Genome-wide analysis of human global and transcription-coupled excision repair of UV damage at single-nucleotide resolution

Genes and Development

Volumn 29, Issue 9, 2015, Pages 948-960

  Hu, Jinchuan ^a   Adar, Sheera ^b   Selby, Christopher P ^a   Lieb, Jason D ^c   Sancar, Aziz ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

Divergent transcription; Genome wide; Nucleotide excision repair; Transcription coupled repair; UV damage

Indexed keywords

PYRIMIDINE; PYRIMIDINE DIMER; RNA; NUCLEOTIDE; PYRIMIDINE-PYRIMIDONE DIMER;

ARTICLE; AUTORADIOGRAPHY; CELL MUTANT; CHROMATIN; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; EXCISION REPAIR; GENETIC ASSOCIATION; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INCISION; PRIORITY JOURNAL; PROMOTER REGION; RADIATION INJURY; TRANSCRIPTION INITIATION SITE; ULTRAVIOLET RADIATION; WILD TYPE; CELL LINE; ENHANCER REGION; GENETIC TRANSCRIPTION; GENETICS; RADIATION RESPONSE;

CELL LINE; DNA DAMAGE; DNA REPAIR; ENHANCER ELEMENTS, GENETIC; GENOME-WIDE ASSOCIATION STUDY; HUMANS; NUCLEOTIDES; PROMOTER REGIONS, GENETIC; PYRIMIDINE DIMERS; TRANSCRIPTION, GENETIC; ULTRAVIOLET RAYS;

EID: 84929463303     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.261271.115     Document Type: Article

References (64)

1. Adam S, Polo SE, Almouzni G. 2014. How to restore chromatin structure and function in response to DNA damage— let the chaperones play. Delivered on 9 July 2013 at the 38th FEBS Congress in St Petersburg, Russia. FEBS J 281: 2315-2323.
2. Anders S, Pyl PT, Huber W. 2014. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31: 166-169.
3. Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114-2120.
4. Bryan DS, Ransom M, Adane B, York K, Hesselberth JR. 2014. High resolution mapping of modified DNA nucleobases using excision repair enzymes. Genome Res 24: 1534-1542.
5. Choi JH, Gaddameedhi S, Kim SY, Hu J, Kemp MG, Sancar A. 2014. Highly specific and sensitive method for measuring nucleotide excision repair kinetics of ultraviolet photoproducts in human cells. Nucleic Acids Res 42: e29.
6. Cleaver JE, Lam ET, Revet I. 2009. Disorders of nucleotide excision repair: the genetic and molecular basis of heterogeneity. Nat Rev Genet 10: 756-768.
7. Core LJ, Waterfall JJ, Lis JT. 2008. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 322: 1845-1848.
8. Core LJ, Martins AL, Danko CG, Waters CT, Siepel A, Lis JT. 2014. Analysis of nascent RNA identifies a unified architecture of initiation regions at mammalian promoters and enhancers. Nat Genet 46: 1311-1320.
9. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp PA, et al. 2010. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci 107: 21931-21936.
10. Denissenko MF, Pao A, Tang M, Pfeifer GP. 1996. Preferential formation of benzo[a]pyrene adducts at lung cancer mutational hotspots in P53. Science 274: 430-432.
11. Douki T, Cadet J. 2001. Individual determination of the yield of the main UV-induced dimeric pyrimidine photoproducts in DNA suggests a high mutagenicity of CC photolesions. Biochemistry 40: 2495-2501.
12. Drapkin R, Reardon JT, Ansari A, Huang JC, Zawel L, Ahn K, Sancar A, Reinberg D. 1994. Dual role of TFIIH in DNA excision repair and in transcription by RNA polymerase II. Nature 368: 769-772.
13. The ENCODE Project Consortium. 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489: 57-74.
14. Ernst J, Kellis M. 2010. Discovery and characterization of chromatin states for systematic annotation of the human genome. Nat Biotechnol 28: 817-825.
15. Fong YW, Cattoglio C, Tjian R. 2013. The intertwined roles of transcription and repair proteins. Mol Cell 52: 291-302.
16. Gaddameedhi S, Kemp MG, Reardon JT, Shields JM, Smith-Roe SL, Kaufmann WK, Sancar A. 2010. Similar nucleotide excision repair capacity in melanocytes and melanoma cells. Cancer Res 70: 4922-4930.
17. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA. 2007. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130: 77-88.
18. Gyenis A, Umlauf D, Ujfaludi Z, Boros I, Ye T, Tora L. 2014. UVB induces a genome-wide acting negative regulatory mechanism that operates at the level of transcription initiation in human cells. PLoS Genet 10: e1004483.
19. Hah N, Murakami S, Nagari A, Danko CG, Kraus WL. 2013. Enhancer transcripts mark active estrogen receptor binding sites. Genome Res 23: 1210-1223.
20. Hanawalt PC, Spivak G. 2008. Transcription-coupled DNA repair: two decades of progress and surprises. Nat Rev Mol Cell Biol 9: 958-970.
21. Heffernan TP, Simpson DA, Frank AR, Heinloth AN, Paules RS, Cordeiro-Stone M, Kaufmann WK. 2002. An ATR- and Chk1-dependent S checkpoint inhibits replicon initiation following UVC-induced DNA damage. Mol Cell Biol 22: 8552-8561.
22. Hu J, Choi JH, Gaddameedhi S, Kemp MG, Reardon JT, Sancar A. 2013. Nucleotide excision repair in human cells: fate of the excised oligonucleotide carrying DNA damage in vivo. J Biol Chem 288: 20918-20926.
23. Huang JC, Svoboda DL, Reardon JT, Sancar A. 1992. Human nucleotide excision nuclease removes thymine dimers from DNA by incising the 22nd phosphodiester bond 5′ and the 6th phosphodiester bond 3′ to the photodimer. Proc Natl Acad Sci 89: 3664-3668.
24. Kemp MG, Reardon JT, Lindsey-Boltz LA, Sancar A. 2012. Mechanism of release and fate of excised oligonucleotides during nucleotide excision repair. J Biol Chem 287: 22889-22899.
25. Kemp MG, Gaddameedhi S, Choi JH, Hu J, Sancar A. 2014. DNA repair synthesis and ligation affect the processing of excised oligonucleotides generated by human nucleotide excision repair. J Biol Chem 289: 26574-26583.
26. Kim TH, Barrera LO, Zheng M, Qu C, Singer MA, Richmond TA, WuY, Green RD, Ren B. 2005.Ahigh-resolution map of active promoters in the human genome. Nature 436: 876-880.
27. Kim TK, Hemberg M, Gray JM, Costa AM, Bear DM, Wu J, Harmin DA, Laptewicz M, Barbara-Haley K, Kuersten S, et al. 2010. Widespread transcription at neuronal activity-regulated enhancers. Nature 465: 182-187.
28. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. 2013. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14: R36.
29. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
30. Le May N, Mota-Fernandes D, Velez-Cruz R, Iltis I, Biard D, Egly JM. 2010.NERfactors are recruited to active promoters and facilitate chromatin modification for transcription in the absence of exogenous genotoxic attack. Mol Cell 38: 54-66.
31. Li S, Waters R, Smerdon MJ. 2000. Low- and high-resolution mapping of DNA damage at specific sites. Methods 22: 170-179.
32. Li W, Selvam K, Ko T, Li S. 2014. Transcription bypass of DNA lesions enhances cell survival but attenuates transcription coupled DNA repair. Nucleic Acids Res 42: 13242-13253.
33. Lindsey-Boltz LA, Sancar A. 2007. RNA polymerase: the most specific damage recognition protein in cellular responses to DNA damage? Proc Natl Acad Sci 104: 13213-13214.
34. Mellon I, Spivak G, Hanawalt PC. 1987. Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell 51: 241-249.
35. Mitchell DL. 1988. The relative cytotoxicity of (6-4) photoproducts and cyclobutane dimers in mammalian cells. Photochem Photobiol 48: 51-57.
36. Mitchell DL, Jen J, Cleaver JE. 1992. Sequence specificity of cyclobutane pyrimidine dimers in DNA treated with solar (ultraviolet B) radiation. Nucleic Acids Res 20: 225-229.
37. Mu D, Park CH, Matsunaga T, Hsu DS, Reardon JT, Sancar A. 1995. Reconstitution of human DNA repair excision nuclease in a highly defined system. J Biol Chem 270: 2415-2418.
38. Mu D, Hsu DS, Sancar A. 1996. Reaction mechanism of human DNA repair excision nuclease. J Biol Chem 271: 8285-8294.
39. Mu D, Tursun M, Duckett DR, Drummond JT, Modrich P, Sancar A. 1997. Recognition and repair of compound DNA lesions (base damage and mismatch) by human mismatch repair and excision repair systems. Mol Cell Biol 17: 760-769.
40. Pavlidis P, Noble WS. 2003. Matrix2png: a utility for visualizing matrix data. Bioinformatics 19: 295-296.
41. Pfeifer GP, Drouin R, Riggs AD, Holmquist GP. 1991. In vivo mapping of a DNA adduct at nucleotide resolution: detection of pyrimidine (6-4) pyrimidone photoproducts by ligation-mediated polymerase chain reaction. Proc Natl Acad Sci 88: 1374-1378.
42. Powell JR, Bennett MR, Evans KE, Yu S, Webster RM, Waters R, Skinner N, Reed SH. 2015. 3D-DIP-Chip: a microarray-based method to measure genomic DNA damage. Sci Rep 5: 7975.
43. Reardon JT, Sancar A. 2003. Recognition and repair of the cyclobutane thymine dimer, a major cause of skin cancers, by the human excision nuclease. Genes Dev 17: 2539-2551.
44. Reardon JT, Sancar A. 2005. Nucleotide excision repair. Prog Nucleic Acid Res Mol Biol 79: 183-235.
45. Sancar A. 1996. DNA excision repair. Annu Rev Biochem 65: 43-81.
46. Selby CP, Sancar A. 1993. Molecular mechanism of transcriptionrepair coupling. Science 260: 53-58.
47. Selby CP, Sancar A. 2006.Acryptochrome/photolyase class of enzymes with single-stranded DNA-specific photolyase activity. Proc Natl Acad Sci 103: 17696-17700.
48. Selby CP, Sancar A. 2012. The second chromophore in Drosophila photolyase/cryptochrome family photoreceptors. Biochemistry 51: 167-171.
49. Selby CP, Drapkin R, Reinberg D, Sancar A. 1997. RNA polymerase II stalled at a thymine dimer: footprint and effect on excision repair. Nucleic Acids Res 25: 787-793.
50. Shin H, Liu T, Manrai AK, Liu XS. 2009. CEAS: cis-regulatory element annotation system. Bioinformatics 25: 2605-2606.
51. Sugasawa K, Ng JM, Masutani C, Iwai S, van der Spek PJ, Eker AP, Hanaoka F, Bootsma D, Hoeijmakers JH. 1998. Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol Cell 2: 223-232.
52. Svoboda DL, Taylor JS, Hearst JE, Sancar A. 1993. DNA repair by eukaryotic nucleotide excision nuclease. Removal of thymine dimer and psoralen monoadduct by HeLa cell-free extract and of thymine dimer by Xenopus laevis oocytes. J Biol Chem 268: 1931-1936.
53. Teng Y, Bennett M, Evans KE, Zhuang-Jackson H, Higgs A, Reed SH, Waters R. 2011.Anovel method for the genome-wide high resolution analysis of DNA damage. Nucleic Acids Res 39: e10.
54. Tornaletti S, Pfeifer GP. 1994. Slow repair of pyrimidine dimmers at p53 mutation hotspots in skin cancer. Science 263: 1436-1438.
55. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515.
56. van Hoffen A, Venema J, Meschini R, van Zeeland AA, Mullenders LH. 1995. Transcription-coupled repair removes both cyclobutane pyrimidine dimers and 6-4 photoproducts with equal efficiency and in a sequential way from transcribed DNA in xeroderma pigmentosum group C fibroblasts. EMBO J 14: 360-367.
57. van Vuuren AJ, Vermeulen W, Ma L, Weeda G, Appeldoorn E, Jaspers NG, van der Eb AJ, Bootsma D, Hoeijmakers JH, Humbert S, et al. 1994. Correction of xeroderma pigmentosum repair defect by basal transcription factor BTF2 (TFIIH). EMBO J 13: 1645-1653.
58. Venema J, Mullenders LH, Natarajan AT, van Zeeland AA, Mayne LV. 1990. The genetic defect in Cockayne syndrome is associated with a defect in repair of UV-induced DNA damage in transcriptionally active DNA. Proc Natl Acad Sci 87: 4707-4711.
59. Venema J, van Hoffen A, Karcagi V, Natarajan AT, van Zeeland AA, Mullenders LH. 1991. Xeroderma pigmentosum complementation group C cells remove pyrimidine dimers selectively from the transcribed strand of active genes. Mol Cell Biol 11: 4128-4134.
60. Wakasugi M, Sancar A. 1998. Assembly, subunit composition, and footprint of human DNA repair excision nuclease. Proc Natl Acad Sci 95: 6669-6674.
61. Wang D, Garcia-Bassets I, Benner C, Li W, Su X, Zhou Y, Qiu J, Liu W, Kaikkonen MU, Ohgi KA, et al. 2011. Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA. Nature 474: 390-394.
62. Wood RD. 1997. Nucleotide excision repair in mammalian cells. J Biol Chem 272: 23465-23468.
63. Zavala AG, Morris RT, Wyrick JJ, Smerdon MJ. 2014. High-resolution characterization of CPD hotspot formation in human fibroblasts. Nucleic Acids Res 42: 893-905.
64. Zentner GE, Tesar PJ, Scacheri PC. 2011. Epigenetic signatures distinguish multiple classes of enhancers with distinct cellular functions. Genome Res 21: 1273-1283.