1932

Abstract

Until recently, DNA damage arising from physiological DNA metabolism was considered a detrimental by-product for cells. However, an increasing amount of evidence has shown that DNA damage could have a positive role in transcription activation. In particular, DNA damage has been detected in transcriptional elements following different stimuli. These physiological DNA breaks are thought to be instrumental for the correct expression of genomic loci through different mechanisms. In this regard, although a plethora of methods are available to precisely map transcribed regions and transcription start sites, commonly used techniques for mapping DNA breaks lack sufficient resolution and sensitivity to draw a robust correlation between DNA damage generation and transcription. Recently, however, several methods have been developed to map DNA damage at single-nucleotide resolution, thus providing a new set of tools to correlate DNA damage and transcription. Here, we review how DNA damage can positively regulate transcription initiation, the current techniques for mapping DNA breaks at high resolution, and how these techniques can benefit future studies of DNA damage and transcription.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genom-091416-035314
2017-08-31
2024-06-21
Loading full text...

Full text loading...

/deliver/fulltext/genom/18/1/annurev-genom-091416-035314.html?itemId=/content/journals/10.1146/annurev-genom-091416-035314&mimeType=html&fmt=ahah

Literature Cited

  1. Adam S, Polo SE. 1.  2014. Blurring the line between the DNA damage response and transcription: the importance of chromatin dynamics. Exp. Cell Res. 329:148–53 [Google Scholar]
  2. Aguilera A. 2.  2002. The connection between transcription and genomic instability. EMBO J 21:195–201 [Google Scholar]
  3. Aguilera A, García-Muse T. 3.  2012. R loops: from transcription byproducts to threats to genome stability. Mol. Cell 46:115–24 [Google Scholar]
  4. Aymard F, Bugler B, Schmidt CK, Guillou E, Caron P. 4.  et al. 2014. Transcriptionally active chromatin recruits homologous recombination at DNA double-strand breaks. Nat. Struct. Mol. Biol. 21:366–74 [Google Scholar]
  5. Baranello L, Kouzine F, Wojtowicz D, Cui K, Przytycka TM. 5.  et al. 2014. DNA break mapping reveals topoisomerase II activity genome-wide. Int. J. Mol. Sci. 15:13111–22 [Google Scholar]
  6. Baranello L, Wojtowicz D, Cui K, Devaiah BN, Chung HJ. 6.  et al. 2016. RNA polymerase II regulates topoisomerase 1 activity to favor efficient transcription. Cell 165:357–71 [Google Scholar]
  7. Bartkova J, Horejsí Z, Koed K, Krämer A, Tort F. 7.  et al. 2005. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434:864–70 [Google Scholar]
  8. Beishline K, Kelly CM, Olofsson BA, Koduri S, Emrich J. 8.  et al. 2012. Sp1 facilitates DNA double-strand break repair through a nontranscriptional mechanism. Mol. Cell. Biol. 32:3790–99 [Google Scholar]
  9. Beletskii A, Bhagwat AS. 9.  1996. Transcription-induced mutations: increase in C to T mutations in the nontranscribed strand during transcription in Escherichia coli. . PNAS 93:13919–24 [Google Scholar]
  10. Beletskii A, Bhagwat AS. 10.  1997. Correlation between transcription and C to T mutations in the non-transcribed DNA strand. Biol. Chem. 379:549–51 [Google Scholar]
  11. Belotserkovskii BP, Liu R, Tornaletti S, Krasilnikova MM, Mirkin SM, Hanawalt PC. 11.  2010. Mechanisms and implications of transcription blockage by guanine-rich DNA sequences. PNAS 107:12816–21 [Google Scholar]
  12. Berthelot V, Mouta-Cardoso G, Hégarat N, Guillonneau F, François J-C. 12.  et al. 2016. The human DNA ends proteome uncovers an unexpected entanglement of functional pathways. Nucleic Acids Res 44:4721–33 [Google Scholar]
  13. Branzei D, Foiani M. 13.  2008. Regulation of DNA repair throughout the cell cycle. Nat. Rev. Mol. Cell Biol. 9:297–308 [Google Scholar]
  14. Bunch H, Lawney BP, Lin Y-F, Asaithamby A, Murshid A. 14.  et al. 2015. Transcriptional elongation requires DNA break-induced signalling. Nat. Commun. 6:10191 [Google Scholar]
  15. Callegari AJ. 15.  2016. Does transcription-associated DNA damage limit lifespan?. DNA Repair 41:1–7 [Google Scholar]
  16. Canela A, Sridharan S, Sciascia N, Tubbs A, Meltzer P. 16.  et al. 2016. DNA breaks and end resection measured genome-wide by end sequencing. Mol. Cell 63.5:898–911 [Google Scholar]
  17. Capozzo I, Iannelli F, Francia S, d'Adda di Fagagna F. 17.  2017. Express or repress? The transcriptional dilemma of damaged chromatin. FEBS J 284:2133–47 [Google Scholar]
  18. Chakraborty A, Tapryal N, Venkova T, Horikoshi N, Pandita RK. 18.  et al. 2016. Classical non-homologous end-joining pathway utilizes nascent RNA for error-free double-strand break repair of transcribed genes. Nat. Commun. 7:13049 [Google Scholar]
  19. Chaudhuri AR, Hashimoto Y, Herrador R, Neelsen KJ, Fachinetti D. 19.  et al. 2012. Topoisomerase I poisoning results in PARP-mediated replication fork reversal. Nat. Struct. Mol. Biol. 19:417–23 [Google Scholar]
  20. Chen J, Zhu F, Weaks RL, Biswas AK, Guo R. 20.  et al. 2011. E2F1 promotes the recruitment of DNA repair factors to sites of DNA double-strand breaks. Cell Cycle 10:1287–94 [Google Scholar]
  21. Chiarle R, Zhang Y, Frock RL, Lewis SM, Molinie B. 21.  et al. 2011. Genome-wide translocation sequencing reveals mechanisms of chromosome breaks and rearrangements in B cells. Cell 147:107–19 [Google Scholar]
  22. Ciccia A, Elledge SJ. 22.  2010. The DNA damage response: making it safe to play with knives. Mol. Cell 40:179–204 [Google Scholar]
  23. Cleaver JE, Lam ET, Revet I. 23.  2009. Disorders of nucleotide excision repair: the genetic and molecular basis of heterogeneity. Nat. Rev. Genet. 10:756–68 [Google Scholar]
  24. Compe E, Egly J-M. 24.  2012. TFIIH: when transcription met DNA repair. Nat. Rev. Mol. Cell Biol. 13:353–54 [Google Scholar]
  25. Cowell IG, Sunter NJ, Singh PB, Austin CA, Durkacz BW, Tilby MJ. 25.  2007. γH2AX foci form preferentially in euchromatin after ionising-radiation. PLOS ONE 2:e1057 [Google Scholar]
  26. Crosetto N, Mitra A, Silva MJ, Bienko M, Dojer N. 26.  et al. 2013. Nucleotide-resolution DNA double-strand break mapping by next-generation sequencing. Nat. Methods 10:361–65 [Google Scholar]
  27. d'Adda di Fagagna F. 27.  2014. A direct role for small non-coding RNAs in DNA damage response. Trends Cell Biol 24:171–78 [Google Scholar]
  28. D'Alessandro G, d'Adda di Fagagna F. 28.  2017. Transcription and DNA damage: holding hands or crossing swords?. J. Mol. Biol. In press. https://doi.org/10.1016/j.jmb.2016.11.002 [Crossref] [Google Scholar]
  29. Datta A, Jinks-Robertson S. 29.  1995. Association of increased spontaneous mutation rates with high levels of transcription in yeast. Science 268:1616–19 [Google Scholar]
  30. David SS, O'Shea VL, Kundu S. 30.  2007. Base-excision repair of oxidative DNA damage. Nature 447:941–50 [Google Scholar]
  31. Dedrick RL, Chamberlin MJ. 31.  1985. Studies on transcription of 3′-extended templates by mammalian RNA polymerase II. Parameters that affect the initiation and elongation reactions. Biochemistry 24:2245–53 [Google Scholar]
  32. Di Micco R, Fumagalli M, Cicalese A, Piccinin S, Gasparini P. 32.  et al. 2006. Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 444:638–42 [Google Scholar]
  33. Di Micco R, Sulli G, Dobreva M, Liontos M, Botrugno O. 33.  et al. 2011. Interplay between oncogene-induced DNA damage response and heterochromatin in senescence and cancer. Nat. Cell Biol. 13:292–302 [Google Scholar]
  34. Dong J, Panchakshari RA, Zhang T, Zhang Y, Hu J. 34.  et al. 2015. Orientation-specific joining of AID-initiated DNA breaks promotes antibody class switching. Nature 525:134–39 [Google Scholar]
  35. Duquette ML, Handa P, Vincent JA, Taylor AF, Maizels N. 35.  2004. Intracellular transcription of G-rich DNAs induces formation of G-loops, novel structures containing G4 DNA. Genes Dev 18:1618–29 [Google Scholar]
  36. Feng W, Di Rienzi SC, Raghuraman MK, Brewer BJ, Sclafani R. 36.  2011. Replication stress-induced chromosome breakage is correlated with replication fork progression and is preceded by single-stranded DNA formation. G3 1:327–35 [Google Scholar]
  37. Flick KE, Jurica MS, Monnat RJ, Stoddard BL. 37.  1998. DNA binding and cleavage by the nuclear intron-encoded homing endonuclease I-PpoI. Nature 394:96–101 [Google Scholar]
  38. Francia S, Michelini F, Saxena A, Tang D, de Hoon M. 38.  et al. 2012. Site-specific DICER and DROSHA RNA products control the DNA-damage response. Nature 488:231–35 [Google Scholar]
  39. French S. 39.  1992. Consequences of replication fork movement through transcription units in vivo. Science 258:1362 [Google Scholar]
  40. Frit P, Kwon K, Coin F, Auriol J, Dubaele S. 40.  et al. 2002. Transcriptional activators stimulate DNA repair. Mol. Cell 10:1391–401 [Google Scholar]
  41. Frock RL, Hu J, Meyers RM, Ho Y, Kii E, Alt FW. 41.  2014. Genome-wide detection of DNA double-stranded breaks induced by engineered nucleases. Nat. Biotechnol. 33:179–86 [Google Scholar]
  42. Fumagalli M, Rossiello F, Clerici M, Barozzi S, Cittaro D. 42.  et al. 2012. Telomeric DNA damage is irreparable and causes persistent DNA-damage-response activation. Nat. Cell Biol. 14:355–65 [Google Scholar]
  43. Gagné J-P, Pic É, Isabelle M, Krietsch J, Éthier C. 43.  et al. 2012. Quantitative proteomics profiling of the poly(ADP-ribose)-related response to genotoxic stress. Nucleic Acids Res 40:7788–805 [Google Scholar]
  44. García-Rubio M, Huertas P, González-Barrera S, Aguilera A. 44.  2003. Recombinogenic effects of DNA-damaging agents are synergistically increased by transcription in Saccharomyces cerevisiae: new insights into transcription-associated recombination. Genetics 165:457–66 [Google Scholar]
  45. Ge H, Martinez E, Chiang C-M, Roeder RG. 45.  1996. Activator-dependent transcription by mammalian RNA polymerase II: in vitro reconstitution with general transcription factors and cofactors. Methods Enzymol 274:57–71 [Google Scholar]
  46. Ghezraoui H, Piganeau M, Renouf B, Renaud J-B, Sallmyr A. 46.  et al. 2014. Chromosomal translocations in human cells are generated by canonical nonhomologous end-joining. Mol. Cell 55:829–42 [Google Scholar]
  47. Goelet P, Castellucci VF, Schacher S, Kandel ER. 47.  1986. The long and the short of long-term memory: a molecular framework. Nature 322:419–22 [Google Scholar]
  48. Gostissa M, Alt FW, Chiarle R. 48.  2011. Mechanisms that promote and suppress chromosomal translocations in lymphocytes. Annu. Rev. Immunol. 29:319–50 [Google Scholar]
  49. Green P, Ewing B, Miller W, Thomas PJ, Green ED. 49.  2003. Transcription-associated mutational asymmetry in mammalian evolution. Nat. Genet. 33:514–17 [Google Scholar]
  50. Grégoire M-C, Massonneau J, Leduc F, Arguin M, Brazeau M-A, Boissonneault G. 50.  2016. Quantification and genome-wide mapping of DNA double-strand breaks. DNA Repair 48:63–68 [Google Scholar]
  51. Guy L, Roten C-AH. 51.  2004. Genometric analyses of the organization of circular chromosomes: a universal pressure determines the direction of ribosomal RNA genes transcription relative to chromosome replication. Gene 340:45–52 [Google Scholar]
  52. Hartung ML, Gruber DC, Koch KN, Grüter L, Rehrauer H. 52.  et al. 2015. H. pylori-induced DNA strand breaks are introduced by nucleotide excision repair endonucleases and promote NF-κB target gene expression. Cell Rep 13:70–79 [Google Scholar]
  53. Helmrich A, Ballarino M, Nudler E, Tora L. 53.  2013. Transcription-replication encounters, consequences and genomic instability. Nat. Struct. Mol. Biol. 20:412–18 [Google Scholar]
  54. Helmrich A, Ballarino M, Tora L. 54.  2011. Collisions between replication and transcription complexes cause common fragile site instability at the longest human genes. Mol. Cell 44:966–77 [Google Scholar]
  55. Herman RK, Dworkin NB. 55.  1971. Effect of gene induction on the rate of mutagenesis by ICR-191 in Escherichia coli. . J. Bacteriol. 106:543–50 [Google Scholar]
  56. Hoeijmakers JH. 56.  2009. DNA damage, aging, and cancer. N. Engl. J. Med. 361:1475–85 [Google Scholar]
  57. Hoffman EA, McCulley A, Haarer B, Arnak R, Feng W. 57.  2015. Break-seq reveals hydroxyurea-induced chromosome fragility as a result of unscheduled conflict between DNA replication and transcription. Genome Res 25:402–12 [Google Scholar]
  58. Hu J, Meyers RM, Dong J, Panchakshari RA, Alt FW, Frock RL. 58.  2016. Detecting DNA double-stranded breaks in mammalian genomes by linear amplification-mediated high-throughput genome-wide translocation sequencing. Nat Protoc 11:853–71 [Google Scholar]
  59. Huertas P, Aguilera A. 59.  2003. Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination. Mol. Cell 12:711–21 [Google Scholar]
  60. Huvet M, Nicolay S, Touchon M, Audit B, d'Aubenton-Carafa Y. 60.  et al. 2007. Human gene organization driven by the coordination of replication and transcription. Genome Res 17:1278–85 [Google Scholar]
  61. Iacovoni JS, Caron P, Lassadi I, Nicolas E, Massip L. 61.  et al. 2010. High-resolution profiling of γH2AX around DNA double strand breaks in the mammalian genome. EMBO J 29:1446–57 [Google Scholar]
  62. Iannelli F, Galbiati A, Capozzo I, Nguyen Q, Magnuson B. 61a.  et al. 2017. A damaged genome's transcriptional landscape through multilayered expression profiling around in situ-mapped DNA double-strand breaks. Nat. Commun 8:15656 [Google Scholar]
  63. Iannone R, Inga A, Luque-Romero FL, Menichini P, Abbondandolo A. 62.  et al. 1997. Mutation spectra analysis suggests that N-(2-chloroethyl)-Nγ-cyclohexyl-N-nitrosourea-induced lesions are subject to transcription-coupled repair in Escherichia coli. . Mol. Carcinog. 19:39–45 [Google Scholar]
  64. Ikura T, Tashiro S, Kakino A, Shima H, Jacob N. 63.  et al. 2007. DNA damage-dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics. Mol. Cell. Biol. 27:7028–40 [Google Scholar]
  65. Jackson SP, Bartek J. 64.  2009. The DNA-damage response in human biology and disease. Nature 461:1071–78 [Google Scholar]
  66. Jackson SP, MacDonald JJ, Lees-Miller S, Tjian R. 65.  1990. GC box binding induces phosphorylation of Sp1 by a DNA-dependent protein kinase. Cell 63:155–65 [Google Scholar]
  67. Ju B-G, Lunyak VV, Perissi V, Garcia-Bassets I, Rose DW. 66.  et al. 2006. A topoisomerase IIβ-mediated dsDNA break required for regulated transcription. Science 312:1798–802 [Google Scholar]
  68. Kadesch TR, Chamberlin MJ. 67.  1982. Studies of in vitro transcription by calf thymus RNA polymerase II using a novel duplex DNA template. J. Biol. Chem. 257:5286–95 [Google Scholar]
  69. Kim D, Bae S, Park J, Kim E, Kim S. 68.  et al. 2015. Digenome-seq: genome-wide profiling of CRISPR-Cas9 off-target effects in human cells. Nat. Methods 12:237–43 [Google Scholar]
  70. Kim N, Jinks-Robertson S. 69.  2012. Transcription as a source of genome instability. Nat. Rev. Genet. 13:204–14 [Google Scholar]
  71. Kramer KM, Brock JA, Bloom K, Moore JK, Haber JE. 70.  1994. Two different types of double-strand breaks in Saccharomyces cerevisiae are repaired by similar RAD52-independent, nonhomologous recombination events. Mol. Cell. Biol. 14:1293–301 [Google Scholar]
  72. Krishnakumar R, Kraus WL. 71.  2010. PARP-1 regulates chromatin structure and transcription through a KDM5B-dependent pathway. Mol. Cell 39:736–49 [Google Scholar]
  73. Kumari A, Lim YX, Newell AH, Olson SB, McCullough AK. 72.  2012. Formaldehyde-induced genome instability is suppressed by an XPF-dependent pathway. DNA Repair 11:236–46 [Google Scholar]
  74. Kunkel TA, Erie DA. 73.  2005. DNA mismatch repair. Annu. Rev. Biochem. 74:681–710 [Google Scholar]
  75. Leduc F, Faucher D, Bikond Nkoma G, Grégoire M-C, Arguin M. 74.  et al. 2011. Genome-wide mapping of DNA strand breaks. PLOS ONE 6:e17353 [Google Scholar]
  76. Lensing SV, Marsico G, Hänsel-Hertsch R, Lam EY, Tannahill D, Balasubramanian S. 75.  2016. DSBCapture: in situ capture and sequencing of DNA breaks. Nat. Methods 13:855–57 [Google Scholar]
  77. Lescure B, Chestier A, Yaniv M. 76.  1978. Transcription of polyoma virus DNA in vitro: II. Transcription of superhelical and linear polyoma DNA by RNA polymerase II. J. Mol. Biol. 124:73–85 [Google Scholar]
  78. Lescure B, Dauguet C, Yaniv M. 77.  1978. Transcription of polyoma virus DNA in vitro: III. Localization of calf thymus RNA polymerase II binding sites. J. Mol. Biol. 124:87–96 [Google Scholar]
  79. Levine M, Cattoglio C, Tjian R. 78.  2014. Looping back to leap forward: transcription enters a new era. Cell 157:13–25 [Google Scholar]
  80. Lewis MK, Burgess RR. 79.  1982. Eukaryotic RNA polymerases. Nucleic Acids: Part B PD Boyer 109–53 Enzymes 15 New York: Academic [Google Scholar]
  81. Li B-H, Ebbert A, Bockrath R. 80.  1999. Transcription-modulated repair in Escherichia coli evident with UV-induced mutation spectra in supF. J. Mol. Biol. 294:35–48 [Google Scholar]
  82. Lieber MR. 81.  2010. The mechanism of double-strand DNA break repair by the nonhomologous DNA end joining pathway. Annu. Rev. Biochem. 79:181–211 [Google Scholar]
  83. Lindahl T, Barnes DE. 82.  2000. Repair of endogenous DNA damage. Cold Spring Harb. Symp. Quant. Biol. 65:127–33 [Google Scholar]
  84. Liu LF, Wang JC. 83.  1987. Supercoiling of the DNA template during transcription. PNAS 84:7024–27 [Google Scholar]
  85. Lukas J, Lukas C, Bartek J. 84.  2011. More than just a focus: the chromatin response to DNA damage and its role in genome integrity maintenance. Nat. Cell Biol. 13:1161–69 [Google Scholar]
  86. Madabhushi R, Gao F, Pfenning AR, Pan L, Yamakawa S. 85.  et al. 2015. Activity-induced DNA breaks govern the expression of neuronal early-response genes. Cell 161:1592–605 [Google Scholar]
  87. Majewski J. 86.  2003. Dependence of mutational asymmetry on gene-expression levels in the human genome. Am. J. Hum. Genet. 73:688–92 [Google Scholar]
  88. Manley JL, Fire A, Cano A, Sharp PA, Gefter ML. 87.  1980. DNA-dependent transcription of adenovirus genes in a soluble whole-cell extract. PNAS 77:3855–59 [Google Scholar]
  89. Maser RS, Mirzoeva OK, Wells J, Olivares H, Williams BR. 88.  et al. 2001. Mre11 complex and DNA replication: linkage to E2F and sites of DNA synthesis. Mol. Cell. Biol. 21:6006–16 [Google Scholar]
  90. Massip L, Caron P, Iacovoni JS, Trouche D, Legube G. 89.  2010. Deciphering the chromatin landscape induced around DNA double strand breaks. Cell Cycle 9:2963–72 [Google Scholar]
  91. Matsui T, Segall J, Weil PA, Roeder RG. 90.  1980. Multiple factors required for accurate initiation of transcription by purified RNA polymerase II. J. Biol. Chem. 255:11992–96 [Google Scholar]
  92. McVey M, Lee SE. 91.  2008. MMEJ repair of double-strand breaks (director's cut): deleted sequences and alternative endings. Trends Genet 24:529–38 [Google Scholar]
  93. Mellon I, Spivak G, Hanawalt PC. 92.  1987. Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell 51:241–49 [Google Scholar]
  94. Meng FL, Du Z, Federation A, Hu J, Wang Q. 93.  et al. 2014. Convergent transcription at intragenic super-enhancers targets AID-initiated genomic instability. Cell 159:1538–48 [Google Scholar]
  95. Michalik KM, Böttcher R, Förstemann K. 94.  2012. A small RNA response at DNA ends in Drosophila. Nucleic Acids Res 40:9596–603 [Google Scholar]
  96. Mishina Y, Duguid EM, He C. 95.  2006. Direct reversal of DNA alkylation damage. Chem. Rev. 106:215–32 [Google Scholar]
  97. Mitra A, Skrzypczak M, Ginalski K, Rowicka M. 96.  2015. Strategies for achieving high sequencing accuracy for low diversity samples and avoiding sample bleeding using Illumina platform. PLOS ONE 10:e0120520 [Google Scholar]
  98. Moné MJ, Volker M, Nikaido O, Mullenders LHF, van Zeeland AA. 97.  et al. 2001. Local UV-induced DNA damage in cell nuclei results in local transcription inhibition. EMBO Rep 2:1013–17 [Google Scholar]
  99. Nougayrède J-P, Homburg S, Taieb F, Boury M, Brzuszkiewicz E. 98.  et al. 2006. Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science 313:848–51 [Google Scholar]
  100. Nudler E. 99.  2012. RNA polymerase backtracking in gene regulation and genome instability. Cell 149:1438–45 [Google Scholar]
  101. Nudler E, Mustaev A, Goldfarb A, Lukhtanov E. 100.  1997. The RNA-DNA hybrid maintains the register of transcription by preventing backtracking of RNA polymerase. Cell 89:33–41 [Google Scholar]
  102. Ohle C, Tesorero R, Schermann G, Dobrev N, Sinning I, Fischer T. 101.  2016. Transient RNA-DNA hybrids are required for efficient double-strand break repair. Cell 167:1001–13.e7 [Google Scholar]
  103. Oliveira TY, Resch W, Jankovic M, Casellas R, Nussenzweig MC, Klein IA. 102.  2012. Translocation capture sequencing: a method for high throughput mapping of chromosomal rearrangements. J. Immunol. Methods 375:176–81 [Google Scholar]
  104. Pankotai T, Bonhomme C, Chen D, Soutoglou E. 103.  2012. DNAPKcs-dependent arrest of RNA polymerase II transcription in the presence of DNA breaks. Nat. Struct. Mol. Biol. 19:276–82 [Google Scholar]
  105. Perillo B, Ombra MN, Bertoni A, Cuozzo C, Sacchetti S. 104.  et al. 2008. DNA oxidation as triggered by H3K9me2 demethylation drives estrogen-induced gene expression. Science 319:202–6 [Google Scholar]
  106. Periyasamy M, Patel H, Lai CF, Nguyen VTM, Nevedomskaya E. 105.  et al. 2015. APOBEC3B-mediated cytidine deamination is required for estrogen receptor action in breast cancer. Cell Rep 13:108–21 [Google Scholar]
  107. Peter BJ, Ullsperger C, Hiasa H, Marians KJ, Cozzarelli NR. 106.  1998. The structure of supercoiled intermediates in DNA replication. Cell 94:819–27 [Google Scholar]
  108. Petermann E, Helleday T. 107.  2010. Pathways of mammalian replication fork restart. Nat. Rev. Mol. Cell Biol. 11:683–87 [Google Scholar]
  109. Petruska J, Arnheim N, Goodman MF. 108.  1996. Stability of intrastrand hairpin structures formed by the CAG/CTG class of DNA triplet repeats associated with neurological diseases. Nucleic Acids Res 24:1992 [Google Scholar]
  110. Polo SE, Jackson SP. 109.  2011. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev 25:409–33 [Google Scholar]
  111. Pommier Y, Sun Y, Huang SN, Nitiss JL. 110.  2016. Roles of eukaryotic topoisomerases in transcription, replication and genomic stability. Nat. Rev. Mol. Cell Biol. 17:703–21 [Google Scholar]
  112. Price BD, D'Andrea AD. 111.  2013. Chromatin remodeling at DNA double-strand breaks. Cell 152:1344–54 [Google Scholar]
  113. Puc J, Kozbial P, Aggarwal AK, Rosenfeld MG, Puc J. 112.  et al. 2015. Ligand-dependent enhancer activation regulated by topoisomerase-I activity. Cell 160:367–80 [Google Scholar]
  114. Ran FA, Cong L, Yan WX, Scott DA, Gootenberg JS. 113.  et al. 2015. In vivo genome editing using Staphylococcus aureus Cas9. Nature 520:186–90 [Google Scholar]
  115. Ratner JN, Balasubramanian B, Corden J, Warren SL, Bregman DB. 114.  1998. Ultraviolet radiation-induced ubiquitination and proteasomal degradation of the large subunit of RNA polymerase II: implications for transcription-coupled DNA repair. J. Biol. Chem. 273:5184–89 [Google Scholar]
  116. Rouet P, Smih F, Jasin M. 115.  1994. Expression of a site-specific endonuclease stimulates homologous recombination in mammalian cells. PNAS 91:6064–68 [Google Scholar]
  117. San Filippo J, Sung P, Klein H. 116.  2008. Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem. 77:229–57 [Google Scholar]
  118. Sancar A, Lindsey-Boltz LA, Ünsal-Kaçmaz K, Linn S. 117.  2004. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73:39–85 [Google Scholar]
  119. Saxowsky TT, Doetsch PW. 118.  2006. RNA polymerase encounters with DNA damage: transcription-coupled repair or transcriptional mutagenesis?. Chem. Rev. 106:474–88 [Google Scholar]
  120. Schmidts I, Böttcher R, Mirkovic-Hösle M, Förstemann K. 119.  2016. Homology directed repair is unaffected by the absence of siRNAs in Drosophila melanogaster. Nucleic Acids Res 44:8261–71 [Google Scholar]
  121. Schuster-Bockler B, Lehner B. 120.  2012. Chromatin organization is a major influence on regional mutation rates in human cancer cells. Nature 488:504–7 [Google Scholar]
  122. Schwabish MA, Struhl K. 121.  2004. Evidence for eviction and rapid deposition of histones upon transcriptional elongation by RNA polymerase II. Mol. Cell. Biol. 24:10111–17 [Google Scholar]
  123. Schwer B, Wei P-C, Chang AN, Kao J, Du Z. 122.  et al. 2016. Transcription-associated processes cause DNA double-strand breaks and translocations in neural stem/progenitor cells. PNAS 113:201525564 [Google Scholar]
  124. Shanbhag NM, Rafalska-Metcalf IU, Balane-Bolivar C, Janicki SM, Greenberg RA. 123.  2010. ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell 141:970–81 [Google Scholar]
  125. Shandilya J, Roberts SGE. 124.  2012. The transcription cycle in eukaryotes: from productive initiation to RNA polymerase II recycling. Biochim. Biophys. Acta 1819:391–400 [Google Scholar]
  126. Shi L, Tang X, Tang G. 125.  2016. GUIDE-seq to detect genome-wide double-stranded breaks in plants. Trends Plant Sci 21:815–18 [Google Scholar]
  127. Shiloh Y. 126.  2006. The ATM-mediated DNA-damage response: taking shape. Trends Biochem. Sci. 31:402–10 [Google Scholar]
  128. Solovjeva LV, Svetlova MP, Chagin VO, Tomilin NV. 127.  2007. Inhibition of transcription at radiation-induced nuclear foci of phosphorylated histone H2AX in mammalian cells. Chromosome Res 15:787–97 [Google Scholar]
  129. Srivatsan A, Tehranchi A, MacAlpine DM, Wang JD. 128.  2010. Co-orientation of replication and transcription preserves genome integrity. PLOS Genet 6:e1000810 [Google Scholar]
  130. Storici F, Bebenek K, Kunkel TA, Gordenin DA, Resnick MA. 129.  2007. RNA-templated DNA repair. Nature 447:338–41 [Google Scholar]
  131. Stork CT, Bocek M, Crossley MP, Sollier J, Sanz LA. 130.  et al. 2016. Co-transcriptional R-loops are the main cause of estrogen-induced DNA damage. eLife 5:e17548 [Google Scholar]
  132. Sun Y, Jiang X, Chen S, Fernandes N, Price BD. 131.  2005. A role for the Tip60 histone acetyltransferase in the acetylation and activation of ATM. PNAS 102:13182–87 [Google Scholar]
  133. Svejstrup JQ. 132.  2010. The interface between transcription and mechanisms maintaining genome integrity. Trends Biochem. Sci. 35:333–38 [Google Scholar]
  134. Thomas BJ, Rothstein R. 133.  1989. Elevated recombination rates in transcriptionally active DNA. Cell 56:619–30 [Google Scholar]
  135. Toller IM, Neelsen KJ, Steger M, Hartung ML, Hottiger MO. 134.  et al. 2011. Carcinogenic bacterial pathogen Helicobacter pylori triggers DNA double-strand breaks and a DNA damage response in its host cells. PNAS 108:14944–49 [Google Scholar]
  136. Tsai SQ, Zheng Z, Nguyen NT, Liebers M, Topkar VV. 135.  et al. 2014. GUIDE-seq enables genome-wide profiling of off-target cleavage by CRISPR-Cas nucleases. Nat. Biotechnol. 33:187–97 [Google Scholar]
  137. Tu Y, Tornaletti S, Pfeifer GP. 136.  1996. DNA repair domains within a human gene: selective repair of sequences near the transcription initiation site. EMBO J 15:675–83 [Google Scholar]
  138. Tuduri S, Crabbé L, Conti C, Tourrière H, Holtgreve-Grez H. 137.  et al. 2009. Topoisomerase I suppresses genomic instability by preventing interference between replication and transcription. Nat. Cell Biol. 11:1315–24 [Google Scholar]
  139. Veres A, Gosis BS, Ding Q, Collins R, Ragavendran A. 138.  et al. 2014. Low incidence of off-target mutations in individual CRISPR-Cas9 and TALEN targeted human stem cell clones detected by whole-genome sequencing. Cell Stem Cell 15:27–30 [Google Scholar]
  140. Wang X, Wang Y, Wu X, Wang J, Wang Y. 139.  et al. 2015. Unbiased detection of off-target cleavage by CRISPR-Cas9 and TALENs using integrase-defective lentiviral vectors. Nat. Biotechnol. 33:175–78 [Google Scholar]
  141. Wei W, Ba Z, Gao M, Wu Y, Ma Y. 140.  et al. 2012. A role for small RNAs in DNA double-strand break repair. Cell 149:101–12 [Google Scholar]
  142. Wei X, Samarabandu J, Devdhar RS, Siegel AJ, Acharya R, Berezney R. 141.  1998. Segregation of transcription and replication sites into higher order domains. Science 281:1502–5 [Google Scholar]
  143. Wells RD, Ashizawa T. 142.  2011. Genetic Instabilities and Neurological Diseases Int. Rev. Res. Ment. Retard 31 New York: Academic, 2nd ed.. [Google Scholar]
  144. West AE, Greenberg ME. 143.  2011. Neuronal activity-regulated gene transcription in synapse development and cognitive function. Cold Spring Harb. Perspect. Biol. 3:a005744 [Google Scholar]
  145. Westover KD, Bushnell DA, Kornberg RD. 144.  2004. Structural basis of transcription: separation of RNA from DNA by RNA polymerase II. Science 303:1014–16 [Google Scholar]
  146. Woodard RL, Lee K, Huang J, Dynan WS. 145.  2001. Distinct roles for Ku protein in transcriptional reinitiation and DNA repair. J. Biol. Chem. 276:15423–33 [Google Scholar]
  147. Woodfine K, Fiegler H, Beare DM, Collins JE, McCann OT. 146.  et al. 2004. Replication timing of the human genome. Hum. Mol. Genet. 13:191–202 [Google Scholar]
  148. Yan WX, Mirzazadeh R, Garnerone S, Scott D, Schneider MW. 147.  et al. 2017. BLISS is a versatile and quantitative method for genome-wide profiling of DNA double-strand breaks. Nat. Commun. 815058 [Google Scholar]
  149. Zhang Y, McCord RP, Ho Y-J, Lajoie BR, Hildebrand DG. 148.  et al. 2012. Chromosomal translocations are guided by the spatial organization of the genome. Cell 148:908–21 [Google Scholar]
  150. Zhang Y, Yuan F, Wu X, Rechkoblit O, Taylor JS. 149.  et al. 2000. Error-prone lesion bypass by human DNA polymerase η. Nucleic Acids Res 28:4717–24 [Google Scholar]
  151. Zhao X-N, Usdin K. 150.  2015. The repeat expansion diseases: the dark side of DNA repair. DNA Repair 32:96–105 [Google Scholar]
/content/journals/10.1146/annurev-genom-091416-035314
Loading
/content/journals/10.1146/annurev-genom-091416-035314
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error