Advertisement

DNA Methylation Profiles of Female Steroid Hormone-Driven Human Malignancies

  • M. Campan
  • D. J. Weisenberger
  • P. W. LairdEmail author
Chapter
Part of the Current Topics in Microbiology and Immunology book series (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.

Keywords

Endometrial Cancer Promoter Hypermethylation Sporadic Breast Cancer Female Steroid Proximal Colon Cancer 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 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 107:580–582PubMedCrossRefGoogle Scholar
  2. 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 20:1509–1518PubMedCrossRefGoogle Scholar
  3. 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 93:807–815PubMedGoogle Scholar
  4. Alley PG, McNee RK (1986) Age and sex differences in right colon cancer. Dis Colon Rectum 29:227–229PubMedGoogle Scholar
  5. 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 13:1558–1568PubMedGoogle Scholar
  6. 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 10:5998–6005PubMedCrossRefGoogle Scholar
  7. 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 60:5329–5333PubMedGoogle Scholar
  8. 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 262:2750–2756PubMedGoogle Scholar
  9. 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 64:5861–5869PubMedCrossRefGoogle Scholar
  10. Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16:6–21PubMedCrossRefGoogle Scholar
  11. 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 74:664–669PubMedCrossRefGoogle Scholar
  12. 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 81:217–229PubMedGoogle Scholar
  13. 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 56:714–716PubMedCrossRefGoogle Scholar
  14. 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 18:1957–1965PubMedCrossRefGoogle Scholar
  15. 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 100:913–919PubMedCrossRefGoogle Scholar
  16. Clarke CL, Sutherland RL (1990) Progestin regulation of cellular proliferation. Endocr Rev 11:266–301PubMedCrossRefGoogle Scholar
  17. Claus EB, Schildkraut JM, Thompson WD, Risch NJ (1996) The genetic attributable risk of breast and ovarian cancer. Cancer 77:2318–2324PubMedCrossRefGoogle Scholar
  18. Cohen CJ, Rahaman J (1995) Endometrial cancer. Management of high risk and recurrence including the tamoxifen controversy. Cancer 76:2044–2052PubMedCrossRefGoogle Scholar
  19. Coles B, Ketterer B (1990) The role of glutathione and glutathione transferases in chemical carcinogenesis. Crit Rev Biochem Mol Biol 25:47–70PubMedGoogle Scholar
  20. Conneely OM, Mulac-Jericevic B, Lydon JP (2003) Progesterone-dependent regulation of female reproductive activity by two distinct progesterone receptor isoforms. Steroids 68:771–778PubMedCrossRefGoogle Scholar
  21. 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 24:132–138PubMedCrossRefGoogle Scholar
  22. Cowley SM, Parker MG (1999) A comparison of transcriptional activation by ER alpha and ER beta. J Steroid Biochem Mol Biol 69:165–175PubMedCrossRefGoogle Scholar
  23. 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–1212SPubMedGoogle Scholar
  24. 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 61:3105–3109PubMedGoogle Scholar
  25. 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 43:587–590PubMedGoogle Scholar
  26. 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 63:1148–1149Google Scholar
  27. 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 530:9–17PubMedGoogle Scholar
  28. 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 59:2302–2306PubMedGoogle Scholar
  29. 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 61:3410–3418PubMedGoogle Scholar
  30. Eden S, Cedar H (1994) Role of DNA methylation in the regulation of transcription. Curr Opin Genet Dev 4:255–259PubMedCrossRefGoogle Scholar
  31. Egger G, Liang G, Aparicio A, Jones PA (2004) Epigenetics in human disease and prospects for epigenetic therapy. Nature 429:457–463PubMedCrossRefGoogle Scholar
  32. 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
  33. Esteller M(2000) Epigenetic lesions causing genetic lesions in human cancer: promoter hypermethylation of DNA repair genes. Eur J Cancer 36:2294–2300Google Scholar
  34. 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 58:4515–4518PubMedGoogle Scholar
  35. 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 17:2413–2417PubMedCrossRefGoogle Scholar
  36. 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 59:793–797PubMedGoogle Scholar
  37. 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 92:564–569PubMedCrossRefGoogle Scholar
  38. 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 60:2368–2371PubMedGoogle Scholar
  39. Esteller M, Corn PG, Baylin SB, Herman JG (2001a) A gene hypermethylation profile of human cancer. Cancer Res 61:3225–3229PubMedGoogle Scholar
  40. 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 10:3001–3007PubMedCrossRefGoogle Scholar
  41. 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 87:237–246PubMedCrossRefGoogle Scholar
  42. 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 284:1354–1356PubMedCrossRefGoogle Scholar
  43. Fazzari MJ, Greally JM (2004) Epigenomics: beyond CpG islands. Nat Rev Genet 5:446–455PubMedCrossRefGoogle Scholar
  44. Feltus FA, Lee EK, Costello JF, Plass C, Vertino PM (2003) Predicting aberrant CpG island methylation. Proc Natl Acad Sci U S A 100:12253–12258PubMedCrossRefGoogle Scholar
  45. 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 33:451–457PubMedCrossRefGoogle Scholar
  46. 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 36:97–102PubMedGoogle Scholar
  47. Furner SE, Davis FG, Nelson RL, Haenszel W (1989) A case-control study of large bowel cancer and hormone exposure in women. Cancer Res 49:4936–4940PubMedGoogle Scholar
  48. 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 156:1997–2005PubMedGoogle Scholar
  49. 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 198:442–449PubMedCrossRefGoogle Scholar
  50. 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 347:1066–1071PubMedCrossRefGoogle Scholar
  51. Hilakivi-Clarke L (2000) Estrogens, BRCA1, and breast cancer. Cancer Res 60:4993–5001PubMedGoogle Scholar
  52. Hla T, Neilson K (1992) Human cyclooxygenase-2 cDNA. Proc Natl Acad Sci U S A 89:7384–7388PubMedCrossRefGoogle Scholar
  53. Ho SM (2003) Estrogen, progesterone and epithelial ovarian cancer. Reprod Biol Endocrinol 1:73PubMedCrossRefGoogle Scholar
  54. 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 157:5512–5520PubMedGoogle Scholar
  55. Huang TH, Perry MR, Laux DE (1999) Methylation profiling of CpG islands in human breast cancer cells. Hum Mol Genet 8:459–470PubMedCrossRefGoogle Scholar
  56. Iacopetta B (2003) Aberrant DNA methylation: have we entered the era of more than one type of colorectal cancer? Am J Pathol 162:1043–1045PubMedGoogle Scholar
  57. 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 64:6476–6481PubMedCrossRefGoogle Scholar
  58. Issa JP (2000) CpG-island methylation in aging and cancer. Curr Top Microbiol Immunol 249:101–118PubMedGoogle Scholar
  59. 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 7:536–540PubMedCrossRefGoogle Scholar
  60. Jhaveri MS, Morrow CS (1998) Methylation-mediated regulation of the glutathione S-transferase P1 gene in human breast cancer cells. Gene 210:1–7PubMedCrossRefGoogle Scholar
  61. 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 85:69–73PubMedCrossRefGoogle Scholar
  62. 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 57:808–811PubMedGoogle Scholar
  63. 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 9:1603–1614PubMedGoogle Scholar
  64. 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 55:5556–5560PubMedGoogle Scholar
  65. Kelsey JL, Bernstein L (1996) Epidemiology and prevention of breast cancer. Annu Rev Public Health 17:47–67PubMedCrossRefGoogle Scholar
  66. Kinyamu HK, Archer TK (2004) Modifying chromatin to permit steroid hormone receptor-dependent transcription. Biochim Biophys Acta 1677:30–45PubMedGoogle Scholar
  67. Kondo Y, Issa JP (2004) Epigenetic changes in colorectal cancer. Cancer Metastasis Rev 23:29–39PubMedCrossRefGoogle Scholar
  68. 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 10:28–32PubMedCrossRefGoogle Scholar
  69. Laghi L, Bianchi P, Malesci A (2003) Gender difference for promoter methylation pattern of hMLH1 and p16 in sporadic MSI colorectal cancer. Gastroenterology 124:1165–1166PubMedGoogle Scholar
  70. Laird PW (2003) The power and the promise of DNA methylation markers. Nat Rev Cancer 3:253–266PubMedCrossRefGoogle Scholar
  71. 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 2:805–810PubMedGoogle Scholar
  72. Lazennec G, Bresson D, Lucas A, Chauveau C, Vignon F (2001) ER beta inhibits proliferation and invasion of breast cancer cells. Endocrinology 142:4120–4130PubMedCrossRefGoogle Scholar
  73. 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 69–75Google Scholar
  74. Lee S, Hwang KS, Lee HJ, Kim JS, Kang GH (2004) Aberrant CpG island hypermethylation of multiple genes in colorectal neoplasia. Lab Invest 84:884–893PubMedCrossRefGoogle Scholar
  75. 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 160:605–612PubMedGoogle Scholar
  76. 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 64:8184–8192PubMedCrossRefGoogle Scholar
  77. Li CI, Daling JR, Malone KE (2003) Incidence of invasive breast cancer by hormone receptor status from 1992 to 1998. J Clin Oncol 21:28–34PubMedCrossRefGoogle Scholar
  78. 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 3:28PubMedCrossRefGoogle Scholar
  79. 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 54:4590–4594PubMedGoogle Scholar
  80. Malagelada JR, Go VL, Summerskill WH, Gamble WS (1973) Bile acid secretion and biliary bile acid composition altered by cholecystectomy. Am J Dig Dis 18:455–459PubMedCrossRefGoogle Scholar
  81. Malaney S, Daly RJ (2001) The ras signaling pathway in mammary tumorigenesis and metastasis. J Mammary Gland Biol Neoplasia 6:101–113PubMedCrossRefGoogle Scholar
  82. 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 119:598PubMedGoogle Scholar
  83. 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 14:979–984PubMedCrossRefGoogle Scholar
  84. 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 61:5875–5884PubMedGoogle Scholar
  85. 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 14:115–121PubMedCrossRefGoogle Scholar
  86. Marra G, Boland CR (1996) DNA repair and colorectal cancer. Gastroenterol Clin North Am 25:755–772PubMedCrossRefGoogle Scholar
  87. 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 32:569–577PubMedCrossRefGoogle Scholar
  88. 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 72:87–92PubMedCrossRefGoogle Scholar
  89. McMichael AJ, Potter JD (1980) Reproduction, endogenous and exogenous sex hormones, and colon cancer: a review and hypothesis. J Natl Cancer Inst 65:1201–1207PubMedGoogle Scholar
  90. 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 3:331–333PubMedGoogle Scholar
  91. 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 121:1300–1309PubMedCrossRefGoogle Scholar
  92. 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 23:2442–2453PubMedCrossRefGoogle Scholar
  93. 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 21:7981–7990PubMedCrossRefGoogle Scholar
  94. 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 199:471–478PubMedCrossRefGoogle Scholar
  95. 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 85:6518–6522PubMedCrossRefGoogle Scholar
  96. 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 21:5696–5703PubMedCrossRefGoogle Scholar
  97. 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 22:4584–4594PubMedCrossRefGoogle Scholar
  98. Narayan S, Roy D (2003) Role of APC and DNA mismatch repair genes in the development of colorectal cancers. Mol Cancer 2:41PubMedCrossRefGoogle Scholar
  99. 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 60:4346–4348PubMedGoogle Scholar
  100. 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 6:4026–4032PubMedGoogle Scholar
  101. Niederacher D, Yan HY, An HX, Bender HG, Beckmann MW (1999) CDKN2A gene inactivation in epithelial sporadic ovarian cancer. Br J Cancer 80:1920–1926PubMedCrossRefGoogle Scholar
  102. 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 81:1535–1565PubMedGoogle Scholar
  103. 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 24:1615–1623PubMedCrossRefGoogle Scholar
  104. 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 33:650–656PubMedGoogle Scholar
  105. 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 84:143–150PubMedCrossRefGoogle Scholar
  106. 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 86:282–284PubMedCrossRefGoogle Scholar
  107. 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 3:41–47PubMedCrossRefGoogle Scholar
  108. 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 277:1508–1510PubMedCrossRefGoogle Scholar
  109. 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 10:5349–5354PubMedCrossRefGoogle Scholar
  110. 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 63:1114–1121PubMedGoogle Scholar
  111. 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 10:4444–4449PubMedCrossRefGoogle Scholar
  112. Pfeifer GP, Yoon JH, Liu L, Tommasi S, Wilczynski SP, Dammann R (2002) Methylation of the RASSF1A gene in human cancers. Biol Chem 383:907–914PubMedCrossRefGoogle Scholar
  113. 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 14:947–956PubMedCrossRefGoogle Scholar
  114. Pike MC, Pearce CL, Wu AH (2004) Prevention of cancers of the breast, endometrium and ovary. Oncogene 23:6379–6391PubMedCrossRefGoogle Scholar
  115. Pomare EW, Heaton KW (1973) The effect of cholecystectomy on bile salt metabolism. Gut 14:753–762PubMedGoogle Scholar
  116. Rajagopalan H, Bardelli A, Lengauer C, Kinzler KW, Vogelstein B, Velculescu VE (2002) Tumorigenesis: RAF/RAS oncogenes and mismatch-repair status. Nature 418:934PubMedCrossRefGoogle Scholar
  117. 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 8:3324–3331PubMedGoogle Scholar
  118. 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 39:2533–2539PubMedCrossRefGoogle Scholar
  119. Reddy BS, Narasawa T, Weisburger JH, Wynder EL (1976) Promoting effect of sodium deoxycholate on colon adenocarcinomas in germfree rats. J Natl Cancer Inst 56:441–442PubMedGoogle Scholar
  120. Risinger JI, Berchuck A, Kohler MF, Watson P, Lynch HT, Boyd J (1993) Genetic instability of microsatellites in endometrial carcinoma. Cancer Res 53:5100–5103PubMedGoogle Scholar
  121. 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 61:97–102PubMedGoogle Scholar
  122. Sasaki M, Kotcherguina L, Dharia A, Fujimoto S, Dahiya R (2001b) Cytosinephosphoguanine methylation of estrogen receptors in endometrial cancer. Cancer Res 61:3262–3266PubMedGoogle Scholar
  123. 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 23:1009–1013PubMedGoogle Scholar
  124. 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 9:961–968PubMedGoogle Scholar
  125. 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 124:626–633PubMedCrossRefGoogle Scholar
  126. 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 20:4586–4590PubMedCrossRefGoogle Scholar
  127. 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 199:289–297PubMedCrossRefGoogle Scholar
  128. 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 10:467–473PubMedCrossRefGoogle Scholar
  129. 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 89:2637–2645PubMedCrossRefGoogle Scholar
  130. 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 18:2335–2341PubMedCrossRefGoogle Scholar
  131. 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 158:1121–1127PubMedGoogle Scholar
  132. 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 25:693–701PubMedCrossRefGoogle Scholar
  133. Tamaru H, Selker EU (2001) A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414:277–283PubMedCrossRefGoogle Scholar
  134. Todoroki I, Friedman GD, Slattery ML, Potter JD, Samowitz W (1999) Cholecystectomy and the risk of colon cancer. Am J Gastroenterol 94:41–46PubMedCrossRefGoogle Scholar
  135. 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 96:8681–8686CrossRefGoogle Scholar
  136. 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 97:710–715PubMedCrossRefGoogle Scholar
  137. 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 60:4044–4048PubMedGoogle Scholar
  138. Turunen MJ, Kivilaakso EO (1981) Increased risk of colorectal cancer after cholecystectomy. Ann Surg 194:639–641PubMedGoogle Scholar
  139. 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 7:1244–1255PubMedCrossRefGoogle Scholar
  140. 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 62:2378–2384PubMedGoogle Scholar
  141. Vernick LJ, Kuller LH, Lohsoonthorn P, Rycheck RR, Redmond CK (1980) Relationship between cholecystectomy and ascending colon cancer. Cancer 45:392–395PubMedCrossRefGoogle Scholar
  142. 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 275:35669–35672PubMedCrossRefGoogle Scholar
  143. 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 202:215–223PubMedCrossRefGoogle Scholar
  144. Watson P, Lynch HT (1993) Extracolonic cancer in hereditary nonpolyposis colorectal cancer. Cancer 71:677–685PubMedCrossRefGoogle Scholar
  145. Welcsh PL, King MC (2001) BRCA1 and BRCA2 and the genetics of breast and ovarian cancer. Hum Mol Genet 10:705–713PubMedCrossRefGoogle Scholar
  146. 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 9:2277–2287PubMedGoogle Scholar
  147. Widschwendter M, Jones PA (2002) DNA methylation and breast carcinogenesis. Oncogene 21:5462–5482PubMedCrossRefGoogle Scholar
  148. 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 64:3807–3813PubMedCrossRefGoogle Scholar
  149. 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 8:501–506PubMedGoogle Scholar
  150. 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 82:1197–1207PubMedCrossRefGoogle Scholar
  151. 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 136:231–235PubMedCrossRefGoogle Scholar
  152. 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 33:322–325PubMedCrossRefGoogle Scholar
  153. 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 94:212–217PubMedCrossRefGoogle Scholar
  154. 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 92:7416–7419PubMedCrossRefGoogle Scholar
  155. 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 61:203–210PubMedCrossRefGoogle Scholar
  156. 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 1:300–306PubMedGoogle Scholar
  157. 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 62:3663–3666PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2006

Authors and Affiliations

  1. 1.Department of Surgery and Department of Biochemistry and Molecular Biology, Keck School of Medicine, USC/Norris Comprehensive Cancer CenterUniversity of Southern CaliforniaLos AngelesUSA

Personalised recommendations