Mitochondrial membrane permeabilization during the apoptotic process

Annals of the New York Academy of Sciences

Volumn 887, Issue , 1999, Pages 18-30

  Jacotot, Etienne ^a   Costantini, Paola ^a   Laboureau, Eric ^a   Zamzami, Naoufal ^a   Susin, Santos A ^a   Kroemer, Guido ^a,b  

^a CNRS   (France)

^b NONE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; CALCIUM; CASPASE; CERAMIDE DERIVATIVE; MEMBRANE PROTEIN; NITRIC OXIDE; NUCLEASE; PROTEIN; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BID; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

APOPTOSIS; CELL ULTRASTRUCTURE; CONFERENCE PAPER; DRUG DEVELOPMENT; ENZYME ACTIVATION; HUMAN; MEMBRANE BINDING; MEMBRANE CHANNEL; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; NONHUMAN; PERMEABILITY BARRIER; PROTEIN TRANSPORT; SECOND MESSENGER; SIGNAL TRANSDUCTION;

EID: 0033386851     PISSN: 00778923     EISSN: None     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.1999.tb07919.x     Document Type: Conference Paper

References (70)

1. 1. Kroemer, G. et al. 1995. The biochemistry of apoptosis. FASEB J. 9: 1277-1287.
2. 2. Kroemer, G., N. Zamzami & S.A. Susin. 1997. Mitochondrial control of apoptosis. Immunol Today. 18: 44-51.
3. 3. Kroemer, G. 1997. Mitochondrial implication in apoptosis. Towards an endosymbiotic hypothesis of apoptosis evolution. Cell Death Diff. 4: 443-456.
4. 4. Kroemer, G., B. Dallaporta & M. Resche-Rigon. 1998. The mitochondrial death/ life regulator in apoptosis and necrosis. Annu. Rev. Physiol. 60: 619-642.
5. 5. Liu, X. S. et al. 1996. Induction of apoptotic program in cell-free extracts: requirement for DATP and cytochrome C. Cell. 86: 147-157.
6. 6. Xiang, J., D.T. Chao & S.J. Korsmeyer. 1996. Bax-induced cell death may not require interleukin 16-converting enzyme-like proteases. Proc. Natl. Acad. Sci. USA. 93: 14559-14563.
7. 7. Kluck, R.M. et al. 1997. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science. 275: 1132-1136.
8. 8. Vander Heiden, M.G. et al. 1997. Bcl-XL regulates the membrane potential and volume homeostasis of mitochondria. Cell. 91: 627-637.
9. 9. Green, D.R. & J.C. Reed. 1998. Mitochondria and apoptosis. Science 281: 1309-1312.
10. 10. Scaffidi, C. et al. 1998. Two CD95 (APO-I/Fas) signaling pathways. EMBO J. 17: 1675-1687.
11. 11. Stennicke, H.R. et al. 1998. Pro-caspase-3 is a major physiological target of caspase-8. J Biol. Chem. 273: 27084-27090.
12. 12. Kroemer, G. 1997. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat. Med. 3: 614-620.
13. 13. Zamzami, N. et al. 1998. Subcellular and submitochondrial mechanisms of apoptosis inhibition by Bcl-2-related proteins. Oncogene 16: 2265-2282.
14. 14. Nicholson, D.W. & N.A. Thornberry. 1997. Caspases: killer proteases. Trends Biochem. Sci. 22: 299-306.
15. 15. Ashkenazi, A. & V. M. Dixit. 1998. Death receptors: signaling and modulation. Science 276: 111-113.
16. 16. Green, D.R. & G. Kroemer. 1998. The central execution of apoptosis: mitochondria or caspases? Trends Cell Biol. 8: 267-271.
17. 17. Gross, A. et al. 1998. Enforced dimerization of Bax results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J. 17: 3878-3885.
18. 18. Wolter, K.G. et al. 1997. Movement of Bax from the cytosol to mitochondria during apoptosis. J. Cell Biol. 139: 1281-1292.
19. 19. Goping, I.S. et al. 1998. Regulated targeting of Bax to mitochondria. J. Cell Biol. 143: 207-215.
20. 20. Pastorino, J.G. et al. 1998. The overexpression of Bax produces cell death upon induction of the mitochondrial permeability transition. J. Biol. Chem. 273: 71770-7777.
21. 21. Marzo, I. et al. 1998. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281: 2027-2031.
22. 22. Jürgensmeier, J.M. et al. 1998. Bax directly induces release of cytochrome c from isolated mitochondria. Proc. Natl. Acad Sci. USA. 95: 4997-5002.
23. 2+ ions. J. Cell Biol. 143: 217-224.
24. 24. Shimizu, S. et al. 1998. Bcl-2 prevents apoptotic mitochondrial dysfunction by regulating proton flux. Proc. Natl. Acad Sci. USA. 95: 1455-1459.
25. 25. Luo, X., I. Budiharjo, H. Zou, C. Slaughter & X. Wang. 1998. Bid, a Bcl-2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell. 481-490.
26. 26. Li, H. et al. 1998. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 94: 491-501.
27. 27. Cosulich, S.C. et al. 1997. Regulation of apoptosis by BH3 domains in a cell-free system. Curr. Biol. 12: 913-920.
28. 28. Susin, S.A. et al. 1997. The central executioner of apoptosis. Multiple links between protease activation and mitochondria in Fas/Apo-I/CD95-and ceramide-induced apoptosis. J. Exp. Med. 186: 25-37.
29. 29. Marzo, I. et al. 1998. The permeability transition pore complex: a target for apoptosis regulation by caspases and Bcl-2 related proteins. J. Exp. Med. 187: 1261-1271.
30. 30. Cheng, E.H. Y. et al. 1997. Conversion of Bcl-2 to a Bax-like death effector by caspases. Science 278: 1966-1968.
31. 31. Zoratti, M. & I. Szabò. 1995. The mitochondrial permeability transition. Biochem. Biophys. Acta-Rev. Biomembranes 1241: 139-176.
32. 32. DeMaria, R. et al. 1997. Requirement for GD3 ganglioside in CD95-and ceramide-induced apoptosis. Science 277: 1652-1655.
33. 33. Susin, S.A., N. Zamzami & G. Kroemer. 1998. Mitochondrial regulation of apoptosis. Doubt no more. Biochim. Biophys. Acta (Bioenergetics). 1366: 151-165.
34. +) and nitric oxide simultaneously causes Cyclosporin A-sensitive mitochondrial calcium efflux and depolarisation. Biochem. Pharmacol. 51: 267-273.
35. 35. Scarlett, J.L., M.A. Packer, C.M. Porteous & M.P. Murphy. 1996. Alterations to glutathione and nicotinamide nucleotides during the mitochondrial permeability transition induced by peroxynitrite. Biochem. Pharmacol. 52: 1047-1055.
36. 36. Hortelano, S. et al. 1997. Nitric oxide induces apoptosis via triggering mitochondrial permeability transition. FEBS Lett. 410: 373-377.
37. 37. Ruvolo, P.P. et al. 1998. A functional role for mitochondrial protein kinase C alpha in Bcl2 phosphorylation and suppression of apoptosis. J. Biol. Chem. 273: 25436-25442.
38. 38. Zha, J.P. et al. 1996. Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L). Cell 87: 619-628.
39. 39. Bardelli, A., et al. 1996. HGF receptor associates with the anti-apoptotic protein BAG-1 and prevents cell death. EMBO J. 15: 6205-6212.
40. 40. Bernardi, P. 1996. The permeability transition pore. Control points of a cyclosporin A-sensitive mitochondrial channel involved in cell death. Biochim. Biophys. Acta (Bioenergetics) 1275: 5-9.
41. 41. Halestrap, A.P. et al. 1998. Elucidating the molecular mechanism of the permeability transition and its role in reperfusion injury of the heart. Biochim. Biophys. Acta 1366: 79-94.
42. 42. Beutner, G. et al. 1996. Complexes between kinases, mitochondrial porin, and adenylate translocator in rat brain resemble the permeability transition pore. FEBS Lett. 396: 189-195.
43. 43. Beutner, G. et al. 1998. Complexes between porin, hexokinase, mitochondrial creatine kinase and adenylate translocator display properties of the permeability transition pore. Implication of regulation of permeability transition by the kinases. Biochim. Biophys. Acta-Biomembranes 1368: 7-18.
44. 44. Zamzami, N. et al. 1995. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med. 182: 367-377.
45. 45. Zamzami, N. et al. 1996. Mitochondrial control of nuclear apoptosis. J. Exp. Med. 183: 1533-1544.
46. 46. Pastorino, J. G. et al. 1996. The cytotoxicity of tumor necrosis factor depends on induction of the mitochondrial permeability transition. J. Biol. Chem. 271: 29792-29799.
47. 47. Marchetti, P. et al. 1996. Mitochondrial permeability transition is a central coordinating event of apoptosis. J. Exp. Med. 184: 1155-1160.
48. 48. Polyak, K. et al. 1997. A model for p53-induced apoptosis. Nature 389: 300-305.
49. 49. Bradham, C.A. et al. 1998. The mitochondrial permeability transition is required for tumor necrosis factor alpha-mediated apoptosis and cytochrome c release. Mol. Cell. Biol. 18: 6353-6364.
50. 50. Rück, A., et al. 1998. Reconstituted adenine nucleotide translocator forms a channel for small molecules comparable to the mitochondrial permeability transition pore. FEBS Lett. 426:97-101.
51. 51. Zamzami, N. et al. 1998. The thiol-crosslinking agent diamide overcomes the apoptosis-inhibitory effect of Bcl-2 by enforcing mitochondrial permeability transition. Oncogene 16: 1055-1063.
52. 52. Ravagnan, L. et al. 1998. Lonidamine triggers apoptosis via a direct, Bcl-2-inhibited effect on the mitochondrial permeability transition pore. Oncogene. In press.
53. 53. Tang, D. G. et al. 1998. Apoptosis in the absence of cytochrome c accumulation in the cytosol. Biochem. Biophys. Res. Commun. 242: 380-384.
54. 54. Adachi, S.,R.A. Gottlieb & B.M. Babior. 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.
55. 55. Kuwana, T. et al. 1998. Apoptosis induction by caspase-8 is amplified through the mitochondrial release of cytochrome c. J. Biol. Chem. 273: 16589-16594.
56. 56. Hirsch, T. et al. 1998. PK11195, a ligand of the mitochondrial benzodiazepin receptor, facilitates the induction of apoptosis and reverses Bcl-2-mediated cytoprotection. Exp. Cell Res. 241: 426-434.
57. 57. Fulda, S. et al. 1998. Molecular ordering of apoptosis induced by anti-cancer drugs in neuroblastoma cells. Cancer Res. 58: 4453-4460.
58. 58. Costantini, P. et al. 1996. Modulation of the mitochondrial permeability transition pore by pyridine nucleotides and dithiol oxidation at two separate sites. J. Biol. Chem. 271: 6746-6751.
59. 59. Klingenberg, M. 1980. The ADP-ATP translocation in mitochondria, a membrane potential controlled transport. J. Membrane Biol. 56: 97-105.
60. 2+. Biochemistry 35: 8483-8488.
61. 61. Halestrap, A.P., K.Y. Woodfield & C.P. Connern. 1997. Oxidative stress, thiol reagents, and membrane potential modulate the mitochondrial permeability transition by affecting nucleotide binding to the adenine nucleotide translocase. J. Biol. Chem. 272: 3346-3354.
62. 62. Nicolli, A. et al. 1996. Interactions of cyclophilin with mitochondrial inner membrane and regulation of the permeability transition pore, a cyclosporin A-sensitive channel. J. Biol. Chem. 271: 2185-2192.
63. 63. Connern, C.P. & A.P. Halestrap. 1994. Recruitment of mitochondrial cyclophilin to the mitochondrial inner membrane under conditions of oxidative stress that enhance the opening of a calcium-sensitive non-specific channel. Biochem. J. 302: 321-324.
64. 64. Oltvai, Z.N., C.L. Milliman & S.J. Korsmeyer. 1993. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programed cell death. Cell. 74: 609-619.
65. 65. McEnery, M.W. et al. 1992. Isolation of the mitochondrial benzodiazepine receptor: Association with the voltage-dependent anion channel and the adenine nucleotide carrier. Proc. Natl. Acad. Sci. USA. 89: 3170-3174.
66. 66. Pastorino, J.G. et al. 1994. Protoporphyrin IX, an endogenous ligand of the peripheral benzodiazepin receptor, potentiates induction of the mitochondrial permeability transition and the killing of culture hepatocytes by rotenone. J. Biol. Chem. 269: 31041-31046.
67. 67. Marchetti, P. et al. 1996. Mitochondrial permeability transition triggers lymphocyte apoptosis. J. Immunol. 157: 4830-4836.
68. 68. Hodge, T. & M. Colombini. 1997. Regulation of metabolite flux through voltage-gating of VDAC channels. J. Membr. Biol. 157: 271-279.
69. 69. O'Gorman, E. et al. 1997. The role of creatine kinase in inhibition of mitochondrial permeability transition. FEBS Lett. 414: 253-257.
70. 70. Bernardi, P. & V. Petronilli. 1996. The permeability transition pore as a mitochondrial calcium release channel; a Critical appraisal. J. Bioenerg. Biomembr. 28: 129-136.