Expression of the E. coli Fpg protein in CHO cells lowers endogenous oxypurine clustered damage levels and decreases accumulation of endogenous Hprt mutations

Environmental and Molecular Mutagenesis

Volumn 47, Issue 5, 2006, Pages 311-319

  Paul, Sunirmal ^a,c   Gros, Laurent ^b,d   Laval, Jacques ^b   Sutherland, Betsy M ^a  

^a BROOKHAVEN NATIONAL LABORATORY   (United States)

^b INSTITUT GUSTAVE ROUSSY   (France)

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

^d Ecole Normale Superieure de Cachan   (France)

Author keywords

Clustered damages; DNA damage; DNA repair; fpg protein; Oxidized purines

Indexed keywords

DNA FORMAMIDOPYRIMIDINE GLYCOSYLASE; HYDROXYPURINE; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; OXYPYRIMIDINE; PURINE DERIVATIVE; PYRIMIDINE DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL GENE; CELL REGENERATION; CHO CELL; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; ESCHERICHIA COLI; GENE FREQUENCY; GENE MUTATION; GENOTYPE; HPRT GENE; MAMMAL CELL; NONHUMAN;

CRICETULUS GRISEUS; ESCHERICHIA COLI; MAMMALIA;

EID: 33745116918     PISSN: 08936692     EISSN: 10982280     Source Type: Journal    
DOI: 10.1002/em.20208     Document Type: Article

References (43)

1. Asagoshi K, Yamada T, Terato H, Ohyama Y, Monden Y, Arai T, Nishimura S, Aburatani H, Lindahl T, Ide H. 2000. Distinct repair activities of human 7,8-dihydro-8-oxoguanine DNA glycosylase and formamidopyrimidine DNA glycosylase for formamidopyrimidine and 7,8-dihydro-8-oxoguanine. J Biol Chem 275:4956-4964.
2. Bennett PV, Cintron NS, Gros L, Laval J, Sutherland BM. 2004. Are endogenous clustered DNA damages induced in human cells? Free Radic Biol Med 37:488-499.
3. Bennett PV, Cuomo NL, Paul S, Tafrov ST, Sutherland BM. 2005. Endogenous DNA damage clusters in human skin, 3-D model, and cultured skin cells. Free Radic Biol Med 39:832-839.
4. Boiteux S, O'Connor TR, Lederer F, Gouyette A, Laval J. 1990. Homogeneous Escherichia coli FPG protein. A DNA glycosylase which excises imidazole ring-opened purines and nicks DNA at apurinic/apyrimidinic sites. J Biol Chem 265:3916-3922.
5. Castaing B, Geiger A, Seliger H, Nehls P, Laval J, Zelwer C, Boiteux S. 1993. Cleavage and binding of a DNA fragment containing a single 8-oxoguanine by wild type and mutant FPG proteins. Nucleic Acids Res 21:2899-2905.
6. Chaudhry MA, Weinfeld M. 1997. Reactivity of human apurinic/apyrimidinic endonuclease and Escherichia coli exonuclease III with bistranded abasic sites in DNA. J Biol Chem 272:15650-15655.
7. Chu G, Vollrath D, Davis RW. 1986. Separation of large DNA molecules by contour-clamped homogeneous electric field. Science 234:1582-1585.
8. Cussac C, Laval F. 1996. Reduction of the toxicity and mutagenicity of aziridine in mammalian cells harboring the Escherichia coli fpg gene. Nucleic Acids Res 24:1742-1746.
9. David-Cordonnier MH, Cunniffe SM, Hickson ID, O'Neill P. 2002. Efficiency of incision of an AP site within clustered DNA damage by the major human AP endonuclease. Biochemistry 41:634-642.
10. Evans HH, Ricanati M, Horng M-F, Jian Q, Mend J, Olive P. 1993. DNA double-strand break rejoining deficiency in TK6 and other human B-lymphoblast cell lines. Radiat Res 134:307-315.
11. Freeman SE, Blackett AD, Monteleone DC, Setlow RB, Sutherland BM, Sutherland JC. 1986. Quantitation of radiation-, chemical-, or enzyme-induced single strand breaks in nonradioactive DNA by alkaline gel electrophoresis: application to pyrimidine dimers Anal Biochem 158:119-129.
12. Georgakilas AG, Bennett PV, Sutherland BM. 2002. High efficiency detection of bistranded abasic clusters in γ-irradiated DNA by putrescine. Nucleic Acids Res 30:2800-2808.
13. Georgakilas AG, Bennett PV, Wilson DM, III, Sutherland BM. 2004 Processing of bistranded abasic DNA clusters in gamma-irradiated human hematopoietic cells. Nucleic Acids Res 32:5609-5620.
14. Gulston M, de Lara C, Jenner T, Davis E, O'Neill P. 2004. Processing of clustered DNA damage generates additional double-strand breaks in mammalian cells post-irradiation. Nucleic Acids Res 32:1602-1609.
15. Harrison L, Hatahet Z, Wallace S. 1999. In vitro repair of synthetic ionizing radiation-induced multiply damaged DNA sites. J Mol Biol 290:667-684.
16. Hawley RG. 2001. Progress toward vector design for hematopoietic stem cell gene therapy. Curr Gene Ther 1:1-17.
17. He YH, Xu Y, Kobune M, Wu M, Kelley MR, Martin WJ, II. 2002. Escherichia coli FPG, human OGG1 reduce DNA damage and cytotoxicity by BCNU in human lung cells. Am J Physiol Lung Cell Mol Physiol 282:L50-L55.
18. Hemminki K. 1984. Reactions of ethyleneimine with guanosine and deoxyguanosine. Chem Biol Interact 48:249-260.
19. Hill JW, Hazra TK, Izumi T, Mitra S. 2001. Stimulation of human 8-oxoguanine-DNA glycosylase by AP-endonuclease: potential coordination of the initial steps in base excision repair. Nucleic Acids Res 29:430-438.
20. Hollenbach S, Dhenaut A, Eckert I, Radicella JP, Epe B. 1999. Overexpression of Ogg1 in mammalian cells: effects on induced and spontaneous oxidative DNA damage and mutagenesis. Carcinogenesis 20:1863-1868.
21. Hsie AW, Casciano DA, Couch DB, Krahn DF, O'Neill JP, Whitfield BL. 1981. The use of Chinese hamster ovary cells to quantify specific locus mutation and to determine mutagenicity of chemicals. A report of the gene-tox program. Mutat Res 86:193-214.
22. Jaruga P, Speina E, Gackowski D, Tudek B, Olinski R. 2000. Endogenous oxidative DNA base modifications analysed with repair enzymes and GC/MS technique. Nucleic Acids Res 28:E16.
23. Klungland A, Rosewell I, Hollenbach S, Larsen E, Daly G, Epe B, Seeberg E, Lindahl T, Barnes DE. 1999. Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage. Proc Natl Acad Sci U S A 96:13300-13305.
24. Kobune M, Xu Y, Baum C, Kelley MR, Williams DA. 2001. Retrovirus-mediated expression of the base excision repair proteins, formamidopyrimidine DNA glycosylase or human oxoguanine DNA glycosylase, protects hematopoietic cells from N,N′,N″-triethylenethiophosphoramide (thioTEPA)-induced toxicity in vitro and in vivo. Cancer Res 61:5116-5125.
25. Kremer TM, Rinne ML, Xu Y, Chen XM, Kelley MR. 2004. Protection of pulmonary epithelial cells from oxidative stress by hMYH adenine glycosylase. Respir Res 5:16.
26. Kunkel TA. 1999. The high cost of living. American Association for Cancer Research Special Conference: endogenous sources of mutations, Fort Myers, Florida, USA, 11-15 November 1998. Trends Genet 15:93-94.
27. Laval F. 1994. Expression of the E. coli fpg gene in mammalian cells reduces the mutagenicity of γ-rays. Nucleic Acids Res 22:4943-4946.
28. Minowa O, Arai T, Hirano M, Monden Y, Nakai S, Fukuda M, Itoh M, Takano H, Hippou Y, Aburatani H, Masumura K, Nohmi T, Nishimura S, Noda T. 2000. Mmh/Ogg1 gene inactivation results in accumulation of 8-hydroxyguanine in mice. Proc Natl Acad Sci U S A 97:4156-4161.
29. O'Connor TR, Boiteux S, Laval J. 1988. Ring-opened 7-methylguanine residues in DNA are a block to in vitro DNA synthesis. Nucleic Acids Res 16:5879-5894.
30. Osterod M, Hollenbach S, Hengstler JG, Barnes DE, Lindahl T, 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. Carcinogenesis 22:1459-1463.
31. Roldan-Arjona T, Wei Y-F, Carter KC, Klungland A, Anselmino C, Wang R-P, Augustus M, Lindahl T. 1997. Molecular cloning and functional expression of a human cDNA encoding the antimutator enzyme 8-hydroxyguanine-DNA glycosylase. Proc Natl Acad Sci U S A 94:8016-8020.
32. Ropolo M, Geroldi A, Degan P, Andreotti V, Zupo S, Poggi A, Reed A, Kelley M, Frosina G. 2006. Accelerated repair and reduced mutagenicity of oxidative DNA damage in human bladder cells expressing the E. coli FPG protein. Int J Cancer 118:1628-1634.
33. Shibutani S, Takeshita M, Grollman AP. 1991. Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature 349:431-434.
34. Sutherland BM, Bennett PV, Sidorkina O, Laval J. 2000. DNA damage clusters induced by ionizing radiation in isolated DNA, in human cells. Proc Natl Acad Sci U S A 97:103-108.
35. Sutherland BM, Bennett PV, Cintron NS, Guida P, Laval J. 2003. Low levels of endogenous oxidative damage cluster levels in unirradiated viral and human DNAs. Free Radic Biol Med 35:495-503.
36. Sutherland JC. 1990. Electronic imaging systems for quantitative electrophoresis of DNA. In: Freeman SE, Fukishima E, Green ER, editors. Non-invasive Techniques in Biology and Medicine. San Francisco:San Francisco Press. pp 125-134.
37. Sutherland JC, Lin B, Monteleone DC, Mugavero J, Sutherland BM, Trunk J. 1987. Electronic imaging system for direct and rapid quantitation of fluorescence from electrophoretic gels: application to ethidium bromide-stained DNA. Anal Biochem 163:446-457.
38. Sutherland JC, Monteleone DC, Sutherland BM. 1997. Computer network for data acquisition, storage and analysis. J Photochem Photobiol B 40:14-22.
39. Tchou J, Bodepudi V, Shibutani S, Antoshechkin I, Miller J, Grollman AP, Johnson F. 1994. Substrate specificity of Fpg protein. Recognition and cleavage of oxidatively damaged DNA. J Biol Chem 269:15318-15324.
40. Wallace SS. 2002. Biological consequences of free radical-damaged DNA bases. Free Radic Biol Med 33:1-14.
41. Wu M, He YH, Kobune M, Xu Y, Kelley MR, Martin WJ, II. 2002. Protection of human lung cells against hyperoxia using the DNA base excision repair genes hOgg1 and Fpg. Am J Respir Crit Care Med 166:192-199.
42. Yang N, Galick H, Wallace SS. 2004. Attempted base excision repair of ionizing radiation damage in human lymphoblastoid cells produces lethal and mutagenic double strand breaks. DNA Repair (Amst) 3:1323-1334.
43. Zharkov DO, Shoham G, Grollman AP. 2003. Structural characterization of the Fpg family of DNA glycosylases. DNA Repair (Amst) 2:839-862.