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DNA Methylation Profiles of Female Steroid Hormone-Driven Human Malignancies

  • Chapter
DNA Methylation: Development, Genetic Disease and Cancer

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 310))

Abstract

Tumor DNA contains valuable clues about the origin and pathogenesis of human cancers. Alterations in DNA methylation can lead to silencing of genes associated with distinct tumorigenic pathways. These pathway-specific DNA methylation changes help define tumor-specific DNA methylation profiles that can be used to further our understanding of tumor development, as well as provide tools for molecular diagnosis and early detection of cancer. Female sex hormones have been implicated in the etiology of several of the women’s cancers including breast, endometrial, ovarian, and proximal colon cancers. We have reviewed the DNA methylation profiles of these cancers to determine whether the hormonal regulation of these cancers results in specific DNA methylation alterations. Although subsets of tumors in each of these four types of cancers were found to share some DNA methylation alterations, we did not find evidence for global hormone-specific DNA methylation alterations, suggesting that female sex hormones may participate in different tumorigenic pathways that are associated with distinct DNA methylation-based molecular signatures. One such pathway may include MLH1 methylation in the context of the CpG island methylator phenotype.

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References

  • Adem C, Soderberg CL, Cunningham JM, Reynolds C, Sebo TJ, Thibodeau SN, Hartmann LC, Jenkins RB (2003) Microsatellite instability in hereditary and sporadic breast cancers. Int J Cancer 107:580–582

    Article  PubMed  CAS  Google Scholar 

  • Agathanggelou A, Honorio S, Macartney DP, Martinez A, Dallol A, Rader J, Fullwood P, Chauhan A, Walker R, Shaw JA, Hosoe S, Lerman MI, Minna JD, Maher ER, Latif F (2001) Methylation associated inactivation of RASSF1A from region 3p21.3 in lung, breast and ovarian tumours. Oncogene 20:1509–1518

    Article  PubMed  CAS  Google Scholar 

  • Akahira J, Suzuki T, Ito K, Kaneko C, Darnel AD, Moriya T, Okamura K, Yaegashi N, Sasano H (2002) Differential expression of progesterone receptor isoforms A and B in the normal ovary, and in benign, borderline, and malignant ovarian tumors. Jpn J Cancer Res 93:807–815

    PubMed  CAS  Google Scholar 

  • Alley PG, McNee RK (1986) Age and sex differences in right colon cancer. Dis Colon Rectum 29:227–229

    PubMed  CAS  Google Scholar 

  • Althuis MD, Fergenbaum JH, Garcia-Closas M, Brinton LA, Madigan MP, Sherman ME (2004) Etiology of hormone receptor-defined breast cancer: a systematic review of the literature. Cancer Epidemiol Biomarkers Prev 13:1558–1568

    PubMed  CAS  Google Scholar 

  • Bae YK, Brown A, Garrett E, Bornman D, Fackler MJ, Sukumar S, Herman JG, Gabrielson E (2004) Hypermethylation in histologically distinct classes of breast cancer. Clin Cancer Res 10:5998–6005

    Article  PubMed  CAS  Google Scholar 

  • Baldwin RL, Nemeth E, Tran H, Shvartsman H, Cass I, Narod S, Karlan BY (2000) BRCA1 promoter region hypermethylation in ovarian carcinoma: a population-based study. Cancer Res 60:5329–5333

    PubMed  CAS  Google Scholar 

  • Bandyopadhyay GK, Imagawa W, Wallace D, Nandi S (1987) Linoleate metabolites enhance the in vitro proliferative response of mouse mammary epithelial cells to epidermal growth factor. J Biol Chem 262:2750–2756

    PubMed  CAS  Google Scholar 

  • Bardin A, Hoffmann P, Boulle N, Katsaros D, Vignon F, Pujol P, Lazennec G (2004) Involvement of estrogen receptor beta in ovarian carcinogenesis. Cancer Res 64:5861–5869

    Article  PubMed  CAS  Google Scholar 

  • Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16:6–21

    Article  PubMed  CAS  Google Scholar 

  • Breivik J, Lothe RA, Meling GI, Rognum TO, Borresen-Dale AL, Gaudernack G (1997) Different genetic pathways to proximal and distal colorectal cancer influenced by sex-related factors. Int J Cancer 74:664–669

    Article  PubMed  CAS  Google Scholar 

  • Burri N, Shaw P, Bouzourene H, Sordat I, Sordat B, Gillet M, Schorderet D, Bosman FT, Chaubert P (2001) Methylation silencing and mutations of the p14ARF and p16INK4a genes in colon cancer. Lab Invest 81:217–229

    PubMed  CAS  Google Scholar 

  • Butcher D, Hassanein K, Dudgeon M, Rhodes J, Holmes FF (1985) Female gender is a major determinant of changing subsite distribution of colorectal cancer with age. Cancer 56:714–716

    Article  PubMed  CAS  Google Scholar 

  • Catteau A, Harris WH, Xu CF, Solomon E (1999) Methylation of the BRCA1 promoter region in sporadic breast and ovarian cancer: correlation with disease characteristics. Oncogene 18:1957–1965

    Article  PubMed  CAS  Google Scholar 

  • Chagpar A, Magliocco A, Kerviche A, Tan L, Walley B, DeCoteau JF (2004) The replication error phenotype is associated with the development of distant metastases in hormonally treated patients with breast carcinoma. Cancer 100:913–919

    Article  PubMed  Google Scholar 

  • Clarke CL, Sutherland RL (1990) Progestin regulation of cellular proliferation. Endocr Rev 11:266–301

    Article  PubMed  CAS  Google Scholar 

  • Claus EB, Schildkraut JM, Thompson WD, Risch NJ (1996) The genetic attributable risk of breast and ovarian cancer. Cancer 77:2318–2324

    Article  PubMed  CAS  Google Scholar 

  • Cohen CJ, Rahaman J (1995) Endometrial cancer. Management of high risk and recurrence including the tamoxifen controversy. Cancer 76:2044–2052

    Article  PubMed  CAS  Google Scholar 

  • Coles B, Ketterer B (1990) The role of glutathione and glutathione transferases in chemical carcinogenesis. Crit Rev Biochem Mol Biol 25:47–70

    PubMed  CAS  Google Scholar 

  • Conneely OM, Mulac-Jericevic B, Lydon JP (2003) Progesterone-dependent regulation of female reproductive activity by two distinct progesterone receptor isoforms. Steroids 68:771–778

    Article  PubMed  CAS  Google Scholar 

  • Costello JF, Fruhwald MC, Smiraglia DJ, Rush LJ, Robertson GP, Gao X, Wright FA, Feramisco JD, Peltomaki P, Lang JC, Schuller DE, Yu L, Bloomfield CD, Caligiuri MA, Yates A, Nishikawa R, Su Huang H, Petrelli NJ, Zhang X, O’Dorisio MS, Held WA, Cavenee WK, Plass C (2000) Aberrant CpG-island methylation has non-random and tumour-type-specific patterns. Nat Genet 24:132–138

    Article  PubMed  CAS  Google Scholar 

  • Cowley SM, Parker MG (1999) A comparison of transcriptional activation by ER alpha and ER beta. J Steroid Biochem Mol Biol 69:165–175

    Article  PubMed  CAS  Google Scholar 

  • Cross HS, Kallay E, Lechner D, Gerdenitsch W, Adlercreutz H, Armbrecht HJ (2004) Phytoestrogens and vitamin D metabolism: a new concept for the prevention and therapy of colorectal, prostate, and mammary carcinomas. J Nutr 134:1207S–1212S

    PubMed  Google Scholar 

  • Dammann R, Yang G, Pfeifer GP (2001) 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 61:3105–3109

    PubMed  CAS  Google Scholar 

  • Davis FG, Furner SE, Persky V, Koch M (1989) The influence of parity and exogenous female hormones on the risk of colorectal cancer. Int J Cancer 43:587–590

    PubMed  CAS  Google Scholar 

  • de Leeuw WJ, van Puijenbroek M, Tollenaar RA, Cornelisse CJ, Vasen HF, Morreau H (2003) Correspondence re: A. Muller et al., Exclusion of breast cancer as an integral tumor of hereditary nonpolyposis colorectal cancer. Cancer Res 62:1014–1019, 2002. Cancer Res 63:1148–1149

    Google Scholar 

  • Dominguez G, Silva J, Garcia JM, Silva JM, Rodriguez R, Munoz C, Chacon I, Sanchez R, Carballido J, Colas A, Espana P, Bonilla F (2003) Prevalence of aberrant methylation of p14ARF over p16INK4a in some human primary tumors. Mutat Res 530:9–17

    PubMed  CAS  Google Scholar 

  • Eads CA, Danenberg KD, Kawakami K, Saltz LB, Danenberg PV, Laird PW (1999) CpG island hypermethylation in human colorectal tumors is not associated with DNA methyltransferase overexpression. Cancer Res 59:2302–2306

    PubMed  CAS  Google Scholar 

  • Eads CA, Lord RV, Wickramasinghe K, Long TI, Kurumboor SK, Bernstein L, Peters JH, DeMeester SR, DeMeester TR, Skinner KA, Laird PW (2001) Epigenetic patterns in the progression of esophageal adenocarcinoma. Cancer Res 61:3410–3418

    PubMed  CAS  Google Scholar 

  • Eden S, Cedar H (1994) Role of DNA methylation in the regulation of transcription. Curr Opin Genet Dev 4:255–259

    Article  PubMed  CAS  Google Scholar 

  • Egger G, Liang G, Aparicio A, Jones PA (2004) Epigenetics in human disease and prospects for epigenetic therapy. Nature 429:457–463

    Article  PubMed  CAS  Google Scholar 

  • Ehrlich M, Woods CB, Yu MC, Dubeau L, Yang F, Campan M, Weisenberger DJ, Long TI, Youn B, Fiala ES, Laird PW (2006) Quantitative analysis of associations between DNA hypermethylation, hypomethylation, and DNMT RNA levels in ovarian tumors. Oncogene (in press)

    Google Scholar 

  • Esteller M(2000) Epigenetic lesions causing genetic lesions in human cancer: promoter hypermethylation of DNA repair genes. Eur J Cancer 36:2294–2300

    Google Scholar 

  • Esteller M, Corn PG, Urena JM, Gabrielson E, Baylin SB, Herman JG (1998a) Inactivation of glutathione S-transferase P1 gene by promoter hypermethylation in human neoplasia. Cancer Res 58:4515–4518

    PubMed  CAS  Google Scholar 

  • Esteller M, Levine R, Baylin SB, Ellenson LH, Herman JG (1998b) MLH1 promoter hypermethylation is associated with the microsatellite instability phenotype in sporadic endometrial carcinomas. Oncogene 17:2413–2417

    Article  PubMed  CAS  Google Scholar 

  • Esteller M, Hamilton SR, Burger PC, Baylin SB, Herman JG (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

    PubMed  CAS  Google Scholar 

  • Esteller M, Silva JM, Dominguez G, Bonilla F, Matias-Guiu X, Lerma E, Bussaglia E, Prat J, Harkes IC, Repasky EA, Gabrielson E, Schutte M, Baylin SB, Herman JG (2000a) Promoter hypermethylation and BRCA1 inactivation in sporadic breast and ovarian tumors. J Natl Cancer Inst 92:564–569

    Article  PubMed  CAS  Google Scholar 

  • Esteller M, Toyota M, Sanchez-Cespedes M, Capella G, Peinado MA, Watkins DN, Issa JP, Sidransky D, Baylin SB, Herman JG (2000b) Inactivation of the DNA repair gene O6-methylguanine-DNA methyltransferase by promoter hypermethylation is associated with G to A mutations in K-ras in colorectal tumorigenesis. Cancer Res 60:2368–2371

    PubMed  CAS  Google Scholar 

  • Esteller M, Corn PG, Baylin SB, Herman JG (2001a) A gene hypermethylation profile of human cancer. Cancer Res 61:3225–3229

    PubMed  CAS  Google Scholar 

  • Esteller M, Fraga MF, Guo M, Garcia-Foncillas J, Hedenfalk I, Godwin AK, Trojan J, Vaurs-Barriere C, Bignon YJ, Ramus S, Benitez J, Caldes T, Akiyama Y, Yuasa Y, Launonen V, Canal MJ, Rodriguez R, Capella G, Peinado MA, Borg A, Aaltonen LA, Ponder BA, Baylin SB, Herman JG (2001b) DNA methylation patterns in hereditary human cancers mimic sporadic tumorigenesis. Hum Mol Genet 10:3001–3007

    Article  PubMed  CAS  Google Scholar 

  • Everson GT, McKinley C, Kern F Jr (1991) Mechanisms of gallstone formation in women. Effects of exogenous estrogen (Premarin) and dietary cholesterol on hepatic lipid metabolism. J Clin Invest 87:237–246

    Article  PubMed  CAS  Google Scholar 

  • Fan S, Wang J, Yuan R, Ma Y, Meng Q, Erdos MR, Pestell RG, Yuan F, Auborn KJ, Goldberg ID, Rosen EM (1999) BRCA1 inhibition of estrogen receptor signaling in transfected cells. Science 284:1354–1356

    Article  PubMed  CAS  Google Scholar 

  • Fazzari MJ, Greally JM (2004) Epigenomics: beyond CpG islands. Nat Rev Genet 5:446–455

    Article  PubMed  CAS  Google Scholar 

  • Feltus FA, Lee EK, Costello JF, Plass C, Vertino PM (2003) Predicting aberrant CpG island methylation. Proc Natl Acad Sci U S A 100:12253–12258

    Article  PubMed  CAS  Google Scholar 

  • Flototto T, Djahansouzi S, Glaser M, Hanstein B, Niederacher D, Brumm C, Beckmann MW (2001) Hormones and hormone antagonists: mechanisms of action in carcinogenesis of endometrial and breast cancer. Horm Metab Res 33:451–457

    Article  PubMed  CAS  Google Scholar 

  • Froggatt NJ, Green J, Brassett C, Evans DG, Bishop DT, Kolodner R, Maher ER (1999) A common MSH2 mutation in English and North American HNPCC families: origin, phenotypic expression, and sex specific differences in colorectal cancer. J Med Genet 36:97–102

    PubMed  CAS  Google Scholar 

  • Furner SE, Davis FG, Nelson RL, Haenszel W (1989) A case-control study of large bowel cancer and hormone exposure in women. Cancer Res 49:4936–4940

    PubMed  CAS  Google Scholar 

  • Furuuchi K, Tada M, Yamada H, Kataoka A, Furuuchi N, Hamada J, Takahashi M, Todo S, Moriuchi T (2000) Somatic mutations of the APC gene in primary breast cancers. Am J Pathol 156:1997–2005

    PubMed  CAS  Google Scholar 

  • Garinis GA, Menounos PG, Spanakis NE, Papadopoulos K, Karavitis G, Parassi I, Christeli E, Patrinos GP, Manolis EN, Peros G (2002) Hypermethylation-associated transcriptional silencing of E-cadherin in primary sporadic colorectal carcinomas. J Pathol 198:442–449

    Article  PubMed  CAS  Google Scholar 

  • Gelber RD, Cole BF, Goldhirsch A, Rose C, Fisher B, Osborne CK, Boccardo F, Gray R, Gordon NH, Bengtsson NO, Sevelda P (1996) Adjuvant chemotherapy plus tamoxifen compared with tamoxifen alone for postmenopausal breast cancer: metaanalysis of quality-adjusted survival. Lancet 347:1066–1071

    Article  PubMed  CAS  Google Scholar 

  • Hilakivi-Clarke L (2000) Estrogens, BRCA1, and breast cancer. Cancer Res 60:4993–5001

    PubMed  CAS  Google Scholar 

  • Hla T, Neilson K (1992) Human cyclooxygenase-2 cDNA. Proc Natl Acad Sci U S A 89:7384–7388

    Article  PubMed  CAS  Google Scholar 

  • Ho SM (2003) Estrogen, progesterone and epithelial ovarian cancer. Reprod Biol Endocrinol 1:73

    Article  PubMed  Google Scholar 

  • Huang M, Sharma S, Mao JT, Dubinett SM (1996) Non-small cell lung cancer-derived soluble mediators and prostaglandin E2 enhance peripheral blood lymphocyte IL-10 transcription and protein production. J Immunol 157:5512–5520

    PubMed  CAS  Google Scholar 

  • Huang TH, Perry MR, Laux DE (1999) Methylation profiling of CpG islands in human breast cancer cells. Hum Mol Genet 8:459–470

    Article  PubMed  CAS  Google Scholar 

  • Iacopetta B (2003) Aberrant DNA methylation: have we entered the era of more than one type of colorectal cancer? Am J Pathol 162:1043–1045

    PubMed  Google Scholar 

  • Ibanez de Caceres I, Battagli C, Esteller M, Herman JG, Dulaimi E, Edelson MI, Bergman C, Ehya H, Eisenberg BL, Cairns P (2004) Tumor cell-specificBRCA1 and RASSF1A hypermethylation in serum, plasma, and peritoneal fluid from ovarian cancer patients. Cancer Res 64:6476–6481

    Article  PubMed  Google Scholar 

  • Issa JP (2000) CpG-island methylation in aging and cancer. Curr Top Microbiol Immunol 249:101–118

    PubMed  CAS  Google Scholar 

  • Issa JP, Ottaviano YL, Celano P, Hamilton SR, Davidson NE, Baylin SB (1994) Methylation of the oestrogen receptor CpG island links ageing and neoplasia in human colon. Nat Genet 7:536–540

    Article  PubMed  CAS  Google Scholar 

  • Jhaveri MS, Morrow CS (1998) Methylation-mediated regulation of the glutathione S-transferase P1 gene in human breast cancer cells. Gene 210:1–7

    Article  PubMed  CAS  Google Scholar 

  • Jin Z, Tamura G, Tsuchiya T, Sakata K, Kashiwaba M, Osakabe M, Motoyama T (2001) Adenomatous polyposis coli (APC) gene promoter hypermethylation in primary breast cancers. Br J Cancer 85:69–73

    Article  PubMed  CAS  Google Scholar 

  • Kane MF, Loda M, Gaida GM, Lipman J, Mishra R, Goldman H, Jessup JM, Kolodner R (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

    PubMed  CAS  Google Scholar 

  • Kastner P, Krust A, Turcotte B, Stropp U, Tora L, Gronemeyer H, Chambon P (1990) Two distinct estrogen-regulated promoters generate transcripts encoding the two functionally different human progesterone receptor forms A and B. EMBO J 9:1603–1614

    PubMed  CAS  Google Scholar 

  • Katabuchi H, van Rees B, Lambers AR, Ronnett BM, Blazes MS, Leach FS, Cho KR, Hedrick L (1995) Mutations in DNA mismatch repair genes are not responsible for microsatellite instability in most sporadic endometrial carcinomas. Cancer Res 55:5556–5560

    PubMed  CAS  Google Scholar 

  • Kelsey JL, Bernstein L (1996) Epidemiology and prevention of breast cancer. Annu Rev Public Health 17:47–67

    Article  PubMed  CAS  Google Scholar 

  • Kinyamu HK, Archer TK (2004) Modifying chromatin to permit steroid hormone receptor-dependent transcription. Biochim Biophys Acta 1677:30–45

    PubMed  CAS  Google Scholar 

  • Kondo Y, Issa JP (2004) Epigenetic changes in colorectal cancer. Cancer Metastasis Rev 23:29–39

    Article  PubMed  CAS  Google Scholar 

  • Krassenstein R, Sauter E, Dulaimi E, Battagli C, Ehya H, Klein-Szanto A, Cairns P (2004) Detection of breast cancer in nipple aspirate fluid by CpG island hypermethylation. Clin Cancer Res 10:28–32

    Article  PubMed  CAS  Google Scholar 

  • Laghi L, Bianchi P, Malesci A (2003) Gender difference for promoter methylation pattern of hMLH1 and p16 in sporadic MSI colorectal cancer. Gastroenterology 124:1165–1166

    PubMed  Google Scholar 

  • Laird PW (2003) The power and the promise of DNA methylation markers. Nat Rev Cancer 3:253–266

    Article  PubMed  CAS  Google Scholar 

  • Lapidus RG, Ferguson AT, Ottaviano YL, Parl FF, Smith HS, Weitzman SA, Baylin SB, Issa JP, Davidson NE (1996) Methylation of estrogen and progesterone receptor gene 5′ CpG islands correlates with lack of estrogen and progesterone receptor gene expression in breast tumors. Clin Cancer Res 2:805–810

    PubMed  CAS  Google Scholar 

  • Lazennec G, Bresson D, Lucas A, Chauveau C, Vignon F (2001) ER beta inhibits proliferation and invasion of breast cancer cells. Endocrinology 142:4120–4130

    Article  PubMed  CAS  Google Scholar 

  • Leake R, Owens O (1990) The prognosis values of steroid receptors, growth factors, and growth factor receptors in ovarian cancer. In: Sharp F, Mason W, Leake R (eds) Ovarian cancer, biological and therapeutic challenges. Chapman and Hall Medical, London, pp 69–75

    Google Scholar 

  • Lee S, Hwang KS, Lee HJ, Kim JS, Kang GH (2004) Aberrant CpG island hypermethylation of multiple genes in colorectal neoplasia. Lab Invest 84:884–893

    Article  PubMed  CAS  Google Scholar 

  • Lehmann U, Langer F, Feist H, Glockner S, Hasemeier B, Kreipe H (2002) Quantitative assessment of promoter hypermethylation during breast cancer development. Am J Pathol 160:605–612

    PubMed  CAS  Google Scholar 

  • Leu YW, Yan PS, Fan M, Jin VX, Liu JC, Curran EM, Welshons WV, Wei SH, Davuluri RV, Plass C, Nephew KP, Huang TH (2004) Loss of estrogen receptor signaling triggers epigenetic silencing of downstream targets in breast cancer. Cancer Res 64:8184–8192

    Article  PubMed  CAS  Google Scholar 

  • Li CI, Daling JR, Malone KE (2003) Incidence of invasive breast cancer by hormone receptor status from 1992 to 1998. J Clin Oncol 21:28–34

    Article  PubMed  CAS  Google Scholar 

  • Lind GE, Thorstensen L, Lovig T, Meling GI, Hamelin R, Rognum TO, Esteller M, Lothe RA (2004) A CpG island hypermethylation profile of primary colorectal carcinomas and colon cancer cell lines. Mol Cancer 3:28

    Article  PubMed  CAS  Google Scholar 

  • Liu B, Parsons RE, Hamilton SR, Petersen GM, Lynch HT, Watson P, Markowitz S, Willson JK, Green J, de la Chapelle A, et al (1994) hMSH2 mutations in hereditary nonpolyposis colorectal cancer kindreds. Cancer Res 54:4590–4594

    PubMed  CAS  Google Scholar 

  • Malagelada JR, Go VL, Summerskill WH, Gamble WS (1973) Bile acid secretion and biliary bile acid composition altered by cholecystectomy. Am J Dig Dis 18:455–459

    Article  PubMed  CAS  Google Scholar 

  • Malaney S, Daly RJ (2001) The ras signaling pathway in mammary tumorigenesis and metastasis. J Mammary Gland Biol Neoplasia 6:101–113

    Article  PubMed  CAS  Google Scholar 

  • Malkhosyan SR, Yamamoto H, Piao Z, Perucho M (2000) Late onset and high incidence of colon cancer of the mutator phenotype with hypermethylated hMLH1 gene in women. Gastroenterology 119:598

    PubMed  CAS  Google Scholar 

  • Mandelson MT, Miglioretti D, Newcomb PA, Harrison R, Potter JD (2003) Hormone replacement therapy in relation to survival in women diagnosed with colon cancer. Cancer Causes Control 14:979–984

    Article  PubMed  Google Scholar 

  • Markl ID, Cheng J, Liang G, Shibata D, Laird PW, Jones PA (2001) Global and genespecific epigenetic patterns in human bladder cancer genomes are relatively stable in vivo and in vitro over time. Cancer Res 61:5875–5884

    PubMed  CAS  Google Scholar 

  • Marks JR, Huper G, Vaughn JP, Davis PL, Norris J, McDonnell DP, Wiseman RW, Futreal PA, Iglehart JD (1997) BRCA1 expression is not directly responsive to estrogen. Oncogene 14:115–121

    Article  PubMed  CAS  Google Scholar 

  • Marra G, Boland CR (1996) DNA repair and colorectal cancer. Gastroenterol Clin North Am 25:755–772

    Article  PubMed  CAS  Google Scholar 

  • Matias-Guiu X, Catasus L, Bussaglia E, Lagarda H, Garcia A, Pons C, Munoz J, Arguelles R, Machin P, Prat J (2001) Molecular pathology of endometrial hyperplasia and carcinoma. Hum Pathol 32:569–577

    Article  PubMed  CAS  Google Scholar 

  • McCluskey LL, Chen C, Delgadillo E, Felix JC, Muderspach LI, Dubeau L (1999) Differences in p16 gene methylation and expression in benign and malignant ovarian tumors. Gynecol Oncol 72:87–92

    Article  PubMed  CAS  Google Scholar 

  • McMichael AJ, Potter JD (1980) Reproduction, endogenous and exogenous sex hormones, and colon cancer: a review and hypothesis. J Natl Cancer Inst 65:1201–1207

    PubMed  CAS  Google Scholar 

  • Medeiros AC, Nagai MA, Neto MM, Brentani RR (1994) Loss of heterozygosity affecting the APC and MCC genetic loci in patients with primary breast carcinomas. Cancer Epidemiol Biomarkers Prev 3:331–333

    PubMed  CAS  Google Scholar 

  • Miyakura Y, Sugano K, Konishi F, Ichikawa A, Maekawa M, Shitoh K, Igarashi S, Kotake K, Koyama Y, Nagai H (2001) Extensive methylation of hMLH1 promoter region predominates in proximal colon cancer with microsatellite instability. Gastroenterology 121:1300–1309

    Article  PubMed  CAS  Google Scholar 

  • Montano MM, Deng H, Liu M, Sun X, Singal R (2004) Transcriptional regulation by the estrogen receptor of antioxidative stress enzymes and its functional implications. Oncogene 23:2442–2453

    Article  PubMed  CAS  Google Scholar 

  • Moreno-Bueno G, Hardisson D, Sanchez C, Sarrio D, Cassia R, Garcia-Rostan G, Prat J, Guo M, Herman JG, Matias-Guiu X, Esteller M, Palacios J (2002) Abnormalities of the APC/beta-catenin pathway in endometrial cancer. Oncogene 21:7981–7990

    Article  PubMed  CAS  Google Scholar 

  • Moreno-Bueno G, Hardisson D, Sarrio D, Sanchez C, Cassia R, Prat J, Herman JG, Esteller M, Matias-Guiu X, Palacios J (2003) Abnormalities of E-and P-cadherin and catenin (beta-, gamma-catenin, and p120ctn) expression in endometrial cancer and endometrial atypical hyperplasia. J Pathol 199:471–478

    Article  PubMed  CAS  Google Scholar 

  • Moscow JA, Townsend AJ, Goldsmith ME, Whang-Peng J, Vickers PJ, Poisson R, Legault-Poisson S, Myers CE, Cowan KH (1988) Isolation of the human anionic glutathione S-transferasec DNA and the relation of its gene expression to estrogen-receptor content in primary breast cancer. Proc Natl Acad Sci U S A 85:6518–6522

    Article  PubMed  CAS  Google Scholar 

  • Murata H, Khattar NH, Kang Y, Gu L, Li GM (2002) Genetic and epigenetic modification of mismatch repair genes hMSH2 and hMLH1 in sporadic breast cancer with microsatellite instability. Oncogene 21:5696–5703

    Article  PubMed  CAS  Google Scholar 

  • Nagasaka T, Sasamoto H, Notohara K, Cullings HM, Takeda M, Kimura K, Kambara T, MacPhee DG, Young J, Leggett BA, Jass JR, Tanaka N, Matsubara N (2004) Colorectal cancer with mutation in BRAF, KRAS, and wild-type with respect to both oncogenes showing different patterns of DNA methylation. J Clin Oncol 22:4584–4594

    Article  PubMed  CAS  Google Scholar 

  • Narayan S, Roy D (2003) Role of APC and DNA mismatch repair genes in the development of colorectal cancers. Mol Cancer 2:41

    Article  PubMed  Google Scholar 

  • Nass SJ, Herman JG, Gabrielson E, Iversen PW, Parl FF, Davidson NE, Graff JR (2000) Aberrant methylation of the estrogen receptor and E-cadherin 5′ CpG islands increases with malignant progression in human breast cancer. Cancer Res 60:4346–4348

    PubMed  CAS  Google Scholar 

  • Navari JR, Roland PY, Keh P, Salvesen HB, Akslen LA, Iversen OE, Das S, Kothari R, Howey S, Phillips B (2000) Loss of estrogen receptor (ER) expression in endometrial tumors is not associated with de novo methylation of the 5′ end of the ER gene. Clin Cancer Res 6:4026–4032

    PubMed  CAS  Google Scholar 

  • Niederacher D, Yan HY, An HX, Bender HG, Beckmann MW (1999) CDKN2A gene inactivation in epithelial sporadic ovarian cancer. Br J Cancer 80:1920–1926

    Article  PubMed  CAS  Google Scholar 

  • Nilsson S, Makela S, Treuter E, Tujague M, Thomsen J, Andersson G, Enmark E, Pettersson K, Warner M, Gustafsson JA (2001) Mechanisms of estrogen action. Physiol Rev 81:1535–1565

    PubMed  CAS  Google Scholar 

  • Nishimura M, Saito T, Yamasaki H, Kudo R (2003) Suppression of gap junctional intercellular communication via 5′ CpG island methylation in promoter region of E-cadherin gene in endometrial cancer cells. Carcinogenesis 24:1615–1623

    Article  PubMed  CAS  Google Scholar 

  • Nolan RD, Danilowicz RM, Eling TE (1988) Role of arachidonic acid metabolism in the mitogenic response of BALB/c 3T3 fibroblasts to epidermal growth factor. Mol Pharmacol 33:650–656

    PubMed  CAS  Google Scholar 

  • Norrie MW, Hawkins NJ, Todd AV, Meagher AP, O’Connor TW, Ward RL (2003) Inactivation of p16INK4a by CpG hypermethylation is not a frequent event in colorectal cancer. J Surg Oncol 84:143–150

    Article  PubMed  CAS  Google Scholar 

  • O’Doherty AM, Church SW, Russell SE, Nelson J, Hickey I (2002) Methylation status of oestrogen receptor-alpha gene promoter sequences in human ovarian epithelial cell lines. Br J Cancer 86:282–284

    Article  PubMed  CAS  Google Scholar 

  • Oliveira Ferreira F, Napoli Ferreira CC, Rossi BM, Toshihiko Nakagawa W, Aguilar S Jr, Monteiro Santos EM, Vierira Costa ML, Lopes A (2004) Frequency of extra-colonic tumors in hereditary nonpolyposis colorectal cancer (HNPCC) and familial colorectal cancer (FCC) Brazilian families: an analysis by a Brazilian Hereditary Colorectal Cancer Institutional Registry. Fam Cancer 3:41–47

    Article  PubMed  Google Scholar 

  • Paech K, Webb P, Kuiper GG, Nilsson S, Gustafsson J, Kushner PJ, Scanlan TS (1997) Differential ligand activation of estrogen receptors ERalpha and ERbeta at AP1 sites. Science 277:1508–1510

    Article  PubMed  CAS  Google Scholar 

  • Parrella P, Poeta ML, Gallo AP, Prencipe M, Scintu M, Apicella A, Rossiello R, Liguoro G, Seripa D, Gravina C, Rabitti C, Rinaldi M, Nicol T, Tommasi S, Paradiso A, Schittulli F, Altomare V, Fazio VM (2004) Nonrandom distribution of aberrant promoter methylation of cancer-related genes in sporadic breast tumors. Clin Cancer Res 10:5349–5354

    Article  PubMed  CAS  Google Scholar 

  • Paz MF, Fraga MF, Avila S, Guo M, Pollan M, Herman JG, Esteller M (2003) Asystematic profile of DNA methylation in human cancer cell lines. Cancer Res 63:1114–1121

    PubMed  CAS  Google Scholar 

  • Pellise M, Castells A, Gines A, Agrelo R, Sole M, Castellvi-Bel S, Fernandez-Esparrach G, Llach J, Esteller M, Bordas JM, Pique JM (2004) Detection of lymph node micrometastases by gene promoter hypermethylation in samples obtained by endosonography-guided fine-needle aspiration biopsy. Clin Cancer Res 10:4444–4449

    Article  PubMed  CAS  Google Scholar 

  • Pfeifer GP, Yoon JH, Liu L, Tommasi S, Wilczynski SP, Dammann R (2002) Methylation of the RASSF1A gene in human cancers. Biol Chem 383:907–914

    Article  PubMed  CAS  Google Scholar 

  • Pijnenborg JM, Kisters N, van Engeland M, Dunselman GA, de Haan J, de Goeij AF, Groothuis PG (2004) APC, beta-catenin, and E-cadherin and the development of recurrent endometrial carcinoma. Int J Gynecol Cancer 14:947–956

    Article  PubMed  CAS  Google Scholar 

  • Pike MC, Pearce CL, Wu AH (2004) Prevention of cancers of the breast, endometrium and ovary. Oncogene 23:6379–6391

    Article  PubMed  CAS  Google Scholar 

  • Pomare EW, Heaton KW (1973) The effect of cholecystectomy on bile salt metabolism. Gut 14:753–762

    PubMed  CAS  Google Scholar 

  • Rajagopalan H, Bardelli A, Lengauer C, Kinzler KW, Vogelstein B, Velculescu VE (2002) Tumorigenesis: RAF/RAS oncogenes and mismatch-repair status. Nature 418:934

    Article  PubMed  CAS  Google Scholar 

  • Rathi A, Virmani AK, Schorge JO, Elias KJ, Maruyama R, Minna JD, Mok SC, Girard L, Fishman DA, Gazdar AF (2002) Methylation profiles of sporadic ovarian tumors and nonmalignant ovaries from high-risk women. Clin Cancer Res 8:3324–3331

    PubMed  CAS  Google Scholar 

  • Reddy BS, Wynder EL (1977) Metabolic epidemiology of colon cancer. Fecal bile acids and neutral sterols in colon cancer patients and patients with adenomatous polyps. Cancer 39:2533–2539

    Article  PubMed  CAS  Google Scholar 

  • Reddy BS, Narasawa T, Weisburger JH, Wynder EL (1976) Promoting effect of sodium deoxycholate on colon adenocarcinomas in germfree rats. J Natl Cancer Inst 56:441–442

    PubMed  CAS  Google Scholar 

  • Risinger JI, Berchuck A, Kohler MF, Watson P, Lynch HT, Boyd J (1993) Genetic instability of microsatellites in endometrial carcinoma. Cancer Res 53:5100–5103

    PubMed  CAS  Google Scholar 

  • Sasaki M, Dharia A, Oh BR, Tanaka Y, Fujimoto S, Dahiya R (2001a) Progesterone receptor B gene inactivation and CpG hypermethylation in human uterine endometrial cancer. Cancer Res 61:97–102

    PubMed  CAS  Google Scholar 

  • Sasaki M, Kotcherguina L, Dharia A, Fujimoto S, Dahiya R (2001b) Cytosinephosphoguanine methylation of estrogen receptors in endometrial cancer. Cancer Res 61:3262–3266

    PubMed  CAS  Google Scholar 

  • Schneider-Stock R, Boltze C, Peters B, Hopfner T, Meyer F, Lippert H, Roessner A (2003) Differences in loss of p16INK4 protein expression by promoter methylation between left-and right-sided primary colorectal carcinomas. Int J Oncol 23:1009–1013

    PubMed  CAS  Google Scholar 

  • Sharma S, Stolina M, Yang SC, Baratelli F, Lin JF, Atianzar K, Luo J, Zhu L, Lin Y, Huang M, Dohadwala M, Batra RK, Dubinett SM (2003) Tumor cyclooxygenase 2-dependent suppression of dendritic cell function. Clin Cancer Res 9:961–968

    PubMed  CAS  Google Scholar 

  • Shen L, Kondo Y, Hamilton SR, Rashid A, Issa JP (2003) P14 methylation in human colon cancer is associated with microsatellite instability and wild-type p53. Gastroenterology 124:626–633

    Article  PubMed  CAS  Google Scholar 

  • Silva J, Dominguez G, Silva JM, Garcia JM, Gallego I, Corbacho C, Provencio M, Espana P, Bonilla F (2001) Analysis of genetic and epigenetic processes that influence p14ARF expression in breast cancer. Oncogene 20:4586–4590

    Article  PubMed  CAS  Google Scholar 

  • Silva J, Silva JM, Dominguez G, Garcia JM, Cantos B, Rodriguez R, Larrondo FJ, Provencio M, Espana P, Bonilla F (2003) Concomitant expression of p16INK4a and p14ARF in primary breast cancer and analysis of inactivation mechanisms. J Pathol 199:289–297

    Article  PubMed  CAS  Google Scholar 

  • Slattery ML, Anderson K, Samowitz W, Edwards SL, Curtin K, Caan B, Potter JD (1999) Hormone replacement therapy and improved survival among postmenopausal women diagnosed with colon cancer (USA). Cancer Causes Control 10:467–473

    Article  PubMed  CAS  Google Scholar 

  • Soslow RA, Dannenberg AJ, Rush D, Woerner BM, Khan KN, Masferrer J, Koki AT (2000) COX-2 is expressed in human pulmonary, colonic, and mammary tumors. Cancer 89:2637–2645

    Article  PubMed  CAS  Google Scholar 

  • Strathdee G, MacKean MJ, Illand M, Brown R (1999) A role for methylation of the hMLH1 promoter in loss of hMLH1 expression and drug resistance in ovarian cancer. Oncogene 18:2335–2341

    Article  PubMed  CAS  Google Scholar 

  • Strathdee G, Appleton K, Illand M, Millan DW, Sargent J, Paul J, Brown R (2001) Primary ovarian carcinomas display multiple methylator phenotypes involving known tumor suppressor genes. Am J Pathol 158:1121–1127

    PubMed  CAS  Google Scholar 

  • Strathdee G, Davies BR, Vass JK, Siddiqui N, Brown R (2004) Cell type-specific methylation of an intronic CpG island controls expression of the MCJ gene. Carcinogenesis 25:693–701

    Article  PubMed  CAS  Google Scholar 

  • Tamaru H, Selker EU (2001) A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414:277–283

    Article  PubMed  CAS  Google Scholar 

  • Todoroki I, Friedman GD, Slattery ML, Potter JD, Samowitz W (1999) Cholecystectomy and the risk of colon cancer. Am J Gastroenterol 94:41–46

    Article  PubMed  CAS  Google Scholar 

  • Toyota M, Ahuja N, Ohe-Toyota M, Herman JG, Baylin SB, Issa JP (1999) CpG island methylator phenotype in colorectal cancer. ProcNatl Acad Sci U S A 96:8681–8686

    Article  CAS  Google Scholar 

  • Toyota M, Ohe-Toyota M, Ahuja N, Issa JP (2000a) Distinct genetic profiles in colorectal tumors with or without the CpG island methylator phenotype. Proc Natl Acad Sci U S A 97:710–715

    Article  PubMed  CAS  Google Scholar 

  • Toyota M, Shen L, Ohe-Toyota M, Hamilton SR, Sinicrope FA, Issa JP (2000b) Aberrant methylation of the Cyclooxygenase 2 CpG island in colorectal tumors. Cancer Res 60:4044–4048

    PubMed  CAS  Google Scholar 

  • Turunen MJ, Kivilaakso EO (1981) Increased risk of colorectal cancer after cholecystectomy. Ann Surg 194:639–641

    PubMed  CAS  Google Scholar 

  • Vegeto E, Shahbaz MM, Wen DX, Goldman ME, O’Malley BW, McDonnell DP (1993) Human progesterone receptor A form is a cell-and promoter-specific repressor of human progesterone receptor B function. Mol Endocrinol 7:1244–1255

    Article  PubMed  CAS  Google Scholar 

  • Velicescu M, Weisenberger DJ, Gonzales FA, Tsai YC, Nguyen CT, Jones PA (2002) Cell division is required for de novo methylation of CpG islands in bladder cancer cells. Cancer Res 62:2378–2384

    PubMed  CAS  Google Scholar 

  • Vernick LJ, Kuller LH, Lohsoonthorn P, Rycheck RR, Redmond CK (1980) Relationship between cholecystectomy and ascending colon cancer. Cancer 45:392–395

    Article  PubMed  CAS  Google Scholar 

  • Vos MD, Ellis CA, Bell A, Birrer MJ, Clark GJ (2000) Ras uses the novel tumor suppressor RASSF1 as an effector to mediate apoptosis. J Biol Chem 275:35669–35672

    Article  PubMed  CAS  Google Scholar 

  • Wang C, Horiuchi A, Imai T, Ohira S, Itoh K, Nikaido T, Katsuyama Y, Konishi I (2004) Expression of BRCA1 protein in benign, borderline, and malignant epithelial ovarian neoplasms and its relationship to methylation and allelic loss of the BRCA1 gene. J Pathol 202:215–223

    Article  PubMed  CAS  Google Scholar 

  • Watson P, Lynch HT (1993) Extracolonic cancer in hereditary nonpolyposis colorectal cancer. Cancer 71:677–685

    Article  PubMed  CAS  Google Scholar 

  • Welcsh PL, King MC (2001) BRCA1 and BRCA2 and the genetics of breast and ovarian cancer. Hum Mol Genet 10:705–713

    Article  PubMed  CAS  Google Scholar 

  • Whitcomb BP, Mutch DG, Herzog TJ, Rader JS, Gibb RK, Goodfellow PJ (2003) Frequent HOXA11 and THBS2 promoter methylation, and a methylator phenotype in endometrial adenocarcinoma. Clin Cancer Res 9:2277–2287

    PubMed  CAS  Google Scholar 

  • Widschwendter M, Jones PA (2002) DNA methylation and breast carcinogenesis. Oncogene 21:5462–5482

    Article  PubMed  CAS  Google Scholar 

  • Widschwendter M, Siegmund KD, Muller HM, Fiegl H, Marth C, Muller-Holzner E, Jones PA, Laird PW (2004) Association of breast cancer DNA methylation profiles with hormone receptor status and response to tamoxifen. Cancer Res 64:3807–3813

    Article  PubMed  CAS  Google Scholar 

  • Wiencke JK, Zheng S, Lafuente A, Lafuente MJ, Grudzen C, Wrensch MR, Miike R, Ballesta A, Trias M (1999) Aberrant methylation of p16INK4a in anatomic and gender-specific subtypes of sporadic colorectal cancer. Cancer Epidemiol Biomarkers Prev 8:501–506

    PubMed  CAS  Google Scholar 

  • Wingo PA, Ries LA, Rosenberg HM, Miller DS, Edwards BK (1998) Cancer incidence and mortality, 1973–1995: a report card for the U.S. Cancer 82:1197–1207

    Article  PubMed  CAS  Google Scholar 

  • Wong YF, Chung TK, Cheung TH, Nobori T, Yu AL, Yu J, Batova A, Lai KW, Chang AM (1999) Methylation of p16INK4A in primary gynecologic malignancy. Cancer Lett 136:231–235

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto H, Min Y, Itoh F, Imsumran A, Horiuchi S, Yoshida M, Iku S, Fukushima H, Imai K (2002) Differential involvement of the hypermethylator phenotype in hereditary and sporadic colorectal cancers with high-frequency microsatellite instability. Genes Chromosomes Cancer 33:322–325

    Article  PubMed  CAS  Google Scholar 

  • Yoon JH, Dammann R, Pfeifer GP (2001) Hypermethylation of the CpG island of the RASSF1A gene in ovarian and renal cell carcinomas. Int J Cancer 94:212–217

    Article  PubMed  CAS  Google Scholar 

  • Yoshiura K, Kanai Y, Ochiai A, Shimoyama Y, Sugimura T, Hirohashi S (1995) Silencing of the E-cadherin invasion-suppressor gene by CpG methylation in human carcinomas. Proc Natl Acad Sci U S A 92:7416–7419

    Article  PubMed  CAS  Google Scholar 

  • Zhao Y, Agarwal VR, Mendelson CR, Simpson ER (1997) Transcriptional regulation of CYP19 gene (aromatase) expression in adipose stromal cells in primary culture. J Steroid Biochem Mol Biol 61:203–210

    Article  PubMed  CAS  Google Scholar 

  • Zhou H, Luo MP, Schonthal AH, Pike MC, Stallcup MR, Blumenthal M, Zheng W, Dubeau L (2002) Effect of reproductive hormones on ovarian epithelial tumors. I. Effect on cell cycle activity. Cancer Biol Ther 1:300–306

    PubMed  CAS  Google Scholar 

  • Zysman M, Saka A, Millar A, Knight J, Chapman W, Bapat B (2002) Methylation of adenomatous polyposis coli in endometrial cancer occurs more frequently in tumors with microsatellite instability phenotype. Cancer Res 62:3663–3666

    PubMed  CAS  Google Scholar 

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  1. Department of Surgery and Department of Biochemistry and Molecular Biology, Keck School of Medicine, USC/Norris Comprehensive Cancer Center, University of Southern California, 1441 Eastlake Avenue, Room 6418, Los Angeles, CA, 90089-9176, USA

    M. Campan, D. J. Weisenberger & P. W. Laird

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  1. M. Campan
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  2. D. J. Weisenberger
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  3. P. W. Laird
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  1. Institut für Genetik, Universität zu Köln, Zülpicher Str. 47, 50674, Köln, Germany

    Walter Doerfler  & Petra Böhm  & 

  2. Institut für Klinische und Molekulare Virologie, Universität Erlangen, Schlossgarten 4, 91054, Erlangen, Germany

    Walter Doerfler

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Campan, M., Weisenberger, D.J., Laird, P.W. (2006). DNA Methylation Profiles of Female Steroid Hormone-Driven Human Malignancies. In: Doerfler, W., Böhm, P. (eds) DNA Methylation: Development, Genetic Disease and Cancer. Current Topics in Microbiology and Immunology, vol 310. Springer, Berlin, Heidelberg . https://doi.org/10.1007/3-540-31181-5_8

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