Uterine gland formation in mice is a continuous process, requiring the ovary after puberty, but not after parturition

Biology of Reproduction

Volumn 85, Issue 5, 2011, Pages 954-964

  Stewart, C Allison ^a   Fisher, Sara J ^a   Wang, Ying ^a   David Stewart, M ^a,b   Hewitt, Sylvia C ^c   Rodriguez, Karina F ^c   Korach, Kenneth S ^c   Behringer, Richard R ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b University of Houston   (United States)

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

Author keywords

Endometrium; Female reproductive tract; Uterine gland; Uterus

Indexed keywords

BETA CATENIN; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; PROGESTERONE;

ADULTHOOD; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; EMBRYO; ENDOMETRIUM; FEMALE; GONAD DEVELOPMENT; GONAD DYSFUNCTION; HYPOTHALAMUS HYPOPHYSIS GONAD SYSTEM; MOUSE; NEWBORN; NONHUMAN; OVARIECTOMY; OVARY FUNCTION; POSTNATAL DEVELOPMENT; PREPUBERTY; PRIORITY JOURNAL; PUBERTY; PUERPERIUM; UTERINE GLAND FORMATION; UTERUS GROWTH; UTERUS HORN;

ANIMALS; ANIMALS, NEWBORN; BETA CATENIN; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; GENITALIA, FEMALE; MICE; OVARIECTOMY; OVARY; PARTURITION; PROGESTERONE; SEXUAL MATURATION; UTERUS;

MUS;

EID: 81055126920     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.091470     Document Type: Article

References (62)

1. Stewart CL, Kaspar P, Brunet LJ, Bhatt H, Gadi I, Kontgen F, Abbondanzo SJ. Blastocyst implantation depends on maternal expression of leukemia inhibitory factor. Nature 1992; 359:76-79.
2. Zhu LJ, Bagchi MK, Bagchi IC. Attenuation of calcitonin gene expression in pregnant rat uterus leads to a block in embryonic implantation. Endocrinology 1998; 139:330-339.
3. Gray CA, Taylor KM, Ramsey WS, Hill JR, Bazer FW, Bartol FF, Spencer TE. Endometrial glands are required for preimplantation conceptus elongation and survival. Biol Reprod 2001; 64:1608-1613.
4. Hu J, Gray CA, Spencer TE. Gene expression profiling of neonatal mouse uterine development. Biol Reprod 2004; 70:1870-1876.
5. Brody JR, Cunha GR. Histologic, morphometric, and immunocytochemical analysis of myometrial development in rats and mice: I. Normal development. Am J Anat 1989; 186:1-20.
6. Cunha GR. Epithelial-stromal interactions in development of the urogenital tract. Int Rev Cytol 1976; 47:137-194.
7. Yamashita S, Newbold RR, McLachlan JA, Korach KS. The role of the estrogen receptor in uterine epithelial proliferation and cytodifferentiation in neonatal mice. Endocrinology 1990; 127:2456-2463.
8. Kurita T, Young P, Brody JR, Lydon JP, O'Malley BW, Cunha GR. Stromal progesterone receptors mediate the inhibitory effects of progesterone on estrogen-induced uterine epithelial cell deoxyribonucleic acid synthesis. Endocrinology 1998; 139:4708-4713.
9. 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.
10. Franco HL, Dai D, Lee KY, Rubel CA, Roop D, Boerboom D, Jeong JW, Lydon JP, Bagchi IC, Bagchi MK, Demayo FJ. WNT4 is a key regulator of normal postnatal uterine development and progesterone signaling during embryo implantation and decidualization in the mouse. FASEB J 2011; 25:1176-1187.
11. Miller C, Sassoon DA. Wnt-7a maintains appropriate uterine patterning during the development of the mouse female reproductive tract. Development 1998; 125:3201-3211.
12. Mericskay M, Kitajewski J, Sassoon D. Wnt5a is required for proper epithelial-mesenchymal interactions in the uterus. Development 2004; 131:2061-2072.
13. Hayashi K, Yoshioka S, Reardon SN, Rucker EB III, Spencer TE, DeMayo FJ, Lydon JP, MacLean JA II. WNTs in the neonatal mouse uterus: potential regulation of endometrial gland development. Biol Reprod 2011; 84:308-319.
14. Arango NA, Szotek PP, Manganaro TF, Oliva E, Donahoe PK, Teixeira J. Conditional deletion of beta-catenin in the mesenchyme of the developing mouse uterus results in a switch to adipogenesis in the myometrium. Dev Biol 2005; 288:276-283.
15. Jeong JW, Lee HS, Franco HL, Broaddus RR, Taketo MM, Tsai SY, Lydon JP, DeMayo FJ. Beta-catenin mediates glandular formation and dysregulation of beta-catenin induces hyperplasia formation in the murine uterus. Oncogene 2009; 28:31-40.
16. Hernandez Gifford JA, Hunzicker-Dunn ME, Nilson JH. Conditional deletion of beta-catenin mediated by Amhr2cre in mice causes female infertility. Biol Reprod 2009; 80:1282-1292.
17. 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.
18. Gendron RL, Paradis H, Hsieh-Li HM, Lee DW, Potter SS, Markoff E. Abnormal uterine stromal and glandular function associated with maternal reproductive defects in Hoxa-11 null mice. Biol Reprod 1997; 56:1097- 1105.
19. Gonzalez G, Behringer RR. Dicer is required for female reproductive tract development and fertility in the mouse. Mol Reprod Dev 2009; 76:678- 688.
20. Hong X, Luense LJ, McGinnis LK, Nothnick WB, Christenson LK. Dicer1 is essential for female fertility and normal development of the female reproductive system. Endocrinology 2008; 149:6207-6212.
21. 125I]iododeoxyuridine. Endocrinology 1983; 113:582-587.
22. Branham WS, Sheehan DM. Ovarian and adrenal contributions to postnatal growth and differentiation of the rat uterus. Biol Reprod 1995; 53:863-872.
23. Spencer TE, Wiley AA, Bartol FF. Neonatal age and period of estrogen exposure affect porcine uterine growth, morphogenesis, and protein synthesis. Biol Reprod 1993; 48:741-751.
24. Bartol FF, Johnson LL, Floyd JG, Wiley AA, Spencer TE, Buxton DF, Coleman DA. Neonatal exposure to progesterone and estradiol alters uterine morphology and luminal protein content in adult beef heifers. Theriogenology 1995; 43:835-844.
25. Bartol FF, Wiley AA, Coleman DA, Wolfe DF, Riddell MG. Ovine uterine morphogenesis: effects of age and progestin administration and withdrawal on neonatal endometrial development and DNA synthesis. J Anim Sci 1988; 66:3000-3009.
26. 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.
27. Wilson JG. Reproductive capacity of adult female rats treated prepubertally with estrogenic hormone. Anat Rec 1943; 86:341-359.
28. Branham WS, Sheehan DM, Zehr DR, Ridlon E, Nelson CJ. The postnatal ontogeny of rat uterine glands and age-related effects of 17beta-estradiol. Endocrinology 1985; 117:2229-2237.
29. 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.
30. Sananes N, Baulieu EE, Le Goascogne C. Treatment of neonatal rats with progesterone alters the capacity of the uterus to form deciduomata. J Reprod Fertil 1980; 58:271-273.
31. Dohler KD, Wuttke W. Changes with age in levels of serum gonadotropins, prolactin and gonadal steroids in prepubertal male and female rats. Endocrinology 1975; 97:898-907.
32. Salamonsen LA. Tissue injury and repair in the female human reproductive tract. Reproduction 2003; 125:301-311.
33. Gray CA, Stewart MD, Johnson GA, Spencer TE. Postpartum uterine involution in sheep: histoarchitecture and changes in endometrial gene expression. Reproduction 2003; 125:185-198.
34. Jischa S, Walter I, Nowotny N, Palm F, Budik S, Kolodziejek J, Aurich C. Uterine involution and endometrial function in postpartum pony mares. Am J Vet Res 2008; 69:1525-1534.
35. Al-Bassam MA, Thomson RG, O'Donnell L. Normal postpartum involution of the uterus in the dog. Can J Comp Med 1981; 45:217-232. 36. O'Shea JD, Wright PJ. Involution and regeneration of the endometrium following parturition in the ewe. Cell Tissue Res 1984; 236:477-485.
36. Garris DR. Postpartum regeneration of the guinea pig endometrium: relationship to serum estradiol and progesterone concentrations. Anat Rec 1984; 210:41-44.
37. Shimizu K, Takabe S, Hokano M. Correlation between number of placental detachments and amount of postpartum uterine involution in mice. Acta Anat (Basel) 1985; 122:87-90.
38. de Catanzaro D, Muir C, Beaton EA, Jetha M. Noninvasive repeated measurement of urinary progesterone, 17beta-estradiol, and testosterone in developing, cycling, pregnant, and postpartum female mice. Steroids 2004; 69:687-696.
39. 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 2011; 24:4660-4667.
40. Kimura T, Basu SL, Nandi S. Nature of induced persistent vaginal cornification in mice. I. Effect of neonatal treatment with various doses of steroids. J Exp Zool 1967; 165:71-87.
41. Jones LA, Bern HA. Long-term effects of neonatal treatment with progesterone, alone and in combination with estrogen, on the mammary gland and reproductive tract of female BALB/cfC3H mice. Cancer Res 1977; 37:67-75.
42. Gray CA, Bazer FW, Spencer TE. Effects of neonatal progestin exposure on female reproductive tract structure and function in the adult ewe. Biol Reprod 2001; 64:797-804.
43. Deutscher E, Hung-Chang Yao H. Essential roles of mesenchyme-derived beta-catenin in mouse mullerian duct morphogenesis. Dev Biol 2007; 307:227-236.
44. Tanwar PS, Lee HJ, Zhang L, Zukerberg LR, Taketo MM, Rueda BR, Teixeira JM. Constitutive activation of beta-catenin in uterine stroma and smooth muscle leads to the development of mesenchymal tumors in mice. Biol Reprod 2009; 81:545-552.
45. Cunha GR, Chung LW, Shannon JM, Taguchi O, Fujii H. Hormone-induced morphogenesis and growth: role of mesenchymal-epithelial interactions. Recent Prog Horm Res 1983; 39:559-598.
46. 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.
47. Winuthayanon W, Hewitt SC, Orvis GD, Behringer RR, Korach KS. Uterine epithelial estrogen receptor alpha is dispensable for proliferation but essential for complete biological and biochemical responses. Proc Natl Acad Sci U S A 2010; 107:19272-19277.
48. Yamashita S, Newbold RR, McLachlan JA, Korach KS. Developmental pattern of estrogen receptor expression in female mouse genital tracts. Endocrinology 1989; 125:2888-2896.
49. Spencer TE, Stagg AG, Joyce MM, Jenster G, Wood CG, Bazer FW, Wiley AA, Bartol FF. Discovery and characterization of endometrial epithelial messenger ribonucleic acids using the ovine uterine gland knockout model. Endocrinology 1999; 140:4070-4080.
50. Gray CA, Bartol FF, Taylor KM, Wiley AA, Ramsey WS, Ott TL, Bazer FW, Spencer TE. Ovine uterine gland knock-out model: effects of gland ablation on the estrous cycle. Biol Reprod 2000; 62:448-456.
51. Gray CA, Taylor KM, Bazer FW, Spencer TE. Mechanisms regulating norgestomet inhibition of endometrial gland morphogenesis in the neonatal ovine uterus. Mol Reprod Dev 2000; 57:67-78.
52. Carpenter KD, Gray CA, Bryan TM, Welsh TH Jr, Spencer TE. Estrogen and antiestrogen effects on neonatal ovine uterine development. Biol Reprod 2003; 69:708-717.
53. Chen JC, Wiley AA, Ho TY, Frankshun AL, Hord KM, Bartol FF, Bagnell CA. Transient estrogen exposure from birth affects uterine expression of developmental markers in neonatal gilts with lasting consequences in pregnant adults. Reproduction; 139:623-630.
54. Taylor KM, Gray CA, Joyce MM, Stewart MD, Bazer FW, Spencer TE. Neonatal ovine uterine development involves alterations in expression of receptors for estrogen, progesterone, and prolactin. Biol Reprod 2000; 63:1192-1204.
55. Heap RB, Flint AP, Gadsby JG. Role of embryonic signals in the establishment of pregnancy. Br Med Bull 1979; 35:129-135.
56. Stewart MD, Johnson GA, Gray CA, Burghardt RC, Schuler LA, Joyce MM, Bazer FW, Spencer TE. Prolactin receptor and uterine milk protein expression in the ovine endometrium during the estrous cycle and pregnancy. Biol Reprod 2000; 62:1779-1789.
57. Wimsatt WA. New histological observations on the placenta of the sheep. Am J Anat 1950; 87:391-436.
58. Burton GJ, Jaunaiux E. Maternal vascularization of the human placenta: does the embryo develop in a hypoxic environment? Gynecol Obstet Fertil 2001; 29:503-508.
59. Burton GJ, Watson AL, Hempstock J, Skepper JN, Jauniaux E. Uterine glands provide histiotrophic nutrition for the human fetus during the first trimester of pregnancy. J Clin Endocrinol Metab 2002; 87:2954-2959.
60. Slayden OD, Brenner RM. Hormonal regulation and localization of estrogen, progestin and androgen receptors in the endometrium of nonhuman primates: effects of progesterone receptor antagonists. Arch Histol Cytol 2004; 67:393-409.
61. Moutsatsou P, Sekeris CE. Estrogen and progesterone receptors in the endometrium. Ann N Y Acad Sci 1997; 816:99-115.
62. Estrogen and progesterone receptors in the endometrium