Multiple roles of the ERCC1-XPF endonuclease in DNA repair and resistance to anticancer drugs

Anticancer Research

Volumn 30, Issue 9, 2010, Pages 3223-3232

  Kirschner, Kristina ^a   Melton, David W ^b  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Chemotherapy; DNA repair; ERCC1; Review; XPF

Indexed keywords

ANTINEOPLASTIC AGENT; CISPLATIN; ENDONUCLEASE; EXCISION REPAIR CROSS COMPLEMENTING PROTEIN 1; MESSENGER RNA; PACLITAXEL; RIBONUCLEOTIDE REDUCTASE; DNA BINDING PROTEIN; ERCC1 PROTEIN, HUMAN; XERODERMA PIGMENTOSUM GROUP F PROTEIN;

BLADDER CANCER; CANCER CHEMOTHERAPY; CANCER STAGING; CANCER SURVIVAL; CHEMOSENSITIVITY; COLORECTAL CANCER; DNA BINDING; DNA RECOMBINATION; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ESOPHAGUS CANCER; EXCISION REPAIR; GENE EXPRESSION; GENETIC TRANSCRIPTION; HEAD AND NECK CANCER; HUMAN; LUNG NON SMALL CELL CANCER; METASTASIS; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN TARGETING; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; SKIN CANCER; XERODERMA PIGMENTOSUM; ANIMAL; DRUG RESISTANCE; GENETICS; NEOPLASM; SIGNAL TRANSDUCTION;

ANIMALS; DNA REPAIR; DNA-BINDING PROTEINS; DRUG RESISTANCE, NEOPLASM; ENDONUCLEASES; HUMANS; NEOPLASMS; SIGNAL TRANSDUCTION;

EID: 77958535871     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (77)

1. Westerveld A, Hoeijmakers JH, van Duin M, de Wit J, Odijk H, Pastink A, Wood RD and Bootsma D: Molecular cloning of a human DNA repair gene. Nature 310: 425-429, 1984. (Pubitemid 14051113)
2. Gaillard PH and Wood RD: Activity of individual ERCC1 and XPF subunits in DNA nucleotide excision repair. Nucleic Acids Res 29: 872-879, 2001.
3. Tripsianes K, Folkers GE, Zheng C, Das D, Grinstead JS, Kaptein R and Boelens R: Analysis of the XPA and ssDNA-binding surfaces on the central domain of human ERCC1 reveals evidence for subfunctionalization. Nucleic Acids Res 35: 5789-5798, 2007.
4. Tripsianes K, Folkers G, Ab E, Das D, Odijk H, Jaspers NG, Hoeijmakers JH, Kaptein R and Boelens R: The structure of the human ERCC1/XPF interaction domains reveals a complementary role for the two proteins in nucleotide excision repair. Structure 13: 1849-1858, 2005.
5. Orelli B, McClendon TB, Tsodikov OV, Ellenberger T, Niedernhofer LJ and Scharer OD: The XPA-binding domain of ERCC1 is required for nucleotide excision repair but not other DNA repair pathways. J Biol Chem 285: 3705-3712, 2010.
6. Tsodikov OV, Enzlin JH, Scharer OD and Ellenberger T: Crystal structure and DNA binding functions of ERCC1, a subunit of the DNA structure-specific endonuclease XPF-ERCC1. Proc Natl Acad Sci USA 102: 11236-11241, 2005.
7. Tsodikov OV, Ivanov D, Orelli B, Staresincic L, Shoshani I, Oberman R, Scharer OD, Wagner G and Ellenberger T: Structural basis for the recruitment of ERCC1-XPF to nucleotide excision repair complexes by XPA. EMBO J 26: 4768-4776, 2007.
8. Yagi T, Wood RD and Takebe H: A low content of ERCC1 and a 120 kDa protein is a frequent feature of group F xeroderma pigmentosum fibroblast cells. Mutagenesis 12: 41-44, 1997. (Pubitemid 27042050)
9. Arora S, Kothandapani A, Tillison K, Kalman-Maltese V and Patrick SM: Down-regulation of XPF-ERCC1 enhances cisplatin efficacy in cancer cells. DNA Repair (Amst), 2010 (doi:10.1016/j.dnarep, 2010.03.10).
10. van Duin M, de Wit J, Odijk H, Westerveld A, Yasui A, Koken MH, Hoeijmakers JH and Bootsma D: Molecular characterization of the human excision repair gene ERCC-1: cDNA cloning and amino acid homology with the yeast DNA repair gene RADIO. Cell 44: 913-923, 1986.
11. Cleaver JE, Lam ET and Revet I: Disorders of nucleotide excision repair: the genetic and molecular basis of heterogeneity. Nat Rev Genet 10: 756-768, 2009.
12. de Boer J and Hoeijmakers JH: Nucleotide excision repair and human syndromes. Carcinogenesis 21: 453-460, 2000.
13. Gillet LC and Scharer OD: Molecular mechanisms of mammalian global genome nucleotide excision repair. Chem Rev 106: 253-276, 2006. (Pubitemid 43316557)
14. Enzlin JH and Scharer OD: The active site of the DNA repair endonuclease XPF-ERCC1 forms a highly conserved nuclease motif. Embo J 21: 2045-2053, 2002.
15. Sargent RG, Rolig RL, Kilburn AE, Adair GM, Wilson JH and Nairn RS: Recombination-dependent deletion formation in mammalian cells deficient in the nucleotide excision repair gene ERCC1. Proc Natl Acad Sci USA 94: 13122-13127, 1997.
16. Ahmad A, Robinson AR, Duensing A, van Drunen E, Beverloo HB, Weisberg DB, Hasty P, Hoeijmakers JH and Niedernhofer LJ: ERCC1-XPF endonuclease facilitates DNA double-strand break repair. Mol Cell Biol 28: 5082-5092, 2008.
17. Sargent RG, Meservy JL, Perkins BD, Kilburn AE, Intody Z, Adair GM, Nairn RS and Wilson JH: Role of the nucleotide excision repair gene ERCC1 in formation of recombination-dependent rearrangements in mammalian cells. Nucleic Acids Res 28: 3771-3778, 2000.
18. Yan CT, Boboila C, Souza EK, Franco S, Hickernell TR, Murphy M, Gumaste S, Geyer M, Zarrin AA, Manis JP, Rajewsky K and Alt FW: IgH class switching and translocations use a robust non-classical end-joining pathway. Nature 449: 478-482, 2007.
19. Adair GM, Rolig RL, Moore-Faver D, Zabelshansky M, Wilson JH and Nairn RS: Role of ERCC1 in removal of long non-homologous tails during targeted homologous recombination. Embo J 19: 5552-5561, 2000.
20. Kuraoka I, Kobertz WR, Ariza RR, Biggerstaff M, Essigmann JM and Wood RD: Repair of an interstrand DNA cross-link initiated by ERCC1-XPF repair/recombination nuclease. J Biol Chem 275: 26632-26636, 2000.
21. Fisher LA, Bessho M and Bessho T: Processing of a psoralen DNA interstrand cross-link by XPF-ERCC1 complex in vitro. J Biol Chem 283: 1275-1281, 2008.
22. Melton DW, Ketchen AM, Nunez F, Bonatti-Abbondandolo S, Abbondandolo A, Squires S and Johnson RT: Cells from ERCC1-deficient mice show increased genome instability and a reduced frequency of S-phase-dependent illegitimate chromosome exchange but a normal frequency of homologous recombination. J Cell Sci 111(Pt 3): 395-404, 1998.
23. Al-Minawi AZ, Lee YF, Hakansson D, Johansson F, Lundin C, Saleh-Gohari N, Schultz N, Jenssen D, Bryant HE, Meuth M, Hinz JM and Helleday T: The ERCC1/XPF endonuclease is required for completion of homologous recombination at DNA replication forks stalled by inter-strand cross-links. Nucleic Acids Res 37: 6400-6413, 2009.
24. Paques F and Haber JE: Two pathways for removal of nonhomologous DNA ends during double-strand break repair in Saccharomyces cerevisiae. Mol Cell Biol 17: 6765-6771, 1997. (Pubitemid 27451224)
25. Zheng H, Wang X, Legerski RJ, Glazer PM and Li L: Repair of DNA interstrand cross-links: interactions between homology-dependent and homology-independent pathways. DNA Repair (Amst) 5: 566-574, 2006.
26. Al-Minawi AZ, Saleh-Gohari N and Helleday T: The ERCC1/XPF endonuclease is required for efficient single-strand annealing and gene conversion in mammalian cells. Nucleic Acids Res 36: 1-9, 2008.
27. Sarkar S, Davies AA, Ulrich HD and McHugh PJ: DNA interstrand crosslink repair during G1 involves nucleotide excision repair and DNA polymerase zeta. Embo J 25: 1285-1294, 2006.
28. Zhang N, Liu X, Li L and Legerski R: Double-strand breaks induce homologous recombinational repair of interstrand cross-links via cooperation of MSH2, ERCC1-XPF, REV3, and the Fanconi anemia pathway. DNA Repair (Amst) 6: 1670-1678, 2007. (Pubitemid 47600111)
29. Zhu XD, Niedernhofer L, Kuster B, Mann M, Hoeijmakers JH and de Lange T: ERCC1/XPF removes the 3′ overhang from uncapped telomeres and represses formation of telomeric DNA-containing double minute chromosomes. Mol Cell 12: 1489-1498, 2003.
30. Munoz P, Blanco R, Flores JM and Blasco MA: XPF nuclease-dependent telomere loss and increased DNA damage in mice overexpressing TRF2 result in premature aging and cancer. Nat Genet 37: 1063-1071, 2005.
31. Wu Y, Zacal NJ, Rainbow AJ and Zhu XD: XPF with mutations in its conserved nuclease domain is defective in DNA repair but functions in TRF2-mediated telomere shortening. DNA Repair (Amst) 6: 157-166, 2007.
32. Petit C and Sancar A: Nucleotide excision repair: from E. coli to man. Biochimie 81: 15-25, 1999.
33. Sijbers AM, van Voorst Vader PC, Snoek JW, Raams A, Jaspers NG and Kleijer WJ: Homozygous R788W point mutation in the XPF gene of a patient with xeroderma pigmentosum and late-onset neurologic disease. J Invest Dermatol 110: 832-836, 1998.
34. Matsumura Y, Nishigori C, Yagi T, Imamura S and Takebe H: Characterization of molecular defects in xeroderma pigmentosum group F in relation to its clinically mild symptoms. Hum Mol Genet 7: 969-974, 1998. (Pubitemid 28256589)
35. Niedernhofer LJ, Garinis GA, Raams A, Lalai AS, Robinson AR, Appeldoorn E, Odijk H, Oostendorp R, Ahmad A, van Leeuwen W, Theil AF, Vermeulen W, van der Horst GT, Meinecke P, Kleijer WJ, Vijg J, Jaspers NG and Hoeijmakers JH: A new progeroid syndrome reveals that genotoxic stress suppresses the somatotroph axis. Nature 444: 1038-1043, 2006.
36. Jaspers NG, Raams A, Silengo MC, Wijgers N, Niedernhofer LJ, Robinson AR, Giglia-Mari G, Hoogstraten D, Kleijer WJ, Hoeijmakers JH and Vermeulen W: First reported patient with human ERCC1 deficiency has cerebro-oculo-facio-skeletal syndrome with a mild defect in nucleotide excision repair and severe developmental failure. Am J Hum Genet 80: 457-466, 2007.
37. McWhir J, Selfridge J, Harrison DJ, Squires S and Melton DW: Mice with DNA repair gene (ERCC-1) deficiency have elevated levels of p53, liver nuclear abnormalities and die before weaning. Nat Genet 5: 217-224, 1993.
38. Weeda G, Donker I, de Wit J, Morreau H, Janssens R, Vissers CJ, Nigg A, van Steeg H, Bootsma D and Hoeijmakers JH: Disruption of mouse ERCC1 results in a novel repair syndrome with growth failure, nuclear abnormalities and senescence. Curr Biol 7: 427-439, 1997.
39. Nunez F, Chipchase MD, Clarke AR and Melton DW: Nucleotide excision repair gene (ERCC1) deficiency causes G(2) arrest in hepatocytes and a reduction in liver binucleation: the role of p53 and p21. FASEB J 14: 1073-1082, 2000. (Pubitemid 30350388)
40. Kirschner K, Singh R, Prost S and Melton DW: Characterisation of Ercc1 deficiency in the liver and in conditional ERCC1-deficient primary hepatocytes in vitro. DNA Repair (Amst) 6: 304-316, 2007.
41. Dolle ME, Busuttil RA, Garcia AM, Wijnhoven S, van Drunen E, Niedernhofer LJ, van der Horst G, Hoeijmakers JH, van Steeg H and Vijg J: Increased genomic instability is not a prerequisite for shortened lifespan in DNA repair-deficient mice. Mutat Res 596: 22-35, 2006.
42. Prasher JM, Lalai AS, Heijmans-Antonissen C, Ploemacher RE, Hoeijmakers JH, Touw IP and Niedernhofer LJ: Reduced hematopoietic reserves in DNA interstrand crosslink repair-deficient Ercc1-/- mice. EMBO J 24: 861-871, 2005.
43. Doig J, Anderson C, Lawrence NJ, Selfridge J, Brownstein DG and Melton DW: Mice with skin-specific DNA repair gene (ERCC1) inactivation are hypersensitive to ultraviolet irradiation-induced skin cancer and show more rapid actinic progression. Oncogene 25: 6229-6238, 2006. (Pubitemid 44564740)
44. Tian M, Shinkura R, Shinkura N and Alt FW: Growth retardation, early death, and DNA repair defects in mice deficient for the nucleotide excision repair enzyme XPF. Mol Cell Biol 24: 1200-1205, 2004.
45. Simon GR, Sharma S, Cantor A, Smith P and Bepler G: ERCC1 expression is a predictor of survival in resected patients with non-small cell lung cancer. Chest 127: 978-983, 2005.
46. Olaussen KA, Dunant A, Fouret P, Brambilla E, Andre F, Haddad V, Taranchon E, Filipits M, Pirker R, Popper HH, Stahel R, Sabatier L, Pignon JP, Tursz T, Le Chevalier T and Soria JC: DNA repair by ERCC1 in non-small cell lung cancer and cisplatin-based adjuvant chemotherapy. N Engl J Med 355: 983-991, 2006.
47. Wang L, Wei J, Qian X, Yin H, Zhao Y, Yu L, Wang T and Liu B: ERCC1 and BRCA1 mRNA expression levels in metastatic malignant effusions is associated with chemosensitivity to cisplatin and/or docetaxel. BMC Cancer 8: 97, 2008.
48. Jun HJ, Ahn MJ, Kim HS, Yi SY, Han J, Lee SK, Ahn YC, Jeong HS, Son YI, Baek JH and Park K: ERCC1 expression as a predictive marker of squamous cell carcinoma of the head and neck treated with cisplatin-based concurrent chemoradiation. Br J Cancer 99: 167-172, 2008.
49. Kwon HC, Roh MS, Oh SY, Kim SH, Kim MC, Kim JS and Kim HJ: Prognostic value of expression of ERCC1, thymidylate synthase, and glutathione S-transferase P1 for 5-fluorouracil/oxaliplatin chemotherapy in advanced gastric cancer. Ann Oncol 18: 504-509, 2007.
50. Matsubara J, Nishina T, Yamada Y, Moriwaki T, Shimoda T, Kajiwara T, Nakajima TE, Kato K, Hamaguchi T, Shimada Y, Okayama Y, Oka T and Shirao K: Impacts of excision repair cross-complementing gene 1 (ERCC1), dihydropyrimidine dehydrogenase, and epidermal growth factor receptor on the outcomes of patients with advanced gastric cancer. Br J Cancer 98: 832-839, 2008.
51. Bellmunt J, Paz-Ares L, Cuello M, Cecere FL, Albiol S, Guillem V, Gallardo E, Carles J, Mendez P, de la Cruz JJ, Taron M, Rosell R and Baselga J: Gene expression of ERCC1 as a novel prognostic marker in advanced bladder cancer patients receiving cisplatin-based chemotherapy. Ann Oncol 18: 522-528, 2007.
52. Kim MK, Cho KJ, Kwon GY, Park SI, Kim YH, Kim JH, Song HY, Shin JH, Jung HY, Lee GH, Choi KD and Kim SB: ERCC1 predicting chemoradiation resistance and poor outcome in oesophageal cancer. Eur J Cancer 44: 54-60, 2008.
53. Weberpals J, Garbuio K, O'Brien A, Clark-Knowles K, Doucette S, Antoniouk O, Goss G and Dimitroulakos J: The DNA repair proteins BRCA1 and ERCC1 as predictive markers in sporadic ovarian cancer. Int J Cancer 124: 806-815, 2009.
54. Dabholkar M, Vionnet J, Bostick-Bruton F, Yu JJ and Reed E: Messenger RNA levels of XPAC and ERCC1 in ovarian cancer tissue correlate with response to platinum-based chemotherapy. J Clin Invest 94: 703-708, 1994.
55. Akita H, Zheng Z, Takeda Y, Kim C, Kittaka N, Kobayashi S, Marubashi S, Takemasa I, Nagano H, Dono K, Nakamori S, Monden M, Mori M, Doki Y and Bepler G: Significance of RRM1 and ERCC1 expression in resectable pancreatic adenocarcinoma. Oncogene 28: 2903-2909, 2009.
56. Isla D, Sarries C, Rosell R, Alonso G, Domine M, Taron M, Lopez-Vivanco G, Camps C, Botia M, Nunez L, Sanchez-Ronco M, Sanchez JJ, Lopez-Brea M, Barneto I, Paredes A, Medina B, Artal A and Lianes P: Single nucleotide polymorphisms and outcome in docetaxel-cisplatin-treated advanced non-small cell lung cancer. Ann Oncol 15: 1194-1203, 2004.
57. Yu JJ, Lee KB, Mu C, Li Q, Abernathy TV, Bostick-Bruton F and Reed E: Comparison of two human ovarian carcinoma cell lines (A2780/CP70 and MCAS) that are equally resistant to platinum, but differ at codon 118 of the ERCC1 gene. Int J Oncol 16: 555-560, 2000.
58. Zienolddiny S, Campa D, Lind H, Ryberg D, Skaug V, Stangeland L, Phillips DH, Canzian F and Haugen A: Polymorphisms of DNA repair genes and risk of non-small cell lung cancer. Carcinogenesis 27: 560-567, 2006. (Pubitemid 43372885)
59. Smith S, Su D, Rigault de la Longrais IA, Schwartz P, Puopolo M, Rutherford TJ, Mor G, Yu H and Katsaros D: ERCC1 genotype and phenotype in epithelial ovarian cancer identify patients likely to benefit from paclitaxel treatment in addition to platinum-based therapy. J Clin Oncol 25: 5172-5179, 2007.
60. Park DJ, Zhang W, Stoehlmacher J, Tsao-Wei D, Groshen S, Gil J, Yun J, Sones E, Mallik N and Lenz HJ: ERCC1 gene polymorphism as a predictor for clinical outcome in advanced colorectal cancer patients treated with platinum-based chemotherapy. Clin Adv Hematol Oncol 1: 162-166, 2003.
61. Woelfelschneider A, Popanda O, Lilla C, Linseisen J, Mayer C, Celebi O, Debus J, Bartsch H, Chang-Claude J and Schmezer P: A distinct ERCC1 haplotype is associated with mRNA expression levels in prostate cancer patients. Carcinogenesis 29: 1758-1764, 2008.
62. Moreno V, Gemignani F, Landi S, Gioia-Patricola L, Chabrier A, Blanco I, Gonzalez S, Guino E, Capella G and Canzian F: Polymorphisms in genes of nucleotide and base excision repair: risk and prognosis of colorectal cancer. Clin Cancer Res 12: 2101-2108, 2006.
63. Saebo M, Skjelbred CF, Nexo BA, Wallin H, Hansteen IL, Vogel U and Kure EH: Increased mRNA expression levels of ERCC1, OGG1 and RAI in colorectal adenomas and carcinomas. BMC Cancer 6: 208, 2006.
64. Skjelbred CF, Saebo M, Nexo BA, Wallin H, Hansteen IL, Vogel U and Kure EH: Effects of polymorphisms in ERCC1, ASE-1 and RAI on the risk of colorectal carcinomas and adenomas: a case-control study. BMC Cancer 6: 175, 2006.
65. Monzo M, Moreno I, Navarro A, Ibeas R, Artells R, Gel B, Martinez F, Moreno J, Hernandez R and Navarro-Vigo M: Single nucleotide polymorphisms in nucleotide excision repair genes XPA, XPD, XPG and ERCC1 in advanced colorectal cancer patients treated with first-line oxaliplatin/fluoropyrimidine. Oncology 72: 364-370, 2007.
66. Kamikozuru H, Kuramochi H, Hayashi K, Nakajima G and Yamamoto M: ERCC1 codon 118 polymorphism is a useful prognostic marker in patients with pancreatic cancer treated with platinum-based chemotherapy. Int J Oncol 32: 1091-1096, 2008.
67. McWilliams RR, Bamlet WR, Cunningham JM, Goode EL, de Andrade M, Boardman LA and Petersen GM: Polymorphisms in DNA repair genes, smoking, and pancreatic adenocarcinoma risk. Cancer Res 68: 4928-4935, 2008.
68. Povey JE, Darakhshan F, Robertson K, Bisset Y, Mekky M, Rees J, Doherty V, Kavanagh G, Anderson N, Campbell H, MacKie RM and Melton DW: DNA repair gene polymorphisms and genetic predisposition to cutaneous melanoma. Carcinogenesis 28: 1087-1093, 2007.
69. Yu JJ, Thornton K, Guo Y, Kotz H and Reed E: An ERCC1 splicing variant involving the 5′-UTR of the mRNA may have a transcriptional modulatory function. Oncogene 20: 7694-7698, 2001.
70. Winter AG, Dorgan C and Melton DW: Expression of a splicing variant in the 5′-UTR of the human ERCC1 gene is not cancer related. Oncogene 24: 2110-2113, 2005. (Pubitemid 40516205)
71. Chen HY, Shao CJ, Chen FR, Kwan AL and Chen ZP: Role of ERCC1 promoter hypermethylation in drug resistance to cisplatin in human gliomas. Int J Cancer 126: 1944-1954, 2010.
72. Li Q, Gardner K, Zhang L, Tsang B, Bostick-Bruton F and Reed E: Cisplatin induction of ERCC-1 mRNA expression in A2780/CP70 human ovarian cancer cells. J Biol Chem 273: 23419-23425, 1998.
73. Yan QW, Reed E, Zhong XS, Thornton K, Guo Y and Yu JJ: MZF1 possesses a repressively regulatory function in ERCC1 expression. Biochem Pharmacol 71: 761-771, 2006.
74. Ko JC, Su YJ, Lin ST, Jhan JY, Ciou SC, Cheng CM and Lin YW: Suppression of ERCC1 and Rad51 expression through ERK1/2 inactivation is essential in emodin-mediated cytotoxicity in human non-small cell lung cancer cells. Biochem Pharmacol 79: 655-664, 2010.
75. Helleday T, Petermann E, Lundin C, Hodgson B and Sharma RA: DNA repair pathways as targets for cancer therapy. Nat Rev Cancer 8: 193-204, 2008.
76. Barakat KH, Torin Huzil J, Luchko T, Jordheim L, Dumontet C and Tuszynski J: Characterization of an inhibitory dynamic pharmacophore for the ERCC1-XPA interaction using a combined molecular dynamics and virtual screening approach. J Mol Graph Model 28: 113-130, 2009.
77. Jiang H and Yang LY: Cell cycle checkpoint abrogator UCN-01 inhibits DNA repair: association with attenuation of the interaction of XPA and ERCC1 nucleotide excision repair proteins. Cancer Res 59: 4529-4534, 1999.