Repair of cisplatin-induced DNA interstrand crosslinks by a replication-independent pathway involving transcription-coupled repair and translesion synthesis

Nucleic Acids Research

Volumn 40, Issue 18, 2012, Pages 8953-8964

  Enoiu, Milica ^a   Jiricny, Josef ^a   Schärer, Orlando D ^a,b  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN; DNA POLYMERASE; DNA POLYMERASE REV1; DNA POLYMERASE ZETA; MITOMYCIN; PROTEIN CSB; PROTEIN XPF; PROTEIN XPG; REGULATOR PROTEIN; UNCLASSIFIED DRUG; XERODERMA PIGMENTOSUM GROUP A PROTEIN; XERODERMA PIGMENTOSUM GROUP C PROTEIN;

ANIMAL CELL; ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL SURVIVAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA CROSS LINKING; DNA REPLICATION; DNA SYNTHESIS INHIBITION; DNA TRANSCRIPTION; DRUG EFFECT; EMBRYO; EXCISION REPAIR; GENE ACTIVITY; GENE EXPRESSION REGULATION; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; MOLECULAR STABILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; REPORTER GENE; SIGNAL TRANSDUCTION;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE; CISPLATIN; CRICETINAE; CRICETULUS; CROSS-LINKING REAGENTS; DNA; DNA ADDUCTS; DNA DAMAGE; DNA MISMATCH REPAIR; DNA REPAIR; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; HOMOLOGOUS RECOMBINATION; HUMANS; MICE; NUCLEOTIDYLTRANSFERASES; PLASMIDS; TRANSCRIPTION, GENETIC;

EID: 84867568370     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks670     Document Type: Article

References (80)

1. Noll, D. M., Mason, T. M. and Miller, P. S. (2006) Formation and repair of interstrand cross-links in DN A. Chem. Rev., 106, 277-301.
2. Scharer, O. D. (2005) DNA interstrand crosslinks: natural and drug-induced DNA adducts that induce unique cellular responses. Chembiochem, 6, 27-32.
3. Stone, M. P., Cho, Y. J., Huang, H. et al. (2008) Interstrand DNA cross-links induced by alpha, beta-unsaturated aldehydes derived from lipid peroxidation and environmental sources. Acc. Chem. Res., 41, 793-804.
4. Helleday, T., Petermann, E., Lundin, C., Hodgson, B. and Sharma, R. A. (2008) DNA repair pathways as targets for cancer therapy. Nat. Rev. Cancer, 8, 193-204. (Pubitemid 351301852)
5. Kartalou, M. and Essigmann, J. M. (2001) Mechanisms of resistance to cisplatin. Mutat. Res., 478, 23-43. (Pubitemid 32530848)
6. Kelland, L. (2007) The resurgence of platinum-based cancer chemotherapy. Nat. Rev. Cancer, 7, 573-584. (Pubitemid 47106628)
7. Moldovan, G. L. and D'Andrea, A. D. (2009) How the fanconi anemia pathway guards the genome. Annu. Rev. Genet., 43, 223-249.
8. Raschle, M., Knipsheer, P.,-enoiu, M. et al. (2008) Mechanism of replication-coupled DNA interstrand crosslink repair. Cell, 134, 969-980.
9. Guainazzi, A. and Scharer, O. D. (2010) Using synthetic DNA interstrand crosslinks to elucidate repair pathways and identify new therapeutic targets for cancer chemotherapy. Cell. Mol. Life Sci., 67, 3683-3697.
10. Muniandy, P. A., Liu, J., Majumdar, A., Liu, S.-t. and Seidman, M. M. (2010) DNA interstrand crosslink repair in mammalian cells: step by step. Crit. Rev. Biochem. Mol. Biol., 45, 23-49.
11. Berardini, M., Foster, P. L. and Loechler, E. L. (1999) DNA polymerase II (polB) is involved in a new DNA repair pathway for DNA interstrand cross-links in Escherichia coli. J. Bacteriol., 181, 2878-2882. (Pubitemid 29211106)
12. Berardini, M., Mackay, W. and Loechler, E. L. (1997) Evidence for a recombination-independent pathway for the repair of DNA interstrand cross-links based on a site-specific study with nitrogen mustard. Biochemistry, 36, 3506-3513. (Pubitemid 27143503)
13. Hlavin, E. M., Smeaton, M. B., Noronha, A. M., Wilds, C. J. and Miller, P. S. (2010) Cross-link structure affects replication-independent DNA interstrand cross-link repair in mammalian cells. Biochemistry, 49, 3977-3988.
14. Sarkar, S., Davies, A. A., Ulrich, H. D. and McHugh, P. J. (2006) DNA interstrand crosslink repair during G1 involves nucleotide excision repair and DNA polymerase zeta. EMBO J., 25, 1285-1294.
15. Shen, X., Jun, S., O'Neal, L. E. et al. (2006) REV3 and REV1 play major roles in recombination-independent repair of DNA interstrand cross-links mediated by monoubiquitinated proliferating cell nuclear antigen (PCNA). J. Biol. Chem., 281, 13869-13872. (Pubitemid 43848310)
16. Wang, X., Peterson, C. A., Zheng, H. et al. (2001) Involvement of nucleotide excision repair in a recombination-independent and error-prone pathway of DNA interstrand cross-link repair. Mol. Cell. Biol., 21, 713-720. (Pubitemid 32104720)
17. Zheng, H., Wang, X., Warren, A. J. et al. (2003) Nucleotide excision repair- and polymerase eta-mediated error-prone removal of mitomycin C interstrand cross-links. Mol. Cell. Biol., 23, 754-761. (Pubitemid 36050566)
18. Jung, Y. and Lippard, S. J. (2007) Direct cellular responses to platinum-induced DNA damage. Chem. Rev., 107, 1387-1407. (Pubitemid 46864967)
19. Moggs, J. G., Szymkowski, D. E., Yamada, M. et al. (1997) Differential human nucleotide excision repair of paired and mispaired cisplatin-DNA adducts. Nucleic Acids Res., 25, 480-491.
20. Zamble, D. B., Mu, D., Reardon, J. T. et al. (1996) Repair of cisplatin-DNA adducts by the mammalian excision nuclease. Biochemistry, 35, 10004-10013. (Pubitemid 26269915)
21. Ang, W. H., Myint, M. and Lippard, S. J. (2010) Transcription inhibition by platinum-DNA cross-links in live mammalian cells. J. Am. Chem. Soc., 132, 7429-7435.
22. Hofr, C. and Brabec, V. (2001) Thermal and thermodynamic properties of duplex DNA containing site-specific interstrand cross-link of antitumor cisplatin or its clinically ineffective trans isomer. J. Biol. Chem., 276, 9655-9661.
23. Tremeau-Bravard, A., Riedl, T.,-egly, J. M. and Dahmus, M. E. (2004) Fate of RNA polymerase II stalled at a cisplatin lesion. J. Biol. Chem., 279, 7751-7759. (Pubitemid 38294658)
24. Kiziltepe, T., Yan, A., Dong, M. et al. (2005) Delineation of the chemical pathways underlying nitric oxide-induced homologous recombination in mammalian cells. Chem. Biol., 12, 357-369. (Pubitemid 40406283)
25. Enoiu, M., Ho, T. V., Long, D. T., Walter, J. C. and Scharer, O. D. (2012) Construction of plasmids containing site-specific DNA interstrand crosslinks for biochemical and cell biological studies. Methods Mol. Biol., 920, 203-219.
26. Ellison, A. R., Nouspikel, T., Jaspers, N. G., Clarkson, S. G. and Gruenert, D. C. (1998) Complementation of transformed fibroblasts from patients with combined xeroderma pigmentosum-Cockayne syndrome. Exp. Cell Res., 243, 22-28. (Pubitemid 28397630)
27. Jansen, J. G., Tsaalbi-Shtylik, A., Hendriks, G. et al. (2009) Mammalian polymerase zeta is essential for post-replication repair of UV-induced DNA lesions. DNA Repair, 8, 1444-1451.
28. Yang, I. Y., Hashimoto, K., de Wind, N., Blair, I. A. and Moriya, M. (2009) Two distinct translesion synthesis pathways across a lipid peroxidation-derived DNA adduct in mammalian cells. J. Biol. Chem., 284, 191-198.
29. de Wind, N., Dekker, M., Berns, A., Radman, M. and te Riele, H. (1995) Inactivation of the mouse Msh2 gene results in mismatch repair deficiency, methylation tolerance, hyperrecombination, and predisposition to cancer. Cell, 82, 321-330.
30. Nakatsu, Y., Asahina, H., Citterio, E. et al. (2000) XAB2, a novel tetratricopeptide repeat protein involved in transcription-coupled DNA repair and transcription. J. Biol. Chem., 275, 34931-34937.
31. Cejka, P., Stojic, L., Mojas, N. et al. (2003) Methylation-induced G(2)/M arrest requires a full complement of the mismatch repair protein hMLH1. EMBO J., 22, 2245-2254. (Pubitemid 36565547)
32. Bi, X., Slater, D. M., Ohmori, H. and Vaziri, C. (2005) DNA polymerase kappa is specifically required for recovery from the benzo[a]pyrene-dihydrodiol epoxide (BPDE)-induced S-phase checkpoint. J. Biol. Chem., 280, 22343-22355. (Pubitemid 40827891)
33. McDonald, J. P., Frank, E. G., Plosky, B. S. et al. (2003) 129-derived strains of mice are deficient in DNA polymerase iota and have normal immunoglobulin hypermutation. J. Exp. Med., 198, 635-643. (Pubitemid 37040397)
34. Bassett, E., King, N. M., Bryant, M. F. et al. (2004) The role of DNA polymerase eta in translesion synthesis past platinum-DNA adducts in human fibroblasts. Cancer Res., 64, 6469-6475. (Pubitemid 39297902)
35. Kannouche, P., Broughton, B. C., Volker, M. et al. (2001) Domain structure, localization, and function of DNA polymerase eta, defective in xeroderma pigmentosum variant cells. Genes Dev., 15, 158-172. (Pubitemid 32107662)
36. Garcia-Higuera, I., Taniguchi, T., Ganesan, S. et al. (2001) Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol. Cell, 7, 249-262. (Pubitemid 32206493)
37. Levitus, M., Waisfisz, Q., Godthelp, B. C. et al. (2005) The DNA helicase BRIP1 is defective in Fanconi anemia complementation group. J. Nat. Genet., 37, 934-935. (Pubitemid 43086148)
38. Howard-Flanders, P., Theriot, L. and Stedeford, J. B. (1969) Some properties of excision-defective recombination-deficient mutants of Escherichia coli K-12. J. Bacteriol., 97, 1134-1141.
39. Perez, C., Leng, M. and Malinge, J. M. (1997) Rearrangement of interstrand cross-links into intrastrand cross-links in cis- diamminedichloroplatinum(II)-modified DN A. Nucleic Acids Res., 25, 896-903. (Pubitemid 27299850)
40. Huang, J. C., Zamble, D. B., Reardon, J. T., Lippard, S. J. and Sancar, A. (1994) HMG-domain proteins specifically inhibit the repair of the major DNA adduct of the anticancer drug cisplatin by human excision nuclease. Proc. Natl. Acad. Sci. US A., 91, 10394-10398. (Pubitemid 24329003)
41. Cleaver, J. E., Thompson, L. H., Richardson, A. S. and States, J. C. (1999) A summary of mutations in the UV-sensitive disorders: xeroderma pigmentosum, Cockayne syndrome, and trichothiodystrophy. Hum. Mutat., 14, 9-22. (Pubitemid 29309939)
42. Cullinane, C., Mazur, S. J.,-essigmann, J. M., Phillips, D. R. and Bohr, V. A. (1999) Inhibition of RNA polymerase II transcription in human cell extracts by cisplatin DNA damage. Biochemistry, 38, 6204-6212.
43. Gillet, L. C. and Scharer, O. D. (2006) Molecular mechanisms of mammalian global genome nucleotide excision repair. Chem. Rev., 106, 253-276.
44. Hanawalt, P. C. and Spivak, G. (2008) Transcription-coupled DNA repair: two decades of progress and surprises. Nat. Rev. Mol. Cell. Biol., 9, 958-970.
45. Deans, A. J. and West, S. C. (2011) DNA interstrand crosslink repair and cancer. Nat. Rev. Cancer, 11, 467-480.
46. Wu, Q., Christensen, L. A., Legerski, R. J. and Vasquez, K. M. (2005) Mismatch repair participates in error-free processing of DNA interstrand crosslinks in human cells. EMBO Rep., 6, 551-557.
47. Zhang, N., Lu, X., Zhang, X., Peterson, C. A. and Legerski, R. J. (2002) hMutSbeta is required for the recognition and uncoupling of psoralen interstrand cross-links in vitro. Mol. Cell. Biol., 22, 2388-2397. (Pubitemid 34224641)
48. Fiumicino, S., Martinelli, S., Colussi, C. et al. (2000) Sensitivity to DNA cross-linking chemotherapeutic agents in mismatch repair-defective cells in vitro and in xenografts. Int. J. Cancer, 85, 590-596. (Pubitemid 30075141)
49. Zhao, J., Jain, A., Iyer, R. R., Modrich, P. L. and Vasquez, K. M. (2009) Mismatch repair and nucleotide excision repair proteins cooperate in the recognition of DNA interstrand crosslinks. Nucleic Acids Res., 37, 4420-4429.
50. Papouli, E., Cejka, P. and Jiricny, J. (2004) Dependence of the cytotoxicity of DNA-damaging agents on the mismatch repair status of human cells. Cancer Res., 64, 3391-3394. (Pubitemid 38657910)
51. Ho, T. V. and Scharer, O. D. (2010) Translesion DNA synthesis polymerases in DNA interstrand crosslink repair. Environ. Mol. Mutagen., 51, 552-566.
52. Gan, G. N., Wittschieben, J. P., Wittschieben, B. O. and Wood, R. D. (2008) DNA polymerase zeta (pol zeta) in higher eukaryotes. Cell Res., 18, 174-183.
53. Hicks, J. K., Chute, C. L., Paulsen, M. T. et al. (2010) Differential roles for DNA polymerases eta, zeta, and REV1 in lesion bypass of intrastrand versus interstrand DNA cross-links. Mol. Cell. Biol., 30, 1217-1230.
54. Nojima, K., Hochegger, H., Saberi, A. et al. (2005) Multiple repair pathways mediate tolerance to chemotherapeutic cross-linking agents in vertebrate cells. Cancer Res., 65, 11704-11711. (Pubitemid 41821731)
55. Prakash, S., Johnson, R. E. and Prakash, L. (2005) Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu. Rev. Biochem., 74, 317-353. (Pubitemid 40995510)
56. Ho, T. V., Guainazzi, A., Derkunt, S. B.,-enoiu, M. and Scharer, O. D. (2011) Structure-dependent bypass of DNA interstrand crosslinks by translesion synthesis polymerases. Nucleic Acids Res., 39, 7455-7464.
57. Minko, I. G., Harbut, M. B., Kozekov, I. D. et al. (2008) Role for DNA polymerase kappa in the processing of N2-N2-guanine interstrand crosslinks. J. Biol. Chem., 283, 17075-17082.
58. Yamanaka, K., Minko, I. G., Takata, K. et al. (2010) Novel enzymatic function of DNA polymerase nu in translesion DNA synthesis past major groove DNA-peptide and DNA-DNA cross-links. Chem. Res. Toxicol., 23, 689-695.
59. Albertella, M. R., Green, C. M., Lehmann, A. R. and O'Connor, M. J. (2005) A role for polymerase eta in the cellular tolerance to cisplatin-induced damage. Cancer Res., 65, 9799-9806. (Pubitemid 41541457)
60. Ogi, T., Limsirichaikul, S., Overmeer, R. M. et al. (2010) Three DNA polymerases, recruited by different mechanisms, carry out NER repair synthesis in human cells. Mol. Cell, 37, 714-727.
61. Jonnalagadda, V. S., Matsuguchi, T. and Engelward, B. P. (2005) DNA Repair, 4, 594-605.
62. Angelov, T., Guainazzi, A. and Scharer, O. D. (2009) Generation of DNA interstrand cross-links by post-synthetic reductive amination. Org. Lett., 11, 661-664.
63. Hoy, C. A., Thompson, L. H., Mooney, C. L. and Salazar, E. P. (1985) Defective DNA cross-link removal in Chinese hamster cell mutants hypersensitive to bifunctional alkylating agents. Cancer Res., 45, 1737-1743. (Pubitemid 15079132)
64. Wood, R. D. (2010) Mammalian nucleotide excision repair proteins and interstrand crosslink repair. Environ. Mol. Mutagen., 51, 520-526.
65. Furuta, T., Ueda, T., Aune, G. et al. (2002) Transcription-coupled nucleotide excision repair as a determinant of cisplatin sensitivity of human cells. Cancer Res., 62, 4899-4902. (Pubitemid 34984411)
66. McKay, B. C., Becerril, C. and Ljungman, M. (2001) P53 plays a protective role against UV- and cisplatin-induced apoptosis in transcription-coupled repair proficient fibroblasts. Oncogene, 20, 6805-6808. (Pubitemid 33020609)
67. Kohli, M. and Jorgensen, T. J. (1999) The influence of SV40 immortalization of human fibroblasts on p53-dependent radiation responses. Biochem. Biophys. Res. Commun., 257, 168-176. (Pubitemid 29299065)
68. Muniandy, P. A., Thapa, D., Thazhathveetil, A. K., Liu, S.-t. and Seidman, M. M. (2009) Repair of laser-localized DNA interstrand cross-links in G1 phase mammalian cells. J. Biol. Chem., 284, 27908-27917.
69. Bessho, T., Mu, D. and Sancar, A. (1997) Initiation of DNA interstrand cross-link repair in humans: the nucleotide excision repair system makes dual incisions 50 to the cross-linked base and removes a 22- to 28-nucleotide-long damage-free strand. Mol. Cell. Biol., 17, 6822-6830. (Pubitemid 27505911)
70. Mu, D., Bessho, T., Nechev, L. V. et al. (2000) DNA interstrand cross-links induce futile repair synthesis in mammalian cell extracts. Mol. Cell. Biol., 20, 2446-2454. (Pubitemid 30152052)
71. Coste, F., Malinge, J. M., Serre, L. et al. (1999) Crystal structure of a double-stranded DNA containing a cisplatin interstrand cross-link at 1.63 A resolution: hydration at the platinated site. Nucleic Acids Res., 27, 1837-1846. (Pubitemid 29209625)
72. Huang, H., Zhu, L., Reid, B. R., Drobny, G. P. and Hopkins, P. B. (1995) Solution structure of a cisplatin-induced DNA interstrand cross-link. Science, 270, 1842-1845. (Pubitemid 26007235)
73. Min, J. H. and Pavletich, N. P. (2007) Recognition of DNA damage by the Rad4 nucleotide excision repair protein. Nature, 449, 570-575. (Pubitemid 47525148)
74. Knipscheer, P., Raschle, M., Smogorzewska, A. et al. (2009) The Fanconi Anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science, 326, 1698-701.
75. Ben-Yehoyada, M., Wang, L. C., Kozekov, I. D. et al. (2009) Checkpoint signaling from a single DNA interstrand crosslink. Mol Cell, 35, 704-715.
76. Shen, X., Do, H., Li, Y. et al. (2009) Recruitment of Fanconi anemia and breast cancer proteins to DNA damage sites is differentially governed by replication. Mol. Cell, 35, 716-723.
77. Smeaton, M. B., Hlavin, E. M., McGregor Mason, T. et al. (2008) Distortion-dependent unhooking of interstrand cross-links in mammalian cell extracts. Biochemistry, 47, 9920-9930.
78. Jamieson, E. R. and Lippard, S. J. (1999) Structure, recognition, and processing of cisplatin-DNA adducts. Chem. Rev., 99, 2467-2498.
79. Kartalou, M. and Essigmann, J. M. (2001) Recognition of cisplatin adducts by cellular proteins. Mutat. Res., 478, 1-21. (Pubitemid 32530847)
80. Wynne, P., Newton, C., Ledermann, J. A. et al. (2007) Enhanced repair of DNA interstrand crosslinking in ovarian cancer cells from patients following treatment with platinum-based chemotherapy. Br. J. Cancer, 97, 927-933. (Pubitemid 47519316)