Damage, repair, and mutagenesis in nuclear genes after mouse forebrain ischemia-reperfusion

Journal of Neuroscience

Volumn 16, Issue 21, 1996, Pages 6795-6806

  Liu, Philip K ^a   Hsu, Chung Y ^b   Dizdaroglu, Mirai ^c   Floyd, Robert A ^d   Kow, Yoke W ^e   Karakaya, Asuman ^c,f   Rabow, Lois E ^e   Cui, Jian K ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NATIONAL INSTITUTE OF STANDARDS AND TECHNOLOGY   (United States)

^d OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^e EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f ANKARA UNIVERSITY   (Turkey)

Author keywords

apoptosis; brain; dementia; mutation; oxidative stress; stroke

Indexed keywords

DNA; DNA GLYCOSYLTRANSFERASE; FREE RADICAL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN ISCHEMIA; CONTROLLED STUDY; DEMENTIA; DNA DAMAGE; DNA REPAIR; FOREBRAIN; GENE MUTATION; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; STROKE;

EID: 0029973192     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-21-06795.1996     Document Type: Article

References (108)

1. Akman SA, Forrest GP, Doroshow JH, Dizdaroglu M (1991) Mutation of potassium permanganate- and hydrogen peroxide-treated plasmid pZ189 replicating in CV-1 monkey kidney cells. Mutat Res 261:123-130.
2. Althaus JS, Andrus PK, Williams CM, VonVoigtlaner PF, Cazers AR, Hall ED (1993) The use of salicylate hydroxylation to detect hydroxyl radical generation in ischemic and traumatic brain injury. Mol Chem Neuropathol 20:147-162.
3. Andrus PK, Taylor BM, Sun FF, Hall ED (1994) Effects of the lipid peroxidation inhibitor tirilazad mesylate (U-74006F) on gerbil brain eicosanoid levels following ischemia and reperfusion. Brain Res 659:126-132.
4. Barone FC, Knudsen DJ, Nelson AH, Feuerstein GZ, Willette RN (1993) Mouse strain differences in susceptibility to cerebral ischemia are related to cerebral vascular anatomy. J Cereb Blood Flow Metab 13:683-692.
5. Beauchamp C, Fridovich I (1970) A mechanism for the production of ethylene from methional. J Biol Chem 245:4641-4646.
6. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and Superoxide. Proc Natl Acad Sci USA 87:1620-1624.
7. Boerrigter METI, Vijg J (1993) Studies on DNA repair defects in degenerative brain disease. Age Ageing 22:S44-S52.
8. Bohr VA, Smith CA, Okumoto DS, Hanawalt PC (1985) DNA repair in an active gene: removal of pyrimidine dimers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell 40:359-369.
9. Boiteux S, O'Connor TR, Lederer F, Gouyette A, Lavai J (1990) Homogenous Escherichia coli Fpg protein: a DNA glycosylase which excises imidazole ring-opened purines and nicks DNA at apurinic/apyrimidine sites. J Biol Chem 165:3918-3922.
10. Boiteux S, Gajewski E, Laval J, Dizdaroglu M (1992) Substrate specificity of the Escherichia coli Fpg protein (formamidopyrimidine-DNA glycosylase): excision of purine lesions in DNA produced by ionizing radiation or photosensitization. Biochemistry 31:106-110.
11. Cerutti P, Larsson R, Krupitza G, Muehlematter D, Crawford D, Amstad P (1989) Pathophysiological mechanisms of active oxygen. Mutat Res 214:81-88.
12. Chamberlain S, Lewis PD (1982) Studies of cellular hypersensitivity to ionising radiation in Friedreich's ataxia. J Neurol Neurosurg Psychiatry 45:1136-1138.
13. Chan PH, Longar S, Fishman RA (1987) Protective effects of liposome-entrapped superoxide dismutase on posttraumatic brain edema. Ann Neurol 21:540-547.
14. Chance B, Sies H, Boveris A (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev 59:527-605.
15. Chetsanga CJ, Lindahl T (1979) Release of 7-methylguanine residues whose imidazole rings have been opened from damaged DNA by a DNA glycosylase from Escherichia coli. Nucleic Acids Res 6:3673-3684.
16. Colotta F, Polentarutti N, Sironi M, Mantovani A (1992) Expression and involvement of c-fos and c-jun protooncogenes in programmed cell death induced by growth factor deprivation in lymphoid cell lines. J Biol Chem 267:18278-18283.
17. Corral-Debrinski M, Horton T, Lott MT, Shoffner JM, Beal MF, Wallace DC (1992) Mitochondrial DNA deletions in human brain: regional variability and increase with advanced age. Nature Genet 2:324-329.
18. Cortopassi GA, Shibata D, Soong N-W, Arnheim N (1992) A pattern of accumulation of a somatic deletion of mitochondrial DNA in aging human tissues. Proc Natl Acad Sci USA 89:7370-7374.
19. Crow JP, Spruell C, Chen J, Gunn C, Ischiropoulos H, Tsai M, Smith CD, Radi R, Koppenol WH, Beckman JS (1994) On the pH-dependent yield of hydroxyl radical products from peroxynitrite. Free Radic Biol Med 16:331-338.
20. Danenberg PV, Horikoshi T, Volkenandt M, Danenberg K, Lenz H-J, Shea LCC, Dicker AP, Simoneau A, Jones PA, Bertino JR (1992) Detection of point mutations in human DNA by analysis of RNA conformation polymorphism(s). Nucleic Acids Res 20:573-579,
21. Dizdaroglu M (1992) Oxidative damage to DNA in mammalian chromatin. Mutat Res 275:331-342.
22. Dizdaroglu M (1994) Chemical determination of oxidative DNA damage by gas chromatography-mass spectrometry. Methods Enzymol 234:3-16.
23. Du C, Hu R, Csernansky CA, Hsu CY, Choi DW (1996) Very delayed infarction after mild focal cerebral ischemia: a role for apoptosis? J Cereb Blood Flow Metab 16:195-201.
24. Dugan LL, Choi DW (1994) Excitotoxicity, free radicals, and cell membrane changes. Ann Neurol 35:S17-S21.
25. Dugan LL, Lin TS, He YY, Hsu CY, Choi DW (1995) Detection of free radicals by microdialysis/spin trapping EPR following focal cerebral ischemia and reperfusion and a cautionary note on the stability of 5,5-dimethyl-1-pyrroline N-oxide (DMPO). Free Radic Res 23:27-32.
26. Evans DAP, Van Der Kleij AAM, Sonnemans MAF, Burbach JPH, Van Leeuwen FW (1994) Frameshift mutations at two hotspots in vasopressin transcripts in post-mitotic neurons. Proc Natl Acad Sci USA 91:6059-6063.
27. Feig DI, Loeb LA (1993) Mechanisms of mutation by oxidative DNA damage: reduced fidelity of mammalian DNA polymerase β. Biochemistry 32:4466-4473.
28. Feig DI, Loeb LA (1994) Oxygen radical induced mutagenesis is DNA polymerase specific. J Mol Biol 235:33-41.
29. Feig DI, Sowers LC, Loeb LA (1994) Reverse chemical mutagenesis: identification of the mutagenic lesions resulting from reactive oxygen species-mediated damage to DNA. Proc Natl Acad Sci USA 91:6609-6613.
30. Floyd RA, Carney JM (1992) Free radical damage to protein and DNA: mechanisms involved and relevant observations on brain undergoing oxidative stress. Ann Neurol 32:S22-S27.
31. Fraga CG, Shigenaga MK, Park J-W, Degan P, Ames BN (1990) Oxidative damage to DNA during aging: 8-hydroxy-2′-deoxyguanosine in rat organ DNA and urine. Proc Natl Acad Sci USA 87:4533-4537.
32. Gaubatz JW, Tan BH (1994) Aging affects the levels of DNA damage in postmitotic cells. Ann NY Acad Sci 719:97-107.
33. Goate A, Chartier-Harlin M-C, Mullan M, Brown J, Crawford F, Fidani L, Giuffra L, Hanes A, Irving N, James L, Mant R, Newton P, Rooke K, Roques P, Talbot C, Pericak-Vance M, Roses A, Williamson R, Rossor M, Owen M, Hardy J (1991) Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349:704-706.
34. Grammas P, Liu G-J, Wood K, FJoyd RA (1993) Anoxia/reoxygenation induces hydroxyl free radical formation in brain microvessels. Free Radic Biol Med 14:553-557.
35. Halliwell B, Gutteridge JMC (1984) Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 219:1-14.
36. Hatahet Z, Kow YW, Purmal AA, Cunningham RP, Wallace SS (1994) New substrates for old enzymes: 5-hydroxy-2′-deoxycytidine and 5-hydroxy-2′-deoxyuridine are substrates for Escherichia coli endonuclease III and formamidopyrimidine DNA N-glycosylase, while 5-hydroxy-2′-deoxyuridine is a substrate for uracil DNA N-glycosylase. J Biol Chem 269:18814-18820.
37. Hayakawa M, Hattori K, Sugiyama S, Ozawa T (1992) Age-associated oxygen damage and mutations in mitochondrial DNA in human hearts. Biochem Biophys Res Commun 189:979-985.
38. He YY, Hsu CY, Ezrin AM, Miller MS (1993) Polyethylene glycolconjugated superoxide dismutase in focal cerebral ischemia and reperfusion. Am J Physiol 265:H252-H256.
39. Huang Z, Huang PL, Panahian N, Dalkara T, Fishman MC, Moskowitz MA (1994) Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science 265:1883-1885.
40. Huie RT, Padmaja S (1993) The reaction of NO with superoxide. Free Radic Res 18:195-199.
41. Imaizumi S, Woolworth V, Fishman RA, Chan PH (1990) Liposome-entrapped superoxide dismutase reduces cerebral infarction in cerebral ischemia in rats. Stroke 21:1312-1317.
42. Imlay JA, Linn S (1988) DNA damage and oxygen radical toxicity. Science 240:1302-1309.
43. Jaruga P, Dizdaroglu M (1996) Repair of products of oxidative DNA base damage in human cells. Nucleic Acids Res 24:1386-1394.
44. Kasai H, Crain PF, Kuchino Y, Nishimura S, Ootsuyama A, Tanooka H (1986) Formation of 8-hydroxyguanine moiety in cellular DNA by agents producing oxygen radicals and evidence for its repair. Carcinogenesis 7:1849-1851.
45. Kasprzak KS, Diwan BA, Rice JM, Misra M, Riggs CW, Olinski R, Dizdaroglu M (1992) Nickel (II)-mediated oxidative DNA base damage in renal and hepatic chromatin of pregnant rats and their fetuses: possible relevance to carcinogenesis. Chem Res Toxicol 5:809-815.
46. Kinouchi H, Epstein CJ, Mizui T, Carlson E, Chen SF, Chan PH (1991) Attenuation of focal cerebral ischemic injury in transgenic mice overexpressing CuZn superoxide dismutase. Proc Natl Acad Sci USA 88:11158-11162.
47. Kohler SW, Provost GS, Fieck A, Kretz PL, Bullock WO, Sorge JA, Putman DL, Short JM (1991) Spectra of spontaneous and mutagen-induced mutations in the lacI gene in transgenic mice. Proc Natl Acad Sci USA 88:7958-7962.
48. Kruk PA, Rampino NJ, Bohr VA (1995) DNA damage and repair in telomeres: relation to aging. Proc Natl Acad Sci USA 92:258-262.
49. Kuchino Y, Mori F, Kasai H, Inoue H, Iwai S, Miura K, Ohtsuka E, Nishimura S (1987) Misreading of DNA templates containing 8-hydroxydeoxyguanosine at the modified base and at adjacent residues. Nature 327:77-79.
50. Kunkel TA (1990) Misalignment-mediated DNA synthesis errors. Biochemistry 29:8003-8011.
51. Lavin MF, Bates P, Le Poidevin P, Chen PC (1989) Normal inhibition of DNA synthesis following γ-irradiation of radiosensitive cell lines from patients with Down's syndrome and Alzheimer's disease. Mutat Res 218:41-47.
52. Lehninger AL (1982) Electron transport, oxidative phosphorylation, and regulation of ATP production. In: Principles of Biochemistry (Anderson S, Fox J, eds), pp 467-510. New York: Worth.
53. Levy-Lahad E, Wasco W, Poorkaj P, Romano DM, Oshima J, Pettingell WH, Yu C-E, Jondro PD, Schmidt SD, Wang K, Crowley AC, Fu Y-H, Guenette SY, Galas D, Nemens E, Wijsman EM, Bird TD, Schellenberg GD, Tanzi RE (1995a) Candidate gene for the chromosome 1 familial Alzheimer's disease locus. Science 269:973-977.
54. Levy-Lahad E, Wijsman EM, Nemens E, Anderson L, Goddard KAB, Weber JL, Bird TD, Schellenberg GD (1995b) A familial Alzheimer's disease locus on chromosome 1. Science 269:970-973.
55. Li Y, Chopp M, Jiang N, Zaloga C (1995a) In situ detection of DNA fragmentation after focal cerebral ischemia in mice. Mol Brain Res 28:164-168.
56. Li Y, Sharov VG, Jiang N, Zaloga C, Sabbah HN, Chopp M (1995b) Ultrastructural and light microscopic evidence of apoptosis after middle cerebral artery occlusion in the rat. Am J Pathol 146:1045-1051.
57. Linnik MD, Zobrist RH, Hatfield MD (1993) Evidence supporting a role for programmed cell death in focal cerebral ischemia in rats. Stroke 24:2002-2008.
58. Lipton SA, Choi Y-B, Pan Z-H, Lei SZ, Chen H-SV, Sucher NJ, Loscaizo J, Singel DJ, Stamler JS (1993) A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 364:626-632.
59. Liu PK (1993) Enhanced expression of α-type DNA polymerase genes reduces AZT cytotoxicity in hamster tr5 cells. Somatic Cell Mol Genet 19:211-220.
60. 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.
61. Liu PK, Trujillo JM, Monnat Jr RJ (1993) Spectrum of spontaneous mutation in animal cells containing an aphidicolin-resistant DNA polymerase alpha. Mutat Res 288:229-236.
62. Liu PK, Kraus E, Wu TA, Strong LC, Tainsky AM (1996) Analysis of genomic instability in Li-Fraumeni fibroblasts with germline p53 mutations. Oncogene 12:2267-2278.
63. Loeb LA, Liu PK, Fry M (1986) DNA polymerase-α: enzymology, function, fidelity, and mutagenesis. Prog Nucleic Acid Res Mol Biol 33:57-110.
64. McBride OW, Kozak CA, Wilson SH (1990) Mapping of the gene for DNA polymerase β to mouse chromosome 8. Cytogenet Cell Genet 53:108-111.
65. McBride TJ, Preston BD, Loeb LA (1991) Mutagenic spectrum resulting from DNA damage by oxygen radicals. Biochemistry 30:207-213.
66. McGovern D, Webb T (1982) Sensitivity to ionising radiation of lymphocytes from Huntington's chorea patients compared to controls. J Med Genet 19:168-174.
67. Malinski T, Bailey F, Zhang ZG, Chopp M (1993) Nitric oxide measured by a prophyrinic microsensory in rat brain after transient middle cerebral artery occlusion. J Cereb Blood Flow Metab 13:355-358.
68. Marragos CM, Andrews AW, Keefer LK, Elespuru RK (1993) Mutagenicity of glyceryl trinitrate (nitroglycerin) in Salmonella typhimurium. Mutat Res 298:187-195.
69. Martin GM (1991) Genetic and environmental modulations of chromosomal stability: their roles in aging and oncogenesis. Ann NY Acad Sci 621:401-417.
70. Matsumiya N, Koehler RC, Kirsch JR, Traystman RJ (1991) Conjugated Superoxide dismutase reduces extent of caudate injury after transient focal ischemia in cats. Stroke 22:1193-1200.
71. Mazzarello P, Poloni M, Spadari S, Focher F (1992) DNA repair mechanisms in neurological diseases: facts and hypotheses. J Neurol Sci 112:4-14.
72. Mecocci P, MacGarvey U, Kaufman AE, Koontz D, Shoffner JM, Wallace DC, Beal MF (1993) Oxidative damage to mitochondrial DNA shows marked age-dependent increases in human brain. Ann Neurol 34:609-616.
73. Mellon I, Spivak G, Hanawalt PC (1987) Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell 51:241-249.
74. Moraes EC, Keyse SM, Pidoux M, Tyrrell RM (1989) The spectrum of mutations generated by passage of a hydrogen peroxide damaged shuttle vector plasmid through a mammalian host. Nucleic Acids Res 17:8301-8312.
75. Moraes EC, Keyse SM, Tyrrell RM (1990) Mutagenesis by hydrogen peroxide treatment of mammalian cells: a molecular analysis. Carcinogenesis 11:283-293.
76. Mori T, Hori Y, Dizdaroglu M (1993) DNA base damage generated in vivo in hepatic chromatin of mice upon whole body γ-irradiation. Int J Radiat Biol 64:645-650.
77. Moshell AN, Tarone RE, Barrett SF, Robbins JH (1980) Radiosensitivity in Huntington's disease: implications for pathogenesis and presymptomatic diagnosis. Lancet i:9-11.
78. Nguyen T, Brunson D, Crespi CL, Penman BW, Wishnok JS, Tannebaum SR (1992) DNA damage and mutation in human cells exposed to nitric oxide in vitro. Proc Natl Acad Sci USA 89:3030-3034.
79. Otsuka F, Tarone RE, Seguin LR, Robbins JH (1985) Hypersensitivity to ionizing radiation in cultured cells from Down's syndrome patients. J Neurol Sci 69:103-112.
80. Oury TD, Piantadosi CA, Crapo JD (1993) Cold-induced brain edema in mice. J Biol Chem 268:15394-15398.
81. Robbins JH, Otsuka F, Tarone RE, Polinsky RJ, Brumback RA, Moshell AN, Nee LE, Ganges MB, Cayeux SJ (1983) Radiosensitiviry in Alzheimer disease and Parkinson disease. Lancet i:468-469.
82. Robbins JH, Scudiero DA, Otsuka F, Tarone RE, Brumback RA, Wirtschafter JD, Polinsky RJ, Barrett SF, Moshell AN, Scarpinat RG (1984) Hypersensitivity to DNA-damaging agents in cultured cells from patients with Usher's syndrom and Duchenne muscular dystrophy. J Neurol Neurosurg Psychiatry 47:391-398.
83. Robbins JH, Brumback RA, Polinsky RJ, Wirtschafter JD, Tarone RE, Scudiero DA, Otsuka F (1985) Hypersensitivity to DNA-damaging agents in abiotrophies: a new explanation for degeneration of neurons, photoreceptors, and muscle in Alzheimer, Parkinson, and Huntington disease, retinitis pigmentosa, and Duchenne muscular dystrophy. Basic Life Sci 35:315-344.
84. Sakamoto A, Ohnishi ST, Ohnishi T, Ogawa R (1991) Relationship between free radical production and lipid peroxidation during ischemia and reperfusion injury in the rat brain. Brain Res 554:186-192.
85. Salminen A, Liu PK, Hsu CY (1995) Alteration of transcription factor binding activities in the ischemic rat brain. Biochem Biophys Res Commun 212:939-944.
86. Satoh MS, Jones CJ, Wood RD, Lindahl T (1993) DNA excision-repair defect of xeroderma pigmentosum prevents removal of a class of oxygen free radical-induced base lesions. Proc Natl Acad Sci USA 90:6335-6339.
87. Schellenberg GD, Bird TD, Wijsman EM, Orr HT, Anderson L, Nemens E, White JA, Bonnycastle L, Weber JL, Alonso ME (1992) Genetic linkage evidence for a familial Alzheimer's disease locus on chromosome 14. Science 258:668-671.
88. Schmutte C, Rideout III WM, Shen J-C, Jones PA (1994) Mutagenicity of nitric oxide is not caused by deamination of cytosine or 5-methylcytosine in double-stranded DNA. Carcinogenesis 15:2899-2903.
89. Scudiero DA, Meyer SA, Clatterbuck BE, Tarone RE, Robbins JH (1981) Hypersensitivity to N-methyl-N-nitro-N-nitrosoguanidine in fibroblasts from patients with Huntington disease, familial dysautonomia, and other primary neuronal degenerations. Proc Natl Acad Sci USA 78:6451-6455.
90. Scudiero DA, Polinsky RJ, Brumback RA, Tarone RE, Nee LE, Robbins JH (1986) Alzheimer disease fibroblasts are hypersensitive to the lethal effects of a DNA-damaging chemical. Mutat Res 159:125-131.
91. Sen S, Phillis JW (1993) Alpha-phenyl-tert-butyl-nitrone (PBN) attenuates hydroxyl radical production during ischemia and reperfusion injury of rat brain: an EPR study. Free Radic Res 19:255-265.
92. Sherrington R, Rogaev EI, Liang Y, Rogaeva EA, Levesque G, Ikeda M, Chi H, Lin C, Li G, Holman K, Tsuda T, Mar L, Foncin J-F, Bruni AC, Montesi MP, Sorbi S, Rainero I, Pinessi L, Nee L, Chumakov I, Pollen D, Brookes A, Sanseau P, Polinsky RJ, Wasco W, Da Silva HAR, Haines JL, Pericak-Vance MA, Tanzi RE, Roses AD, Fraser PE, Rommens JM, St. George-Hyslop PH (1995) Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease. Nature 375:754-760.
93. Shibutani S, Grollman AP (1993) On the mechanism of frameshift (deletion) mutagenesis in vitro. J Biol Chem 268:11703-11710.
94. Shibutani S, Takeshita M, Grollman AP (1991) Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature 349:431-434.
95. Suzuki T, Akaike N, Ueno K-I, Tanaka Y, Himori N (1995) MAO inhibitors, clorgyline and lazabemide, prevent hydroxyl radical generation caused by brain ischemia/reperfusion in mice. Pharmacology 50:357-362.
96. Tarone RE, Scudiero DA, Robbins JH (1983) Statistical methods for in vitro cell survival assays. Mutat Res 111:79-96.
97. Tarone RE, Otsuka F, Robbins JH (1984) A sensitive assay for detecting hypersensitivity to ionizing radiation in lymphoblastoid lines from patients with Duchenne muscular dystrophy and primary neuronal degenerations. J Neurol Sci 65:367-381.
98. Tchou J, Kasai H, Shibutani S, Chung M-H, Laval J, Grollman AP, Nishimura S (1991) 8-oxoguanine (8-hydroxyguanine) DNA glycosylase and its substrate specificity. Proc Natl Acad Sci USA 88:4690-4694.
99. Tkeshelashvili LK, McBride T, Spence K, Loeb LA (1991) Mutation spectrum of copper-induced DNA damage [erratum appears in (1992) J Biol Chem 267:13778]. J Biol Chem 266:6401-6406.
100. Tobi SE, Moquet JE, Edwards AA, Lloyd DC, Itzhahi RF (1990) Chromosomal radiosensitivity of lymphocytes from Alzheimer's disease patients. J Med Genet 27:437-440.
101. Tobita M, Nagano I, Nakamura S, Kogure K (1991) XXI-18. DNA single-strand breaks in postischemic gerbil brain detected by in situ nick translation. J Cereb Blood Flow Metab 11[Suppl 2]:S361.
102. Wink DA, Kasprzak KS, Maragos CM, Elespuru RK, Misra M, Dunams TM, Cebula TA, Koch WH, Andrews AW, Allen JS, Keefer LK (1991) DNA deaminating ability and genotoxicity of nitric oxide and its progenitors. Science 254:1001-1003.
103. Wink DA, Laval J (1994) The Fpg protein, a DNA repair enzyme, is inhibited by the biomediator nitric oxide in vitro and in vivo. Carcinogenesis 15:2125-2129.
104. Wood ML, Dizdaroglu M, Gajewski E, Essigmann JM (1990) Mechanistic studies of ionizing radiation and oxidative mutagenesis: genetic effects of a single 8-hydroxyguanine (7-hydro-8-oxoguanine) residue inserted at a unique site in a viral genome. Biochemistry 29:7024-7032.
105. Yamaguchi M, Hirose F, Hayashi Y, Nishimnoto Y, Matsukage A (1987) Murine DNA polymerase β gene: mapping of transcription initiation sites and the nucleotide sequence of the putative promoter region. Mol Cell Biol 7:2012-2018.
106. Yang G, Chan PH, Chen J, Carlson E, Chen SF, Weinstein P, Epstein CJ, Kamii H (1994) Human copper-zinc Superoxide dismutase transgenic mice are highly resistant to reperfusion injury after focal cerebral ischemia. Stroke 25:165-170.
107. Zhang C, Baumer A, Maxwell RJ, Linnane AW, Nagley P (1992) Multiple mitochondrial DNA deletions in an elderly human individual. FEBS Lett 297:34-38.
108. Zhang J, Dawson VL, Dawson TM, Snyder SH (1994) Nitric oxide activation of poly(ADP-ribose)synthetase in neurotoxicity. Science 263: 687-689.