Constitutive promoter methylation of BRCA1 and RAD51C in patients with familial ovarian cancer and early-onset sporadic breast cancer

Human Molecular Genetics

Volumn 21, Issue 21, 2012, Pages 4669-4679

  Hansmann, Tamara ^a   Pliushch, Galyna ^a   Leubner, Monika ^a   Kroll, Patricia ^a   Endt, Daniela ^a   Gehrig, Andrea ^a   Preisler Adams, Sabine ^b   Wieacker, Peter ^b   Haaf, Thomas ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; BISULFITE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN P53;

ADULT; AGED; ARTICLE; BLOOD CELL; BREAST CANCER; CANCER PATIENT; CANCER SUSCEPTIBILITY; CELL TYPE; CONTROLLED STUDY; DNA METHYLATION; FAMILIAL CANCER; FEMALE; GENE FREQUENCY; GENE MUTATION; GENE SILENCING; HUMAN; MAJOR CLINICAL STUDY; MALE; OVARY CANCER; PHYSICAL DEVELOPMENT; PRIORITY JOURNAL; PROMOTER REGION; PYROSEQUENCING; RAD51C GENE; TUMOR SUPPRESSOR GENE;

ADULT; AGE OF ONSET; BRCA1 PROTEIN; BREAST NEOPLASMS; CELL TRANSFORMATION, NEOPLASTIC; DNA METHYLATION; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; FEMALE; GENE SILENCING; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MUTATION; OVARIAN NEOPLASMS; PROMOTER REGIONS, GENETIC;

EID: 84867784222     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds308     Document Type: Article

References (48)

1. Antoniou, A.C. and Chenevix-Trench, G. (2010) Common genetic variants and cancer risk in Mendelian cancer syndromes. Curr. Opin. Genet. Dev., 20, 299-307.
2. O'Donovan, P.J. and Livingston, D.M. (2010) BRCA1 and BRCA2: breast/ovarian cancer susceptibility gene products and participants in DNA double-strand break repair. Carcinogenesis, 31, 961-967.
3. Ghoussaini, M., Fletcher, O., Michailidou, K., Turnbull, C., Schmidt, M.K., Dicks, E., Dennis, J., Wang, Q., Humphreys, M.K., Luccarini, C. et al. (2012) Genome-wide association analysis identifies three new breast cancer susceptibility loci. Nat. Genet., 44, 312-318.
4. Baylin, S.B., Esteller, M., Rountree, M.R., Bachman, K.E., Schuebel, K. and Herman, J.G. (2001) Aberrant patterns of DNA methylation, chromatin formation and gene expression in cancer. Hum. Mol. Genet., 10, 687-692.
5. Esteller, M. (2008) Epigenetics in cancer. N. Engl. J. Med., 358, 1148-1159.
6. Jaenisch, R. and Bird, A. (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet., 33 (suppl.), 245-254.
7. Weber, M., Hellmann, I., Stadler, M.B., Ramos, L., Pääbo, S., Rebhan, M. and Schübeler, D. (2007) Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat. Genet., 39, 457-466.
8. Ehrlich, M. (2006) Cancer-linked DNA hypomethylation and its relationship to hypermethylation. Curr. Top. Microbiol. Immunol., 10, 251-274.
9. Herman, J.G. and Baylin, S.B. (2003) Gene silencing in cancer in association with promoter hypermethylation. N. Engl. J. Med., 349, 2042-2054.
10. Dobrovic, A. and Kristensen, L.S. (2009) DNA methylation, epimutations and cancer predisposition. Int. J. Biochem. Cell Biol., 41, 34-39.
11. Bianco, T., Chenevix-Trench, G., Walsh, D.C., Cooper, J.E. and Dobrovic, A. (2000) Tumour-specific distribution of BRCA1 promoter region methylation supports a pathogenetic role in breast and ovarian cancer. Carcinogenesis, 21, 147-151.
12. Rice, J.C., Ozcelik, H., Maxeiner, P., Andrulis, I. and Futscher, B.W. (2000) Methylation of the BRCA1 promoter is associated with decreased BRCA1 mRNA levels in clinical breast cancer specimens. Carcinogenesis, 21, 1761-1765.
13. Esteller, M., Silva, J.M., Dominguez, G., Bonilla, F., Matias-Guiu, X., Lerma, E., Bussaglia, E., Prat, J., Harkes, I.C., Repasky, E.A. et al. (2000) Promoter hypermethylation and BRCA1 inactivation in sporadic breast and ovarian tumors. J. Natl. Cancer Inst., 92, 564-569.
14. Wei, M., Grushko, T.A., Dignam, J., Hagos, F., Nanda, R., Sveen, L., Xu, J., Fackenthal, J., Tretiakova, M., Das, S. et al. (2005) BRCA1 promoter methylation in sporadic breast cancer is associated with reduced BRCA1 copy number and chromosome 17 aneusomy. Cancer Res., 65, 10692-10699.
15. Baldwin, R.L., Nemeth, E., Tran, H., Shvartsman, H., Cass, I., Narod, S. and Karlan, B.Y. (2000) BRCA1 promoter region hypermethylation in ovarian carcinoma: a population-based study. Cancer Res., 60, 5329-5333.
16. Wilcox, C.B., Baysal, B.E., Gallion, H.H., Strange, M.A. and DeLoia, J.A. (2005) High-resolution methylation analysis of the BRCA1 promoter in ovarian tumors. Cancer Genet. Cytogenet., 59, 114-122.
17. Seeber, L.M. and van Diest, P.J. (2012) Epigenetics in ovarian cancer. Methods Mol. Biol., 863, 253-269.
18. Hitchins, M.P. and Ward, R.L. (2009) Constitutional (germline) MLH1 epimutation as an aetiological mechanism for hereditary non-polyposis colorectal cancer. J. Med. Genet., 46, 793-802.
19. Hitchins, M.P., Rapkins, R.W., Kwok, C.T., Srivastava, S., Wong, J.J., Khachigian, L.M., Polly, P., Goldblatt, J. and Ward, R.L. (2011) Dominantly inherited constitutional epigenetic silencing of MLH1 in a cancer-affected family is linked to a single nucleotide variant within the 5'UTR. Cancer Cell, 20, 200-213.
20. Chan, T.L., Yuen, S.T., Kong, C.K., Chan, Y.W., Chan, A.S., Ng, W.F., Tsui, W.Y., Lo, M.W., Tam, W.Y., Li, V.S. et al. (2006) Heritable germline epimutation of MSH2 in a family with hereditary nonpolyposis colorectal cancer. Nat. Genet., 38, 1178-1183.
21. Ligtenberg, M.J., Kuiper, R.P., Chan, T.L., Goossens, M., Hebeda, K.M., Voorendt, M., Lee, T.Y., Bodmer, D., Hoenselaar, E., Hendriks-Cornelissen, S.J. et al. (2009) Heritable somatic methylation and inactivation of MSH2 in families with Lynch syndrome due to deletion of the 3 ' exons of TACSTD1. Nat. Genet., 41, 112-117.
22. Raval, A., Tanner, S.M., Byrd, J.C., Angerman, E.B., Perko, J.D., Chen, S.S., Hackanson, B., Grever, M.R., Lucas, D.M., Matkovic, J.J. et al. (2007) Downregulation of death-associated protein kinase 1 (DAPK1) in chronic lymphocytic leukemia. Cell, 129, 879-890.
23. Galetzka, D., Hansmann, T., El Hajj, N., Weis, E., Irmscher, B., Ludwig, M., Schneider-Raetzke, B., Kohlschmidt, N., Beyer, V., Bartsch, O. et al. (2012) Monozygotic twins discordant for constitutive BRCA1 promoter methylation, childhood cancer and secondary cancer. Epigenetics, 7, 47-54.
24. Snell, C., Krypuy, M. and Wong, E.M., kConFab investigators, Loughrey, M.B. and Dobrovic, A. (2008) BRCA1 promoter methylation in peripheral blood DNA of mutation negative familial breast cancer patients with a BRCA1 tumour phenotype. Breast Cancer Res., 10, R12.
25. Kontorovich, T., Cohen, Y., Nir, U. and Friedman, E. (2009) Promoter methylation patterns of ATM, ATR, BRCA1, BRCA2 and p53 as putative cancer risk modifiers in Jewish BRCA1/BRCA2 mutation carriers. Breast Cancer Res. Treat., 116, 195-200.
26. Al-Moghrabi, N., Al-Qasem, A.J. and Aboussekhra, A. (2011) Methylation-related mutations in the BRCA1 promoter in peripheral blood cells from cancer-free women. Int. J. Oncol., 39, 129-135.
27. Iwamoto, T., Yamamoto, N., Taguchi, T., Tamaki, Y. and Noguchi, S. (2011) BRCA1 promoter methylation in peripheral blood cells is associated with increased risk of breast cancer with BRCA1 promoter methylation. Breast Cancer Res. Treat., 129, 69-77.
28. Wong, E.M., Southey, M.C., Fox, S.B., Brown, M.A., Dowty, J.G., Jenkins, M.A., Giles, G.G., Hopper, J.L. and Dobrovic, A. (2011) Constitutional methylation of the BRCA1 promoter is specifically associated with BRCA1 mutation-associated pathology in early-onset breast cancer. Cancer Prev. Res., 4, 23-33.
29. Flanagan, J.M., Munoz-Alegre, M., Henderson, S., Tang, T., Sun, P., Johnson, N., Fletcher, O., Dos Santos Silva, I., Peto, J., Boshoff, C. et al. (2009) Gene-body hypermethylation of ATM in peripheral blood DNA of bilateral breast cancer patients. Hum. Mol. Genet., 18, 1332-1342.
30. Brennan, K., Garcia-Closas, M., Orr, N., Fletcher, O., Jones, M., Ashworth, A., Swerdlow, A., Thorne, H., KConFab Investigators, Riboli, E. et al. (2012) Intragenic ATM methylation in peripheral blood DNA as a biomarker of breast cancer risk. Cancer Res., 72, 2304-2313.
31. Bock, C., Walter, J., Paulsen, M. and Lengauer, T. (2008) Inter-individual variation of DNA methylation and its implications for large-scale epigenome mapping. Nucleic Acids Res., 36, e55.
32. Schneider, E., Pliushch, G., El Hajj, N., Galetzka, D., Puhl, A., Schorsch, M., Frauenknecht, K., Riepert, T., Tresch, A., Müller, A.M. et al. (2010) Spatial, temporal and interindividual epigenetic variation of functionally important DNA methylation patterns. Nucleic Acids Res., 38, 3880-3890.
33. Xie, H., Wang, M., de Andrade, A., Bonaldo, M.F., Galat, V., Arndt, K., Rajaram, V., Goldman, S., Tomita, T. and Soares, M.B. (2011) Genome-wide quantitative assessment of variation in DNA methylation patterns. Nucleic Acids Res., 39, 4099-4108.
34. Feinberg, A.P. (2007) Phenotypic plasticity and the epigenetics of human disease. Nature, 447, 433-440.
35. Alegría-Torres, J.A., Baccarelli, A. and Bollati, V. (2011) Epigenetics and lifestyle. Epigenomics, 3, 267-377.
36. Sontag, L.B., Lorincz, M.C. and Georg Luebeck, E. (2006) Dynamics, stability and inheritance of somatic DNA methylation imprints. J. Theor. Biol., 242, 890-899.
37. Jackson, K., Soutto, M., Peng, D., Hu, T., Marshal, D. and El-Rifai, W. (2011) Epigenetic silencing of somatostatin in gastric cancer. Dig. Dis. Sci., 56, 125-130.
38. Magdinier, F., Billard, L.M., Wittmann, G., Frappart, L., Benchaïb, M., Lenoir, G.M., Guérin, J.F. and Dante, R. (2000) Regional methylation of the 5' end CpG island of BRCA1 is associated with reduced gene expression in human somatic cells. FASEB J., 14, 1585-1594.
39. Tost, J., Dunker, J. and Gut, I.G. (2003) Analysis and quantification of multiple methylation variable positions in CpG islands by pyrosequencing. Biotechniques, 35, 152-156.
40. Meindl, A., Hellebrand, H., Wiek, C., Erven, V., Wappenschmidt, B., Niederacher, D., Freund, M., Lichtner, P., Hartmann, L., Schaal, H. et al. (2010) Germline mutations in breast and ovarian cancer pedigrees establish RAD51C as a human cancer susceptibility gene. Nat. Genet, 42, 410-414.
41. Thompson, E.R., Boyle, S.E., Johnson, J., Ryland, G.L., Sawyer, S., Choong, D.Y., kConFab, Chenevix-Trench, G., Trainer, A.H., Lindeman, G.J. et al. (2012) Analysis of RAD51C germline mutations in high-risk breast and ovarian cancer families and ovarian cancer patients. Hum. Mutat., 33, 95-99.
42. Reik, W., Dean, W. and Walter, J. (2001) Epigenetic reprogramming in mammalian development. Science, 293, 1089-1093.
43. El Hajj, N., Trapphoff, T., Linke, M., May, A., Hansmann, T., Kuhtz, J., Reifenberg, K., Heinzmann, J., Niemann, H., Daser, A. et al. (2011) Limiting dilution bisulfite (pyro)sequencing reveals parent-specific methylation patterns in single oocytes and early embryos. Epigenetics, 6, 1176-1188.
44. Dworkin, A.M., Spearman, A.D., Tseng, S.Y., Sweet, K. and Toland, A.E. (2009) Methylation not a frequent 'second hit' in tumors with germline BRCA mutations. Fam. Cancer, 8, 339-346.
45. Chen, Y., Toland, A.E., McLennan, J., Fridlyand, J., Crawford, B., Costello, J.F. and Ziegler, J.L. (2006) Lack of germ-line promoter methylation in BRCA1-negative families with familial breast cancer. Genet. Test., 10, 281-284.
46. Warnecke, P.M., Mann, J.R., Frommer, M. and Clark, S.J. (1988) Bisulfite sequencing in preimplantation embryos: DNA methylation profile of the upstream region of the mouse imprinted H19 gene. Genomics, 51, 182-190.
47. Li, L.C. and Dahiya, R. (2002) Methprimer: designing primers for methylation PCRs. Bioinformatics, 18, 1427-1431.
48. Bock, C., Reither, S., Mikeska, T., Paulsen, M., Walter, J. and Lengauer, T. (2005) BiQ Analyzer: visualization and quality control for DNA methylation data from bisulfite sequencing. Bioinformatics, 21, 4067-4068.