© 2000 by Oxford University Press
Journal of the National Cancer Institute, Vol. 92, No. 7, 564-569,
April 5, 2000
© 2000 Oxford University Press
REPORTS |
Promoter Hypermethylation and BRCA1 Inactivation in Sporadic Breast and Ovarian Tumors
Affiliations of authors: M. Esteller, S. B. Baylin, J. G. Herman, Tumor Biology, The Johns Hopkins Oncology Center, Baltimore, MD; J. M. Silva, G. Dominguez, F. Bonilla, Department of Medical Oncology, Clinica Puerta de Hierro, Madrid, Spain; X. Matias-Guiu, E. Lerma, E. Bussaglia, J. Prat, Department of Pathology, Hospital de la Santa Creu i Sant Pau, Barcelona, Spain; I. C. Harkes, M. Schutte, Department of Medical Oncology, Josephine Nefkens Institute, University Hospital Rotterdam, The Netherlands; E. A. Repasky, Department of Molecular Immunology, Roswell Park Cancer Institute, Buffalo, NY; E. Gabrielson, Department of Pathology, The Johns Hopkins School of Medicine, Baltimore.
Correspondence to: James G. Herman, M.D., The Johns Hopkins Oncology Center, 1650 N. Bond St., Baltimore, MD 21231(e-mail: hermanji{at}jhmi.edu).
Background: Inherited mutations in the BRCA1 gene may be responsible for almost half of inherited breast carcinomas. However, somatic (acquired) mutations in BRCA1 have not been reported, despite frequent loss of heterozygosity (LOH or loss of one copy of the gene) at the BRCA1 locus and loss of BRCA1 protein in tumors. To address whether BRCA1 may be inactivated by pathways other than mutations in sporadic tumors, we analyzed the role of hypermethylation of the gene's promoter region. Methods: Methylation patterns in the BRCA1 promoter were assessed in breast cancer cell lines, xenografts, and 215 primary breast and ovarian carcinomas by methylation-specific polymerase chain reaction (PCR). BRCA1 RNA expression was determined in cell lines and seven xenografts by reverse transcription–PCR. P values are two-sided. Results: The BRCA1 promoter was found to be unmethylated in all normal tissues and cancer cell lines tested. However, BRCA1 promoter hypermethylation was present in two breast cancer xenografts, both of which had loss of the BRCA1 transcript. BRCA1 promoter hypermethylation was present in 11 (13%) of 84 unselected primary breast carcinomas. BRCA1 methylation was strikingly associated with the medullary (67% methylated; P = .0002 versus ductal) and mucinous (55% methylated; P = .0033 versus ductal) subtypes, which are overrepresented in BRCA1 families. In a second series of 66 ductal breast tumors informative for LOH, nine (20%) of 45 tumors with LOH had BRCA1 hypermethylation, while one (5%) of 21 without LOH was methylated (P = .15). In ovarian neoplasms, BRCA1 methylation was found only in tumors with LOH, four (31%) of 13 versus none of 18 without LOH (P = .02). The BRCA1 promoter was unmethylated in other tumor types. Conclusion: Silencing of the BRCA1 gene by promoter hypermethylation occurs in primary breast and ovarian carcinomas, especially in the presence of LOH and in specific histopathologic subgroups. These findings support a role for this tumor suppressor gene in sporadic breast and ovarian tumorigenesis.
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 P. Osin, Y-J. Lu, J. Stone, T. Crook, R. S. Houlston, M. Gasco, B. A. Gusterson, and J. Shipley Distinct Genetic and Epigenetic Changes in Medullary Breast Cancer International Journal of Surgical Pathology, July 1, 2003; 11(3): 153 - 158. [Abstract] [PDF]
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 S. Thakur, T. Nakamura, G. Calin, A. Russo, J. F. Tamburrino, M. Shimizu, G. Baldassarre, S. Battista, A. Fusco, R. P. Wassell, et al. Regulation of BRCA1 Transcription by Specific Single-Stranded DNA Binding Factors Mol. Cell. Biol., June 1, 2003; 23(11): 3774 - 3787. [Abstract] [Full Text] [PDF]
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I. Krop, P. Maguire, J. Lahti-Domenici, G. Lodeiro, A. Richardson, H. K. Johannsdottir, H. Nevanlinna, A. Borg, R. Gelman, R. B. Barkardottir, et al. Lack of HIN-1 Methylation in BRCA1-linked and "BRCA1-like" Breast Tumors Cancer Res., May 1, 2003; 63(9): 2024 - 2027. [Abstract] [Full Text] [PDF]
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B. Segura-Pacheco, C. Trejo-Becerril, E. Perez-Cardenas, L. Taja-Chayeb, I. Mariscal, A. Chavez, C. Acuna, A. M. Salazar, M. Lizano, and A. Duenas-Gonzalez Reactivation of Tumor Suppressor Genes by the Cardiovascular Drugs Hydralazine and Procainamide and Their Potential Use in Cancer Therapy Clin. Cancer Res., May 1, 2003; 9(5): 1596 - 1603. [Abstract] [Full Text] [PDF]
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A. Rathi, A. K. Virmani, J. O. Schorge, K. J. Elias, R. Maruyama, J. D. Minna, S. C. Mok, L. Girard, D. A. Fishman, and A. F. Gazdar Methylation Profiles of Sporadic Ovarian Tumors and nonmalignant Ovaries from High-Risk Women Clin. Cancer Res., November 1, 2002; 8(11): 3324 - 3331. [Abstract] [Full Text] [PDF]
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C. Plass Cancer epigenomics Hum. Mol. Genet., October 1, 2002; 11(20): 2479 - 2488. [Abstract] [Full Text] [PDF]
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S. Sarkar, B. C. Roy, N. Hatano, T. Aoyagi, K. Gohji, and R. Kiyama A Novel Ankyrin Repeat-containing Gene (Kank) Located at 9p24 Is a Growth Suppressor of Renal Cell Carcinoma J. Biol. Chem., September 20, 2002; 277(39): 36585 - 36591. [Abstract] [Full Text] [PDF]
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J. L. Hilton, J. P. Geisler, J. A. Rathe, M. A. Hattermann-Zogg, B. DeYoung, and R. E. Buller Inactivation of BRCA1 and BRCA2 in Ovarian Cancer J Natl Cancer Inst, September 18, 2002; 94(18): 1396 - 1406. [Abstract] [Full Text] [PDF]
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Q. Yang, M. Nakamura, Y. Nakamura, G. Yoshimura, T. Suzuma, T. Umemura, Y. Shimizu, I. Mori, T. Sakurai, and K. Kakudo Two-Hit Inactivation of FHIT by Loss of Heterozygosity and Hypermethylation in Breast Cancer Clin. Cancer Res., September 1, 2002; 8(9): 2890 - 2893. [Abstract] [Full Text] [PDF]
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I. A. Hedenfalk Gene Expression Profiling of Hereditary and Sporadic Ovarian Cancers Reveals Unique BRCA1 and BRCA2 Signatures J Natl Cancer Inst, July 3, 2002; 94(13): 960 - 961. [Full Text] [PDF]
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A. A. Jazaeri, C. J. Yee, C. Sotiriou, K. R. Brantley, J. Boyd, and E. T. Liu Gene Expression Profiles of BRCA1-Linked, BRCA2-Linked, and Sporadic Ovarian Cancers J Natl Cancer Inst, July 3, 2002; 94(13): 990 - 1000. [Abstract] [Full Text] [PDF]
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K. Sobczak and W. J. Krzyzosiak Structural Determinants of BRCA1 Translational Regulation J. Biol. Chem., May 3, 2002; 277(19): 17349 - 17358. [Abstract] [Full Text] [PDF]
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 K. Miyamoto, T. Fukutomi, K. Asada, K. Wakazono, H. Tsuda, T. Asahara, T. Sugimura, and T. Ushijima Promoter Hypermethylation and Post-transcriptional Mechanisms for Reduced BRCA1 Immunoreactivity in Sporadic Human Breast Cancers Jpn. J. Clin. Oncol., March 1, 2002; 32(3): 79 - 84. [Abstract] [Full Text] [PDF]
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L.-w. Tan, T. Bianco, and A. Dobrovic Variable promoter region CpG island methylation of the putative tumor suppressor gene Connexin 26 in breast cancer Carcinogenesis, February 1, 2002; 23(2): 231 - 236. [Abstract] [Full Text] [PDF]
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J. P. Geisler, M. A. Hatterman-Zogg, J. A. Rathe, and R. E. Buller Frequency of BRCA1 Dysfunction in Ovarian Cancer J Natl Cancer Inst, January 2, 2002; 94(1): 61 - 67. [Abstract] [Full Text] [PDF]
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M. Esteller, M. F. Fraga, M. Guo, J. Garcia-Foncillas, I. Hedenfalk, A. K. Godwin, J. Trojan, C. Vaurs-Barriere, Y.-J. Bignon, S. Ramus, et al. DNA methylation patterns in hereditary human cancers mimic sporadic tumorigenesis Hum. Mol. Genet., December 1, 2001; 10(26): 3001 - 3007. [Abstract] [Full Text] [PDF]
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S. Dhar, R. Bhargava, M. Yunes, B. Li, J. Goyal, S. P. Naber, D. E. Wazer, and V. Band Analysis of Normal Epithelial Cell Specific-1 (NES1)/Kallikrein 10 mRNA Expression by in Situ Hybridization, a Novel Marker for Breast Cancer Clin. Cancer Res., November 1, 2001; 7(11): 3393 - 3398. [Abstract] [Full Text] [PDF]
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I. E. Krop, D. Sgroi, D. A. Porter, K. L. Lunetta, R. LeVangie, P. Seth, C. M. Kaelin, E. Rhei, M. Bosenberg, S. Schnitt, et al. HIN-1, a putative cytokine highly expressed in normal but not cancerous mammary epithelial cells PNAS, July 24, 2001; (2001) 171138398. [Abstract] [Full Text] [PDF]
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Y. Yuan, R. Mendez, A. Sahin, and J. L. Dai Hypermethylation Leads to Silencing of the SYK Gene in Human Breast Cancer Cancer Res., July 1, 2001; 61(14): 5558 - 5561. [Abstract] [Full Text] [PDF]
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A. K. Virmani, A. Rathi, U. G. Sathyanarayana, A. Padar, C. X. Huang, H. T. Cunnigham, A. J. Farinas, S. Milchgrub, D. M. Euhus, M. Gilcrease, et al. Aberrant Methylation of the Adenomatous Polyposis Coli (APC) Gene Promoter 1A in Breast and Lung Carcinomas Clin. Cancer Res., July 1, 2001; 7(7): 1998 - 2004. [Abstract] [Full Text] [PDF]
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L. Chen, N. Matsubara, T. Yoshino, T. Nagasaka, N. Hoshizima, Y. Shirakawa, Y. Naomoto, H. Isozaki, K. Riabowol, and N. Tanaka Genetic Alterations of Candidate Tumor Suppressor ING1 in Human Esophageal Squamous Cell Cancer Cancer Res., June 1, 2001; 61(11): 4345 - 4349. [Abstract] [Full Text] [PDF]
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J. F Costello and C. Plass Methylation matters J. Med. Genet., May 1, 2001; 38(5): 285 - 303. [Abstract] [Full Text]
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R. Dammann, G. Yang, and G. P. Pfeifer Hypermethylation of the CpG Island of Ras Association Domain Family 1A (RASSF1A), a Putative Tumor Suppressor Gene from the 3p21.3 Locus, Occurs in a Large Percentage of Human Breast Cancers Cancer Res., April 1, 2001; 61(7): 3105 - 3109. [Abstract] [Full Text]
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M. Esteller, P. G. Corn, S. B. Baylin, and J. G. Herman A Gene Hypermethylation Profile of Human Cancer Cancer Res., April 1, 2001; 61(8): 3225 - 3229. [Abstract] [Full Text]
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M. T. Hartsough, S. E. Clare, M. Mair, A. G. Elkahloun, D. Sgroi, C. K. Osborne, G. Clark, and P. S. Steeg Elevation of Breast Carcinoma Nm23-H1 Metastasis Suppressor Gene Expression and Reduced Motility by DNA Methylation Inhibition Cancer Res., March 1, 2001; 61(5): 2320 - 2327. [Abstract] [Full Text]
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G. Strathdee, K. Appleton, M. Illand, D. W. M. Millan, J. Sargent, J. Paul, and R. Brown Primary Ovarian Carcinomas Display Multiple Methylator Phenotypes Involving Known Tumor Suppressor Genes Am. J. Pathol., March 1, 2001; 158(3): 1121 - 1127. [Abstract] [Full Text] [PDF]
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I. Hedenfalk, D. Duggan, Y. Chen, M. Radmacher, M. Bittner, R. Simon, P. Meltzer, B. Gusterson, M. Esteller, M. Raffeld, et al. Gene-Expression Profiles in Hereditary Breast Cancer N. Engl. J. Med., February 22, 2001; 344(8): 539 - 548. [Abstract] [Full Text] [PDF]
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K.-A. Phillips Immunophenotypic and Pathologic Differences Between BRCA1 and BRCA2 Hereditary Breast Cancers J. Clin. Oncol., November 1, 2000; 18(90001): 107s - 112. [Abstract] [Full Text] [PDF]
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R. L. Baldwin, E. Nemeth, H. Tran, H. Shvartsman, I. Cass, S. Narod, and B. Y. Karlan BRCA1 Promoter Region Hypermethylation in Ovarian Carcinoma: A Population-based Study Cancer Res., October 1, 2000; 60(19): 5329 - 5333. [Abstract] [Full Text]
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S. B. Baylin, S. A. Belinsky, and J. G. Herman Aberrant Methylation of Gene Promoters in Cancer--Concepts, Misconcepts, and Promise J Natl Cancer Inst, September 20, 2000; 92(18): 1460 - 1461. [Full Text] [PDF]
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L. Hilakivi-Clarke Estrogens, BRCA1, and Breast Cancer Cancer Res., September 1, 2000; 60(18): 4993 - 5001. [Abstract] [Full Text]
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E. R. Fearon BRCA1 and E-Cadherin Promoter Hypermethylation and Gene Inactivation in Cancer--Association or Mechanism? J Natl Cancer Inst, April 5, 2000; 92(7): 515 - 517. [Full Text] [PDF]
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I. E. Krop, D. Sgroi, D. A. Porter, K. L. Lunetta, R. LeVangie, P. Seth, C. M. Kaelin, E. Rhei, M. Bosenberg, S. Schnitt, et al. HIN-1, a putative cytokine highly expressed in normal but not cancerous mammary epithelial cells PNAS, August 14, 2001; 98(17): 9796 - 9801. [Abstract] [Full Text] [PDF]
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