Transcription-coupled homologous recombination after oxidative damage

DNA Repair

Volumn 44, Issue , 2016, Pages 76-80

  Wei, Leizhen ^a,b   Levine, Arthur Samuel ^a,b   Lan, Li ^a,b  

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

CSB; Genome stability; Homologous recombination; RNA template; Transcription

Indexed keywords

COCKAYNE SYNDROME B PROTEIN; PROTEIN; RNA; UNCLASSIFIED DRUG; DNA; DNA HELICASE; DNA LIGASE; ERCC6 PROTEIN, HUMAN; RNA POLYMERASE II;

CELL SURVIVAL; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; DNA TRANSCRIPTION; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; SOMATIC CELL; BASE MISPAIRING; CELL CYCLE G1 PHASE; COCKAYNE SYNDROME; DOUBLE STRANDED DNA BREAK; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MISMATCH REPAIR; PATHOLOGY;

BASE PAIR MISMATCH; COCKAYNE SYNDROME; DNA; DNA BREAKS, DOUBLE-STRANDED; DNA HELICASES; DNA MISMATCH REPAIR; DNA REPAIR ENZYMES; G1 PHASE; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; HUMANS; OXIDATIVE STRESS; RNA POLYMERASE II; TRANSCRIPTION, GENETIC;

EID: 84971659442     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2016.05.009     Document Type: Review

References (65)

1. [1] Friedberg, E.C., A history of the DNA repair and mutagenesis field: I. The discovery of enzymatic photoreactivation. DNA Repair 33 (2015), 35–42.
2. [2] Salmon, T.B., Evert, B.A., Song, B., Doetsch, P.W., Biological consequences of oxidative stress-induced DNA damage in Saccharomyces cerevisiae. Nucleic Acids Res. 32 (2004), 3712–3723.
3. [3] Marnett, L.J., Oxyradicals and DNA damage. Carcinogenesis 21 (2000), 361–370.
4. [4] Friedberg, E.C., Aguilera, A., Gellert, M., Hanawalt, P.C., Hays, J.B., Lehmann, A.R., Lindahl, T., Lowndes, N., Sarasin, A., Wood, R.D., DNA repair: from molecular mechanism to human disease. DNA Repair 5 (2006), 986–996.
5. [5] Hoeijmakers, J.H., Genome maintenance mechanisms are critical for preventing cancer as well as other aging-associated diseases. Mech. Ageing Dev. 128 (2007), 460–462.
6. [6] van Schooten, F.J., Knaapen, A.M., Izzotti, A., DNA damage, mutagenesis and cardiovascular disease. Mutat. Res. 621 (2007), 1–4.
7. [7] Bauer, M., Goldstein, M., Christmann, M., Becker, H., Heylmann, D., Kaina, B., Human monocytes are severely impaired in base and DNA double-strand break repair that renders them vulnerable to oxidative stress. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 21105–21110.
8. [8] Saxowsky, T.T., Doetsch, P.W., RNA polymerase encounters with DNA damage: transcription-coupled repair or transcriptional mutagenesis?. Chem. Rev. 106 (2006), 474–488.
9. [9] Mellon, I., Spivak, G., Hanawalt, P.C., Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell 51 (1987), 241–249.
10. [10] Donahue, B.A., Yin, S., Taylor, J.S., Reines, D., Hanawalt, P.C., Transcript cleavage by RNA polymerase II arrested by a cyclobutane pyrimidine dimer in the DNA template. Proc. Natl. Acad. Sci. U. S. A. 91 (1994), 8502–8506.
11. [11] Jessulat, M., Alamgir, M., Salsali, H., Greenblatt, J., Xu, J., Golshani, A., Interacting proteins Rtt109 and Vps75 affect the efficiency of non-homologous end-joining in Saccharomyces cerevisiae. Arch. Biochem. Biophys. 469 (2008), 157–164.
12. [12] Pan, X., Ye, P., Yuan, D.S., Wang, X., Bader, J.S., Boeke, J.D., A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell 124 (2006), 1069–1081.
13. [13] Davierwala, A.P., Haynes, J., Li, Z., Brost, R.L., Robinson, M.D., Yu, L., Mnaimneh, S., Ding, H., Zhu, H., Chen, Y., Cheng, X., Brown, G.W., Boone, C., Andrews, B.J., Hughes, T.R., The synthetic genetic interaction spectrum of essential genes. Nat. Genet. 37 (2005), 1147–1152.
14. [14] Schramke, V., Neecke, H., Brevet, V., Corda, Y., Lucchini, G., Longhese, M.P., Gilson, E., Geli, V., The set1Delta mutation unveils a novel signaling pathway relayed by the Rad53-dependent hyperphosphorylation of replication protein A that leads to transcriptional activation of repair genes. Genes Dev. 15 (2001), 1845–1858.
15. [15] Collins, S.R., Miller, K.M., Maas, N.L., Roguev, A., Fillingham, J., Chu, C.S., Schuldiner, M., Gebbia, M., Recht, J., Shales, M., Ding, H., Xu, H., Han, J., Ingvarsdottir, K., Cheng, B., Andrews, B., Boone, C., Berger, S.L., Hieter, P., Zhang, Z., Brown, G.W., Ingles, C.J., Emili, A., Allis, C.D., Toczyski, D.P., Weissman, J.S., Greenblatt, J.F., Krogan, N.J., Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446 (2007), 806–810.
16. [16] Biswas, D., Takahata, S., Xin, H., Dutta-Biswas, R., Yu, Y., Formosa, T., Stillman, D.J., A role for Chd1 and Set2 in negatively regulating DNA replication in Saccharomyces cerevisiae. Genetics 178 (2008), 649–659.
17. [17] Kanaar, R., Hoeijmakers, J.H., van Gent, D.C., Molecular mechanisms of DNA double strand break repair. Trends Cell Biol. 8 (1998), 483–489.
18. [18] Li, X., Heyer, W.D., Homologous recombination in DNA repair and DNA damage tolerance. Cell Res. 18 (2008), 99–113.
19. [19] White, M.F., Homologous recombination in the archaea: the means justify the ends. Biochem. Soc. Trans. 39 (2011), 15–19.
20. [20] Lu, R., Pal, J., Buon, L., Nanjappa, P., Shi, J., Fulciniti, M., Tai, Y.T., Guo, L., Yu, M., Gryaznov, S., Munshi, N.C., Shammas, M.A., Targeting homologous recombination and telomerase in Barrett's adenocarcinoma: impact on telomere maintenance, genomic instability and tumor growth. Oncogene 33 (2014), 1495–1505.
21. [21] Kogoma, T., Stable DNA replication: interplay between DNA replication, homologous recombination, and transcription. Microbiol. Mol. Biol. Rev. 61 (1997), 212–238.
22. [22] Moynahan, M.E., Jasin, M., Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat. Rev. Mol. Cell Biol. 11 (2010), 196–207.
23. [23] Goldfarb, T., Lichten, M., Frequent and efficient use of the sister chromatid for DNA double-strand break repair during budding yeast meiosis. PLoS Biol., 8, 2010, e1000520.
24. [24] Manfrini, N., Clerici, M., Wery, M., Colombo, C.V., Descrimes, M., Morillon, A., d'Adda di Fagagna, F., Longhese, M.P., Resection is responsible for loss of transcription around a double-strand break in Saccharomyces cerevisiae. Elife, 4, 2015.
25. [25] Mullenders, L., DNA damage mediated transcription arrest: step back to go forward. DNA Repair 36 (2015), 28–35.
26. [26] Velez-Cruz, R., Egly, J.M., Cockayne syndrome group B (CSB) protein: at the crossroads of transcriptional networks. Mech. Ageing Dev. 134 (2013), 234–242.
27. [27] Groisman, R., Kuraoka, I., Chevallier, O., Gaye, N., Magnaldo, T., Tanaka, K., Kisselev, A.F., Harel-Bellan, A., Nakatani, Y., CSA-dependent degradation of CSB by the ubiquitin-proteasome pathway establishes a link between complementation factors of the Cockayne syndrome. Genes Dev. 20 (2006), 1429–1434.
28. [28] Ohnishi, T., Mori, E., Takahashi, A., DNA double-strand breaks: their production, recognition, and repair in eukaryotes. Mutat. Res. 669 (2009), 8–12.
29. [29] Cahill, D., Connor, B., Carney, J.P., Mechanisms of eukaryotic DNA double strand break repair. Front. Biosci. 11 (2006), 1958–1976.
30. [30] Price, B.D., D'Andrea, A.D., Chromatin remodeling at DNA double-strand breaks. Cell 152 (2013), 1344–1354.
31. [31] Boiteux, S., Jinks-Robertson, S., DNA repair mechanisms and the bypass of DNA damage in Saccharomyces cerevisiae. Genetics 193 (2013), 1025–1064.
32. [32] Zhou, W., Doetsch, P.W., Transcription bypass or blockage at single-strand breaks on the DNA template strand: effect of different 3′ and 5′ flanking groups on the T7 RNA polymerase elongation complex. Biochemistry 33 (1994), 14926–14934.
33. [33] Nakanishi, N., Fukuoh, A., Kang, D., Iwai, S., Kuraoka, I., Effects of DNA lesions on the transcription reaction of mitochondrial RNA polymerase: implications for bypass RNA synthesis on oxidative DNA lesions. Mutagenesis 28 (2013), 117–123.
34. [34] Kakarougkas, A., Ismail, A., Chambers, A.L., Riballo, E., Herbert, A.D., Kunzel, J., Lobrich, M., Jeggo, P.A., Downs, J.A., Requirement for PBAF in transcriptional repression and repair at DNA breaks in actively transcribed regions of chromatin. Mol. Cell 55 (2014), 723–732.
35. [35] Bohr, V.A., Smith, C.A., Okumoto, D.S., Hanawalt, P.C., 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 (1985), 359–369.
36. [36] Hanawalt, P.C., Spivak, G., Transcription-coupled DNA repair: two decades of progress and surprises. Nat. Rev. Mol. Cell Biol. 9 (2008), 958–970.
37. [37] Hanawalt, P.C., Controlling the efficiency of excision repair. Mutat. Res. 485 (2001), 3–13.
38. [38] Davis, L., Maizels, N., Homology-directed repair of DNA nicks via pathways distinct from canonical double-strand break repair. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), E924–932.
39. [39] Aymard, F., Bugler, B., Schmidt, C.K., Guillou, E., Caron, P., Briois, S., Iacovoni, J.S., Daburon, V., Miller, K.M., Jackson, S.P., Legube, G., Transcriptionally active chromatin recruits homologous recombination at DNA double-strand breaks. Nat. Struct. Mol. Biol. 21 (2014), 366–374.
40. [40] Lan, L., Nakajima, S., Wei, L., Sun, L., Hsieh, C.L., Sobol, R.W., Bruchez, M., Van Houten, B., Yasui, A., Levine, A.S., Novel method for site-specific induction of oxidative DNA damage reveals differences in recruitment of repair proteins to heterochromatin and euchromatin. Nucleic Acids Res. 42 (2014), 2330–2345.
41. [41] Lan, L., Ui, A., Nakajima, S., Hatakeyama, K., Hoshi, M., Watanabe, R., Janicki, S.M., Ogiwara, H., Kohno, T., Kanno, S., Yasui, A., The ACF1 complex is required for DNA double-strand break repair in human cells. Mol. Cell 40 (2010), 976–987.
42. [42] Wei, L., Nakajima, S., Bohm, S., Bernstein, K.A., Shen, Z., Tsang, M., Levine, A.S., Lan, L., DNA damage during the G0/G1 phase triggers RNA-templated, Cockayne syndrome B-dependent homologous recombination. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), E3495–3504.
43. [43] Janicki, S.M., Tsukamoto, T., Salghetti, S.E., Tansey, W.P., Sachidanandam, R., Prasanth, K.V., Ried, T., Shav-Tal, Y., Bertrand, E., Singer, R.H., Spector, D.L., From silencing to gene expression: real-time analysis in single cells. Cell 116 (2004), 683–698.
44. [44] Bulina, M.E., Chudakov, D.M., Britanova, O.V., Yanushevich, Y.G., Staroverov, D.B., Chepurnykh, T.V., Merzlyak, E.M., Shkrob, M.A., Lukyanov, S., Lukyanov, K.A., A genetically encoded photosensitizer. Nat. Biotechnol. 24 (2006), 95–99.
45. [45] Carpentier, P., Violot, S., Blanchoin, L., Bourgeois, D., Structural basis for the phototoxicity of the fluorescent protein KillerRed. FEBS Lett. 583 (2009), 2839–2842.
46. [46] Keskin, H., Shen, Y., Huang, F., Patel, M., Yang, T., Ashley, K., Mazin, A.V., Storici, F., Transcript-RNA-templated DNA recombination and repair. Nature 515 (2014), 436–439.
47. [47] Batenburg, N.L., Thompson, E.L., Hendrickson, E.A., Zhu, X.D., Cockayne syndrome group B protein regulates DNA double-strand break repair and checkpoint activation. EMBO J. 34 (2015), 1399–1416.
48. [48] Storici, F., Bebenek, K., Kunkel, T.A., Gordenin, D.A., Resnick, M.A., RNA-templated DNA repair. Nature 447 (2007), 338–341.
49. [49] Ciaffardini, F., Nicolai, S., Caputo, M., Canu, G., Paccosi, E., Costantino, M., Frontini, M., Balajee, A.S., Proietti-De-Santis, L., The cockayne syndrome B protein is essential for neuronal differentiation and neuritogenesis. Cell Death Dis., 5, 2014, e1268.
50. [50] Cleaver, J.E., Brennan-Minnella, A.M., Swanson, R.A., Fong, K.W., Chen, J., Chou, K.M., Chen, Y.W., Revet, I., Bezrookove, V., Mitochondrial reactive oxygen species are scavenged by Cockayne syndrome B protein in human fibroblasts without nuclear DNA damage. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), 13487–13492.
51. [51] Greenhaw, G.A., Hebert, A., Duke-Woodside, M.E., Butler, I.J., Hecht, J.T., Cleaver, J.E., Thomas, G.H., Horton, W.A., Xeroderma pigmentosum and Cockayne syndrome: overlapping clinical and biochemical phenotypes. Am. J. Hum. Genet. 50 (1992), 677–689.
52. [52] Wilson, B.T., Stark, Z., Sutton, R.E., Danda, S., Ekbote, A.V., Elsayed, S.M., Gibson, L., Goodship, J.A., Jackson, A.P., Keng, W.T., King, M.D., McCann, E., Motojima, T., Murray, J.E., Omata, T., Pilz, D., Pope, K., Sugita, K., White, S.M., Wilson, I.J., The Cockayne Syndrome Natural History (CoSyNH) study: clinical findings in 102 individuals and recommendations for care. Genet. Med. 18 (2016), 483–493.
53. [53] Nance, M.A., Berry, S.A., Cockayne syndrome: review of 140 cases. Am. J. Med. Genet. 42 (1992), 68–84.
54. [54] Weidenheim, K.M., Dickson, D.W., Rapin, I., Neuropathology of Cockayne syndrome: evidence for impaired development, premature aging, and neurodegeneration. Mech. Ageing Dev. 130 (2009), 619–636.
55. [55] Kamiuchi, S., Saijo, M., Citterio, E., de Jager, M., Hoeijmakers, J.H., Tanaka, K., Translocation of Cockayne syndrome group A protein to the nuclear matrix: possible relevance to transcription-coupled DNA repair. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 201–206.
56. [56] Jin, J., Arias, E.E., Chen, J., Harper, J.W., Walter, J.C., A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Mol. Cell 23 (2006), 709–721.
57. [57] Groisman, R., Polanowska, J., Kuraoka, I., Sawada, J., Saijo, M., Drapkin, R., Kisselev, A.F., Tanaka, K., Nakatani, Y., The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell 113 (2003), 357–367.
58. [58] Kitsera, N., Gasteiger, K., Luhnsdorf, B., Allgayer, J., Epe, B., Carell, T., Khobta, A., Cockayne syndrome: varied requirement of transcription-coupled nucleotide excision repair for the removal of three structurally different adducts from transcribed DNA. PLoS One, 9, 2014, e94405.
59. [59] Brooks, P.J., Blinded by the UV light: how the focus on transcription-coupled NER has distracted from understanding the mechanisms of Cockayne syndrome neurologic disease. DNA Repair 12 (2013), 656–671.
60. [60] Wei, L., Lan, L., Yasui, A., Tanaka, K., Saijo, M., Matsuzawa, A., Kashiwagi, R., Maseki, E., Hu, Y., Parvin, J.D., Ishioka, C., Chiba, N., BRCA1 contributes to transcription-coupled repair of DNA damage through polyubiquitination and degradation of Cockayne syndrome B protein. Cancer Sci. 102 (2011), 1840–1847.
61. [61] McCallum, G.P., Wong, A.W., Wells, P.G., Cockayne syndrome B protects against methamphetamine-enhanced oxidative DNA damage in murine fetal brain and postnatal neurodevelopmental deficits. Antioxid. Redox Signal. 14 (2011), 747–756.
62. [62] Ropolo, M., Cappelli, E., Foresta, M., Poggi, A., Proietti-De-Santis, L., Frosina, G., Defective resolution of pH2AX foci and enhanced DNA breakage in ionizing radiation-treated cockayne syndrome B cells. IUBMB Life 63 (2011), 272–276.
63. [63] Sakai, A., Sakasai, R., Kakeji, Y., Kitao, H., Maehara, Y., PARP and CSB modulate the processing of transcription-mediated DNA strand breaks. Genes Genet. Syst. 87 (2012), 265–272.
64. [64] Nakatsu, Y., Asahina, H., Citterio, E., Rademakers, S., Vermeulen, W., Kamiuchi, S., Yeo, J.P., Khaw, M.C., Saijo, M., Kodo, N., Matsuda, T., Hoeijmakers, J.H., Tanaka, K., XAB2, a novel tetratricopeptide repeat protein involved in transcription-coupled DNA repair and transcription. J. Biol. Chem. 275 (2000), 34931–34937.
65. [65] Bradsher, J., Auriol, J., Proietti de Santis, L., Iben, S., Vonesch, J.L., Grummt, I., Egly, J.M., CSB is a component of RNA pol I transcription. Mol. Cell 10 (2002), 819–829.