Simultaneous age-related depolarization of mitochondrial membrane potential and increased mitochondrial reactive oxygen species production correlate with age-related glutamate excitotoxicity in rat hippocampal neurons

Journal of Neuroscience Research

Volumn 85, Issue 5, 2007, Pages 1018-1032

  Parihar, Mordhwaj S ^a,b   Brewer, Gregory J ^a  

^a SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Axon dendrite; Confocal microscopy; Excitotoxicity; Mitochondrial energetics; Neurodegenerative diseases; Oxidative injury

Indexed keywords

REACTIVE OXYGEN METABOLITE;

AGING; ANIMAL EXPERIMENT; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; DEPOLARIZATION; ENERGY RESOURCE; EXCITOTOXICITY; HIPPOCAMPUS; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; STRESS;

AGING; ANIMALS; CELL AGING; CELLS, CULTURED; GLUTAMIC ACID; HIPPOCAMPUS; MEMBRANE POTENTIAL, MITOCHONDRIAL; NERVE DEGENERATION; NEURODEGENERATIVE DISEASES; NEURONS; NEUROTOXINS; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; RATS; RATS, INBRED F344; REACTIVE OXYGEN SPECIES;

EID: 34147219139     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21218     Document Type: Article

References (97)

1. Aarts M, Iihara K, Wei WL, Xiong ZG, Arundine M, Cerwinski W, MacDonald JF, Tymianski M. 2003. A key role for TRPM7 channels in anoxic neuronal death. Cell 115:863-877.
2. Anderson MF, Sims NR. 2002. The effects of focal ischemia and reperfusion on the glutathione content of mitochondria from rat brain subregions. J Neurochem 81:541-549.
3. Aw TY. 2003. Cellular redox: a modulator of intestinal epithelial cell proliferation. News Physiol Sci 18:201-204.
4. Barja G. 1998. Mitochondrial free radical production and aging in mammals and birds. Ann N Y Acad Sci 854:224-238.
5. Barrientos A, Moraes CT. 1999. Titrating the effects of mitochondrial complex I impairment in the cell physiology. J Biol Chem 274:16188-16197.
6. Batandier C, Leverve X, Fontaine E. 2004. Opening of the mitochondrial permeability transition pore induces reactive oxygen species production at the level of the respiratory chain complex I. J Biol Chem 279:17197-17204.
7. Beal MF. 1998. Mitochondrial dysfunction in neurodegenerative diseases. Biochim Biophys Acta 1366:211-223.
8. Beckman KB, Ames BN. 1998. Mitochondrial aging: open questions. Ann N Y Acad Sci 854:118-127.
9. Belousov VV, Fradkov AF, Lukyanov KA, Staroverov DB, Shakhbazov KS, Terskikh AV, Lukyanov S. 2006. Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat Methods 3:281-286.
10. Brewer GJ. 1997. Isolation and culture of adult rat hippocampal neurons. J Neurosci Methods 71:143-155.
11. Brewer GJ. 1998. Age-related toxicity to lactate, glutamate, and beta-amyloid in cultured adult neurons. Neurobiol Aging 19:561-568.
12. Brewer GJ. 1999. Regeneration and proliferation of embryonic and adult rat hippocampal neurons in culture. Exp Neurol 159:237-247.
13. Brewer GJ, Price PJ. 1996. Viable cultured neurons in ambient carbon dioxide and hibernation storage for a month. Neuroreport 7:1509-1512.
14. Brewer GJ, Wallimann TW. 2000. Protective effect of the energy precursor creatine against toxicity of glutamate and beta-amyloid in rat hippocampal neurons. J Neurochem 74:1968-1978.
15. Brewer GJ, Torricelli JR, Evege EK, Price PJ. 1993. Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res 35:567-576.
16. Brewer GJ, Lim A, Capps NG, Torricelli JR. 2005. Age-related calcium changes, oxyradical damage, caspase activation and nuclear condensation in hippocampal neurons in response to glutamate and beta-amyloid. Exp Gerontol 40:426-437.
17. Brewer GJ, Reichensperger JD, Brinton RD. 2006. Prevention of age-related dysregulation of calcium dynamics by estrogen in neurons. Neurobiol Aging 27:306-317.
18. Cadenas E, Boveris A, Ragan CI, Stoppani AO. 1977. Production of superoxide radicals and hydrogen peroxide by NADH-ubiquinone reductase and ubiquinol-cytochrome c reductase from beef-heart mitochondria. Arch Biochem Biophys 180:248-257.
19. Castilho RF, Ward MW, Nicholls DG. 1999. Oxidative stress, mitochondrial function, and acute glutamate excitotoxicity in cultured cerebellar granule cells. J Neurochem 72:1394-1401.
20. Chang DT, Honick AS, Reynolds IJ. 2006. Mitochondrial trafficking to synapses in cultured primary cortical neurons. J Neurosci 26:7035-7045.
21. Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, Lesnefsky EJ. 2003. Production of reactive oxygen species by mitochondria: central role of complex III. J Biol Chem 278:36027-36031.
22. Collins TJ, Berridge MJ, Lipp P, Bootman MD. 2002. Mitochondria are morphologically and functionally heterogeneous within cells. EMBO J 21:1616-1627.
23. Coyle JT, Puttfarcken P. 1993. Oxidative stress, glutamate, and neurodegenerative disorders. Science 262:689-695.
24. Dugan LL, Sensi SL, Canzoniero LM, Handran SD, Rothman SM, Lin TS, Goldberg MP, Choi DW. 1995. Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-D-aspartate. J Neurosci 15:6377-6388.
25. +: implications for neurodegeneration. J Neurochem 63:584-591.
26. Ehrenberg B, Montana V, Wei MD, Wuskell JP, Loew LM. 1988. Membrane potential can be determined in individual cells from the nernstian distribution of cationic dyes. Biophys J 53:785-794.
27. Eimerl S, Schramm M. 1994. The quantity of calcium that appears to induce neuronal death. J Neurochem 62:1223-1226.
28. Evans MS, Collings MA, Brewer GJ. 1998. Electrophysiology of embryonic, adult and aged rat hippocampal neurons in serum-free culture. J Neurosci Methods 79:37-46.
29. Fernandez-Gomez FJ, Galindo MF, Gomez-Lazaro M, Gonzalez-Garcia C, Cena V, Aguirre N, Jordan J. 2005. Involvement of mitochondrial potential and calcium buffering capacity in minocycline cytoprotective actions. Neuroscience 133:959-967.
30. Fleury C, Mignotte B, Vayssiere JL. 2002. Mitochondrial reactive oxygen species in cell death signaling. Biochimie 84:131-141.
31. Floyd RA, West M, Hensley K. 2001. Oxidative biochemical markers; clues to understanding aging in long-lived species. Exp Gerontol 36:619-shy; 640.
32. Gottlieb E, Vander Heiden MG, Thompson CB. 2000. Bcl-x(L) prevents the initial decrease in mitochondrial membrane potential and subsequent reactive oxygen species production during tumor necrosis factor alpha-induced apoptosis. Mol Cell Biol 20:5680-5689.
33. Guerrieri F, Capozza G, Kalous M, Papa S. 1992. Age-related changes of mitochondrial F0F1 ATP synthase. Ann N Y Acad Sci 671:395-402.
34. Ha HC, Snyder SH. 1999. Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc Natl Acad Sci U S A 96:13978-13982.
35. Hagen TM, Yowe DL, Bartholomew JC, Wehr CM, Do KL, Park JY, Ames BN. 1997. Mitochondrial decay in hepatocytes from old rats: membrane potential declines, heterogeneity and oxidants increase. Proc Natl Acad Sci U S A 94:3064-3069.
36. Hagen TM, Ingersoll RT, Lykkesfeldt J, Liu J, Wehr CM, Vinarsky V, Bartholomew JC, Ames AB. 1999. (R)-alpha-lipoic acid-supplemented old rats have improved mitochondrial function, decreased oxidative damage, and increased metabolic rate. FASEB J 13:411-418.
37. 2+ accumulation in cortical cell culture correlates with subsequent neuronal degeneration. J Neurosci 13:1993-2000.
38. Huang HM, Fowler C, Xu H, Zhang H, Gibson GE. 2005. Mitochondrial function in fibroblasts with aging in culture and/or Alzheimer's disease. Neurobiol Aging 26:839-848.
39. Ischiropoulos H, Gow A, Thom SR, Kooy NW, Royall JA, Crow JP. 1999. Detection of reactive nitrogen species using 2,7-dichlorodihydrofluorescein and dihydrorhodamine 123. Methods Enzymol 301:367-373.
40. 2+ load, but not by mitochondrial depolarization. FEBS Lett 529:351-355.
41. Khachaturian ZS. 1994. Calcium hypothesis of Alzheimer's disease and brain aging. Ann N Y Acad Sci 747:1-11.
42. Kopsidas G, Kovalenko SA, Kelso JM, Linnane AW. 1998. An age-associated correlation between cellular bioenergy decline and mtDNA rearrangements in human skeletal muscle. Mutat Res 421:27-36.
43. 2+-induced mitochondrial membrane permeabilization: role of coenzyme Q redox state. Am J Physiol 269:C141-C147.
44. 2+ is dependent on mitochondrial-generated reactive oxygen species. FEBS Lett 378:150-152.
45. Kroemer G, Reed JC. 2000. Mitochondrial control of cell death. Nat Med 6:513-519.
46. Kroemer G, Dallaporta B, Resche-Rigon M. 1998. The mitochondrial death/life regulator in apoptosis and necrosis. Annu Rev Physiol 60:619-642.
47. + oxidation-reduction state. Biochem J 368:545-553.
48. Kushnareva YE, Wiley SE, Ward MW, Andreyev AY, Murphy AN. 2005. Excitotoxic injury to mitochondria isolated from cultured neurons. J Biol Chem 280:28894-28902.
49. Kuznetsov AV, Usson Y, Leverve X, Margreiter R. 2004. Subcellular heterogeneity of mitochondrial function and dysfunction: evidence obtained by confocal imaging. Mol Cell Biochem 256-257:359-365.
50. Kwong LK, Sohal RS. 1998. Substrate and site specificity of hydrogen peroxide generation in mouse mitochondria. Arch Biochem Biophys 350:118-126.
51. Kwong LK, Sohal RS. 2000. Age-related changes in activities of mitochondrial electron transport complexes in various tissues of the mouse. Arch Biochem Biophys 373:16-22.
52. LaFerla FM. 2002. Calcium dyshomeostasis and intracellular signalling in Alzheimer's disease. Nat Rev Neurosci 3:862-872.
53. Lafon-Cazal M, Pietri S, Culcasi M, Bockaert J. 1993. NMDA-dependent superoxide production and neurotoxicity. Nature 364:535-537.
54. LeBel CP, Ischiropoulos H, Bondy SC. 1992. Evaluation of the probe 2′,7′-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 5:227-231.
55. Lemasters JJ, Nieminen AL, Qian T, Trost LC, Elmore SP, Nishimura Y, Crowe RA, Cascio WE, Bradham CA, Brenner DA, Herman B. 1998. The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis and autophagy. Biochim Biophys Acta 1366:177-196.
56. Li J, Spletter ML, Johnson DA, Wright LS, Svendsen CN, Johnson JA. 2005. Rotenone-induced caspase 9/3-independent and -dependent cell death in undifferentiated and differentiated human neural stem cells. J Neurochem 92:462-476.
57. Lifshitz J, Janmey PA, McIntosh TK. 2006. Photon correlation spectroscopy of brain mitochondrial populations: application to traumatic brain injury. Exp Neurol 197:318-329.
58. Liu Y, Fiskum G, Schubert D. 2002. Generation of reactive oxygen species by the mitochondrial electron transport chain. J Neurochem 80:780-787.
59. Liu R, Liu W, Doctrow SR, Baudry M. 2003. Iron toxicity in organotypic cultures of hippocampal slices: role of reactive oxygen species. J Neurochem 85:492-502.
60. Luetjens CM, Bui NT, Sengpiel B, Munstermann G, Poppe M, Krohn AJ, Bauerbach E, Krieglstein J, Prehn JH. 2000. Delayed mitochondrial dysfunction in excitotoxic neuron death: cytochrome c release and a secondary increase in superoxide production. J Neurosci 20:5715-5723.
61. Manczak M, Jung Y, Park BS, Partovi D, Reddy PH. 2005. Time-course of mitochondrial gene expressions in mice brains: implications for mitochondrial dysfunction, oxidative damage, and cytochrome c in aging. J Neurochem 92:494-504.
62. Murchison D, Zawieja DC, Griffith WH. 2004. Reduced mitochondrial buffering of voltage-gated calcium influx in aged rat basal forebrain neurons. Cell Calcium 36:61-75.
63. Nicholls DG, Budd SL. 2000. Mitochondria and neuronal survival. Physiol Rev 80:315-360.
64. Nicholls DG, Ward MW. 2000. Mitochondrial membrane potential and neuronal glutamate excitotoxicity: mortality and millivolts. Trends Neurosci 23:166-174.
65. Nicholls DG, Budd SL, Castilho RF, Ward MW. 1999. Glutamate excitotoxicity and neuronal energy metabolism. Ann N Y Acad Sci 893:1-12.
66. Patel JR, Brewer GJ. 2003. Age-related changes in neuronal glucose uptake in response to glutamate and beta-amyloid. J Neurosci Res 72:527-536.
67. Peng TI, Greenamyre JT. 1998. Privileged access to mitochondria of calcium influx through N-methyl-D-aspartate receptors. Mol Pharmacol 53:974-980.
68. Pivovarova NB, Nguyen HV, Winters CA, Brantner CA, Smith CL, Andrews SB. 2004. Excitotoxic calcium overload in a subpopulation of mitochondria triggers delayed death in hippocampal neurons. J Neurosci 24:5611-5622.
69. Poon HF, Shepherd HM, Reed TT, Calabrese V, Stella AM, Pennisi G, Cai J, Pierce WM, Klein JB, Butterfield DA. 2006. Proteomics analysis provides insight into caloric restriction mediated oxidation and expression of brain proteins associated with age-related impaired cellular processes: mitochondrial dysfunction, glutamate dysregulation and impaired protein synthesis. Neurobiol Aging 27:1020-1034.
70. Prehn JH. 1998. Mitochondrial transmembrane potential and free radical production in excitotoxic neurodegeneration. Naunyn Schmiedebergs Arch Pharmacol 357:316-322.
71. Rebrin I, Kamzalov S, Sohal RS. 2003. Effects of age and caloric restriction on glutathione redox state in mice. Free Radic Biol Med 35:626-635.
72. Reddy PH. 2006. Amyloid precursor protein-mediated free radicals and oxidative damage: implications for the development and progression of Alzheimer's disease. J Neurochem 96:1-13.
73. 2+: their relationship to apoptosis and oncogenesis. FEBS Lett 325:104-107.
74. Sastre J, Millan A, Asuncion JG, Pla R, Juan G, Pallardo FV, O'Connor E, Martin JA, Droy-Lefaix MT, Vina J. 1998. A ginkgo biloba extract (EGb 761) prevents mitochondrial aging by protecting against oxidative stress. Free Radic Biol Med 24:298-304.
75. Scaduto RC, Jr, Grotyohann LW. 1999. Measurement of mitochondrial membrane potential using fluorescent rhodamine derivatives. Biophys J 76:469-477.
76. Schinder AF, Olson EC, Spitzer NC, Montal M. 1996. Mitochondrial dysfunction is a primary event in glutamate neurotoxicity. J Neurosci 16:6125-6133.
77. Skulachev VP. 2001. The programmed death phenomena, aging, and the Samurai law of biology. Exp Gerontol 36:995-1024.
78. Skulachev VP. 2006. Bioenergetic aspects of apoptosis, necrosis and mitoptosis. Apoptosis 11:473-485.
79. Solenski NJ, Kostecki VK, Dovey S, Periasamy A. 2003. Nitric-oxide-induced depolarization of neuronal mitochondria: implications for neuronal cell death. Mol Cell Neurosci 24:1151-1169.
80. Starkov AA, Polster BM, Fiskum G. 2002. Regulation of hydrogen peroxide production by brain mitochondria by calcium and Bax. J Neurochem 83:220-228.
81. Starkov AA, Chinopoulos C, Fiskum G. 2004. Mitochondrial calcium and oxidative stress as mediators of ischemic brain injury. Cell Calcium 36:257-264.
82. Stout AK, Raphael HM, Kanterewicz BI, Klann E, Reynolds IJ. 1998. Glutamate-induced neuron death requires mitochondrial calcium uptake. Nat Neurosci 1:366-373.
83. Tirosh O, Sen CK, Roy S, Packer L. 2000. Cellular and mitochondrial changes in glutamate-induced HT4 neuronal cell death. Neuroscience 97:531-541.
84. Turrens JF. 2003. Mitochondrial formation of reactive oxygen species. J Physiol 552:335-344.
85. Turrens JF, Freeman BA, Levitt JG, Crapo JD. 1982. The effect of hyperoxia on superoxide production by lung submitochondrial particles. Arch Biochem Biophys 217:401-410.
86. Vercesi AE, Kowaltowski AJ, Grijalba MT, Meimcke AR, Castilho RF. 1997. The role of reactive oxygen species in mitochondrial permeability transition. Biosci Rep 17:43-52.
87. Vergun O, Sobolevsky AI, Yelshansky MV, Keelan J, Khodorov BI, Duchen MR. 2001. Exploration of the role of reactive oxygen species in glutamate neurotoxicity in rat hippocampal neurones in culture. J Physiol 531:147-163.
88. Vesce S, Jekabsons MB, Johnson-Cadwell LI, Nicholls DG. 2005. Acute glutathione depletion restricts mitochondrial ATP export in cerebellar granule neurons. J Biol Chem 280:38720-38728.
89. Votyakova TV, Reynolds IJ. 2001. DeltaPsi(m)-dependent and -independent production of reactive oxygen species by rat brain mitochondria. J Neurochem 79:266-277.
90. Wadia JS, Chalmers-Redman RM, Ju WJ, Carlile GW, Phillips JL, Fraser AD, Tatton WG. 1998. Mitochondrial membrane potential and nuclear changes in apoptosis caused by serum and nerve growth factor withdrawal: time course and modification by (-)-deprenyl. J Neurosci 18: 932-947.
91. Wallace DC. 1999. Mitochondrial diseases in man and mouse. Science 283:1482-1488.
92. Weiss JN, Korge P, Honda HM, Ping P. 2003. Role of the mitochondrial permeability transition in myocardial disease. Circ Res 93:292-301.
93. White RJ, Reynolds IJ. 1996. Mitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxin exposure. J Neurosci 16:5688-5697.
94. Wrona M, Patel K, Wardman P. 2005. Reactivity of 2′,7′- dichlorodihydrofluorescein and dihydrorhodamine 123 and their oxidized forms toward carbonate, nitrogen dioxide, and hydroxyl radicals. Free Radic Biol Med 38:262-270.
95. 2+ homeostasis in aged cerebellar granule neurons in brain slices. J Neurosci 22:10761-10771.
96. Zoratti M, Szabo I. 1995. The mitochondrial permeability transition. Biochim Biophys Acta 1241:139-176.
97. Zorov DB, Filburn CR, Klotz LO, Zweier JL, Sollott SJ. 2000. Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med 192:1001-1014.