Bax, Reactive Oxygen, and Cytochrome c Release in Neuronal Apoptosis

Antioxidants and Redox Signaling

Volumn 5, Issue 5, 2003, Pages 589-596

  Kirkland, Rebecca A ^a   Franklin, James L ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C; NERVE GROWTH FACTOR; NEUROTROPHIC FACTOR; PROTEIN BAX; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; EMBRYO DEVELOPMENT; GENE DOSAGE; GRANULE CELL; HUMAN; MITOCHONDRIAL MEMBRANE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REVIEW; SYMPATHETIC NERVE CELL;

EID: 0142139353     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/152308603770310257     Document Type: Review

References (71)

1. Adrian C and Martin SJ. The mitochondrial apoptosome: a killer unleashed by the cytochrome seas. Trends Biochem Sci 26: 390-397, 2001.
2. Basaňez G, Sharpe JC, Galanis J, Brandt TB, Hardwick JM, and Zimmerberg J. Bax-type apoptotic proteins porate pure lipid bilayers through a mechanism sensitive to intrinsic monolayer curvature. J Biol Chem 52: 49360-49365, 2000.
3. Bogoyevitch MA, Ketterman AJ, and Sugden PH. Cellular stresses differentially activate c-Jun N-terminal protein kinases and extracellular signal-regulated protein kinases in cultured ventricular myocytes. J Biol Chem 270: 29710-29717, 1995.
4. Cai J and Jones DP. Superoxide in apoptosis: mitochondrial generation triggered by cytochrome c loss. J Biol Chem 273: 11401-11404, 1998.
5. Chen J, Nagayama T, Jin K, Stetler RA, Zhu RL, Graham SH, and Simon RP. Induction of caspase-3-like protease may mediate delayed neuronal death in the hippocampus after transient cerebral ischemia. J Neurosci 18: 4914-4928, 1998.
6. L through caspase interaction. Proc Natl Acad Sci U S A 95: 554-559, 1998.
7. Costantini P, Bruey JM, Castedo M, Metivier D, Loeffler M, Susin SA, Ravagnan L, Zamzami N, Garrido C, and Kroemer G. Pre-processed caspase-9 contained in mitochondria participates in apoptosis. Cell Death Differ 9: 82-88, 2002.
8. Deckwerth TL and Johnson EM Jr. Temporal analysis of events associated with programmed cell death (apoptosis) of sympathetic neurons deprived of nerve growth factor. J Cell Biol 123: 1207-1222, 1993.
9. Deckwerth TL, Elliot JL, Knudson CM, Johnson EM Jr, Snider WD, and Korsmeyer SJ. BAX is required for neuronal death after trophic factor deprivation and during development. Neuron 17: 401-411, 1996.
10. Deckwerth TL, Easton RM, Knudson CM, Korsmeyer SJ, and Johnson EM Jr. Placement of the BCL2 family member BAX in the death pathway of sympathetic neurons activated by trophic factor deprivation. Exp Neurol 152: 150-162, 1998.
11. Dérijard B, Hibi M, Wu I, Barrett T, Su B, Deng T, Karin M, and Davis RJ. Jnk1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 76: 1025-1037, 1994.
12. Deshmukh M and Johnson EM Jr. Evidence of a novel event during neuronal death: development of competence-to-die in response to cytoplasmic cytochrome c. Neuron 21: 695-705, 1998.
13. Deshmukh M, Vasilakos J, Deckwerth TL, Lampe PA, Shivers BD, and Johnson EM Jr. Genetic and metabolic status of NGF-deprived sympathetic neurons saved by an inhibitor of ICE-family proteases. J Cell Biol 135: 1341-1354, 1996.
14. Du C, Hu R, Csernansky CA, Hsu CY, and Choi DW. Very delayed infarction after mild focal cerebral ischemia: a role for apoptosis? J Cereb Blood Flow Metab 16: 195-201, 1996.
15. Du C, Fang M, Li Y, Li L, and Wang X. Smac, a mitochondrial protein that promotes cytochrome-c dependent caspase activation by eliminating IAP inhibition. Cell 102: 33-42, 2000.
16. Dugan LL, Creedon DJ, Johnson EM Jr, and Holtzman DM. Rapid suppression of free radical formation by nerve growth factor involves the mitogen-activated protein kinase pathway. Proc Natl Acad Sci U S A 94: 4086-4091, 1997.
17. Ellerby LM, Ellerby HM, Park SM, Holleran AL, Murphy AN, Fiskum G, Kane DJ, Testa MP, Kayalar C, and Bredesen DE. Shift of the cellular oxidation-reduction potential in neural cells expressing Bcl-2. J Neurochem 67: 1259-1267, 1996.
18. Esposti MD and McLennan H. Mitochondria and cells produce reactive oxygen species in virtual anaerobosis: relevance to ceramide-induced apoptosis. FEBS Lett 430: 338-342, 1998.
19. Estus S, Zaks WJ, Freeman RS, Gruda M, Bravo R, and Johnson EM Jr. Altered gene expression in neurons during programmed cell death: identification of c-jun as necessary for neuronal apoptosis. J Cell Biol 127: 1717-1727, 1994.
20. Ferrari G, Yan CYI, and Greene LA. N-Acetylcysteine (D-and L-stereoisomers) prevents apoptotic death of neuronal cells. J Neurosci 15: 2857-2866, 1995.
21. Greenlund LJS, Deckwerth TL, and Johnson EM Jr. Superoxide dismutase delays neuronal apoptosis: a role for reactive oxygen species in programmed neuronal death. Neuron 14: 303-315, 1995.
22. Halestrap AP, Woodfield K, and Connern CP. 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, 1997.
23. Halliwell B and Gutteridge JMC. Free Radicals in Biology and Medicine. New York: Oxford University Press, 1999.
24. Ham J, Babij C, Whitfield J, Pfarr CM, Lallemand D, Yaniv M, and Rubin LL. A c-Jun dominant negative mutant protects sympathetic neurons against programmed cell death. Neuron 14: 927-939, 1995.
25. Ham J, Eilers A, Whitfield J, Neame SJ, and Shah B. c-Jun and the transcriptional control of neuronal apoptosis. Biochem Pharmacol 60: 1015-1021, 2000.
26. Harris CA and Johnson EM Jr. BH3-only Bcl-2 family members are coordinately regulated by the JNK pathway and require Bax to induce apoptosis in neurons. J Biol Chem 41: 37754-37760, 2001.
27. Harris CA, Deshmukh M, Tsui-Pierchala B, Maroney AC, and Johnson EM Jr. Inhibition of the c-Jun N-terminal kinase signaling pathway by the mixed lineage kinase inhibitor CEP-1347 (KT7515) preserves metabolism and growth of trophic factor-deprived neurons. J Neurosci 22: 103-113, 2002.
28. Hockenbery DM, Oltvai ZN, Yin X, Milliman CL, and Korsmeyer SJ. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75: 241-251, 1993.
29. Imaizumi K, Tsuda M, Imai Y, Wanaka A, Takagi T, and Tohyama M. Molecular cloning of a novel polypeptide, DP5, induced during programmed neuronal death. J Biol Chem 272: 18842-18848, 1997.
30. Jacobson J and Duchen MR. What nourishes me, destroys me: towards a new mitochondrial biology. Cell Death Differ 8: 963-966, 2001.
31. Jacobson MD and Raff MC. Programmed cell death and Bcl-2 protection in very low oxygen. Nature 374: 814-816, 1995.
32. Kane DJ, Sarafian TA, Anton R, Hahn H, Gralla EB, Valentine JS, Ord T, and Bredesen DE. Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. Science 262: 1274-1277, 1993.
33. Kerr JFR, Wyllie AH, and Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26: 239-257, 1972.
34. Kirkland RA and Franklin JL. Evidence for redox regulation of cytochrome c release during programmed neuronal death: antioxidant effects of protein synthesis and caspase inhibition. J Neurosci 21: 1949-1963, 2001.
35. Kirkland RA, Windelbom JA, Kasprzak JM, and Franklin JL. A Bax induced pro-oxidant state is critical for cytochrome c release in programmed neuronal death. J Neurosci 22: 6480-6490, 2002.
36. Kluck RM, Bossy-Wetzel E, Green DR, and Newmeyer DD. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275: 1132-1136, 1997.
37. Krebs JF, Armstrong RC, Srinivasan A, Aja T, Wong AM, Aboy A, Sayers R, Pham B, Vu T, Hoang K, Karanewsky DS, Leist C, Schmitz A, Wu JC, Tomaselli KJ, and Fritz LC. Activation of membrane-associated procaspase 3 is regulated by Bcl-2. J Cell Biol 144: 915-926, 1999.
38. Kroemer G. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat Med 3: 614-620, 1997.
39. Kuwana T, Mackey MR, Perkins G, Ellisman MH, Latterich M, Schneiter R, Green DR, and Newmeyer DD. Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111: 331-342, 2002.
40. Li LY, Luo X, and Wang X. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 412: 95-99, 2001.
41. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, and Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479-489, 1997.
42. Liu X, Kim CN, Yang J, Jemmerson R, and Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86: 147-157, 1996.
43. Madesh M and Hajnóczky G. VDAC-dependent permeabilization of the outer mitochondrial membrane by superoxide induces rapid and massive cytochrome c release. J Cell Biol 155: 1003-1015, 2001.
44. Martin DP, Schmidt RE, DiStefano PS, Lowry OH, Carter JG, and Johnson EM Jr. Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J Cell Biol 106: 829-844, 1988.
45. Martinou JC and Green DR. Breaking the mitochondrial barrier. Nat Rev Mol Cell Biol 2: 63-67, 2001.
46. Miller TM and Johnson EM Jr. Metabolic and genetic analysis of apoptosis in potassium/serum-deprived rat cerebellar granule cells. J Neurosci 16: 7487-7495, 1996.
47. Miller TM, Moulder KL, Knudson CM, Creedon DJ, Deshmukh M, Korsmeyer SJ, and Johnson EM Jr. Bax deletion further orders the cell death pathway in cerebellar granule cells and suggests a caspase-independent pathway in cell death. J Cell Biol 139: 205-217, 1997.
48. Nakai M, Takeda A, Cleary ML, and Endo T. The Bcl-2 protein is inserted into the outer membrane but not into the inner membrane of rat liver mitochondria in vitro. Biochem Biophys Res Commun 196:233-239, 1993.
49. Neame SJ, Rubin LL, and Philpott KL. Blocking cytochrome c activity within intact neurons inhibits apoptosis. J Cell Biol 142: 1583-1593, 1998.
50. Newmeyer DD and Ferguson-Miller S. Mitochondria: releasing power of life and unleashing the machineries of death. Cell 112: 481-490, 2003.
51. Oppenheim RW. Cell death during development of the nervous system. Annu Rev Neurosci 14: 453-501, 1991.
52. Pavlov EV, Priault M, Pietkiewicz D, Cheng EHY, Antonsson B, Manon S, Korsmeyer SJ, Mannella CA, and Kinnally KW. A novel, high conductance channel of mitochondria linked to apoptosis in mammalian cells and Bax expression in yeast. J Cell Biol 155: 725-731, 2001.
53. Putcha GV, Deshmukh M, and Johnson EM Jr. Bax translocation is a critical event in neuronal apoptosis: regulation by neuroprotectants, Bcl-2, and caspases. J Neurosci 19: 7476-7485, 1999.
54. Putcha GV, Moulder KL, Golden JP, Bouillet P, Adams JA, Strasser A, and Johnson EM Jr. Induction of BIM, a proapoptotic BH3-only Bcl-2 family member, is critical for neuronal apoptosis. Neuron 29: 615-628, 2001.
55. Ricci J, Gottlieb RA, and Green DR. Caspase-mediated loss of mitochondrial function and generation of reactive oxygen species during apoptosis. J Cell Biol 160: 65-73, 2003.
56. Rossé T, Olivier R, Monney L, Rager M, Conus S, Fellay I, Jansen B, and Bomer C. Bcl-2 prolongs cell survival after Bax-induced release of cytochrome c. Nature 391: 496-499, 1998.
57. Saito M, Korsmeyer SJ, and Schlesinger PH. BAX-dependent transport of cytochrome c reconstituted in pure liposomes. Nat Cell Biol 2: 553-555, 2000.
58. Sarafian TA and Bredesen DE. Is apoptosis mediated by reactive oxygen species? Free Radic Res 21: 1-8, 1994.
59. Schlesinger PH, Gross A, Yin X, Yamamoto K, Saito M, Waksman G, and Korsmeyer SJ. Comparison of the ion channel characteristics of proapoptotic Bax and antiapoptotic BCL-2. Proc Natl Acad Sci U S A 94: 11357-11362, 1997.
60. Schulz JB, Weller M, and Klockgether T. Potassium deprivation-induced apoptosis of cerebellar granule neurons: a sequential requirement for new mRNA and protein synthesis, ICE-like protease activity, and reactive oxygen species. J Neurosci 15: 4696-4706, 1996.
61. Shimizu S, Eguchi Y, Kosaka H, Kamiike W, Matsuda H, and Tsujimoto Y. Prevention of hypoxia-induced cell death by Bcl-2 and Bcl-xL. Nature 374: 811-813, 1995.
62. Sugawara T, Noshita N, Lewén A, Gasche Y, Ferrand-Drake M, Fujimura M, Morita-Fujimura Y, and Chan PH. Overexpression of copper/zinc superoxide dismutase in transgenic rats protects vulnerable neurons against ischemic damage by blocking the mitochondrial pathway of caspase activation. J Neurosci 22: 209-217, 2002.
63. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, and Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397: 441-446, 1999.
64. Tan S, Sagara Y, Liu Y, Maher P, and Schubert D. The regulation of reactive oxygen species production during programmed cell death. J Cell Biol 141: 1423-1432, 1998.
65. Tsujimoto Y and Shimizu S. VDAC regulation by the Bcl-2 family of proteins. Cell Death Differ 7: 1174-1181, 2000.
66. Turrens JF. Superoxide production by the mitochondrial respiratory chain. Biosci Rep 17: 3-8, 1997.
67. White FA, Keller-Peck CR, Knudson CM, Korsmeyer SJ, and Snider WD. Widespread elimination of naturally occurring neuronal death in Bax-deficient mice. J Neurosci 18: 1428-1439, 1998.
68. Wigdal SS, Kirkland RA, Franklin JL, and Haak-Frendscho M. Cytochrome c release precedes mitochondrial membrane potential loss in cerebellar granule neuron apoptosis: lack of mitochondrial swelling. J Neurochem 22: 1029-1038, 2002.
69. Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG, and Youle RJ. Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol 139: 1281-1292, 1997.
70. Yuan J and Yanker BA. Apoptosis in the nervous system. Nature 407: 802-809, 2001.
71. Zou H, Henzel WJ, Liu X, Lutschg A, and Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90: 405-413, 1997.