Role of nitric oxide in genotoxicity: Implication for carcinogenesis

Cancer and Metastasis Reviews

Volumn 17, Issue 1, 1998, Pages 25-37

  Felley Bosco, Emanuela ^a,b  

^a Dpt Pharmacol and Toxicol   (Switzerland)

^b University of Lausanne Departement de Pharmacologie et de Toxicologie   (Switzerland)

Author keywords

Cancer; Inflammation; Mutations; Nitric oxide; Oxidative damage; Peroxynitrite

Indexed keywords

NITRIC OXIDE; PEROXYNITRITE;

CARCINOGENESIS; DEAMINATION; DNA STRAND BREAKAGE; GENE MUTATION; GENOTOXICITY; LIPID PEROXIDATION; MUTAGENICITY; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW;

ANIMALS; DNA DAMAGE; HUMANS; NEOPLASMS; NITRIC OXIDE;

EID: 0031923330     PISSN: 01677659     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1005948420548     Document Type: Review

References (107)

1. Gardner AW: Trauma and squamous skin cancer. The Lancet 1: 760-761, 1959
2. Collins RH, Feldman M, Fordtran JS: Colon cancer, dysplasia, and surveillance in patients with ulcerative colitis. N Engl J Med 316: 1654-1658, 1987
3. Korelitz BI: Carcinoma of the intestinal tract in Crohn's disease: results of a survey conducted by the National Foundation for Ileitis and colitis. Am J Gastroenterol 78: 44-46, 1983
4. Kantor AF, Hartge P, Hoover RN, Fraumeni JF: Epidemiological characteristics of squamous cell carcinoma and adenocarcinoma of the bladder. Cancer Res 48: 3853-3855, 1988
5. Lowenfels AB, Maisonneuve P, Cavallini G, Amman RW, Lankisch PG, Anderson JR, Dimagno EP, Andren-Sandberg A, Domellof L: Pancreatitis and the risk of pancreatic cancer. N Engl J Med 328: 1433-1437, 1993
6. Correa P: A human model of gastric carcinogenesis. Cancer Res 48: 3553-3560, 1988
7. Haswell-Elkins MR, Satrung S, Tsuda M, Mairiang E, Esumi H, Sithithaworn P, Mairiang P, Saitoh M, Yongvanit P, Elkins DB: Liver fluke infection and cholangiocarcinoma: model of endogenous nitric oxide and extragastric nitrosation in human carcinogenesis. Mutat Res 305: 241-252, 1994
8. Oshima H, Bartsch H: Chronic infections and inflammatory processes as cancer risk factors: possible role of nitric oxide in carcinogenesis. Mutat Res 305: 253-264, 1994
9. Tamir S, Tannenbaum SR: The role of nitric oxide (NO) in the carcinogenic process. BBA 1288: f31-f36, 1996
10. Liu RH, Hotchkiss: Potential genotoxicity of chronically elevated nitric oxide: a review. Mutat Res 339: 73-89, 1995
11. Arroyo PL, Hatch-Pigott V, Mower HF, Cooney RV: Mutagenicity of nitric oxide and its inhibition by antioxidants. Mutat Res 281: 193-202, 1992
12. Isomura K, Chikahira M, Teranishi K, Hamada K: Induction of mutations and chromosome aberrations in lung cells following in vivo exposure of rats to nitrogen oxides. Mutat Res 136: 119-125, 1984
13. Wink DA, Kasprzak KS, Maragos CM, Elespuru RK, Misra M, Dunams TM, Cebula TA, Koch WH, Andrews AW, Allen JS, Keefer LK: DNA deaminating ability and genotoxicity of nitric oxide and its progenitors. Science 254: 1001-1003, 1991
14. Nguyen T, Brunson D, Crespi CL, Penman BW, Wishnok JS, Tannenbaum SR: DNA damage and mutation in human cells exposed to nitric oxide in vitro. Proc Natl Acad Sci USA 89: 3030-3034, 1992
15. Tamir S, Burney S, Tannenbaum SR: DNA damage by nitric oxide. Chem Res Toxicol 9: 821-827, 1996
16. Gal A, Wogan GN: Mutagenesis associated with nitric oxide production in transgenic SJL mice. Proc Natl Acad Sci USA 93: 15102-15107, 1996
17. Merchant K, Chen H, Gonzales TC, Keefer LK, Ramsay Shaw B: Deamination of single-stranded DNA cytosine residues in aerobic nitric oxide solution at micromolar total NO exposures. Chem Res Toxicol 9: 891-896, 1996
18. Beckman JS, Koppenol WH: Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and the ugly. Am J Physiol 271: C1424-C1437, 1996
19. Ambs S, Hussain SP, Harris CC: Interactive effects of nitric oxide and the p53 tumor suppressor gene in carcinogenesis and tumor progression. Faseb J. in press
20. Routledge MN, Wink DA, Keefer LK, Dipple A: DNA sequence changes induced by two nitric oxide-donor drugs in the supF assay. Chem Res Toxicol 7: 628-632, 1994
21. Routledge MN, Wink DA, Keefer LK, Dipple A: Mutations induced by satured aqueous nitric oxide in the pSP189 supF gene in human Ad293 and E. coli MBM7070 cells. Carcinogenesis 14: 1251-1254, 1993
22. Görsdorf S, Appel KE, Engeholm C, Günter O: Nitrogen dioxide induces DNA single-strand breaks in cultured Chinese hamster cells. Carcinogenesis 11: 37-41, 1940
23. Krupitza G, Cerutti P: Poly ADP-ribosylation of histones in intact human keratinocytes. Biochem 28: 4054-4060, 1989
24. Satoh MS, Lindahl T: Role of poly(ADP-ribose) formation in DNA repair. Nature 356: 356-358, 1992
25. Christen S, Gee P, Ames BN: Mutagenicity of nitric oxide in base pair specific Salmonella tester strains: TA7000 series. In: Lester Packer (ed) Methods in Enzymology (vol 269). San Diego, Academic Press, 1996, pp 267-278
26. Schmutte C, Rideout WM, Shen J-C, Jones PA: Mutagenicity of nitric oxyde is not caused by deamination of cytosine or 5-methylcytosine in double-stranded DNA. Carcinogenesis 15: 2899-2903, 1994
27. Pacelli R, Wink DA, Cook JA, Krishna MC, DeGraff W, Friedman N, Tsokos M, Samuni A, Mitchell JB: Nitric oxide potentiates hydrogen peroxide-induced killing of Escherischia coli. J Exp Med 182: 1469-1479, 1995
28. Nunoshiba T, Rojas-Walker T, Wishnok JS, Tannenbaum SR, Demple B: Activation by nitric oxide of an oxidative-stress response that defends Escherichia coli against activated macrophages. Proc Natl Acad Sci USA 90: 9993-9997, 1993
29. Hidalgo E, Ding H, Demple B: Redox signal transduction: mutations shifting [2Fe-2s] centers of the SoxR sensor-regulator to the oxidized form. Cell 82: 121-129, 1997
30. Amabile-Cuevas CF, Demple B: Molecular characterization of the soxRS genes of Escherichia coli: two genes control a superoxide stress regulon. NAR 19: 4479-4484, 1991
31. Chou JH, Greenberg JT, Demple B: Posttranscriptional repression of Escherichia coli OmpF protein in response to redox stress: positive control of the micF antisense RNA by the soxRS locus. J Bacteriology 175: 1026-1031, 1993
32. Harris CC, Hollstein M: Clinical implications of the p53 tumor-suppressor gene. N Engl J Med 329: 1318-1327, 1993
33. Felley-Bosco E, Mirkovitch J, Ambs S, Macé K, Pfeifer A, Keefer LK, Harris CC: Nitric oxide and ethylnitrosourea: relative mutagenicity in the p53 tumor suppressor and hypoxanthine-phosphoribosyltransferase genes. Carcinogenesis 16: 2069-2074, 1995
34. Tornaletti S, Pfeifer GP: Complete and tissue-independent methylation of CpG sites in the p53 gene: implications for mutations in human cancers. Oncogene 1493-1499, 1995
35. Schmalix WA, Singh JJ, Kapfhammer P, Stadler J, Nussler AK, Geller DA, Billiar TR, Simmons RL, Greim H, Doehmer J: Stable expression of human inducible nitric oxide synthase in V79 Chinese hamster cells. Biochem Pharm 52: 1365-1374, 1996
36. Luperchio S, Tamir S, Tannenbaum SR: NO-induced oxidative stress and glutathione metabolism in rodent and human cells. Free Rad Biol Med 2: 513-519, 1996
37. Wink DA, Nims RW, Darbyshire JF, Christodoulu D, Hanbauer I, Cox GW, Laval F, Laval J, Cook JA, Krishna MC, DeGraff WG, Mitchell JB: Reaction kinetics for nitrosation of cysteine and glutathione in aerobic nitric oxide solutions at neutral pH. Insights into the fate and physiological effects of intermediates generated in the NO/O2 reaction. Chem Res Toxicol 7: 519-525, 1994
38. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA: Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 87: 1620-1624, 1990
39. Wink DA, Hanbauer I, Krishna MC, DeGraff W, Gamson J, Mitchell JB: Nitric oxide protects against cellular damage and cytotoxicity from oxygen species. Proc Natl Acad Sci USA 90: 9813-9817, 1993
40. Ischiropoulos H, Zhu L, Beckman JS: Peroxynitrite formation from macrophage-derived nitric oxide. Arch Biochem Biophys 298: 446-451, 1992
41. Zingarelli B, O'Coonor M, Wong H, Salzman AL, Szabo C: Peroxynitrite-mediated DNA strand breakage activates poly-adenosine diphosphate ribosyl synthetase and causes cellular energy depletion in macrophages stimulated with bacterial lipolysaccharide. J Immunol 156: 350-358, 1996
42. Koppenol WH, Moreno JJ, Pryor WA, Ischiropoulos H, Beckman JS: Peroxynitrite, a cloaked oxidant formed by nitric oxide and superoxide. Chem Res Toxicol 5:834-842, 1992
43. Inoue S, Kawanishi S: Oxidative damage induced by simoultaneous generation of nitric oxide and superoxide. Febs Lett 371: 86-88, 1995
44. deRojas-Walker T, Tamir S, Ji H, Wishnok JS, Tannenbaum SR: Nitric oxide induces oxidative damage in addition to deamination in macrophage DNA. Chem Res Toxicol 8: 473-477, 1995
45. Miles AM, Gibson M, Kirshna M, Cook JC, Grisham MB: Effects of superoxide on nitric oxide dependent N-nitrosation reactions. Free Rad Res 23: 379-390, 1995
46. Lewis RS, Tamir S, Tannenbaum SR, Deen WM: Kinetic analysis of the fate of nitric oxide synthesized by macrophages in vitro. J Biol Chem 270: 29350-29355, 1995
47. Weitzman SA, Stossel TP: Mutation caused by human phagocytes. Science 212: 546-547, 1981
48. Epe B, Ballmaier D, Roussyn I, Briviba K, Sies H: DNA damage by peroxinitrite characterized with DNA repair enzymes. NAR 24: 4105-4110, 1996
49. Hentze MW, Kuhn LC: Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc Natl Acad Sci USA 93: 8175-8182, 1996
50. Keyer K, Imlay JA: Superoxide accelerates DNA damage by elevating free-iron levels. Proc Natl Acad Sci USA 93: 13635-13640, 1996
51. Hausladen A, Fridovitch I: Superoxide and peroxynitrite inactivate aconitase, but nitric oxide does not. J Biol Chem 269: 29405-29408, 1994
52. Castro L, Rodriguez M, Radi R: Aconitase is readily inactivated by peroxynitrite, but not by its precursor, nitric oxide. J Biol Chem 269: 29409-29415, 1994
53. Groves JT, Marla SS: Peroxynitrite-induced DNA strand scission mediated by a manganese prophyrin. J Am Chem Soc 117: 9578-9579, 1995
54. Salgo MG, Stone K, Squadrito GL, Pryor WA: Peroxynitrite causes DNA nicks in plasmid pBR322. Biochem Biophys Res Commun 210: 1025-1030, 1995
55. Szabo C, Zingarelli B, O'Connor M, Salzman AL: DNA strand breakage, activation of poly(ADP-ribose) synthetase, and cellular energy depletion are involved in the cytotoxicity in macrophages and smooth muscle cells exposed to peroxynitrite. Proc Natl Acad Sci USA 93: 1753-1758, 1996
56. Miles AM, Bohle DS, Glassbrenner PA, Hansert B, Wink DA, Grisham MB: Modulation of superoxide-dependent oxidation and hydroxylation reactions by nitric oxide. J Biol Chem 271: 40-47, 1996
57. Uppu RM, Squadrito GL, Cueto R, Pryor WA: Selecting the most appropriate synthesis of peroxynitrite. In: Packer L (ed) Methods in Enzymology (vol 269). San Diego, Academic Press, 1996, pp 285-296
58. Amaya Y, Yamazaki KI, Sato K, Noda T, Nishimo T: Proteolytic conversion of xanthine dehydrogenase from NAD-dependent type to the O2-dependent type. J Biol Chem 265: 14170-14175, 1990
59. Cote CG, Yu F-S, Zulueta JJ, Vosatka RJ, Hassoun PM: Regulation of intracellular xanthine oxidase by endothelial-derived nitric oxide. Am J Physiol 271: L869-L874, 1996
60. Szatrowski TP, Nathan CF: Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res 51: 794-798, 1991
61. Grum CM, Ragsdale RA, Ketai LH, Simon RH: Plasma xanthine oxidase in patients with adult respiratory distress syndrome. J Crit Care 2: 22-26, 1991
62. Haddad IY, Pataki G, Hu P, Galliani C, Beckman JS, Matalon S: Quantitation of nitrotyrosine levels in lung sections of patients and animals with acute lung injury. JCI 94: 2407-2413, 1994
63. Juedes MJ, Wogan GN: Peroxynitrite-induced mutation spectra of pSP189 following replication in bacteria and in human cells. Mutat Res 349: 51-61, 1996
64. Yermilov V, Rubio J, Becchi M, Friesen MD, Pignatelli B, Oshima H: Formation of 8-nitroguanine by the reaction of guanine with peroxonitrite in vitro. Carcinogenesis 16: 2045-2050, 1995
65. Douki T, Cadet J, Ames BN: An adduct between peroxynitrite and 2′-deoxyguanosine: 4,5-dihydro-5-hydroxy-4-(nitrosooxy)-2′-deoxyguanosine.Chem Res Toxicol 9: 2-7, 1996
66. Marletta M: Mammalian synthesis of nitrite, nitrate, nitric oxide, and N-nitrosating agents. Chem Res Toxicol 1: 249-257, 1988
67. Miwa M, Stuehr DJ, Marletta MA, Wishnok JS, Tannenbaum SR: Nitrosation of amines by stimulated macrophages. Carcinogenesis 8: 955-958, 1987
68. Iyengar R, Stuehr DJ, Marletta MA: Macrophage synthesis of nitrite, nitrate, and N-nitrosamines: precursor and role of the respiratory burst. Proc Natl Acad Sci USA 84: 6369-6373, 1987
69. Kosaka H, Wishnok JS, Miwa M, Lead CD, Tannenbaum SR: Nitrosation by stimulated macrophages. Inhibitors, enhancers and substrates. Carcinogenesis 10: 563-566, 1989
70. Marnett LJ, Burcham PC: Endogenous DNA adducts: potential and paradox. Chem Res Toxicol 6: 771-785, 1993
71. Stamler JS, Karaki O, Osborne JA, Simon DI, Keaney J, Vita J, Siegel DJV RC, Loscalzo J: Nitric oxide circulates in mammalian plasma primarily as an S-nitroso adduct of serum albumin. Proc Natl Acad Sci USA 89: 7674-7677, 1992
72. Gaston H, Reilly J, Drazen JM, Fackler J, Ramdev P, Arnelle D, Mullins ME, Sugerbaker DJ, Chee C, Singel DJ, Loscalzo J, Stamler JS: Endogenous nitrogen oxides and bronchodilator S-nitrosothiols in human airways. Proc Natl Acad Sci USA 90: 10957-10961, 1993
73. Singh SP, Wishnok JS, Keshive M, Deen WM, Tannenbaum SR: The chemistry of the S-nitrosoglutathione/glulathione system. Proc Natl Acad Sci USA 93: 14428-14433, 1996
74. Lipton SA, Choi YB, Pan Z-H, Lei SZ, Chen H-SV, Sucher NJ, Loscalzo J, Singel DJ, Stamler JA: A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 364: 626-632, 1993
75. Broillet M-C, Firestein S: Direct activation of the olfactory cyclic nucleotide-gated channel through modification of sulfhydryl groups by NO compounds. Neuron 16: 377-385, 1996
76. Lander HM, Ogiste JS, Pearce SF, Levi R, Novogrodsky A: Nitric oxide-stimulated guanine nuceotide exchange on p21 ras. J Biol Chem 270: 7017-7020, 1995
77. Caselli A, Camici G, Manao G, Moneti G, Pazzagli L, Cappugi G, Ramponi G: Nitric oxide causes inactivation of the low molecular weight phosphotyrosine protein phosphatase. J Biol Chem 269: 24878-24882, 1994
78. Haijar D, Lander HM, Pearce SF, Upmacis RK, Pomerantz KB: Nitric oxide enhances prostaglandin-H synthase activity by a heme-independent mechanism: evidence implicating nitrosothiols. J Am Chem Soc 117: 3340-3346, 1995
79. Lander HM, Milbank AJ, Tauras JM, Hajjar DP, Hempstead BL, Schwartz GD, Kraemer RT, Mirza UA, Chait BT, Campbell Burk S, Quilliam LA: Redox regulation of cell signalling. Nature 381: 380-381, 1996
80. De Groote MA, Granger D, Xu Y, Campbell G, Prince R, Fang F: Genetic and redox determinants of nitric oxide cytotoxicity in a salmonella typhimurium model. Proc Natl Acad Sci USA 92: 6399-6403, 1995
81. De Groote MA, Testermann T, Xu T, Stauffer G, Fang FC: Homocysteine antagonism of nitric oxide-related cytostasis in salmonella typhimurium. Science 272: 414-417, 1996
82. Hausladen A, Privalle CT, Keng T, DeAngelo J, Stamler JS: Nitrosative stress: activation of the transcription factor OxyR. Cell 86: 719-729, 1996
83. Christman MF, Morgan RW, Jacobson FS, Ames BN: Positive control of a regulation for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cell 41: 753-762, 1985
84. Forrester K, Ambs S, Lupold SE, Kapust RB, Spillare EA, Weinberg WC, Felley-Bosco E, Wang X, Geller DA, Tzeng E, Billiar TR, Harris CC: Nitric oxide-induced p53 accumulation and regulation of inducible nitric oxide synthase expression by wild-type p53. Proc Natl Acad Sci USA 93: 2442-2447, 1996
85. Messmer UK, Ankarcrona M, Nicotera P, Brüne B: P53 expression in nitric oxide-induced apoptosis. FEBS Lett 355: 23-26, 1994
86. Messmer UK, Brüne B: Nitric oxide (NO) in apoptotic versus necrotic RAW 264.7 macrophage cell death: the role of NO-donor exposure. NAD + content, and p53 accumulation. Arch Biochem Biophys 327: 1-10, 1996
87. Muhl H, Sandau K, Brüne B, Briner VA, Pfeilschifter J: Nitric oxide donors induce apoptosis in glomerular mesangial cells, epithelial cells and endothelial cells. Europ J Pharmacol 317: 137-149, 1996
88. Green MHL: Influence of environmental and genetic factors on variation in human response to SNA damaging agents. Environ Pharmacol Toxicol 2: 151-155, 1996
89. Radi R, Beckman JS, Bush KM, Freeman BA: Peroxynitrite-induced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxide. Arch Biochem Biophys 288: 481-487, 1991
90. Bartsch H: DNA adducts in human carcinogenesis: etiological relevance and structure-activity relationship. Mutat Res 340: 67-79, 1996
91. El Ghisassi F, Barbin A, Nair J, Bartsch H: Formation of 1,N6-ethenoadenine and 3,N4-ethenocytosine by lipid peroxidation products and nucleic acid bases. Chem Res Toxicol 8: 278-283, 1995
92. Marnett LJ: Generation of mutagens during arachidonic acid metabolism. Cancer Met Rev 13: 303-308, 1994
93. Bartsch H, Barbin A, Marion MJ, Nair J, Guichard Y: Formation, detection, and role in carcinogenesis of ethenobases in DNA. Drug Metab Rev 26: 349-379, 1994
94. Eberhart CE, Coffey RJ, Radhika A, Giardiello FM, Ferrebach S, DuBois RN: Up-regulation of cyclooxygenase 2 gene expression in human colorectal adenomas and adenocarcinomas. Gastroenterol 107: 1183-1188, 1994
95. Kargman SL, O'Neill GP, Vickers PJ, Evans JF, Mancini JA, Jothi S: Expression of prostaglandin G/H synthase-1 and -2 protein in human colon cancer. Cancer Res 55: 2556-2559, 1995
96. Asai K, Kimura S, Kato H, Kondo M, Hla T: Expression of cyclooxygenase-1 and -2 in human colorectal cancer. Cancer Res 55: 3785-3789, 1995
97. Wink DA, Laval J: The Fpg protein, a DNA repair enzyme, is inhibited by the biomediator nitric oxide in vitro and in vivo. Carcinogenesis 15: 2125-2129, 1994
98. Laval J, Wink DA: Inhibition by nitric oxide of the repair protein, O6-methylguanine-DNA-methyltransferase. Carcinogenesis 15: 443-447, 1994
99. Graziewicz M, Wink DA, Laval F: Nitric oxide inhibits DNA ligase activity: potential mechanisms for NO-mediated DNA damage. Carcinogenesis 17: 2501-2505, 1996
100. Laird PW, Jaenisch R: DNA methylation and cancer. Hum Mol Genet 3: 1487-1495, 1994
101. Nedderman P, Gallinari P, Lettieri T, Schmid D, Truong O, Hsuan JJ, Wiebauer K, Jiricny J: Cloning and expression of human G/T mismatch-specific thymine-DNA glycosylase. J Biol Chem 271: 12767-12774, 1996
102. Dosanjh MK, Chenna A, Kim E, Fraenkel-Conrat H, Samson L, Singer B: Allfour known xcyclic adducts formed in DNA by the vinyl chloride metabolite chloroacetaldehyde are released by a human glycosylase. Proc Natl Acad Sci USA 91: 1024-1028, 1994
103. Jacob A, Bopp A, Hagen U: In vitro repair of single-strand breaks in gamma-irradiated DNA by polynucleotide ligase. Int J radiat Biol 22: 431-435, 1972
104. Wood RD: DNA repair in eukaryotes. Annu Rev Biochem 65: 135-167, 1996
105. Felley-Bosco E, Buzard GS, Billiar TR, Keefer LK: Nitric oxide, altered DNA, and mammalian disease. In: Aruoma OI, Halliwell B (eds) Molecular Biology of Free radicals in Human Diseases, in press
106. Dröge W, Schulze-Osthoff K, Mihm S, Galter D, Schenk H, Eck H-P, Roth S, Gmünder H: Functions of glutathione and glutathione disulfide in immunology and immunopathology. Faseb J 8: 1131-1138, 1994
107. Folkman J: Angiogenesis in cancer, vascular, rheumatoid and other disease. Nature Med 1: 27-31, 1995