Mitochondrial Permeability Transition Triggers Lymphocyte Apoptosis

Journal of Immunology

Volumn 157, Issue 11, 1996, Pages 4830-4836

  Marchetti, Philippe ^a   Hirsch, Tamara ^a   Zamzami, Naoufal ^a   Castedo, Maria ^a   Decaudin, Didier ^a   Susin, Santos A ^a   Masse, Benjamin ^a   Kroemer, Guido ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLVALYL ALANYL ASPARTYL FLUOROMETHYL KETONE; BENZYLOXYCARBONYLVALYL-ALANYL-ASPARTYL FLUOROMETHYL KETONE; PEPTIDE CHLOROMETHYL KETONE; PROTEIN BCL 2; PROTEINASE INHIBITOR; PROTOPORPHYRIN; REACTIVE OXYGEN METABOLITE;

ANIMAL; APOPTOSIS; ARTICLE; BAGG ALBINO MOUSE; CELL MEMBRANE POTENTIAL; CHROMATIN; CYTOLOGY; DRUG EFFECT; IN VITRO STUDY; INTRACELLULAR MEMBRANE; LYMPHOCYTE; METABOLISM; MITOCHONDRION; MOUSE; PERMEABILITY; PHYSIOLOGY; PROTEIN SYNTHESIS; T LYMPHOCYTE;

AMINO ACID CHLOROMETHYL KETONES; ANIMALS; APOPTOSIS; CHROMATIN; INTRACELLULAR MEMBRANES; LYMPHOCYTES; MEMBRANE POTENTIALS; MICE; MICE, INBRED BALB C; MITOCHONDRIA; PERMEABILITY; PROTEASE INHIBITORS; PROTEIN BIOSYNTHESIS; PROTO-ONCOGENE PROTEINS C-BCL-2; PROTOPORPHYRINS; REACTIVE OXYGEN SPECIES; T-LYMPHOCYTES;

EID: 0030471143     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (66)

1. Attardi, G., and O. Schatz. 1988. Biogenesis of mitochondria. Annu. Rev. Cell Biol. 4:289.
2. Chen, L. B. 1988. Mitochondrial membrane potential in living cells. Annu. Rev. Cell Biol. 4:155.
3. 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.
4. Vayssière, 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.
5. Zamzami, N., P. Marchetti, M. Castedo, C. Zanin, J.-L. Vayssière, P. X. Petit, and G. Kroemer. 1995. Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo. J. Exp. Med. 181:1661.
6. Petit, P. X., H. LeCoeur, E. Zorn, C. Dauguet, B. Mignotte, and M. L. Gougeon. 1995. Alterations of mitochondrial structure and function are early events of dexamethasone-induced thymocyte apoptosis. J. Cell. Biol. 130:157.
7. 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-acetylcysteine in tumor necrosis factor-alpha-induced apoptosis in U937 cells: the role of mitochondria. Exp. Cell Res. 220:232.
8. Castedo, M., A. Macho, N. Zamzami, T. Hirsch, P. Marchetti, J. Uriel, and G. Kroemer. 1995. Mitochondrial perturbations define lymphocytes undergoing apoptotic depletion in vivo. Eur. J. Immunol. 25:3277.
9. Kroemer, G., P. X. Petit, N. Zamzami, J.-L. Vayssière, and B. Mignotte. 1995. The biochemistry of apoptosis. FASEB J. 9:1277.
10. Zamzami, N., P. Marchetti, M. Castedo, D. Decaudin, A. Macho, T. Hirsch, S. A. Susin, P. X. Petit, B. Mignotte, and G. Kroemer. 1995. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med. 182:367.
11. Macho, A., M. Castedo, 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.
12. Osborne, B. A., S. W. Smith, Z.-G. Liu, K. A. McLaughlin, L. Grimm, and L. M. Schwartz. 1994. Identification of genes induced during apoptosis in T cells. Immunol. Rev. 142:301.
13. Jacobson, M. D., J. F. Burne, and M. C. Raff. 1994. Programmed cell death and Bcl-2 protection in the absence of a nucleus. EMBO J. 13:1899.
14. Schulze-Osthoff, K., H. Walczak, W. Droge, and P. H. Krammer. 1994. Cell nucleus and DNA fragmentation are not required for apoptosis. J. Cell Biol. 127:15.
15. Newmeyer, D. D., D. M. Farschon, and J. C. Reed. 1994. Cell-free apoptosis in Xenopus egg extracts: inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochondria. Cell 79:353.
16. Martin, S. J., D. D. Newmeyer, S. Mathisa, D. M. Farschon, H. G. Wang, J. C. Reed, R. N. Kolesnick, and D. R. Green. 1995. Cell-free reconstitution of Fas-, UV radiation- and ceramide-induced apoptosis. EMBO J. 14:5191.
17. Zamzami, N., S. A. Susin, P. Marchetti, T. Hirsch, I. Gómez-Monterrey, M. Castedo, and G. Kroemer. 1996. Mitochondrial control of nuclear apoptosis. J. Exp. Med. 183:1533.
18. Bernardi, P., K. M. Broekemeier, and D. R. Pfeiffer. 1994. Recent progress on regulation of the mitochondrial permeability transition pore; a cyclosporin-sensitive pore in the inner mitochondrial membrane. J. Bioenerg. Biomembr. 26:509.
19. Zoratti, M., and I. Szabò. 1995. The mitochondrial permeability transition. Biochim. Biophys. Acta 1241:139.
20. Bernardi, P., and V. Petronilli. 1996. The permeability transition pore as a mitochondrial calcium release channel: a critical appraisal. J. Bioenerg. Biomembr. 28:129.
21. McEnery, M. W., A. M. Snowman, R. R. Trifiletti, and S. H. Snyder. 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.
22. 2+. J. Biol. Chem. 268:1011.
23. Nicolli, A., E. Basso, V. Petronilli, R. M. Wenger, and P. Bernardi. 1996. Interactions of cyclophilin wild mitochondrial inner membrane and regulation of the permeability transition pore, a cyclosporin A-sensitive channel. J. Biol. Chem. 271:2185.
24. 2+ concentration. Arch. Biochem. Biophys. 269:365.
25. Kroemer, G. 1995. The pharmacology of T cell apoptosis. Adv. Immunol. 58:211.
26. Boutry, M., and M. Briquet. 1982. Mitochondrial modifications associated with the cytoplasmic male sterility in faba beans. Eur. J. Biochem. 127:129.
27. Petit, P. X., J. E. O'Connor, D. Grunwald, and S. C. Brown. 1990. Analysis of the membrane potential of rat- and mouse-liver mitochondria by flow cytometry and possible applications. Eur. J. Biochem. 220:389.
28. Lumbach, G. W. M., H. C. Cox, and W. Berends. 1970. Elucidation of the chemical structure of bongkrekic acid. I. Isolation, purification and properties of bongkrekic acid. Tetrahedron 26:5993.
29. Green, D. R., A. Mahboubi, W. Nishioka, S. Oja, F. Echeverri, Y. Shi, J. Glynn, Y. Yang, J. Ashwell, and R. Bissonnette. 1994. Promotion and inhibition of activation-induced apoptosis in T-cell hybridomas by oncogenes and related signals. Immunol. Rev. 142:321.
30. Pastorino, J. G., G. Simbula, E. Gilfor, J. B. Hoek, and J. L. Farber. 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.
31. Nicoletti, I., G. Migliorati, M. C. Pagliacci, and C. Riccardi. 1991. A rapid simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods 139:271.
32. + T cells in mice tolerant to Staphylococcus aureus enterotoxin B. Nature 349:245.
33. Broekemeier, K. M., M. E. Dempsey, and D. R. Pfeifler. 1989. Cyclosporin A is a potent inhibitor of the inner membrane permeability transition in liver mitochondria. J. Biol. Chem. 264:7826.
34. Szabo, I., and M. Zoratti. 1991. The giant channel of the inner mitochondrial membrane is inhibited by cyclosporin A. J. Biol. Chem. 266:3376.
35. Petronilli, V., A. Nicolli, P. Costantini, R. Colonna, and P. Bernardi. 1994. Regulation of the permeability transition pore, a voltage-dependent mitochondrial channel inhibited by cyclosporin A. Biochim. Biophys. Acta 1187:255.
36. Marty, I., G. Brandolin, J. Gagnon, R. Brasseur, and P. V. Vignais. 1992. Topography of the membrane-bound ADP/ATP carrier assessed by enzymatic proteolysis. Biochemistry 31:4058.
37. Majima, E., Y. Shinohara, N. Yamaguchi, Y. M. Hong, and H. Terada. 1994. Importance of loops of mitochondrial ADP/ATP carrier for its transport activity deduced from reactivities of its cysteine residues with the sulfhydryl reagent cosin-5-maleimide. Biochemistry 33:9530.
38. 2+-induced large-amplitude swelling of liver and heart mitochondria by cyclosporin is probably caused by the inhibitor binding to mitochondrial-matrix peptidyl-prolyl cis-trans isomerase and preventing it interacting with the adenine nucleotide translocase. Biochem. J. 268:153.
39. Kinnally, K. W., D. B. Zorov, Y. N. Antonenko, S. H. Snyder, M. W. McEnery, and H. Tedeschi. 1993. Mitochondrial benzodiazepine receptor linked to inner membrane ion channels by nanomolar actions of ligands. Proc. Natl. Acad. Sci. USA 90:1374.
40. Rothe, G., and G. Valet. 1990. Flow cytometric analysis of respiratory burst activity in phagocytes with hydroethidine and 2′,7′-dichlorofluorescin. J. Leukocyte Biol. 47:440.
41. Carter, W. O., P. K. Narayanan, and J. P. Robinson. 1994. Intracellular hydrogen peroxide and superoxide anion detection in endothelial cells. J. Leukocyte Biol. 55:253.
42. Verma, A., J. S. Nye, and S. H. Snyder. 1988. Porphyrins are endogenous ligands for the mitochondrial (peripheral-type) benzodiazepine receptor. Proc. Natl. Acad. Sci. USA 84:2256.
43. 3H]-PK 11195 binding to platelets. Neuroreport 5:1093.
44. Klingenberg, M. 1980. The ADP-ATP translocation in mitochondria, a membrane potential controlled transport. J. Membr. Biol. 56:97.
45. 2+ and phosphate. Biochem. Biophys. Res. Commun. 111: 792.
46. McConkey, D. J., P. Hartzell, M. Jondal, and S. Orrenius. 1989. Inhibition of DNA fragmentation in thymocytes and isolated thymocyte nuclei by agents that stimulate protein kinase C. J. Biol. Chem. 264:13399.
47. Fearnhead, H. O., A. J. Rivett, D. Dinsdale, and G. M. Cohen. 1995. A preexisting protease is a common effector of thymocyte apoptosis mediated by diverse stimuli. FEBS Lett. 357:242.
48. Fearnhead, H. O., D. Dinsdale, and G. M. Cohen. 1995. An interleukin-1 beta-converting enzyme-like protease is a common mediator of apoptosis in thymocytes. FEBS Lett. 375:283.
49. Zhivotovsky, B., A. Gahm, M. Ankarcrona, P. Nicotera, and S. Orrenius. 1995. Multiple proteases are involved in thymocyte apoptosis. Exp. Cell Res. 221:404.
50. Pronk, G. J., K. Ramer, P. Amiri, and L. T. Williams. 1996. Requirement of an ICE-like protease for induction of apoptosis and ceramide generation by REAPER. Science 271:808.
51. Krajewski, S., S. Tanaka, S. Takayama, M. J. Schibler, 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.
52. Chinnaiyan, A. M., K. Orth, K. Orourke, H. J. Duan, G. G. Poirier, and V. M. Dixit. 1996. Molecular ordering of the cell death pathway-Bcl-2 and Bcl-X(L) function upstream of the CED-3-like apoptotic proteases. J. Biol. Chem. 271: 4573.
53. Slee, E. A., H. J. Zhu, S. C. Chow, M. Macfarlane, D. W. Nicholson, and G. M. Cohen. 1996. Benzyloxycarbonyl-Val-Ala-Asp (OMe) fluoromethylketone (Z-VAD.fmk) inhibits apoptosis by blocking the processing of CPP32. Biochem. J. 315:21.
54. Liu, X., C. N. Kim, J. Yang, R. Jemmerson, and X. Wang. 1996. Induction of apoptic program in cell-tree extracts: requirement for dATP and cytochrome C. Cell 86:147.
55. Susin, S., 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.
56. 2+-dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress. Biochem. J. 255:357.
57. 2+], but not by butyrate. Biochem. J. 268:147.
58. Mehendale, H. M., R. A. Roth, A. J. Gandolfi, J. E. Klaunig, J. J. Lemasters, and L. R. Curtis. 1994. Novel mechanisms in chemically induced hepatotoxicity. FASEB J. 8:1285.
59. 2+-activated inner membrane pore of heart mitochondria. Eur. J. Biochem. 230:1125.
60. Pastorino, J. G., J. W. Snyder, A. Serroni, J. B. Hoek, and J. L. Farber. 1993. Cyclosporin and carnitine prevent the anoxic death of cultured hepatocytes by inhibiting the mitochondrial permeability transition. J. Biol. Chem. 268:13791.
61. 2+ depletion prevents anoxic death of hepalocytes by inhibiting mitochondrial permeability transition. Am. J. Physiol. 268:C676.
62. Hennet, T., G. Bertoni, C. Richter, and E. Peterhans. 1993. Expression of BCL-2 protein enhances the survival of mouse fibrosarcoid cells in tumor necrosis factor-mediated cytotoxicity. Cancer Res. 53:1456.
63. Kane, D. J., T. A. Sarafian, R. Anton, H. Hahn, E. B. Gralla, J. S. Valentine, T. Örd, and D. E. Bredesen. 1993. Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. Science 262:1274.
64. Kane, D. J., T. Ord, R. Anton, and D. E. Bredesen. 1995. Expression of bcl-2 inhibits necrotic neural cell death. J. Neurosci. Res. 40:269.
65. Martinou, J. C., Dubois-Dauphin-M., J. K. Staple, I. Rodriguez, H. Frankowski, M. Missotten, P. Albertini, D. Talabot, S. Catsikas, C. Pietra, and J. Huarte. 1994. Overexpression of Bcl-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia. Neuron 13:1017.
66. Carayon, P., M. Portier, D. Dussossoy, A. Bord, G. Petitpretre, X. Canat, G. Le Fur, and P. Casellas. 1996. Involvement of peripheral benzodiazepine receptors in the protection of hematopoietic cells against oxygen radical species. Blood 87:3170.