Environmental estrogens differentially engage the histone methyltransferase EZH2 to increase risk of uterine tumorigenesis

Molecular Cancer Research

Volumn 10, Issue 4, 2012, Pages 546-557

  Greathouse, K Leigh ^a,f   Bredfeldt, Tiffany ^a   Everitt, Jeffrey I ^b   Lin, Kevin ^a   Berry, Tia ^a,d   Kannan, Kurunthachalam ^c   Mittelstadt, Megan L ^d   Ho, Shuk Mei ^e   Walker, Cheryl L ^a,d  

^a UNIVERSITY OF TEXAS   (United States)

^b GLAXOSMITHKLINE   (United States)

^c STATE UNIVERSITY OF NEW YORK   (United States)

^d UNIVERSITY OF TEXAS   (United States)

^e UNIVERSITY OF CINCINNATI MEDICAL CENTER   (United States)

^f NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ESTROGEN; ESTROGEN RECEPTOR; GENISTEIN; HISTONE METHYLTRANSFERASE; HISTONE METHYLTRANSFERASE ENHANCER OF ZESTE HOMOLOG 2; PHOSPHATIDYLINOSITOL 3 KINASE; PHYTOESTROGEN; PROTEIN KINASE B; UNCLASSIFIED DRUG; XENOESTROGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INCIDENCE; CANCER RISK; CARCINOGENESIS; CHROMATIN; CONTROLLED STUDY; CORRELATION ANALYSIS; ENVIRONMENTAL EXPOSURE; ENZYME PHOSPHORYLATION; EPIGENETICS; FEMALE; GENE EXPRESSION; GENOME; MYOMETRIUM; NONHUMAN; PRIORITY JOURNAL; RAT; RISK ASSESSMENT; UTERUS MYOMA;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; DNA-BINDING PROTEINS; ESTROGENS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENISTEIN; HISTONE-LYSINE N-METHYLTRANSFERASE; HUMANS; IMMUNOHISTOCHEMISTRY; RATS; RISK FACTORS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; UTERINE NEOPLASMS;

EID: 84859850513     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-11-0605     Document Type: Article

References (52)

1. Kyung-Chul C, Eui-Bae J, Leung PCK. Impact of environmental endocrine disruption on the reproductive system for human health. Immunol Endocrine Metab Agents Med Chem 2006;6:3-13. (Pubitemid 43796742)
2. Newbold RR, Banks EP, Bullock B, Jefferson WN. Uterine adenocarcinoma in mice treated neonatally with genistein. Cancer Res 2001;61: 4325-8. (Pubitemid 32685752)
3. Palmer JR, Wise LA, Hatch EE, Troisi R, Titus-Ernstoff L, Strohsnitter W, et al. Prenatal diethylstilbestrol exposure and risk of breast cancer. Cancer Epidemiol Biomarkers Prev 2006;15:1509-14. (Pubitemid 44299324)
4. Camp EA, Coker AL, Robboy SJ, Noller KL, Goodman KJ, Titus-Ernstoff LT, et al. Breast cancer screening in women exposed in utero to diethylstilbestrol. J Womens Health (Larchmt) 2009;18:547-52.
5. D'Aloisio AA, Baird DD, DeRoo LA, Sandler DP. Association of intrauterine and early-life exposures with diagnosis of uterine leiomyomata by 35 years of age in the Sister Study. Environ Health Perspect 2010;118:375-81.
6. Wise LA, Palmer JR, Rowlings K, Kaufman RH, Herbst AL, Noller KL, et al. Risk of benign gynecologic tumors in relation to prenatal diethylstilbestrol exposure. Obstet Gynecol 2005;105:167-73. (Pubitemid 40189928)
7. Newbold RR, Jefferson WN, Padilla-Banks E. Long-term adverse effects of neonatal exposure to bisphenol A on the murine female reproductive tract. Reprod Toxicol 2007;24:253-8. (Pubitemid 47393609)
8. Howdeshell KL, Hotchkiss AK, Thayer KA, Vandenbergh JG, vom Saal FS. Exposure to bisphenol A advances puberty. Nature 1999;401: 763-4. (Pubitemid 129515829)
9. Schonfelder G, Friedrich K, Paul M, Chahoud I. Developmental effects of prenatal exposure to bisphenol A on the uterus of rat offspring. Neoplasia 2004;6:584.
10. Kato H, Ota T, Furuhashi T, Ohta Y, Iguchi T. Changes in reproductive organs of female rats treated with bisphenol A during the neonatal period. Reprod Toxicol 2003;17:283.
11. Nikaido Y, Danbara N, Tsujita-Kyutoku M, Yuri T, Uehara N, Tsubura A. Effects of prepubertal exposure to xenoestrogen on development of estrogen target organs in female CD-1 mice. In Vivo 2005;19: 487-94. (Pubitemid 40568125)
12. Prins GS, Tang WY, Belmonte J, Ho SM. Developmental exposure to bisphenol A increases prostate cancer susceptibility in adult rats: epigenetic mode of action is implicated. Fertil Steril 2008; 89:e41. (Pubitemid 351749388)
13. Setchell KD, Zimmer-Nechemias L, Cai J, Heubi JE. Isoflavone content of infant formulas and the metabolic fate of these phytoestrogens in early life. Am J Clin Nutr 1998;68:1453S-61S. (Pubitemid 28550929)
14. Walker CL, Stewart EA. Uterine fibroids: the elephant in the room. Science 2005;308:1589-92. (Pubitemid 40807499)
15. Jefferson WN, Padilla-Banks E, Newbold RR. Disruption of the female reproductive system by the phytoestrogen genistein. Reprod Toxicol 2007;23:308.
16. Cook JD, Davis BJ, Cai SL, Barrett JC, Conti CJ, Walker CL. Interaction between genetic susceptibility and early-life environmental exposure determines tumor-suppressor-gene penetrance. Proc Natl Acad Sci U S A 2005;102:8644-9. (Pubitemid 40862789)
17. Walker CL, Hunter D, Everitt JI. Uterine leiomyoma in the Eker rat: a unique model for important diseases of women. Genes Chromosomes Cancer 2003;38:349-56. (Pubitemid 37466936)
18. Cook JD, Davis BJ, Goewey JA, Berry TD, Walker CL. Identification of a sensitive period for developmental programming that increases risk for uterine leiomyoma in Eker rats. Reprod Sci 2007;14:121-36. (Pubitemid 351168831)
19. Greathouse KL, Cook JD, Lin K, Davis BJ, Berry TD, Bredfeldt TG, et al. Identification of uterine leiomyoma genes developmentally reprogrammed by neonatal exposure to diethylstilbestrol. Reprod Sci 2008;15:765-78.
20. Couse JF, Korach KS. Estrogen receptor-alpha mediates the detrimental effects of neonatal diethylstilbestrol (DES) exposure in the murine reproductive tract. Toxicology 2004;205:55-63. (Pubitemid 39359151)
21. Glidewell-Kenney C, Hurley LA, Pfaff L, Weiss J, Levine JE, Jameson JL. Nonclassical estrogen receptor alpha signaling mediates negative feedback in the female mouse reproductive axis. Proc Natl Acad Sci U S A 2007;104:8173-7. (Pubitemid 47185894)
22. Chen JR, Plotkin LI, Aguirre JI, Han L, Jilka RL, Kousteni S, et al. Transient versus sustained phosphorylation and nuclear accumulation of ERKs underlie anti-versus pro-apoptotic effects of estrogens. J Biol Chem 2005;280:4632-8. (Pubitemid 40288632)
23. Kousteni S, Chen JR, Bellido T, Han L, Ali AA, O'Brien CA, et al. Reversal of bone loss in mice by nongenotropic signaling of sex steroids. Science 2002;298:843-6. (Pubitemid 35231540)
24. Chen Z, Yuhanna IS, Galcheva-Gargova Z, Karas RH, Mendelsohn ME, Shaul PW. Estrogen receptor alpha mediates the nongenomic activation of endothelial nitric oxide synthase by estrogen. J Clin Invest 1999;103:401-6. (Pubitemid 29069990)
25. Watson CS, Bulayeva NN, Wozniak AL, Alyea RA. Xenoestrogens are potent activators of nongenomic estrogenic responses. Steroids 2007;72:124-34. (Pubitemid 46273492)
26. Li X, Zhang S, Safe S. Activation of kinase pathways in MCF-7 cells by 17[beta]-estradiol and structurally diverse estrogenic compounds. J Steroid Biochem Mol Biol 2006;98:122-32. (Pubitemid 43153783)
27. Bredfeldt TG, Greathouse KL, Safe SH, Hung MC, Bedford MT, Walker CL. Xenoestrogen-induced regulation of EZH2 and histone methylation via estrogen receptor signaling to PI3K/AKT. Mol Endocrinol 2010;24:993-1006.
28. Prins GS, Ye SH, Birch L, Ho SM, Kannan K. Serum bisphenol A pharmacokinetics and prostate neoplastic responses following oral and subcutaneous exposures in neonatal Sprague-Dawley rats. Reprod Toxicol 2011;31:1-9.
29. Hugo ER, Brandebourg TD, Woo JG, Loftus J, Alexander JW, Ben-Jonathan N. Bisphenol A at environmentally relevant doses inhibits adiponectin release from human adipose tissue explants and adipocytes. Environ Health Perspect 2008;116:1642-7.
30. Ho SM, Tang WY, Belmonte de Frausto J, Prins GS. Developmental exposure to estradiol and bisphenol A increases susceptibility to prostate carcinogenesis and epigenetically regulates phosphodiesterase type 4 variant 4. Cancer Res 2006;66:5624-32. (Pubitemid 43927114)
31. Cha TL, Zhou BP, Xia W,Wu Y, Yang CC, Chen CT, et al. Akt-mediated phosphorylation of EZH2 suppresses methylation of lysine 27 in histone H3. Science 2005;310:306-10. (Pubitemid 41457195)
32. Burroughs CD, Mills KT, Bern HA. Long-term genital tract changes in female mice treated neonatally with coumestrol. Reprod Toxicol 1990;4:127-35.
33. Katsuda S, Yoshida M, Watanabe G, Taya K, Maekawa A. Irreversible effects of neonatal exposure to p-tert-octylphenol on the reproductive tract in female rats. Toxicol Appl Pharmacol 2000;165:217-26. (Pubitemid 30429905)
34. Walker CL, Cesen-Cummings K, Houle C, Baird D, Barrett JC, Davis B. Protective effect of pregnancy for development of uterine leiomyoma. Carcinogenesis 2001;22:2049-52. (Pubitemid 34065402)
35. Routledge EJ, White R, Parker MG, Sumpter JP. Differential effects of xenoestrogens on coactivator recruitment by estrogen receptor (ER) alpha and ERbeta. J Biol Chem 2000;275:35986-93.
36. Bouskine A, Nebout M, Brucker-Davis F, Benahmed M, Fenichel P. Low doses of bisphenol A promote human seminoma cell proliferation by activating PKA and PKG via a membrane G-protein-coupled estrogen receptor. Environ Health Perspect 2009;117: 1053-8.
37. Prins GS, Birch L, Couse JF, Choi I, Katzenellenbogen B, Korach KS. Estrogen imprinting of the developing prostate gland is mediated through stromal estrogen receptor alpha: studies with alphaERKO and betaERKO mice. Cancer Res 2001;61:6089-97. (Pubitemid 32762544)
38. Mowa CN, Iwanaga T. Developmental changes of the oestrogen receptor-alpha and -beta mRNAs in the female reproductive organ of the rat-an analysis by in situ hybridization. J Endocrinol 2000;167: 363-9. (Pubitemid 32047543)
39. Sarraf SA, Stancheva I. Methyl-CpG binding protein MBD1 couples histone H3 methylation at lysine 9 by SETDB1 to DNA replication and chromatin assembly. Mol Cell 2004;15:595-605. (Pubitemid 39141786)
40. Fuks F, Hurd PJ, Wolf D, Nan X, Bird AP, Kouzarides T. The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J Biol Chem 2003;278:4035-40. (Pubitemid 36801137)
41. Esteve PO. Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication. Genes Dev 2006;20: 3089-103.
42. Plath K, Fang J, Mlynarczyk-Evans SK, Cao R, Worringer KA, Wang H, et al. Role of histone H3 lysine 27 methylation in X inactivation. Science 2003;300:131-5. (Pubitemid 36423045)
43. Muller J, Hart CM, Francis NJ, Vargas ML, Sengupta A, Wild B, et al. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 2002;111:197-208. (Pubitemid 35292440)
44. Leu YW, Yan PS, Fan M, Jin VX, Liu JC, Curran EM, et al. Loss of estrogen receptor signaling triggers epigenetic silencing of downstream targets in breast cancer. Cancer Res 2004;64: 8184-92. (Pubitemid 39491754)
45. Li S, Washburn KA, Moore R, Uno T, Teng C, Newbold RR, et al. Developmental exposure to diethylstilbestrol elicits demethylation of estrogen-responsive lactoferrin gene in mouse uterus. Cancer Res 1997;57:4356-9. (Pubitemid 27413446)
46. Kim MS, Kondo T, Takada I, Youn MY, Yamamoto Y, Takahashi S, et al. DNA demethylation in hormone-induced transcriptional derepression. Nature 2009;461:1007-12.
47. Dolinoy DC, Huang D, Jirtle RL. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc Natl Acad Sci U S A 2007;104:13056-61. (Pubitemid 351737592)
48. Rubin BS, Murray MK, Damassa DA, King JC, Soto AM. Perinatal Exposure to Low Doses of Bisphenol A Affects Body Weight, Patterns of Estrous Cyclicity, and Plasma LH Levels. Environ Health Perspect 2001;109:675.
49. Newbold RR, Jefferson WN, Padilla-Banks E. Prenatal exposure to bisphenol a at environmentally relevant doses adversely affects the murine female reproductive tract Later in life. Environ Health Perspect 2009;117:879-85.
50. Faber KA, Hughes CL Jr. Dose-response characteristics of neonatal exposure to genistein on pituitary responsiveness to gonadotropin releasing hormone and volume of the sexually dimorphic nucleus of the preoptic area (SDN-POA) in postpubertal castrated female rats. Reprod Toxicol 1993;7:35-9.
51. Fernandez M, Bianchi M, Lux-Lantos V, Libertun C. Neonatal exposure to bisphenol a alters reproductive parameters and gonadotropin releasing hormone signaling in female rats. Environ Health Perspect 2009;117:757-62.
52. Adachi T, Ono Y, Koh K-B, Takashima K, Tainaka H, Matsuno Y, et al. Long-term alteration of gene expression without morphological change in testis after neonatal exposure to genistein in mice: toxicogenomic analysis using cDNA microarray. Food Chem Toxicol 2004; 42:445.