim, J. Yang, R. Jemmerson, and X. Wang. 1996. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell. 86:147-157.
33. Macho, A., M. Casledo, P. Marchetti, J.J. Aguilar, D. Decaudin, N. Zamzami, P.M. Girard, J. Uriel, and G. Kroemer. 1995. Mitochondrial dysfunctions in circulating T lymphocytes from human immunodeficiency virus-1 carriers. Blood. 86:2481-2487.
34. Martin, S., G. Amarante-Mendes, L. Shi, T.-H. Chuang, C. Casiano, G. O'Brian, P. Fitzgerald, E. Tan, G. Bokoch, A. Greenberg, and D. Green. 1996. The cytotoxic cell protease granzyme B initiates apoptosis in a cell-free system by proteolytic processing and activation of the ICE/CED-3 family protease. CPP32, via a novel two-step mechanism. EMBO (Eur. Mol. Biol. Organ.) J. 15:2407-2416.
35. Martin, S.J., and D.R. Green. 1995. Protease activation during apoptosis: death by a thousand cuts? Cell. 82:349-352.
36. Muzio, M., A.M. Chinnaiyan, F.C. Kischkel, K. O'Rourke, A. Shevchenko, J. Ni, C. Scaffidi, J.D. Bretz, M. Zhang, R. Gentz, et al. 1996. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell. 85:817-827.
37. Muzio, M., G.S. Salvesen, and V.M. Dixit. 1997. FLICE induced apoptosis in a cell-free system - cleavage of caspase zymogens. J. Biol. Chem. 272:2952-2956.
38. Newmeyer, D.D., D.M. Farschon, and J.C. Reed. 1994. Cell-tree apoptosis in Xenopus egg extracts: inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochondria. Cell. 79:353-364.
39. Nicholson, D.W., A. Ali, N.A. Thornberry, J.P. Vaillancouty, C.K. Ding, M. Gallant, Y. Gareau, P.R. Griffin, M. Labele, Y.A. Lazcbnik, et al. 1995. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature. 376:37-43.
40. Nicholson, D.W., and W.C. McMurray. 1984. CDP-diglyceride hvdrolase from pig liver mitochondria. Can. J. Biochem. Cell Biol. 62:1205-1216.
41. Nicholson, D.W., and N.A. Thornberry. 1997. Caspases: killer proteases. Trends Biochem. Sci. 22:299-306.
42. Nicholson, D.W., H. Kohler, and W. Neupert. 1987. Import of cytochrome c into mitochondria. Cytochrome cheme lyase. Eur. J. Biochem. 164:147-157.
43. Olmsted, J.B. 1981. Affinity purification of antibodies from diazotrzed paper blots of heterogeneous protein samples. J. Biol. Chem. 256:11955-11957.
44. Orth, K., K. O'Rourke, G.S. Salvesen, and V.M. Dixit. 1996. Molecular ordering of apoptotic mammalian CED-3/ICE-like proteases. J. Biol. Chem. 271: 20977-20980.
45. Petit, P.X., H. Lecoeur, E. Zorn, C. Dauguel, B. Mignotte, and M.-L. Gougeon. 1995. Alterations in mitochondrial structure and function are early events of dexamethasone-induced thymocyte apoptosis. J Cell Biol. 130:157-167.
46. Quan, L.T., A. Caputo, R.C. Bleakley, D.J. Pickup, and G.S. Salveson. 1995. Granzyme B is inhibited by the cowpox virus serpin cytokine response modifier A. J. Biol. Chem. 270:10377-10379.
47. Quart, L.T., M. Tewari, K. O'Rourke, V. Dixit, S.J. Snipas, G.G. Poirier, C. Ray, D.J. Pickup, and G.S. Salveson. 1996. Proteolytic activation of the cell death protease Yama/CPP32 by granzyme B. Proc. Natl. Acad. Sci. USA. 93: 1972-1976.
48. Reed, J.C. 1994. Bcl-2 and the regulation of programmed cell death. J. Cell Biol. 124:1-6.
49. Reed, J.C. 1997a. Cytochrome c: can't live with it - can't live without it. Cell. 91: 559-562.
50. Reed, J. 1997e. Double identity for proteins of the Bcl-2 family. Nature. 387: 773-776.
51. Rotonda, J., D.W. Nicholson, K.M. Fazil, M. Gallant, Y. Gareau, M. Labele, E.P. Peterson, D.M. Rasper, R. Ruel, J.P. Vaillancourt, et al. 1996. The three-dimensional structure of apopain/CPP32, a key mediator of apoptosis. Nat. Struct. Biol. 3:619-625.
52. Salvesen, G., and V.M. Dixit. 1997. Caspases: intracellular signaling by proteolysis. Cell. 91:443-446.
53. Scoggan, K.A., D.W. Nicholson, and A.W. Ford-Huichinson. 1996. Regulation of leukotriene-hiosynthetic enzymes during differentiation of myelocytic HL-60) cells to eosinophilic or neutrophilic cells. Eur. J. Biochem. 230:572-578.
54. Shi, L., G. Chen, G. MacDonald, L. Bergeron, H. Li. M. Miura, R.J. Rotello, D.K. Miller, T. Seshadri, J. Yuan, and A.H. Greenberg. 1996. Activation of an interleukin 1β converting enzyme-dependent apoptosis pathway by granzyme B. Proc. Natl. Acad. Sci. USA. 93:11002-11007.
55. Strasser, A., A.W. Harris, D.C.S. Huang, P.H. Krammer, and S. Cory. 1995. Bcl-2 and Fas/APO-1 regulate distinct pathways to lymphocyte apoptosis. EMBO (Eur. Mol. Biol. Organ.). J. 14:6136-6147.
56. Susin, S.A., N. Zamzami, M. Castedo, E. Daugas, H.G. Wang, S. Geley, F. Fassy, J.C. Reed, and G. Kroemer. 1997. The central executioner of apoptosis: multiple connections between protease activation and mitochondria in Fas/APO-1/CD95- and ceramide-induced apoptosis. J. Exp. Med. 186:25-37.
57. Susin, S.A., N. Zamzami, M. Castedo, T. Hirsch, P. Marchetti, A. Macho, E. Daugas, M. Geuskens, and G. Kroemer. 1996. Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J. Exp. Med. 184:1331-1341.
58. Taylor, I.C.A., S. Roy, P. Yaswen, M.R. Stampfer, and H.E. Varmus. 1995. Mouse mammary tumors express elevated levels of RNA encoding the murine homolog of SKY, a putative receptor kinase. J. Biol. Chem. 270:6872-6880.
59. Thompson, C.B. 1995. Apoptosis in the pathogenesis and treatment of disease. Science. 267:1456-1462.
60. Thornberry N.A., T.A. Ranon, E.P. Peterson, D.M. Rasper.,T. Timkey, M. Garcia-Calvo, V.M. Houtzager, P.A. Nordstrom.,S. Roy, J.P. Vaillancourt. et al. 1997. A combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis. J. Biol. Chem. 272:17907-17911.
61. L regulates the membrane potential and volume homeostasis of mitochondria. Cell. 91:627-637.
62. Vaux, D.L. 1997. CED-4: the third horseman of apoptosis. Cell. 90:389-590.
63. Vaux, D.L., and A. Strasser. 1996. The molecular biology of apoptosis. Proc. Natl. Acad. Sci. USA. 93:2239-2244.
64. Vavssiere, J.-L., P.X. Petit, Y. Risler, and B. Mignotte. 1994. Commitment to apoptosis is associated with changes in mitochondrial biogenesis and activity in cell lines conditionally immortalized with simian virus 40. Proc. Natl. Acad. Sci. USA. 91:11752-11756.
65. White, E. 1996. Life, death, and the pursuit of apoptosis. Genes Dev. 10:1-15.
66. Wu. D., H.D. Wallen, and G. Nunez. 1997. Interaction and regulation of subcellular localization of CED-4 by CED-9. Science. 275:1126-1129.
67. Yang, J., X. Liu, K. Bhalla, C.N. Kim, A.M. Ibrado, J. Cai, T.-I. Peng, D.P. Jones, X. Wang, X.S. Liu, et al. 1997. Prevention of apoplosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science. 275:1129-1132.
68. Yin, X.-M., Z.N. Oltvai, D.J. Veis-Novack, G.P. Linette, and S.J. Korsmeyer. 1994. Bcl-2 gene family and the regulation of programmed cell death. Cold Spring Harbor Symp. Quant. Biol. 59:387-394.
69. Zamzami, N., P. Marchetti, M. Castedo, D. Decaudin, A. Macho, T. Hirsch, S. Susin, P.X. Petit, G.B. Mignolte, and G. Kroemer. 1995a. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med. 182:367-377.
70. Zamzami, N., P. Marchetti, M. Castedo, C. Zanin, J.-L. Vayssiere, P.X. Petit, and G. Kroemer. 1995b. Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo. J. Exp. Med. 181:1661-1672.
71. Zamzami, N., S.A. Susin, P. Marchetti, T. Hirsch, I. Gomez-Monterrey, M. Castedo, and G. Kroemer. 1996. Mitochondrial control of nuclear apoptosis. J. Exp. Med. 183:1533-1544.
72. Zou, H., W.J. Henzel, X. Liu. A. Lutschg, and X. Wang. 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.