The chemistry of DNA damage from nitric oxide and peroxynitrite

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 424, Issue 1-2, 1999, Pages 37-49

  Burney, Samar ^a   Caulfield, Jennifer L ^a   Niles, Jacquin C ^a   Wishnok, John S ^a   Tannenbaum, Steven R ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

DNA damage; Nitric oxide; Peroxynitrite

Indexed keywords

NITRIC OXIDE; PEROXYNITRITE;

DEAMINATION; DNA DAMAGE; OXIDATION; PRIORITY JOURNAL; REVIEW;

EID: 0033535369     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0027-5107(99)00006-8     Document Type: Article

References (94)

1. Snyder S.H., Bredt D.S. Biological roles of nitric oxide. Sci. Am. 266:1992;68-77.
2. Gross S.S., Wolin M.S. Nitric oxide: pathophysiological mechanisms. Annu. Rev. Physiol. 57:1995;737-769.
3. Lancaster J.R. Jr. Nitric oxide in cells. Am. Sci. 80:1992;248-259.
4. MacMicking J., Xie Q., Nathan C. Nitric oxide and macrophage function. Annu. Rev. Immunol. 15:1997;323-350.
5. Moncada S., Palmer R.M.J., Higgs E.A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharm. Rev. 43:1991;109-142.
6. Nathan C. Nitric oxide as a secretory product of mammalian cells. FASEB J. 6:1992;3051-3064.
7. Stamler J.S., Singel D.J., Loscalzo J. Biochemistry of nitric oxide and its redox-activated forms. Science. 258:1992;1898-1902.
8. Tamir S., Burney S., Tannenbaum S.R. DNA damage by nitric oxide. Chem. Res. Toxicol. 9:1996;821-827.
9. Feldman P.L., Griffith O.W., Stuehr D.J. The surprising life of nitric oxide. C&EN. Dec. 20:1993;26-38.
10. Schmidt H.H., Walter U. NO at work. Cell. 78:1994;919-925.
11. Subczynski W.K., Lomnicka M., Hyde J.S. Permeability of nitric oxide through lipid bilayer membranes. Free Rad. Res. Commun. 24:1996;343-349.
12. Marletta M.A., Yoon P.S., Iyengar R., Leaf C.D., Wishnok J.S. Macrophage oxidation of L-arginine to nitrite and nitrate: nitric oxide is an intermediate. Biochemistry. 27:1988;8706-8711.
13. Marletta M.A. Mammalian synthesis of nitrite, nitrate, nitric oxide, and N-nitrosating agents. Chem. Res. Toxicol. 1:1988;249-257.
14. Hibbs J.B., Taintor R.R., Vavrin Z., Rachlin E.M. Nitric oxide: a cytotoxic activated macrophage effector molecule. Biochem. Biophys. Res. Commun. 157:1988;87-94.
15. Hibbs J.B., Vavrin Z., Taintor R.R. L-Arginine is required for expression of the activated macrophage effector mechanism causing selective metabolic inhibition in target cells. J. Immunol. 138:1987;550-565.
16. Ohshima H., Bartsch H. Chronic infections and inflammatory processes as cancer risk factors: possible role of nitric oxide in carcinogenesis. Mutat. Res. 305:1994;253-264.
17. Singer I.I., Kawka D.W., Scott S., Weidner J.R., Mumford R.A., Riehl T.E., Stenson W.F. Expression of inducible nitric oxide synthase and nitrotyrosine in colonic epithelium in inflammatory bowel disease. Gastroenterology. 111:1996;871-885.
18. Green L.C., Skipper P.L., Turesky R.J., Bryant M.S., Tannenbaum S.R. In vivo dosimetry of 4-aminobiphenyl in rats via a cysteine adduct in hemoglobin. Cancer Res. 44:1984;4254-4259.
19. Routledge M.N., Wink D.A., Keefer L.K., Dipple A. Mutations induced by saturated aqueous nitric oxide in the pSP189 supF gene in human Ad293 and E. coli MBM7070 cells. Carcinogenesis. 14:1993;1251-1254.
20. S. Christen, P. Gee, B.N. Ames, in: L. Packer (Ed.), Mutagenicity of nitric oxide in base pair-specific Salmonella tester strains: TA7000 Series, Vol. 24, Meth. Enzymol., Academic Press, San Diego, 1997, pp. 267-278.
21. Nguyen T., Brunson D., Crespi C.L., Penman B.W., Wishnok J.S., Tannenbaum S.R. DNA damage and mutation in human cells exposed to nitric oxide in vitro. Proc. Natl. Acad. Sci. USA. 89:1992;3024-3030.
22. Zhuang J.C., Wogan G.N. Growth and viability of macrophages continuously stimulated to produce nitric oxide. Proc. Natl. Acad. Sci. USA. 94:1997;11875-11880.
23. Gal A., Wogan G.N. Mutagenesis associated with nitric oxide production in transgenic SJL mice. Proc. Natl. Acad. Sci. USA. 93:1996;15102-15107.
24. Kroncke K.D., Brenner H.-H., Rodriguez M.-L., Etzkorn K., Noack E.A., Kolb H., Kolb-Bachofen V. Pancreatic islet cells are highly susceptible towards the cytotoxic effects of chemically generated nitric oxide. Biochim. Biophys. Acta. 1182:1993;221-229.
25. Ionnidis I., Groot H. Cytotoxicity of nitric oxide in Fu5 rat hepatoma cells: Evidence for co-operative action with hydrogen peroxide. Biochem. J. 296:1993;341-345.
26. Lipton S.A., Choi Y.-B., Pan Z.-H., Lei S.Z., Vincent 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.
27. Burney S., Tamir S., Gal A., Tannenbaum S.R. A mechanistic analysis of nitric oxide-induced cellular toxicity. Nitric Oxide: Biol. Chem. 1:1997;130-144.
28. Lepoivre M., Flaman J.-M., Bobe P., Lemaire G., Henry Y. Quenching of the tyrosyl free radical of ribonucleotide reductase by nitric oxide. J. Biol. Chem. 269:1994;21891-21897.
29. Zhang J., Dawson V.L., Dawson T.M., Snyder S.H. Nitric oxide activation of poly(ADP-ribose)synthetase in neurotoxicity. Science. 263:1994;687-689.
30. Szabo C., Ohshima H. DNA damage induced by peroxynitrite: subsequent biological effects. Nitric Oxide: Biol. Chem. 1:1997;373-385.
31. Tamir S., Lewis R.S., de Rojas Walker T., Deen W.M., Wishnok J.S., Tannenbaum S.R. The influence of delivery rate on the chemistry and biological effects of nitric oxide. Chem. Res. Toxicol. 6:1993;895-899.
32. Doyle M.P., Hoekstra J.W. Oxidation of nitrogen oxides by bound dioxygen in hemoproteins. J. Inorg. Biochem. 14:1981;351-358.
33. Olson J.S. Stopped-flow, rapid mixing measurements of ligand binding to hemoglobin and red cells. Meth. Enzymol. 76:1981;631-651.
34. Kwon N.S., Stuehr D.J., Nathan C.F. Inhibition of tumor cell ribonucleotide reductase by macrophage-derived nitric oxide. J. Exp. Med. 174:1991;761-767.
35. Roy B., Lepoivre M., Henry Y., Fontecave M. Inhibition of ribonucleotide reductase by nitric oxide derived from thionitrites: reversible modifications of both subunits. Biochemistry. 34:1995;5411-5418.
36. Henry Y., Ducrocq C., Drapier J.C., Servent D., Pellat C., Guissani A. Nitric oxide, a biological effector: electron paramagnetic resonance detection of nitrosyl-iron-protein complexes in whole cells. Eur. Biophys. J. 20:1991;1-15.
37. Messner U.K., Brune B. Modification of macrophage glyceraldehyde-3-phosphate dehydrogenase in response to nitric oxide. Eur. J. Pharmacol. 302:1996;171-182.
38. ̂), the only nitrogen monoxide redox form capable of activating soluble guanylyl cyclase. Biochem. Pharmacol. 51:1996;1593-1600.
39. F. Murad, U. Forstermann, M. Nakane, J. Pollock, R. Tracey, T. Matsumotot, W. Buechler, The nitric oxide-cyclic GMP signal transduction system for intracellular and intercellular communication, in: B.L. Brown, P.R.M. Dobson (Eds.), Advances in Second Messenger and Phosphoprotein Research, Vol. 13, Raven Press, New York, 1993, pp. 101-109.
40. Rubbo H., Darley-Usmar V.M., Freeman B.A. Nitric oxide regulation of tissue free radical injury. Chem. Res. Toxicol. 9:1996;809-820.
41. Stone J.R., Marletta M.A. Soluble guanylate cyclase from bovine lung: activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states. Biochemistry. 33:1994;5636-5640.
42. Hobbs A.J., Ignarro L.J. Nitric oxide-cyclic GMP signal transduction system. Meth. Enzymol. 269:1996;134-148.
43. Beckman J.S., Beckman T.W., Chen J., Marshall P.A., Freeman B.A. Apparent hydroxl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA. 87:1990;1620-1624.
44. Huie R.E., Padmaja S. The reaction of NO with superoxide. Free Rad. Res. Commun. 18:1993;195-199.
45. Beckman J.S. Oxidative damage and tyrosine nitration by peroxynitrite. Chem. Res. Toxicol. 9:1996;836-844.
46. Assreuy J., Cunha F.Q., Epperlein M.M., Noronha-Dutra A.A., O'Donnell C.A., Liew F.Y., Moncada S. Production of nitric oxide and superoxide by activated macrophages and killing of Leishmania major. Eur. J. Immunol. 24:1994;672-676.
47. Miles A.M., Bohle D.S., Glassbrenner P.A., Hansert B., Wink D.A., Grisham M.G. Modulation of superoxide-dependent oxidation and hydroxylation reactions by nitric oxide. J. Biol. Chem. 274:1996;40-47.
48. Xia Y., Dawson V.L., Dawson T.M., Snyder S.H., Zweier J.L. Nitric oxide synthase generates superoxide and nitric oxide in arginine-depleted cells leading to peroxynitrite-mediated cellular injury. Proc. Natl. Acad. Sci. USA. 93:1996;6770-6774.
49. Radi R., Beckman J.S., Bush K.M., Freeman B.A. Peroxynitrite oxidation of sulfhydryls. J. Biol. Chem. 266:1991;4244-4259.
50. Koppenol W.H., Pryor W.A., Moreno J.J., Ischiropoulos H., Beckman J.S. Peroxynitrite, a cloaked oxidant formed by nitric oxide and superoxide. Chem. Res. Toxicol. 6:1992;834-842.
51. Uppu R.M., Squadrito G.L., Pryor W.A. Acceleration of peroxynitrite oxidations by carbon dioxide. Arch. Biochem. Biophys. 327:1996;335-343.
52. Ischiropoulos H., Zhu L., Chen J., Tsai M., Martin J.C., Smith C.D., Beckman J.S. Peroxynitrite-mediated tyrosine nitration catalyzed by superoxide dismutase. Arch. Biochem. Biophys. 298:1992;431-437.
53. Beckman J.S., Ischiropoulos H., Zhu L., Van der Woerd M., Smith C., Chen J., Harrison J., Martin J.C., Tsai M. Kinetics of superoxide dismutase- and iron-catalyzed nitration of phenolics by peroxynitrite. Arch. Biochem. Biophys. 298:1992;438-445.
54. Lymar S.V., Hurst J.K. Rapid reaction between peroxonitrite ion and carbon dioxide: implications for biological activity. J. Am. Chem. Soc. 117:1995;8867-8868.
55. Lymar S.V., Jiang Q., Hurst J.K. Mechanism of carbon dioxide-catalyzed oxidation of tyrosine by peroxynitrite. Biochemistry. 35:1996;7855-7861.
56. E.D. Hughes, C.K. Ingold, J.H. Ridd, Nitrosation, diazotization, and deamination, J. Chem. Soc., (1958) 58-98.
57. Turney T.A., Wright G.A. Nitrous acid and nitrosation. Chem. Rev. 59:1959;497-513.
58. Lewis R.S., Tannenbaum S.R., Deen W.M. Kinetics of N-nitrosation in oxygenated nitric oxide solutions at physiological pH: role of nitrous anhydride and effects of phosphate and chloride. J. Am. Chem. Soc. 117:1995;3933-3939.
59. Lewis R.S., Deen W.M. Kinetics of the reaction of nitric oxide with oxygen in aqueous solutions. Chem. Res. Toxicol. 7:1994;568-574.
60. 2 reaction. Chem. Res. Toxicol. 6:1993;23-27.
61. Keshive M., Singh S., Wishnok J.S., Tannenbaum S.R., Deen W.M. Kinetics of S-nitrosation of thiols in nitric oxide solutions. Chem. Res. Toxicol. 9:1996;988-993.
62. Luperchio S., Tamir S., Tannenbaum S. NO-induced oxidative stress and glutathione metabolism in rodent and human cells. Free Rad. Biol. Med. 21:1996;513-519.
63. 2 Reaction. Chem. Res. Toxicol. 7:1994;519-525.
64. S.R. Tannenbaum, S. Tamir, T. deRojas-Walker, J.S. Wishnok, DNA damage and cytotoxicity by nitric oxide, in: R.N. Loeppky, C.J. Michejda (Eds.), Nitrosamines and Related N-Nitroso Compounds, Vol. 10, American Chemical Society, Washington, D.C., 1994, pp. 120-135.
65. Loeb L.A., Preston B.D. Mutagenesis by apurinic/apyrimidinic sites. Ann. Rev. Genet. 20:1986;201-230.
66. Lindahl T., Andersson A. Rate of chain breakage at apurinic sites in double-stranded deoxyribonucleic acid. Biochemistry. 11:1972;3618-3623.
67. Domena J.D., Timmer R.T., Dicharry S.A., Mosbaugh D.W. Purification and properties of mitochondrial uracil-DNA glycosylase from rat liver. Biochemistry. 27:1988;6742-6751.
68. Caulfield J.L., Wishnok J.S., Tannenbaum S.R. Nitric oxide-induced deamination of cytosine and guanine in deoxynucleosides and oligonucleotides. J. Biol. Chem. 273:1998;12689-12695.
69. Suzuki T., Yamaoka R., Nishi M., Ide H., Makino K. Isolation and characterization of a novel product, 2′-deoxyoxanosine, from 2′-deoxyguanosine, oligodeoxynucleotide, and calf thymus DNA treated by nitrous acid and nitric oxide. J. Am. Chem. Soc. 118:1996;2515-2516.
70. Geidushek E.P. Reversible DNA. Proc. Natl. Acad. Sci. USA. 47:1961;950-955.
71. Shapiro R., Dubelman S., Feinberg A.M., Crain P.F., McCloskey J.A. Isolation and identification of cross linked nucleosides from nitrous-acid treated deoxyribonucleic acid. J. Am. Chem. Soc. 99:1977;302-303.
72. J.L. Caulfield, The chemistry of nitric oxide-induced deamination and cross-linking of DNA, Massachusetts Institute of Technology. Ph.D. Thesis, 1997, pp. 1-153.
73. Ischiropoulos H., Zhu L., Beckman J.S. Peroxynitrite formation from macrophage-derived nitric oxide. Arch. Biochem. Biophys. 298:1992;446-451.
74. Lewis R.S., Tamir S., Tannenbaum S.R., Deen W.M. Kinetic analysis of the fate of nitric oxide synthesized by macrophages in Vitro. J. Biol. Chem. 270:1995;29350-29355.
75. deRojas-Walker T., Tamir S., Ji H., Wishnok J.S., Tannenbaum S.R. Nitric oxide induces oxidative damage in addition to deamination in macrophage DNA. Chem. Res. Toxicol. 8:1995;473-477.
76. ̂. Proc. Natl. Acad. Sci. USA. 93:1996;11499-11503.
77. Kennedy L.J., Moore K. Jr., Caulfield J.L., Tannenbaum S.R., Dedon P.C. Quantitation of 8-oxoguanine and strand breaks produced by four oxidizing agents. Chem. Res. Toxicol. 10:1997;386-392.
78. King P.A., Anderson V.E., Edwards J.O., Gustafson G., Plumb R.C., Suggs J.W. A stable solid that generates hydroxyl radical upon dissolution in aqueous solutions: Reaction with proteins and nucleic acid. J. Am. Chem. Soc. 114:1992;5430-5432.
79. Salgo M.G., Stone K., Squadrito G.L., Battista J.R., Pryor W.A. Peroxynitrite causes DNA nicks in plasmid pBR322. Biochem. Biophys. Res. Commun. 210:1995;1025-1030.
80. J. Rubio, V. Yermilov, H. Ohshima, DNA damage induced by peroxynitrite: formation of 8-nitroguanine and base propenals, in: S. Moncada, J. Stamler, S. Gross, E.A. Higgs (Eds.), The Biology of Nitric Oxide, Portland Press proceedings, London, 1996, p. 34.
81. Yermilov V., Yoshie Y., Rubio J., Ohshima H. Effects of carbon dioxide/bicarbonate on induction of DNA single-strand breaks and formation of 8-nitroguanine, 8-oxoguanine and base-propenal mediated by peroxynitrite. FEBS Lett. 399:1996;67-70.
82. Cullis P.M., Malone M.E., Merson-Davies L.A. Guanine radical cations are precursors of 7,8-dihydro-8-oxo-2′-deoxyguanosine but are not precursors of immediate strand breaks in DNA. J. Am. Chem. Soc. 118:1996;2775-2781.
83. Yermilov V., Rubio J., Becchi M., Friesen M.D., Pignatelli B., Ohshima H. Formation of 8-nitroguanine by the reaction of guanine with peroxynitrite in vitro. Carcinogenesis. 16:1995;2045-2050.
84. Eiserich J.P., Hristova M., Cross C.E., Jones A.D., Freeman B.A., Halliwell B., van der Vliet A. Formation of nitric oxide-derived inflammatory oxidants by myeloperoxidase in neutrophils. Nature. 391:1998;393-397.
85. van der Vliet A., Eiserich J.P., Halliwell B., Cross C.E. Formation of reactive nitrogen species during peroxidase-catalyzed oxidation of nitrite. A potential additional mechanism of nitric oxide-dependent toxicity. J. Biol. Chem. 272:1997;7617-7625.
86. Yermilov V., Rubio J., Ohshima H. Formation of 8-nitroguanine in DNA treated with peroxynitrite in vitro and its rapid removal from DNA by depurination. FEBS Lett. 376:1995;207-210.
87. Douki T., Cadet J. Peroxynitrite mediated oxidation of purine bases of nucleosides and isolated DNA. Free Rad. Res. 24:1996;369-380.
88. Douki T., Cadet J., Ames B.N. An adduct between peroxynitrite and 2′-deoxyguanosine:4,5-dihydro-5-hydroxy-4-(nitrosooxy)- 2′-deoxyguanosine. Chem. Res. Toxicol. 9:1996;3-7.
89. Uppu R.M., Cueto R., Squadrito G.L., Salgo M.G., Pryor W.A. Competitive reactions of peroxynitrite with 2′-deoxyguanosine and 7,8-dihydro-8-oxo-2′-deoxyguanosine (8-oxodG): relevance to the formation of 8-oxodG in DNA exposed to peroxynitrite. Free Rad. Biol. Med. 21:1996;407-411.
90. Epe B., Ballmaier D., Roussyn I., Briviba K., Sies H. DNA damage by peroxynitrite characterized with DNA repair enzymes. Nucleic Acids Res. 24:1996;4105-4110.
91. Toyokuni S., Sagripanti J.L. Iron-mediated DNA damage: sensitive detection of DNA strand breakage catalyzed by iron. J. Inorg. Biochem. 47:1992;241-248.
92. Kasai H., Yamaizumi Z., Berger M., Cadet J. Photosensitized formation of 7,8-Dihydro-8-oxo-2′-deoxyguanosine (8-hydroxy-2′-deoxyguanosine) in DNA by riboflavin - a non singlet oxygen mediated reaction. J. Am. Chem. Soc. 114:1992;9692-9694.
93. Buchko G.W., Wagner J.R., Cadet J., Raoul S., Weinfeld M. Methylene blue-mediated photooxidation of 7,8-dihydro-8-oxo-2′-deoxyguanosine. Biochim. Biophys. Acta. 1263:1995;17-24.
94. Raoul S., Cadet J. Photosensitized reaction of 8-oxo-7,8-dihydro-2′-deoxyguanosine: identification of 1-(2-deoxy-β-D-erythro-pentofuranosyl)cyanuric acid as the major singlet oxygen oxidation product. J. Am. Chem. Soc. 118:1996;1892-1898.