Oxidative damage on RNA nucleobases

Chemical Biology of Nucleic Acids: Fundamentals and Clinical Applications

Volumn , Issue , 2014, Pages 75-94

  Küpfer, Pascal A ^a   Leumann, Christian J ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

8 Oxo guanosine; Modified RNA; Reactive oxygen species; Reverse transcription; RNA oxidation

Indexed keywords

EID: 84936811567     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-642-54452-1_5     Document Type: Chapter

References (113)

1. Aas PA, Otterlei M, Falnes PO et al (2003) Human and bacterial oxidative demethylases repair alkylation damage in both RNA and DNA. Nature 421:859-863
2. Akaike T, Fujii S, Kato A et al (2000) Viral mutation accelerated by nitric oxide production during infection in vivo. FASEB J 14:1447-1454
3. Barciszewski J, Barciszewska M, Siboska G et al (1999) Some unusual nucleic acid bases are products of hydroxyl radical oxidation of DNA and RNA. Mol Biol Rep 26:231-238
4. Basu AK, Wood ML, Niedernhofer LJ et al (1993) Mutagenic and genotoxic effects of three vinyl chloride-induced DNA lesions: 1, N6-ethenoadenine, 3, N4-ethenocytosine, and 4-amino-5-(imidazol-2-yl)imidazole. Biochemistry 32:12793-12801
5. Beckman JS, Beckman TW, Chen J et al (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci U S A 87:1620-1624
6. Bolisetty S, Jaimes E (2013) Mitochondria and reactive oxygen species: physiology and pathophysiology. Int J Mol Sci 14:6306-6344
7. Bradley-Whitman M, Lovell M (2013) Increased oxidative damage in RNA in Alzheimer’s disease progression. J Anal Bioanal Tech. doi:10.4172/2155-9872.s2-004
8. Brand MD (2010) The sites and topology of mitochondrial superoxide production. Exp Gerontol 45:466-472
9. Brawn K, Fridovich I (1981) DNA strand scission by enzymically generated oxygen radicals. Arch Biochem Biophys 206:414-419
10. Burgdorf LT, Carell T (2002) Synthesis, stability, and conformation of the formamidopyrimidine G DNA lesion. Chemistry 8:293-301
11. Burney S, Niles JC, Dedon PC et al (1999) DNA damage in deoxynucleosides and oligonucleotides treated with peroxynitrite. Chem Res Toxicol 12:513-520
12. Cadenas E, Davies KJA (2000) Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 29:222-230
13. Cadet J, Douki T, Ravanat J-L (2010) Oxidatively generated base damage to cellular DNA. Free Radic Biol Med 49:9-21
14. Calabretta A, Leumann CJ (2013) Base pairing and miscoding properties of 1, N6-ethenoadenine-and 3, N4-ethenocytosine-containing RNA oligonucleotides. Biochemistry 52:1990-1997
15. Cantara WA, Crain PF, Rozenski J et al (2011) The RNA modification database, RNAMDB: 2011 update. Nucleic Acids Res 39(suppl 1):D195-D201
16. Chang Y, Kong Q, Shan X et al (2008) Messenger RNA oxidation occurs early in disease pathogenesis and promotes motor neuron degeneration in ALS. PLoS One 3:e2849
17. Cheng KC, Cahill DS, Kasai H et al (1992) 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G→T and A→C substitutions. J Biol Chem 267:166-172
18. 15N NMR spectroscopy. Nucleic Acids Res 19:1041-1046
19. 15N nuclear magnetic resonance studies on the tautomerism of 8-hydroxy-2′-deoxyguanosine, 8-hydroxyguanosine, and other C8-substituted guanine nucleosides. Chem Res Toxicol 3:445-452
20. Crich D, Mo X-S (1997) Nucleotide C3′,4′-radical cations and the effect of a 2′-oxygen substituent. The DNA/RNA paradox. J Am Chem Soc 119:249-250
21. Cui S, Kim Y-H, Jin C-H et al (2009) Synthesis and base pairing properties of DNA-RNA heteroduplex containing 5-hydroxyuridine. BMB Rep 42:373-379
22. Dedon PC (2007) The chemical toxicology of 2-deoxyribose oxidation in DNA. Chem Res Toxicol 21:206-219
23. Defoiche J, Zhang Y, Lagneaux L et al (2009) Measurement of ribosomal RNA turnover in vivo by use of deuterium-labeled glucose. Clin Chem 55:1824-1833
24. El Ghissassi F, Barbin A, Nair J et al (1995) Formation of 1, N6-ethenoadenine and 3,-N4-ethenocytosine by lipid peroxidation products and nucleic acid bases. Chem Res Toxicol 8:278-283
25. Erlacher MD, Polacek N (2008) Ribosomal catalysis: the evolution of mechanistic concepts for peptide bond formation and peptidyl-tRNA hydrolysis. RNA Biol 5:5-12
26. Evans MD, Dizdaroglu M, Cooke MS (2004) Oxidative DNA damage and disease: induction, repair and significance. Mutat Res 567:1-61
27. Fiala ES, Conaway CC, Mathis JE (1989) Oxidative DNA and RNA damage in the livers of Sprague-Dawley rats treated with the hepatocarcinogen 2-nitropropane. Cancer Res 49:5518-5522
28. Gannett PM, Sura TP (1993) Base pairing of 8-oxoguanosine and 8-oxo-2′-deoxyguanosine with 2′-deoxyadenosine, 2′-deoxycytosine, 2′-deoxyguanosine, and thymidine. Chem Res Toxicol 6:690-700
29. Guschlbauer W, Duplaa A-M, Guy A et al (1991) Structure and in vitro replication of DNA templates containing 7,8-dihydro-8-oxoadenine. Nucleic Acids Res 19:1753-1758
30. Hangauer MJ, Vaughn IW, McManus MT (2013) Pervasive transcription of the human genome produces thousands of previously unidentified long intergenic noncoding RNAs. PLoS Genet 9:e1003569
31. Hayakawa H, Sekiguchi M (2006) Human polynucleotide phosphorylase protein in response to oxidative stress. Biochemistry 45:6749-6755
32. Hayakawa H, Hofer A, Thelander L et al (1999) Metabolic fate of oxidized guanine ribonucleotides in mammalian cells. Biochemistry 38:3610-3614
33. Hayakawa H, Kuwano M, Sekiguchi M (2001) Specific binding of 8-oxoguanine-containing RNA to polynucleotide phosphorylase protein. Biochemistry 40:9977-9982
34. Hayakawa H, Uchiumi T, Fukuda T et al (2002) Binding capacity of human YB-1 protein for RNA containing 8-oxoguanine. Biochemistry 41:12739-12744
35. Hecht SM (1994) RNA degradation by bleomycin, a naturally occurring bioconjugate. Bioconjug Chem 5:513-526
36. Hofer T, Badouard C, Bajak E et al (2005) Hydrogen peroxide causes greater oxidation in cellular RNA than in DNA. Biol Chem 386:333
37. Hofer T, Seo Arnold Y, Prudencio M et al (2006) A method to determine RNA and DNA oxidation simultaneously by HPLC-ECD: greater RNA than DNA oxidation in rat liver after doxorubicin administration. Biol Chem 387:103-111
38. Ide H, Akamatsu K, Kimura Y et al (1993) Synthesis and damage specificity of a novel probe for the detection of abasic sites in DNA. Biochemistry 32:8276-8283
39. Ishibashi T, Hayakawa H, Ito R et al (2005) Mammalian enzymes for preventing transcriptional errors caused by oxidative damage. Nucleic Acids Res 33:3779-3784
40. Ito Y, Ozawa A, Sawasaki T et al (2002) OsRALyase1, a putative F-Box protein identified in rice, Oryza sativa, with enzyme activity identical to that of wheat RALyase. Biosci Biotechnol Biochem 66:2727-2731
41. Ito R, Hayakawa H, Sekiguchi M et al (2005) Multiple enzyme activities of Escherichia coli MutT protein for sanitization of DNA and RNA precursor pools. Biochemistry 44:6670-6674
42. Kajitani K, Yamaguchi H, Dan Y et al (2006) MTH1, an oxidized purine nucleoside triphosphatase, suppresses the accumulation of oxidative damage of nucleic acids in the hippocampal microglia during kainate-induced excitotoxicity. J Neurosci 26:1688-1698
43. Kamiya H, Miura H, Murata-Kamiya N et al (1995) 8-Hydroxyadenine (7, 8-dihydro-8-oxoadenine) induces misincorporation in in vitro DNA synthesis and mutations in NIH 3T3 cells. Nucleic Acids Res 23:2893-2899
44. Karuppanapandian T, Moon J-C, Kim C et al (2011) Reactive oxygen species in plants: their generation, signal transduction, and scavenging mechanisms. Aust J Crop Sci 5:709-725
45. Kennedy LJ, Moore K, Caulfield JL et al (1997) Quantitation of 8-oxoguanine and strand breaks produced by four oxidizing agents. Chem Res Toxicol 10:386-392
46. Kim SK, Yokoyama S, Takaku H et al (1998) Oligoribonucleotides containing 8-oxo-7,8-dihydroguanosine and 8-oxo-7,8-dihydro-2′-O-methylguanosine: synthesis and base pairing properties. Bioorg Med Chem Lett 8:939-944
47. Kim SK, Kim JY, Yokoyama S et al (1999) Misreading of RNA templates containing 8-oxo-7,8-dihydroguanosine or 8-oxo-2′-O-methylguanosine in cDNA synthesis by reverse transcriptases. Nucleosides Nucleotides 18:1335-1337
48. Kim SK, Kim JY, Baek AK et al (2002) Base pairing properties of 8-oxo-7,8-dihydroadenosine in cDNA synthesis by reverse transcriptases. Bioorg Med Chem Lett 12:1977-1980
49. Kim SK, Lee SH, Kwon O-S et al (2004) DNA-RNA heteroduplex containing 8-oxo-7,8-dihydroguanosine: base pairing, structures, and thermodynamic stability. J Biochem Mol Biol 37:657-662
50. Koga Y, Taniguchi Y, Sasaki S (2013) Synthesis of the oligoribonucleotides incorporating 8-oxo-guanosine and evaluation of their base pairing properties. Nucleosides Nucleotides Nucleic Acids 32:124-136
51. Kong Q, Lin C-L (2010) Oxidative damage to RNA: mechanisms, consequences, and diseases. Cell Mol Life Sci 67:1817-1829
52. Kouchakdjian M, Bodepudi V, Shibutani S et al (1991) NMR structural studies of the ionizing radiation adduct 7-hydro-8-oxodeoxyguanosine (8-oxo-7H-dG) opposite deoxyadenosine in a DNA duplex. 8-Oxo-7H-dG(syn):dA(anti) alignment at lesion site. Biochemistry 30:1403-1412
53. Kreutzer DA, Essigmann JM (1998) Oxidized, deaminated cytosines are a source of C^T transitions in vivo. Proc Natl Acad Sci USA 95:3578-3582
54. Küpfer PA, Leumann CJ (2007) The chemical stability of abasic RNA compared to abasic DNA. Nucleic Acids Res 35:58-68
55. Küpfer PA, Leumann CJ (2011) Synthesis, base pairing properties and trans-lesion synthesis by reverse transcriptases of oligoribonucleotides containing the oxidatively damaged base 5-hydroxycytidine. Nucleic Acids Res 39:9422-9432
56. La Francois CJ, Jang YH, Cagin T et al (2000) Conformation and proton configuration of pyrimidine deoxynucleoside oxidation damage products in water. Chem Res Toxicol 13:462-470
57. Lenaz G (2012) Mitochondria and reactive oxygen species. Which role in physiology and pathology? In: Scatena R, Bottoni P, Giardina B (eds) Advances in mitochondrial medicine, vol 942, Advances in experimental medicine and biology. Springer, Dordrecht, pp 93-136
58. Leonard GA, Guy A, Brown T et al (1992) Conformation of guanine:8-oxoadenine base pairs in the crystal structure of d(CGCGAATT(O8A)GCG). Biochemistry 31:8415-8420
59. Lesko SA, Lorentzen RJ, Ts’o POP (1980) Role of superoxide in deoxyribonucleic acid strand scission. Biochemistry 19:3023-3028
60. Levine RL, Yang I-Y, Hossain M et al (2000) Mutagenesis induced by a single 1,-N6-ethenodeoxyadenosine adduct in human cells. Cancer Res 60:4098-4104
61. Li Z, Wu J, Deleo CJ (2006) RNA damage and surveillance under oxidative stress. IUBMB Life 58:581-588
62. Liu M, Gong X, Alluri Ravi K, Wu J, Sablo T, Li Z (2012) Characterization of RNA damage under oxidative stress in Escherichia coli. Biol Chem 393:123-132
63. Masuda M, Nishino H, Ohshima H (2002) Formation of 8-nitroguanosine in cellular RNA as a biomarker of exposure to reactive nitrogen species. Chem Biol Interact 139:187-197
64. Moriya M, Ou C, Bodepudi V et al (1991) Site-specific mutagenesis using a gapped duplex vector: a study of translesion synthesis past 8-oxodeoxyguanosine in E. coli. Mutat Res 254:281-288
65. Moriya M, Zhang W, Johnson F et al (1994) Mutagenic potency of exocyclic DNA adducts: marked differences between Escherichia coli and simian kidney cells. Proc Natl Acad Sci U S A 91:11899-11903
66. Nathan C, Cunningham-Bussel A (2013) Beyond oxidative stress: an immunologist’s guide to reactive oxygen species. Nat Rev Immunol 13:349-361
67. Nelson PT, Keller JN (2007) RNA in brain disease: no longer just “the messenger in the middle”. J Neuropathol Exp Neurol 66:461-468
68. Neyhart GA, Cheng C-C, Thorp HH (1995) Kinetics and mechanism of the oxidation of sugars and nucleotides by oxoruthenium(IV): model studies for predicting cleavage patterns in polymeric DNA and RNA. J Am Chem Soc 117:1463-1471
69. Nguyen KV, Burrows CJ (2011) A prebiotic role for 8-oxoguanosine as a flavin mimic in pyrimidine dimer photorepair. J Am Chem Soc 133:14586-14589
70. Nguyen KV, Burrows CJ (2012a) Photorepair of cyclobutane pyrimidine dimers by 8-oxopurine nucleosides. J Phys Org Chem 25:574-577
71. Nguyen KV, Burrows CJ (2012b) Whence flavins? Redox-active ribonucleotides link metabolism and genome repair to the RNA world. Acc Chem Res 45:2151-2159
72. Niles JC, Wishnok JS, Tannenbaum SR (2006) Peroxynitrite-induced oxidation and nitration products of guanine and 8-oxoguanine: structures and mechanisms of product formation. Nitric Oxide 14:109-121
73. Novo E, Parola M (2008) Redox mechanisms in hepatic chronic wound healing and fibrogenesis. Fibrogenesis Tissue Repair 1:5
74. Nunomura A, Hofer T, Moreira PI et al (2009) RNA oxidation in Alzheimer disease and related neurodegenerative disorders. Acta Neuropathol (Berl) 118:151-166
75. Ogasawara T, Sawasaki T, Morishita R et al (1999) A new class of enzyme acting on damaged ribosomes: ribosomal RNA apurinic site specific lyase found in wheat germ. EMBO J 18:6522-6531
76. Pacher P, Beckman JS, Liaudet L (2007) Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87:315-424
77. 2 with nonadjacent G(syn):A+(anti) mispairs. Biochemistry 38:2826-2831
78. Pandya GA, Moriya M (1996) 1, N6-ethenodeoxyadenosine, a DNA adduct highly mutagenic in mammalian cells. Biochemistry 35:11487-11492
79. Pogozelski WK, Tullius TD (1998) Oxidative strand scission of nucleic acids: routes initiated by hydrogen abstraction from the sugar moiety. Chem Rev 98:1089-1108
80. Poulsen HE, Specht E, Broedbaek K et al (2012) RNA modifications by oxidation: a novel disease mechanism? Free Radic Biol Med 52:1353-1361
81. Pryor WA (1986) Oxy-radicals and related species: their formation, lifetimes, and reactions. Annu Rev Physiol 48:657-667
82. Radi R, Peluffo G, Alvarez MN et al (2001) Unraveling peroxynitrite formation in biological systems. Free Radic Biol Med 30:463-488
83. Richter C, Park JW, Ames BN (1988) Normal oxidative damage to mitochondrial and nuclear DNA is extensive. Proc Natl Acad Sci USA 85:6465-6467
84. Salgo MG, Bermudez E, Squadrito GL et al (1995) Peroxynitrite causes DNA damage and oxidation of thiols in rat thymocytes. Arch Biochem Biophys 322:500-505
85. Schneider JE, Phillips JR, Pye Q et al (1993) Methylene blue and rose bengal photoinactivation of RNA bacteriophages: comparative studies of 8-oxoguanine formation in isolated RNA. Arch Biochem Biophys 301:91-97
86. Sekiguchi T, Ito R, Hayakawa H et al (2013) Elimination and utilization of oxidized guanine nucleotides in the synthesis of RNA and its precursors. J Biol Chem 288:8128-8135
87. Shan X, Chang Y, Lin CL (2007) Messenger RNA oxidation is an early event preceding cell death and causes reduced protein expression. FASEB J 21:2753-2764
88. Sharova LV, Sharov AA, Nedorezov T et al (2009) Database for mRNA half-life of 19977 genes obtained by DNA microarray analysis of pluripotent and differentiating mouse embryonic stem cells. DNA Res 16:45-58
89. Shen Z, Wu W, Hazen SL (2000) Activated leukocytes oxidatively damage DNA, RNA, and the nucleotide pool through halide-dependent formation of hydroxyl radical. Biochemistry 39:5474-5482
90. Shibutani S, Bodepudi V, Johnson F et al (1993) Translesional synthesis on DNA templates containing 8-oxo-7,8-dihydrodeoxyadenosine. Biochemistry 32:4615-4621
91. Srivastava SC, Raza SK, Misra R (1994) 1, N6-etheno deoxy andribo adenosine and 3, N4-etheno deoxy and ribo cytidine phosphoramidites. Strongly fluorescent structures for selective introduction in defined sequence DNA and RNA molecules. Nucleic Acids Res 22:1296-1304
92. Steenken S, Jovanovic SV (1997) How easily oxidizable is DNA? One-electron reduction potentials of adenosine and guanosine radicals in aqueous solution. J Am Chem Soc 119:617-618
93. Steenken S, Jovanovic SV, Bietti M, Bernhard K (2000) The trap depth (in DNA) of 8-oxo-7,8-dihydro-2′-deoxyguanosine as derived from electron-transfer equilibria in aqueous solution. J Am Chem Soc 122:2373-2374
94. Suen W, Spiro TG, Sowers LC et al (1999) Identification by UV resonance Raman spectroscopy of an imino tautomer of 5-hydroxy-2′-deoxycytidine, a powerful base analog transition mutagen with a much higher unfavored tautomer frequency than that of the natural residue 2′-deoxycytidine. Proc Natl Acad Sci USA 96:4500-4505
95. Szabó C, Ohshima H (1997) DNA damage induced by peroxynitrite: subsequent biological effects. Nitric Oxide 1:373-385
96. Szabó C, Ischiropoulos H, Radi R (2007) Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat Rev Drug Discov 6:662-680
97. Taddei F, Hayakawa H, Bouton M-F et al (1997) Counteraction by MutT protein of transcriptional errors caused by oxidative damage. Science 278:128-130
98. Tanaka M, Chock PB, Stadtman ER (2007) Oxidized messenger RNA induces translation errors. Proc Natl Acad Sci USA 104:66-71
99. Tanaka M, Han S, Küpfer PA et al (2011a) An assay for RNA oxidation induced abasic sites using the aldehyde reactive probe. Free Radic Res 45:237-247
100. Tanaka M, Han S, Küpfer PA et al (2011b) Quantification of oxidized levels of specific RNA species using an aldehyde reactive probe. Anal Biochem 417:142-148
101. Thorp HH (2000) The importance of being r: greater oxidative stability of RNA compared with DNA. Chem Biol 7:R33-R36
102. Tullius T, Dombroski B (1985) Iron(II) EDTA used to measure the helical twist along any DNA molecule. Science 230:679-681
103. Tullius TD, Greenbaum JA (2005) Mapping nucleic acid structure by hydroxyl radical cleavage. Curr Opin Chem Biol 9:127-134
104. Uesugi S, Ikehara M (1977) Carbon-13 magnetic resonance spectra of 8-substituted purine nucleosides. Characteristic shifts for the syn conformation. J Am Chem Soc 99:3250-3253
105. Wang D, Kreutzer DA, Essigmann JM (1998) Mutagenicity and repair of oxidative DNA damage: insights from studies using defined lesions. Mutat Res 400:99-115
106. Wood ML, Dizdaroglu M, Gajewski E et al (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
107. Wu J, Li Z (2008) Human polynucleotide phosphorylase reduces oxidative RNA damage and protects HeLa cell against oxidative stress. Biochem Biophys Res Commun 372:288-292
108. Wu J, Jiang Z, Liu M et al (2009) Polynucleotide phosphorylase protects Escherichia coli against oxidative stress. Biochemistry 48:2012-2020
109. Yanagawa H, Ogawa Y, Ueno M et al (1990) A novel minimum ribozyme with oxidoreduction activity. Biochemistry 29:10585-10589
110. Yanagawa H, Ogawa Y, Ueno M (1992) Redox ribonucleosides. Isolation and characterization of 5-hydroxyuridine, 8-hydroxyguanosine, and 8-hydroxyadenosine from Torula yeast RNA. J Biol Chem 267:13320-13326
111. Yang E, van Nimwegen E, Zavolan M et al (2003) Decay rates of human mRNAs: correlation with functional characteristics and sequence attributes. Genome Res 13:1863-1872
112. Yermilov V, Rubio J, Ohshima H (1995) Formation of 8-nitroguanine in DNA treated with peroxynitrite in vitro and its rapid removal from DNA by depurination. FEBS Lett 376:207-210
113. Yermilov V, Yoshie Y, Rubio J et al (1996) 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 399:67-70