Sequential acquisition of mitochondrial and plasma membrane alterations during early lymphocyte apoptosis

Journal of Immunology

Volumn 157, Issue 2, 1996, Pages 512-521

  Castedo, Maria ^a   Hirsch, Tamara ^a   Susin, Santos A ^a   Zamzami, Naoufal ^a   Marchetti, Philippe ^a   Macho, Antonio ^a   Kroemer, Guido ^a,b  

^a CNRS   (France)

^b NONE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DEXAMETHASONE; DNA FRAGMENT; MENADIONE; PHOSPHATIDYLSERINE; PROTEIN P53; PROTEINASE INHIBITOR; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL DEATH; CELL MEMBRANE; CHROMATIN CONDENSATION; CONTROLLED STUDY; CYTOFLUOROMETRY; ETIOLOGY; FEMALE; LYMPHOCYTE; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; REGULATOR GENE; RESPIRATORY CHAIN;

ANIMALS; APOPTOSIS; CELL MEMBRANE; FEMALE; GENES, P53; LYMPHOCYTES; MICE; MICE, INBRED BALB C; MICE, MUTANT STRAINS; PHOSPHATIDYLSERINES; SUBMITOCHONDRIAL PARTICLES; TIME FACTORS;

EID: 0029944880     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (67)

1. Kerr, J. F. R., A. H. Wyllie, and A. R. Currie. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26:239.
2. Willie, A. H. 1980. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284:555.
3. 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.
4. 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.
5. Henkart, P. A. 1995. Apoptosis: O death, where is thy sting? J. Immunol. 154: 4905.
6. Lazebnik, Y. A., S. Cole, C. A. Cooke, W. G. Nelson, and W. C. Earnshaw. 1993. Nuclear events of apoptosis in vitro in cell-free mitotic extracts: a model system for analysis of the active phase of apoptosis. J. Cell Biol. 123:7.
7. 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.
8. 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.
9. 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.
10. 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.
11. 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.
12. 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.
13. 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.
14. 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.
15. Kroemer, G., P. X. Petit, N. Zamzami, J.-L. Vayssière, and B. Mignotte. 1995. The biochemistry of apoptosis. FASEB J. 9:1277.
16. Zamzami, N., S. A. Susin, P. Marchetti, T. Hirsch, M. Castedo, and G. Kroemer. 1996. Mitochondrial control of nuclear apoptosis. J. Exp. Med. 183:1533.
17. Cohen, J. J. 1993. Apoptosis. Immunol. Today 14:126.
18. Savill, J., V. Fadok, P. Henson, and C. Haslett. 1993. Phagocyte recognition of cells undergoing apoptosis. Immunol. Today 14:131.
19. Hopkinson-Wooley, J., D. Hughes, S. Gordon, and P. Martin. 1994. Macrophage recruitment during limb development and wound healing in the embryonic and foetal mouse. J. Cell Sci. 107:1159.
20. Taniguchi, K., N. Sato, and Y. Uchiyala. 1995. Apoptosis and heterophagy of medial edge epithelial cells of the secondary palatine shelves during fusion. Arch. Histol. Cytol. 58:191.
21. Gonzalo, J. A., A. González-García, C. Martínez-A., and G. Kroemer. 1993. Glucocorticoid-mediated control of the clonal deletion and activation of peripheral T cells in vivo. J. Exp. Med. 177:1239.
22. Matsubara, K., M. Kubota, K. Kuwakado, H. Hirota, Y. Wakazono, Y. Akiyama, H. Mikawa, and S. Adachi. 1994. Induction of apoptosis in childhood acute leukemia by chemotherapeutic agents: failure to detect evidence of apoptosis in vivo. Eur. J. Haematol. 52:47.
23. Kaufmann, Y., A. Many, G. Rechavi, O. Mor, M. Biniaminov, E. Rosenthal, M. Levanon, J. Davidsohn, I. Aizman, Z. Mark, F. Broksimoni, and B. Ramot. 1995. Lymphoma with recurrent cycles of spontaneous remission and relapse: possible role of apoptosis. N. Engl. J. Med. 332:507.
24. Surh, C. D., and J. Sprent. 1994. T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 372:100.
25. Fadok, V. A., D. R. Voelker, P. A. Campbell, J. J. Cohen, D. L. Bratton, and P. M. Henson. 1992. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148:2207.
26. Koopman, G., C. P. M. Reutelingsperger, G. A. M. Kuijten, R. M. J. Keehnen, S. T. Pals, and M. H. J. van Oers. 1994. Annexin V for flow cytometry detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84: 1415.
27. Martin, S. J., C. P. M. Reutelingsperger, A. J. McGahon, J. A. Rader, R. C. A. A. van Schie, D. M. LaFace, and D. R. Green. 1995. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J. Exp. Med. 182:1545.
28. Verthoven, B., R. A. Schlegel, and P. Williamson. 1995. Mechanisms of phosphatidylserine exposure, a phagocyte recognition signal, on apoptotic T lymphocytes. J. Exp. Med. 182:1597.
29. Savill, J. S., P. M. Henson, and C. Haslett. 1989. Phagocytosis of aged human neutrophils by macrophages is mediated by a novel "charge-sensitive" recognition mechanism. J. Clin. Invest. 84:1518.
30. Savill, J., I. Dransfield, N. Hogg, and C. Haslett. 1990. Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature 343:170.
31. + T cells undergoing apoptosis: a mechanism for T cell clearance during resolution of viral infections. J. Exp. Med. 180:1943.
32. Tsuji, S., K. Kaji, and S. Nagasawa. 1994. Activation of the alternative pathway of human complement by apoptotic umbilical vein endothelial cells. J. Biochem. 116:794.
33. Donehower, L. A., M. Harvey, B. L. Slagle, M. J. McArthur, C. A. Montgomery, J. S. Butel, and A. Bradley. 1992. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumors. Nature 356:215.
34. 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.
35. Aten, J., P. Prigent, P. Poncet, C. Blanpied, N. Claessen, P. Druet, and F. Hirsch. 1995. Mercuric chloride-induced programmed cell death of a murine T cell hybridoma. I. Effect of the proto-oncogene Bcl-2. Cell Immunol. 161:98.
36. intermediate T cells in the liver of normal adult mice: implications for lpr pathogenesis. Int. Immunol. 6:533.
37. 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.
38. 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.
39. Petit, J. M., A. Maftah, M. H. Ratinaud, and R. Julien. 1992. 10 N-nonyclacridine orange interacts with cardiolipin and allows for the quantification of phospholipids in isolated mitochondria. Eur. J. Biochem. 209:267.
40. Schlegel, R. A., M. Stevens, K. Lumley-Sapansky, and P. Williamson. 1993. Altered lipid packing identifies apoptotic thymocytes. Immunol. Lett. 36:283.
41. Vermes, I., C. Haaren, H. Steffens-Nakken, and C. Reutelingsperger. 1995. A novel assay for apoptosis: flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled annexin V. J. Immunol. Methods 184:39.
42. 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.
43. Huang, L., G. Soldevila, M. Leeker, R. Flavell, and I. N. Crispe. 1994. The liver eliminates T cells undergoing antigen-triggered apoptosis in vivo. Immunity 1:741.
44. Costantini, P., B. V. Chernyak, V. Petronilli, and P. Bernardi. 1995. Selective inhibition of the mitochondrial permeability transition pore at the oxidation-reduction sensitive dithiol by monobromobimane. FEBS Lett. 362:239.
45. Klingenberg, M. 1980. The ADP-ATP translocation in mitochondria, a membrane potential controlled transport. J. Membr. Biol. 56:97.
46. 2+ and phosphate. Biochem. Biophys. Res. Commun. 111: 792.
47. 2+-induced large-amplitute 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.
48. 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 sulfhydril reagent eosin-5-maleimide. Biochemistry 33:9530.
49. Hoffmann, B., A. Stockl, M. Schlame, K. Beyer, and M. Klingenberg. 1994. The reconstituted ADP/ATP carriers activity has an absolute requirement for cardiolipin as shown in cysteine mutants. J. Biol. Chem. 269:1940.
50. Clarke, A. R., C. A. Purdie, D. J. Harrison, R. G. Morris, C. C. Bird, M. L. Hooper, and A. H. Wyllie. 1993. Thymocyte apoptosis induced by p53-dependent and independent pathways. Nature 362:849.
51. Lowe, S. W., E. M. Schmitt, S. W. Smith, B. A. Osborne, and T. Jack. 1993. p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature 362: 847.
52. Lagasse, E., and I. L. Weissman. 1994. bcl-2 inhibits apoptosis of neutrophils but not their engulfment by macrophages. J. Exp. Med. 179:1047.
53. Broekemeier, K. M., M. E. Dempsey, and D. R. Pfeiffer. 1989. Cyclosporin A is a potent inhibitor of the inner membrane permeability transition in liver mitochondria. J. Biol. Chem. 264:7826.
54. Szabó, I., and M. Zoratti. 1991. The giant channel of the inner mitochondrial membrane is inhibited by cyclosporin A. J. Biol. Chem. 266:3376.
55. Zoratti, M., and I. Szabó. 1994. Electrophysiology of the inner mitochondrial membrane. J. Bioenerg. Biomembr. 26:543.
56. 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.
57. 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. Biochem. Biophys. Acta 1187:255.
58. Savage, M. K., and D. J. Reed. 1994. Release of mitochondrial glutathione and calcium by a cyclosporin A-sensitive mechanism occurs without large amplitude swelling. Arch. Biochem. Biophys. 315:142.
59. Zoratti, M., and I. Szabò. 1995. The mitochondrial permeability transition. Biochem. Biophys. Acta - Rev. Biomembranes 1241:139.
60. 2+: their relationship to apoptosis and oncogenesis. FEBS Lett. 325:104.
61. Costantini, P., B. V. Chernyak, V. Petronilli, and P. Bernardi. 1996. Modulation of the mitochondrial permeability transition pore by pyridine nucleotides and dithiol oxidation at two separate sites. J. Biol. Chem. 271:6746.
62. Aguilar, H. I., R. Botla, A. S. Arora, S. F. Bronk, and O. J. Gores. 1996. Induction of the mitochondrial permeability transition by protease activity in rats: a mechanism of hepatocyte necrosis. Gastroenterology 110:558.
63. Pfeiffer, D. R., T. I. Gudz, S. A. Novgorodov, and W. L. Erdahl. 1995. The peptide mastoparan is a potent facilitator of the mitochondrial permeability transition. J. Biol. Chem. 270:4923.
64. Kristal, B. S., B. K. Park, and B. P. Yu. 1996. 4-Hydroxyhexenal is a potent inducer of the mitochondrial permeability transition. J. Biol. Chem. 271:6033.
65. Menon, A. K. 1995. Flippases. Trends Cell Biol. 5:355.
66. Martin, S. J., C. A. O'Brien, W. K. Nishioka, A. J. McGahon, A. Mahbouri, T. C. Saido, and D. R. Green. 1995. Proteolysis of fodrin (non-erythroid spectrin) during apoptosis. J. Biol. Chem. 270:6425.
67. Hockenbery, D. M., Z. N. Oltvai, X.-M. Yin, C. L. Milliman, and S. J. Korsmeyer. 1993. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75:241.