Uterine epithelial cell estrogen receptor alpha-dependent and -independent genomic profiles that underlie estrogen responses in mice

Biology of Reproduction

Volumn 91, Issue 5, 2014, Pages

  Winuthayanon, Wipawee ^a   Hewitt, Sylvia C ^a   Korach, Kenneth S ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

Epithelium; Estradiol estradiol receptor; Proliferation; Stroma; Uterus

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; PROGESTERONE; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE REGULATION; CELL PROLIFERATION; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; GENE EXPRESSION; MICROARRAY ANALYSIS; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; UTERUS; UTERUS GROWTH; ANIMAL; CELL CULTURE; DRUG EFFECTS; FOLLICULAR PHASE; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY;

MUS;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; EPITHELIAL CELLS; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; FOLLICULAR PHASE; GENE EXPRESSION REGULATION; MICE; MICE, KNOCKOUT; MICROARRAY ANALYSIS; TRANSCRIPTOME; UTERUS;

EID: 84930510162     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.114.120170     Document Type: Article

References (40)

1. Tabibzadeh S. The signals and molecular pathways involved in human menstruation, a unique process of tissue destruction and remodelling. Mol Hum Reprod 1996; 2:77-92.
2. Couse JF, Korach KS. Estrogen receptor null mice: what have we learned and where will they lead us? Endocr Rev 1999; 20:358-417.
3. Couse JF, Lindzey J, Grandien K, Gustafsson JA, Korach KS. Tissue distribution and quantitative analysis of estrogen receptor-alpha (ERalpha) and estrogen receptor-beta (ERbeta) messenger ribonucleic acid in the wild-type and ERalpha-knockout mouse. Endocrinology 1997; 138: 4613-4621.
4. Wang H, Eriksson H, Sahlin L. Estrogen receptors alpha and beta in the female reproductive tract of the rat during the estrous cycle. Biol Reprod 2000; 63:1331-1340.
5. Hewitt SC, Li L, Grimm SA, Chen Y, Liu L, Li Y, Bushel PR, Fargo D, Korach KS. Research resource: whole-genome estrogen receptor alpha binding in mouse uterine tissue revealed by ChIP-seq. Mol Endocrinol 2012; 26:887-898.
6. Griffith JS, Jensen SM, Lunceford JK, Kahn MW, Zheng Y, Falase EA, Lyttle CR, Teuscher C. Evidence for the genetic control of estradiolregulated responses. Implications for variation in normal and pathological hormone-dependent phenotypes. Am J Pathol 1997; 150:2223-2230.
7. Perez MC, Furth EE, Matzumura PD, Lyttle CR. Role of eosinophils in uterine responses to estrogen. Biol Reprod 1996; 54:249-254.
8. Pollard JW, Pacey J, Cheng SV, Jordan EG. Estrogens and cell death in murine uterine luminal epithelium. Cell Tissue Res 1987; 249:533-540.
9. Quarmby VE, Korach KS. The influence of 17 beta-estradiol on patterns of cell division in the uterus. Endocrinology 1984; 114:694-702.
10. Hewitt SC, Deroo BJ, Hansen K, Collins J, Grissom S, Afshari CA, Korach KS. Estrogen receptor-dependent genomic responses in the uterus mirror the biphasic physiological response to estrogen. Mol Endocrinol 2003; 17:2070-2083.
11. Cunha GR, Chung LW, Shannon JM, Reese BA. Stromal-epithelial interactions in sex differentiation. Biol Reprod 1980; 22:19-42.
12. DiAugustine RP, Petrusz P, Bell GI, Brown CF, Korach KS, McLachlan JA, Teng CT. Influence of estrogens on mouse uterine epidermal growth factor precursor protein and messenger ribonucleic acid. Endocrinology 1988; 122:2355-2363.
13. Zhu L, Pollard JW. Estradiol-17beta regulates mouse uterine epithelial cell proliferation through insulin-like growth factor 1 signaling. Proc Natl Acad Sci U S A 2007; 104:15847-15851.
14. Hom YK, Young P, Wiesen JF, Miettinen PJ, Derynck R, Werb Z, Cunha GR. Uterine and vaginal organ growth requires epidermal growth factor receptor signaling from stroma. Endocrinology 1998; 139:913-921.
15. Nelson KG, Takahashi T, Lee DC, Luetteke NC, Bossert NL, Ross K, Eitzman BE, McLachlan JA. Transforming growth factor-alpha is a potential mediator of estrogen action in the mouse uterus. Endocrinology 1992; 131:1657-1664.
16. Winuthayanon W, Hewitt SC, Orvis GD, Behringer RR, Korach KS. Uterine epithelial estrogen receptor a is dispensable for proliferation but essential for complete biological and biochemical responses. Proc Natl Acad Sci U S A 2010; 107:19272-19277.
17. Cooke PS, Buchanan DL, Young P, Setiawan T, Brody J, Korach KS, Taylor J, Lubahn DB, Cunha GR. Stromal estrogen receptors mediate mitogenic effects of estradiol on uterine epithelium. Proc Natl Acad Sci U S A 1997; 94:6535-6540.
18. Mantena SR, Kannan A, Cheon YP, Li Q, Johnson PF, Bagchi IC, Bagchi MK. C/EBPbeta is a critical mediator of steroid hormone-regulated cell proliferation and differentiation in the uterine epithelium and stroma. Proc Natl Acad Sci U S A 2006; 103:1870-1875.
19. Huang CC, Orvis GD, Wang Y, Behringer RR. Stromal-to-epithelial transition during postpartum endometrial regeneration. PLoS One 2012; 7: e44285.
20. Pan H, Zhu L, Deng Y, Pollard JW. Microarray analysis of uterine epithelial gene expression during the implantation window in the mouse. Endocrinology 2006; 147:4904-4916.
21. Hewitt SC, Korach KS. Estrogenic activity of bisphenol A and 2,2-bis(phydroxyphenyl)- 1,1,1-trichloroethane (HPTE) demonstrated in mouse uterine gene profiles. Environ Health Perspect 2011; 119:63-70.
22. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002; 30:207-210.
23. Ray S, Pollard JW. KLF15 negatively regulates estrogen-induced epithelial cell proliferation by inhibition of DNA replication licensing. Proc Natl Acad Sci U S A 2012; 109:E1334-1343.
24. Valdes G, Figueroa CD, Corthorn J. Temporospatial changes of kallikreinlike enzymes during the estrous cycle and pregnancy in the rat uterus. Biol Reprod 1996; 55:236-245.
25. Rajapakse S, Yamano N, Ogiwara K, Hirata K, Takahashi S, Takahashi T. Estrogen-dependent expression of the tissue kallikrein gene (Klk1) in the mouse uterus and its implications for endometrial tissue growth. Mol Reprod Dev 2007; 74:1053-1063.
26. Martin L, Finn CA, Trinder G. Hypertrophy and hyperplasia in the mouse uterus after oestrogen treatment: an autoradiographic study. J Endocrinol 1973; 56:133-144.
27. Stewart CL, Kaspar P, Brunet LJ, Bhatt H, Gadi I, Kontgen F, Abbondanzo SJ. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 1992; 359:76-79.
28. Lee K, Jeong J, Kwak I, Yu CT, Lanske B, Soegiarto DW, Toftgard R, Tsai MJ, Tsai S, Lydon JP, DeMayo FJ. Indian hedgehog is a major mediator of progesterone signaling in the mouse uterus. Nat Genet 2006; 38:1204-1209.
29. Wakitani S, Hondo E, Phichitraslip T, Stewart CL, Kiso Y. Upregulation of Indian hedgehog gene in the uterine epithelium by leukemia inhibitory factor during mouse implantation. J Reprod Dev 2008; 54:113-116.
30. Li Q, Kannan A, DeMayo FJ, Lydon JP, Cooke PS, Yamagishi H, Srivastava D, Bagchi MK, Bagchi IC. The antiproliferative action of progesterone in uterine epithelium is mediated by Hand2. Science 2011; 331:912-916.
31. Yamanouchi H, Umezu T, Tomooka Y. Reconstruction of oviduct and demonstration of epithelial fate determination in mice. Biol Reprod 2010; 82:528-533.
32. Hewitt SC, Collins J, Grissom S, Deroo B, Korach KS. Global uterine genomics in vivo: microarray evaluation of the estrogen receptor alphagrowth factor cross-talk mechanism. Mol Endocrinol 2005; 19:657-668.
33. Logan CY, Nusse R. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 2004; 20:781-810.
34. Hou X, Tan Y, Li M, Dey SK, Das SK. Canonical Wnt signaling is critical to estrogen-mediated uterine growth. Mol Endocrinol 2004; 18: 3035-3049.
35. Zhang L, Patterson AL, Teixeira JM, Pru JK. Endometrial stromal betacatenin is required for steroid-dependent mesenchymal-epithelial cross talk and decidualization. Reprod Biol Endocrinol 2012; 10:75.
36. Couse JF, Curtis SW, Washburn TF, Lindzey J, Golding TS, Lubahn DB, Smithies O, Korach KS. Analysis of transcription and estrogen insensitivity in the female mouse after targeted disruption of the estrogen receptor gene. Mol Endocrinol 1995; 9:1441-1454.
37. Hewitt SC, Kissling GE, Fieselman KE, Jayes FL, Gerrish KE, Korach KS. Biological and biochemical consequences of global deletion of exon 3 from the ER alpha gene. FASEB J 2010; 24:4660-4667.
38. Franco HL, Rubel CA, Large MJ, Wetendorf M, Fernandez-Valdivia R, Jeong JW, Spencer TE, Behringer RR, Lydon JP, Demayo FJ. Epithelial progesterone receptor exhibits pleiotropic roles in uterine development and function. FASEB J 2012; 26:1218-1227.
39. Filant J, Spencer TE. Cell-specific transcriptional profiling reveals candidate mechanisms regulating development and function of uterine epithelia in mice. Biol Reprod 2013; 89:86.
40. Hewitt SC, Li L, Grimm SA, Winuthayanon W, Hamilton KJ, Pockette B, Rubel CA, Pedersen LC, Fargo D, Lanz RB, DeMayo FJ, Schutz G, et al. Novel DNA motif binding activity observed in vivo with an estrogen receptor alpha mutant mouse. Mol Endocrinol 2014; 28:899-911.