AlkB reverses etheno DNA lesions caused by lipid oxidation in vitro and in vivo

Nature Structural and Molecular Biology

Volumn 12, Issue 10, 2005, Pages 855-860

  Delaney, James C ^a,b   Smeester, Lisa ^a,b   Wong, Cintyu ^a   Frick, Lauren E ^a,b   Taghizadeh, Koli ^b   Wishnok, John S ^a,b   Drennan, Catherine L ^a,b   Samson, Leona D ^a,b   Essigmann, John M ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b USA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; CYTOSINE; DNA; GLYCOL; GLYOXAL; LIPID; PROTEIN; PROTEIN ALKB; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BIOCHEMISTRY; CHEMICAL BOND; CONTROLLED STUDY; DNA DAMAGE; EPOXIDATION; ESCHERICHIA COLI; HYDROLYSIS; IN VITRO STUDY; IN VIVO STUDY; LIPID OXIDATION; MUTAGENICITY; NONHUMAN; PRIORITY JOURNAL; TOXICITY;

ACETALDEHYDE; ADENINE; CYTOSINE; DNA ADDUCTS; DNA DAMAGE; DNA GLYCOSYLASES; DNA REPAIR; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; LIPID PEROXIDATION; MIXED FUNCTION OXYGENASES; MUTAGENESIS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MAMMALIA;

EID: 27144535750     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb996     Document Type: Article

References (40)

1. Aravind, L. & Koonin, E.V. The DNA-repair protein AlkB, EGL-9, and leprecan define new families of 2-oxoglutarate- and iron-dependent dioxygenases. Genome Biol. 2, Research 0007 (2001).
2. Trewick, S.C., Henshaw, T.F., Hausinger, R.P., Lindahl, T. & Sedgwick, B. Oxidative demethylation by Escherichia coli AlkB directly reverts DNA base damage. Nature 419, 174-178 (2002).
3. Falnes, P.O., Johansen, R.F. & Seeberg, E. AlkB-mediated oxidative demethylation reverses DNA damage in Escherichia coli. Nature 419, 178-182 (2002).
4. Duncan, T. et al. Reversal of DNA alkylation damage by two human dioxygenases. Proc. Natl. Acad. Sci. USA 99, 16660-16665 (2002).
5. Koivisto, P., Duncan, T., Lindahl, T. & Sedgwick, B. Minimal methylated substrate and extended substrate range of Escherichia coli AlkB protein, a 1-methyladenine-DNA dioxygenase. J. Biol. Chem. 278, 44348-44354 (2003).
6. Koivisto, P., Robins, P., Lindahl, T. & Sedgwick, B. Demethylation of 3-methylthymine in DNA by bacterial and human DNA dioxygenases. J. Biol. Chem. 279, 40470-40474 (2004).
7. Delaney, J.C. & Essigmann, J.M. Mutagenesis, genotoxicity, and repair of 1-methyl-adenine, 3-alkylcytosines, 1-methylguanine, and 3-methylthymine in alkB Escherichia coli. Proc. Natl. Acad. Sci. USA 101, 14051-14056 (2004).
8. Falnes, P.O. Repair of 3-methylthymine and 1-methylguanine lesions by bacterial and human AlkB proteins. Nucleic Acids Res. 32, 6260-6267 (2004).
9. Aas, P.A. et al. Human and bacterial oxidative demethylases repair alkylation damage in both RNA and DNA. Nature 421, 859-863 (2003).
10. Ougland, R. et al. AlkB restores the biological function of mRNA and tRNA inactivated by chemical methylation. Mol. Cell 16, 107-116 (2004).
11. Sedgwick, B. Repairing DNA-methylation damage. Nat. Rev. Mol. Cell Biol. 5, 148-157 (2004).
12. Ames, B.N., Shigenaga, M.K. & Hagen, T.M. Oxidants, antioxidants, and the degenerative diseases of aging. Proc. Natl. Acad. Sci. USA 90, 7915-7922 (1993).
13. Bjelland, S. & Seeberg, E. Mutagenicity, toxicity and repair of DNA base damage induced by oxidation. Mutat. Res. 531, 37-80 (2003).
14. Klaunig, J.E. & Kamendulis, L.M. The role of oxidative stress in carcinogenesis. Annu. Rev. Pharmacol. Toxicol. 44, 239-267 (2004).
15. Dedon, P.C. & Tannenbaum, S.R. Reactive nitrogen species in the chemical biology of inflammation. Arch. Biochem. Biophys. 423, 12-22 (2004).
16. Evans, M.D., Dizdaroglu, M. & Cooke, M.S. Oxidative DNA damage and disease: induction, repair and significance. Mutat. Res. 567, 1-61 (2004).
17. 4-ethenocytosine by lipid peroxidation products and nucleic acid bases. Chem. Res. Toxicol. 8, 278-283 (1995).
18. Chung, F.L., Chen, H.J. & Nath, R.G. Lipid peroxidation as a potential endogenous source for the formation of exocyclic DNA adducts. Carcinogenesis 17, 2105-2111 (1996).
19. Marnett, L.J. Oxyradicals and DNA damage. Carcinogenesis 21, 361-370 (2000).
20. Blair, I.A. Lipid hydroperoxide-mediated DNA damage. Exp. Gerontol. 36, 1473-1481 (2001).
21. 2-etheno-2′-deoxyguanosine adducts. Chem. Res. Toxicol. 18, 780-786 (2005).
22. 32P-postlabeling. Carcinogenesis 16, 613-617 (1995).
23. Barbin, A. et al. Endogenous deoxyribonucleic acid (DNA) damage in human tissues: a comparison of ethenobases with aldehydic DNA lesions. Cancer Epidemiol. Biomarkers Prev. 12, 1241-1247 (2003).
24. Barbin, A. Etheno-adduct-forming chemicals: from mutagenicity testing to tumor mutation spectra. Mutat. Res. 462, 55-69 (2000).
25. 6-ethenoadenine when present in DNA. Nucleic Acids Res. 23, 3750-3755 (1995).
26. 4-ethenocytosine, a highly mutagenic adduct, is a primary substrate for Escherichia coli double-stranded uracil-DNA glycosylase and human mismatch-specific thymine-DNA glycosylase. Proc. Natl. Acad. Sci. USA 95, 8508-8513 (1998).
27. Engelward, B.P. et al. Base excision repair deficient mice lacking the Aag alkyladenine DNA glycosylase. Proc. Natl. Acad. Sci. USA 94, 13087-13092 (1997).
28. 6-etheno- deoxyadenosine DNA lesions from lung and liver in vivo. DNA Repair (Amst.) 3, 257-265 (2004).
29. Pandya, G.A., Yang, I.Y., Grollman, A.P. & Moriya, M. Escherichia coli responses to a single DNA adduct. J. Bacteriol. 182, 6598-6604 (2000).
30. Mroczkowska, M.M., Kolasa, I.K. & Kusmierek, J.T. Chloroacetaldehyde-induced mutagenesis in Escherichia coli: specificity of mutations and modulation by induction of the adaptive response to alkylating agents. Mutagenesis 8, 341-348 (1993).
31. Borys, E., Mroczkowska-Slupska, M.M. & Kusmierek, J.T. The induction of adaptive response to alkylating agents in Escherichia coli reduces the frequency of specific C → T mutations in chloroacetaldehyde-treated M13 glyU phage. Mutagenesis 9, 407-410 (1994).
32. 4-ethenocytosine, and 4-amino-5-(imidazol-2-yl)imidazole. Biochemistry 32, 12793-12801 (1993).
33. 6-ethenodeoxyadenosine, a DNA adduct highly mutagenic in mammalian cells. Biochemistry 35, 11487-11492 (1996).
34. 6-ethenodeoxyadenosine adduct in human cells. Cancer Res. 60, 4098-4104 (2000).
35. Moriya, M., Zhang, W., Johnson, F. & Grollman, A.P. Mutagenic potency of exocyclic DNA adducts: marked differences between Escherichia coli and simian kidney cells. Proc. Natl. Acad. Sci. USA 91, 11899-11903 (1994).
36. Palejwala, V.A., Simha, D. & Humayun, M.Z. Mechanisms of mutagenesis by exocyclic DNA adducts. Transfection of M13 viral DNA bearing a site-specific adduct shows that ethenocytosine is a highly efficient RecA-independent mutagenic noninstructional lesion. Biochemistry 30, 8736-8743 (1991).
37. Singer, B. & Bartsch, H. (eds.). Exocyclic DNA Adducts in Mutagenesis and Carcinogenesis (International Agency for Research on Cancer, Lyon, France, 1999).
38. Thornburg, L.D., Lai, M.T., Wishnok, J.S. & Stubbe, J. A non-heme iron protein with heme tendencies: an investigation of the substrate specificity of thymine hydroxylase. Biochemistry 32, 14023-14033 (1993).
39. Nair, J. et al. Lipid peroxidation-induced etheno-DNA adducts in the liver of patients with the genetic metal storage disorders Wilson's disease and primary hemochromatosis. Cancer Epidemiol. Biomarkers Prev. 7, 435-440 (1998).
40. Bartsch, H. & Nair, J. Oxidative stress and lipid peroxidation-derived DNA-lesions in inflammation driven carcinogenesis. Cancer Detect. Prev. 28, 385-391 (2004).