Global genome nucleotide excision repair is organized into domains that promote efficient DNA repair in chromatin

Genome Research

Volumn 26, Issue 10, 2016, Pages 1376-1387

  Yu, Shirong ^a,c,d   Evans, Katie ^a,c   Van Eijk, Patrick ^a   Bennett, Mark ^a   Webster, Richard M ^a   Leadbitter, Matthew ^a   Teng, Yumin ^a   Waters, Raymond ^a   Jackson, Stephen P ^b   Reed, Simon H ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c CAMBRIDGE EPIGENETIX   (United Kingdom)

^d CRESCENDO BIOLOGICS LTD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL DNA; GENOMIC DNA; HISTONE ACETYLTRANSFERASE GCN5; HISTONE H3; GCN5 PROTEIN, S CEREVISIAE; HISTONE; HISTONE ACETYLTRANSFERASE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; BUDDING YEAST; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; DNA FLANKING REGION; EXCISION REPAIR; FUNGAL GENOME; HISTONE ACETYLATION; NONHUMAN; PRIORITY JOURNAL; ULTRAVIOLET IRRADIATION; ACETYLATION; DNA REPAIR; GENETICS; METABOLISM; MUTATION RATE; PROTEIN PROCESSING; SACCHAROMYCES CEREVISIAE;

ACETYLATION; CHROMATIN; DNA REPAIR; GENOME, FUNGAL; HISTONE ACETYLTRANSFERASES; HISTONES; MUTATION RATE; PROTEIN PROCESSING, POST-TRANSLATIONAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84989844852     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.209106.116     Document Type: Article

References (48)

1. Adam S, Dabin J, Polo SE. 2015. Chromatin plasticity in response to DNA damage: the shape of things to come. DNA Repair (Amst) 32: 120-126.
2. Adar S, Hu J, Lieb JD, Sancar A. 2016. Genome-wide kinetics of DNA excision repair in relation to chromatin state and mutagenesis. Proc Natl Acad Sci 113: E2124-E2133.
3. Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SA, Behjati S, Biankin AV, Bignell GR, Bolli N, Borg A, Borresen-Dale AL, et al. 2013a. Signatures of mutational processes in human cancer. Nature 500: 415-421.
4. Alexandrov LB, Nik-Zainal S, Wedge DC, Campbell PJ, Stratton MR. 2013b. Deciphering signatures of mutational processes operative in human cancer. Cell Rep 3: 246-259.
5. Bennett M, Evans KE, Yu S, Teng Y, Webster RM, Powell J, Waters R, Reed SH. 2015. Sandcastle: software for revealing latent information in multiple experimental ChIP-chip datasets via a novel normalisation procedure. Sci Rep 5: 13395.
6. Boscheron C, Maillet L, Marcand S, Tsai-Pflugfelder M, Gasser SM, Gilson E. 1996. Cooperation at a distance between silencers and proto-silencers at the yeast HML locus. EMBO J 15: 2184-2195.
7. Buchman AR, Kimmerly WJ, Rine J, Kornberg RD. 1988. Two DNA-binding factors recognize specific sequences at silencers, upstream activating sequences, autonomously replicating sequences, and telomeres in Saccharomyces cerevisiae. Mol Cell Biol 8: 210-225.
8. The Cancer Genome Atlas Research Network, Weinstein JN, Collisson EA, Mills GB, Shaw KRM, Ozenberger BA, Ellrott K, Shmulevich I, Sander C, Stuart JM. 2013. The Cancer Genome Atlas Pan-Cancer analysis project. Nat Genet 45: 1113-1120.
9. Flaus A, Owen-Hughes T. 2011. Mechanisms for ATP-dependent chromatin remodelling: the means to the end. FEBS J 278: 3579-3595.
10. Fousteri M, Mullenders LH. 2008. Transcription-coupled nucleotide excision repair in mammalian cells: molecular mechanisms and biological effects. Cell Res 18: 73-84.
11. Friedberg EC. 2003. DNA damage and repair. Nature 421: 436-440.
12. Ganapathi M, Palumbo MJ, Ansari SA, He Q, Tsui K, Nislow C, Morse RH. 2011. Extensive role of the general regulatory factors, Abf1 and Rap1, in determining genome-wide chromatin structure in budding yeast. Nucleic Acids Res 39: 2032-2044.
13. Gillette TG, Yu S, Zhou Z, Waters R, Johnston SA, Reed SH. 2006. Distinct functions of the ubiquitin-proteasome pathway influence nucleotide excision repair. EMBO J 25: 2529-2538.
14. Haradhvala NJ, Polak P, Stojanov P, Covington KR, Shinbrot E, Hess JM, Rheinbay E, Kim J, Maruvka YE, Braunstein LZ, et al. 2016. Mutational strand asymmetries in cancer genomes reveal mechanisms of DNA damage and repair. Cell 164: 538-549.
15. Hartley PD, Madhani HD. 2009. Mechanisms that specify promoter nucleosome location and identity. Cell 137: 445-458.
16. Hoeijmakers JH. 1993. Nucleotide excision repair I: from E. coli to yeast. Trends Genet 9: 173-177.
17. Hoeijmakers JHJ. 1994. Human nucleotide excision-repair syndromes: molecular clues to unexpected intricacies. Eur J Cancer 30A: 1912-1921.
18. Holmquist GP, Gao S. 1997. Somatic mutation theory, DNA repair rates, and the molecular epidemiology of p53 mutations. Mutat Res 386: 69-101.
19. Hu J, Adar S, Selby CP, Lieb JD, Sancar A. 2015. Genome-wide analysis of human global and transcription-coupled excision repair of UV damage at single-nucleotide resolution. Genes Dev 29: 948-960.
20. Kapetanaki MG, Guerrero-Santoro J, Bisi DC, Hsieh CL, Rapic-Otrin V, Levine AS. 2006. The DDB1-CUL4ADDB2 ubiquitin ligase is deficient in xeroderma pigmentosum group E and targets histone H2A at UV-damaged DNA sites. Proc Natl Acad Sci 103: 2588-2593.
21. Kasinathan S, Orsi GA, Zentner GE, Ahmad K, Henikoff S. 2014. High-resolution mapping of transcription factor binding sites on native chromatin. Nat Methods 11: 203-209.
22. Lan L, Nakajima S, Kapetanaki MG, Hsieh CL, Fagerburg M, Thickman K, Rodriguez-Collazo P, Leuba SH, Levine AS, Rapic-Otrin V. 2012. Monoubiquitinated histone H2A destabilizes photolesion-containing nucleosomes with concomitant release of UV-damaged DNA-binding protein E3 ligase. J Biol Chem 287: 12036-12049.
23. Mellon I, Spivak G, Hanawalt PC. 1987. Selective removal of transcriptionblocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell 51: 241-249.
24. Miyake T, Reese J, Loch CM, Auble DT, Li R. 2004. Genome-wide analysis of ARS (autonomously replicating sequence) binding factor 1 (Abf1p)-mediated transcriptional regulation in Saccharomyces cerevisiae. J Biol Chem 279: 34865-34872.
25. Nik-Zainal S, Alexandrov LB, Wedge DC, Van Loo P, Greenman CD, Raine K, Jones D, Hinton J, Marshall J, Stebbings LA, et al. 2012. Mutational processes molding the genomes of 21 breast cancers. Cell 149: 979-993.
26. Ozonov EA, van Nimwegen E. 2013. Nucleosome free regions in yeast promoters result from competitive binding of transcription factors that interact with chromatin modifiers. PLoS Comput Biol 9: e1003181.
27. Perera D, Poulos RC, Shah A, Beck D, Pimanda JE, Wong JW. 2016. Differential DNA repair underlies mutation hotspots at active promoters in cancer genomes. Nature 532: 259-263.
28. Pintard L, Willems A, Peter M. 2004. Cullin-based ubiquitin ligases: Cul3-BTB complexes join the family. EMBO J 23: 1681-1687.
29. Polo SE. 2015. Reshaping chromatin after DNA damage: the choreography of histone proteins. J Mol Biol 427: 626-636.
30. 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.
31. R Core Team. 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.Rproject.org/.
32. Ramsey KL, Smith JJ, Dasgupta A, Maqani N, Grant P, Auble DT. 2004. The NEF4 complex regulates Rad4 levels and utilizes Snf2/Swi2-related ATPase activity for nucleotide excision repair. Mol Cell Biol 24: 6362-6378.
33. Reed SH, Akiyama M, Stillman B, Friedberg EC. 1999. Yeast autonomously replicating sequence binding factor is involved in nucleotide excision repair. Genes Dev 13: 3052-3058.
34. Rhode PR, Elsasser S, Campbell JL. 1992. Role of multifunctional autonomously replicating sequence binding factor 1 in the initiation of DNA replication and transcriptional control in Saccharomyces cerevisiae. Mol Cell Biol 12: 1064-1077.
35. Sabarinathan R, Mularoni L, Deu-Pons J, Gonzalez-Perez A, Lopez-Bigas N. 2016. Nucleotide excision repair is impaired by binding of transcription factors to DNA. Nature 532: 264-267.
36. Schlecht U, Erb I, Demougin P, Robine N, Borde V, van Nimwegen E, Nicolas A, Primig M. 2008. Genome-wide expression profiling, in vivo DNA binding analysis, and probabilistic motif prediction reveal novel Abf1 target genes during fermentation, respiration, and sporulation in yeast. Mol Biol Cell 19: 2193-2207.
37. Teng Y, Bennett M, Evans KE, Zhuang-Jackson H, Higgs A, Reed SH, Waters R. 2011. A novel method for the genome-wide high resolution analysis of DNA damage. Nucleic Acids Res 39: e10.
38. Verhage R, Zeeman AM, Degroot N, Gleig F, Bang DD, Vandeputte P, Brouwer J. 1994. The RAD7 and RAD16 genes, which are essential for pyrimidine dimer removal from the silent mating type loci, are also required for repair of the nontranscribed strand of an active gene in Saccharomyces cerevisiae. Mol Cell Biol 14: 6135-6142.
39. Willems AR, Schwab M, Tyers M. 2004. A hitchhiker's guide to the cullin ubiquitin ligases: SCF and its kin. Biochim Biophys Acta 1695: 133-170.
40. Yarragudi A, Parfrey LW, Morse RH. 2007. Genome-wide analysis of transcriptional dependence and probable target sites for Abf1 and Rap1 in Saccharomyces cerevisiae. Nucleic Acids Res 35: 193-202.
41. Yu S, Owen-Hughes T, Friedberg EC, Waters R, Reed SH. 2004. The yeast Rad7/Rad16/Abf1 complex generates superhelical torsion in DNA that is required for nucleotide excision repair. DNA Repair 3: 277-287.
42. Yu Y, Teng Y, Liu H, Reed SH, Waters R. 2005. UV irradiation stimulates histone acetylation and chromatin remodeling at a repressed yeast locus. Proc Natl Acad Sci 102: 8650-8655.
43. Yu S, Smirnova JB, Friedberg EC, Stillman B, Akiyama M, Owen-Hughes T, Waters R, Reed SH. 2009. ABF1-binding sites promote efficient global genome nucleotide excision repair. J Biol Chem 284: 966-973.
44. Yu S, Teng Y, Waters R, Reed SH. 2011. How chromatin is remodelled during DNA repair of UV-induced DNA damage in Saccharomyces cerevisiae. PLoS Genet 7: e1002124.
45. Zentner GE, Kasinathan S, Xin B, Rohs R, Henikoff S. 2015. ChEC-seq kinetics discriminates transcription factor binding sites by DNA sequence and shape in vivo. Nat Commun 6: 8733.
46. Zhang X, Yu Q, Olsen L, Bi X. 2012. Functions of protosilencers in the formation and maintenance of heterochromatin in Saccharomyces cerevisiae. PLoS One 7: e37092.
47. Zhou Z, Humphryes N, van Eijk P, Waters R, Yu S, Kraehenbuehl R, Hartsuiker E, Reed SH. 2015. UV induced ubiquitination of the yeast Rad4-Rad23 complex promotes survival by regulating cellular dNTP pools. Nucleic Acids Res 43: 7360-7370.
48. Zou Y, Yu Q, Bi X. 2006. Asymmetric positioning of nucleosomes and directional establishment of transcriptionally silent chromatin by Saccharomyces cerevisiae silencers. Mol Cell Biol 26: 7806-7819.