Retroactive pathway involving mitochondria in electroloaded cytochrome c-induced apoptosis: Protective properties of Bcl-2 and Bcl-XL

Experimental Cell Research

Volumn 289, Issue 2, 2003, Pages 195-210

  Gabriel, Bruno ^b   Sureau, Franck ^a   Casselyn, Marina ^a   Teissié, Justin ^b   Petit, Patrice Xavier ^a  

^a CHU Cochin Port Royal ^*  (France)

^b INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

Author keywords

Apoptosis; Bcl 2 Bcl XL; Caspases activation; Cytochrome c; Electropermeabilisation; Flow cytometry; Mitochondrial transmembrane potential

Indexed keywords

ALDEHYDE DERIVATIVE; ALLOGRAFT INFLAMMATORY FACTOR 1; AMINO ACID DERIVATIVE; CASPASE; CYTOCHROME C; LIPID; N ACETYLASPARTYLGLUTAMYLVALYLASPARTIC ACID ALDEHYDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; POTASSIUM; PROTEIN; PROTEIN BCL 2; PROTEIN BCL XL; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SECONDARY MITOCHONDRIA DERIVED ACTIVATOR OF CASPASE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; DOWNSTREAM PROCESSING; ELECTRICITY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; LIPID OXIDATION; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; PHENOTYPE; POTASSIUM TRANSPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION;

EID: 0141788635     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-4827(03)00255-6     Document Type: Article

References (66)

1. Li F., Srinivasan A., Wang Y., Armstrong R., Tomaselli K.J., Fritz L.C. Cell-specific induction of apoptosis by microinjection of cytochrome c. Bcl-XL has activity independent of cytochrome c release. J. Biol Chem. 272:1997;30299-30305.
2. Zou H., Henzel W.J., Liu X., Lutschg A., Wang X. Apaf-1, A human protein homologous to C. elegans CED-4, participates in cytochrome c-dependant activation of caspase-3. Cell. 90:1997;405-413.
3. Susin S.A., Lorenzo H.K., Zamzami N., Marzo I., Snow E.B., Brothers G.M., Mangion J., Jacotot E., Costantini P., Loeffler M., Larochette N., Goodlett D.R., Aebersold R., Siderovski D.P., Penninger J.M., Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature. 397:1999;441-445.
4. Srinivasula S.M., Datta P., Fan X.J., Fernandes-Alnemri T., Huang Z., Alnemri E.S. Molecular determinants of the caspase-promoting activity of Smac/DIABLO and its role in the death receptor pathway. J. Biol. Chem. 275:2000;36152-36157.
5. Martins L.M., Iaccarino I., Tenev T., Gschmeissner S., Totty N.F., Lemoine N.R., Savopoulos J., Gray C.W., Creasy C.L., Dingwall C., Downward J. The serine protease Omi/HtrA2 regulates apoptosis by binding XIAP through a Reaper-like motif. J. Biol. Chem. 277:2001;439-444.
6. van Loo G., van Gurp M., Depuydt B., Srinivasula S.M., Rodriguez I., Alnemri E.S., Gevaert K., Vandekerckhove J., Declercq W., Vandenabeele P. The serine protease Omi/HtrA2 is released from mitochondria during apoptosis. Omi interacts with caspase-inhibitor XIAP and induces enhanced caspase activity. Cell Death Differ. 9:2002;20-26.
7. Parrish J., Li L., Klotz K., Ledwich D., Wang X., Xue D. Mitochondrial endonuclease G is important for apoptosis in C. elegans. Nature. 412:2001;90-94.
8. van Loo G., Schotte P., van Gurp M., Demol H., Hoorelbeke B., Gevaert K., Rodriguez I., Ruiz-Carrillo A., Vandekerckhove J., Declercq W., Beyaert R., Vandenabeele P. Endonuclease G a mitochondrial protein released in apoptosis and involved in caspase-independent DNA degradation . Cell Death Differ. 8:2001;1136-1142.
9. Vayssière J.-L., Petit P.X., Risler Y., Mignotte B. 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. 91:1994;11752-11756.
10. Petit P.X., Lecoeur H., Zorn E., Dauguet C., Mignotte B., Gougeon M.L. Alterations of mitochondrial structure and function are early events of dexamethasone-induced thymocyte apoptosis. J. Cell Biol. 130:1995;157-167.
11. Zamzami N., Marchetti P., Castedo M., Zanin C., Vayssière J.-L., Petit P.X., Kroemer G. Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo. J. Exp. Med. 181:1995;1661-1672.
12. Zamzami N., Marchetti P., Castedo M., Decaudin D., Macho A., Hirsch T., Susin S.A., Petit P.X., Mignotte B., Kroemer G. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med. 182:1995;367-377.
13. Finkel E. The mitochondrion is it central to apoptosis? Science. 292:2001;624-626.
14. Kroemer G., Petit P.X., Zamzami N., Vayssière J.-L., Mignotte B. The biochemistry of apoptosis. FASEB J. 9:1995;1277-1287.
15. Petit P.X., Susin S.A., Zamzami N., Mignotte B., Kroemer G. Mitochondria and programmed cell death back to the future . FEBS Lett. 396:1996;7-14.
16. Green D.R., Reed J.C. Mitochondria and apoptosis. Science. 281:1998;1309-1312.
17. Mignotte B., Vayssiere J.L. Mitochondria and apoptosis. Eur. J. Biochem. 252:1998;1-15.
18. Kroemer G., Reed J.C. Mitochondrial control of cell death. Nat. Med. 6:2000;513-519.
19. Strasser A., O'Connor L., Dixit V.M. Apoptosis signaling. Annu. Rev. Biochem. 69:2000;217-245.
20. I. Marzo, S.A. Susin, P.X. Petit, L. Ravagnan, C. Brenner, N. Zamzami, G. Kroener, Caspases disrupt mitochondrial membrane barrier function, FEBS Lett. 427 (1998) 198-202.
21. Cosulich S.C., Savory P.J., Clarke P.R. Bcl-2 regulates amplification of caspase activation by cytochrome c. Curr Biol. 9:1999;147-150.
22. Zhivotovsky B., Orrenius S., Brustugun O.T., Doskeland S.O. Injected cytochrome c induces apoptosis. [letter] [see comments] Nature. 391:1998;449-450.
23. Kluck R.M., Bossy-Wetzel E., Green D.R., Newmeyer D.D. The release of cytochrome c from mitochondria a primary site for Bcl-2 regulation of apoptosis . Science. 275:1997;1132-1136.
24. Yang J., Liu X., Bhalla K., Kim C.N., Ibrado A.M., Cai J., Peng T.-I., Jones D.P., Wang X. Prevention of apoptosis by Bcl-2 release of cytochrome c from mitochondria blocked . Science. 275:1997;1129-1132.
25. Haraguchi M., Torii S., Matsuzawa S., Xie Z., Kitada S., Krajewski S., Yoshida H., Mak T.W., Reed J.C. Apoptotic protease activating factor 1 (Apaf-1)-independent cell death suppression by Bcl-2. J. Exp. Med. 191:2000;1709-1720.
26. Moriishi K., Huang D.C., Cory S., Adams J.M. Bcl-2 family members do not inhibit apoptosis by binding the caspase activator Apaf-1. Proc. Natl. Acad. Sci. USA. 96:1999;9683-9688.
27. Hausmann G., O'Reilly L.A., van Driel R., Beaumont J.G., Strasser A., Adams J.M., Huang D.C. Pro-apoptotic apoptosis protease-activating factor 1 (Apaf-1) has a cytoplasmic localization distinct from Bcl-2 or Bcl-x(L). J. Cell Biol. 149:2000;623-634.
28. Hu Y., Benedict M.A., Wu D., Inohara N., Nunez G. 1998, Bcl-XL interacts with Apaf-1 and inhibits Apaf-1-dependent caspase-9 activation. Proc. Natl. Acad. Sci. USA. 95:1998;4386-4391.
29. Garland J.M., Rubin C. Cytochrome c induces caspase-dependent apoptosis in intact hematopietic cells and overides apoptosis suppression mediated by Bcl-2, growth factor signalling, MAP-kinase-kinase, and malignant changes. Blood. 92:1998;1235-1246.
30. K.J. Gilmore, H.E. Quinn, M.R. Wilson, Pinocytic loading of cytochrome c into intact cells specifically induces caspase-dependent permeabilization of mitochondria: evidence for a cytochrome c feedback loop, Cell Death Differ. (2001) 631-639.
31. Hofmann F., Ohnimus H., Scheller C., Strupp W., Zimmermann U., Jassoy C. Electric field pulses can induce apoptosis. J. Membr. Biol. 169:1999;103-109.
32. Shimokawa T., Okumura K., Ra C. DNA induces apoptosis in electroporated human promonocytic cell line U937. Biochem. Biophys. Res. Commun. 270:2000;94-99.
33. Bonnafous P., Vernhes M., Teissie J., Gabriel B. The generation of reactive-oxygen species associated with long-lasting pulse-induced electropermeabilisation of mammalian cells is based on a non-destructive alteration of the plasma membrane. Biochim. Biophys. Acta. 1461:1999;123-134.
34. Meldrum R.A., Bowl M., Ong S.B., Richardson S. Optimisation of electroporation for biochemical experiments in live cells. Biochem. Biophys. Res. Commun. 256:1999;235-239.
35. F. Aillet, H. Masuti, C. Elbim, H. Raoul, L. Chêne, M.T. Nugeyre, C. Paya, F. Barré-Sinousi, M.A. Gougerot-Pocidallo, N. Israel, Human immunodeficiency virus induces a dual regulation of Bcl-2, resulting in a persistent infection of CD4+ T- or monocytic cell lines, J. Virol. (1998) 9698-9705.
36. Srivastava R.K., Sollott S.J., Khan L., Hansford R., Lakatta E.G., Longo D.L. Bcl-2 and Bcl-X(L) block thapsigargin-induced nitric oxide generation, c-Jun NH(2)-terminal kinase activity, and apoptosis. Mol. Cell. Biol. 19:1999;5659-5674.
37. Chaloupka R., Petit P.X., Israel N., Sureau F. Overexpression of Bcl-2 does not protect from hypericin photo-induced mitochondrial membrane depolarization, but delay subsequent events in the apoptotic pathway. FEBS Lett. 462:1999;295-301.
38. Gabriel B., Teissie J. Generation of reactive-oxygen species induced by electropermeabilization of Chinese hamster ovary cells and their consequence on cell viability. Eur. J. Biochem. 223:1994;25-33.
39. Rottenberg H., Wu S. Quantitative assay by flow cytometry of the mitochondrial membrane potential in intact cells. Biochim. Biophys. Acta. 1404:1998;393-404.
40. Gendron M.C., Schrantz N., Métivier D., Kroemer G., Maciorowska Z., Sureau F., Koester S., Petit P.X. Oxidation of pyrimidine nucleotides during Fas- and ceramide-induced apoptosis correlation with changes in mitochondria, gluthation depletion, intracellular acidification and caspase-3 activation . Biochem. J. 353:2001;357-367.
41. Nicoletti I., Miglioratti G., Pagliacci F., Grignani F., Riccardi C. A rapid and simple method for measuring thymocyutes apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods. 139:1991;271-279.
42. Hoffschir F., Daya-Grosjean L., Petit P.X., Nocentini S., Dutrillaux B., Sarasin A., Vuillaume M. Low catalase activity in Xeroderma pigmentosum fibroblasts and SV40-transformed human cell lines is directly related to decreased intracellular level of the cofactor. NADPH, Free Radic. Biol. Med. 24:1998;809-816.
43. Meuvis K.N., Boens F.D., De Schryver F.D., Gallay J., Vaincent M. Photophysics of the fluorescent K+ indicator PBFI. Biophys. J. 68:1995;2469-2473.
44. Gabriel B., Teissie J. Control by electrical parameters of short- and long-term cell death resulting from electropermeabilization of Chinese hamster ovary cells. Biochim. Biophys. Acta. 1266:1995;171-178.
45. Brustugun O.T., Fladmark K.E., Doskeland S.O., Orrenius S., Zhivotovsky B. Apoptosis induced by microinjection of cytochrome c is caspase-dependent and is inhibited by Bcl-2 [published erratum appears in Cell Death Differ. 6 (1999) 301]. Cell Death Differ. 5:1998;660-668.
46. Gabriel B., Teissie J. Direct observation in the millisecond time range of fluorescent molecule asymmetrical interaction with the electropermeabilized cell membrane. Biophys. J. 73:1997;2630-2637.
47. Bhuyan A.K., Varshney A., Mathew M.K. Resting membrane potential as a marker of apoptosis studies on Xenopus oocytes microinjected with cytochrome c . Cell Death Differ. 8:2001;63-69.
48. Maccarrone M., Bladergroen M.R., Rosato N., Finazzi Agro A.F. Role of lipid peroxidation in electroporation-induced cell permeability. Biochem. Biophys. Res. Commun. 209:1995;417-425.
49. Liu W., Kato M., Akhand A.A., Hayakawa A., Suzuki H., Miyata T., Kurokawa K., Hotta Y., Ishikawa N., Nakashima I. 4-hydroxynonenal induces a cellular redox status-related activation of the caspase cascade for apoptotic cell death. J. Cell Sci. 113:2000;635-641.
50. G. Kroemer, The proto-oncogene Bcl-2 and its role in regulating apoptosis, Nat. Med. 3, 614-620.
51. Voehringer D.W., Meyn R.E. Redox aspects of Bcl-2 function. Antioxid. Redox. Signal. 2:1997;537-550.
52. Esposti M.D., Hatzinisiriou I., McLennan H., Ralph S. Bcl-2 and mitochondrial oxygen radicals, New approaches with reactive oxygen species-sensitive probes. J. Biol. Chem. 274:1999;29831-29837.
53. Ellerby L.M., Ellerby H.M., Park S.M., Holleran A.L., Murphy A.N., Fiskum G., Kane D.J., Testa M.P., Kayalar C., Bredesen D.E. Shift of the cellular oxidation-reduction potential in neural cells expressing Bcl-2. J. Neurochem. 67:1996;1259-1267.
54. Hockenbery D.M., Oltvai Z.N., Yin X.-M., Milliman C.L., Korsmeyer S.J. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell. 75:1993;241-251.
55. Kane D.J., Sarafian T.A., Anton R., Hahn H., Gralla E.B., Valentine J.S., Örd T., Bredesen D.E. Bcl-2 inhibition of neural death decreased generation of reactive oxygen species . Science. 262:1993;1274-1277.
56. Wiedau-Pazos M., Trudell J.R., Altenbach C., Kane D.J., Hubbell W.L., Bredesen D.E. Expression of bcl-2 inhibits cellular radical generation. Free Radic. Res. 24:1996;205-212.
57. Hampton M.B., Zhivotovsky B., Slater A.F., Burgess D.H., Orrenius S. Importance of the redox state of cytochrome c during caspase activation in cytosolic extracts. Biochem J. 329:1998;95-99.
58. Adrain C., Creagh E.M., Martin S.J. Apoptosis-associated release of Smac/DIABLO from mitochondria requires active caspases and is blocked by Bcl-2. EMBO J. 20:2001;6627-6636.
59. Arnoult D., Parone P., Martinou J.C., Antonsson B., Estaquier J., Ameisen J.C. Mitochondrial release of apoptosis-inducing factor occurs downstream of cytochrome c release in response to several proapoptotic stimuli. J. Cell Biol. 159:2002;923-929.
60. Cheng E.H., Kirsch D.G., Clem R.J., Ravi R., Kastan M.B., Bedi A., Ueno K., Hardwick J.M. Conversion of Bcl-2 to a Bax-like death effector by caspases. Science. 278:1997;1966-1968.
61. Clem R.J., Cheng E.H., Karp C.L., Kirsch D.G., Ueno K., Takahashi A., Kastan M.B., Griffin D.E., Earnshaw W.C., Veliuona M.A., Hardwick J.M. Modulation of cell death by Bcl-XL through caspase interaction. Proc. Natl. Acad. Sci. USA. 95:1998;554-559.
62. Pan G., O'Rourke K., Dixit V.M. Caspase-9, Bcl-XL, and Apaf-1 form a ternary complex. J. Biol. Chem. 273:1998;5841-5845.
63. Conus S., Rosse T., Borner C. Failure of Bcl-2 family members to interact with Apaf-1 in normal and apoptotic cells. Cell Death Differ. 7:2000;947-954.
64. Du C., Fang M., Li Y., Li L., Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell. 102:2000;33-42.
65. Rosse T., Olivier R., Monney L., Rager M., Conus S., Fellay I., Jansen B., Borner C. Bcl-2 prolongs cell survival after Bax-induced release of cytochrome c. Nature. 391:1998;496-499.
66. Ricci J.E., Gottlieb R.A., Green D.R. Caspase-mediated loss of mitochondrial function and generation of reactive oxygen species during apoptosis. J. Cell Biol. 160:2003;65-75.