Neonatal uterine and vaginal cell proliferation and adenogenesis are independent of estrogen receptor 1 (ESR1) in the mouse

Biology of Reproduction

Volumn 92, Issue 3, 2015, Pages

  Nanjappa, Manjunatha K ^a   Medrano, Theresa I ^a   March, Amelia G ^a   Cooke, Paul S ^a  

^a University of Florida College of Veterinary Medicine   (United States)

Author keywords

17 estradiol; Progesterone; Uterine glands

Indexed keywords

ESTROGEN RECEPTOR ALPHA; PROGESTERONE;

ADENOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL SIZE; COMPARATIVE STUDY; CONTROLLED STUDY; ENDOMETRIUM; ENDOMETRIUM CELL; FEMALE; KNOCKOUT MOUSE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUBERTY; SEXUAL DEVELOPMENT; VAGINA; WEANING; WILD TYPE; ANIMAL; ANIMAL MODEL; C57BL MOUSE; CYTOLOGY; DEFICIENCY; EPITHELIUM CELL; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; HETEROZYGOTE; PHYSIOLOGY; SEXUAL MATURATION; TIME FACTOR; UTERUS;

MUS;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; CELL PROLIFERATION; EPITHELIAL CELLS; ESTROGEN RECEPTOR ALPHA; FEMALE; GENOTYPE; HETEROZYGOTE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, ANIMAL; PROGESTERONE; SEXUAL MATURATION; TIME FACTORS; UTERUS; VAGINA;

EID: 84928312809     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.114.125724     Document Type: Article

References (48)

1. Finn CA, Martin L. The role of the oestrogen secreted before oestrus in the preparation of the uterus for implantation in the mouse. J Endocrinol 1970; 47:431-438.
2. Finn CA, Martin L. Patterns of cell division in the mouse uterus during early pregnancy. J Endocrinol 1967; 39:593-597.
3. Ogasawara Y, Okamoto S, Kitamura Y, Matsumoto K. Proliferative pattern of uterine cells from birth to adulthood in intact, neonatally castrated, and/or adrenalectomized mice, assayed by incorporation of [125I]iododeoxyuridine. Endocrinology 1983; 113:582-587.
4. Bigsby RM, Cunha GR. Estrogen stimulation of deoxyribonucleic acid synthesis in uterine epithelial cells which lack estrogen receptors. Endocrinology 1986; 119:390-396.
5. Bigsby RM, Cunha GR. Effects of progestins and glucocorticoids on deoxyribonucleic acid synthesis in the uterus of the neonatal mouse. Endocrinology 1985; 117:2520-2526.
6. Nelson KG, Takahashi T, Bossert NL, Walmer DK, McLachlan JA. Epidermal growth factor replaces estrogen in the stimulation of female genital-tract growth and differentiation. Proc Natl Acad Sci U S A 1991; 88:21-25.
7. Curtis SW, Washburn T, Sewall C, DiAugustine R, Lindzey J, Couse JF, Korach KS. Physiological coupling of growth factor and steroid receptor signaling pathways: estrogen receptor knockout mice lack estrogen-like response to epidermal growth factor. Proc Natl Acad Sci U S A 1996; 93: 12626-12630.
8. Klotz DM, Hewitt SC, Ciana P, Raviscioni M, Lindzey JK, Foley J, Maggi A, DiAugustine RP, Korach KS. Requirement of estrogen receptor-alpha in insulin-like growth factor-1 (IGF-1)-induced uterine responses and in vivo evidence for IGF-1/estrogen receptor cross-talk. J Biol Chem 2002; 277:8531-8537.
9. Kato S, Endoh H, Masuhiro Y, Kitamoto T, Uchiyama S, Sasaki H, Masushige S, Gotoh Y, Nishida E, Kawashima H, Metzger D, Chambon P. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science 1995; 270:1491-1494.
10. Ignar-Trowbridge DM, Teng CT, Ross KA, Parker MG, Korach KS, McLachlan JA. Peptide growth factors elicit estrogen receptor-dependent transcriptional activation of an estrogen-responsive element. Mol Endocrinol 1993; 7:992-998.
11. Tarleton BJ, Wiley AA, Bartol FF. Endometrial development and adenogenesis in the neonatal pig: effects of estradiol valerate and the antiestrogen ICI 182,780. Biol Reprod 1999; 61:253-263.
12. Taylor KM, Chen C, Gray CA, Bazer FW, Spencer TE. Expression of messenger ribonucleic acids for fibroblast growth factors 7 and 10, hepatocyte growth factor, and insulin-like growth factors and their receptors in the neonatal ovine uterus. Biol Reprod 2001; 64:1236-1246.
13. Tarleton BJ, Wiley AA, Spencer TE, Moss AG, Bartol FF. Ovaryindependent estrogen receptor expression in neonatal porcine endometrium. Biol Reprod 1998; 58:1009-1019.
14. Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M. Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development 2000; 127:4277-4291.
15. Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, Smithies O. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci U S A 1993; 90:11162-11166.
16. Kurita T, Cooke PS, Cunha GR. Epithelial-stromal tissue interaction in paramesonephric (Müllerian) epithelial differentiation. Dev Biol 2001; 240:194-211.
17. Yamashita S, Newbold RR, McLachlan JA, Korach KS. Developmental pattern of estrogen receptor expression in female mouse genital tracts. Endocrinology 1989; 125:2888-2896.
18. Newbold RR, Hanson RB, Jefferson WN. Ontogeny of lactoferrin in the developing mouse uterus: a marker of early hormone response. Biol Reprod 1997; 56:1147-1157.
19. Cunha GR, Shannon JM, Vanderslice KD, Sekkingstad M, Robboy SJ. Autoradiographic analysis of nuclear estrogen binding sites during postnatal development of the genital tract of female mice. J Steroid Biochem 1982; 17:281-286.
20. Quarmby VE, Korach KS. The influence of 17 beta-estradiol on patterns of cell division in the uterus. Endocrinology 1984; 114:694-702.
21. 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.
22. 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.
23. Kurita T, Lee K, Saunders PT, Cooke PS, Taylor JA, Lubahn DB, Zhao C, Mäkelä S, Gustafsson JA, Dahiya R, Cunha GR. Regulation of progesterone receptors and decidualization in uterine stroma of the estrogen receptor-alpha knockout mouse. Biol Reprod 2001; 64:272-283.
24. Bigsby RM, Young PC. Progesterone and dexamethasone inhibition of uterine epithelial cell proliferation: studies with antiprogesterone compounds in the neonatal mouse. J Steroid Biochem Mol Biol 1993; 46: 253-257.
25. Cooke PS, Ekman GC, Kaur J, Davila J, Bagchi IC, Clark SG, Dziuk PJ, Hayashi K, Bartol FF. Brief exposure to progesterone during a critical neonatal window prevents uterine gland formation in mice. Biol Reprod 2012; 86:63.
26. Sridharan S, Simon L, Meling DD, Cyr DG, Gutstein DE, Fishman GI, Guillou F, Cooke PS. Proliferation of adult sertoli cells following conditional knockout of the Gap junctional protein GJA1 (connexin 43) in mice. Biol Reprod 2007; 76:804-812.
27. Jeong JW, Kwak I, Lee KY, Kim TH, Large MJ, Stewart CL, Kaestner KH, Lydon JP, DeMayo FJ. Foxa2 is essential for mouse endometrial gland development and fertility. Biol Reprod 2010; 83:396-403.
28. Filant J, Lydon JP, Spencer TE. Integrated chromatin immunoprecipitation sequencing and microarray analysis identifies FOXA2 target genes in the glands of the mouse uterus. FASEB J 2014; 28:230-243.
29. Stewart CA, Fisher SJ, Wang Y, Stewart MD, Hewitt SC, Rodriguez KF, Korach KS, Behringer RR. Uterine gland formation in mice is a continuous process, requiring the ovary after puberty, but not after parturition. Biol Reprod 2011; 85:954-964.
30. Filant J, Zhou H, Spencer TE. Progesterone inhibits uterine gland development in the neonatal mouse uterus. Biol Reprod 2012; 86(146): 141-149.
31. Sone M, Oyama K, Mohri Y, Hayashi R, Clevers H, Nishimori K. LGR4 expressed in uterine epithelium is necessary for uterine gland development and contributes to decidualization in mice. FASEB J 2013; 27:4917-4928.
32. Yin Y, Huang WW, Lin C, Chen H, MacKenzie A, Ma L. Estrogen suppresses uterine epithelial apoptosis by inducing birc1 expression. Mol Endocrinol 2008; 22:113-125.
33. Ignar-Trowbridge DM, Pimentel M, Parker MG, McLachlan JA, Korach KS. Peptide growth factor cross-talk with the estrogen receptor requires the A/B domain and occurs independently of protein kinase C or estradiol. Endocrinology 1996; 137:1735-1744.
34. Joel PB, Smith J, Sturgill TW, Fisher TL, Blenis J, Lannigan DA. pp90rsk1 regulates estrogen receptor-mediated transcription through phosphorylation of Ser-167. Mol Cell Biol 1998; 18:1978-1984.
35. Kuhara A, Tsuji M, Tsujimura T, Sugihara A, Yamada N, Terada N. Comparison of sensitivities of uterine cells in their proliferation responding to epidermal growth factor and estrogen between neonatal and postneonatal mice. In Vivo 1999; 13:487-491.
36. Aronica SM, Katzenellenbogen BS. Stimulation of estrogen receptormediated transcription and alteration in the phosphorylation state of the rat uterine estrogen receptor by estrogen, cyclic adenosine monophosphate, and insulin-like growth factor-I. Mol Endocrinol 1993; 7:743-752.
37. Catalano S, Mauro L, Marsico S, Giordano C, Rizza P, Rago V, Montanaro D, Maggiolini M, Panno ML, Andó S. Leptin induces, via ERK1/ERK2 signal, functional activation of estrogen receptor alpha in MCF-7 cells. J Biol Chem 2004; 279:19908-19915.
38. Hom YK, Young P, Thomson AA, Cunha GR. Keratinocyte growth factor injected into female mouse neonates stimulates uterine and vaginal epithelial growth. Endocrinology 1998; 139:3772-3779.
39. Masui F, Matsuda M, Mori T. Involvement of keratinocyte growth factor (KGF)-KGF receptor signaling in developmental estrogenization syndrome of mouse vagina. Cell Tissue Res 2004; 318:591-598.
40. Falck L, Forsberg JG. Immunohistochemical studies on the expression and estrogen dependency of EGF and its receptor and C-fos proto-oncogene in the uterus and vagina of normal and neonatally estrogen-treated mice. Anat Rec 1996; 245:459-471.
41. Bossert NL, Nelson KG, Ross KA, Takahashi T, McLachlan JA. Epidermal growth factor binding and receptor distribution in the mouse reproductive tract during development. Dev Biol 1990; 142:75-85.
42. Hu J, Gray CA, Spencer TE. Gene expression profiling of neonatal mouse uterine development. Biol Reprod 2004; 70:1870-1876.
43. Sato T, Wang G, Hardy MP, Kurita T, Cunha GR, Cooke PS. Role of systemic and local IGF-I in the effects of estrogen on growth and epithelial proliferation of mouse uterus. Endocrinology 2002; 143:2673-2679.
44. Pillai SB, Rockwell LC, Sherwood OD, Koos RD. Relaxin stimulates uterine edema via activation of estrogen receptors: blockade of its effects using ICI 182,780, a specific estrogen receptor antagonist. Endocrinology 1999; 140:2426-2429.
45. Yan W, Chen J, Wiley AA, Crean-Harris BD, Bartol FF, Bagnell CA. Relaxin (RLX) and estrogen affect estrogen receptor alpha, vascular endothelial growth factor, and RLX receptor expression in the neonatal porcine uterus and cervix. Reproduction 2008; 135:705-712.
46. Frankshun AL, Ho TY, Reimer DC, Chen J, Lasano S, Steinetz BG, Bartol FF, Bagnell CA. Characterization and biological activity of relaxin in porcine milk. Reproduction 2011; 141:373-380.
47. Curtis SW, Clark J, Myers P, Korach KS. Disruption of estrogen signaling does not prevent progesterone action in the estrogen receptor alpha knockout mouse uterus. Proc Natl Acad Sci U S A 1999; 96:3646-3651.
48. Paria BC, Tan J, Lubahn DB, Dey SK, Das SK. Uterine decidual response occurs in estrogen receptor-alpha-deficient mice. Endocrinology 1999; 140:2704-2710.