Targeted deletion of the genes encoding NTH1 and NEIL1 DNA N-glycosylases reveals the existence of novel carcinogenic oxidative damage to DNA

DNA Repair

Volumn 8, Issue 7, 2009, Pages 786-794

  Chan, Michael K ^a   Ocampo Hafalla, Maria T ^a   Vartanian, Vladimir ^b   Jaruga, Pawel ^c,d   Kirkali, Güldal ^c,e   Koenig, Karen L ^a   Brown, Stuart ^a   Lloyd, R Stephen ^b   Dizdaroglu, Miral ^c   Teebor, George W ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c NATIONAL INSTITUTE OF STANDARDS AND TECHNOLOGY   (United States)

^d NICOLAUS COPERNICUS UNIVERSITY   (Poland)

^e DOKUZ EYLUL UNIVERSITY   (Turkey)

Author keywords

Base excision repair; Cancer; K ras; Mouse; NEIL1; NTH1

Indexed keywords

DNA GLYCOSYLASE MUTY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CHEMICAL ANALYSIS; CONTROLLED STUDY; DNA DAMAGE; EXCISION REPAIR; EXPERIMENTAL MOUSE; FEMALE; GENE DELETION; GENE MUTATION; GENOTYPE; INCIDENCE; KNOCKOUT MOUSE; LIVER TUMOR; LUNG TUMOR; MALE; MOUSE; MUTAGENIC ACTIVITY; MUTATION; NONHUMAN; OXIDATION; PHENOTYPE; PRIORITY JOURNAL;

ANIMALS; BASE SEQUENCE; BRAIN; DEOXYRIBONUCLEASE (PYRIMIDINE DIMER); DNA DAMAGE; DNA GLYCOSYLASES; DNA MUTATIONAL ANALYSIS; FEMALE; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GENE DELETION; GENES, RAS; GUANINE; KIDNEY; LIVER; LIVER NEOPLASMS; LUNG NEOPLASMS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; MICE, KNOCKOUT; MUTATION; OXIDATION-REDUCTION; PYRIMIDINES;

BACTERIA (MICROORGANISMS); MUS;

EID: 67349140639     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2009.03.001     Document Type: Article

References (45)

1. Al-Tassan N., Chmiel N.H., Maynard J., Fleming N., Livingston A.L., Williams G.T., Hodges A.K., Davies D.R., David S.S., Sampson J.R., and Cheadle J.P. Inherited variants of MYH associated with somatic G:C → T:A mutations in colorectal tumors. Nat. Genet. 30 (2002) 227-232
2. Michaels M.L., Cruz C., Grollman A.P., and Miller J.H. Evidence that MutY and MutM combine to prevent mutations by an oxidatively damaged form of guanine in DNA. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 7022-7025
3. Tajiri T., Maki H., and Sekiguchi M. Functional cooperation of MutT, MutM and MutY proteins in preventing mutations caused by spontaneous oxidation of guanine nucleotide in Escherichia coli. Mutat. Res. 336 (1995) 257-267
4. Aburatani H., Hippo Y., Ishida T., Takashima R., Matsuba C., Kodama T., Takao M., Yasui A., Yamamoto K., and Asano M. Cloning and characterization of mammalian 8-hydroxyguanine-specific DNA glycosylase/apurinic, apyrimidinic lyase, a functional MutM homologue. Cancer Res. 57 (1997) 2151-2156
5. Bjorâs M., Luna L., Johnsen B., Hoff E., Haug T., Rognes T., and Seeberg E. Opposite base-dependent reactions of a human base excision repair enzyme on DNA containing 7,8-dihydro-8-oxoguanine and abasic sites. EMBO J. 16 (1997) 6314-6322
6. Shinmura K., Kasai H., Sasaki A., Sugimura H., and Yokota J. 8-hydroxyguanine (7, 8-dihydro-8-oxoguanine) DNA glycosylase and AP lyase activities of hOGG1 protein and their substrate specificity. Mutat. Res. 385 (1997) 75-82
7. Chow E., Thirlwell C., Macrae F., and Lipton L. Colorectal cancer and inherited mutations in base-excision repair. Lancet Oncol. 5 (2004) 600-606
8. Sampson J.R., Jones S., Dolwani S., and Cheadle J.P. MutYH (MYH) and colorectal cancer. Biochem Soc. Trans. 33 (2005) 679-683
9. David S.S., O'Shea V.L., and Kundu S. Base-excision repair of oxidative DNA damage. Nature 447 (2007) 941-950
10. Kastrinos F., and Syngal S. Recently identified colon cancer predispositions: MYH and MSH6 mutations. Semin. Oncol. 34 (2007) 418-424
11. Xie Y., Yang H., Cunanan C., Okamoto K., Shibata D., Pan J., Barnes D.E., Lindahl T., McIlhatton M., Fishel R., and Miller J.H. Deficiencies in mouse Myh and Ogg1 result in tumor predisposition and G to T mutations in codon 12 of the K-Ras oncogene in lung tumors. Cancer Res. 64 (2004) 3096-3102
12. Sakamoto K., Tominaga Y., Yamauchi K., Nakatsu Y., Sakumi K., Yoshiyama K., Egashira A., Kura S., Yao T., Tsuneyoshi M., Maki H., Nakabeppu Y., and Tsuzuki T. MUTYH-null mice are susceptible to spontaneous and oxidative stress induced intestinal tumorigenesis. Cancer Res. 67 (2007) 6599-6604
13. Zuo S., Boorstein R.J., and Teebor G.W. Oxidative damage to 5-methylcytosine in DNA. Nucleic Acids Res. 23 (1995) 3239-3243
14. Dizdaroglu M. Base-excision repair of oxidative DNA damage by DNA glycosylases. Mutat. Res. 591 (2005) 45-59
15. Hu J., de Souza-Pinto N.C., Haraguchi K., Hogue B.A., Jaruga P., Greenberg M.M., Dizdaroglu M., and Bohr V.A. Repair of formamidopyrimidines in DNA involves different glycosylases: role of the OGG1, NTH1, and NEIL1 enzymes. J. Biol. Chem. 280 (2005) 40544-40551
16. Jaruga P., Birinciogluc M., Rosenquist T.A., and Dizdaroglu M. Mouse NEIL1 protein is specific for excision of 2,6-diamino-4-hydroxy-5-formamidopyrimidine and 4, 6-diamino-5-formamidopyrimidine from oxidatively damaged DNA. Biochemistry 43 (2004) 15909-15914
17. Hazra T.K., Izumi T., Boldough I., Imhoff B., Kow Y.W., Jaruga P., Dizdaroglu M., and Mitra S. Identification and characterization of a human DNA glycosylase for repair of modified bases in oxidatively damaged DNA. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 3523-3528
18. Hailer M.K., Slade P.G., Martin B.D., Rosenquist T.A., and Sugden K.D. Recognition of the oxidized lesions spiroiminodihydantoin and guanidinohydantoin in DNA by the mammalian base excision repair glycosylases NEIL1 and NEIL2. DNA Repair (Amst) 4 (2005) 41-50
19. Krishnamurthy N., Zhao X., Burrows C.J., and David S.S. Superior removal of hydantoin lesions relative to other oxidized bases by the human DNA glycosylase hNEIL1. Biochemistry 47 (2008) 7137-7146
20. Ocampo M.T., Chaung W., Marenstein D.R., Chan M.K., Altamirano A., Basu A.K., Boorstein R.J., Cunningham R.P., and Teebor G.W. Targeted deletion of mNth1 reveals a novel DNA repair enzyme activity. Mol. Cell Biol. 22 (2002) 6111-6121
21. Vartanian V., Lowell B., Minko I.G., Wood T.G., Ceci J.D., George S., Ballinger S.W., Corless C.L., McCullough A.K., and Lloyd R.S. The metabolic syndrome resulting from a knockout of the NEIL1 DNA glycosylase. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 1864-1869
22. Hofer T., Seo A.Y., Prudencio M., and Leeuwenburgh C. 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 (2006) 103-111
23. Cadet J., Douki T., Gasparutto D., and Ravanat J.L. Oxidative damage to DNA: formation, measurement and biochemical features. Mutat. Res. 531 (2003) 5-23
24. Boiteux S., Gajewski E., Laval J., and Dizdaroglu M. Substrate specificity of the Escherichia coli Fpg protein (formamidopyrimidine-DNA glycosylase): excision of purine lesions in DNA produced by ionizing radiation or photosensitization. Biochemistry 31 (1992) 106-110
25. Jaruga P., Kirkali G., and Dizdaroglu M. Measurement of formamidopyrimidines in DNA. Free Radic. Biol. Med. 45 (2008) 1601-1609
26. Reddy P., Jaruga P., O'Connor T., Rodriguez H., and Dizdaroglu M. Overexpression and rapid purification of Escherichia coli formamidopyrimidine-DNA glycosylase. Protein Expr. Purif. 34 (2004) 126-133
27. Nelson R.A., Boyd S.J., Ziegelstein R.C., Herning R., Cadet J.L., Henningfield J.E., Schuster C.R., Contoreggi C., and Gorelick D.A. Effect of rate of administration on subjective and physiological effects of intravenous cocaine in humans. Drug Alcohol Depend. 82 (2006) 19-24
28. Dizdaroglu M. Quantitative determination of oxidative base damage in DNA by stable isotope-dilution mass spectrometry. FEBS Lett. 315 (1993) 1-6
29. Dizdaroglu M., Bauche C., Rodriguez H., and Laval J. Novel substrates of Escherichia coli nth protein and its kinetics for excision of modified bases from DNA damaged by free radicals. Biochemistry 39 (2000) 5586-5592
30. Gasparutto D., Muller E., Boiteux S., and Cadet J. Excision of the oxidatively formed 5-hydroxyhydantoin and 5-hydroxy-5-methylhydantoin pyrimidine lesions by Escherichia coli and Saccharomyces cerevisiae DNA N-glycosylases. Biochim. Biophys. Acta. 1790 (2009) 16-24
31. Meuwissen R., and Berns A. Mouse models for human lung cancer. Genes Dev. 19 (2005) 643-664
32. Wakamatsu N., Devereux T.R., Hong H.H., and Sills R.C. Overview of the molecular carcinogenesis of mouse lung tumor models of human lung cancer. Toxicol. Pathol. 35 (2007) 75-80
33. Esposito G. Complementary techniques: laser capture microdissection-increasing specificity of gene expression profiling of cancer specimens. Adv. Exp. Med. Biol. 593 (2007) 54-65
34. Budimlija Z.M., Lechpammer M., Popiolek D., Fogt F., Prinz M., and Bieber F.R. Forensic applications of laser capture microdissection: use in DNA-based parentage testing and platform validation. Croat. Med. J. 46 (2005) 549-555
35. Krishnamurthy N., Haraguchi K., Greenberg M.M., and David S.S. Efficient removal of formamidopyrimidines by 8-oxoguanine glycosylases. Biochemistry 47 (2008) 1043-1050
36. Wiederholt C.J., Delaney M.O., Pope M.A., David S.S., and Greenberg M.M. Repair of DNA containing Fapy.dG and its beta-C-nucleoside analogue by formamidopyrimidine DNA glycosylase and MutY. Biochemistry 42 (2003) 9755-9760
37. Karahalil B., Hogue B.A., De Souza-Pinto N.C., and Bohr V.A. Base excision repair capacity in mitochondria and nuclei: tissue-specific variations. FASEB J. 16 (2002) 1895-1902
38. Russo M.T., De Luca G., Degan P., Parlanti E., Dogliotti E., Barnes D.E., Lindahl T., Yang H., Miller J.H., and Bignami M. Accumulation of the oxidative base lesion 8-hydroxyguanine in DNA of tumor-prone mice defective in both the Myh and Ogg1 DNA glycosylases. Cancer Res. 64 (2004) 4411-4414
39. Parsons J.L., and Elder R.H. DNA N-glycosylase deficient mice: a tale of redundancy. Cancer Res. 531 (2003) 165-175
40. Kreutzer D.A., and Essigmann J.M. Oxidized, deaminated cytosines are a source of C → T transitions in vivo. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 3578-3582
41. Hazra T.K., Kow Y.W., Hatahet Z., Imhoff B., Boldogh I., Mokkapati S.K., Mitra S., and Izumi T. Identification and characterization of a novel human DNA glycosylase for repair of cytosine-derived lesions. J. Biol. Chem. 277 (2002) 30417-30420
42. Reardon J.T., Bessho T., Kung H.C., Bolton P.H., and Sancar A. In vitro repair of oxidative DNA damage by human nucleotide excision repair system: possible explanation for neurodegeneration in xeroderma pigmentosum patients. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 9463-9468
43. -/- mice. Cancer Res. 67 (2007) 5156-5161
44. Hahn F.F., Gigliotti A., and Hutt J.A. Comparative oncology of lung tumors. Toxicol. Pathol. 35 (2007) 130-135
45. Naugler W.E., Sakurai T., Kim S., Maeda S., Kim K., Elsharkawy A.M., and Karin M. Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science 317 (2007) 121-124