DNA damage induced by peroxynitrite: Subsequent biological effects

Nitric Oxide - Biology and Chemistry

Volumn 1, Issue 5, 1997, Pages 373-385

  Szabó, Csaba ^a   Ohshima, Hiroshi ^b  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

Author keywords

8 oxoguanine; 8 nitroguanine; Apoptosis; Cancer; Diabetes; DNA strand break; Endotoxin; Free radical; Inflammation; Nitric oxide; Peroxynitrite; Poly(ADP ribose) synthetase; Septic shock; Stroke; Superoxide

Indexed keywords

8 HYDROXYGUANINE; 8 NITROGUANINE; DNA; GUANINE DERIVATIVE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NITRIC OXIDE; PEROXYNITRITE; SUPEROXIDE; UNCLASSIFIED DRUG;

APOPTOSIS; CARCINOGENESIS; DNA DAMAGE; DNA STRAND BREAKAGE; ENZYME ACTIVATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW;

EID: 0031423789     PISSN: 10898603     EISSN: None     Source Type: Journal    
DOI: 10.1006/niox.1997.0143     Document Type: Review

References (107)

1. Beckman J. S., Beckman T. W., Chen J., Marshall P. A., Freeman B. A. Apparent hydroxyl radical production by peroxynitrite: Implication for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA. 87:1990;1620-1624.
2. Beckman J. S., Koppenol W. H. Nitric oxide, superoxide, and peroxynitrite: The good, the bad, and ugly. Am. J. Physiol. 271:1996;C1424-C1437.
3. Pryor W., Squadrito G. The chemistry of peroxynitrite: A product from the reaction of nitric oxide with superoxide. Am. J. Physiol. 268:1995;L699-L722.
4. Rubbo H., Radi R., Trujillo M., Telleri R., Kalyanaraman B., Barnes S., Kirk M., Freeman B. A. Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation. Formation of novel nitrogen-containing oxidized lipid derivatives. J. Biol. Chem. 269:1994;26066-26075.
5. Szabó C., Salzman A. L., Ischiropoulos H. Peroxynitrite-mediated oxidation of dihydrorhodamine 123 occurs in early stages of endotoxic and hemorrhagic shock and ischemia-reperfusion injury. FEBS Lett. 372:1995;229-232.
6. Miles A. M., Bohle D. S., Glassbrenner P. A., Hansert B., Wink D. A., Grisham M. B. Modulation of superoxide-dependent oxidation and hydroxylation reactions by nitric oxide. J. Biol. Chem. 271:1996;40-47.
7. Crow J. P., Beckman J. S. The role of peroxynitrite in nitric oxide-mediated toxicity. Curr. Top. Microbiol. Immunol. 196:1995;57-73.
8. Szabó C. The role of peroxynitrite in the pathophysiology of shock, inflammation and ischemia-reperfusion injury. Shock. 6:1996;79-88.
9. Yermilov V., Rubio J., Becchi M., Friesen M. D., Pignatelli B., Ohshima H. Formation of 8-nitroguanine by the reaction of guanine with peroxynitritein vitro. Carcinogenesis. 16:1995;2045-2050.
10. 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.
11. Koppenol W. H., Moreno J. J., Pryor W. A., Ischiropoulos H., Beckman J. S. Peroxynitrite, a cloaked oxidant formed by nitric oxide and superoxide. Chem. Res. Toxicol. 5:1992;834-842.
12. Douki T., Cadet J. Peroxynitrite mediated oxidation of purine bases of nucleosides and isolated DNA. Free Radicals Res. 24:1996;369-380.
13. J. Rubio, V. Yermilov, H. Ohshima, 1996, DNA damage induced by peroxynitrite: Formation of 8-nitroguanine and base propenals, The Biology of Nitric Oxide, 34, Portland Press proceedings, London.
14. 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.
15. Giloni L., Takeshita M., Johnson F., Iden C., Grollman A. P. Bleomycine-induced strand-scission of DNA. Mechanism of deoxyribose cleavage. J. Biol. Chem. 256:1981;8608-8615.
16. Janicek M. F., Haseltine W. A., Henner W. D. Malondialdehyde precursors in gamma-irradiated DNA, deoxynucleotides and deoxynucleosides. Nucleic Acids Res. 13:1985;9011-9029.
17. Burger R. M., Drlica K., Birdsall B. The DNA cleavage pathway of iron bleomycin. Strand scission precedes deoxyribose 3-phosphate bond cleavage. J. Biol. Chem. 269:1994;25978-25985.
18. Yermilov V., Rubio J., Ohshima H. Formation of 8-nitroguanine in DNA treated with peroxynitritein vitro. FEBS Lett. 376:1995;207-210.
19. Spencer J. P., Wong J., Jenner A., Aruoma O. I., Cross C. E., Halliwell B. Base modification and strand breakage in isolated calf thymus DNA and in DNA from human skin epidermal keratinocytes exposed to peroxynitrite or 3-morpholinosydnonimine. Chem. Res. Toxicol. 9:1996;1152-1158.
20. 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 Radical Biol. Med. 21:1996;407-411.
21. Inoue S., Kawanishi S. Oxidative DNA damage induced by simultaneous generation of nitric oxide and superoxide. FEBS Lett. 371:1995;86-88.
22. Fiala E. S., Sodum R. S., Bhattacharya M., Li H. (-)-Epigallocatechin gallate, a polyphenolic tea antioxidant, inhibits peroxynitrite-mediated formation of 8-oxodeoxyguanosine and 3-nitrotyrosine. Experientia. 52:1996;922-926.
23. 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.
24. Kennedy L. J., Moore K. Jr., Caulfild J. L., Tannenbaum S. L., Dedon P. C. Quantitation of 8-oxoguanine and strand breaks produced by four oxidizing agents. Chem. Res. Toxicol. 10:1997;386-392.
25. Hogg N., Darley Usmar V. M., Wilson M. T., Moncada S. Production of hydroxyl radicals from the simultaneous generation of superoxide and nitric oxide. Biochem. J. 281:1992;419-424.
26. 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.
27. Juedes M. J., Wogan G. N. Peroxynitrite-induced mutation spectra of pSP189 following replication in bacteria and in human cells. Mutat. Res. 349:1996;51-61.
28. 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 andE. coli. Carcinogenesis. 14:1993;1251-1254.
29. Routledge M. N., Wink D. A., Keefer L. K., Dipple A. DNA sequence changes induced by two nitric oxide donor drugs in the supF assay. Chem. Res. Toxicol. 7:1994;628-632.
30. King P. A., Anderson V. E., Edwards J. O., Gustav G., Plumb R. C., Suggs J. W. A stable solid that generates hydroxyl radical dissolutions in aqueous solutions: Reaction with proteins and nucleic acid. J. Am. Chem. Soc. 114:1992;5430-5432.
31. Groves J. T., Marla S. S. Peroxynitrite-induced DNA strand scission mediated by a manganese porphyrin. J. Am. Chem. Soc. 117:1995;9578-9579.
32. 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.
33. Roussyn I., Briviba K., Masumoto H., Sies H. Selenium-containing compounds protect DNA from single-strand breaks caused by peroxynitrite. Arch. Biochem. Biophys. 330:1996;216-218.
34. Yoshie Y., Ohshima H. Nitric oxide synergistically enhances DNA strand breakage induced by polyhydroxyaromatic compounds, but inhibits that induced by the Fenton reaction. Arch. Biochem. Biophys. 342:1997;13-21.
35. Tamir S., Burney S., Tannenbaum S. R. DNA damage by nitric oxide. Chem. Res. Toxicol. 9:1996;821-827.
36. Yoshie Y., Ohshima H. Synergistic induction of DNA strand breakage by cigarette tar and nitric oxide. Carcinogenesis. 18:1997;1359-1363.
37. Salgo M. G., Bermudez E., Squadrito G., Pryor W. DNA damage and oxidation of thiols peroxynitrite causes in rat thymocytes. Arch. Biochem. Biophys. 322:1995;500-505.
38. Gilad E., Cuzzocrea S., Zingarelli B., Salzman A. L., Szabó C. Melatonin is a scavenger of peroxynitrite. Life Sci. 60:1997;PL169-174.
39. Zingarelli B., Day B. J., Crapo J., Salzman A. L., Szabó C. The potential involvement of peroxynitrite in the pathogenesis of endotoxic shock. Br. J. Pharmacol. 120:1997;259-267.
40. Faulkner K. M., Liochev S. I., Fridowich I. Stable Mn(III) prophyrins mimic cuperoxide dismutasein vitroin vivo. J. Biol. Chem. 269:1994;23471-23476.
41. Szabó C., Day B. J., Salzman A. L. Evaluation of the relative contribution of nitric oxide and peroxynitrite to the suppression of mitochondrial respiration in immunostimulated macrophages, using a novel mesoporphyrin superoxide dismutase analog and peroxynitrite scavenger. FEBS Lett. 381:1996;82-86.
42. Kennedy M., Szabó C., Salzman A. L. Activation of poly(ADP-ribose) synthetase mediates hyperpermeability induced by peroxynitrite in human intestinal epithelial cells. Crit. Care Med. 5:1997;A68.
43. Szabó C., Zingarelli B., O'Connor M., Salzman A. L. DNA strand breakage, activation of poly-ADP ribosyl synthetase, and cellular energy depletion are involved in the cytotoxicity in macrophages and smooth muscle cells exposed to peroxynitrite. Proc. Natl. Acad. Sci. USA. 93:1996;1753-1758.
44. Szabó C., Zingarelli B., Salzman A. L. Role of poly-ADP ribosyltransferase activation in the nitric oxide- and peroxynitrite-induced vascular failure. Circ. Res. 78:1996;1051-1063.
45. Zingarelli B., O'Connor M., Wong H., Salzman A. L., Szabó C. Peroxynitrite-mediated DNA strand breakage activates poly-ADP ribosyl synthetase and causes cellular energy depletion in macrophages stimulated with bacterial lipopolysaccharide. J. Immunol. 156:1996;350-358.
46. Shulte-Frohlinde D., von Sonntag C. Radiolysis of DNA and model systems in the presence of oxygen. Sies H. Oxidative Stress. 1985;11-40 Academic Press, London.
47. Ueta K., Hayashi O. ADP-ribosylation. Annu. Rev. Biochem. 54:1985;73-100.
48. Lautier D., Lagueux J., Thiboldeau J., Menard L., Poirier G. G. Molecular and biochemical features of poly(ADP-ribose) metabolism. Mol. Cell. Biochem. 122:1993;171-193.
49. Szabó C. DNA strand breakage and activation of poly-ADP ribosyltransferase: A cytotoxic pathway triggered by peroxynitrite. Free Radical Biol. Med. 21:1996;855-869.
50. Wang Z. Q., Auer B., Stingl L., Berghammer H., Haidacher D., Schweiger M., Wagner E. F. Mice lacking ADPRT and poly(ADP-ribosyl)ation develop normally but are susceptible to skin disease. Genes Dev. 9:1995;510-520.
51. Berger S. J., Sudar D. C., Berger N. A. Metabolic consequences of DNA damage: DNA damage induces alterations in glucose metabolism by activation of poly (ADP-ribose) polymerase. Biochem. Biophys. Res. Commun. 134:1986;227-232.
52. Schraufstatter I., Hinshaw D., Hyslop P., Spragg R., Cochrane C. Oxidant injury of cells. DNA strand breaks activate polyadenosine diphosphate-ribose polymerase and lead to depletion of nicotinamide adenine dinucleotide. J. Clin. Invest. 77:1986;1312-1330.
53. Schraufstatter I. U., Hyslop P. A., Jackson J. H., Cochrane C. G. Oxidant-induced DNA damage of target cells. J. Clin. Invest. 82:1988;1040-1050.
54. Thies R. L., Autor A. P. Reactive oxygen injury to cultured pulmonary artery endothelial cells: Mediation by poly(ADP-ribose) polymerase activation causing NAD depletion and altered energy balance. Arch. Biochem. Biophys. 286:1991;353-363.
55. Berger N. A. Oxidant-induced cytotoxicity: A challenge for metabolic modulation. Am. J. Respir. Cell. Mol. Biol. 4:1991;1-3.
56. Cochrane C. G. Mechanisms of oxidant injury of cells. Mol. Aspects Med. 12:1991;137-147.
57. Szabó C., Saunders C., O'Connor M., Salzman A. L. Peroxynitrite causes energy depletion and increases permeability via activation of poly-ADP ribosyl synthetase in pulmonary epithelial cells. Am. J. Mol. Cell. Respir. Biol. 16:1997;105-109.
58. Szabó C., Cuzzocrea S., Zingarelli B., O'Connor M., Salzman A. L. Endothelial dysfunction in endotoxic shock: Importance of the activation of poly(ADP ribose) synthetase (PARS) by peroxynitrite. J. Clin. Invest. 100:1997;723-725.
59. Cuzzocrea S., Zingarelli B., Costantino G., Szabó A., Salzman A. L., Caputi A. P., Szabó C. Beneficial effects of 3-aminobenzamide, an inhibitor of poly (ADP-ribose) synthetase in a rat model of splanchnic artery occlusion and reperfusion. Br. J. Pharmacol. 121:1997;1065-1074.
60. Gilad E., Zingarelli B., Salzman A. L., Szabó C. Protection by inhibition of poly(ADP-ribose) synthetase against oxidant injury in cardiac myoblasts in vitro. J. Mol. Cell Cardiol. 1997.
61. Zingarelli B., Cuzzocrea S., Zsengeller Z., Salzman A. L., Szabó C. Beneficial effect of inhibition of poly-ADP ribose synthetase activity in myocardial ischemia-reperfusion injury. Cardiovasc. Res. 1997.
62. Thiemermann C., Bowes J., Myint F. P., Vane J. R. Inhibition of the activity of poly(ADP ribose) synthetase reduces ischemia-reperfusion injury in the heart and skeletal muscle. Proc. Natl. Acad. Sci. USA. 94:1997;679-683.
63. Szabó C., Lim L. H., Cuzzocrea S., Getting S. J., Zingarelli B., Flower R. J., Salzman A. L., Perretti M. Inhibition of poly (ADP-ribose) synthetase exerts anti-inflammatory effects and inhibits neutrophil recruitment. J. Exp. Med. 186:1997;1041-1049.
64. Radons J., Heller B., Burkle A., Hartmann B., Rodriguez M. L., Kroncke K. D., Burkart V., Kolb H. Nitric oxide toxicity in islet cells involves poly(ADP-ribose) polymerase activation and concomitant NAD depletion. Biochem. Biophys. Res. Commun. 199:1994;1270-1277.
65. Bellmann K., Wenz A., Radons J., Burkart V., Kleemann R., Kolb H. Heat shock induces resistance in rat pancreatic islet cells against nitric oxide, oxygen radicals and streptozotocin toxicityin vitro. J. Clin. Invest. 95:1995;2840-2845.
66. Heller B., Wang Z. Q., Wagner E. F., Radons J., Burkle A., Fehsel K., Burkart V., Kolb H. Inactivation of the poly(ADP-ribose) polymerase gene affects oxygen radical and nitric oxide toxicity in islet cells. J. Biol. Chem. 270:1995;11176-11180.
67. Eizirik D. L., Delaney C. A., Green M. H. L., Cunningham J. M., Thorpe J. R., Pipeleers D. G., Hellerstrom C., Green I. C. Nitric oxide donors decrease the function and survival of human pancreatic islets. Mol. Cell. Endocrinol. 118:1996;71-83.
68. 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.
69. Zhang J., Pieper A., Snyder S. H. Poly(ADP-ribose) synthetase activation: An early indicator of neurotoxic DNA damage. J. Neurochem. 65:1995;1411-1414.
70. Zhang J., Steiner J. P. Nitric oxide synthase, immunophyllins and poly(ADP-ribose) synthetase: Novel targets for the development of neuroprotective drugs. Neurol. Res. 17:1995;285-288.
71. Cosi C., Suzuki H., Milani D., Facci L., Menegazzi M., Vantini G., Kanai Y., Skaper S. D. Poly(ADP-ribose) polymerase: Early involvement in glutamate-induced neurotoxicity in cultured cerebellar granule cells. J. Neurosci. Res. 39:1994;38-46.
72. Wallis R. A., Panizzon K. L., Hanry D., Wasterlain C. G. Neuroprotection against nitric oxide injury with inhibitors of ADP-ribosylation. Neuroreport. 5:1993;245-248.
73. Didier M., Bursztajn S., Adamec E., Passani L., Nixon R. A., Coyle J. T., Wei J. Y., Berman S. A. DNA strand breaks induced by sustained glutamate excitotoxicity in primary neuronal cultures. J. Neurosci. 16:1996;2238-2250.
74. Endres M., Wang Z. Q., Namura S., Waeber C., Moskowitz M. A. Ischemic brain injury is mediated by the activation of poly (ADP-ribose) synthetase. J. Cerebral Blood Flow Metabol. 1997.
75. Denicola A., Rubbo H., Rodriguez D., Radi R. Peroxynitrite-mediated cytotoxicity toTrypanosoma cruzi. Arch. Biochem. Biophys. 304:1993;279-286.
76. Salgo M. G., Squadrito G. L., Pryor W. A. Peroxynitrite causes apoptosis in rat thymocytes. Biochem. Biophys. Res. Commun. 215:1995;1111-1118.
77. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P., Lipton S. Apoptosis and necrosis: Two distinct events induced, respectively, by mild and intense insults with NMDA or nitric oxide/superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. USA. 92:1995;7162-7166.
78. Lin K. T., Xue J. Y., Nomen M., Spur B., Wong P. Y. Peroxynitrite-induced apoptosis in HL-60 cells. J. Biol. Chem. 270:1995;16487-16490.
79. 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.
80. Kröncke K. D., Fehsel K., Kolb-Bachofen V. Nitric oxide: Cytotoxicity versus cytoprotection - How, why, when, where? Nitric Oxide Biol. Chem. 1:1997;107-120.
81. Burney S., Tamir S., Gal A., Tannenbaum S. R. A mechanistic analysis of nitric oxide induced cytotoxicity. Nitric Oxide Biol. Chem. 1:1997;130-144.
82. Monti D., Troiano L., Tropea F., Grassilli E., Cossarizza A., Barozzi D., Pelloni M. C., Tamassia M. G., Bellomo G., Francheschi C. Apoptosis - programmed cell death: A role in the aging process? Am. J. Clin. Nutr. 55:1995;1208S-1214S.
83. Nicholson D. W., All A., Thornberry N. A., Vaillancourt J. P., Ding C. K., Gallant M., Gareau Y., Griffin P. R., Labelle M., Lazebnik Y. A., Munday N. A., Raju S. M., Smulson M. E., Yamin T. T., Yu V. L., Miller D. K. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature. 376:1995;37-43.
84. Kuo M. L., Chau Y. P., Wang J. H., Shiah S. G. Inhibitors of poly(ADP-ribose) polymerase block nitric oxide-induced apoptosis but not differentiation in human leukemia HL-60 cells. Biochem. Biophys. Res. Commun. 219:1996;502-508.
85. Messmer U. K., Brune B. Nitric oxide in apoptotic cersus necrotic RAW 264.7 macrophage cell death: The role of NO-donor exposure, NAD content and p53 accumulation. Arch. Biochem. Biophys. 327:1996;1-10.
86. Messmer U. K., Reimer D. M., Reed J. C., Brune B. Nitric oxide induced poly(ADP-ribose) polymerase cleavage in RAS 264.7 macrophage apoptosis is blocked by Bcl-2. FEBS Lett. 384:1996;162-166.
87. 22. Gastroenterology. 109:1995;472-482.
88. Szabó C., O'Connor M., Salzman A. L. Nitric oxide and peroxynitrite cause DNA fragmentation in vascular smooth muscle cells. Crit. Care Med. 5:1997;A51.
89. Leist M., Single B., Künstle G., Volbracht C., Hentze H., Nicotera P. Apoptosis in the absence of poly(ADP-ribose) polymerase. Biochem. Biophys. Res. Commun. 233:1997;518-519.
90. Gordon L. I., Weitzman S. A. Review: Inflammation and cancer. Cancer J. 6:1993;257-261.
91. 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.
92. Greenblatt M. S., Bennett W. P., Hollstein M., Harris C. C. Mutations in the p53 tumor suppressor gene: Clues to cancer etiology and molecular pathogenesis. Cancer Res. 54:1994;4855-4878.
93. Pryor W. A. Biological effects of cigarette smoke, wood smoke, and the smoke from plastics: The use of electron spin resonance. Free Radical Biol. Med. 13:1992;659-676.
94. Muller T., Haussmann H. J., Schepers G. Evidence for peroxynitrite as an oxidative stress-inducing compound of aqueous cigarette smoke fractions. Carcinogenesis. 18:1997;295-301.
95. Asano K., Chee C. B., Gaston B., Lilly C. M., Gerard C., Drazen J. M., Stamler J. S. Constitutive and inducible nitric oxide synthase gene expression, regulation, and activity in human lung epithelial cells. Proc. Natl. Acad. Sci. USA. 91:1994;10089-10093.
96. Guo F. H., De Raeve H. R., Rice T. W., Stuehr D. J., Thunnissen F. B., Erzurum S. C. Continuous nitric oxide synthesis by inducible nitric oxide synthase in normal human airway epithelium in vivo. Proc. Natl. Acad. Sci. USA. 92:1995;7809-7813.
97. Yoshie Y., Ohshima H. Synergistic induction of DNA strand breakage by catecholestrogen and nitric oxide: implications for hormonal carcinogenesis. Free Rad. Biol. Med. 1997.
98. Thomsen L. L., Miles D. W., Happerfield L., Bobrow L. G., Knowles R. G., Moncada S. Nitric oxide synthase activity in human breast cancer. Br. J. Cancer. 72:1995;41-44.
99. Tschugguel W., Knogler W., Czerwenka K., Mildner M., Weninger W., Zeillinger R., Huber J. C. Presence of endothelial calcium-dependent nitric oxide synthase in breast apocrine metaplasia. Br. J. Cancer. 74:1996;1423-1426.
100. Mannick E. E., Bravo L. E., Zarama G., Realpe J. L., Zhang X. J., Ruiz B., Fontham E. T., Mera R., Miller M. J., Correa P. Inducible nitric oxide synthase, nitrotyrosine, and apoptosis inHelicobacter pylori. Cancer Res. 56:1996;3238-3243.
101. Tsuji S., Kawano S., Tsujii M., Takei Y., Tanaka M., Sawaoka H., Nagano K., Fusamoto H., Kamada T. Helicobacter pylori. Cancer Lett. 108:1996;195-200.
102. Rachmilewitz D., Karmeli F., Eliakim R., Stalnikowicz R., Ackerman Z., Amir G., Stamler J. S. Enhanced gastric nitric oxide synthase activity in duodenal ulcer patients. Gut. 35:1994;1394-1397.
103. B. Pignatelli, B. Bancel, J. Estève, C. Malaveille, S. Calmels, P. Correa, L. M. Patricot, M. Laval, N. Lyandrat, F. Smit, H. Ohshima, 1996, Helicobacter pylori, Recent Advances in Gastroenterological Carcinogenesis, E. TaharaK. SugimachiT. Oohara, 1221, 1225.
104. Boughton Smith N. K., Evans S. M., Hawkey C. J., Cole A. T., Balsitis M., Whittle B. J., Moncada S. Nitric oxide synthase activity in ulcerative colitis and Crohn's disease. Lancet. 342:1993;338-340.
105. Middleton S. J., Shorthouse M., Hunter J. O. Increased nitric oxide synthesis in ulcerative colitis. Lancet. 341:1993;465-466.
106. 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.
107. Rachmilewitz D., Stamler J. S., Karmeli F., Mullins M. E., Singel D. J., Loscalzo J., Xavier R. J., Podolsky D. K. Peroxynitrite-induced rat colitis - A new model of colonic inflammation. Gastroenterology. 105:1993;1681-1688.