Repeat estradiol exposure differentially regulates protein expression patterns for estrogen receptor and E-cadherin in older mouse ovarian surface epithelium: Implications for replacement and adjuvant hormone therapies?

Steroids

Volumn 77, Issue 6, 2012, Pages 674-685

  Gulliver, Linda S M ^a   Hurst, Peter R ^b  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

E cadherin; Estradiol; Estrogen receptor; Hormone therapies; Older ovary

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; UVOMORULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD LEVEL; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; MESOTHELIUM; MOUSE; NONHUMAN; OVARIAN SURFACE EPITHELIUM; PROTEIN EXPRESSION; TISSUE LEVEL; UTERUS WEIGHT;

ADJUVANTS, PHARMACEUTIC; AGING; ANIMALS; BROMODEOXYURIDINE; CADHERINS; CELL SIZE; EPITHELIUM; ESTRADIOL; FEMALE; GENE EXPRESSION REGULATION; HORMONE REPLACEMENT THERAPY; MICE; ORGAN SIZE; OVARY; PROTEIN TRANSPORT; RECEPTORS, ESTROGEN; TIME FACTORS; UTERUS;

MUS;

EID: 84859816587     PISSN: 0039128X     EISSN: 18785867     Source Type: Journal    
DOI: 10.1016/j.steroids.2012.02.015     Document Type: Article

References (88)

1. Auersperg N, Ota T, Mitchell GW. Early events in ovarian epithelial carcinogenesis: progress and problems in experimental approaches. Int J Gynecol Cancer 2002;12(6):691-703. (Pubitemid 35388036)
2. Auersperg N, Wong AS, Choi KC, Kang SK, Leung PC. Ovarian surface epithelium: biology, endocrinology, and pathology. Endocr Rev 2001;22(2):255-88. (Pubitemid 32458162)
3. Gougeon A. Dynamics of human follicular growth:morphologic, dynamic and functional aspects. In: Leung PC, Adashi EY, editors. The ovary (2nd ed.). San Diego: Elsevier Academic Press; 2004. p. 25-43.
4. Scully RE. Ovarian tumors. A review. Am J Pathol 1977;87(3):686-720.
5. Scully RE. Pathology of ovarian cancer precursors. J Cell Biochem Suppl 1995;23:208-18. (Pubitemid 26032877)
6. Wise PM, Smith MJ, Dubal DB, Wilson ME, Krajnak KM, Rosewell KL. Neuroendocrine influences and repercussions of the menopause. Endocr Rev 1999;20(3):243-8. (Pubitemid 30649806)
7. Treloar AE. Menstrual cyclicity and the pre-menopause. Maturitas 1981;3(3-4):249-64. (Pubitemid 12145694)
8. Danilovich N, Ram Sairam M. Recent female mouse models displaying advanced reproductive aging. Exp Gerontol 2006;41(2):117-22. (Pubitemid 43165684)
9. Nass TE, LaPolt PS, Judd HL, Lu JK. Alterations in ovarian steroid and gonadotrophin secretion preceding the cessation of regular oestrous cycles in ageing female rats. J Endocrinol 1984;100(1):43-50. (Pubitemid 14198694)
10. Prior JC. Perimenopause: the complex endocrinology of the menopausal transition. Endocr Rev 1998;19(4):397-428. (Pubitemid 29116375)
11. Prior JC. Ovarian aging and the perimenopausal transition: the paradox of endogenous ovarian hyperstimulation. Endocrine 2005;26(3):297-300. (Pubitemid 41271096)
12. Shifren JL, Schiff I. The aging ovary. J Womens Health Gend Based Med 2000;9(Suppl 1):S3-7. (Pubitemid 30116515)
13. Djahanbakhch O, Ezzati M, Zosmer A. Reproductive ageing in women. J Pathol 2007;211(2):219-31. (Pubitemid 46195520)
14. Rodriguez C, Patel AV, Calle EE, Jacob EJ, Thun MJ. Estrogen replacement therapy and ovarian cancer mortality in a large prospective study of US women. JAMA 2001;285(11):1460-5. (Pubitemid 32221894)
15. Lacey Jr JV, Mink PJ, Lubin JH, Sherman ME, Troisi R, Hartge P, et al. Menopausal hormone replacement therapy and risk of ovarian cancer. JAMA 2002;288(3):334-41. (Pubitemid 34761612)
16. Lacey Jr JV, Brinton LA, Leitzmann MF, Mouw T, Hollenbeck A, Schatzkin A, et al. Menopausal hormone therapy and ovarian cancer risk in the National Institutes of Health-AARP Diet and Health Study Cohort. J Natl Cancer Inst 2006;98(19):1397-405. (Pubitemid 44530716)
17. Riman T, Dickman PW, Nilsson S, Correia N, Nordlinder H, Magnusson CM, et al. Hormone replacement therapy and the risk of invasive epithelial ovarian cancer in Swedish women. J Natl Cancer Inst 2002;94(7):497-504. (Pubitemid 34411288)
18. Folsom AR, Anderson JP, Ross JA. Estrogen replacement therapy and ovarian cancer. Epidemiology 2004;15(1):100-4. (Pubitemid 40417003)
19. Mills PK, Riordan DG, Cress RD. Epithelial ovarian cancer risk by invasiveness and cell type in the Central Valley of California. Gynecol Oncol 2004;95(1):215-25. (Pubitemid 39286301)
20. Pearce CL, Chung K, Pike MC, Wu AH. Increased ovarian cancer risk associated with menopausal estrogen therapy is reduced by adding a progestin. Cancer 2009;115(3):531-9.
21. Moorman PG, Schildkraut JM, Calingaert B, Halabi S, Berchuck A. Menopausal hormones and risk of ovarian cancer. Am J Obstet Gynecol 2005;193(1):76-82. (Pubitemid 40991829)
22. Clow OL, Hurst PR, Fleming JS. Changes in the mouse ovarian surface epithelium with age and ovulation number. Mol Cell Endocrinol 2002;191(1):105-11.
23. Laviolette LA, Garson K, Macdonald EA, Senterman MK, Courville K, Crane CA, et al. 17beta-estradiol accelerates tumor onset and decreases survival in a transgenic mouse model of ovarian cancer. Endocrinology 2010;151(3):929-38.
24. Gulliver LS, Hurst PR. Novel approaches to quantify estradiol-induced loss of ERbeta1 protein in older mouse ovarian surface epithelium: new tools to assess the role of ER protein subtypes in predisposing to ovarian epithelial cancer? Horm, Cancer 2011;2(4):204-13.
25. Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schutz G, Umesono K, et al. The nuclear receptor superfamily: the second decade. Cell 1995;83(6):835-9.
26. Fox EM, Davis RJ, Shupnik MA. ERbeta in breast cancer-onlooker, passive player, or active protector? Steroids 2008;73(11):1039-51.
27. Leung YK, Mak P, Hassan S, Ho SM. Estrogen receptor (ER)-beta isoforms: a key to understanding ER-beta signaling. Proc Natl Acad Sci USA 2006;103(35):13162-7. (Pubitemid 44338933)
28. White R, Lees JA, Needham M, Ham J, Parker M. Structural organization and expression of the mouse estrogen receptor. Mol Endocrinol 1987;1(10):735-44. (Pubitemid 17166939)
29. Kuiper GG, Enmark E, Pelto-Huikko M, Nilsson S, Gustafsson JA. Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci USA 1996;93(12):5925-30. (Pubitemid 26190778)
30. Mosselman S, Polman J, Dijkema R. ER beta: identification and characterization of a novel human estrogen receptor. FEBS Lett 1996;392(1):49-53. (Pubitemid 26268330)
31. Tremblay GB, Tremblay A, Copeland NG, Gilbert DJ, Jenkins NA, Labrie F, et al. Cloning, chromosomal localization, and functional analysis of the murine estrogen receptor beta. Mol Endocrinol 1997;11(3):353-65. (Pubitemid 27106331)
32. Couse JF, Hewitt SC, Korach KS. Steroid receptors in the ovary and uterus. In: Neill JD, editor. Knobil and Neill's physiology of reproduction (3rd ed.). London: Elsevier Academic Press; 2006. p. 593-678.
33. Cowley SM, Hoare S, Mosselman S, Parker MG. Estrogen receptors alpha and beta form heterodimers on DNA. J Biol Chem 1997;272(32):19858-62. (Pubitemid 27340081)
34. Pace P, Taylor J, Suntharalingam S, Coombes RC, Ali S. Human estrogen receptor beta binds DNA in a manner similar to and dimerizes with estrogen receptor alpha. J Biol Chem 1997;272(41):25832-8. (Pubitemid 27438906)
35. Tremblay GB, Tremblay A, Labrie F, Giguere V. Dominant activity of activation function 1 (AF-1) and differential stoichiometric requirements for AF-1 and -2 in the estrogen receptor alpha-beta heterodimeric complex. Mol Cell Biol 1999;19(3):1919-27. (Pubitemid 29098250)
36. Li X, Huang J, Yi P, Bambara RA, Hilf R, Muyan M. Single-chain estrogen receptors (ERs) reveal that the ERalpha/beta heterodimer emulates functions of the ERalpha dimer in genomic estrogen signaling pathways. Mol Cell Biol 2004;24(17):7681-94. (Pubitemid 39121493)
37. Perez-Gracia JL, Carrasco EM. Tamoxifen therapy for ovarian cancer in the adjuvant and advanced settings: systematic review of the literature and implications for future research. Gynecol Oncol 2002;84(2):201-9. (Pubitemid 34139799)
38. Ho SM. Estrogen, progesterone and epithelial ovarian cancer. Reprod Biol Endocrinol 2003;7(1):73.
39. Hillier SG, Anderson RA, Williams AR, Tetsuka M. Expression of oestrogen receptor alpha and beta in cultured human ovarian surface epithelial cells. Mol Hum Reprod 1998;4(8):811-5. (Pubitemid 28392026)
40. Lau KM, Mok SC, Ho SM. Expression of human estrogen receptor-alpha and - beta, progesterone receptor, and androgen receptor mRNA in normal and malignant ovarian epithelial cells. Proc Natl Acad Sci USA 1999;96(10):5722-7. (Pubitemid 29234685)
41. Syed V, Ulinski G, Mok SC, Yiu GK, Ho SM. Expression of gonadotropin receptor and growth responses to key reproductive hormones in normal and malignant human ovarian surface epithelial cells. Cancer Res 2001;61(18):6768-76. (Pubitemid 32896499)
42. Bai W, Oliveros-Saunders B, Wang Q, Acevedo-Duncan ME, Nicosia SV. Estrogen stimulation of ovarian surface epithelial cell proliferation. In Vitro Cell Dev Biol Anim 2000;36(10):657-66. (Pubitemid 32164666)
43. Stewart SL, Querec TD, Gruver BN, O'Hare B, Babb JS, Patriotis C. Gonadotropin and steroid hormones stimulate proliferation of the rat ovarian surface epithelium. J Cell Physiol 2004;198(1):119-24. (Pubitemid 38120972)
44. Silva EG, Tornos C, Deavers M, Kaisman K, Gray K, Gershenson D. Induction of epithelial neoplasms in the ovaries of guinea pigs by estrogenic stimulation. Gynecol Oncol 1998;71(2):240-6. (Pubitemid 28550807)
45. Kang JS, Lee BJ, Ahn B, Kim DJ, Nam SY, Yun YW, et al. Expression of estrogen receptor alpha and beta in the uterus and vagina of immature rats treated with 17-ethinyl estradiol. J Vet Med Sci 2003;65(12):1293-7. (Pubitemid 41365427)
46. Lazennec G. Estrogen receptor beta, a possible tumor suppressor involved in ovarian carcinogenesis. Cancer Lett 2006;231(2):151-7. (Pubitemid 43038725)
47. Brandenberger AW, Tee MK, Jaffe RB. Estrogen receptor alpha (ER-alpha) and beta (ER-beta) mRNAs in normal ovary, ovarian serous cystadenocarcinoma and ovarian cancer cell lines: down-regulation of ER-beta in neoplastic tissues. J Clin Endocrinol Metab 1998;83(3):1025-8. (Pubitemid 28496985)
48. Chan KK, Wei N, Liu SS, Xiao-Yun L, Cheung AN, Ngan HY. Estrogen receptor subtypes in ovarian cancer: a clinical correlation. Obstet Gynecol 2008;111(1):144-51.
49. Bonkhoff H, Fixemer T, Hunsicker I, Remberger K. Estrogen receptor expression in prostate cancer and premalignant prostatic lesions. Am J Pathol 1999;155(2):641-7. (Pubitemid 29370414)
50. Jakimiuk AJ, Weitsman SR, Yen HW, Bogusiewicz M, Magoffin DA. Estrogen receptor alpha and beta expression in theca and granulosa cells from women with polycystic ovary syndrome. J Clin Endocrinol Metab 2002;87(12):5532-8. (Pubitemid 36034356)
51. Takeichi M. Cadherin cell adhesion receptors as a morphogenetic regulator. Science 1991;251(5000):1451-5. (Pubitemid 121000430)
52. Auersperg N, Pan J, Grove BD, Peterson T, Fisher J, Maines-Bandiera S, et al. Ecadherin induces mesenchymal-to-epithelial transition in human ovarian surface epithelium. Proc Natl Acad Sci USA 1999;96(11):6249-54. (Pubitemid 29256651)
53. Ong A, Maines-Bandiera SL, Roskelley CD, Auersperg N. An ovarian adenocarcinoma line derived from SV40/E-cadherin-transfected normal human ovarian surface epithelium. Int J Cancer 2000;85(3):430-7. (Pubitemid 30030419)
54. Davies BR, Worsley SD, Ponder BA. Expression of E-cadherin, alpha-catenin and beta-catenin in normal ovarian surface epithelium and epithelial ovarian cancers. Histopathology 1998;32(1):69-80.
55. Cho EY, Choi Y, Chae SW, Sohn JH, Ahn GH. Immunohistochemical study of the expression of adhesion molecules in ovarian serous neoplasms. Pathol Int 2006;56(2):62-70.
56. Hudson LG, Zeineldin R, Stack MS. Phenotypic plasticity of neoplastic ovarian epithelium: unique cadherin profiles in tumor progression. Clin Exp Metastasis 2008;25(6):643-55.
57. MacCalman CD, Farookhi R, Blaschuk OW. Estradiol regulates E-cadherin mRNA levels in the surface epithelium of the mouse ovary. Clin Exp Metastasis 1994;12(4):276-82. (Pubitemid 24257065)
58. Allred DC, Carlson RW, Berry DA, Burstein HJ, Edge SB, Goldstein LJ, et al. NCCN task force report: estrogen receptor and progesterone receptor testing in breast cancer by immunohistochemistry. J Natl Compr Canc Netw 2009;7(Suppl 6):S1-S21 (quiz S2-3).
59. Wong AS, Maines-Bandiera SL, Rosen B, Wheelock MJ, Johnson KR, Leung PC, et al. Constitutive and conditional cadherin expression in cultured human ovarian surface epithelium: influence of family history of ovarian cancer. Int J Cancer 1999;81(2):180-8. (Pubitemid 29144744)
60. Mobbs CV, Finch CE. Estrogen-induced impairments as a mechanism in reproductive senescence of female C57BL/6J mice. J Gerontol 1992;47(2):B48-51.
61. Hirshfield AN, DeSanti AM. Patterns of ovarian cell proliferation in rats during the embryonic period and the first three weeks postpartum. Biol Reprod 1995;53(5):1208-21.
62. Burdette JE, Kurley SJ, Kilen SM, Mayo KE, Woodruff TK. Gonadotropin-induced superovulation drives ovarian surface epithelia proliferation in CD1 mice. Endocrinology 2006;147(5):2338-45.
63. Gundersen HJ, Bendtsen TF, Korbo L, Marcussen N, Moller A, Nielsen K, et al. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 1988;96(5):379-94.
64. Gould ML, Hurst PR, Nicholson HD. The effects of oestrogen receptors alpha and beta on testicular cell number and steroidogenesis in mice. Reproduction 2007;134(2):271-9. (Pubitemid 47278800)
65. Fleming JS, McQuillan HJ, Millier MJ, Beaugie CR, Livingstone V. E-cadherin expression and bromodeoxyuridine incorporation during development of ovarian inclusion cysts in age-matched breeder and incessantly ovulated CD-1 mice. Reprod Biol Endocrinol 2007;5:14.
66. Gundersen HJ, Jensen EB. Stereological estimation of the volume-weighted mean volume of arbitrary particles observed on random sections. J Microsc 1985;138(Pt 2):127-42. (Pubitemid 15066551)
67. Syed V, Ulinski G, Mok SC, Ho SM. Reproductive hormone-induced, STAT3-mediated interleukin 6 action in normal and malignant human ovarian surface epithelial cells. J Natl Cancer Inst 2002;94(8):617-29. (Pubitemid 34498649)
68. Choi KC, Kang SK, Tai CJ, Auersperg N, Leung PC. Estradiol up-regulates antiapoptotic Bcl-2 messenger ribonucleic acid and protein in tumorigenic ovarian surface epithelium cells. Endocrinology 2001;142(6):2351-60. (Pubitemid 32473090)
69. Karlan BY, Jones J, Greenwald M, Lagasse LD. Steroid hormone effects on the proliferation of human ovarian surface epithelium in vitro. Am J Obstet Gynecol 1995;173(1):97-104.
70. Wright JW, Toth-Fejel S, Stouffer RL, Rodland KD. Proliferation of rhesus ovarian surface epithelial cells in culture: lack of mitogenic response to steroid or gonadotropic hormones. Endocrinology 2002;143(6):2198-207. (Pubitemid 34521565)
71. Pietras RJ, Szego CM. Endometrial cell calcium and oestrogen action. Nature 1975;265:357-9.
72. Rambo CO, Szego CM. Estrogen action at endometrial membranes: alterations in luminal surface detectable within seconds. J Cell Biol 1983;97(3):679-85. (Pubitemid 13007185)
73. Doisneau-Sixou SF, Sergio CM, Carroll JS, Hui R, Musgrove EA, Sutherland RL. Estrogen and antiestrogen regulation of cell cycle progression in breast cancer cells. Endocr Relat Cancer 2003;10(2):179-86. (Pubitemid 36758647)
74. Tong W, Pollard JW. Progesterone inhibits estrogen-induced cyclin D1 and cdk4 nuclear translocation, cyclin E- and cyclin A-cdk2 kinase activation, and cell proliferation in uterine epithelial cells in mice. Mol Cell Biol 1999;19(3):2251-64. (Pubitemid 29098283)
75. Simoes Mde J, Simoes Rdos S, Haidar MA, Baracat EC, Soares Jr JM. Proliferation of the superficial epithelium of ovaries in senile female rats following oral administration of conjugated equine estrogens. Clinics (Sao Paulo) 2008;63(3):381-8.
76. Parrott JA, Kim G, Mosher R, Skinner MK. Expression and action of keratinocyte growth factor (KGF) in normal ovarian surface epithelium and ovarian cancer. Mol Cell Endocrinol 2000;167(1-2):77-87.
77. Doraiswamy V, Parrott JA, Skinner MK. Expression and action of transforming growth factor alpha in normal ovarian surface epithelium and ovarian cancer. Biol Reprod 2000;63(3):789-96. (Pubitemid 30659274)
78. Zhang Y, Kulp SK, Sugimoto Y, Farrar WB, Brueggemeier RW, Lin YC. Keratinocyte growth factor (KGF) induces aromatase activity in cultured MCF-7 human breast cancer cells. Anticancer Res 1998;18(4A):2541-6. (Pubitemid 28386548)
79. Qian X, Karpova T, Sheppard AM, McNally J, Lowy DR. E-cadherin-mediated adhesion inhibits ligand-dependent activation of diverse receptor tyrosine kinases. EMBO J 2004;23(8):1739-48. (Pubitemid 38649637)
80. Perrais M, Chen X, Perez-Moreno M, Gumbiner BM. E-cadherin homophilic ligation inhibits cell growth and epidermal growth factor receptor signaling independently of other cell interactions. Mol Biol Cell 2007;18(6):2013-25. (Pubitemid 46911354)
81. Reddy P, Liu L, Ren C, Lindgren P, Boman K, Shen Y, et al. Formation of E-cadherin- mediated cell-cell adhesion activates AKT and mitogen activated protein kinase via phosphatidylinositol 3 kinase and ligand-independent activation of epidermal growth factor receptor in ovarian cancer cells. Mol Endocrinol 2005;19(10):2564-78. (Pubitemid 41362669)
82. Leung PC, Choi JH. Endocrine signaling in ovarian surface epithelium and cancer. Hum Reprod Update 2007;13(2):143-62. (Pubitemid 46323192)
83. Ignar-Trowbridge DM, Nelson KG, Bidwell MC, Curtis SW, Washburn TF, McLachlan JA, et al. Coupling of dual signaling pathways: epidermal growth factor action involves the estrogen receptor. Proc Natl Acad Sci USA 1992;89(10):4658-62.
84. Salamanca CM, Maines-Bandiera SL, Leung PC, Hu YL, Auersperg N. Effects of epidermal growth factor/hydrocortisone on the growth and differentiation of human ovarian surface epithelium. J Soc Gynecol Investig 2004;11(4):241-51. (Pubitemid 38561370)
85. Maruo T, Ladines-Llave CA, Samoto T, Matsuo H, Manalo AS, Ito H, et al. Expression of epidermal growth factor and its receptor in the human ovary during follicular growth and regression. Endocrinology 1993;132(2):924-31. (Pubitemid 23056159)
86. Anakk S, Ku CY, Vore M, Strobel HW. Insights into gender bias: rat cytochrome P450 3A9. J Pharmacol Exp Ther 2003;305(2):703-9. (Pubitemid 36459190)
87. Parrott JA, Nilsson E, Mosher R, Magrane G, Albertson D, Pinkel D, et al. Stromal-epithelial interactions in the progression of ovarian cancer: influence and source of tumor stromal cells. Mol Cell Endocrinol 2001;175(1-2):29-39. (Pubitemid 32372541)
88. Forster C, Makela S, Warri A, Kietz S, Becker D, Hultenby K, et al. Involvement of estrogen receptor beta in terminal differentiation of mammary gland epithelium. Proc Natl Acad Sci USA 2002;99(24):15578-83. (Pubitemid 35407484)