Tissue selective estrogen complexes (TSECs) differentially modulate markers of proliferation and differentiation in endometrial cells

Reproductive Sciences

Volumn 20, Issue 2, 2013, Pages 129-137

  Kulak, Jaime ^a,b   Ferriani, Rui A ^c   Komm, Barry S ^d   Taylor, Hugh S ^a,e  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d PFIZER INC   (United States)

^e YALE UNIVERSITY   (United States)

Author keywords

EMX2; HOXA10; ishikawa; leukemia inhibitory factor (LIF); progesterone receptor; SERMS; TSECS

Indexed keywords

BAZEDOXIFENE; ESTRADIOL; ESTROGEN; LASOFOXIFENE; LEUKEMIA INHIBITORY FACTOR; MESSENGER RNA; PROGESTERONE; PROGESTERONE RECEPTOR; RALOXIFENE; SELECTIVE ESTROGEN RECEPTOR MODULATOR; TAMOXIFEN; TISSUE SELECTIVE ESTROGEN COMPLEX; TRANSCRIPTION FACTOR EMX2; TRANSCRIPTION FACTOR HOXA10; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DRUG EFFECT; ENDOMETRIUM CELL; GENE EXPRESSION; PRIORITY JOURNAL;

BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; ENDOMETRIUM; ESTROGEN RECEPTOR MODULATORS; ESTROGENS, CONJUGATED (USP); FEMALE; HOMEODOMAIN PROTEINS; HUMANS; RECEPTORS, PROGESTERONE; TRANSCRIPTION FACTORS;

EID: 84871549832     PISSN: 19337191     EISSN: 19337205     Source Type: Journal    
DOI: 10.1177/1933719112463251     Document Type: Article

References (59)

1. US Census Bureau. Table 1: annual estimates of the population by sex and five year age groups for the United States: April 1st, 2007. NC-EST20070-01. May 2008.
2. Gallagher JC, levine JP. Preventing osteoporosis in symptomatic postmenopausal women. Menopause. 2011 ; 18 (1). 109-118
3. Bachmann GA. Menopausal vasomotor symptoms: a review of causes, effects and evidence-based treatment options. J Reprod Med. 2005 ; 50 (3). 155-165
4. Panay N, Maamari R. Treatment of postmenopausal vaginal atrophy with 10-mug estradiol vaginal tablets. Menopause Int. 2012 ; 18: 15-19
5. Taylor HS, Manson JE. Update in hormone therapy use in menopause. J Clin Endocrinol Metab. 2011 ; 96 (2). 255-264
6. Hardie C, Bain C, Walters M. Hormone replacement therapy: the risks and benefits of treatment. J R Coll Physicians Edinb. 2009 ; 39 (4). 324-326
7. Buick DL, Crook D, Horne R. Women's perceptions of hormone replacement therapy: risks and benefits (1980-2002). A literature review. Climacteric. 2005 ; 8 (1). 24-35
8. Anderson GL, Limacher M, Assaf AR, et al. Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women's Health Initiative randomized controlled trial. JAMA. 2004 ; 291 (14). 1701-1712
9. LaCroix AZ, Chlebowski RT, Manson JE, et al. Health outcomes after stopping conjugated equine estrogens among postmenopausal women with prior hysterectomy: a randomized controlled trial. JAMA. 2011 ; 305 (13). 1305-1314
10. Lethaby A, Farquar C, Sakris A, Roberts H, Jepson R, Barlow D. Hormone replacement therapy in postmenopausal women: endometrial hyperplasia and irregular bleeding. Cochrane Database Syst Rev. 2000 ; 2: CD000402
11. Rossouw JE, Anderson GL, Prentice RL, et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA. 2002 ; 288 (3). 321-333
12. Chlebowski RT, Anderson GL, Gass M, et al. Estrogen plus progestin and breast cancer incidence and mortality in postmenopausal women. JAMA. 2010 ; 304 (15). 1684-1692
13. Pickar JH, Mirkin S. Tissue-selective agents: selective estrogen receptor modulators and the tissue-selective estrogen complex. Menopause Int. 2010 ; 16 (3). 121-128
14. Cummings SR, Eckert S, Krueger KA, et al. The effect of raloxifene on risk of breast cancer in postmenopausal women: results from the MORE randomized trial. Multiple Outcomes of Raloxifene Evaluation. JAMA. 1999 ; 281 (23). 2189-2197
15. Barkhem T, Carlsson B, Nilsson Y, Enmark E, Gustafsson J, Nilsson S. Differential response of estrogen receptor alpha and estrogen receptor beta to partial estrogen agonists/antagonists. Mol Pharmacol. 1998 ; 54 (1). 105-112
16. Shang Y, Brown M. Molecular determinants for the tissue specificity of SERMs. Science. 2002 ; 295 (5564). 2465-2468
17. Klinge CM. Estrogen receptor interaction with co-activators and co-repressors. Steroids. 2000 ; 65 (5). 227-251
18. Miller CP. SERMs: evolutionary chemistry, revolutionary biology. Curr Pharm Des. 2002 ; 8 (23). 2089-2111
19. Chia S, Gradishar W. Fulvestrant: expanding the endocrine treatment options for patients with hormone receptor-positive advanced breast cancer. Breast. 2008 ; 17 (suppl 3). S16 - S21
20. Valachis A, Mauri D, Polyzos NP, Mavroudis D, Georgoulias V, Casazza G. Fulvestrant in the treatment of advanced breast cancer: a systematic review and meta-analysis of randomized controlled trials. Crit Rev Oncol Hematol. 2010 ; 73 (3). 220-227
21. Stovall DW, Tanner-Kurtz K, Pinkerton JV. Tissue-selective estrogen complex bazedoxifene and conjugated estrogens for the treatment of menopausal vasomotor symptoms. Drugs. 2011 ; 71 (13). 1649-1657
22. Gennari L, Merlotti D, De Paola V, Martini G, Nuti R. Bazedoxifene for the prevention of postmenopausal osteoporosis. Ther Clin Risk Manag. 2008 ; 4 (6). 1229-1242
23. Berrodin TJ, Chang KC, Komm BS, Freedman LP, Nagpal S. Differential biochemical and cellular actions of Premarin estrogens: distinct pharmacology of bazedoxifene-conjugated estrogens combination. Mol Endocrinol. 2009 ; 23 (1). 74-85
24. Lessey BA, Ilesanmi AO, Castelbaum AJ, et al. Characterization of the functional progesterone receptor in an endometrial adenocarcinoma cell line (Ishikawa): progesterone-induced expression of the alpha1 integrin. J Steroid Biochem Mol Biol. 1996 ; 59 (1). 31-39
25. Ishiwata I, Ishiwata C, Nagayama T, Ishikawa H. Histogenesis and culture of human uterine carcinosarcoma. Cancer Res. 1981 ; 41 (5). 1978-1983
26. Smith CC, Taylor HS. Xenoestrogen exposure imprints expression of genes (Hoxa10) required for normal uterine development. FASEB J. 2007 ; 21 (1). 239-246
27. Komm BS, Kharode YP, Bodine PV, Harris HA, Miller CP, Lyttle CR. Bazedoxifene acetate: a selective estrogen receptor modulator with improved selectivity. Endocrinology. 2005 ; 146 (9). 3999-4008
28. Daftary GS, Taylor HS. Endocrine regulation of HOX genes. Endocr Rev. 2006 ; 27 (4). 331-355
29. Vitiello D, Pinard R, Taylor HS. Gene expression profiling reveals putative HOXA10 downstream targets in the periimplantation mouse uterus. Reprod Sci. 2008 ; 15 (5). 529-535
30. Taylor HS, Arici A, Olive D, Igarashi P. HOXA10 is expressed in response to sex steroids at the time of implantation in the human endometrium. J Clin Invest. 1998 ; 101 (7). 1379-1384
31. Taylor HS, Daftary GS, Selam B. Endometrial HOXA10 expression after controlled ovarian hyperstimulation with recombinant follicle-stimulating hormone. Fertil Steril. 2003 ; 80 (suppl 2). 839-843
32. Daftary GS, Taylor HS. Implantation in the human: the role of HOX genes. Semin Reprod Med. 2000 ; 18 (3). 311-320
33. Das SK. Regional development of uterine decidualization: molecular signaling by Hoxa-10. Mol Reprod Dev. 2010 ; 77 (5). 387-396
34. Daftary GS, Taylor HS. Pleiotropic effects of Hoxa10 on the functional development of peri-implantation endometrium. Mol Reprod Dev. 2004 ; 67 (1). 8-14
35. Zanatta A, Rocha AM, Carvalho FM, et al. The role of the Hoxa10/HOXA10 gene in the etiology of endometriosis and its related infertility: a review. J Assist Reprod Genet. 2010 ; 27 (12). 701-710
36. Salamonsen LA, Nie G, Dimitriadis E, Robb L. Genes involved in implantation. Reprod Fertil Dev. 2001 ; 13 (1). 41-49
37. Senturk LM, Arici A. Leukemia inhibitory factor in human reproduction. Am J Reprod Immunol. 1998 ; 39 (2). 144-151
38. O'Malley BW. Steroid hormone receptors as transactivators of gene expression. Breast Cancer Res Treat. 1991 ; 18 (2). 67-71
39. Williams-Brown MY, Salih SM, Xu X, et al. The effect of tamoxifen and raloxifene on estrogen metabolism and endometrial cancer risk. J Steroid Biochem Mol Biol. 2011 ; 126 (3-5). 78-86
40. Kharode Y, Bodine PV, Miller CP, Lyttle CR, Komm BS. The pairing of a selective estrogen receptor modulator, bazedoxifene, with conjugated estrogens as a new paradigm for the treatment of menopausal symptoms and osteoporosis prevention. Endocrinology. 2008 ; 149 (12). 6084-6091
41. Archer DF, Lewis V, Carr BR, Olivier S, Pickar JH. Bazedoxifene/ conjugated estrogens (BZA/CE): incidence of uterine bleeding in postmenopausal women. Fertil Steril. 2009 ; 92 (3). 1039-1044
42. Lass A, Weiser W, Munafo A, Loumaye E. Leukemia inhibitory factor in human reproduction. Fertil Steril. 2001 ; 76 (6). 1091-1096
43. Salamonsen LA, Menkhorst EED. Leukemia inhibitory factor and human endometrial receptivity. Indian J Physiol Pharmacol. 2010 ; 54: 17-26
44. Kimber SJ. Leukaemia inhibitory factor in implantation and uterine biology. Reproduction. 2005 ; 130 (2). 131-145
45. Cullinan EB, Abbondanzo SJ, Anderson PS, Pollard JW, Lessey BA, Stewart CL. Leukemia inhibitory factor (LIF) and LIF receptor expression in human endometrium suggests a potential autocrine/paracrine function in regulating embryo implantation. Proc Natl Acad Sci U S A. 1996 ; 93 (7). 3115-3200
46. Sawai K, Matsuzaki N, Okada T, et al. Human decidual cell biosynthesis of leukemia inhibitory factor: regulation by decidual cytokines and steroid hormones. Biol Reprod. 1997 ; 56 (5). 1274-1280
47. Barakat RR. The effect of tamoxifen on the endometrium. Oncology (Williston Park). 1995 ; 9 (2). 129-134
48. Kedar RP, Bourne TH, Powles TJ, et al. Effects of tamoxifen on uterus and ovaries of postmenopausal women in a randomised breast cancer prevention trial. Lancet. 1994 ; 343 (8909). 1318-1321
49. Lahti E, Blanco G, Kauppila A, Apaja-Sarkkinen M, Taskinen PJ, Laatikainen T. Endometrial changes in postmenopausal breast cancer patients receiving tamoxifen. Obstet Gynecol. 1993 ; 81 (5 pt 1). 660-664
50. Allan GF, Hutchins A, Liu X, Clancy J. Induction of the progesterone receptor gene in estrogen target cells monitored by branched DNA signal amplification. Steroids. 2001 ; 66 (9). 663-671
51. Bramlett KS, Burris TP. Target specificity of selective estrogen receptor modulators within human endometrial cancer cells. J Steroid Biochem Mol Biol. 2003 ; 86 (1). 27-34
52. Troy PJ, Daftary GS, Bagot CN, Taylor HS. Transcriptional repression of peri-implantation EMX2 expression in mammalian reproduction by HOXA10. Mol Cell Biol. 2003 ; 23 (1). 1-13
53. Noonan FC, Mutch DG, Ann Mallon M, Goodfellow PJ. Characterization of the homeodomain gene EMX2: sequence conservation, expression analysis, and a search for mutations in endometrial cancers. Genomics. 2001 ; 76 (1-3). 37-44
54. Taylor HS, Fei X. Emx2 regulates mammalian reproduction by altering endometrial cell proliferation. Mol Endocrinol. 2005 ; 19 (11). 2839-2846
55. Peiffer-Schneider S, Noonan FC, Mutch DG, et al. Mapping an endometrial cancer tumor suppressor gene at 10q25 and development of a bacterial clone contig for the consensus deletion interval. Genomics. 1998 ; 52 (1). 9-16
56. Duggan ST, McKeage K. Bazedoxifene: a review of its use in the treatment of postmenopausal osteoporosis. Drugs. 2011 ; 71 (16). 2193-2212
57. Silverman S, Christiansen C. Individualizing osteoporosis therapy. Osteoporos Int. 2012 ; 23 (3). 797-809
58. Taylor HS. Using bazedoxifene plus conjugated estrogens for treating postmenopuasal women: a comprehensive review. Menopause. 2012 ; 19 (4). 479-485
59. Archer DF, Pinkerton JV, Utian WH, et al. Bazedoxifene, a selective estrogen receptor modulator: effects on the endometrium, ovaries, and breast from a randomized controlled trial in osteoporotic postmenopausal women. Menopause. 2009 ; 16 (6). 1109-1115