DNA repair: From genome maintenance to biomarker and therapeutic target

Clinical Cancer Research

Volumn 17, Issue 22, 2011, Pages 6973-6984

  Jalal, Shadia ^a   Earley, Jennifer N ^a   Turchi, John J ^a,b  

^a Division of Hematology and Oncology   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BIOLOGICAL MARKER; CARBOPLATIN; CISPLATIN; CYCLINE; DACARBAZINE; DNA; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; DNA GLYCOSYLTRANSFERASE; DOUBLE STRANDED DNA; ETOPOSIDE; EXCISION REPAIR CROSS COMPLEMENTING PROTEIN 1; INIPARIB; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; OLAPARIB; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PROTEIN MLH1; PROTEIN MSH2; RAD52 PROTEIN; TEMOZOLOMIDE; XRCC1 PROTEIN;

ACCURACY; BREAST CANCER; CANCER RISK; CARCINOGENESIS; COLORECTAL CANCER; COMET ASSAY; DNA DAMAGE; DNA DETERMINATION; DNA REPAIR; DNA STRAND BREAKAGE; DRUG RESPONSE; DRUG TARGETING; EXCISION REPAIR; GENE; GENE MUTATION; GENETIC ANALYSIS; HEREDITARY NONPOLYPOSIS COLORECTAL CANCER; HUMAN; LUNG CANCER; MALIGNANT NEOPLASTIC DISEASE; MISMATCH REPAIR; MLH1 GENE; MSH2 GENE; ONCOGENE; OVARY CANCER; OVERALL SURVIVAL; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROSTATE CANCER; REPRODUCIBILITY; REVIEW; STOMACH CANCER; TRIPLE NEGATIVE BREAST CANCER; XERODERMA PIGMENTOSUM;

BIOLOGICAL MARKERS; CYTOGENETICS; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA REPAIR; HUMANS; MOLECULAR TARGETED THERAPY; NEOPLASMS; SIGNAL TRANSDUCTION;

EID: 81255138410     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-11-0761     Document Type: Review

References (93)

1. Kennedy RD, D'Andrea AD. DNA repair pathways in clinical practice: lessons from pediatric cancer susceptibility syndromes. J Clin Oncol 2006;24:3799-808. (Pubitemid 46622318)
2. Rolig RL, McKinnon PJ. Linking DNA damage and neurodegeneration. Trends Neurosci 2000;23:417-24.
3. Akbari M, Krokan HE. Cytotoxicity and mutagenicity of endogenous DNA base lesions as potential cause of human aging. Mech Ageing Dev 2008;129:353-65.
4. Negrini S, Gorgoulis VG, Halazonetis TD. Genomic instability-an evolving hallmark of cancer. Nat Rev Mol Cell Biol 2010;11:220-8.
5. Olaussen KA, Dunant A, Fouret P, Brambilla E, André F, Haddad V, et al. IALT Bio Investigators. DNA repair by ERCC1 in non-small-cell lung cancer and cisplatin-based adjuvant chemotherapy.NEngl JMed 2006;355:983-91. (Pubitemid 44343542)
6. de Boer J, Hoeijmakers JH. Nucleotide excision repair and human syndromes. Carcinogenesis 2000;21:453-60. (Pubitemid 30137930)
7. Warmerdam DO, Kanaar R. Dealing with DNA damage: relationships between checkpoint and repair pathways. Mutat Res 2010;704:2-11.
8. Cimprich KA, Cortez D. ATR: an essential regulator of genome integrity. Nat Rev Mol Cell Biol 2008;9:616-27. (Pubitemid 352032926)
9. Tornaletti S. DNA repair in mammalian cells: Transcription-coupled DNA repair: directing your effort where it's most needed. Cell Mol Life Sci 2009;66:1010-20.
10. McCulloch SD, Kunkel TA. The fidelity of DNA synthesis by eukaryotic replicative and translesion synthesis polymerases. Cell Res 2008;18:148-61.
11. Ricciardone MD, Ozçelik T, Cevher B, Ozdaǧ H, Tuncer M, Gürgey A, et al. Human MLH1 deficiency predisposes to hematological malignancy and neurofibromatosis type 1. Cancer Res 1999;59:290-3. (Pubitemid 29048854)
12. Whiteside D, McLeod R, Graham G, Steckley JL, Booth K, Somerville MJ, et al. A homozygous germ-line mutation in the human MSH2 gene predisposes to hematological malignancy and multiple café-au-lait spots. Cancer Res 2002;62:359-62. (Pubitemid 34106403)
13. Lynch HT, de la Chapelle A. Genetic susceptibility to non-polyposis colorectal cancer. J Med Genet 1999;36:801-18. (Pubitemid 29520569)
14. Vasen HF, Watson P, Mecklin JP, Lynch HT. New clinical criteria for hereditary nonpolyposis colorectal cancer (HNPCC, Lynch syndrome) proposed by the International Collaborative group on HNPCC. Gastroenterology 1999;116:1453-6. (Pubitemid 29258894)
15. Barrow E, Alduaij W, Robinson L, Shenton A, Clancy T, Lalloo F, et al. Colorectal cancer in HNPCC: cumulative lifetime incidence, survival and tumour distribution.Areport of 121 families with proven mutations. Clin Genet 2008;74:233-42.
16. Laghi L, Bianchi P, Malesci A. Differences and evolution of the methods for the assessment of microsatellite instability. Oncogene 2008;27: 6313-21.
17. Annunziata CM, Bates SE. PARP inhibitors in BRCA1/BRCA2 germline mutation carriers with ovarian and breast cancer. F1000 Biol Rep 2010;2:10.
18. Lord CJ, Ashworth A. Targeted therapy for cancer using PARP inhibitors. Curr Opin Pharmacol 2008;8:363-9.
19. Robertson KA, Bullock HA, Xu Y, Tritt R, Zimmerman E, Ulbright TM, et al. Altered expression of Ape1/ref-1 in germ cell tumors and overexpression in NT2 cells confers resistance to bleomycin and radiation. Cancer Res 2001;61:2220-5. (Pubitemid 32692051)
20. Albertella MR, Lau A, O'Connor MJ. The overexpression of specialized DNA polymerases in cancer. DNA Repair (Amst) 2005;4:583-93. (Pubitemid 40462046)
21. Friedberg EC, Aguilera A, Gellert M, Hanawalt PC, Hays JB, Lehmann AR, et al. DNA repair: from molecular mechanism to human disease. DNA Repair (Amst) 2006;5:986-96. (Pubitemid 44137486)
22. Shuck SC, Short EA, Turchi JJ. Eukaryotic nucleotide excision repair: from understanding mechanisms to influencing biology. Cell Res 2008;18:64-72.
23. King MC, Marks JH, Mandell JBNewYork Breast Cancer Study Group. Breast and ovarian cancer risks due to inherited mutations in BRCA1 and BRCA2. Science 2003;302:643-6. (Pubitemid 37310920)
24. Mahaney BL, Meek K, Lees-Miller SP. Repair of ionizing radiation-induced DNA double-strand breaks by non-homologous end-joining. Biochem J 2009;417:639-50.
25. Schwarz K, Ma YM, Pannicke U, Lieber MR. Human severe combined immune deficiency and DNA repair. Bioessays 2003;25: 1061-70. (Pubitemid 37411766)
26. Wang Y, Ghosh G, Hendrickson EA. Ku86 represses lethal telomere deletion events in human somatic cells. Proc Natl Acad Sci U S A 2009;106:12430-5.
27. O'Connor MJ, Martin NM, Smith GC. Targeted cancer therapies based on the inhibition of DNA strand break repair. Oncogene 2007;26: 7816-24. (Pubitemid 350242461)
28. Wang LC, Stone S, Hoatlin ME, Gautier J. Fanconi anemia proteins stabilize replication forks. DNA Repair (Amst) 2008;7:1973-81.
29. McKinnon PJ, Caldecott KW. DNA strand break repair and human genetic disease. Annu Rev Genomics Hum Genet 2007;8:37-55.
30. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000;100: 57-70. (Pubitemid 30046295)
31. Wu X, Gu J, Spitz MR. Mutagen sensitivity: a genetic predisposition factor for cancer. Cancer Res 2007;67:3493-5. (Pubitemid 46762125)
32. Li C, Wang LE, Wei Q. DNA repair phenotype and cancer susceptibility - a mini review. Int J Cancer 2009;124:999-1007.
33. Wang LE, Xiong P, Zhao H, Spitz MR, Sturgis EM, Wei Q. Chromosome instability and risk of squamous cell carcinomas of head and neck. Cancer Res 2008;68:4479-85.
34. Wang LE, Xiong P, Strom SS, Goldberg LH, Lee JE, Ross MI, et al. In vitro sensitivity to ultraviolet B light and skin cancer risk: a case-control analysis. J Natl Cancer Inst 2005;97:1822-31. (Pubitemid 43033903)
35. Spitz MR, Hsu TC, Wu X, Fueger JJ, Amos CI, Roth JA. Mutagen sensitivity as a biological marker of lung cancer risk in African Americans. Cancer Epidemiol Biomarkers Prev 1995;4:99-103.
36. Wu X, Lin J, Etzel CJ, Dong Q, Gorlova OY, Zhang Q, et al. Interplay between mutagen sensitivity and epidemiological factors in modulatinglung cancer risk. Int J Cancer 2007;120:2687-95. (Pubitemid 46651292)
37. Xiong P, Bondy ML, Li D, Shen H, Wang LE, Singletary SE, et al. Sensitivity to benzo(a)pyrene diol-epoxide associated with risk of breast cancer in young women and modulation by glutathione S-transferase polymorphisms: a case-control study. Cancer Res 2001; 61:8465-9. (Pubitemid 33131126)
38. Erdei E, Lee SJ, Wei Q, Wang LE, Song YS, Bovbjerg D, et al. Reliability of mutagen sensitivity assay: an inter-laboratory comparison. Mutagenesis 2006;21:261-4. (Pubitemid 44543339)
39. Athas WF, Hedayati MA, Matanoski GM, Farmer ER, Grossman L. Development and field-test validation of an assay for DNA repair in circulating human lymphocytes. Cancer Res 1991;51:5786-93.
40. Wang LE, Li C, Strom SS, Goldberg LH, Brewster A, Guo Z, et al. Repair capacity for UV light induced DNA damage associated with risk of nonmelanoma skin cancer and tumor progression. Clin Cancer Res 2007;13:6532-9. (Pubitemid 350075045)
41. Wang LE, Hu Z, Sturgis EM, Spitz MR, Strom SS, Amos CI, et al. Reduced DNA repair capacity for removing tobacco carcinogen-induced DNA adducts contributes to risk of head and neck cancer but not tumor characteristics. Clin Cancer Res 2010;16:764-74.
42. Shen H, Spitz MR, Qiao Y, Guo Z,WangLE, Bosken CH, et al. Smoking, DNA repair capacity and risk of nonsmall cell lung cancer. Int J Cancer 2003;107:84-8. (Pubitemid 37100089)
43. Cheng L, Eicher SA, Guo Z, Hong WK, Spitz MR, Wei Q. Reduced DNA repair capacity in head and neck cancer patients. Cancer Epidemiol Biomarkers Prev 1998;7:465-8. (Pubitemid 28354107)
44. Wei QY, Cheng L, Hong WK, Spitz MR. ReducedDNArepair capacity in lung cancer patients. Cancer Res 1996;56:4103-7. (Pubitemid 26304997)
45. Wei Q, Cheng L, Amos CI, Wang LE, Guo Z, Hong WK, et al. Repair of tobacco carcinogen-induced DNA adducts and lung cancer risk: a molecular epidemiologic study. J Natl Cancer Inst 2000;92:1764-72.
46. Gajecka M, Rydzanicz M, Jaskula-Sztul R, Wierzbicka M, Szyfter W, Szyfter K. ReducedDNArepair capacity in laryngeal cancer subjects. A comparison of phenotypic and genotypic results. Adv Otorhinolaryngol 2005;62:25-37.
47. Schmezer P, Rajaee-Behbahani N, Risch A, Thiel S, Rittgen W, Drings P, et al. Rapid screening assay for mutagen sensitivity and DNA repair capacity in human peripheral blood lymphocytes. Mutagenesis 2001;16:25-30. (Pubitemid 32049210)
48. McArt DG, McKerr G, Saetzler K, Howard CV, Downes CS, Wasson GR. Comet sensitivity in assessing DNA damage and repair in different cell cycle stages. Mutagenesis 2010;25:299-303.
49. El-Zein RA, Monroy CM, Cortes A, Spitz MR, Greisinger A, Etzel CJ. Rapid method for determination of DNA repair capacity in human peripheral blood lymphocytes amongst smokers. BMC Cancer 2010;10:439.
50. Orlow I, Park BJ, Mujumdar U, Patel H, Siu-Lau P, Clas BA, et al. DNA damage and repair capacity in patients with lung cancer: prediction of multiple primary tumors. J Clin Oncol 2008;26:3560-6.
51. Olive PL, Banáth JP. The comet assay: a method to measure DNA damage in individual cells. Nat Protoc 2006;1:23-9.
52. Rosenberger A, Rossler U, Hornhardt S, Sauter W, Bickeboller H, Wichmann HE, et al. Validation of a fully automated COMET assay: 1.75 million single cells measured over a 5 year period. DNA Repair (Amst) 2011;10:322-37.
53. Mah LJ, El-Osta A, Karagiannis TC. gammaH2AX: a sensitive molecular marker of DNA damage and repair. Leukemia 2010;24:679-86.
54. Yuan J,Adamski R, Chen J. Focus on histone variant H2AX: to be or not to be. FEBS Lett 2010;584:3717-24.
55. Podhorecka M, Skladanowski A, Bozko P. H2AX phosphorylation: its role in DNA damage response and cancer therapy. J Nucleic Acids 2010;2010:920161.
56. Saviozzi S, Ceppi P, Novello S, Ghio P, Lo Iacono M, Borasio P, et al. Non-small cell lung cancer exhibits transcript overexpression of genes associated with homologous recombination andDNAreplication pathways. Cancer Res 2009;69:3390-6.
57. McLaren DB, Pickles T, Thomson T, Olive PL. Impact of nicotinamide on human tumour hypoxic fraction measured using the comet assay. Radiother Oncol 1997;45:175-82. (Pubitemid 27521091)
58. Zijno A, Porcedda P, Saini F, Allione A, Garofalo B, Marcon F, et al. Unsuitability of lymphoblastoid cell lines as surrogate of cryopreserved isolated lymphocytes for the analysis of DNA double-strand break repair activity. Mutat Res 2010;684:98-105.
59. Mazzei F, Guarrera S, Allione A, Simonelli V, Narciso L, Barone F, et al. 8-Oxoguanine DNA-glycosylase repair activity and expression: a comparison between cryopreserved isolated lymphocytes and EBV-derived lymphoblastoid cell lines. Mutat Res 2011;718:62-7.
60. Herrera M, Dominguez G, Garcia JM, Peña C, Jimenez C, Silva J, et al. Differences in repair of DNA cross-links between lymphocytes and epithelial tumor cells from colon cancer patients measured in vitro with the comet assay. Clin Cancer Res 2009;15:5466-72.
61. Stott SL, Hsu CH, Tsukrov DI, Yu M, Miyamoto DT, Waltman BA, et al. Isolation of circulating tumor cells using a microvortex-generating herringbone-chip. Proc Natl Acad Sci U S A 2010;107:18392-7.
62. Wu X, Gu J, Dong Q, Huang M, Do KA, Hong WK, et al. Joint effect of mutagen sensitivity and insulin-like growth factors in predicting the risk of developing secondary primary tumors and tumor recurrence in patients with head and neck cancer. Clin Cancer Res 2006;12: 7194-201. (Pubitemid 44974522)
63. Chao DL, MaleyCC,WuX, Farrow DC, Galipeau PC, Sanchez CA, et al. Mutagen sensitivity and neoplastic progression in patients with Barrett's esophagus: a prospective analysis. Cancer Epidemiol Biomarkers Prev 2006;15:1935-40. (Pubitemid 44664271)
64. Sigurdson AJ, Jones IM, Wei Q, Wu X, Spitz MR, Stram DA, et al. Prospective analysis of DNA damage and repair markers of lung cancer risk from the Prostate, Lung, Colorectal and Ovarian (PLCO) Cancer Screening Trial. Carcinogenesis 2011;32:69-73.
65. Helleday T, Petermann E, Lundin C, Hodgson B, Sharma RA. DNA repair pathways as targets for cancer therapy. Nat Rev Cancer 2008;8: 193-204. (Pubitemid 351301852)
66. Woźniak K, Bøasiak J. Recognition and repair of DNA-cisplatin adducts. Acta Biochim Pol 2002;49:583-96. (Pubitemid 135700585)
67. Olaussen KA, Mountzios G, Soria JC. ERCC1 as a risk stratifier in platinum-based chemotherapy for nonsmall-cell lung cancer. Curr Opin Pulm Med 2007;13:284-9. (Pubitemid 46847293)
68. Bhagwat NR, Roginskaya VY, Acquafondata MB, Dhir R, Wood RD, Niedernhofer LJ. Immunodetection of DNA repair endonuclease ERCC1-XPF in human tissue. Cancer Res 2009;69:6831-8.
69. Niedernhofer LJ, Bhagwat N, Wood RD. ERCC1 and non-small-cell lung cancer. N Engl J Med 2007;356:2538-40, author reply 2540-1.
70. Wakasugi M, Sancar A. Assembly, subunit composition, and footprint of human DNA repair excision nuclease. Proc Natl Acad Sci U S A 1998;95:6669-74. (Pubitemid 28278038)
71. McHugh PJ, Spanswick VJ, Hartley JA. Repair of DNA interstrand crosslinks: molecular mechanisms and clinical relevance. Lancet Oncol 2001;2:483-90. (Pubitemid 33586303)
72. Arora S, Kothandapani A, Tillison K, Kalman-Maltese V, Patrick SM. Downregulation of XPF-ERCC1 enhances cisplatin efficacy in cancer cells. DNA Repair (Amst) 2010;9:745-53.
73. Trivedi RN, Almeida KH, Fornsaglio JL, Schamus S, Sobol RW.The role of base excision repair in the sensitivity and resistance to temozolomide- mediated cell death. Cancer Res 2005;65:6394-400. (Pubitemid 40994427)
74. Pollack IF, Hamilton RL, Sobol RW, Burnham J, Yates AJ, Holmes EJ, et al. O6-methylguanine-DNA methyltransferase expression strongly correlates with outcome in childhood malignant gliomas: results from the CCG-945 Cohort. J Clin Oncol 2006;24:3431-7. (Pubitemid 46638900)
75. Dopeso H, Mateo-Lozano S, Elez E, Landolfi S, Ramos Pascual FJ, Hernández-Losa J, et al. Aprataxin tumor levels predict response of colorectal cancer patients to irinotecan-based treatment. Clin Cancer Res 2010;16:2375-82.
76. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005;352:997-1003. (Pubitemid 40349502)
77. Graeser M, McCarthy A, Lord CJ, Savage K, Hills M, Salter J, et al. A marker of homologous recombination predicts pathologic complete response to neoadjuvant chemotherapy in primary breast cancer. Clin Cancer Res 2010;16:6159-68.
78. Shuck SC, Turchi JJ. Targeted inhibition of Replication Protein A reveals cytotoxic activity, synergy with chemotherapeutic DNA-damaging agents, and insight into cellular function. Cancer Res 2010;70: 3189-98.
79. Neher TM, Shuck SC, Liu JY, Zhang JT, Turchi JJ. Identification of novel small molecule inhibitors of the XPA protein using in silico based screening. ACS Chem Biol 2010;5:953-65.
80. Anciano Granadillo VJ, Earley JN, Shuck SC, Georgiadis MM, Fitch RW, Turchi JJ. Targeting the OB-folds of replication protein A with small molecules. J Nucleic Acids 2010;2010:304035.
81. Andrews BJ, Turchi JJ. Development of a high-throughput screen for inhibitors of replication protein A and its role in nucleotide excision repair. Mol Cancer Ther 2004;3:385-91. (Pubitemid 39193715)
82. Walton MI, Eve PD, Hayes A, Valenti M, De Haven Brandon A, Box G, et al. The preclinical pharmacology and therapeutic activity of the novel CHK1 inhibitor SAR-020106. Mol Cancer Ther 2010;9: 89-100.
83. Willmore E, Elliott SL, Mainou-Fowler T, Summerfield GP, Jackson GH, O'Neill F, et al. DNA-dependent protein kinase is a therapeutic target and an indicator of poor prognosis in B-cell chronic lymphocytic leukemia. Clin Cancer Res 2008;14:3984-92.
84. Morgan MA, Parsels LA, Zhao L, Parsels JD, Davis MA, Hassan MC, et al. Mechanism of radiosensitization by the Chk1/2 inhibitor AZD7762 involves abrogation of the G2 checkpoint and inhibition of homologous recombinational DNA repair. Cancer Res 2010;70:4972-81.
85. Krishnakumar R, Kraus WL. PARP-1 regulates chromatin structure and transcription through a KDM5B-dependent pathway. Mol Cell 2010; 39:736-49.
86. Krishnakumar R, Kraus WL. The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Mol Cell 2010; 39:8-24.
87. Farmer H, McCabe N, Lord CJ, Tutt AN, Johnson DA, Richardson TB, et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005;434:917-21. (Pubitemid 40559006)
88. Ashworth A. A synthetic lethal therapeutic approach: poly(ADP) ribose polymerase inhibitors for the treatment of cancers deficient in DNA double-strand break repair. J Clin Oncol 2008;26:3785-90.
89. Fong PC, Boss DS, Yap TA, Tutt A, Wu P, Mergui-Roelvink M, et al. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N Engl J Med 2009;361:123-34.
90. O'Shaughnessy J, Osborne C, Pippen JE, Yoffe M, Patt D, Rocha C, et al. Iniparib plus chemotherapy in metastatic triple-negative breast cancer. N Engl J Med 2011;364:205-14.
91. O'Shaughnessy J, Schwartzberg LS, Danso MA, Rugo HS, Miller K, Yardley DA, et al. A randomized phase III study of iniparib (BSI-201) in combination with gemcitabine/carboplatin (G/C) in metastatic triple-negative breast cancer (TNBC). J Clin Oncol 2011;29 (suppl 15): abstr 1007.
92. He JX, Yang CH, Miao ZH. Poly(ADP-ribose) polymerase inhibitors as promising cancer therapeutics. Acta Pharmacol Sin 2010;31:1172-80.
93. Kaelin WG Jr. The concept of synthetic lethality in the context of anticancer therapy. Nat Rev Cancer 2005;5:689-98.