The role of nitric oxide in the radiation-induced effects in the developing brain

In Vivo

Volumn 18, Issue 3, 2004, Pages 281-292

  Gisone, Pablo ^a   Dubner, Diana ^a   Del Rosario Pérez, María ^a   Michelin, Severino ^a   Puntarulo, Susana ^b  

^a Nuclear Regulatory Authority   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Developing brain; Ionizing radiation; Nitric Oxide; Oxidative stress; Review

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCINEURIN; CASPASE; GLUTATHIONE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BCL 2; PROTEIN KINASE (CALCIUM,CALMODULIN); REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; BRAIN DEVELOPMENT; BRAIN INJURY; BRAIN MITOCHONDRION; CELL SURVIVAL; CHEMICAL BINDING; CHEMICAL REACTION; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; IONIZING RADIATION; LIPID PEROXIDATION; MITOCHONDRIAL RESPIRATION; NERVE CELL PLASTICITY; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; REVIEW; SIGNAL TRANSDUCTION;

EID: 4043141548     PISSN: 0258851X     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (146)

1. Kimler BF: Prenatal irradiation: a mayor concern for the developing brain. Int J Radiat Biol 73: 423-434, 1998.
2. Schull WJ: Brain damage among individuals exposed prenatally to ionizing radiation: a 1993 review. Stem Cells 15 Suppl 2: 129-133, 1997.
3. Mishra OP, Fritz KI and Delivoria-Papadopoulos M: NMDA receptor and neonatal hypoxic brain injury. Ment Retard Dev Disabil Res Rev 7: 249-253, 2001.
4. Blomgren K, Zhu C, Hallin U and Hagberg H: Mitochondria and ischemic reperfusion damage in the adult and in the developing brain. Biochem Biophys Res Comm 304: 551-559, 2003.
5. Pettman B and Henderson CE: Neuronal cell death. Neuron 20: 633-647, 1998.
6. Schmidt-Ullrich RK, Dent P, Grant S, Mikkelsen RB and Valerie K: Signal transduction and cellular radiation responses. Rad Res 153: 245-247, 2000.
7. Boje KM: Nitric oxide neurotoxicity in neurodegenerative diseases. Front Biosc 9: 763-776, 2004.
8. Joshi MS, Ponthier JL and Lancaster R: Cellular antioxidant and proxidant actions of nitric oxide. Free Rad Biol Med 27(11/12): 1357-1366, 1999.
9. Moncada S, Palmer RMJ and Higgs EA: Nitric oxide: physiology, pathophysiology and pharmacology. Pharmacol Rev 43: 109-142, 1991.
10. Knowles RG: Nitric oxide, mitochondria and metabolism. Biochem Soc Trans 25: 895-901, 1997.
11. Stamler JS, Singel DJ and Loscalzo J: Biochemistry of nitric oxide and its redox-activated forms. Science 258: 1898-1902, 1992.
12. Basylinski DA and Hollocher TC: Evidence from the reaction between trioxodinitrate (II) and 15NO that trioxidinitrate (II) decomposes into nitrosyl hydride and nitrite in neutral aqueous solution. Inorg Chem 24: 4285-4288, 1985.
13. Goretski J and Hollocher TC: Trapping of nitric oxide produced during denitrification by extracellular hemoglobin. J Biol Chem 263: 2316-2323, 1988.
14. 2. Implications for the action of endothelium-derived relaxing factor (EDRF). Free Rad Res Commun 10: 221-222, 1990.
15. Wink DA and Mitchell JB: Chemical biology of nitric oxide: insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radical Biol Med 25: 434-456, 1998.
16. Davis KL, Martin E, Turko IV and Murad F: Novel effects of nitric oxide. Annu Rev Pharmacol Toxicol 41: 203-236, 2001.
17. Henry Y, Durocq C, Darpier JC, Servent D, Pellat C and Guissani A: Nitric oxide, a biological effector. Electron paramagnetic resonance detection of nitrosyl-iron-protein complexes in whole cells. Eur Biophys J 20: 1-15, 1991.
18. Martin E, Davis K, Bian K, Lee YC and Murad F: Cellular signaling with nitric oxide and cyclic guanosine monophosphate. Semin Perinatol 24: 2-6, 2000.
19. Wink DA, Osawa Y, Darbyshire JF, Jones CR, Eshenaur SC and Nims NW: Inhibition of cytochrome P450 by nitric oxide and a nitric oxide-releasing agent. Arch Biochem Biophys 300: 115-123, 1993.
20. Rubbo H, Parthasarathy S, Barnes S, Kirk M, Kalyanaraman B and Freeman BA: Nitric oxide inhibition of lipoxygenase-dependent liposome and low density lipoprotein oxidation: termination of radical chain propagation reactions and formation of nitrogen containing oxidized lipid derivatives. Arch Biochem Biophys 324: 15-25, 1995.
21. Ford PC, Wink DA and Stanbury DM: Autoxidation kinetics of aqueous nitric oxide. FEBS Lett 326: 1-3, 1993.
22. Dent P, Yacoub A, Contessa J, Caron R, Amorino G, Valerie K, Hagan MP, Grant S and Schmidt-Ulrich R: Stress and radiation-induced activation of multiple intracellular signaling pathways. Radiat Res 159: 283-300, 2003.
23. Dent P, Yacoub A, Fisher PB, Hagan MP and Grant S: MAPK pathways in radiation responses. Oncogene 22(37): 5885-5896, 2003.
24. Perez MR, Dubner D, Michelin S, Leteurtre F, Carosella ED and Gisone PA: Radiation-induced up-regulation of telomerase in KG1a cells is influenced by dose-rate and radiation quality. Int J Radiat Biol 78(12): 1175-1183, 2002.
25. Cataldi A, Zauli G, Di Pietro R, Castorina S and Rana R: Involvement of the pathway phosphatidylinositol-3-kinase/AKT-1 in the establishment of the survival response to ionizing radiation. Cell Signal 13: 369-375, 2001.
26. Yang J, Yu Y, Hamrick HE and Duerksen-Hughes PJ:ATM, ATR and DNA-PK: initiators of the cellular genotoxic stress responses. Carcinogenesis 24(10): 1571-1580, 2003.
27. Cohen-Jonathan E, Bernhard EJ and McKenna WG: How does radiation kill cells? Curr Opin Chem Biol 3: 77-83, 1999.
28. el-Deiry WS: Regulation of p53 downstream genes. Semin Cancer Biol 8: 345-57,1998.
29. Perry ME: Mdm2 in the response to radiation. Mol Cancer Res 2: 9-19, 2004.
30. Fernet M, Ponette V, Deniaud-Alexandre E, Ménissier J, de Murcia G, Giocanti N, Megnin-Chanet F and Favaudon V: Poly(ADP-ribose) polymerase, a major determinant of early response to ionizing radiation. Int J Radiat Biol 76(12): 1621-1629, 2000.
31. Brach MA, Hass R, Sherman ML, Gunji H, Weichselbaum R and Kufe D: Ionizing radiation induces expression and binding activity of the nuclear factor kappa B. J Clin Invest 88: 691-695, 1991.
32. Eferl R and Wagner EF: AP-1: a double-edged sword in tumorigenesis. Nat Rev Cancer 3(11): 859-868, 2003.
33. Vit JP and Rosselli F: Role of the ceramide-signaling pathways in ionizing radiation-induced apoptosis. Oncogene 22: 8645-8652, 2003.
34. Voevodskaya NV and Vanin AF: Gamma-irradiation potentiates L-arginine-dependent nitric oxide formation in mice. Biochem Biophys Res Commun 186: 1423-1428, 1992.
35. Mikoian VD, Voevodskaia NV, Kubrina LN, Malenkova IV and Vanin AF: Exogenous iron and gamma-radiation induces syhthesis of NO-synthetase in mouse liver. Biokhimiia 59: 732-738, 1994.
36. Gorbunov N, Pogue-Geile L, Epperly MW, Bigbee WL, Draviam R, Day BW, Wald N, Watkins SC and Greenberger JS: Activation of the nitric oxide synthase 2 pathway in the response of bone marrow stromal cells to high doses of ionizing radiation. Radiat Res 154: 73-86, 2000.
37. Nakagawa H, Ikota N, Ozawa T and Kotake Y: Dose- and time-dependence of radiation-induced nitric oxide formation in mice as quantified with electron paramagnetic resonance. Nitric Oxide Biol Chem 5: 47-52, 2001.
38. Giannopoulou E, Katsoris P, Polytarchou C and Papadimitriou E: Nitration of cytoskeletal proteins in the chicken embryo chorioallantoic membrane. Arch Biochem Biophys 400: 188-198, 2002.
39. Ailland J, Kampen WU, Schunke M, Trentmann J and Kurz B: Beta irradiation decreases collagen type II synthesis and increases nitric oxide production and cell death in articular chondrocytes. Ann Rheum Dis 62: 1054-1060, 2003.
40. Leach JK, Van Tuyle G, Lin PS, Schmidt-Ullrich R and Mikkelsen RB: Ionizing radiation-induced, mitochondria-dependent generation of reactive oxygen/nitrogen. Cancer Res 61: 3894-3901, 2001.
41. Leach JK, Black SM, Schmidt-Ullrich RK and Mikkelsen RB: Activation of constitutive nitric-oxide synthase activity is an early signaling event induced by ionizing radiation. J Biol Chem 277: 15400-15406, 2002.
42. Matsumoto H, Hayashi S, Hatashita M, Shioura H., Ohtsubo T, Kitai R, Ohnishi T, Yukawa O, Furusawa Y and Kano E: Induction of radioresistance to accelerated carbon-ion beams in recipient cells by nitric oxide excreted from irradiated donor cell of human glioblastoma. Int J Radiat Biol 76: 1649-1657, 2000.
43. Clarencon D, Lestaevel P, Laval JD, Multon E, Gourmelon P, Buguet A and Cespuglio R: Voltammetric measurement of blood nitric oxide in irradiated rats. Int J Radiat Biol 75: 201-208, 1999.
44. Korobov VN, Sorokina LV, Korobova OV and Datsiuk LA: Small doses of X-ray irradiation activate the NO-synthase component of the nitric oxyde cycle. Radiat Biol Radioecol 43: 182-185, 2003.
45. Cohen EP, Fish BL and Moulder JE: The role of nitric oxide in radiation nephropathy. Arch Physiol Biochem 104: 200-206, 1996.
46. Nozaki Y, Hasegawa Y, Takeuchi A, Fan ZH, Isobe KI, Nakashima I and Shimokata K: Nitric oxide as an inflammatory mediator of radiation pneumonitis in rats. Am J Physiol 272: 651-658, 1997.
47. Soloviev AI, Tishkin SM, Parshikov AV, Ivanova IV, Goncharov EV and Gurney AM: Mechanisms of endothelial dysfunction after ionizing radiation: selective impairment of the nitric oxide component of endothelium-dependent vasodilatation. Br J Pharmacol 138: 837-844, 2003.
48. Morel E, Dublineau I and Griffiths NM: Effect of radiation on cAMP, cGMP and Ca++ pathways and their interactions in rat distal colon. Radiat Res 160: 263-272, 2003.
49. Freeman SL and MacNaughton WK: Nitric oxide inhibitable isoforms of adenylate cyclase mediate epithelial secretory dysfunction following exposure to ionising radiation. Gut 53: 214-221, 2004.
50. Sonveaux P, Dessy C, Brouet A, Jordan BF, Gregoire V, Gallez B, Balligand JL and Feron O: Modulation of the tumor vasculature functionality by ionizing radiation accounts for tumor radiosensitization and promotes gene delivery. FASEB J 16: 1979-1981, 2002.
51. Ibuki Y and Goto R: Augmentation of NO production and cytolytic activity of macrophages obtained from mice irradiated with low dose of gamma-rays. J Radiat Res (Tokyo) 36: 209-220, 1995.
52. McKinney LC, Aquilla EM, Coffin D, Wink DA and Vodovotz Y: Ionizing radiation potentiates the induction of nitric oxide synthase by interferon-gamma and/or lipopolysaccharide in murine macrophage lines. Role of tumor necrosis factor alpha. Ann N Y Acad Sci 899: 61-68, 2000.
53. Yoo JC, Pae HO, Choi BM, Kim JD, Kim YM and Chung HT: Ionizing radiation potentiates the induction of nitric oxide synthase by interferon-gamma (IFN-gamma) or IFN-gamma and lipopolysaccharide in BNL-cl.2 murine embryonic liver cells: role of hydrogen peroxide. Free Rad Biol Med 28: 390-396, 2000.
54. Lestaevel P, Clarencon D, Gharib A, Peinnequin A, Cespuglio R, Gourmelon P, Alonso A, Laval JD and Multon E: Nitric oxide voltammetric measurements in the rat brain after gamma irradiation. Radiat Res 160: 631-636, 2003.
55. Gisone P, Boveris AD, Dubner D, Perez MR, Robello E and Puntarulo S: Early neuroprotective effect of nitric oxide in developing brain irradiated in utero. Neurotoxicology 24: 245-253, 2003.
56. Dawson TM, Gonzalez-Zulueta M, Kusci VL and Dawson YL: Nitric oxide diverse actions in the central and peripheral nervous sytem. Neurocient 4: 96-112, 1998.
57. Bredt DS, Ferris CD and Snyder SN: NOS regulatory sites. J Biol Chem 267: 10976-10981, 1992.
58. Dawson TM, Steiner JP, Dawson VL, Dinerman JL, Uhl GR and Snyder SH: Immunosuppresant FK506 enhances phosphorylation of NOS and protects against glutamate neurotoxicity Proc Natl Acad Sci USA 90: 9808-9812, 1993.
59. Contestabile A: Roles of NMDA receptor activity and nitric oxide production in brain development. Brain Res Rev 32: 476-509, 2000.
60. Edelman GM and Gally JA: Nitric oxide: linking space and time in the brain. Proc Natl Acad Sci USA 89: 1651-11652, 1992.
61. Dawson TM and Dawson VL: Nitric oxide actions and pathological roles. Neuroscientist 1: 9-20, 1994.
62. Bredt DS and Snyder SH: Transient NOS neurons in embryonic cerebral cortical plate, sensory ganglia and olfactory epithelium. Neuron 13: 301-313, 1994.
63. Lizosaim I, Weiner CP, Knowles RG and Moncada S: The ontogeny of cerebral and cerebellar NOS in the guinea pig and rat. Ped Res 39: 779-783, 1996.
64. Bredt SD: Molecular Characterization of NOS. Nitric Oxide in Nervous System. Ed Vincent S. Academic Press. 3-19, 1995.
65. Cai Z, Hutchins JB and Rhodes PG: Intrauterine hypoxia-ischemia alters nitric oxide synthase expression and activity in fetal and neonatal rat brain. Dev Brain Res 109: 265-269, 1998.
66. Virgili M, Monti A, Lorusso A, Bentivanti M and Contestabile A: Developmental effects of in vivo and in vitro inhibition of NOS in neurons. Brain Res 839: 164-172, 1999.
67. Peunova N, Kuzin B, Roberts I, O'Cane C and Enikolopov G: Nitric oxide cell multiplication and cell survival. Cold Spring Harb Symp Quant Biol 61: 417-426, 1996.
68. Vasa M, Breitschopf K, Zeiher AM and Dimmeler S: Nitric oxide activates telomerase and delays endothelial cell senescence. Circ Res 87: 540-542, 2000.
69. Mattson MP and Klapper W: Emerging roles for telomerase in neuronal development and apoptosis. J Neurosci Res 63: 1-9, 2001.
70. Burlakova EB, Mikjailov VF and Azurnik VK: The redox homeostasis system in radiation-induced genomic instability Radiat Biol Radioec 41: 489-499, 2001.
71. Epe B, Pflaum M, Haring M, Hegler J and Rudiger H: Use of repair endonucleases to characterize DNA damage induced by reactive oxygen species in cellular and cell free systems. Toxicol Lett 67: 57-62, 1993.
72. Narayanan P, Goodwin E and Lehnet B: Alpha particles initiates biological production of superoxide anions and hydrogen peroxides. Can Res 57: 3963-3971, 1977.
73. Riley PA: Free radicals in biology: oxidative stress and the effects of ionizing radiation. Int J Radiat Biol 65: 27-33, 1994.
74. Hall EJ: In: Radiobiology for the Radiologist. JB Lippincott Co.,Philadelphia, 1994.
75. Rugo RE, Secretan MB and Schiestl RH: X-radiation causes a persistent induction of reactive oxygen species and a delayed reintroduction of TP53 in normal human diploid fibroblasts. Rad Res 158: 210-219, 2002.
76. Tulard A, Hoffschir F, Hirrairet de Boisferon F, Luccioni C and Bravard A: Persistent oxidative stress after ionizing radiation is involved in inherited radiosensitivity. Free Rad Biol Med 35: 68-77, 2003.
77. Bump EA and Brown JM: Role of glutathione in the radiation response of mammalian cells in vitro and in vivo. Pharmacol Therap 47: 117-136, 1990.
78. Wei SJ, Botero A, Hirota K, Bradbury CM, Markovina S, Laszlo A, Spitz DR, Goswami PC, Jodoi J and Gius D: Thioredoxine nuclear translocation and interaction with redox factor-1 activates the activator protein-1 transcription factor in response to ionizing radiation. Can Res 60: 6688-6695, 2000.
79. Hsieh MM; Hegak V, Kelley MR and Deutsch WA: Activation of APE/Ref redox activity is mediated by reactive oxygen species and PKC phosphorylation. Nucleic Acids Res 29: 3116-3122, 2001.
80. Rosemberg PA, Li Y, Ali S, Altiok N, Back SA and Volpe JJ: Intracellular redox state determines whether nitric oxide is toxic or protective to rat oligodendrocytes in culture. J Neurochem 73: 476-484, 1999.
81. Canals S, Casarejo MJ, De Bernardo S, Rodriguez-Martin E and Mena MA: Nitric oxide triggers the toxicity due to glutathione depletion in mid brain cultures through 12-lipooxygenase. J Neurochem 79: 1183-1195, 2001.
82. LoBello M, Nuccetelly M, Caccuri AM, Stella L, Parker MW, Rossjorn J, Mc Kinstry WJ, Mozzi AF, Federici G, Polizio F, Pedersen JZ and Ricci G: Human glutathione transferase P1 and nitric oxide carriers. J Biol Chem 276: 42138-42145, 2001.
83. Behar TN and Colton CA: Redox regulation of neuronal migration in a Down's syndrome model. Free Rad Biol Med 35: 566-575, 2003.
84. Hainaut P and Milner J: Redox modulation of p53 conformation and sequence-specific DNA binding in vitro. Cancer Res 53: 4469-73, 1993.
85. Abate C, Luk D, Gentz R, Rauscher FJ and Curran T: Expression and purification of the leucine zipper and DNA-binding domains of Fos and Jun contact DNA directly. Proc Natl Acad Sci USA 87: 1032-1036, 1990.
86. Staal FJT, Roeder M and Herzemberg RA: Intracellular thiols regulate activation of nuclear factor κB and transcription of human immunodeficiency virus. Proc Natl Acad Sci USA 87: 9943-9947, 1990.
87. Ammendola R, Mesuraca M, Russo T and Cimino F: The DNA-binding efficiency of Sp1 is affected by redox changes. Eur J Biochem 225: 483-489, 1994.
88. Grasser FA, Lamontagne K, Whittake L, Stohr S and Lippsik JS: A highly conserved cysteine in the v-Myb DNA-binding domain is eesential for transformation and transcriptional trans-activation. Oncogene 7: 1005-1009, 1992.
89. Sun Y and Oberley L: Redox regulation of transcriptional activators. Free Rad Biol Med 21: 335-348, 1996.
90. Peranovich TMS, Da Silva AM, Fries DM, Stern A and Monteiro HP: Nitric oxide stimulate tyrosine phosphorylation in murine fibroblasts in the absence and presence of epidermal growth factor. Biochem J 305: 613-619, 1995.
91. Heo J and Campbell S: Mechanism of p21Ras S-nitrosylation and kinetics of nitric oxide-mediated guanine nucleotide exchange. Biochemistry 43: 2314-2322, 2004.
92. Kim H, Shim J, Han PL and Choi EJ: Nitric oxide modulated the c-Jun N-terminal kinase/stress activated protein kinase activity through activating c-Jun terminal kinase kinase. J Biochem 36: 13677-81, 1997.
93. Park HS, Huh SH Kim MS, Lee SH and Choi EJ: Nitric oxide negatively regulates c-Jun N-terminal kinase/stress activated protein by means of S-nitrosylation. Proc Natl Acad Sci USA 97: 14382-14387, 2000.
94. Pigazzi A, Heydrich S, Folli F, Benoit S, Michelson A and Loscalzo J: Nitric oxide inhibits thrombin receptor-activating peptide-induced phosphoinositide 3-kinase activity in human platelets. J Biol Chem 274: 14368-14375, 1999.
95. Padmaja S and Huie RR: The reaction of nitric oxide with organic peroxyl radicals. Biochem Biophys Res Comm 195: 539-544,1993.
96. Rubbo H and Freeman BA: Nitric oxide of lipid peroxidation reaction formation and analysis of nitrogen-containing oxidized lipid derivatives. Meth Enzymol 269: 385-94, 1996.
97. Rubbo H, Radi R, Anselmi D, Kirk M; Barnes S, Buttler J, Eiserich JP and Freeman BA: Nitric oxide reaction with lipid peroxyl radicals spares alpha-tocopherol during lipid peroxidation. Greater oxidant protection from the pair nitric oxide/alpha tocopherol than alpha-tocopherol/ascorbate. J Biol Chem 275: 10812-18, 2000.
98. Mohanakumar KP, Hanbauer I and Chihueh CC: Neuroprotection by nitric oxide against hydroxyl radicals induced nigral neurotoxicity. J Chem Neuroan 14: 195-205, 1998.
99. Estevez AG, Spear N, Thompson JA, Cornwell TL; Radi R, Barbeito L and Beckman JS: Nitric oxide-dependent production of cGMP supports the survival of rat embryonic motor neuron cultured with brain-derived neurotrophic factor. J Neurosc 18: 3708-3714, 1998.
100. Nichols DG and Budd SL: Mitochondria and neuronal survival. Phys Rev 80: 315-360, 2000.
101. Clementi E, Brown GC, Feelish M and Moncada S: Persistent inhibition of cell respitration by NO: crucial role of S-nitrosylation of mitochondrial compex I and protective action of glutathione. Proc Natl Acad Sci USA 95: 7631-7636, 1998.
102. Merad-Boudia M, Nicole A, Santiard-Baron B, Saille C and Ceballos-Picot I: Mitochondrial impairment as an early event in the process of apoptosis induced by glutathione depletion in neural cells: relevance to Parkinson's disease. Biochem Pharmacol 56: 645-655, 1988.
103. Cassina A and Radi R: Differential inhibitory action of NO and ONOO- in mitochondrial electron transport. Arch Biochem Biophys 328: 309-316, 1996.
104. Riobo NA, Clementi E, Melani M, Boveris A, Cadenas E, Moncada S and Poderoso J: Nitric oxide inhibits mitochondrial NADH ubiquinone reductase activity through peroxinitrite formation. Biochem J 359: 139-145, 2000.
105. Jha N, Jurma O, Lalli G, Liu Y, Pettus EIL, Greenamyre JT, Liu RM, Forman ILJ and Andersen JK: Glutathione depletion in PC12 results in selective inhibition of mitochondrial complex I activity. J Biol Chem 275: 26096-26101, 2000.
106. Mitrvic B, Ignarro LS, Montatruque S, Smoll A and Merril JE: Nitric oxide as a potential pathological mechanism in demyelination: its differential effects ion primary glial cells in vitro. Neuroscience 61: 575-585, 1994.
107. Welter R, Yu L and Yu CA: The effects of nitric oxide on electron transport complexes. Arch Biophys Biochem 331: 9-14, 1996.
108. Pearce LL, Epperly MW, Greenberger JS, Pitt BR and Peterson J: Identification of respiratory complexes I and II as mitochondrial sites of damage following exposure to ionizing radiation and NO. Nitric Oxide 5: 128-136, 2001.
109. Castro LA, Robalinho RL, Cayote A, Meneghini R and Radi R: Nitric oxide and peroxynitrite dependent aconitase inactivation and iron-regulatory protein-1 activation in mammalian fibroblasts. Arch Bioch Biophys 359: 215-224,1998.
110. Brown GC and Borutaite V: Nitric oxide inhibition of mitochondrial respiration and its role in cell death. Free Rad Biol Med 33: 1440-1450, 2002.
111. Bolanos JP, Heales SJR, Land J and Clark JB: Effect of peroxynitrite on the mitochondrial respiratory chain: differential susceptibility of neurons and astrocytes in primary cultures. J Neurochem 64: 1965-1972, 1995.
112. Brown GC and Cooper CE: Nanomolar concentrations of NO reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase. FEBS Lett 356: 295-298, 1994.
113. Lehrer-Graiwes SE, Firestein BL and Bredt BS: NO-mediated induction of cytochrome c oxidase mRNA and protein in a mouse macrophage cell line. Neurosc Lett 288: 107-110, 2000.
114. Sarti P, Giuffre A, Barone MC, Forte E, Mastronicola D and Brunori M: Nitric oxide and cytochrome oxidase: reaction mechanisms from the enzyme to the cell. Free Rad Biol Med 5: 509-520, 2003.
115. Beltran B, Mathus A, Duchen MR, Erusalinsky JD and Moncada S: The effect of NO on the cell respiration: a key to understanding its role in cell survival or death. PNAS 97: 14602-14607, 2000.
116. Tsujimoto Y and Shimizu S: Bcl-2 family: life-or-death switch. FEBS Lett 466: 6-10, 2000.
117. Brookes PS, Salinas EP, Darley-Usmar K, Eiserich JP, Freeman BA, Darley-Usmar VM and Anderson PG: Concentration-dependent effects of nitric oxide on mitochondrial permeability transition and cytochrome c release. J Biol Chem 275: 20474-20479, 2000.
118. 2+ independent permeabilization of the inner mitochondrial membrane by peroxynitrite is mediated by membrane protein thiols cross-linking and lipid peroxidation. Arch Biochem Biophys 345: 243-250, 1997.
119. Brüne B, von Knethen A and Sandau KB: Nitric oxide (NO): an effector of apoptosis. Cell Death Differ 6: 969-975, 1999.
120. Chung HT, Pae HO, Choi BM, Billiar TR and Kim YM: Nitric oxide as a bioregulator of apoptosis. Biochem Biophys Res Commun 282: 1075-1079, 2001.
121. Kim P, Zamora R, Petrosko P and Billiar T: The regulatory role of nitric oxide in apoptosis. Int Immunopharmacol 1: 1421-1441, 2001.
122. Kolb JP: Pro-and anti-apoptotic role of nitric oxide, NO. C R Acad Sci III 324: 413-424, 2001.
123. Bonfoco E, Krainc D, Ankarcrona M, Nicotera P and Lipton S: Apoptosis and necrosis: Two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci USA 92: 7162-7166, 1995.
124. Brüne B: Nitric oxide: NO apoptosis or turning it ON?. Cell Death Differ 10: 864-869, 2003.
125. L-Caspase-9 interactions in the developing nervous system: evidence for multiple death pathways. J Neurosci 21: 169-175, 2001.
126. Michelin S, Perez MR, Dubner D and Gisone P: Increased activity and involvement of caspase-3 in radiation-induced apoptosis in neural cells precursors from developing rat brain. Neurotoxicology 25: 387-398, 2004.
127. Romero AA, Gross SR, Cheng KY, Goldsmith NK and Geller HM: An age-related increase in resistance to DNA damage-induced apoptotic cell death is associated with development of DNA repair mechanisms. J Neurochem 84: 1275-1287, 2003.
128. Zhang J, Dawson VL, Dawson TM and Snyder SH: Nitric oxide activation of PARP in neurotoxicity. Science 263: 687-689, 1994.
129. Tamatani M, Ogawa S, Nutsu Y and Toyama M: Involvement of BCL-2 family and caspase-3 like protease in NO mediated neuronal apoptosis. J Neurochem 71: 1588-1596, 1998.
130. Bolaris S, Bozas E, Benekou A, Philippidis H and Stylianopoulou F: In utero radiation induced apoptosis and p53 gene expression in the developing rat brain. Int J Radiat Biol 77: 71-81, 2001.
131. Kolb JP: Mechanisms involved in the pro and anti-apoptotic role of NO in human leukemia. Leukemia 14: 1685-1695, 2000.
132. Chong MJ, Murray MR, Gosink EC, Russell HR, Srinivasan A, Kapsetaki M, Korsmeyer SJ and McKinnon PJ: Atm and Bax cooperate in ionizing radiation-induced apoptosis in the central nervous system. Proc Natl Acad Sci USA 97: 889-894, 2000.
133. Cheng A, Chant S, Milhavet O, Wang S and Mattson M: p38 MAP kinase mediates nitric oxide-induced apoptosis of neural progenitor cells. J Biol Chem 276: 43320-43327, 2001
134. Qiu JH, Asai A, Chi S, Saito H and Kirino T: Proteasome inhibitors induce cytochrome c-caspase-3-1ike protease-mediated apoptosis in cultured cortical neurons. J Neurosci 20: 259-265, 2000.
135. Li J, Billiar TR, Talanian RV and Kim IM: Nitric oxide reversibly inhibits seven members of the caspase family via S-nitrosylation. Biochem Biophys Res Commun 240: 419-424, 1997.
136. Rossig L, Fichtlscherer K, Haendeler J, Zeiher AM and Mulsch A: Nitric oxide inhibits caspase-3 by S-nitrosation in vivo. J Biol Chem 274: 6823-6826, 1999.
137. Dimmeler S, Haendeler J, Nehls M and Zeiher AM: Suppression of apoptosis by nitric oxide via inhibition of interleukin-1β -converting enzyme. J Exp Med 185: 601-608, 1997.
138. Thippeswamy T and Morris M: Cyclic guanosine 3', 5'monophosphate-mediated neuroprotection by nitric oxide in dissociated cultures of rat dorsal root ganglion neurons. Brain Res 774: 116-122, 1997.
139. Ciani E, Virgili M and Contestabile A: Akt pathway mediates a cGMP-dependent survival role of nitric oxide in cerebellar granule neurons. J Neurochem 81: 218-228, 2002.
140. Andoh T, Chiueh C and Chock P: Cyclic GMP-dependent protein kinase regulates the expression of thioredoxin and thioredoxin peroxidase-1 during hormesis in response to oxidative stress-induced apoptosis. J Biol Chem 278: 885-890, 2003.
141. Abe-Dohmae S, Harada N, Yamada K and Tanaka R: Bcl-2 gene is highly expressed during neurogenesis in the central nervous system. Biochem Biophys Res Commun 191: 915-921, 1993.
142. Dawson VL, Dawson TM, London ED, Bredt DS and Snyder SH: Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc Natl Acad Sci USA 88: 6368-6371, 1991.
143. Dawson VL, Dawson TM, Bartley DA, Uhl GR and Snyder SH: Mechanisms of nitric oxide mediated neurotoxicity in primary brain cultures. J Neurosci 13: 2651-2661, 1993.
144. Olney JW: New insights and new issues in developmental neurotoxicology. Neurotoxicology 23: 659-668, 2002.
145. Chen Q, Gong B and Almasan A: Distinct stages of cytochrome c release from mitochondria: evidence for a feedback amplification loop linking caspase activation to mitochondrial dysfunction in genotoxic stress induced apoptosis. Cell Death Differ 7: 227-233, 2000.
146. Lievre V, Becuwe P, Bianchi A, Koziel V, Franck P, Schroeder H, Nabet P, Dauca M and Daval JL: Free radical production and changes in superoxide dismutases associated with hypoxia/reoxygenation-induced apoptosis of embryonic rat forebrain in neurons in culture. Free Rad Biol Med 29: 1291-1301, 2000.