Epigenetic changes of DNA repair genes in cancer

Journal of Molecular Cell Biology

Volumn 3, Issue 1, 2011, Pages 51-58

  Lahtz, Christoph ^a   Pfeifer, Gerd P ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

DNA methylation; DNA repair; Epigenetics

Indexed keywords

EID: 79951470643     PISSN: 16742788     EISSN: 17594685     Source Type: Journal    
DOI: 10.1093/jmcb/mjq053     Document Type: Article

References (115)

1. Agrelo, R., Cheng, W. H., Setien, F., et al. (2006). Epigenetic inactivation of the premature aging Werner syndrome gene in human cancer. Proc. Natl. Acad. Sci. USA 103, 8822-8827. (Pubitemid 43878103)
2. Ai, L., Vo, Q. N., Zuo, C., et al. (2004). Ataxia-telangiectasia-mutated (ATM) gene in head and neck squamous cell carcinoma: promoter hypermethylation with clinical correlation in 100 cases. Cancer Epidemiol. Biomarkers Prev. 13, 150-156. (Pubitemid 38116634)
3. Arai, K., Morishita, K., Shinmura, K., et al. (1997). Cloning of a human homolog of the yeast OGG1 gene that is involved in the repair of oxidative DNA damage. Oncogene 14, 2857-2861. (Pubitemid 27313418)
4. Baylin, S. B., Esteller, M., Rountree, M. R., et al. (2001). Aberrant patterns of DNA methylation, chromatin formation and gene expression in cancer. Hum. Mol. Genet. 10, 687-692. (Pubitemid 32331576)
5. Benachenhou, N., Guiral, S., Gorska-Flipot, I., et al. (1998). Allelic losses and DNA methylation at DNA mismatch repair loci in sporadic colorectal cancer. Carcinogenesis 19, 1925-1929. (Pubitemid 28521932)
6. Bernal, C., Vargas, M., Ossandon, F., et al. (2008). DNA methylation profile in diffuse type gastric cancer: evidence for hypermethylation of the BRCA1 promoter region in early-onset gastric carcinogenesis. Biol. Res. 41, 303-315.
7. Bronner, C. E., Baker, S. M., Morrison, P. T., et al. (1994). Mutation in the DNA mismatch repair gene homologue hMLH1 is associated with hereditary nonpolyposis colon cancer. Nature 368, 258-261.
8. Carter, T., Vancurova, I., Sun, I., et al. (1990). A DNA-activated protein kinase from HeLa cell nuclei. Mol. Cell. Biol. 10, 6460-6471. (Pubitemid 120004590)
9. Catteau, A., Harris, W. H., Xu, C. F., et al. (1999). Methylation of the BRCA1 promoter region in sporadic breast and ovarian cancer: correlation with disease characteristics. Oncogene 18, 1957-1965. (Pubitemid 29150082)
10. Chen, H. Y., Shao, C. J., Chen, F. R., et al. (2010). Role of ERCC1 promoter hypermethylation in drug resistance to cisplatin in human gliomas. Int. J. Cancer 126, 1944-1954.
11. Chevillard, S., Radicella, J. P., Levalois, C., et al. (1998). Mutations in OGG1, a gene involved in the repair of oxidative DNA damage, are found in human lung and kidney tumours. Oncogene 16, 3083-3086. (Pubitemid 28297730)
12. Ciccia, A., and Elledge, S. J. (2010). The DNA damage response: making it safe to play with knives. Mol. Cell 40, 179-204.
13. Czerninski, R., Krichevsky, S., Ashhab, Y., et al. (2009). Promoter hypermethylation of mismatch repair genes, hMLH1 and hMSH2 in oral squamous cell carcinoma. Oral Dis. 15, 206-213.
14. Dhillon, V. S., Shahid, M., and Husain, S. A. (2004). CpG methylation of the FHIT, FANCF, cyclin-D2, BRCA2 and RUNX3 genes in Granulosa cell tumors (GCTs) of ovarian origin. Mol. Cancer 3, 33.
15. Difilippantonio, M. J., Zhu, J., Chen, H. T., et al. (2000). DNA repair protein Ku80 suppresses chromosomal aberrations and malignant transformation. Nature 404, 510-514. (Pubitemid 30186895)
16. Dobrovic, A., and Simpfendorfer, D. (1997). Methylation of the BRCA1 gene in sporadic breast cancer. Cancer Res. 57, 3347-3350. (Pubitemid 27355472)
17. Duncan, J. A., Reeves, J. R., and Cooke, T. G. (1998). BRCA1 and BRCA2 proteins: roles in health and disease. Mol. Pathol. 51, 237-247. (Pubitemid 28480340)
18. Esteller, M., Levine, R., Baylin, S. B., et al. (1998). MLH1 promoter hypermethylation is associated with the microsatellite instability phenotype in sporadic endometrial carcinomas. Oncogene 17, 2413-2417. (Pubitemid 28515395)
19. Esteller, M., Hamilton, S. R., Burger, P. C., et al. (1999). Inactivation of the DNA repair gene O6-methylguanine-DNA methyltransferase by promoter hypermethylation is a common event in primary human neoplasia. Cancer Res. 59, 793-797. (Pubitemid 29086728)
20. Esteller, M., Garcia-Foncillas, J., Andion, E., et al. (2000). Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N. Engl. J. Med. 343, 1350-1354.
21. Fink, D., Zheng, H., Nebel, S., et al. (1997). In vitro and in vivo resistance to cisplatin in cells that have lost DNA mismatch repair. Cancer Res. 57, 1841-1845. (Pubitemid 27209707)
22. Flanagan, J. M., Munoz-Alegre, M., Henderson, S., et al. (2009). Gene-body hypermethylation of ATM in peripheral blood DNA of bilateral breast cancer patients. Hum. Mol. Genet. 18, 1332-1342.
23. Fleisher, A. S., Esteller, M., Wang, S., et al. (1999). Hypermethylation of the hMLH1 gene promoter in human gastric cancers with microsatellite instability. Cancer Res 59, 1090-1095. (Pubitemid 29135970)
24. Fousteri, M., and Mullenders, L. H. (2008). Transcription-coupled nucleotide excision repair in mammalian cells: molecular mechanisms and biological effects. Cell Res. 18, 73-84.
25. Friedberg, E. C. (2001). How nucleotide excision repair protects against cancer. Nat. Rev. Cancer 1, 22-33. (Pubitemid 33741878)
26. Gazzoli, I., Loda, M., Garber, J., et al. (2002). A hereditary nonpolyposis colorectal carcinoma case associated with hypermethylation of the MLH1 gene in normal tissue and loss of heterozygosity of the unmethylated allele in the resulting microsatellite instability-high tumor. Cancer Res 62, 3925-3928. (Pubitemid 34791053)
27. Goldenberg, D., Harden, S., Masayesva, B. G., et al. (2004). Intraoperative molecular margin analysis in head and neck cancer. Arch. Otolaryngol. Head Neck Surg. 130, 39-44. (Pubitemid 38095427)
28. Gras, E., Catasus, L., Arguelles, R., et al. (2001a). Microsatellite instability, MLH-1 promoter hypermethylation, and frameshift mutations at coding mononucleotide repeat microsatellites in ovarian tumors. Cancer 92, 2829-2836. (Pubitemid 33091919)
29. Gras, E., Cortes, J., Diez, O., et al. (2001b). Loss of heterozygosity on chromosome 13q12-q14, BRCA-2 mutations and lack of BRCA-2 promoter hypermethylation in sporadic epithelial ovarian tumors. Cancer 92, 787-795. (Pubitemid 32783064)
30. Gray, M. D., Shen, J. C., Kamath-Loeb, A. S., et al. (1997). The Werner syndrome protein is a DNA helicase. Nat. Genet. 17, 100-103. (Pubitemid 27377541)
31. Guan, H., Ji, M., Hou, P., et al. (2008). Hypermethylation of the DNA mismatch repair gene hMLH1 and its association with lymph node metastasis and T1799A BRAF mutation in patients with papillary thyroid cancer. Cancer 113, 247-255.
32. 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.
33. Hegi, M. E., Diserens, A. C., Gorlia, T., et al. (2005). MGMT gene silencing and benefit from temozolomide in glioblastoma. N. Engl. J. Med. 352, 997-1003. (Pubitemid 40349502)
34. Hendrich, B., and Bird, A. (1998). Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol. Cell. Biol. 18, 6538-6547. (Pubitemid 28500543)
35. Hendrich, B., Hardeland, U., Ng, H. H., et al. (1999). The thymine glycosylase MBD4 can bind to the product of deamination at methylated CpG sites. Nature 401, 301-304.
36. Henneke, G., Friedrich-Heineken, E., and Hubscher, U. (2003). Flap endonuclease 1: a novel tumour suppresser protein. Trends Biochem. Sci. 28, 384-390. (Pubitemid 36851620)
37. Herfarth, K. K., Brent, T. P., Danam, R. P., et al. (1999). A specific CpG methylation pattern of the MGMT promoter region associated with reduced MGMT expression in primary colorectal cancers. Mol. Carcinog. 24, 90-98. (Pubitemid 29115911)
38. Herman, J. G., Umar, A., Polyak, K., et al. (1998). Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc. Natl. Acad. Sci. USA 95, 6870-6875. (Pubitemid 28278073)
39. Hess, C. J., Ameziane, N., Schuurhuis, G. J., et al. (2008). Hypermethylation of the FANCC and FANCL promoter regions in sporadic acute leukaemia. Cell. Oncol. 30, 299-306. (Pubitemid 352032906)
40. Hilton, J. L., Geisler, J. P., Rathe, J. A., et al. (2002). Inactivation of BRCA1 and BRCA2 in ovarian cancer. J. Natl. Cancer Inst. 94, 1396-1406. (Pubitemid 35154144)
41. Hiraoka, L. R., Harrington, J. J., Gerhard, D. S., et al. (1995). Sequence of human FEN-1, a structure-specific endonuclease, and chromosomal localization of the gene (FEN1) in mouse and human. Genomics 25, 220-225.
42. Hitchins, M. P., Wong, J. J., Suthers, G., et al. (2007). Inheritance of a cancerassociated MLH1 germ-line epimutation. N. Engl. J. Med. 356, 697-705.
43. Howard, J. H., Frolov, A., Tzeng, C. W., et al. (2009). Epigenetic downregulation of the DNA repair gene MED1/MBD4 in colorectal and ovarian cancer. Cancer Biol. Ther. 8, 94-100.
44. Iacobuzio-Donahue, C. A., Maitra, A., Olsen, M., et al. (2003). Exploration of global gene expression patterns in pancreatic adenocarcinoma using cDNA microarrays. Am. J. Pathol. 162, 1151-1162. (Pubitemid 36350660)
45. Jackson, S. P., and Bartek, J. (2009). The DNA-damage response in human biology and disease. Nature 461, 1071-1078.
46. Kaina, B., Christmann, M., Naumann, S., et al. (2007). MGMT: key node in the battle against genotoxicity, carcinogenicity and apoptosis induced by alkylating agents. DNA Repair (Amst.) 6, 1079-1099. (Pubitemid 47058389)
47. Kane, M. F., Loda, M., Gaida, G. M., et al. (1997). Methylation of the hMLH1 promoter correlates with lack of expression of hMLH1 in sporadic colon tumors and mismatch repair-defective human tumor cell lines. Cancer Res. 57, 808-811. (Pubitemid 27097998)
48. Kawasaki, T., Ohnishi, M., Suemoto, Y., et al. (2008). WRN promoter methylation possibly connects mucinous differentiation, microsatellite instability and CpG island methylator phenotype in colorectal cancer. Mod. Pathol. 21, 150-158. (Pubitemid 351172166)
49. Kikuchi, K., Taniguchi, Y., Hatanaka, A., et al. (2005). Fen-1 facilitates homologous recombination by removing divergent sequences at DNA break ends. Mol. Cell. Biol. 25, 6948-6955. (Pubitemid 41105895)
50. Kim, W. J., Vo, Q. N., Shrivastav, M., et al. (2002). Aberrant methylation of the ATM promoter correlates with increased radiosensitivity in a human colorectal tumor cell line. Oncogene 21, 3864-3871. (Pubitemid 34620854)
51. Kim, J. M., Sohn, H. Y., Yoon, S. Y., et al. (2005). Identification of gastric cancerrelated genes using a cDNA microarray containing novel expressed sequence tags expressed in gastric cancer cells. Clin. Cancer Res. 11, 473-482. (Pubitemid 40116869)
52. Kim, D. S., Kim, M. J., Lee, J. Y., et al. (2009). Epigenetic inactivation of checkpoint kinase 2 gene in non-small cell lung cancer and its relationship with clinicopathological features. Lung Cancer 65, 247-250.
53. Kim, H. G., Lee, S., Kim, D. Y., et al. (2010). Aberrant methylation of DNA mismatch repair genes in elderly patients with sporadic gastric carcinoma: a comparison with younger patients. J. Surg. Oncol. 101, 28-35.
54. Klungland, A., and Lindahl, T. (1997). Second pathway for completion of human DNA base excision-repair: reconstitution with purified proteins and requirement for DNase IV (FEN1). EMBO J. 16, 3341-3348. (Pubitemid 27234971)
55. Koike, M. (2002). Dimerization, translocation and localization of Ku70 and Ku80 proteins. J. Radiat. Res. (Tokyo) 43, 223-236. (Pubitemid 135691177)
56. Krause, A., Combaret, V., Iacono, I., et al. (2005). Genome-wide analysis of gene expression in neuroblastomas detected by mass screening. Cancer Lett. 225, 111-120. (Pubitemid 40732774)
57. Laird, P. W. (2005). Cancer epigenetics. Hum. Mol. Genet. 14 Spec No 1, R65-R76. (Pubitemid 40542622)
58. Lam, J. S., Seligson, D. B., Yu, H., et al. (2006). Flap endonuclease 1 is overexpressed in prostate cancer and is associated with a high Gleason score. BJU Int. 98, 445-451.
59. LaTulippe, E., Satagopan, J., Smith, A., et al. (2002). Comprehensive gene expression analysis of prostate cancer reveals distinct transcriptional programs associated with metastatic disease. Cancer Res. 62, 4499-4506. (Pubitemid 34827314)
60. Lawes, D. A., Pearson, T., Sengupta, S., et al. (2005). The role of MLH1, MSH2 and MSH6 in the development of multiple colorectal cancers. Br. J. Cancer 93, 472-477. (Pubitemid 43080023)
61. Lee, M. N., Tseng, R. C., Hsu, H. S., et al. (2007). Epigenetic inactivation of the chromosomal stability control genes BRCA1, BRCA2, and XRCC5 in non-small cell lung cancer. Clin. Cancer Res. 13, 832-838.
62. Lim, S. L., Smith, P., Syed, N., et al. (2008). Promoter hypermethylation of FANCF and outcome in advanced ovarian cancer. Br. J. Cancer 98, 1452-1456. (Pubitemid 351543586)
63. Liu, K., Huang, H., Mukunyadzi, P., et al. (2002). Promoter hypermethylation: an important epigenetic mechanism for hMLH1 gene inactivation in head and neck squamous cell carcinoma. Otolaryngol. Head Neck Surg. 126, 548-553. (Pubitemid 41123543)
64. Marsit, C. J., Liu, M., Nelson, H. H., et al. (2004). Inactivation of the Fanconi anemia/BRCA pathway in lung and oral cancers: implications for treatment and survival. Oncogene 23, 1000-1004. (Pubitemid 38250946)
65. Maruya, S., Issa, J. P., Weber, R. S., et al. (2004). Differential methylation status of tumor-associated genes in head and neck squamous carcinoma: incidence and potential implications. Clin. Cancer Res. 10, 3825-3830. (Pubitemid 38697618)
66. Matsuoka, S., Huang, M., and Elledge, S. J. (1998). Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science 282, 1893-1897. (Pubitemid 28555269)
67. Mellai, M., Caldera, V., Annovazzi, L., et al. (2009). MGMT promoter hypermethylation in a series of 104 glioblastomas. Cancer Genomics Prot. 6, 219-227.
68. Miki, Y., Swensen, J., Shattuck-Eidens, D., et al. (1994). A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science 266, 66-71. (Pubitemid 24345325)
69. Nagasaka, T., Rhees, J., Kloor, M., et al. (2010). Somatic hypermethylation of MSH2 is a frequent event in Lynch syndrome colorectal cancers. Cancer Res. 70, 3098-3108.
70. Narayan, G., Arias-Pulido, H., Nandula, S. V., et al. (2004). Promoter hypermethylation of FANCF: disruption of Fanconi anemia-BRCA pathway in cervical cancer. Cancer Res. 64, 2994-2997. (Pubitemid 38581394)
71. Narod, S. A. (2010). BRCA mutations in the management of breast cancer: the state of the art. Nat. Rev. Clin. Oncol. 7, 702-707.
72. 6-methylguanine-DNA methyltransferase (MGMT) gene by in situ hybridization. Mutagenesis 7, 83-85.
73. Nikolova, T., Christmann, M., and Kaina, B. (2009). FEN1 is overexpressed in testis, lung and brain tumors. Anticancer Res. 29, 2453-2459.
74. Ogino, S., Meyerhardt, J. A., Kawasaki, T., et al. (2007). CpG island methylation, response to combination chemotherapy, and patient survival in advanced microsatellite stable colorectal carcinoma. Virchows Arch. 450, 529-537. (Pubitemid 46676250)
75. Olopade, O. I., and Wei, M. (2003). FANCF methylation contributes to chemoselectivity in ovarian cancer. Cancer Cell 3, 417-420. (Pubitemid 38340287)
76. Otto, C. J., Almqvist, E., Hayden, M. R., et al. (2001). The 'flap' endonuclease gene FEN1 is excluded as a candidate gene implicated in the CAG repeat expansion underlying Huntington disease. Clin. Genet. 59, 122-127. (Pubitemid 32220026)
77. Oue, N., Shigeishi, H., Kuniyasu, H., et al. (2001). Promoter hypermethylation of MGMT is associated with protein loss in gastric carcinoma. Int. J. Cancer 93, 805-809. (Pubitemid 32756749)
78. Peng, B., Hodge, D. R., Thomas, S. B., et al. (2005). Epigenetic silencing of the human nucleotide excision repair gene, hHR23B, in interleukin-6-responsive multiple myeloma KAS-6/1 cells. J. Biol. Chem. 280, 4182-4187. (Pubitemid 40288583)
79. Peng, B., Hurt, E. M., Hodge, D. R., et al. (2006). DNA hypermethylation and partial gene silencing of human thymine-DNA glycosylase in multiple myeloma cell lines. Epigenetics 1, 138-145.
80. Pfeifer, G. P. (2006). Mutagenesis at methylated CpG sequences. Curr. Top. Microbiol. Immunol. 301, 259-281. (Pubitemid 43022676)
81. Riedl, T., Hanaoka, F., and Egly, J. M. (2003). The comings and goings of nucleotide excision repair factors on damaged DNA. EMBO J. 22, 5293-5303. (Pubitemid 37222048)
82. Sato, M., Girard, L., Sekine, I., et al. (2003). Increased expression and no mutation of the flap endonuclease (FEN1) gene in human lung cancer. Oncogene 22, 7243-7246. (Pubitemid 37378557)
83. Seedhouse, C. H., Das-Gupta, E. P., and Russell, N. H. (2003). Methylation of the hMLH1 promoter and its association with microsatellite instability in acute myeloid leukemia. Leukemia 17, 83-88. (Pubitemid 36175892)
84. Shamsara, J., Sharif, S., Afsharnezhad, S., et al. (2009). Association between MGMT promoter hypermethylation and p53 mutation in glioblastoma. Cancer Invest. 27, 825-829.
85. Shinmura, K., and Yokota, J. (2001). The OGG1 gene encodes a repair enzyme for oxidatively damaged DNA and is involved in human carcinogenesis. Antioxid. Redox Signal 3, 597-609. (Pubitemid 32785983)
86. Singh, P., Zheng, L., Chavez, V., et al. (2007). Concerted action of exonuclease and Gap-dependent endonuclease activities of FEN-1 contributes to the resolution of triplet repeat sequences (CTG) n-and (GAA) n-derived secondary structures formed during maturation of Okazaki fragments. J. Biol. Chem. 282, 3465-3477. (Pubitemid 47084421)
87. Singh, P., Yang, M., Dai, H., et al. (2008). Overexpression and hypomethylation of flap endonuclease 1 gene in breast and other cancers. Mol. Cancer Res. 6, 1710-1717.
88. Steinmann, K., Sandner, A., Schagdarsurengin, U., et al. (2009). Frequent promoter hypermethylation of tumor-related genes in head and neck squamous cell carcinoma. Oncol. Rep. 22, 1519-1526.
89. Sugasawa, K., Okamoto, T., Shimizu, Y., et al. (2001). A multistep damage recognition mechanism for global genomic nucleotide excision repair. Genes Dev. 15, 507-521. (Pubitemid 32205141)
90. Sullivan, A., Yuille, M., Repellin, C., et al. (2002). Concomitant inactivation of p53 and Chk2 in breast cancer. Oncogene 21, 1316-1324. (Pubitemid 34214497)
91. Suter, C. M., Martin, D. I., and Ward, R. L. (2004). Germline epimutation of MLH1 in individuals with multiple cancers. Nat. Genet. 36, 497-501. (Pubitemid 38620035)
92. Taccioli, G. E., Gottlieb, T. M., Blunt, T., et al. (1994). Ku80: product of the XRCC5 gene and its role in DNA repair and V (D) J recombination. Science 265, 1442-1445. (Pubitemid 24306796)
93. Tano, K., Shiota, S., Collier, J., et al. (1990). Isolation and structural characterization of a cDNA clone encoding the human DNA repair protein for O6-alkylguanine. Proc. Natl. Acad. Sci. USA 87, 686-690.
94. Titze, S., Peters, H., Wahrisch, S., et al. (2010). Differential MSH2 promoter methylation in blood cells of Neurofibromatosis type 1 (NF1) patients. Eur. J. Hum. Genet. 18, 81-87.
95. Tokunaga, E., Okada, S., Kitao, H., et al. (2009). Low incidence of methylation of the promoter region of the FANCF gene in Japanese primary breast cancer. Breast Cancer, in press.
96. Treilleux, I., Chapot, B., Goddard, S., et al. (2007). The molecular causes of low ATM protein expression in breast carcinoma; promoter methylation and levels of the catalytic subunit of DNA-dependent protein kinase. Histopathology 51, 63-69. (Pubitemid 46976372)
97. Vo, Q. N., Kim, W. J., Cvitanovic, L., et al. (2004). The ATM gene is a target for epigenetic silencing in locally advanced breast cancer. Oncogene 23, 9432-9437. (Pubitemid 40069676)
98. Wang, Y. C., Lu, Y. P., Tseng, R. C., et al. (2003). Inactivation of hMLH1 and hMSH2 by promoter methylation in primary non-small cell lung tumors and matched sputum samples. J. Clin. Invest. 111, 887-895.
99. Wang, Z., Li, M., Lu, S., et al. (2006). Promoter hypermethylation of FANCF plays an important role in the occurrence of ovarian cancer through disrupting Fanconi anemia-BRCA pathway. Cancer Biol. Ther. 5, 256-260.
100. Wang, H., Wang, S., Shen, L., et al. (2010). Chk2 down-regulation by promoter hypermethylation in human bulk gliomas. Life Sci. 86, 185-191.
101. Wei, M., Xu, J., Dignam, J., et al. (2008). Estrogen receptor alpha, BRCA1, and FANCF promoter methylation occur in distinct subsets of sporadic breast cancers. Breast Cancer Res. Treat 111, 113-120. (Pubitemid 352009235)
102. Wiebauer, K., and Jiricny, J. (1989). In vitro correction of G. T mispairs to G. C pairs in nuclear extracts from human cells. Nature 339, 234-236. (Pubitemid 19126398)
103. Williams, L. H., Choong, D., Johnson, S. A., et al. (2006). Genetic and epigenetic analysis of CHEK2 in sporadic breast, colon, and ovarian cancers. Clin. Cancer Res. 12, 6967-6972. (Pubitemid 44974490)
104. Wolf, P., Hu, Y. C., Doffek, K., et al. (2001). O6-methylguanine-DNA methyltransferase promoter hypermethylation shifts the p53 mutational spectrum in non-small cell lung cancer. Cancer Res. 61, 8113-8117. (Pubitemid 33091600)
105. Wooster, R., Neuhausen, S. L., Mangion, J., et al. (1994). Localization of a breast cancer susceptibility gene, BRCA2, to chromosome 13q12-13. Science 265, 2088-2090. (Pubitemid 24325690)
106. Wu, X., Wilson, T. E., and Lieber, M. R. (1999). A role for FEN-1 in nonhomologous DNA end joining: the order of strand annealing and nucleolytic processing events. Proc. Natl. Acad. Sci. USA 96, 1303-1308. (Pubitemid 29098446)
107. Wu, Y. H., Tsai Chang, J. H., Cheng, Y. W., et al. (2007). Xeroderma pigmentosum group C gene expression is predominantly regulated by promoter hypermethylation and contributes to p53 mutation in lung cancers. Oncogene 26, 4761-4773.
108. 6-methylguanine-DNA methyltransferase (MGMT) promoter methylation with p53 mutation occurrence in non-small cell lung cancer with different histology, gender, and smoking status. Ann. Surg. Oncol. 15, 3272-3277.
109. Xing, D., Scangas, G., Nitta, M., et al. (2009). A role for BRCA1 in uterine leiomyosarcoma. Cancer Res. 69, 8231-8235.
110. Yang, J., Xu, Z., Li, J., et al. (2010). XPC epigenetic silence coupled with p53 alteration has a significant impact on bladder cancer outcome. J. Urol. 184, 336-343.
111. Yoon, J. H., Iwai, S., O'Connor, T. R., et al. (2003). Human thymine DNA glycosylase (TDG) and methyl-CpG-binding protein 4 (MBD4) excise thymine glycol (Tg) from a Tg:G mispair. Nucleic Acids Res. 31, 5399-5404. (Pubitemid 37441908)
112. Yoshida, K., and Miki, Y. (2004). Role of BRCA1 and BRCA2 as regulators of DNA repair, transcription, and cell cycle in response to DNA damage. Cancer Sci. 95, 866-871. (Pubitemid 40045520)
113. Yu, J., Zhu, T., Wang, Z., et al. (2007). A novel set of DNA methylation markers in urine sediments for sensitive/specific detection of bladder cancer. Clin. Cancer Res. 13, 7296-7304.
114. Zhang, P., Wang, J., Gao, W., et al. (2004). CHK2 kinase expression is downregulated due to promoter methylation in non-small cell lung cancer. Mol. Cancer 3, 14.
115. Zhang, H., Zhang, S., Cui, J., et al. (2008). Expression and promoter methylation status of mismatch repair gene hMLH1 and hMSH2 in epithelial ovarian cancer. Aust. NZ J. Obstet. Gynaecol. 48, 505-509.