Nucleotides function as endogenous chemical sensors for oxidative stress signaling

Journal of Clinical Biochemistry and Nutrition

Volumn 48, Issue 1, 2011, Pages 33-39

  Ihara, Hideshi ^a   Sawa, Tomohiro ^b   Nakabeppu, Yusaku ^c   Akaike, Takaaki ^b  

^a Osaka Prefecture University   (Japan)

^b KUMAMOTO UNIVERSITY   (Japan)

^c KYUSHU UNIVERSITY   (Japan)

Author keywords

Adaptive response; Electrophilic signaling; Nucleotide sensing; Oxidative stress; ROS signaling

Indexed keywords

8 HYDROXYGUANINE; 8 NITROGUANINE; 8 NITROGUANOSINE 3',5' MONOPHOSPHATE; CELL DNA; GUANINE NUCLEOTIDE; GUANOSINE 3',5' CYCLINC MONOPHOSPHATE; KELCH LIKE ECH ASSOCIATED PROTEIN 1; REACTIVE NITROGEN SPECIES; RNA; TRANSCRIPTION FACTOR NF E2; UNCLASSIFIED DRUG;

CELL DEATH; CELL PROTECTION; CELLULAR STRESS SIGNAL; CYTOTOXICITY; ELECTROPHILICITY; ENZYME INDUCTION; HUMAN; MOLECULAR SENSOR; MUTAGENICITY; NITRATION; NITRATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PROTEIN PROCESSING; REVIEW; SECOND MESSENGER; SIGNAL TRANSDUCTION;

EID: 78650727400     PISSN: 09120009     EISSN: None     Source Type: Journal    
DOI: 10.3164/jcbn.11-003FR     Document Type: Review

References (79)

1. Griffith OW, Stuehr DJ. Nitric oxide synthases: properties and catalytic mechanism. Annu Rev Physiol 1995; 57: 707-736.
2. Murad F. Cyclic guanosine monophosphate as a mediator of vasodilation. J Clin Invest 1986; 78: 1-5.
3. Bredt DS, Hwang PM, Snyder SH. Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 1990; 347: 768-770.
4. Nathan C. Nitric oxide as a secretory product of mammalian cells. FASEB J 1992; 6: 3051-3064.
5. Patel RP, Moellering D, Murphy-Ullrich J, Jo H, Beckman JS, Darley-Usmar VM. Cell signaling by reactive nitrogen and oxygen species in atherosclerosis. Free Radic Biol Med 2000; 28: 1780-1794.
6. Madhusoodanan KS, Murad F. NO-cGMP signaling and regenerative medicine involving stem cells. Neurochem Res 2007; 32: 681-694.
7. Hare JM, Stamler JS. NO/redox disequilibrium in the failing heart and cardiovascular system. J Clin Invest 2005; 115: 509-517.
8. Ischiropoulos H, Beckman JS. Oxidative stress and nitration in neurodegeneration: cause, effect, or association? J Clin Invest 2003; 111: 163-169.
9. Nathan C, Shiloh MU. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci USA 2000; 97: 8841-8848.
10. Ohshima H, Bartsch H. Chronic infections and inflammatory processes as cancer risk factors: possible role of nitric oxide in carcinogenesis. Mutat Res 1994; 305: 253-264.
11. Sawa T, Ohshima H. Nitrative DNA damage in inflammation and its possible role in carcinogenesis. Nitric Oxide 2006; 14: 91-100.
12. Zaki MH, Akuta T, Akaike T. Nitric oxide-induced nitrative stress involved in microbial pathogenesis. J Pharmacol Sci 2005; 98: 117-129.
13. Lewis RS, Deen WM. Kinetics of the reaction of nitric oxide with oxygen in aqueous solutions. Chem Res Toxicol 1994; 7: 568-574.
14. Kissner R, Nauser T, Bugnon P, Lye PG, Koppenol WH. Formation and properties of peroxynitrite as studied by laser flash photolysis, high-pressure stopped-flow technique, and pulse radiolysis. Chem Res Toxicol 1997; 10: 1285-1292.
15. Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 1996; 271: C1424-C1437.
16. Ducrocq C, Blanchard B, Pignatelli B, Ohshima H. Peroxynitrite: an endogenous oxidizing and nitrating agent. Cell Mol Life Sci 1999; 55: 1068-1077.
17. Squadrito GL, Pryor WA. Oxidative chemistry of nitric oxide: the roles of superoxide, peroxynitrite, and carbon dioxide. Free Radic Biol Med 1998; 25: 392-403.
18. Akaike T, Noguchi Y, Ijiri S, and et al. Pathogenesis of influenza virus-induced pneumonia: involvement of both nitric oxide and oxygen radicals. Proc Natl Acad Sci USA 1996; 93: 2448-2453.
19. Sawa T, Akaike T, Maeda H. Tyrosine nitration by peroxynitrite formed from nitric oxide and superoxide generated by xanthine oxidase. J Biol Chem 2000; 275: 32467-32474.
20. Okamoto T, Akaike T, Sawa T, Miyamoto Y, van der Vliet A, Maeda H. Activation of matrix metalloproteinases by peroxynitrite-induced protein S-glutathiolation via disulfide S-oxide formation. J Biol Chem 2001; 276: 29596-29602.
21. Eiserich JP, Cross CE, Jones AD, Halliwell B, van der Vliet A. Formation of nitrating and chlorinating species by reaction of nitrite with hypochlorous acid. A novel mechanism for nitric oxide-mediated protein modification. J Biol Chem 1996; 271: 19199-19208. (Pubitemid 26271585)
22. Panasenko OM, Briviba K, Klotz LO, Sies H. Oxidative modification and nitration of human low-density lipoproteins by the reaction of hypochlorous acid with nitrite. Arch Biochem Biophys 1997; 343: 254-259. (Pubitemid 27297589)
23. Wang C, Deen WM. Nitric oxide delivery system for cell culture studies. Ann Biomed Eng 2003; 31: 65-79.
24. Brennan ML, Wu W, Fu X, and et al. A tale of two controversies: defining both the role of peroxidases in nitrotyrosine formation in vivo using eosinophil peroxidase and myeloperoxidase-deficient mice, and the nature of peroxidase-generated reactive nitrogen species. J Biol Chem 2002; 277: 17415-17427.
25. Eiserich JP, Hristova M, Cross CE, and et al. Formation of nitric oxide-derived inflammatory oxidants by myeloperoxidase in neutrophils. Nature 1998; 391: 393-397.
26. Akaike T, Okamoto S, Sawa T, and et al. 8-nitroguanosine formation in viral pneumonia and its implication for pathogenesis. Proc Natl Acad Sci USA 2003; 100: 685-690.
27. Ohshima H, Sawa T, Akaike T. 8-nitroguanine, a product of nitrative DNA damage caused by reactive nitrogen species: formation, occurrence, and implications in inflammation and carcinogenesis. Antioxid Redox Signal 2006; 8: 1033-1045.
28. Sawa T, Tatemichi M, Akaike T, Barbin A, Ohshima H. Analysis of urinary 8-nitroguanine, a marker of nitrative nucleic acid damage, by high-performance liquid chromatography-electrochemical detection coupled with immunoaffinity purification: association with cigarette smoking. Free Radic Biol Med 2006; 40: 711-720.
29. +/- mice. Carcinogenesis 2007; 28: 191-198.
30. Terasaki Y, Akuta T, Terasaki M, and et al. Guanine nitration in idiopathic pulmonary fibrosis and its implication for carcinogenesis. Am J Respir Crit Care Med 2006; 174: 665-673.
31. Yasuhara R, Miyamoto Y, Akaike T, and et al. Interleukin-1β induces death in chondrocyte-like ATDC5 cells through mitochondrial dysfunction and energy depletion in a reactive nitrogen and oxygen species-dependent manner. Biochem J 2005; 389: 315-323.
32. Yoshitake J, Akaike T, Akuta T, and et al. Nitric oxide as an endogenous mutagen for Sendai virus without antiviral activity. J Virol 2004; 78: 8709-8719.
33. Yoshitake J, Kato K, Yoshioka D, and et al. Suppression of NO production and 8-nitroguanosine formation by phenol-containing endocrine-disrupting chemicals in LPS-stimulated macrophages: involvement of estrogen receptor-dependent or -independent pathways. Nitric Oxide 2008; 18: 223-228.
34. Sawa T, Akaike T, Ichimori K, and et al. Superoxide generation mediated by 8-nitroguanosine, a highly redox-active nucleic acid derivative. Biochem Biophys Res Commun 2003; 311: 300-306.
35. Sawa T, Zaki MH, Okamoto T, and et al. Protein S-guanylation by the biological signal 8-nitroguanosine 3′,5′-cyclic monophosphate. Nat Chem Biol 2007; 3: 727-735.
36. Kasai H. Analysis of a form of oxidative DNA damage, 8-hydroxy-2′- deoxyguanosine, as a marker of cellular oxidative stress during carcinogenesis. Mutat Res 1997; 387: 147-163.
37. Sawa T, Arimoto H, Akaike T. Regulation of redox signaling involving chemical conjugation of protein thiols by nitric oxide and electrophiles. Bioconjug Chem 2010; 21: 1121-1129.
38. Nakabeppu Y, Oka S, Sheng Z, Tsuchimoto D, Sakumi K. Programmed cell death triggered by nucleotide pool damage and its prevention by MutT homolog-1 (MTH1) with oxidized purine nucleoside triphosphatase. Mutat Res 2010 DOI:10.1016/j.mrgentox.2010.06.006
39. Loft S, Vistisen K, Ewertz M, Tjønneland A, Overvad K, Poulsen HE. Oxidative DNA damage estimated by 8-hydroxydeoxyguanosine excretion in humans: influence of smoking, gender and body mass index. Carcinogenesis 1992; 13: 2241-2247.
40. Wu LL, Chiou CC, Chang PY, Wu JT. Urinary 8-OHdG: a marker of oxidative stress to DNA and a risk factor for cancer, atherosclerosis and diabetics. Clin Chim Acta 2004; 339: 1-9.
41. Seet RC, Lee CY, Lim EC, and et al. Oxidative damage in Parkinson disease: Measurement using accurate biomarkers. Free Radic Biol Med 2010; 48: 560-566.
42. 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 1995; 376: 207-210.
43. Masuda M, Nishino H, Ohshima H. Formation of 8-nitroguanosine in cellular RNA as a biomarker of exposure to reactive nitrogen species. Chem Biol Interact 2002; 139: 187-197.
44. Zaki MH, Fujii S, Okamoto T, and et al. Cytoprotective function of heme oxygenase 1 induced by a nitrated cyclic nucleotide formed during murine salmonellosis. J Immunol 2009; 182: 3746-3756.
45. Hoki Y, Murata M, Hiraku Y, and et al. 8-Nitroguanine as a potential biomarker for progression of malignant fibrous histiocytoma, a model of inflammation-related cancer. Oncol Rep 2007; 18: 1165-1169.
46. Yuasa I, Ma N, Matsubara H, Fukui Y, Uji Y. Inducible nitric oxide synthase mediates retinal DNA damage in Goto-Kakizaki rat retina. Jpn J Ophthalmol 2008; 52: 314-322.
47. Fujii S, Sawa T, Ihara H, and et al. The critical role of nitric oxide signaling, via protein S-guanylation and nitrated cyclic GMP, in the antioxidant adaptive response. J Biol Chem 2010; 285: 23970-23984.
48. Akaike T. Role of free radicals in viral pathogenesis and mutation. Rev Med Virol 2001; 11: 87-101. (Pubitemid 32267780)
49. Weitzman SA, Stossel TP. Mutation caused by human phagocytes. Science 1981; 212: 546-547.
50. Akaike T, Fujii S, Kato A, and et al. Viral mutation accelerated by nitric oxide production during infection in vivo. FASEB J 2000; 14: 1447-1454. (Pubitemid 30439754)
51. Zhuang JC, Lin C, Lin D, Wogan GN. Mutagenesis associated with nitric oxide production in macrophages. Proc Natl Acad Sci USA 1998; 95: 8286-8291. (Pubitemid 28326105)
52. Gal A, Wogan GN. Mutagenesis associated with nitric oxide production in transgenic SJL mice. Proc Natl Acad Sci USA 1996; 93: 15102-15107. (Pubitemid 27009559)
53. Jaiswal M, LaRusso NF, Burgart LJ, Gores GJ. Inflammatory cytokines induce DNA damage and inhibit DNA repair in cholangiocarcinoma cells by a nitric oxide-dependent mechanism. Cancer Res 2000; 60: 184-190. (Pubitemid 30058750)
54. Juedes MJ, Wogan GN. Peroxynitrite-induced mutation spectra of pSP189 following replication in bacteria and in human cells. Mutat Res 1996; 349: 51-61.
55. Suzuki N, Yasui M, Geacintov NE, Shafirovich V, Shibutani S. Miscoding events during DNA synthesis past the nitration-damaged base 8-nitroguanine. Biochemistry 2005; 44: 9238-9245. (Pubitemid 40943238)
56. Shafirovich V, Mock S, Kolbanovskiy A, Geacintov NE. Photochemically catalyzed generation of site-specific 8-nitroguanine adducts in DNA by the reaction of long-lived neutral guanine radicals with nitrogen dioxide. Chem Res Toxicol 2002; 15: 591-597. (Pubitemid 34326941)
57. Kaneko K, Akuta T, Sawa T, and et al. Mutagenicity of 8-nitroguanosine, a product of nitrative nucleoside modification by reactive nitrogen oxides, in mammalian cells. Cancer Lett 2008; 262: 239-247.
58. Shibutani S, Takeshita M, Grollman AP. Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature 1991; 349: 431-434. (Pubitemid 21926107)
59. Sekiguchi M, Tsuzuki T. Oxidative nucleotide damage: consequences and prevention. Oncogene 2002; 21: 8895-8904. (Pubitemid 36110820)
60. Nakabeppu Y, Sakumi K, Sakamoto K, Tsuchimoto D, Tsuzuki T, Nakatsu Y.. Mutagenesis and carcinogenesis caused by the oxidation of nucleic acids. Biol Chem 2006; 387: 373-379.
61. Toyokuni S, Tanaka T, Hattori Y, and et al. Quantitative immunohistochemical determination of 8-hydroxy-2′-deoxyguanosine by a monoclonal antibody N45.1: its application to ferric nitrilotriacetate-induced renal carcinogenesis model. Lab Invest 1997; 76: 365-374.
62. Zhang J, Perry G, Smith MA, and et al. Parkinson's disease is associated with oxidative damage to cytoplasmic DNA and RNA in substantia nigra neurons. Am J Pathol 1999; 154: 1423-1429.
63. Henderson JP, Byun J, Williams MV, and et al. Bromination of deoxycytidine by eosinophil peroxidase: a mechanism for mutagenesis by oxidative damage of nucleotide precursors. Proc Natl Acad Sci USA 2001; 98: 1631-1636.
64. Morris SM. The genetic toxicology of 5-fluoropyrimidines and 5-chlorouracil. Mutat Res 1993; 297: 39-51.
65. Nakabeppu Y, Tsuchimoto D, Furuichi M, Sakumi K. The defense mechanisms in mammalian cells against oxidative damage in nucleic acids and their involvement in the suppression of mutagenesis and cell death. Free Radic Res 2004; 38: 423-429.
66. Li X, Patel R, Melamed MR, Darzynkiewicz Z. The cell cycle effects and induction of apoptosis by 5-bromouridine in cultures of human leukaemic MOLT-4 and HL-60 cell lines and mitogen-stimulated normal lymphocytes. Cell Prolif 1994; 27: 307-319.
67. Sierakowska H, Shukla RR, Dominski Z, Kole R. Inhibition of pre-mRNA splicing by 5-fluoro-, 5-chloro-, and 5-bromouridine. J Biol Chem 1989; 264: 19185-19191.
68. Taddei F, Hayakawa H, Bouton M, and et al. Counteraction by MutT protein of transcriptional errors caused by oxidative damage. Science 1997; 278: 128-130.
69. Ohshima H, Tatemichi M, Sawa T. Chemical basis of inflammation-induced carcinogenesis. Arch Biochem Biophys 2003; 417: 3-11.
70. Saito Y, Taguchi H, Fujii S, and et al. 8-Nitroguanosines as chemical probes of the protein S-guanylation. Chem Commun 2008; 7: 5984-5986.
71. Dinkova-Kostova AT, Holtzclaw WD, Kensler TW. The role of Keap1 in cellular protective responses. Chem Res Toxicol 2005; 18: 1779-1791.
72. Motohashi H, Yamamoto M. Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol Med 2004; 10: 549-557.
73. Motterlini R, Gonzales A, Foresti R, Clark JE, Green CJ, Winslow RM. Heme oxygenase-1-derived carbon monoxide contributes to the suppression of acute hypertensive responses in vivo. Circ Res 1998; 83: 568-577.
74. Zuckerbraun BS, Billiar TR, Otterbein SL, and et al. Carbon monoxide protects against liver failure through nitric oxide-induced heme oxygenase 1. J Exp Med 2003; 198: 1707-1716.
75. Otterbein LE, Bach FH, Alam J, and et al. Carbon monoxide has antiinflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 2000; 6: 422-428.
76. Doi K, Akaike T, Fujii S, and et al. Induction of haem oxygenase-1 nitric oxide and ischaemia in experimental solid tumours and implications for tumour growth. Br J Cancer 1999; 80: 1945-1954.
77. Tanaka S, Akaike T, Fang J, and et al. Antiapoptotic effect of haem oxygenase-1 induced by nitric oxide in experimental solid tumour. Br J Cancer 2003; 88: 902-909. (Pubitemid 36520878)
78. Oka S, Ohno M, Tsuchimoto D, Sakumi K, Furuichi M, Nakabeppu Y. Two distinct pathways of cell death triggered by oxidative damage to nuclear and mitochondrial DNAs. EMBO J 2008; 27: 421-432. (Pubitemid 351161663)
79. Ichikawa J, Tsuchimoto D, Oka S, and et al. Oxidation of mitochondrial deoxynucleotide pools by exposure to sodium nitroprusside induces cell death. DNA Repair (Amst) 2008; 7: 418-430.