Nitric-oxide-induced depolarization of neuronal mitochondria: Implications for neuronal cell death

Molecular and Cellular Neuroscience

Volumn 24, Issue 4, 2003, Pages 1151-1169

  Solenski, Nina J ^a   Kostecki, Vannessa K ^a   Dovey, Serena ^a   Periasamy, Ammasi ^a  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROTYROSINE; CATALASE; DIETHYLENETRIAMINE; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NITRIC OXIDE; PEROXYNITRITE; REACTIVE NITROGEN SPECIES;

ANIMAL CELL; ARTICLE; BRAIN CELL; CELL DEATH; CONTROLLED STUDY; DEPOLARIZATION; ELECTROPHYSIOLOGY; IMMUNOREACTIVITY; MEMBRANE PERMEABILITY; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; NERVE CELL CULTURE; NERVE CELL NECROSIS; NEUROPROTECTION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0347124689     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2003.08.011     Document Type: Article

References (78)

1. Aizenman E., Brimecombe J.C., Potthoff W.K., Rosenberg P.A. Why is the role of nitric oxide in NMDA receptor function and dysfunction so controversial? Progr. Brain Res. 118:1998;53-71.
2. Akira T., Henry D., Wasterlain C.G. Nitric oxide mediates the sustained opening of NMDA receptor-gated ionic channels which follows transient excitotoxic exposure in hippocampal slices. Brain Res. 652:1994;190-194.
3. Almeida A., Bolanos J.P., Medina J.M. Nitric oxide mediates glutamate-induced mitochondrial depolarization in rat cortical neurons. Brain Res. 816:1999;580-586.
4. Almeida A., Almeida J., Bolanos J.P., Moncada S. Different responses of astrocytes and neurons to nitric oxide the role of glycolytically generated ATP in astrocyte protection . Proc. Nat. Acad. Sci. USA. 98:2001;15294-15299.
5. Almeida A., Delgado-Esteban M., Bolanos J.P., Medina J.M. Oxygen and glucose deprivation induces mitochondrial dysfunction and oxidative stress in neurones but not in astrocytes in primary culture. J. Neurochem. 81:2002;207-217.
6. Alonso D., Encinas J.M., Uttenthal L.O., Bosca L., Serrano J., Fernandez A.P., Castro-Blanco S., Santacana M., Bentura M.L., Richart A., Fernandez-Vizarra P., Rodrigo J. Coexistence of translocated cytochrome c and nitrated protein in neurons of the rat cerebral cortex after oxygen and glucose deprivation. Neuroscience. 111:2002;47-56.
7. Ankarcrona M., Dypbukt J.M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S.A., Nicotera P. Glutamate-induced neuronal death a succession of necrosis or apoptosis depending on mitochondrial function . Neuron. 15:1995;961-973.
8. Aulak K.S., Miyagi M., Yan L., West K.A., Massillon D., Crabb J.W., Stuehr D.J. Proteomic method identifies proteins nitrated in vivo during inflammatory challenge. Proc. Natl. Acad. Sci. USA. 98:2001;12056-12061.
9. Bal-Price A., Brown G.C. Nitric-oxide-induced necrosis and apoptosis in PC12 cells mediated by mitochondria. J. Neurochem. 75:2000;1455-1464.
10. Bal-Price A., Brown G.C. Inflammatory neurodegeneration mediated by nitric oxide from activated glia-inhibiting neuronal respiration, causing glutamate release and excitotoxicity. J. Neurosci. 21:2001;6480-6491.
11. Banker, G., Asmussen, H., Goslin, K., 1998. In: Culturing Nerve Cells. MIT Press, Cambridge.
12. Bon C.L., Garthwaite J. Exogenous nitric oxide causes potentiation of hippocampal synaptic transmission during low-frequency stimulation via the endogenous nitric oxide-cGMP pathway. Eur. J. Neurosci. 14:2001;585-594.
13. Brookes P.S., Salinas E.P., Darley-Usmar K., Eiserich J.P., Freeman B.A., Darley-Usmar V.M., Anderson P.G. Concentration-dependent effects of nitric oxide on mitochondrial permeability transition and cytochrome c release. J. Biol. Chem. 275:2000;20474-20479.
14. Brorson J.R., Zhang H. Disrupted [Ca2+]i homeostasis contributes to the toxicity of nitric oxide in cultured hippocampal neurons. J. Neurochem. 69:1997;1882-1889.
15. Brorson J.R., Schumacker P.T., Zhang H. Nitric oxide acutely inhibits neuronal energy production. The Committees on Neurobiology and Cell Physiology. J. Neurosci. 19:1999;147-158.
16. Budd S.L., Tenneti L., Lishnak T., Lipton S.A. Mitochondrial and extramitochondrial apoptotic signaling pathways in cerebrocortical neurons. Proc. Natl. Acad. Sci. USA. 97:2000;6161-6166.
17. Cassina A., Radi R. Differential inhibitory action of nitric oxide and peroxynitrite on mitochondrial electron transport. Arch. Biochem. Biophys. 328:1996;309-316.
18. Castilho R.F., Ward M.W., Nicholls D.G. Oxidative stress, mitochondrial function, and acute glutamate excitotoxicity in cultured cerebellar granule cells. J. Neurochem. 72:1999;1394-1401.
19. Chang N.S., Pratt N., Heath J., Schultz L., Sleve D., Carey G.B., Zevotek N. Hyaluronidase induction of a WW domain-containing oxidoreductase that enhances tumor necrosis factor cytotoxicity. J. Biol. Chem. 276:2000;3361-3370.
20. Choi Y.B., Lipton S.A. Redox modulation of the NMDA receptor. Cell. Mol. Life Sci. 57:2000;1535-1541.
21. Crompton M., Virji S., Doyle V., Johnson N., Ward J.M. The mitochondrial permeability transition pore. Biochem. Soc. Symp. 66:1999;167-179.
22. Dawson V.L., Dawson T.M., London E.D., Bredt D.S., Snyder S.H. Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc. Natl. Acad. Sci. USA. 88:1991;6368-6371.
23. Dawson V.L., Dawson T.M., Bartley D.A., Uhl G.R., Snyder S.H. Mechanisms of nitric oxide-mediated neurotoxicity in primary brain cultures. J. Neurosci. 13:1993;2651-2661.
24. Dawson V.L., Kizushi V.M., Huang P.L., Snyder S.H., Dawson T.M. Resistance to neurotoxicity in cortical cultures from neuronal nitric oxide synthase-deficient mice. J. Neurosci. 16:1996;2479-2487.
25. Elfering S.L., Sarkela T.M., Giulivi C. Biochemistry of mitochondrial nitric-oxide synthase. J. Biol. Chem. 277:2002;38079-38086.
26. Eliasson M.J., Huang Z., Ferrante R.J., Sasamata M., Molliver M.E., Snyder S.H., Moskowitz M.A. Neuronal nitric oxide synthase activation and peroxynitrite formation in ischemic stroke linked to neural damage. J. Neurosci. 19:1999;5910-5918.
27. Estevez A.G., Radi R., Barbeito L., Shin J.T., Thompson J.A., Beckman J.S. Peroxynitrite-induced cytotoxicity in PC12 cells evidence for an apoptotic mechanism differentially modulated by neurotrophic factors . J. Neurochem. 65:1995;1543-1550.
28. Fitzhugh A.L., Keefer L.K. Diazeniumdiolates pro- and antioxidant applications of the "NONO ates" Free Radi. Biol. Med. 28:2000;1463-1469.
29. Gbadegesin M., Vicini S., Hewett S.J., Wink D.A., Espey M., Pluta R.M., Colton C.A. Hypoxia modulates nitric oxide-induced regulation of NMDA receptor currents and neuronal cell death. Am. J. Physiol. 277:1999;C673-C683.
30. Ghafourifar P., Ritcher C. Nitric oxide synthase activity in mitochondria. FEBS Lett. 418:1997;291-296.
31. Ghafourifar P., Schenk U., Klein S.D., Richter C. Mitochondrial nitric-oxide synthase stimulation causes cytochrome c release from isolated mitochondria. Evidence for intramitochondrial peroxynitrite formation. J. Biol. Chem. 274:1999;31185-31188.
32. Gonzalez-Zulueta M., Ensz L.M., Mukhina G., Lebovitz R.M., Zwacka R.M., Engelhardt F., Oberley L.W., Dawson V.L., Dawson T.M. Manganese superoxide dismutase protects nNOS neurons from NMDA and nitric oxide-mediated neurotoxicity. J. Neurosci. 18:1998;2040-2055.
33. Gow A.J., Chen O., Gole M., Themistocleous M., Lee V., Ischiropoulos H. Two distinct mechanisms of nitric oxide-mediated neuronal cell death show thiol dependency. Am. J. Physiol. Cell. Physiol. 278:2000;C1099-C1107.
34. Greenfield L.J. Jr., Macdonald R.L. Whole-cell and single-channel alpha1 beta1 gamma2S GABAA receptor currents elicited by a "multipuffer" drug application device. Pflugers Arch. Eur. J. Physiol. 432:1996;1080-1090.
35. Griffiths C., Garthwaite J. The shaping of nitric oxide signals by a cellular sink. J. Physiol. 536:2001;855-862.
36. Hortelano S., Alvarez A.M., Bosca L. Nitric oxide induces tyrosine nitration and release of cytochrome c preceding an increase of mitochondrial transmembrane potential in macrophages. FASEB J. 13:1999;2311-2317.
37. Hoyt K.R., Tang L.H., Aizenman E., Reynolds I.J. Nitric oxide modulates NMDA-induced increases in intracellular Ca2+ in cultured rat forebrain neurons. Brain Res. 592:1992;310-316.
38. Kanai A.J., Pearce L.L., Clemens P.R., Birder L.A., VanBibber M.M., Choi S.Y., de Groat W.C., Peterson J. Identification of a neuronal nitric oxide synthase in isolated cardiac mitochondria using electrochemical detection. Proc. Natl. Acad. Sci. USA. 98:2001;14126-14131.
39. Kayahara M., Felderhoff U., Pocock J., Hughes M.N., Mehmet H. Nitric oxide (NO) and the nitrosonium cation (NO+) reduce mitochondrial membrane potential and trigger apoptosis in neuronal PC12 cells. Biochem. Soc. Trans. 26:1998;S340.
40. Keelan J., Vergun O., Duchen M.R. Excitotoxic mitochondrial depolarisation requires both calcium and nitric oxide in rat hippocampal neurons. J. Physiol. 520:1999;t-813.
41. Keller J.N., Kindy M.S., Holtsberg F.W., St Clair D.K., Yen H.C., Germeyer A., Steiner S.M., Bruce-Keller A.J., Hutchins J.B., Mattson M.P. Mitochondrial manganese superoxide dismutase prevents neural apoptosis and reduces ischemic brain injury suppression of peroxynitrite production, lipid peroxidation, and mitochondrial dysfunction . J. Neurosci. 18:1998;687-697.
42. Kindler, D.D., Thiffault, C., Solenski, N.J., Dennis, J., Kostecki, V.K., Jenkins, R., Keeney, P.M., Bennett, J.P., 2003. Neurotoxic nitric oxide rapidly depolarizes and permeabilizes mitochondria by dynamically opening the mitochondrial transition pore. Mol. Cell. Neurosci., 23, 559-573.
43. Lacza Z., Puskar M., Figueroa J.P., Zhang J., Rajapakse N., Busija D.W. Mitochondrial nitric oxide synthase is constitutively active and is functionally upregulated in hypoxia. Free Radic. Biol. Med. 31:2001;1609-1615.
44. Leist M., Fava E., Montecucco C., Nicotera P. Peroxynitrite and nitric oxide donors induce neuronal apoptosis by eliciting autocrine excitotoxicity. Eur. J. Neurosci. 9:1997;1488-1498.
45. Li Y., Copin J.C., Reola L.F., Calagui B., Gobbel G.T., Chen S.F., Sato S., Epstein C.J., Chan P.H. Reduced mitochondrial manganese-superoxide dismutase activity exacerbates glutamate toxicity in cultured mouse cortical neurons. Brain Res. 14:(814):1998;164-170.
46. Lipton S.A., Choi Y.B., Pan Z.H., Lei S.Z., Chen H.S., Sucher N.J., Loscalzo J., Singel D.J., Stamler J.S. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature. 364:1993;626-632.
47. Lipton S.A., Choi Y.B., Sucher N.J., Pan Z.H., Stamler J.S. Redox state, NMDA receptors and NO-related species. Trends Pharmacol. Sci. 17:1996;186-187.
48. Lipton S.A. Distinctive chemistries of no-related species. Neurochem. Int. 29:1996;111-114.
49. Lipton S.A., Choi Y.B., Sucher N.J., Chen H.S. Neuroprotective versus neurodestructive effects of NO-related species. Biofactors. 8:1998;33-40.
50. Lipton S.A., Rayudu P.V., Choi Y.B., Sucher N.J., Chen H.S. Redox modulation of the NMDA receptor by NO-related species. Progr. Brain Res. 118:1998;73-82.
51. Lipton S.A. Neuronal protection and destruction by NO. Cell Death Differentiation. 6:1999;943-951.
52. MacMillan-Crow L.A., Thompson J.A. Tyrosine modifications and inactivation of active site manganese superoxide dismutase mutant (Y34F) by peroxynitrite. Arch. Biochem. Biophys. 366:1999;82-88.
53. Macmillan-Crow L.A., Cruthirds D.L. Invited review manganese superoxide dismutase in disease . Free Radic. Res. 34:2001;325-336.
54. Malinski T., Bailey F., Zhang Z.G., Chopp M. Nitric oxide measured by a porphyrinic microsensor in rat brain after transient middle cerebral artery occlusion. J. Cereb. Blood Flow Metab. 13:1993;355-358.
55. McNaught K.S., Brown G.C. Nitric oxide causes glutamate release from brain synaptosomes. J. Neurochem. 70:1998;1541-1546.
56. Niquet J., Baldwin R.A., Allen S.G., Fujikawa D., Wasterlain C.G. Hypoxic neuronal necrosis protein synthesis-independent activation of a cell death program . Proc. Natl. Acad. Sci. USA. 100:2003;2825-2830.
57. Ochiai-Kanai R., Hasegawa K., Takeuchi Y., Yoshioka H., Sawada T. Immunohistochemical nitrotyrosine distribution in neonatal rat cerebrocortical slices during and after hypoxia. Brain Res. 847:1999;59-70.
58. Palluy O., Rigaud M. Nitric oxide induces cultured cortical neuron apoptosis. Neurosci. Lett. 208:1996;1-4.
59. Peng T.I., Greenamyre J.T. Privileged access to mitochondria of calcium influx through N-methyl-D-aspartate receptors. Mol. Pharmacol. 53:1998;974-980.
60. Peng T.I., Jou M.J., Sheu S.S., Greenamyre J.T. Visualization of NMDA receptor-induced mitochondrial calcium accumulation in striatal neurons. Exp. Neurol. 149:1998;1-12.
61. Pong K., Doctrow S.R., Baudry M. Prevention of 1-methyl-4- phenylpyridinium- and 6-hydroxydopamine- induced nitration of tyrosine hydroxylase and neurotoxicity by EUK-134, a superoxide dismutase and catalase mimetic, in cultured dopaminergic neurons. Brain Res. 881:2000;182-189.
62. Pong K., Doctrow S.R., Huffman K., Adinolfi C.A., Baudry M. Attenuation of zinc-induced intracellular dysfunction and neurotoxicity by a synthetic superoxide dismutase/catalase mimetic, in cultured cortical neurons. Brain Res. 950:2002;218-230.
63. Radi R., Cassina A., Hodara R. Nitric oxide and peroxynitrite interactions with mitochondria. [Review] [66 refs]. Biol. Chem. 383:2002;401-409.
64. Radi R., Rodriguez M., Castro L., Telleri R. Inhibition of mitochondrial electron transport by peroxynitrite. Arch. Biochem. Biophys. 308:1994;89-95.
65. Reynolds I.J. Mitochondrial membrane potential and the permeability transition in excitotoxicity. Ann. N. Y. Acad. Sci. 893:1999;33-41.
66. Roy M., Sapolsky R. Neuronal apoptosis in acute necrotic insults why is this subject such a mess? Trends Neurosci. 22:1999;419-422.
67. Scanlon J.M., Reynolds I.J. Effects of oxidants and glutamate receptor activation on mitochondrial membrane potential in rat forebrain neurons. J. Neurochem. 71:1998;2392-2400.
68. Schinder A.F., Olson E.C., Spitzer N.C., Montal M. Mitochondrial dysfunction is a primary event in glutamate neurotoxicity. J. Neurosci. 16:1996;6125-6133.
69. Sharpe M.A., Ollosson R., Stewart V.C., Clark J.B. Oxidation of nitric oxide by oxomanganese-salen complexes a new mechanism for cellular protection by superoxide dismutase/catalase mimetics. Biochem. J. 366:2002;97-107.
70. Solenski, N.J., Kostecki, V.K., Mangan, P.S., Characterization of cortical neuronal cultures - implications for models of neurological disease. Soc. Neursci. 2002 Abstr. Program No. 730.7. 2002.
71. Sporns O., Jenkinson S. Potassium ion- and nitric oxide-induced exocytosis from populations of hippocampal synapses during synaptic maturation in vitro. Neuroscience. 80:1997;1057-1073.
72. Stewart V.C., Heslegrave A.J., Brown G.C., Clark J.B., Heales S.J. Nitric oxide-dependent damage to neuronal mitochondria involves the NMDA receptor. Eur. J. Neurosci. 15:2002;458-464.
73. Stout A.K., Raphael H.M., Kanterewicz B.I., Klann E., Reynolds I.J. Glutamate-induced neuron death requires mitochondrial calcium uptake. Nat. Neurosci. 1:1998;366-373.
74. Vidwans A.S., Kim S., Coffin D.O., Wink D.A., Hewett S.J. Analysis of the neuroprotective effects of various nitric oxide donor compounds in murine mixed cortical cell culture. J. Neurochem. 72:1999;1843-1852.
75. Viera L., Ye Y.Z., Estevez A.G., Beckman J.S. Methods Enzymol. 301:1999;373-381.
76. Vieira H.L., Belzacq A.S., Haouzi D., Bernassola F., Cohen I., Jacotot E., Ferri K.F., El Hamel C., Bartle L.M., Melino G., Brenner C., Goldmacher V., Kroemer G. The adenine nucleotide translocator a target of nitric oxide, peroxynitrite, and 4-hydroxynonenal . Oncogene. 20:2001;4305-4316.
77. Ward M.W., Rego A.C., Frenguelli B.G., Nicholls D.G. Mitochondrial membrane potential and glutamate excitotoxicity in cultured cerebellar granule cells. J. Neurosci. 20:2000;7208-7219.
78. White R.J., Reynolds I.J. Mitochondrial depolarization in glutamate-stimulated neurons an early signal specific to excitotoxin exposure . J. Neurosci. 16:1996;5688-5697.