The pro-apoptotic proteins, Bid and Bax, cause a limited permeabilization of the mitochondrial outer membrane that is enhanced by cytosol

Journal of Cell Biology

Volumn 147, Issue 4, 1999, Pages 809-822

  Kluck, Ruth M ^a   Degli Esposti, Mauro ^e,f   Perkins, Guy ^b   Renken, Christian ^c   Kuwana, Tomomi ^a   Bossy Wetzel, Ella ^a   Goldberg, Martin ^d   Allen, Terry ^d   Barber, Michael J ^e   Green, Douglas R ^a   Newmeyer, Donald D ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SAN DIEGO STATE UNIVERSITY   (United States)

^d CHRISTIE HOSPITAL   (United Kingdom)

^e UNIVERSITY OF SOUTH FLORIDA   (United States)

^f MONASH UNIVERSITY   (Australia)

Author keywords

Apoptosis; Bax; Bid; Cytochrome c; Mitochondrial outer membrane

Indexed keywords

ADENOSINE TRIPHOSPHATE; CASPASE; CYTOCHROME C;

APOPTOSIS; ARTICLE; ENZYME ACTIVATION; ENZYME ACTIVITY; HYPOTHESIS; KNOCKOUT MOUSE; MEMBRANE PERMEABILITY; MITOCHONDRION; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN ANALYSIS; XENOPUS;

ADENYLATE KINASE; ALAMETHICIN; ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; CARRIER PROTEINS; CELL-FREE SYSTEM; CYTOCHROME C GROUP; CYTOSOL; ELECTRON TRANSPORT COMPLEX III; ELECTRON TRANSPORT COMPLEX IV; INTRACELLULAR MEMBRANES; KINETICS; MALE; MICROSCOPY, ELECTRON; MICROSCOPY, ELECTRON, SCANNING; MITOCHONDRIA, LIVER; OOCYTES; PEPTIDE HYDROLASES; PERMEABILITY; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; XENOPUS LAEVIS;

EID: 0033571045     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.147.4.809     Document Type: Article

References (88)

1. Allen, T.D., and M.W. Goldberg. 1993. High-resolution SEM in cell biology. Trends. Cell Biol. 3:205-208.
2. Allen, T.D., G.R. Bennion, S.A. Rutherford, S. Reipert, A. Ramalho, E. Kiseleva, and M.W. Goldberg. 1996. Accessing nuclear structure for field emission, in lens, scanning electron microscopy (FEISEM). Scanning Microsc. Suppl. 10:149-163.
3. Antonsson, B., F. Conti, A. Ciavatta, S. Montessuit, S. Lewis, I. Martinou, L. Bernasconi, A. Bernard, J.J. Mermod, G. Mazzei, et al. 1997. Inhibition of Bax channel-forming activity by Bcl-2. Science. 277:370-372.
4. Barber, M.J., and P.J. Neame. 1990. A conserved cysteine in molybdenum oxotransferases. J. Biol. Chem. 265:20912-20915.
5. Basanez, G., A. Nechushtan, O. Drozhinin, A. Chanturiya, E. Choe, S. Tutt, K.A. Wood, Y. Hsu, J. Zimmerberg, and R.J. Youle. 1999. Bax, but not Bcl-xL, decreases the lifetime of planar phospholipid bilayer membranes at subnanomolar concentrations. Proc. Natl. Acad. Sci. USA. 96:5492-5497.
6. Beamer, L.J., S.F. Carroll, and D. Eisenberg. 1998. The BPI/LBP family of proteins: a structural analysis of conserved regions. Protein Sci. 7:906-914.
7. Bechinger, B. 1997. Structure and functions of channel-forming peptides: magainins, cecropins, melittin and alamethicin. J. Membr. Biol. 156:197-211.
8. Bernardi, P. 1996. The permeability transition pore. Control points of a cyclosporin A-sensitive mitochondrial channel involved in cell death. Biochim. Biophys. Acta. 1275:5-9.
9. Blackstone, N.W., and D.R. Green. 1999. The evolution of a mechanism of cell suicide. Bioessays. 21:84-88.
10. Bossy-Wetzel, E., D.D. Newmeyer, and D.R. Green. 1998. Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO (Eur. Mol. Biol. Organ.) J. 17:37-49.
11. Brown, J.R., and W.F. Doolittle. 1997. Archaea and the prokaryote-to-eukaryote transition. Microbiol. Mol. Biol. Rev. 61:456-502.
12. Cecconi, F., G. Alvarez-Bolado, B.I. Meyer, K.A. Roth, and P. Gruss. 1998. Apaf1 (CED-4 homolog) regulates programmed cell death in mammalian development. Cell. 94:727-737.
13. Chou, J.J., H. Li, G.S. Salvesen, J. Yuan, and G. Wagner. 1999. Solution structure of BID, an intracellular amplifier of apoptotic signaling. Cell. 96:615-624.
14. Degli Esposti, M., G. Lenaz, G. Izzo, and S. Papa. 1982. Kinetics and sidedness of ubiquinol-cytochrome c reductase in beef-heart mitochondria. FEBS Lett. 146:101-105.
15. Desagher, S., A. Osen-Sand, A. Nichols, R. Eskes, S. Montessuit, S. Lauper, K. Maundrell, B. Antonsson, and J.C. Martinou. 1999. Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J. Cell Biol. 144:891-901.
16. Deshmukh, M., and E.M. Johnson, Jr. 1998. Evidence of a novel event during neuronal death: development of competence-to-die in response to cytoplasmic cytochrome c. Neuron. 21:695-705.
17. Ellerby, H.M., S.J. Martin, L.M. Ellerby, S.S. Naiem, S. Rabizadeh, G.S. Salvesen, C.A. Casiano, N.R. Cashman, D.R. Green, and D.E. Bredesen. 1997. Establishment of a cell-free system of neuronal apoptosis: comparison of premitochondrial, mitochondrial, and postmitochondrial phases. J. Neurosci. 17:6165-6178.
18. 2+ ions. J. Cell Biol. 143:217-224.
19. Farschon, D.M., C. Couture, T. Mustelin, and D.D. Newmeyer. 1997. Temporal phases in apoptosis defined by the actions of Src Homology 2 domains, ceramide, Bcl-2, interleukin-1β converting enzyme family proteases, and a dense membrane fraction. J. Cell Biol. 137:1117-1125.
20. Finucane, D.M., E. Bossy-Wetzel, N.J. Waterhouse, T.G. Cotter, and D.R. Green. 1999. Bax-induced caspase activation and apoptosis via cytochrome c release from mitochondria is inhibitable by Bcl-xL. J. Biol. Chem. 274:2225-2233.
21. Gaikwad, A.S., T. Ramasarma, and C.K. Ramakrishna Kurup. 1991. Brown adipose tissue mitochondria are cytochrome c-subsaturated. Mol. Cell. Biochem. 105:119-125.
22. Green, D.R., and J.C. Reed. 1998. Mitochondria and Apoptosis. Science. 281: 1309-1312.
23. Hackenbrock, C.R. 1968. Ultrastructural bases for metabolically linked mechanical activity in mitochondria. II. Electron transport-linked ultrastructural transformations in mitochondria. J. Cell Biol. 37:345-369.
24. Hakem, R., A. Hakem, G.S. Duncan, J.T. Henderson, M. Woo, M.S. Soengas, A. Elia, J.L. de la Pompa, D. Kagi, W. Khoo, et al. 1998. Differential requirement for caspase 9 in apoptotic pathways in vivo. Cell. 94:339-352.
25. Heiskanen, K.M., M.B. Bhat, H.W. Wang, J. Ma, and A.L. Nieminen. 1999. Mitochondrial depolarization accompanies cytochrome c release during apoptosis in PC6 cells. J. Biol. Chem. 274:5654-5658.
26. Hensey, C., and J. Gautier. 1997. A developmental timer that regulates apoptosis at the onset of gastrulation. Mech. Dev. 69:183-195.
27. Huang, D.C., L.A. O'Reilly, A. Strasser, and S. Cory. 1997. The anti-apoptosis function of Bcl-2 can be genetically separated from its inhibitory effect on cell cycle entry. EMBO (Eur. Mol. Biol. Organ.) J. 16:4628-4638.
28. Innis, M.A., T.R. Beers, and S.P. Craig. 1976. Mitochondrial regulation in sea urchins. I. Mitochondrial ultrastructure transformations and changes in the ADP:ATP ratio at fertilization. Exp Cell Res. 98:47-56.
29. Juin, P., A.O. Hueber, T. Littlewood, and G. Evan. 1999. c-myc-induced sensitization to apoptosis is mediated through cytochrome c release. Genes Dev. 13:1367-1381.
30. Jurgensmeier, J.M., Z. Xie, Q. Deveraux, L. Ellerby, D. Bredesen, and J.C. Reed. 1998. Bax directly induces release of cytochrome c from isolated mitochondria. Proc. Natl. Acad. Sci. USA. 95:4997-5002.
31. Kluck, R.M., E. Bossy-Wetzel, D.R. Green, and D.D. Newmeyer. 1997a. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science. 275:1132-1136.
32. Kluck, R.M., S.J. Martin, B.M. Hoffman, J.S. Zhou, D.R. Green, and D.D. Newmeyer. 1997b. Cytochrome c activation of CPP32-like proteolysis plays a critical role in a Xenopus cell-free apoptosis system. EMBO (Eur. Mol. Biol. Organ.) J. 16:4639-4649.
33. Knight, V.A., P.M. Wiggins, J.D. Harvey, and J.A. O'Brien. 1981. The relationship between the size of mitochondria and the intensity of light that they scatter in different energetic states. Biochim. Biophys. Acta. 637:146-151.
34. Kobayashi, I. 1998. Selfishness and death: raison d'être of restriction, recombination and mitochondria. Trends Genet. 14:368-374.
35. Kohler, C., A. Gahm, T. Noma, A. Nakazawa, S. Orrenius, and B. Zhivotovsky. 1999. Release of adenylate kinase 2 from the mitochondrial intermembrane space during apoptosis. FEBS Lett. 447:10-12.
36. Kuida, K., T.F. Haydar, C.Y. Kuan, Y. Gu, C. Taya, H. Karasuyama, M.S. Su, P. Rakic, and R.A. Flavell. 1998. Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell. 94:325-337.
37. Kuwana, T., J.J. Smith, M. Muzio, V. Dixit, D.D. Newmeyer, and S. Kornbluth. 1998. Apoptosis induction by caspase-8 is amplified through the mitochondrial release of cytochrome c. J. Biol. Chem. 273:16589-16594.
38. 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.
39. Li, F., A. Srinivasan, Y. Wang, R.C. Armstrong, K.J. Tomaselli, and L.C. Fritz. 1997a. Cell-specific induction of apoptosis by microinjection of cytochrome c. Bcl-xL has activity independent of cytochrome c release. J. Biol. Chem. 272:30299-30305.
40. Li, P., D. Nijhawan, I. Budihardjo, S.M. Srinivasula, M. Ahmad, E.S. Alnemri, and X. Wang. 1997b. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 91: 479-489.
41. Li, H., H. Zhu, C.J. Xu, and J. Yuan. 1998. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 94:491-501.
42. Luo, X., I. Budihardjo, H. Zou, C. Slaughter, and X. Wang. 1998. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell. 94:481-490.
43. Mancini, M., B.O. Anderson, E. Caldwell, M. Sedghinasab, P.B. Paty, and D.M. Hockenbery. 1997. Mitochondrial proliferation and paradoxical membrane depolarization during terminal differentiation and apoptosis in a human colon carcinoma cell line. J. Cell Biol. 138:449-469.
44. Mancini, M., D.W. Nicholson, S. Roy, N.A. Thornberry, E.P. Peterson, L.A. Casciola-Rosen, and A. Rosen. 1998. The caspase-3 precursor has a cytosolic and mitochondrial distribution: implications for apoptotic signaling. J. Cell Biol. 140:1485-1495.
45. Mannella, C.A. 1992. The 'ins' and 'outs' of mitochondrial membrane channels. Trends Biochem. Sci. 17:315-320.
46. Margoliash, E., and E.R. Bosshard. 1983. Guided by electrostatics, a textbook protein comes of age. Trends Biochem. Sci. 8:316-320.
47. Martin, W., and M. Muller. 1998. The hydrogen hypothesis for the first eukaryote. Nature. 392:37-41.
48. Martinou, I., S. Desagher, R. Eskes, B. Antonsson, E. André, S. Fakan, and J.-C. Martinou. 1999. The release of cytochrome c from mitochondria during apoptosis of NGF-deprived sympathetic neurons is a reversible event. J. Cell Biol. 144:883-889.
49. Marzo, I., C. Brenner, N. Zamzami, J.M. Jurgensmeier, S.A. Susin, H.L. Vieira, M.C. Prevost, Z. Xie, S. Matsuyama, J.C. Reed, and G. Kroemer. 1998. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science. 281:2027-2031.
50. McDonnell, J.M., D. Fushman, C.L. Milliman, S.J. Korsmeyer, and D. Cowburn. 1999. Solution structure of the proapoptotic molecule BID: a structural basis for apoptotic agonists and antagonists. Cell. 96:625-634.
51. Minn, A.J., P. Velez, S.L. Schendel, H. Liang, S.W. Muchmore, S.W. Fesik, M. Fill, and C.B. Thompson. 1997. Bcl-x(L) forms an ion channel in synthetic lipid membranes. Nature. 385:353-357.
52. Muchmore, S.W., M. Sattler, H. Liang, R.P. Meadows, J.E. Harlan, H.S. Yoon, D. Nettesheim, B.S. Chang, C.B. Thompson, S.-L. Wong, S.-C. Ng, and S.W. Fesik. 1996. X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death. Nature. 381:335-341.
53. Narita, M., S. Shimizu, T. Ito, T. Chittenden, R.J. Lutz, H. Matsuda, and Y. Tsujimoto. 1998. Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. Proc. Natl. Acad. Sci. USA. 95:14681-14686.
54. Neame, S.J., L.L. Rubin, and K.L. Philpott. 1998. Blocking cytochrome c activity within intact neurons inhibits apoptosis. J. Cell Biol. 142:1583-1593.
55. Nechushtan, A., C.L. Smith, Y.T. Hsu, and R.J. Youle. 1999. Conformation of the Bax C-terminus regulates subcellular location and cell death. EMBO (Eur. Mol. Biol. Organ.) J. 18:2330-2341.
56. Newmeyer, D.D. 1998. Analysis of apoptotic events using a cell-free system based on Xenopus laevis eggs. In Weir's Handbook of Experimental Immunology. Vol. III. L.A. Herzenberg, C. Blackwell, and D.M. Weir, editors. Blackwell Scientific. 127.121-127.126.
57. 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. 79:353-364.
58. Nicolay, K., F.D. Laterveer, and W.L. van Heerde. 1994. Effects of amphipathic peptides, including presequences, on the functional integrity of rat liver mitochondrial membranes. J. Bioenerg. Biomembr. 26:327-334.
59. Ord, M.J., and R.A. Smith. 1982. Correlation of mitochondrial form and function in vivo: microinjection of substrate and nucleotides. Cell Tissue Res. 227:129-137.
60. Pastorino, J.G., S.T. Chen, M. Tafani, J.W. Snyder, and J.L. Farber. 1998. The overexpression of Bax produces cell death upon induction of the mitochondrial permeability transition. J. Biol. Chem. 273:7770-7775.
61. Petit, P.X., S.A. Susin, N. Zamzami, B. Mignotte, and G. Kroemer. 1996. Mitochondria and programmed cell death: back to the future. FEBS Lett. 396:7-13.
62. 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. 270:4923-4932.
63. Reed, J.C. 1997. Double identity for proteins of the Bcl-2 family. Nature. 387: 773-776.
64. Rosse, T., R. Olivier, L. Monney, M. Rager, S. Conus, I. Fellay, B. Jansen, and C. Borner. 1998. Bcl-2 prolongs cell survival after Bax-induced release of cytochrome c. Nature. 391:496-499.
65. Samali, A., J. Cai, B. Zhivotovsky, D.P. Jones, and S. Orrenius. 1999. Presence of a pre-apoptotic complex of pro-caspase-3, Hsp60 and Hsp10 in the mitochondrial fraction of Jurkat cells. EMBO (Eur. Mol. Biol. Organ.) J. 18: 2040-2048.
66. Sattler, M., H. Liang, D. Nettesheim, R.P. Meadows, J.E. Harlan, M. Eberstadt, H.S. Yoon, S.B. Shuker, B.S. Chang, A.J. Minn, et al. 1997. Structure of Bcl-xL-Bak peptide complex: recognition between regulators of apoptosis. Science. 275:983-986.
67. Schendel, S.L., Z. Xie, M.O. Montal, S. Matsuyama, M. Montal, and J.C. Reed. 1997. Channel formation by antiapoptotic protein Bcl-2. Proc. Natl. Acad. Sci. USA. 94:5113-5118.
68. Schlesinger, P.H., A. Gross, X.M. Yin, K. Yamamoto, M. Saito, G. Waksman, and S.J. Korsmeyer. 1997. Comparison of the ion channel characteristics of proapoptotic BAX and antiapoptotic BCL-2. Proc. Natl. Acad. Sci. USA. 94: 11357-11362.
69. Schmidt, B., E. Wachter, W. Sebald, and W. Neupert. 1984. Processing peptidase of neurospora mitochondria. Two-step cleavage of imported ATPase subunit 9. Eur. J. Biochem. 144:581-588.
70. Searle, J., T.A. Lawson, P.J. Abbott, B. Harmon, and J.F. Kerr. 1975. An electron-microscope study of the mode of cell death induced by cancer-chemotherapeutic agents in populations of proliferating normal and neoplastic cells. J. Pathol. 116:129-138.
71. Shimizu, S., M. Narita, and Y. Tsujimoto. 1999. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature. 399:483-487.
72. Single, B., M. Leist, and P. Nicotera. 1998. Simultaneous release of adenylate kinase and cytochrome c in cell death. Cell Death Differ. 5:1001-1003.
73. Stenger, S., D.A. Hanson, R. Teitelbaum, P. Dewan, K.R. Niazi, C.J. Froelich, T. Ganz, S. Thoma-Uszynski, A. Melian, C. Bogdan, et al. 1998. An antimicrobial activity of cytolytic T cells mediated by granulysin. Science. 282:121-125.
74. 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.
75. Susin, S.A., H.K. Lorenzo, N. Zamzami, I. Marzo, C. Brenner, N. Larochette, M.C. Prévost, P.M. Alzari, and G. Kroemer. 1999a. Mitochondrial release of Caspase-2 and -9 during the apoptotic process. J. Exp. Med. 189:381-394.
76. Susin, S.A., H.K. Lorenzo, N. Zamzami, I. Marzo, B.E. Snow, G.M. Brothers, J. Mangion, E. Jacotot, P. Costantini, M. Loeffler, N. Larochette, D.R. Goodlett, R. Aebersold, D.P. Siderovski, J.M. Penninger, and G. Kroemer. 1999b. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature. 397:441-446.
77. van Leyen, K., R.M. Duvoisin, H. Engelhardt, and M. Wiedmann. 1998. A function for lipoxygenase in programmed organelle degradation. Nature. 395:392-395.
78. Vander Heiden, M.G., N.S. Chandel, E.K. Williamson, P.T. Schumacker, and C.B. Thompson. 1997. Bcl-xL regulates the membrane potential and volume homeostasis of mitochondria. Cell. 91:627-637.
79. Vander Heiden, M.G., N.S. Chandel, P.T. Schumacker, and C.B. Thompson. 1999. Bcl-xL prevents cell death following growth factor withdrawal by facilitating mitochondrial ATP/ADP exchange. Mol. Cell. 3:159-167.
80. White, S.H., W.C. Wimley, and M.E. Selsted. 1995. Structure, function, and membrane integration of defensins. Curr. Opin. Struct. Biol. 5:521-527.
81. Wikstrom, M., and R. Casey. 1985. The oxidation of exogenous cytochrome c by mitochondria. Resolution of a long-standing controversy. FEBS Lett. 183: 293-298.
82. Wojtczak, L., H. Zaluska, A. Wroniszewska, and A.B. Wojtczak. 1972. Assay for the intactness of the outer membrane in isolated mitochondria. Acta Biochim. Pol. 19:227-234.
83. Wolter, K.G., Y.T. Hsu, C.L. Smith, A. Nechushtan, X.G. Xi, and R.J. Youle. 1997. Movement of Bax from the cytosol to mitochondria during apoptosis. J. Cell Biol. 139:1281-1292.
84. Woolley, G.A., and B.A. Wallace. 1992. Model ion channels: gramicidin and alamethicin. J. Membr. Biol. 129:109-136.
85. Yang, J., X. Liu, K. Bhalla, C.N. Kim, A.M. Ibrado, J. Cai, T.-I. Peng, D.P. Jones, and X. Wang. 1997. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science. 275:1129-1132.
86. Yoshida, H., Y.Y. Kong, R. Yoshida, A.J. Elia, A. Hakem, R. Hakem, J.M. Penninger, and T.W. Mak. 1998. Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell. 94:739-750.
87. Zhivotovsky, B., S. Orrenius, O.T. Brustugun, and S.O. Doskeland. 1998. Injected cytochrome c induces apoptosis. Nature. 391:449-450.
88. Zhuang, J., D. Dinsdale, and G.M. Cohen. 1998. Apoptosis, in human monocytic THP.1 cells, results in the release of cytochrome c from mitochondria prior to their ultracondensation, formation of outer membrane discontinuities and reduction in inner membrane potential. Cell Death Differ. 5:953-962.