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Abstract

Transcription-coupled repair (TCR), discovered as preferential nucleotide excision repair of UV-induced cyclobutane pyrimidine dimers located in transcribed mammalian genes compared to those in nontranscribed regions of the genome, is defined as faster repair of the transcribed strand versus the nontranscribed strand in transcribed genes. The phenomenon, universal in model organisms including , yeast, , mice, and humans, involves a translocase that interacts with both RNA polymerase stalled at damage in the transcribed strand and nucleotide excision repair proteins to accelerate repair. , a notable exception, exhibits TCR but lacks an obvious TCR translocase. Mutations inactivating TCR genes cause increased damage-induced mutagenesis in and severe neurological and UV sensitivity syndromes in humans. To date, only TCR has been reconstituted in vitro with purified proteins. Detailed investigations of TCR using genome-wide next-generation sequencing methods, cryo–electron microscopy, single-molecule analysis, and other approaches have revealed fascinating mechanisms.

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2023-06-20
2024-04-27
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Literature Cited

  1. 1.
    Hanawalt PC, Spivak G. 2008. Transcription-coupled DNA repair: two decades of progress and surprises. Nat. Rev. Mol. Cell Biol. 9:958–70
    [Google Scholar]
  2. 2.
    Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S 2004. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73:39–85
    [Google Scholar]
  3. 3.
    Selby CP. 2017. Mfd protein and transcription-repair coupling in Escherichia coli. Photochem. Photobiol. 93:280–95
    [Google Scholar]
  4. 4.
    Portman JR, Strick TR. 2018. Transcription-coupled repair and complex biology. J. Mol. Biol. 430:4496–512
    [Google Scholar]
  5. 5.
    Strick TR, Portman JR. 2019. Transcription-coupled repair: from cells to single molecules and back again. J. Mol. Biol. 431:4093–102
    [Google Scholar]
  6. 6.
    van den Heuvel D, van der Weegen Y, Boer DEC, Ogi T, Luijsterburg MS. 2021. Transcription-coupled DNA repair: from mechanism to human disorder. Trends Cell Biol. 31:359–71
    [Google Scholar]
  7. 7.
    Sancar A. 1996. DNA excision repair. Annu. Rev. Biochem. 65:43–81
    [Google Scholar]
  8. 8.
    Aravind L, Walker DR, Koonin EV. 1999. Conserved domains in DNA repair proteins and evolution of repair systems. Nucleic. Acids. Res. 27:1223–42
    [Google Scholar]
  9. 9.
    Bohr VA, Smith CA, Okumoto DS, Hanawalt PC. 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 40:359–69
    [Google Scholar]
  10. 10.
    Mellon I, Spivak G, Hanawalt PC. 1987. Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell 51:241–49
    [Google Scholar]
  11. 11.
    Mellon I, Hanawalt PC. 1989. Induction of the Escherichia coli lactose operon selectively increases repair of its transcribed DNA strand. Nature 342:95–98
    [Google Scholar]
  12. 12.
    Nouspikel TP, Hyka-Nouspikel N, Hanawalt PC. 2006. Transcription domain-associated repair in human cells. Mol. Cell. Biol. 26:8722–30
    [Google Scholar]
  13. 13.
    Crowley DJ, Hanawalt PC. 1998. Induction of the SOS response increases the efficiency of global nucleotide excision repair of cyclobutane pyrimidine dimers, but not 6–4 photoproducts, in UV-irradiated Escherichia coli. J. Bacteriol. 180:3345–52
    [Google Scholar]
  14. 14.
    Crowley DJ, Hanawalt PC. 2001. The SOS-dependent upregulation of uvrD is not required for efficient nucleotide excision repair of ultraviolet light induced DNA photoproducts in Escherichia coli. Mutat. Res. 485:319–29
    [Google Scholar]
  15. 15.
    Troelstra C, van Gool A, de Wit J, Vermeulen W, Bootsma D, Hoeijmakers JH. 1992. ERCC6, a member of a subfamily of putative helicases, is involved in Cockayne's syndrome and preferential repair of active genes. Cell 71:939–53
    [Google Scholar]
  16. 16.
    van Gool AJ, Verhage R, Swagemakers SM, van de Putte P, Brouwer J et al. 1994. RAD26, the functional S. cerevisiae homolog of the Cockayne syndrome B gene ERCC6. EMBO J. 13:5361–69
    [Google Scholar]
  17. 17.
    Selby CP, Sancar A. 1991. Gene- and strand-specific repair in vitro: partial purification of a transcription-repair coupling factor. PNAS 88:8232–36
    [Google Scholar]
  18. 18.
    Selby CP, Sancar A. 1993. Molecular mechanism of transcription-repair coupling. Science 260:53–58
    [Google Scholar]
  19. 19.
    Sekelsky JJ, Brodsky MH, Burtis KC. 2000. DNA repair in Drosophila: insights from the Drosophila genome sequence. J. Cell Biol. 150:F31–36
    [Google Scholar]
  20. 20.
    Sekelsky J. 2017. DNA repair in Drosophila: mutagens, models, and missing genes. Genetics 205:471–90
    [Google Scholar]
  21. 21.
    Deger N, Yang Y, Lindsey-Boltz LA, Sancar A, Selby CP. 2019. Drosophila, which lacks canonical transcription-coupled repair proteins, performs transcription-coupled repair. J. Biol. Chem. 294:18092–98
    [Google Scholar]
  22. 22.
    Deger N, Cao X, Selby CP, Gulec S, Kawara H et al. 2022. CSB-independent, XPC-dependent transcription-coupled repair in Drosophila. PNAS 119:e2123163119
    [Google Scholar]
  23. 23.
    Tu Y, Tornaletti S, Pfeifer GP. 1996. DNA repair domains within a human gene: selective repair of sequences near the transcription initiation site. EMBO J. 15:675–83
    [Google Scholar]
  24. 24.
    Mao P, Smerdon MJ, Roberts SA, Wyrick JJ. 2016. Chromosomal landscape of UV damage formation and repair at single-nucleotide resolution. PNAS 113:9057–62
    [Google Scholar]
  25. 25.
    Jin SG, Pettinga D, Johnson J, Li P, Pfeifer GP. 2021. The major mechanism of melanoma mutations is based on deamination of cytosine in pyrimidine dimers as determined by circle damage sequencing. Sci. Adv. 7:eabi6508
    [Google Scholar]
  26. 26.
    Hu J, Lieb JD, Sancar A, Adar S. 2016. Cisplatin DNA damage and repair maps of the human genome at single-nucleotide resolution. PNAS 113:11507–12
    [Google Scholar]
  27. 27.
    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. 29:948–60
    [Google Scholar]
  28. 28.
    Hu J, Adebali O, Adar S, Sancar A. 2017. Dynamic maps of UV damage formation and repair for the human genome. PNAS 114:6758–63
    [Google Scholar]
  29. 29.
    Li W, Sancar A. 2020. Methodologies for detecting environmentally induced DNA damage and repair. Environ. Mol. Mutagen. 61:664–79
    [Google Scholar]
  30. 30.
    Selby CP, Sancar A. 2003. Characterization of transcription-repair coupling factors in E. coli and humans. Methods Enzymol. 371:300–24
    [Google Scholar]
  31. 31.
    Manelyte L, Kim YI, Smith AJ, Smith RM, Savery NJ. 2010. Regulation and rate enhancement during transcription-coupled DNA repair. Mol. Cell 40:714–24
    [Google Scholar]
  32. 32.
    Deaconescu AM, Chambers AL, Smith AJ, Nickels BE, Hochschild A et al. 2006. Structural basis for bacterial transcription-coupled DNA repair. Cell 124:507–20
    [Google Scholar]
  33. 33.
    Kang JY, Llewellyn E, Chen J, Olinares PDB, Brewer J et al. 2021. Structural basis for transcription complex disruption by the Mfd translocase. eLife 10:e62117
    [Google Scholar]
  34. 34.
    Brugger C, Zhang C, Suhanovsky MM, Kim DD, Sinclair AN et al. 2020. Molecular determinants for dsDNA translocation by the transcription-repair coupling and evolvability factor Mfd. Nat. Commun. 11:3740
    [Google Scholar]
  35. 35.
    Howan K, Smith AJ, Westblade LF, Joly N, Grange W et al. 2012. Initiation of transcription-coupled repair characterized at single-molecule resolution. Nature 490:431–34
    [Google Scholar]
  36. 36.
    Haines NM, Kim YI, Smith AJ, Savery NJ. 2014. Stalled transcription complexes promote DNA repair at a distance. PNAS 111:4037–42
    [Google Scholar]
  37. 37.
    Fan J, Leroux-Coyau M, Savery NJ, Strick TR. 2016. Reconstruction of bacterial transcription-coupled repair at single-molecule resolution. Nature 536:234–37
    [Google Scholar]
  38. 38.
    Ho HN, van Oijen AM, Ghodke H. 2020. Single-molecule imaging reveals molecular coupling between transcription and DNA repair machinery in live cells. Nat. Commun. 11:1478
    [Google Scholar]
  39. 39.
    Paudel BP, Xu ZQ, Jergic S, Oakley AJ, Sharma N et al. 2022. Mechanism of transcription modulation by the transcription-repair coupling factor. Nucleic. Acids. Res. 50:5688–712
    [Google Scholar]
  40. 40.
    Selby CP, Witkin EM, Sancar A. 1991. Escherichia coli mfd mutant deficient in “mutation frequency decline” lacks strand-specific repair: in vitro complementation with purified coupling factor. PNAS 88:11574–8
    [Google Scholar]
  41. 41.
    Bockrath RC, Palmer JE. 1977. Differential repair of premutational UV-lesions at tRNA genes in E. coli. Mol. Gen. Genet. 156:133–40
    [Google Scholar]
  42. 42.
    Li BH, Ebbert A, Bockrath R. 1999. Transcription-modulated repair in Escherichia coli evident with UV-induced mutation spectra in supF. J. Mol. Biol. 294:35–48
    [Google Scholar]
  43. 43.
    Witkin EM. 1994. Mutation frequency decline revisited. Bioessays 16:437–44
    [Google Scholar]
  44. 44.
    Witkin EM. 1966. Radiation-induced mutations and their repair. Science 152:1345–53
    [Google Scholar]
  45. 45.
    Witkin EM. 1956. Time, temperature, and protein synthesis: a study of ultraviolet-induced mutation in bacteria. Cold Spring Harb. Symp. Quant. Biol. 21:123–40
    [Google Scholar]
  46. 46.
    George DL, Witkin EM. 1975. Ultraviolet light-induced responses of an mfd mutant of Escherichia coli B/r having a slow rate of dimer excision. Mutat. Res. 28:347–54
    [Google Scholar]
  47. 47.
    Selby CP, Sancar A. 1993. Transcription-repair coupling and mutation frequency decline. J. Bacteriol. 175:7509–14
    [Google Scholar]
  48. 48.
    Selby CP, Sancar A. 1990. Transcription preferentially inhibits nucleotide excision repair of the template DNA strand in vitro. J. Biol. Chem. 265:21330–36
    [Google Scholar]
  49. 49.
    Selby CP, Sancar A. 1994. Mechanisms of transcription-repair coupling and mutation frequency decline. Microbiol. Rev. 58:317–29
    [Google Scholar]
  50. 50.
    Selby CP, Sancar A. 1995. Structure and function of transcription-repair coupling factor. I. Structural domains and binding properties. J. Biol. Chem. 270:4882–89
    [Google Scholar]
  51. 51.
    Selby CP, Sancar A. 1995. Structure and function of transcription-repair coupling factor. II. Catalytic properties. J. Biol. Chem. 270:4890–95
    [Google Scholar]
  52. 52.
    Graves ET, Duboc C, Fan J, Stransky F, Leroux-Coyau M, Strick TR. 2015. A dynamic DNA-repair complex observed by correlative single-molecule nanomanipulation and fluorescence. Nat. Struct. Mol. Biol. 22:452–57
    [Google Scholar]
  53. 53.
    Caron PR, Kushner SR, Grossman L. 1985. Involvement of helicase II (uvrD gene product) and DNA polymerase I in excision mediated by the uvrABC protein complex. PNAS 82:4925–29
    [Google Scholar]
  54. 54.
    Husain I, Van Houten B, Thomas DC, Abdel-Monem M, Sancar A 1985. Effect of DNA polymerase I and DNA helicase II on the turnover rate of UvrABC excision nuclease. PNAS 82:6774–78
    [Google Scholar]
  55. 55.
    Kumura K, Sekiguchi M, Steinum AL, Seeberg E. 1985. Stimulation of the UvrABC enzyme-catalyzed repair reactions by the UvrD protein (DNA helicase II). Nucleic. Acids. Res. 13:1483–92
    [Google Scholar]
  56. 56.
    Orren DK, Selby CP, Hearst JE, Sancar A. 1992. Post-incision steps of nucleotide excision repair in Escherichia coli. Disassembly of the UvrBC-DNA complex by helicase II and DNA polymerase I. J. Biol. Chem. 267:780–88
    [Google Scholar]
  57. 57.
    Adebali O, Chiou YY, Hu J, Sancar A, Selby CP. 2017. Genome-wide transcription-coupled repair in Escherichia coli is mediated by the Mfd translocase. PNAS 114:E2116–25
    [Google Scholar]
  58. 58.
    Park JS, Marr MT, Roberts JW. 2002. E. coli transcription repair coupling factor (Mfd protein) rescues arrested complexes by promoting forward translocation. Cell 109:757–67
    [Google Scholar]
  59. 59.
    Putta S, Prabha S, Bhat V, Fox GC, Walsh MA et al. 2019. Structural insights into the molecular mechanisms of the Mycobacterium evolvability factor Mfd. bioRxiv 728246. https://doi.org/10.1101/728246
    [Google Scholar]
  60. 60.
    Deaconescu AM, Sevostyanova A, Artsimovitch I, Grigorieff N. 2012. Nucleotide excision repair (NER) machinery recruitment by the transcription-repair coupling factor involves unmasking of a conserved intramolecular interface. PNAS 109:3353–58
    [Google Scholar]
  61. 61.
    Le TT, Yang Y, Tan C, Suhanovsky MM, Fulbright RM Jr. et al. 2018. Mfd dynamically regulates transcription via a release and catch-up mechanism. Cell 173:344–57.e15
    [Google Scholar]
  62. 62.
    Park JS, Roberts JW. 2006. Role of DNA bubble rewinding in enzymatic transcription termination. PNAS 103:4870–75
    [Google Scholar]
  63. 63.
    Ho HN, van Oijen AM, Ghodke H. 2018. The transcription-repair coupling factor Mfd associates with RNA polymerase in the absence of exogenous damage. Nat. Commun. 9:1570
    [Google Scholar]
  64. 64.
    Ghodke H, Ho HN, van Oijen AM. 2020. Single-molecule live-cell imaging visualizes parallel pathways of prokaryotic nucleotide excision repair. Nat. Commun. 11:1477
    [Google Scholar]
  65. 65.
    Mellon I, Champe GN. 1996. Products of DNA mismatch repair genes mutS and mutL are required for transcription-coupled nucleotide-excision repair of the lactose operon in Escherichia coli. PNAS 93:1292–97
    [Google Scholar]
  66. 66.
    Adebali O, Sancar A, Selby CP. 2017. Mfd translocase is necessary and sufficient for transcription-coupled repair in Escherichia coli. J. Biol. Chem. 292:18386–91
    [Google Scholar]
  67. 67.
    Kuemmerle NB, Masker WE. 1980. Effect of the uvrD mutation on excision repair. J. Bacteriol. 142:535–46
    [Google Scholar]
  68. 68.
    Schalow BJ, Courcelle CT, Courcelle J. 2012. Mfd is required for rapid recovery of transcription following UV-induced DNA damage but not oxidative DNA damage in Escherichia coli. J. Bacteriol. 194:2637–45
    [Google Scholar]
  69. 69.
    Koehler DR, Courcelle J, Hanawalt PC. 1996. Kinetics of pyrimidine(6–4)pyrimidone photoproduct repair in Escherichia coli. J. Bacteriol. 178:1347–50
    [Google Scholar]
  70. 70.
    George DL, Witkin EM. 1974. Slow excision repair in an mfd mutant of Escherichia coli B/r. Mol. Gen. Genet. 133:283–91
    [Google Scholar]
  71. 71.
    Oller AR, Fijalkowska IJ, Dunn RL, Schaaper RM. 1992. Transcription-repair coupling determines the strandedness of ultraviolet mutagenesis in Escherichia coli. PNAS 89:11036–40
    [Google Scholar]
  72. 72.
    Ayora S, Rojo F, Ogasawara N, Nakai S, Alonso JC. 1996. The Mfd protein of Bacillus subtilis 168 is involved in both transcription-coupled DNA repair and DNA recombination. J. Mol. Biol. 256:301–18
    [Google Scholar]
  73. 73.
    Chambers AL, Smith AJ, Savery NJ. 2003. A DNA translocation motif in the bacterial transcription–repair coupling factor, Mfd. Nucleic. Acids. Res. 31:6409–18
    [Google Scholar]
  74. 74.
    Han J, Sahin O, Barton YW, Zhang Q. 2008. Key role of Mfd in the development of fluoroquinolone resistance in Campylobacter jejuni. PLOS Pathog. 4:e1000083
    [Google Scholar]
  75. 75.
    Ross C, Pybus C, Pedraza-Reyes M, Sung HM, Yasbin RE, Robleto E. 2006. Novel role of mfd: effects on stationary-phase mutagenesis in Bacillus subtilis. J. Bacteriol. 188:7512–20
    [Google Scholar]
  76. 76.
    Wimberly H, Shee C, Thornton PC, Sivaramakrishnan P, Rosenberg SM, Hastings PJ. 2013. R-loops and nicks initiate DNA breakage and genome instability in non-growing Escherichia coli. Nat. Commun. 4:2115
    [Google Scholar]
  77. 77.
    Jinks-Robertson S, Bhagwat AS. 2014. Transcription-associated mutagenesis. Annu. Rev. Genet. 48:341–59
    [Google Scholar]
  78. 78.
    Million-Weaver S, Samadpour AN, Moreno-Habel DA, Nugent P, Brittnacher MJ et al. 2015. An underlying mechanism for the increased mutagenesis of lagging-strand genes in Bacillus subtilis. PNAS 112:E1096–105
    [Google Scholar]
  79. 79.
    Ragheb M, Merrikh H. 2019. The enigmatic role of Mfd in replication-transcription conflicts in bacteria. DNA Repair 81:102659
    [Google Scholar]
  80. 80.
    Ragheb MN, Thomason MK, Hsu C, Nugent P, Gage J et al. 2019. Inhibiting the evolution of antibiotic resistance. Mol. Cell 73:157–65.e5
    [Google Scholar]
  81. 81.
    Ragheb MN, Merrikh C, Browning K, Merrikh H. 2021. Mfd regulates RNA polymerase association with hard-to-transcribe regions in vivo, especially those with structured RNAs. PNAS 118:e2008498118
    [Google Scholar]
  82. 82.
    Portman JR, Brouwer GM, Bollins J, Savery NJ, Strick TR. 2021. Cotranscriptional R-loop formation by Mfd involves topological partitioning of DNA. PNAS 118:e2019630118
    [Google Scholar]
  83. 83.
    Bruning JG, Marians KJ. 2021. Bypass of complex co-directional replication-transcription collisions by replisome skipping. Nucleic. Acids. Res. 49:9870–85
    [Google Scholar]
  84. 84.
    Lindsey-Boltz LA, Sancar A. 2021. The transcription-repair coupling factor Mfd prevents and promotes mutagenesis in a context-dependent manner. Front. Mol. Biosci. 8:668290
    [Google Scholar]
  85. 85.
    Branum ME, Reardon JT, Sancar A. 2001. DNA repair excision nuclease attacks undamaged DNA. A potential source of spontaneous mutations. J. Biol. Chem. 276:25421–26
    [Google Scholar]
  86. 86.
    Hasegawa K, Yoshiyama K, Maki H. 2008. Spontaneous mutagenesis associated with nucleotide excision repair in Escherichia coli. Genes Cells 13:459–69
    [Google Scholar]
  87. 87.
    Zalieckas JM, Wray LV Jr., Fisher SH. 1998. Expression of the Bacillus subtilis acsA gene: position and sequence context affect cre-mediated carbon catabolite repression. J. Bacteriol. 180:6649–54
    [Google Scholar]
  88. 88.
    Zalieckas JM, Wray LV Jr., Ferson AE, Fisher SH. 1998. Transcription-repair coupling factor is involved in carbon catabolite repression of the Bacillus subtilis hut and gnt operons. Mol. Microbiol. 27:1031–38
    [Google Scholar]
  89. 89.
    Kruger S, Gertz S, Hecker M. 1996. Transcriptional analysis of bglPH expression in Bacillus subtilis: evidence for two distinct pathways mediating carbon catabolite repression. J. Bacteriol. 178:2637–44
    [Google Scholar]
  90. 90.
    Willing SE, Richards EJ, Sempere L, Dale AG, Cutting SM, Fairweather NF. 2015. Increased toxin expression in a Clostridium difficile mfd mutant. BMC Microbiol. 15:280
    [Google Scholar]
  91. 91.
    Belitsky BR, Sonenshein AL. 2011. Roadblock repression of transcription by Bacillus subtilis CodY. J. Mol. Biol. 411:729–43
    [Google Scholar]
  92. 92.
    Martin HA, Sundararajan A, Ermi TS, Heron R, Gonzales J et al. 2021. Mfd affects global transcription and the physiology of stressed Bacillus subtilis cells. Front. Microbiol. 12:625705
    [Google Scholar]
  93. 93.
    Cox BS, Parry JM. 1968. The isolation, genetics and survival characteristics of ultraviolet light-sensitive mutants in yeast. Mutat. Res. 6:37–55
    [Google Scholar]
  94. 94.
    Prakash S, Prakash L. 2000. Nucleotide excision repair in yeast. Mutat. Res. 451:13–24
    [Google Scholar]
  95. 95.
    Gregersen LH, Svejstrup JQ. 2018. The cellular response to transcription-blocking DNA damage. Trends Biochem. Sci. 43:327–41
    [Google Scholar]
  96. 96.
    Svejstrup JQ. 2002. Mechanisms of transcription-coupled DNA repair. Nat. Rev. Mol. Cell Biol. 3:21–29
    [Google Scholar]
  97. 97.
    Verhage R, Zeeman AM, de Groot N, Gleig F, Bang DD et al. 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. 14:6135–42
    [Google Scholar]
  98. 98.
    Guzder SN, Sung P, Prakash L, Prakash S. 1998. Affinity of yeast nucleotide excision repair factor 2, consisting of the Rad4 and Rad23 proteins, for ultraviolet damaged DNA. J. Biol. Chem. 273:31541–46
    [Google Scholar]
  99. 99.
    Lejeune D, Chen X, Ruggiero C, Berryhill S, Ding B, Li S 2009. Yeast Elc1 plays an important role in global genomic repair but not in transcription coupled repair. DNA Repair 8:40–50
    [Google Scholar]
  100. 100.
    Guzder SN, Sung P, Prakash L, Prakash S. 1998. The DNA-dependent ATPase activity of yeast nucleotide excision repair factor 4 and its role in DNA damage recognition. J. Biol. Chem. 273:6292–96
    [Google Scholar]
  101. 101.
    Guzder SN, Bailly V, Sung P, Prakash L, Prakash S. 1995. Yeast DNA repair protein RAD23 promotes complex formation between transcription factor TFIIH and DNA damage recognition factor RAD14. J. Biol. Chem. 270:8385–88
    [Google Scholar]
  102. 102.
    Guzder SN, Habraken Y, Sung P, Prakash L, Prakash S. 1995. Reconstitution of yeast nucleotide excision repair with purified Rad proteins, replication protein A, and transcription factor TFIIH. J. Biol. Chem. 270:12973–76
    [Google Scholar]
  103. 103.
    Sung P, Prakash L, Matson SW, Prakash S. 1987. RAD3 protein of Saccharomyces cerevisiae is a DNA helicase. PNAS 84:8951–55
    [Google Scholar]
  104. 104.
    Guzder SN, Sung P, Bailly V, Prakash L, Prakash S. 1994. RAD25 is a DNA helicase required for DNA repair and RNA polymerase II transcription. Nature 369:578–81
    [Google Scholar]
  105. 105.
    Li W, Adebali O, Yang Y, Selby CP, Sancar A. 2018. Single-nucleotide resolution dynamic repair maps of UV damage in Saccharomyces cerevisiae genome. PNAS 115:E3408–15
    [Google Scholar]
  106. 106.
    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. 288:20918–26
    [Google Scholar]
  107. 107.
    Venema J, van Hoffen A, Natarajan AT, van Zeeland AA, Mullenders LH. 1990. The residual repair capacity of xeroderma pigmentosum complementation group C fibroblasts is highly specific for transcriptionally active DNA. Nucleic. Acids. Res. 18:443–48
    [Google Scholar]
  108. 108.
    Terleth C, van Sluis CA, van de Putte P. 1989. Differential repair of UV damage in Saccharomyces cerevisiae. Nucleic. Acids. Res. 17:4433–39
    [Google Scholar]
  109. 109.
    Smerdon MJ, Thoma F. 1990. Site-specific DNA repair at the nucleosome level in a yeast minichromosome. Cell 61:675–84
    [Google Scholar]
  110. 110.
    Sweder KS, Hanawalt PC. 1992. Preferential repair of cyclobutane pyrimidine dimers in the transcribed strand of a gene in yeast chromosomes and plasmids is dependent on transcription. PNAS 89:10696–700
    [Google Scholar]
  111. 111.
    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. 42:13242–53
    [Google Scholar]
  112. 112.
    Guzder SN, Habraken Y, Sung P, Prakash L, Prakash S. 1996. RAD26, the yeast homolog of human Cockayne's syndrome group B gene, encodes a DNA-dependent ATPase. J. Biol. Chem. 271:18314–17
    [Google Scholar]
  113. 113.
    Bhatia PK, Verhage RA, Brouwer J, Friedberg EC. 1996. Molecular cloning and characterization of Saccharomyces cerevisiae RAD28, the yeast homolog of the human Cockayne syndrome A (CSA) gene. J. Bacteriol. 178:5977–88
    [Google Scholar]
  114. 114.
    Xu J, Lahiri I, Wang W, Wier A, Cianfrocco MA et al. 2017. Structural basis for the initiation of eukaryotic transcription-coupled DNA repair. Nature 551:653–57
    [Google Scholar]
  115. 115.
    Yan C, Dodd T, Yu J, Leung B, Xu J et al. 2021. Mechanism of Rad26-assisted rescue of stalled RNA polymerase II in transcription-coupled repair. Nat. Commun. 12:7001
    [Google Scholar]
  116. 116.
    Lee SK, Yu SL, Prakash L, Prakash S. 2001. Requirement for yeast RAD26, a homolog of the human CSB gene, in elongation by RNA polymerase II. Mol. Cell. Biol. 21:8651–56
    [Google Scholar]
  117. 117.
    Selvam K, Ding B, Sharma R, Li S 2019. Evidence that moderate eviction of Spt5 and promotion of error-free transcriptional bypass by Rad26 facilitates transcription coupled nucleotide excision repair. J. Mol. Biol. 431:1322–38
    [Google Scholar]
  118. 118.
    Verhage RA, van Gool AJ, de Groot N, Hoeijmakers JH, van de Putte P, Brouwer J. 1996. Double mutants of Saccharomyces cerevisiae with alterations in global genome and transcription-coupled repair. Mol. Cell. Biol. 16:496–502
    [Google Scholar]
  119. 119.
    Li S, Smerdon MJ. 2004. Dissecting transcription-coupled and global genomic repair in the chromatin of yeast GAL1–10 genes. J. Biol. Chem. 279:14418–26
    [Google Scholar]
  120. 120.
    Duan M, Selvam K, Wyrick JJ, Mao P. 2020. Genome-wide role of Rad26 in promoting transcription-coupled nucleotide excision repair in yeast chromatin. PNAS 117:18608–16
    [Google Scholar]
  121. 121.
    Gregory SM, Sweder KS. 2001. Deletion of the CSB homolog, RAD26, yields Spt strains with proficient transcription-coupled repair. Nucleic. Acids. Res. 29:3080–86
    [Google Scholar]
  122. 122.
    Li S. 2015. Transcription coupled nucleotide excision repair in the yeast Saccharomyces cerevisiae: the ambiguous role of Rad26. DNA Repair 36:43–48
    [Google Scholar]
  123. 123.
    Li W, Li S. 2017. Facilitators and repressors of transcription-coupled DNA repair in Saccharomyces cerevisiae. Photochem. Photobiol. 93:259–67
    [Google Scholar]
  124. 124.
    Li W, Giles C, Li S 2014. Insights into how Spt5 functions in transcription elongation and repressing transcription coupled DNA repair. Nucleic. Acids. Res. 42:7069–83
    [Google Scholar]
  125. 125.
    Ding B, LeJeune D, Li S 2010. The C-terminal repeat domain of Spt5 plays an important role in suppression of Rad26-independent transcription coupled repair. J. Biol. Chem. 285:5317–26
    [Google Scholar]
  126. 126.
    Jansen LE, den Dulk H, Brouns RM, de Ruijter M, Brandsma JA, Brouwer J. 2000. Spt4 modulates Rad26 requirement in transcription-coupled nucleotide excision repair. EMBO J. 19:6498–507
    [Google Scholar]
  127. 127.
    Li S, Smerdon MJ. 2002. Rpb4 and Rpb9 mediate subpathways of transcription-coupled DNA repair in Saccharomyces cerevisiae. EMBO J. 21:5921–29
    [Google Scholar]
  128. 128.
    Tatum D, Li W, Placer M, Li S 2011. Diverse roles of RNA polymerase II-associated factor 1 complex in different subpathways of nucleotide excision repair. J. Biol. Chem. 286:30304–13
    [Google Scholar]
  129. 129.
    Martin-Tumasz S, Brow DA 2015. Saccharomyces cerevisiae Sen1 helicase domain exhibits 5′- to 3′-helicase activity with a preference for translocation on DNA rather than RNA. J. Biol. Chem. 290:22880–89
    [Google Scholar]
  130. 130.
    Peck SA, Hughes KD, Victorino JF, Mosley AL. 2019. Writing a wrong: coupled RNA polymerase II transcription and RNA quality control. WIRES RNA 10:e1529
    [Google Scholar]
  131. 131.
    Ursic D, Chinchilla K, Finkel JS, Culbertson MR. 2004. Multiple protein/protein and protein/RNA interactions suggest roles for yeast DNA/RNA helicase Sen1p in transcription, transcription-coupled DNA repair and RNA processing. Nucleic. Acids. Res. 32:2441–52
    [Google Scholar]
  132. 132.
    Li W, Selvam K, Rahman SA, Li S 2016. Sen1, the yeast homolog of human senataxin, plays a more direct role than Rad26 in transcription coupled DNA repair. Nucleic. Acids. Res. 44:6794–802
    [Google Scholar]
  133. 133.
    Li S, Ding B, Chen R, Ruggiero C, Chen X 2006. Evidence that the transcription elongation function of Rpb9 is involved in transcription-coupled DNA repair in Saccharomyces cerevisiae. Mol. Cell. Biol. 26:9430–41
    [Google Scholar]
  134. 134.
    Geijer ME, Zhou D, Selvam K, Steurer B, Mukherjee C et al. 2021. Elongation factor ELOF1 drives transcription-coupled repair and prevents genome instability. Nat. Cell Biol. 23:608–19
    [Google Scholar]
  135. 135.
    van der Weegen Y, de Lint K, van den Heuvel D, Nakazawa Y, Mevissen TET et al. 2021. ELOF1 is a transcription-coupled DNA repair factor that directs RNA polymerase II ubiquitylation. Nat. Cell Biol. 23:595–607
    [Google Scholar]
  136. 136.
    Nakazawa Y, Hara Y, Oka Y, Komine O, van den Heuvel D et al. 2020. Ubiquitination of DNA damage-stalled RNAPII promotes transcription-coupled repair. Cell 180:1228–44.e24
    [Google Scholar]
  137. 137.
    Li S, Waters R. 1997. Induction and repair of cyclobutane pyrimidine dimers in the Escherichia coli tRNA gene tyrT: Fis protein affects dimer induction in the control region and suppresses preferential repair in the coding region of the transcribed strand, except in a short region near the transcription start site. J. Mol. Biol. 271:31–46
    [Google Scholar]
  138. 138.
    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. PNAS 87:4707–11
    [Google Scholar]
  139. 139.
    Selby CP, Sancar A. 1997. Human transcription-repair coupling factor CSB/ERCC6 is a DNA-stimulated ATPase but is not a helicase and does not disrupt the ternary transcription complex of stalled RNA polymerase II. J. Biol. Chem. 272:1885–90
    [Google Scholar]
  140. 140.
    Selby CP, Sancar A. 1997. Cockayne syndrome group B protein enhances elongation by RNA polymerase II. PNAS 94:11205–9
    [Google Scholar]
  141. 141.
    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. 25:787–93
    [Google Scholar]
  142. 142.
    Kantor GJ, Hull DR. 1984. The rate of removal of pyrimidine dimers in quiescent cultures of normal human and xeroderma pigmentosum cells. Mutat. Res. 132:21–31
    [Google Scholar]
  143. 143.
    Mayne LV, Lehmann AR. 1982. Failure of RNA synthesis to recover after UV irradiation: an early defect in cells from individuals with Cockayne's syndrome and xeroderma pigmentosum. Cancer Res. 42:1473–78
    [Google Scholar]
  144. 144.
    Barrett SF, Robbins JH, Tarone RE, Kraemer KH. 1991. Evidence for defective repair of cyclobutane pyrimidine dimers with normal repair of other DNA photoproducts in a transcriptionally active gene transfected into Cockayne syndrome cells. Mutat. Res. 255:281–91
    [Google Scholar]
  145. 145.
    Chiou YY, Hu J, Sancar A, Selby CP. 2018. RNA polymerase II is released from the DNA template during transcription-coupled repair in mammalian cells. J. Biol. Chem. 293:2476–86
    [Google Scholar]
  146. 146.
    Noe Gonzalez M, Blears D, Svejstrup JQ 2021. Causes and consequences of RNA polymerase II stalling during transcript elongation. Nat. Rev. Mol. Cell Biol. 22:3–21
    [Google Scholar]
  147. 147.
    van der Weegen Y, Golan-Berman H, Mevissen TET, Apelt K, Gonzalez-Prieto R et al. 2020. The cooperative action of CSB, CSA, and UVSSA target TFIIH to DNA damage-stalled RNA polymerase II. Nat. Commun. 11:2104
    [Google Scholar]
  148. 148.
    Kokic G, Wagner FR, Chernev A, Urlaub H, Cramer P. 2021. Structural basis of human transcription-DNA repair coupling. Nature 598:368–72
    [Google Scholar]
  149. 149.
    Agapov A, Olina A, Kulbachinskiy A. 2022. RNA polymerase pausing, stalling and bypass during transcription of damaged DNA: from molecular basis to functional consequences. Nucleic. Acids. Res. 50:3018–41
    [Google Scholar]
  150. 150.
    Brueckner F, Hennecke U, Carell T, Cramer P. 2007. CPD damage recognition by transcribing RNA polymerase II. Science 315:859–62
    [Google Scholar]
  151. 151.
    Selby CP, Lindsey-Boltz LA, Yang Y, Sancar A 2020. Mycobacteria excise DNA damage in 12- or 13-nucleotide-long oligomers by prokaryotic-type dual incisions and performs transcription-coupled repair. J. Biol. Chem. 295:17374–80
    [Google Scholar]
  152. 152.
    Lindsey-Boltz LA, Yang Y, Adebali O, Neupane P, Braunstein M et al. 2022. The Mfd protein is the transcription-repair coupling factor (TRCF) in Mycobacterium smegmatis. J. Biol. Chem. 299:103009
    [Google Scholar]
  153. 153.
    Henning KA, Li L, Iyer N, McDaniel LD, Reagan MS et al. 1995. The Cockayne syndrome group A gene encodes a WD repeat protein that interacts with CSB protein and a subunit of RNA polymerase II TFIIH. Cell 82:555–64
    [Google Scholar]
  154. 154.
    Groisman R, Polanowska J, Kuraoka I, Sawada J, Saijo M et al. 2003. The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell 113:357–67
    [Google Scholar]
  155. 155.
    Anindya R, Mari PO, Kristensen U, Kool H, Giglia-Mari G et al. 2010. A ubiquitin-binding domain in Cockayne syndrome B required for transcription-coupled nucleotide excision repair. Mol. Cell 38:637–48
    [Google Scholar]
  156. 156.
    Zhang X, Horibata K, Saijo M, Ishigami C, Ukai A et al. 2012. Mutations in UVSSA cause UV-sensitive syndrome and destabilize ERCC6 in transcription-coupled DNA repair. Nat. Genet. 44:593–97
    [Google Scholar]
  157. 157.
    Hu J, Selby CP, Adar S, Adebali O, Sancar A. 2017. Molecular mechanisms and genomic maps of DNA excision repair in Escherichia coli and humans. J. Biol. Chem. 292:15588–97
    [Google Scholar]
  158. 158.
    Hu J, Li W, Adebali O, Yang Y, Oztas O et al. 2019. Genome-wide mapping of nucleotide excision repair with XR-seq. Nat. Protoc. 14:248–82
    [Google Scholar]
  159. 159.
    Yang Y, Adebali O, Wu G, Selby CP, Chiou YY et al. 2018. Cisplatin-DNA adduct repair of transcribed genes is controlled by two circadian programs in mouse tissues. PNAS 115:E4777–85
    [Google Scholar]
  160. 160.
    Yimit A, Adebali O, Sancar A, Jiang Y. 2019. Differential damage and repair of DNA-adducts induced by anti-cancer drug cisplatin across mouse organs. Nat. Commun. 10:309
    [Google Scholar]
  161. 161.
    Oztas O, Selby CP, Sancar A, Adebali O. 2018. Genome-wide excision repair in Arabidopsis is coupled to transcription and reflects circadian gene expression patterns. Nat. Commun. 9:1503
    [Google Scholar]
  162. 162.
    Gaddameedhi S, Selby CP, Kaufmann WK, Smart RC, Sancar A. 2011. Control of skin cancer by the circadian rhythm. PNAS 108:18790–95
    [Google Scholar]
  163. 163.
    Kang TH, Lindsey-Boltz LA, Reardon JT, Sancar A. 2010. Circadian control of XPA and excision repair of cisplatin-DNA damage by cryptochrome and HERC2 ubiquitin ligase. PNAS 107:4890–95
    [Google Scholar]
  164. 164.
    Kang TH, Reardon JT, Kemp M, Sancar A. 2009. Circadian oscillation of nucleotide excision repair in mammalian brain. PNAS 106:2864–67
    [Google Scholar]
  165. 165.
    Yang Y, Liu Z, Selby CP, Sancar A. 2019. Long-term, genome-wide kinetic analysis of the effect of the circadian clock and transcription on the repair of cisplatin-DNA adducts in the mouse liver. J. Biol. Chem. 294:11960–68
    [Google Scholar]
  166. 166.
    de Cock JG, Klink EC, Ferro W, Lohman PH, Eeken JC. 1992. Neither enhanced removal of cyclobutane pyrimidine dimers nor strand-specific repair is found after transcription induction of the β3-tubulin gene in a Drosophila embryonic cell line Kc. Mutat. Res. 293:11–20
    [Google Scholar]
  167. 167.
    de Cock JG, Klink EC, Lohman PH, Eeken JC. 1992. Absence of strand-specific repair of cyclobutane pyrimidine dimers in active genes in Drosophila melanogaster Kc cells. Mutat. Res. 274:85–92
    [Google Scholar]
  168. 168.
    Reardon JT, Sancar A. 2004. Thermodynamic cooperativity and kinetic proofreading in DNA damage recognition and repair. Cell Cycle 3:141–44
    [Google Scholar]
  169. 169.
    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. 17:2539–51
    [Google Scholar]
  170. 170.
    Tornaletti S, Reines D, Hanawalt PC. 1999. Structural characterization of RNA polymerase II complexes arrested by a cyclobutane pyrimidine dimer in the transcribed strand of template DNA. J. Biol. Chem. 274:24124–30
    [Google Scholar]
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