Comet-FISH with strand-specific probes reveals transcription-coupled repair of 8-oxoGuanine in human cells

Nucleic Acids Research

Volumn 41, Issue 16, 2013, Pages 7700-7712

  Guo, Jia ^a   Hanawalt, Philip C ^a   Spivak, Graciela ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 HYDROXYGUANINE; 8 OXOG DNA GLYCOSYLASE; ATM PROTEIN; CELL DNA; CELL PROTEIN; DEOXYRIBONUCLEASE; DNA GLYCOSYLASE MUTY; DNA GLYCOSYLTRANSFERASE; PROTEIN CSB; PROTEIN UVSSA; PYRIMIDINE DIMER; RNA POLYMERASE II; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; XERODERMA PIGMENTOSUM GROUP A PROTEIN; 8-HYDROXYGUANINE; CARRIER PROTEIN; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; DRUG DERIVATIVE; ERCC6 PROTEIN, HUMAN; GUANINE; HELICASE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PROTEIN SERINE THREONINE KINASE; TUMOR SUPPRESSOR PROTEIN; UVSSA PROTEIN, HUMAN;

ARTICLE; ATM GENE; COMET ASSAY; COMPARATIVE STUDY; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA TRANSCRIPTION; ENZYME SPECIFICITY; FIBROBLAST; FLUORESCENCE IN SITU HYBRIDIZATION; GENE TARGETING; GENOME ANALYSIS; HUMAN; HUMAN CELL; IRRADIATION; MOLECULAR PROBE; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SENSITIVITY AND SPECIFICITY; SINGLE STRANDED DNA BREAK; ULTRAVIOLET RADIATION; VALIDATION STUDY; BIOSYNTHESIS; CELL LINE; DNA PROBE; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; METHODOLOGY; PHYSIOLOGY;

CARRIER PROTEINS; CELL CYCLE PROTEINS; CELL LINE; COMET ASSAY; DNA HELICASES; DNA PROBES; DNA REPAIR; DNA REPAIR ENZYMES; DNA-BINDING PROTEINS; GUANINE; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; PROTEIN-SERINE-THREONINE KINASES; PYRIMIDINE DIMERS; RNA POLYMERASE II; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEINS;

EID: 84886813438     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt524     Document Type: Article

References (50)

1. David,S.S., O'Shea,V.L. and Kundu,S. (2007) Base-excision repair of oxidative DNA damage. Nature, 447, 941-950.
2. Hasty,P., Campisi,J., Hoeijmakers,J., van Steeg,H. and Vijg,J. (2003) Aging and genome maintenance: lessons from the mouse? Science, 299, 1355-1359.
3. Cooke,M.S., Evans,M.D., Dizdaroglu,M. and Lunec,J. (2003) Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J., 17, 1195-1214.
4. Klungland,A., Rosewell,I., Hollenbach,S., Larsen,E., Daly,G., Epe,B., Seeberg,E., Lindahl,T. and Barnes,D.E. (1999) Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage. Proc. Natl Acad. Sci. USA, 96, 13300-13305.
5. Grollman,A.P. and Moriya,M. (1993) Mutagenesis by 8- oxoguanine: an enemy within. Trends Genet., 9, 246-249.
6. Saxowsky,T.T., Meadows,K.L., Klungland,A. and Doetsch,P.W. (2008) 8-Oxoguanine-mediated transcriptional mutagenesis causes Ras activation in mammalian cells. Proc. Natl Acad. Sci. USA, 105, 18877-18882.
7. Bohr,V.A., Smith,C.A., Okumoto,D.S. and Hanawalt,P.C. (1985) DNA repair in an active gene: removal of pyrimidine dimers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell, 40, 359-369.
8. Mellon,I., Spivak,G. and Hanawalt,P.C. (1987) Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell, 51, 241-249.
9. Hanawalt,P.C. and Spivak,G. (2008) Transcription-coupled DNA repair: two decades of progress and surprises. Nat. Rev. Mol. Cell Biol., 9, 958-970.
10. Tornaletti,S. and Pfeifer,G.P. (1994) Slow repair of pyrimidine dimers at p53 mutation hotspots in skin cancer. Science, 263, 1436-1438.
11. Reis,A.M., Mills,W.K., Ramachandran,I., Friedberg,E.C., Thompson,D. and Queimado,L. (2012) Targeted detection of in vivo endogenous DNA base damage reveals preferential base excision repair in the transcribed strand. Nucleic Acids Res., 40, 206-219.
12. Banerjee,D., Mandal,S.M., Das,A., Hegde,M.L., Das,S., Bhakat,K.K., Boldogh,I., Sarkar,P.S., Mitra,S. and Hazra,T.K. (2011) Preferential repair of oxidized base damage in the transcribed genes of mammalian cells. J. Biol. Chem., 286, 6006-6016.
13. Cabiscol,E., Piulats,E., Echave,P., Herrero,E. and Ros,J. (2000) Oxidative stress promotes specific protein damage in Saccharomyces cerevisiae. J. Biol. Chem., 275, 27393-27398.
14. Farmer,E.E. and Mueller,M.J. (2013) ROS-Mediated Lipid Peroxidation and RES-Activated Signaling. Annu. Rev. Plant. Biol., 64, 429-450.
15. Cadet,J., Douki,T., Gasparutto,D. and Ravanat,J.L. (2003) Oxidative damage to DNA: formation, measurement and biochemical features. Mutat. Res., 531, 5-23.
16. Spivak,G. and Hanawalt,P.C. (2006) Host cell reactivation of plasmids containing oxidative DNA lesions is defective in Cockayne syndrome but wild type in UV-sensitive syndrome fibroblasts. DNA Repair (Amst), 5, 13-22.
17. Sancar,A. and Rupp,W.D. (1983) A novel repair enzyme: UVRABC excision nuclease of Escherichia coli cuts a DNA strand on both sides of the damaged region. Cell, 33, 249-260.
18. Radicella,J.P., Dherin,C., Desmaze,C., Fox,M.S. and Boiteux,S. (1997) Cloning and characterization of hOGG1, a human homolog of the OGG1 gene of Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA, 94, 8010-8015.
19. Spivak,G., Cox,R.A. and Hanawalt,P.C. (2009) New applications of the comet assay: comet-FISH and transcription-coupled DNA repair. Mutat. Res., 681, 44-50.
20. Horváthová ,E., Dusinská ,M., Shaposhnikov,S. and Collins,A.R. (2004) DNA damage and repair measured in different genomic regions using the comet assay with fluorescent in situ hybridization. Mutagenesis, 19, 269-276.
21. Canman,C.E., Lim,D.S., Cimprich,K.A., Taya,Y., Tamai,K., Sakaguchi,K., Appella,E., Kastan,M.B. and Siliciano,J.D. (1998) Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science, 281, 1677-1679.
22. Gately,D.P., Hittle,J.C., Chan,G.K. and Yen,T.J. (1998) Characterization of ATM expression, localization, and associated DNA-dependent protein kinase activity. Mol. Biol. Cell, 9, 2361-2374.
23. Shaposhnikov,S.A., Salenko,V.B., Brunborg,G., Nygren,J. and Collins,A.R. (2008) Single-cell gel electrophoresis (the comet assay): loops or fragments? Electrophoresis, 29, 3005-3012.
24. Rechendorff,K., Witz,G., Adamcik,J. and Dietler,G. (2009) Persistence length and scaling properties of single-stranded DNA adsorbed on modified graphite. J. Chem. Phys., 131, 095103.
25. Rapp,A., Hausmann,M. and Greulich,K.O. (2005) The comet-FISH technique: a tool for detection of specific DNA damage and repair. Methods Mol. Biol., 291, 107-119.
26. Levsky,J.M., Shenoy,S.M., Pezo,R.C. and Singer,R.H. (2002) Single-cell gene expression profiling. Science, 297, 836-840.
27. Downes,C.S., Collins,A.R. and Johnson,R.T. (1979) DNA damage in synchronized HeLa cells irradiated with ultraviolet. Biophys. J., 25, 129-150.
28. Douki,T., Court,M., Sauvaigo,S., Odin,F. and Cadet,J. (2000) Formation of the main UV-induced thymine dimeric lesions within isolated and cellular DNA as measured by high performance liquid chromatography-tandem mass spectrometry. J. Biol. Chem., 275, 11678-11685.
29. Will,O., Mahler,H.C., Arrigo,A.P. and Epe,B. (1999) Influence of glutathione levels and heat-shock on the steady-state levels of oxidative DNA base modifications in mammalian cells. Carcinogenesis, 20, 333-337.
30. Kasai,H., Nishimura,S., Kurokawa,Y. and Hayashi,Y. (1987) Oral administration of the renal carcinogen, potassium bromate, specifically produces 8-hydroxydeoxyguanosine in rat target organ DNA. Carcinogenesis, 8, 1959-1961.
31. Parlanti,E., D'Errico,M., Degan,P., Calcagnile,A., Zijno,A., van der Pluijm,I., van der Horst,G.T., Biard,D.S. and Dogliotti,E. (2012) The cross talk between pathways in the repair of 8-oxo-7,8-dihydroguanine in mouse and human cells. Free Radic. Biol. Med., 53, 2171-2177.
32. Hollenbach,S., Dhénaut,A., Eckert,I., Radicella,J.P. and Epe,B. (1999) Overexpression of Ogg1 in mammalian cells: effects on induced and spontaneous oxidative DNA damage and mutagenesis. Carcinogenesis, 20, 1863-1868.
33. Tuo,J., Müftüoglu,M., Chen,C., Jaruga,P., Selzer,R.R. Jr, Brosh,R.M., Rodriguez,H., Dizdaroglu,M. and Bohr,V.A. (2001) The Cockayne Syndrome group B gene product is involved in general genome base excision repair of 8-hydroxyguanine in DNA. J. Biol. Chem., 276, 45772-45779.
34. Ropolo,M., Degan,P., Foresta,M., D'Errico,M., Lasiglie,D., Dogliotti,E., Casartelli,G., Zupo,S., Poggi,A. and Frosina,G. (2007) Complementation of the oxidatively damaged DNA repair defect in Cockayne syndrome A and B cells by Escherichia coli formamidopyrimidine DNA glycosylase. Free Radic. Biol. Med., 42, 1807-1817.
35. D'Errico,M., Parlanti,E., Teson,M., Degan,P., Lemma,T., Calcagnile,A., Iavarone,I., Jaruga,P., Ropolo,M., Pedrini,A.M. et al. (2007) The role of CSA in the response to oxidative DNA damage in human cells. Oncogene, 26, 4336-4343.
36. Scheibye-Knudsen,M., Ramamoorthy,M., Sykora,P., Maynard,S., Lin,P.C., Minor,R.K. III, Wilson,D.M., Cooper,M., Spencer,R., de Cabo,R. et al. (2012) Cockayne syndrome group B protein prevents the accumulation of damaged mitochondria by promoting mitochondrial autophagy. J. Exp. Med., 209, 855-869.
37. Pascucci,B., Lemma,T., Iorio,E., Giovannini,S., Vaz,B., Iavarone,I., Calcagnile,A., Narciso,L., Degan,P., Podo,F. et al. (2012) An altered redox balance mediates the hypersensitivity of Cockayne syndrome primary fibroblasts to oxidative stress. Aging Cell, 11, 520-529.
38. Spivak,G., Itoh,T., Matsunaga,T., Nikaido,O., Hanawalt,P.C. and Yamaizumi,M (2002) Ultraviolet-sensitive syndrome cells are defective in transcription-coupled repair of cyclobutane pyrimidine dimers. DNA Repair (Amst), 1, 629-643.
39. Pastoriza-Gallego,M., Armier,J. and Sarasin,A. (2007) Transcription through 8-oxoguanine in DNA repair-proficient and Csb-/Ogg1- DNA repair-deficient mouse embryonic fibroblasts is dependent upon promoter strength and sequence context. Mutagenesis, 22, 343-351.
40. Charlet-Berguerand,N., Feuerhahn,S., Kong,S.E., Ziserman,H., Conaway,J.W., Conaway,R. and Egly,J.M. (2006) RNA polymerase II bypass of oxidative DNA damage is regulated by transcription elongation factors. EMBO J., 25, 5481-5491.
41. Nicholl,I.D., Nealon,K. and Kenny,M.K. (1997) Reconstitution of human base excision repair with purified proteins. Biochemistry, 36, 7557-7566.
42. Tornaletti,S., Maeda,L.S., Kolodner,R.D. and Hanawalt,P.C. (2004) Effect of 8-oxoguanine on transcription elongation by T7 RNA polymerase and mammalian RNA polymerase II. DNA Repair (Amst), 3, 483-494.
43. Larsen,E., Kwon,K., Coin,F., Egly,J.M. and Klungland,A. (2004) Transcription activities at 8-oxoG lesions in DNA. DNA Repair (Amst), 3, 1457-1468.
44. Tornaletti,S., Maeda,L.S. and Hanawalt,P.C. (2006) Transcription arrest at an abasic site in the transcribed strand of template DNA. Chem. Res. Toxicol., 19, 1215-1220.
45. Kitsera,N., Stathis,D., Lühnsdorf,B., Müller,H., Carell,T., Epe,B. and Khobta,A. (2011) 8-Oxo-7,8-dihydroguanine in DNA does not constitute a barrier to transcription, but is converted into transcription-blocking damage by OGG1. Nucleic Acids Res., 39, 5926-5934.
46. Letessier,A., Millot,G.A., Koundrioukoff,S., Lachages,A.M., Vogt,N., Hansen,R.S., Malfoy,B., Brison,O. and Debatisse,M. (2011) Cell-type-specific replication initiation programs set fragility of the FRA3B fragile site. Nature, 470, 120-123.
47. Nabel,C.S. and Kohli,R.M. (2011) Demystifying DNA demethylation. Science, 333, 1229-12230.
48. Reijns,M.A., Rabe,B., Rigby,R.E., Mill,P., Astell,K.R., Lettice,L.A., Boyle,S., Leitch,A., Keighren,M., Kilanowski,F. et al. (2012) Enzymatic removal of ribonucleotides from DNA is essential for mammalian genome integrity and development. Cell, 149, 1008-1022.
49. Guo,J., Wang,S., Dai,N., Teo,Y.N. and Kool,E.T. (2011) Multispectral labeling of antibodies with polyfluorophores on a DNA backbone and application in cellular imaging. Proc. Natl Acad. Sci. USA, 108, 3493-3498.
50. Wood,D.K., Weingeist,D.M., Bhatia,S.N. and Engelward,B.P. (2010) Single cell trapping and DNA damage analysis using microwell arrays. Proc. Natl Acad. Sci. USA, 107, 10008-10013.