Bax regulates production of superoxide in both apoptotic and nonapoptotic neurons: Role of caspases

Journal of Neuroscience

Volumn 30, Issue 48, 2010, Pages 16114-16127

  Kirkland, Rebecca A ^a   Saavedra, Geraldine M ^a   Cummings, Brian S ^a   Franklin, James L ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE INHIBITOR; PROTEIN BAX; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; SUPEROXIDE DISMUTASE;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CEREBELLAR GRANULE NEURON; CONTROLLED STUDY; ENZYME ACTIVITY; IMMUNOBLOTTING; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUPERIOR CERVICAL GANGLION;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CASPASE 3; CELLS, CULTURED; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOCHONDRIAL PROTEINS; NEURONS; REACTIVE OXYGEN SPECIES; SUPEROXIDES;

EID: 78649732832     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2862-10.2010     Document Type: Article

References (98)

1. Abramov AY, Scorziello A, Duchen MR (2007) Three distinct mechanisms generate oxygen free radicals in neurons and contribute to cell death during anoxia and reoxygenation. J Neurosci 27:1129-1138.
2. Adrain C, Martin SJ (2001) The mitochondrial apoptosome: a killer unleashed by the cytochrome seas. Trends Biochem Sci 26:390-397.
3. Andreyev AY, Kushnareva YE, Starkov AA (2005) Mitochondrial metabolism of reactive oxygen species. Biochemistry (Mosc) 70:200-214.
4. Barja G (2004) Free radicals and aging. Trends Neurosci 27:595-600.
5. Ben-Ari Z, Pappo O, Cheporko Y, Yasovich N, Offen D, Shainberg A, Leshem D, Sulkes J, Vidne BA, Hochhauser E (2007) Bax ablation protects against hepatic ischemia/reperfusion injury in transgenic mice. Liver Transpl 13:1181-1188.
6. Bouvard V, Zaitchouk T, Vacher M, Duthu A, Canivet M, Choisy-Rossi C, Nieruchalski M, May E (2000) Tissue and cell-specific expression of the p53-target genes: bax, fas, mdm2, and waf1/p21, before and following ionizing irradiation in mice. Oncogene 19:649-660.
7. Cai J, Jones DP (1998) Superoxide in apoptosis: mitochondrial generation triggered by cytochrome c loss. J Biol Chem 273:11401-11404.
8. Cao G, Minami M, Pei W, Yan C, Chen D, O'Horo C, Graham SH, Chen J (2001) Intracellular Bax translocation after transient cerebral ischemia: implications for a role of the mitochondrial apoptotic signaling pathway in ischemic neuronal death. J Cereb Blood Flow Metab 21:321-333.
9. Chen ZX, Pervaiz S (2007) Bcl-2 induces pro-oxidant state by engaging mitochondrial respiration in tumor cells. Cell Death Differ 14:1617-1627.
10. Danial NN, Korsmeyer SJ (2004) Cell death: critical control points. Cell 116:205-219.
11. Deckwerth TL, Johnson EM Jr (1993) Temporal analysis of events associated with programmed cell death (apoptosis) of sympathetic neurons deprived of nerve growth factor. J Cell Biol 123:1207-1222.
12. Deckwerth TL, Elliott JL, Knudson CM, Johnson EM Jr, Snider WD, Korsmeyer SJ (1996) Bax is required for neuronal death after trophic factor deprivation and during development. Neuron 17:401-411.
13. Desagher S, Osen-Sand A, Nichols A, Eskes R, Montessuit S, Lauper S, Maundrell K, Antonsson B, Martinou JC (1999) Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J Cell Biol 144:891-901.
14. Deshmukh M, Johnson EM 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.
15. Deshmukh M, Vasilakos J, Deckwerth TL, Lampe PA, Shivers BD, Johnson EM Jr (1996) Genetic and metabolic status of NGF-deprived sympathetic neurons saved by an inhibitor of ICE-family proteases. J Cell Biol 135:1341-1354.
16. Deshmukh M, Du C, Wang X, Johnson EM Jr (2002) Exogenous Smac induces competence and permits caspase activation in sympathetic neurons. J Neurosci 22:8018-8027.
17. Du C, Fang M, Li Y, Li L, Wang X (2000) Smac, a mitochondrial protein that promotes cytochrome-c dependent caspase activation by eliminating IAP inhibition. Cell 102:33-42.
18. Dugan LL, Creedon DJ, Johnson EM Jr, Holtzman DM (1997) 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.
19. Fiskum G, Craig SW, Decker GL, Lehninger AL (1980) The cytoskeleton of digitonin-treated rat hepatocytes. Proc Natl Acad Sci U S A 77:3430-3434.
20. Fiskum G, Kowaltowksi AJ, Andreyev AY, Kushnareva YE, Starkov AA (2000) Apoptosis-related activities measured with isolated mitochondria and digitonin-permeabilized cells. Methods Enzymol 322:222-234.
21. 2+ influx but not Trk activation. J Neurosci 15:643-664.
22. Goldstein JC, Waterhouse NJ, Juin P, Evan GI, Green DR (2000) The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nat Cell Biol 2:156-162.
23. Green DR (2006) At the gates of death. Cancer Cell 9:328-330.
24. Gdynia G, Grund K, Eckert A, Böck BC, Funke B, Macher-Goeppinger S, Sieber S, Herold-Mende C, Wiestler B, Wiestler OD, Roth W (2007) Basal caspase activity promotes migration and invasiveness in glioblastoma cells. Mol Cancer Res 5:1232-1240.
25. Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine, Ed 4. Oxford: Oxford UP.
26. He L, Wu X, Meylan F, Olson DP, Simone J, Hewgill D, Siegel R, Lipsky PE (2004) Monitoring caspase activity in living cells using fluorescent proteins and flow cytometry. Am J Pathol 164:1901-1913.
27. Hochhauser E, Kivity S, Offen D, Maulik N, Otani H, Barhum Y, Pannet H, Shneyvays V, Shainberg A, Goldshtaub V, Tobar A, Vidne BA (2003) Bax ablation protects against myocardial ischemia-reperfusion injury in transgenic mice. Am J Physiol Circ Physiol 284:H2351-H2359.
28. Hockenbery DM, Oltvai ZN, Yin XM, Milliman CL, Korsmeyer SJ (1993) Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75:241-251.
29. Johnson-Cadwell LI, Jekabsons MB, Wang A, Polster BM, Nicholls DG (2007) "Mild uncoupling" does not decrease mitochondrial superoxide levels in cultured cerebellar granule neurons but decreases spare respiratory capacity and increases toxicity to glutamate and oxidative stress. J Neurochem 101:1619-1631.
30. Karbowski M, Youle RJ (2003) Dynamics of mitochondrial morphology in healthy cells during apoptosis. Cell Death Differ 10:870-880.
31. Karbowski M, Norris KL, Cleland MM, Jeong SY, Youle RJ (2006) Role of Bax and Bak in mitochondrial morphogensis. Nature 443:658-662.
32. Keele BB Jr, McCord JM, Fridovich I (1970) Superoxide dismutase from Escherichia coli B. A new manganese-containing enzyme. J Biol Chem 245:6176-6181.
33. Keeney PM, Xie J, Capaldi RA, Bennett JP Jr (2006) Parkinson's disease brain mitochondrial complex I has oxidatively damaged subunits and is functionally impaired and misassembled. J Neurosci 26:5256-5264.
34. Kirkland RA, Franklin JL (2001) 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.
35. Kirkland RA, Franklin JL (2007a) Bax affects production of reactive oxygen by the mitochondria of nonapoptotic neurons. Exp Neurol 204:458-461.
36. Kirkland RA, Windelborn JA, Kasprzak JM, Franklin JL (2002) A Bax-induced pro-oxidant state is critical for cytochrome c release during programmed neuronal death. J Neurosci 22:6480-6490.
37. Kirkland RA, Saavedra GM, Franklin JL (2007b) Rapid activation of antioxidant defenses by nerve growth factor suppresses reactive oxygen species during neuronal apoptosis: evidence for a role in cytochrome c redistribution. J Neurosci 27:11315-11326.
38. Knudson CM, Tung KS, Tourtellotte WG, Brown GA, Korsmeyer SJ (1995) Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270:96-99.
39. Kober T, König I, Weber M, Kojda G (2003) Diethyldithiocarbamate inhibits the catalytic activity of xanthine oxidase. FEBS Lett 551:99-103.
40. Kokoszka JE, Coskun P, Esposito LA, Wallace DC (2001) Increased mitochondrial oxidative stress in the SOD2 (+/-) mouse results in the age-related decline of mitochondrial function culminating in increased apoptosis. Proc Natl Acad Sci U S A 98:2278-2283.
41. Kowaltowski AJ, Fiskum G (2005) Redox mechanisms of cytoprotection by Bcl-2. Antioxid Redox Signal 7:508-514.
42. Kowaltowski AJ, Vercesi AE, Fiskum G (2000) Bcl-2 prevents mitochondrial permeability transition and cytochrome c release via maintenance of reduced pyridine nucleotides. Cell Death Differ 7:903-910.
43. Krajewska M, Mai JK, Zapata JM, Ashwell KW, Schendel SL, Reed JC, Krajewski S (2002) Dynamics of expression of apoptosis-regulatory proteins Bid, Bcl-2, Bcl-x, Bax, and Bak during development of murine nervous system. Cell Death Differ 9:145-157.
44. Leitch JM, Yick PJ, Culotta VC (2009) The right to choose: multiple pathways for activating copper, zinc superoxide dismutase. J Biol Chem 284:24679-24683.
45. Lesuisse C, Martin LJ (2002) Long-term culture of mouse cortical neurons as a model for neuronal development, aging, and death. J Neurobiol 51:9-23.
46. Li LY, Luo X, Wang X (2001) Endonuclease G is an apoptotic DNAse when released from mitochondria. Nature 412:95-99.
47. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X (1997) Cytochrome c and dATP-dependent formation of Apaf- 1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91:479-489.
48. Li Z, Jo J, Jia J, Lo S, Whitcomb DJ, Jiao S, Cho K, Sheng M (2010) Caspase-3 activation via mitochondria is required for long-term depression and AMPA receptor internalization. Cell 141:859-871.
49. Lin MT, Beal MF (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443:787-795.
50. Liu TH, Beckman JS, Freeman BA, Hogan EL, Hsu CY (1989) Polyethylene glycol-conjugated superoxide dismutase and catalase reduce ischemic brain injury. Am J Physiol 256:H589-H593.
51. Liu Y, Fiskum G, Schubert D (2002) Generation of reactive oxygen species by the mitochondrial electron transport chain. J Neurochem 80:780-787.
52. Lucken-Ardjomande S, Montessuit S, Martinou JC (2008) Contributions to Bax insertion and oligomerization of lipids of the mitochondrial outer membrane. Cell Death Differ 15:929-937.
53. Maklashina E, Ackrell BAC (2004) Is defective electron transport at the hub of aging? Aging Cell 3:21-27.
54. Martin DP, Schmidt RE, DiStefano PS, Lowry OH, Carter JG, Johnson EM Jr (1988) Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J Cell Biol 106:829-844.
55. McCord JM, Fridovich I (1969) Superoxide dismutase an enzymatic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049-6055.
56. McCord JM, Boyle JA, Day ED, Rizzolo LJ, Salin ML (1977) Superoxide and superoxide dismutases (Michelson AM, McCord JM, Fridovich I, eds). London: Academic.
57. Melov S (2004) Modeling mitochondrial function in aging neurons. Trends Neurosci 10:600-606.
58. Melov S, Coskun P, Patel M, Tuinstra R, Cottrell B, Jun AS, Zastawny TH, Dizdaroglu M, Goodman SI, Huang TT, Miziorko H, Epstein CJ, Wallace DC (1999) Mitochondrial disease in superoxide dismutase 2 mutant mice. Proc Natl Acad Sci U S A 96:846-851.
59. Mérino D, Giam M, Hughes PD, Siggs OM, Heger K, O'Reilly LA, Adams JM, Strasser A, Lee EF, Fairlie WD, Bouillet P (2009) The role of BH3-only protein Bim extends beyond inhibiting Bcl-2-like prosurvival proteins. J Cell Biol 186:355-362.
60. Miller RA (2004) "Accelerated aging": a primrose path to insight? Aging Cell 3:47-51.
61. Miller TM, Johnson EM Jr (1996) Metabolic and genetic analysis of apoptosis in potassium/serum-deprived rat cerebellar granule cells. J Neurosci 16:7487-7495.
62. Miller TM, Moulder KL, Knudson CM, Creedon DJ, Deshmukh M, Korsmeyer SJ, Johnson EM Jr (1997) 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.
63. Misra HP (1979) Reaction of copper-zinc superoxide dismutase with diethyldithiocarbamate. J Biol Chem 254:11623-11628.
64. Nhan TQ, Liles WC, Schwartz SM (2006) Physiological functions of caspases beyond cell death. Am J Pathol 169:729-737.
65. Nicholls DG, Budd SL (2000) Mitochondria and neuronal survival. Physiol Rev 80:315-360.
66. Nicholls DG, Ferguson SJ (2002) Bioenergetics 3. London: Academic.
67. Nicholls DG, Ward MW (2000) Mitochondrial membrane potential and cell death: mortality and millivolts. Trends Neurosci 23:166-174.
68. O'Hare MJ, Hou ST, Morris EJ, Cregan SP, Xu Q, Slack RS, Park DS (2000) Induction and modulation of cerebellar granule neuron death by E2F-1. J Biol Chem 275:25358-25364.
69. Pollack M, Phaneuf S, Dirks A, Leeuwenburgh C (2002) The role of apoptosis in the normal aging brain, skeletal muscle, and heart. Ann NY Acad Sci 959:93-107.
70. Polster BM, Robertson CL, Bucci CJ, Suzuki M, Fiskum G (2003) Postnatal brain development and neural cell differentiation modulate mitochondrial Bax and BH3 peptide-induced cytochrome c release. Cell Death Differ 10:365-370.
71. Praticò D, Uryu K, Leight S, Trojanowski JQ, Lee VM (2001) Increased lipid peroxidation precedes amyloid plaque formation in an animal model of Alzheimer amyloidosis. J Neurosci 21:4183-4187.
72. Priault M, Cartron PF, Camougrand N, Antonsson B, Vallette FM, Manon S (2003) Investigation of the role of the c-terminus of Bax and of tc-Bid on Bax interaction with yeast mitochondria. Cell Death Differ 10:1068-1077.
73. Punchard NA, Kelly FJ (1996) Free radicals a practical approach. Oxford: Oxford UP.
74. Putcha GV, Deshmukh M, Johnson EM Jr (2000) Inhibition of apoptotic signaling cascades causes loss of trophic factor dependence during neuronal maturation. J Cell Biol 149:1011-1018.
75. Qian S, Wang W, Yang L, Huang HW (2008) Structure of transmembrane pore induced by Bax-derived peptide: evidence for lipidic pores. Proc Natl Acad Sci U S A 105:17379-17383.
76. Ricci JE, Gottlieb RA, Green DR (2003) Caspase-mediated loss of mitochondrial function and generation of reactive oxygen species during apoptosis. J Cell Biol 160:65-75.
77. Ricci JE, Muñoz-Pinedo C, Fitzgerald P, Bailly-Maitre B, Perkins GA, Yadava N, Scheffler IE, Ellisman MH, Green DR (2004) Disruption of mitochondrial function during apoptosis is mediated by caspase cleavage of the p75 subunit of complex I of the electron transport chain. Cell 117:773-786.
78. Robinson KM, Janes MS, Pehar M, Monette JS, Ross MF, Hagen TM, Murphy MP, Beckman JS (2006) Selective fluorescent imaging of superoxide in vivo using ethidium-based probes. Proc Natl Acad Sci U S A 103: 15038-15043.
79. Ross MF, Kelso GF, Blaikie FH, James AM, Cochemél HM, Filipovska A, Da Ros T, Hurd TR, Smith RAJ, Murphy MP (2005) Lipophilic triphenylphosphonium cations as tools in mitochondrial bioenergetics and free radical biology. Biochemistry (Mosc) 70:222-230. (Pubitemid 40512331)
80. 2 in cultured endothelial cells. Arch Biochem Biophys 302:348-355.
81. Sevilla F, López-Gorgé J, Del Río LA (1982) Characterization of a manganese superoxide dismutase from the higher plant pisum sativum. Plant Physiol 70:1321-1326.
82. Sherer TB, Betarbet R, Testa CM, Seo BB, Richardson JR, Kim JH, Miller GW, Yagi T, Matsuno-Yagi A, Greenamyre JT (2003) Mechanism of toxicity in rotenone models of Parkinson's disease. J Neurosci 23:10756-10764. (Pubitemid 37499681)
83. Shou Y, Li L, Praghakaran K, Borowitz JL, Isom GE (2003) P38 mitogen-activated protein kinase regulates Bax translocation in cyanide-induced apoptosis. Toxicol Sci 75:99-107.
84. Starkov AA, Polster BM, Fiskum G (2002) Regulation of hydrogen peroxide production by brain mitochondria by calcium and Bax. J Neurochem 83:220-228.
85. Steckley D, Karajgikar M, Dale LB, Fuerth B, Swan P, Drummond-Main C, Poulter MO, Ferguson SS, Strasser A, Cregan SP (2007) Puma is a dominant regulator of oxidative stress induced Bax activation and neuronal apoptosis. J Neurosci 27:12989-12999.
86. Su JH, Deng G, Cotman CW (1997) Bax protein expression is increased in Alzheimer's brain: correlation with DNA damage, Bcl-2 expression, and brain pathology. J Neuropath Exp Neurol 56:86-93.
87. Sun W, Winseck A, Vinsant S, Park OH, Kim H, Oppenheim RW (2004) Programmed cell death of adult-generated hippocampal neurons is mediated by the proapoptotic gene bax. J Neurosci 24:11205-11213.
88. Suzuki Y, Imai Y, Nakayama H, Takahashi K, Takio K, Takahashi R (2001) A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death. Mol Cell 8:613-621.
89. Tan S, Sagara Y, Liu Y, Maher P, Schubert D (1998) The regulation of reactive oxygen species production during programmed cell death. J Cell Biol 141:1423-1432.
90. Turrens JF (1997) Superoxide production by the mitochondrial respiratory chain. Bioscience Rep 17:3-8.
91. Valentijn AJ, Upton JP, Bates N, Gilmore AP (2008) Bax targeting to mitochondria occurs via both tail anchor-dependent and -independent mechanisms. Cell Death Differ 15:1243-1254.
92. Vaughn AE, Deshmukh M (2007) Essential postmitochondrial function of p53 uncovered in DNA damage-induced apoptosis in neurons. Cell Death Differ 14:973-981.
93. Vekrellis K, McCarthy MJ, Watson A, Whitfield J., Rubin LL, Ham J (1997) Bax promotes neuronal cell death and is downregulated during the development of the nervous system. Development 124: 1239-1249.
94. Vila M, Jackson-Lewis V, Vukosavic S, Djaldetti R, Liberatore G, Offen D, Korsmeyer SJ, Przedborski S (2001) Bax ablation prevents dopaminergic neurodegeneration in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson's disease. Proc Natl Acad Sci U S A 98:2837-2842.
95. Wright KM, Vaughn AE, Deshmukh M (2007) Apoptosome dependent caspase-3 activation pathway is nonredundant and necessary for apoptosis in sympathetic neurons. Cell Death Differ 14:625-633.
96. Yousefi S, Conus S, Símon HU (2003) Cross-talk between death and survival pathways. Cell Death Differ 10:861-863.
97. Zhao H, Kalivendi S, Zhang H, Joseph J, Nithipatikom K, Vásquez-Vivar J, Kalyanaraman B (2003) Superoxide reacts with hydroethidine but forms a fluorescent product that is distinctly different from ethidium: potential implications in intracellular fluorescence detection of superoxide. Free Radic Biol Med 34:1359-1368.
98. Zhao H, Joseph J, Fales HM, Sokoloski EA, Levine RL, Vasquez-Vivar J, Kalyanaraman B (2005) Detection and characterization of the product of hydroethidine and intracellular superoxide by HPLC and limitations of fluorescence. Proc Natl Acad Sci U S A 102:5727-5732.