Hydrogen peroxide causes greater oxidation in cellular RNA than in DNA
-
Tim Hofer
, Carine Badouard , Edyta Bajak , Jean-Luc Ravanat , Åse Mattsson und Ian A. Cotgreave
Abstract
Human A549 lung epithelial cells were challenged with 18O-labeled hydrogen peroxide ([18O]-H2O2), the total RNA and DNA extracted in parallel, and analyzed for 18O-labeled 8-oxo-7,8-dihydroguanosine ([18O]-8-oxoGuo) and 8-oxo-7,8-dihydro-2′-deoxyguanosine ([18O]-8-oxodGuo) respectively, using high-performance liquid chromatography electrospray ionization tandem mass spectrometry (HPLC-MS/MS). [18O]-H2O2 exposure resulted in dose-response formation of both [18O]-8-oxoGuo and [18O]-8-oxodGuo and 18O-labeling of guanine in RNA was 14–25 times more common than in DNA. Kinetics of formation and subsequent removal of oxidized nucleic acids adducts were also monitored up to 24 h. The A549 showed slow turnover rates of adducts in RNA and DNA giving half-lives of approximately 12.5 h for [18O]-8-oxoGuo in RNA and 20.7 h for [18O]-8-oxodGuo in DNA, respectively.
References
Aas, P.A., Otterlei, M., Falnes, P.Ø., Vågbø, C.B., Skorpen, F., Akbari, M., Sundheim, O., Bjørås, M., Slupphaug, G., Seeberg, E., and Krokan, H.E. (2003). Human and bacterial oxidative demethylases repair alkylation damage in both RNA and DNA. Nature421, 859–863.10.1038/nature01363Suche in Google Scholar
Bray, W.C. and Gorin, M.H. (1932). Ferryl ion, a compound of tetravalent iron. J. Am. Chem. Soc.54, 2124–2125.10.1021/ja01344a505Suche in Google Scholar
Culp, S.J., Cho, B.P., Kadlubar, F.F., and Evans, F.E. (1989). Structural and conformational analyses of 8-hydroxy-2′-deoxyguanosine. Chem. Res. Toxicol.2, 416–422.10.1021/tx00012a010Suche in Google Scholar
Dandrea, T., Hellmold, H., Jonsson, C., Zhivotovsky, B., Hofer, T., Wärngard, L., and Cotgreave, I. (2004). The transcriptosomal response of human A549 lung cells to a hydrogen peroxide-generating system: relationship to DNA damage, cell cycle arrest, and caspase activation. Free Radic. Biol. Med.36, 881–896.10.1016/j.freeradbiomed.2003.12.014Suche in Google Scholar
Dani, S.U. (1997). Molecular turnover and aging. In: Principles of Neural Aging, S.U. Dani, A. Hori, and G.F. Walter, eds. (Amsterdam, The Netherlands: Elsevier).Suche in Google Scholar
De Zwart, L.L., Meerman, J.H.N., Commandeur, J.N.M., and Vermeulen, N.P.E. (1999). Biomarkers of free radical damage applications in experimental animals and in humans. Free Radic. Biol. Med.26, 202–226.10.1016/S0891-5849(98)00196-8Suche in Google Scholar
Downes, A. and Blunt, T.P. (1879). The effect of sunlight upon hydrogen peroxide. Nature20, 521.Suche in Google Scholar
Fenton, H.J.H. (1876). On a new reaction of tartaric acid. Chem. News33, 190.Suche in Google Scholar
Fenton, H.J.H. (1894). Oxidation of tartaric acid in presence of iron. J. Chem. Soc. Trans.65, 899–910.10.1039/CT8946500899Suche in Google Scholar
Fiala, E.S., Conaway, C.C., and Mathis, J.E. (1989). Oxidative DNA and RNA damage in the livers of Sprague-Dawley rats treated with the hepatocarcinogen 2-nitropropane. Cancer Res.49, 5518–5522.Suche in Google Scholar
Finkel, T. and Holbrook, N.J. (2000). Oxidants, oxidative stress and the biology of ageing. Nature408, 239–247.10.1038/35041687Suche in Google Scholar PubMed
Frelon, S., Douki, T., Ravanat, J.-L., Pouget, J.-P., Tornabene, C., and Cadet, J. (2000). High-performance liquid chromatography-tandem mass spectrometry measurement of radiation-induced base damage to isolated and cellular DNA. Chem. Res. Toxicol.13, 1002–1010.10.1021/tx000085hSuche in Google Scholar PubMed
Haber, F. and Weiss, J. (1932). Über die Katalyse des Hydroperoxydes. Naturwissenschaften20, 948–950.10.1007/BF01504715Suche in Google Scholar
Halliwell, B. and Gutteridge, J.M.C. (1999). Free Radicals in Biology and Medicine, 3rd Edition (Oxford, UK: Oxford University Press).Suche in Google Scholar
Hayakawa, H., Uchiumi, T., Fukada, T., Ashizuka, M., Kohno, K., Kuwano, M., and Sekiguchi, M. (2002). Binding capacity of human YB-1 protein for RNA containing 8-oxoguanine. Biochemistry41, 12739–12744.10.1021/bi0201872Suche in Google Scholar PubMed
Helbock, H.J., Beckman, K.B., Shigenaga, M.K., Walter, P.B., Woodall, A.A., Yeo, H.C., and Ames, B.N. (1998). DNA oxidation matters: the HPLC-electrochemical detection assay of 8-oxo-deoxyguanosine and 8-oxo-guanine. Proc. Natl. Acad. Sci. USA95, 288–293.10.1073/pnas.95.1.288Suche in Google Scholar
Hofer, T. (2001). Oxidation of 2′-deoxyguanosine by H2O2-ascorbate: evidence against free OH• and thermodynamic support for two-electron reduction of H2O2. J. Chem. Soc. Perkin Trans.2, 210–213.10.1039/b006394kSuche in Google Scholar
Hofer, T. and Möller, L. (2002). Optimization of the workup procedure for the analysis of 8-oxo-7,8-dihydro-2′-deoxyguanosine with electrochemical detection. Chem. Res. Toxicol.15, 426–432.10.1021/tx015573jSuche in Google Scholar
Jaruga, P. and Dizdaroglu, M. (1996). Repair of products of oxidative DNA base damage in human cells. Nucleic Acids Res.24, 1389–1394.10.1093/nar/24.8.1389Suche in Google Scholar
Kasai, H. (1997). Analysis of a form of oxidative DNA damage, 8-hydroxy-2′-deoxyguanosine, as a marker of cellular oxidative stress during carcinogenesis. Mutat. Res.387, 147–163.10.1016/S1383-5742(97)00035-5Suche in Google Scholar
Klein, J.C., Bleeker, M.J., Saris, C.P., Roelen, H.C.P.F., Brugghe, H.F., van den Elst, H., van der Marel, G.A., van Boom, J.H., Westra, J.G., Kriek, E., and Berns, A.J.M. (1992). Repair and replication of plasmids with site-specific 8-oxodG and 8-AAFdG residues in normal and repair-deficient human cells. Nucleic Acids Res.20, 4437–4443.10.1093/nar/20.17.4437Suche in Google Scholar
Manchot, W. and Wilhelms, O. (1902). Ueber Peroxydbildung beim Eisen. Justus Liebig's Ann. Chem.325, 105–124.Suche in Google Scholar
Maquat, L.E. and Carmichael, G.G. (2001). Quality control of mRNA function. Cell104, 173–176.10.1016/S0092-8674(01)00202-1Suche in Google Scholar
Martinez, G.R., Ravanat, J.-L., Medeiros, M.H.G., Cadet, J., and Di Mascio, P. (2000). Synthesis of a naphthalene endoperoxide as a source of 18O-labeled singlet oxygen for mechanistic studies. J. Am. Chem. Soc.122, 10212–10213.10.1021/ja0016452Suche in Google Scholar
Mattick, J.S. (2004). The hidden genetic program of complex organisms. Sci. Am.291, 60–67.10.1038/scientificamerican1004-60Suche in Google Scholar PubMed
Metzler, D.E. (1977). Biochemistry: The Chemical Reactions of Living Cells, 1st Edition. (New York, USA: Academic Press).Suche in Google Scholar
Nunomura, A., Perry, G., Aliev, G., Hirai, K., Takeda, A., Balraj, E.K., Jones, P.K., Ghanbari, H., Wataya, T., Shimohama, S., et al. (2001). Oxidative damage is the earliest event in Alzheimer disease. J. Neuropathol. Exp. Neurol.60, 759–767.10.1093/jnen/60.8.759Suche in Google Scholar PubMed
Osterod, M., Hollenbach, S., Hengstler, J.G., Barnes, D.E., Lindahl, T., and Epe, B. (2001). Age-related and tissue-specific accumulation of oxidative DNA base damage in 7,8-dihydro-8-oxoguanine-DNA glycosylase (Ogg1)-deficient mice. Carcinogenesis22, 1459–1463.10.1093/carcin/22.9.1459Suche in Google Scholar
Park, E.-M., Shigenaga, M.K., Degan, P., Korn, T.S., Kitzler, J.W., Wehr, C.M., Kolachana, P., and Ames, B.N. (1992). Assay of excised oxidative DNA lesions: isolation of 8-oxoguanine and its nucleoside derivatives from biological fluids with a monoclonal antibody column. Proc. Natl. Acad. Sci. USA89, 3375–3379.10.1073/pnas.89.8.3375Suche in Google Scholar
Ravanat, J.-L., Duretz, B., Guiller, A., Douki, T., and Cadet, J. (1998). Isotope dilution high-performance liquid chromatography-electrospray tandem mass spectrometry assay for the measurement of 8-oxo-7,8-dihydro-2′-deoxyguanosine in biological samples. J. Chromatogr. B715, 349–356.10.1016/S0378-4347(98)00259-XSuche in Google Scholar
Ravanat, J.-L., Di Mascio, P., Martinez, G.R., Medeiros, M.H.G., and Cadet, J. (2000). Singlet oxygen induces oxidation of cellular DNA. J. Biol. Chem.275, 40601–40604.10.1074/jbc.M006681200Suche in Google Scholar
Ravanat, J.-L., Douki, T., Duez, P., Gremaud, E., Herbert, K., Hofer, T., Lasserre, L., Saint-Pierre, C., Favier, A., and Cadet, J. (2002). Cellular background level of 8-oxo-7,8-dihydro-2′-deoxyguanosine: an isotope-based method to evaluate artefactual oxidation of DNA during its extraction and subsequent work-up. Carcinogenesis23, 1911–1918.10.1093/carcin/23.11.1911Suche in Google Scholar
Schönbein, C.F. (1860). Fortsetzung der Beiträge zur nähern Kenntniss des Sauerstoffs. J. Prakt. Chem.79, 65–72.10.1002/prac.18600790111Suche in Google Scholar
Steenken, S. and Jovanovic, S.V. (1997). How easily oxidizable is DNA? One-electron reduction potentials of adenosine and guanosine radicals in aqueous solution. J. Am. Chem. Soc.119, 617–618.10.1021/ja962255bSuche in Google Scholar
Thénard, M.L.J. (1818). Observations sur des nouvelles combinations entre l'oxigéne et divers acides. Ann. Chim. Phys.8, 306–313.Suche in Google Scholar
Wamer, W.G. and Wei, R.R. (1997). In vitro photooxidation of nucleic acids by ultraviolet A radiation. Photochem. Photobiol.65, 560–563.Suche in Google Scholar
Wardman, P. and Candeias, L.P. (1996). Fenton chemistry: an introduction. Radiat. Res.145, 523–531.10.2307/3579270Suche in Google Scholar
Weimann, A., Belling, D., and Poulsen, H.E. (2002). Quantification of 8-oxo-guanine and guanine as the nucleobase, nucleoside and deoxynucleoside forms in human urine by high-performance liquid chromatography-electrospray tandem mass spectrometry. Nucleic Acids Res.30, E7.10.1093/nar/30.2.e7Suche in Google Scholar
Zhang, J., Perry, G., Smith, M.A., Robertson, D., Olson, S.J., Graham, D.G., and Montine, T.J. (1999). Parkinson's disease is associated with oxidative damage to cytoplasmic DNA and RNA in substantia nigra neurons. Am. J. Pathol.154, 1423–1429.10.1016/S0002-9440(10)65396-5Suche in Google Scholar
© by Walter de Gruyter Berlin New York
Artikel in diesem Heft
- Supplementary material to the paper “The connexin gene family in mammals”
- Nicking activity on pBR322 DNA of ribosome inactivating proteins from Phytolacca dioica L. leaves
- Identification of three novel mutations in the dihydropyrimidine dehydrogenase gene associated with altered pre-mRNA splicing or protein function
- The connexin gene family in mammals
- Hydrogen peroxide causes greater oxidation in cellular RNA than in DNA
- Homology modeling and SAR analysis of Schistosoma japonicum cathepsin D (SjCD) with statin inhibitors identify a unique active site steric barrier with potential for the design of specific inhibitors
- Interpretation of the reactivity of peroxidase compound II with phenols and anilines using the Marcus equation
- P. falciparum pro-histoaspartic protease (proHAP) protein peptides bind specifically to erythrocytes and inhibit the invasion process in vitro
- The snake venom metalloproteases berythractivase and jararhagin activate endothelial cells
- Visualisation of transforming growth factor-β1, tissue kallikrein, and kinin and transforming growth factor-β receptors on human clear-cell renal carcinoma cells
- cDNA cloning and heterologous expression of a wheat proteinase inhibitor of subtilisin and chymotrypsin (WSCI) that interferes with digestive enzymes of insect pests
- Proteolytic susceptibility of the serine protease inhibitor trappin-2 (pre-elafin): evidence for tryptase-mediated generation of elafin
- Labelling of four distinct trophozoite falcipains of Plasmodium falciparum by a cystatin-derived probe
Artikel in diesem Heft
- Supplementary material to the paper “The connexin gene family in mammals”
- Nicking activity on pBR322 DNA of ribosome inactivating proteins from Phytolacca dioica L. leaves
- Identification of three novel mutations in the dihydropyrimidine dehydrogenase gene associated with altered pre-mRNA splicing or protein function
- The connexin gene family in mammals
- Hydrogen peroxide causes greater oxidation in cellular RNA than in DNA
- Homology modeling and SAR analysis of Schistosoma japonicum cathepsin D (SjCD) with statin inhibitors identify a unique active site steric barrier with potential for the design of specific inhibitors
- Interpretation of the reactivity of peroxidase compound II with phenols and anilines using the Marcus equation
- P. falciparum pro-histoaspartic protease (proHAP) protein peptides bind specifically to erythrocytes and inhibit the invasion process in vitro
- The snake venom metalloproteases berythractivase and jararhagin activate endothelial cells
- Visualisation of transforming growth factor-β1, tissue kallikrein, and kinin and transforming growth factor-β receptors on human clear-cell renal carcinoma cells
- cDNA cloning and heterologous expression of a wheat proteinase inhibitor of subtilisin and chymotrypsin (WSCI) that interferes with digestive enzymes of insect pests
- Proteolytic susceptibility of the serine protease inhibitor trappin-2 (pre-elafin): evidence for tryptase-mediated generation of elafin
- Labelling of four distinct trophozoite falcipains of Plasmodium falciparum by a cystatin-derived probe