Development of the mammalian female reproductive tract

Journal of Biochemistry

Volumn 137, Issue 6, 2005, Pages 677-683

  Yin, Yan ^a   Ma, Liang ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

DES; M llerian duct; Uterine adenogenesis; Uterus; Wollfian duct

Indexed keywords

DIETHYLSTILBESTROL;

CYTOLOGY; DRUG EFFECT; DRUG MECHANISM; EMBRYO DEVELOPMENT; EMBRYONIC STRUCTURES; EMX2 GENE; FEMALE FERTILITY; FEMALE GENITAL SYSTEM; GENE; GENITAL SYSTEM DISEASE; KNOCKOUT MOUSE; LIM1 GENE; MUELLERIAN DUCT; NONHUMAN; OVIDUCT; PAX2 GENE; PHENOTYPE; SEX DIFFERENTIATION; SHORT SURVEY; UTERINE CERVIX; UTERUS; VAGINA; WNT4 GENE;

ANIMALS; BODY PATTERNING; CELL DIFFERENTIATION; DIETHYLSTILBESTROL; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX; GENITALIA, FEMALE; MALE; MICE; MICE, KNOCKOUT; MULLERIAN DUCTS; UTERUS;

MAMMALIA;

EID: 22344444041     PISSN: 0021924X     EISSN: None     Source Type: Journal    
DOI: 10.1093/jb/mvi087     Document Type: Short Survey

References (76)

1. Bard, J.B.L. and Kaufman, M.H. (1999) The Anatomical Basis of Mouse Development, Academic Press, New York
2. Shawlot, W. and Behringer, R.R. (1995) Requirement for Lim1 in head-organizer function. Nature 374, 425-430
3. Kobayashi, A., Shawlot, W., Kania, A., and Behringer, R.R. (2004) Requirement of Lim1 for female reproductive tract development. Development 131, 539-549
4. Treisman, J., Harris, E., and Desplan, C. (1991) The paired box encodes a second DNA-binding domain in the paired homeo domain protein. Genes Dev. 5, 594-604
5. Dahl, E., Koseki, H., and Balling, R. (1997) Pax genes and organogenesis. Bioessays 19, 755-765
6. Torres, M., Gomez-Pardo, E., and Gruss, P. (1996) Pax2 contributes to inner ear patterning and optic nerve trajectory. Development 122, 3381-3391
7. Urbanek, P., Fetka, I., Meisler, M.H., and Busslinger, M. (1997) Cooperation of Pax2 and Pax5 in midbrain and cerebellum development. Proc. Natl Acad. Sci. USA 94, 5703-5708
8. Torres, M., Gomez-Pardo, E., Dressler, G.R., and Gruss, P. (1995) Pax-2 controls multiple steps of urogenital development. Development 121, 4057-4065
9. Miyamoto, N., Yoshida, M., Kuratani, S., Matsuo, I., and Aizawa, S. (1997) Defects of urogenital development in mice lacking Emx2. Development 124, 1653-1664
10. Nelson, W.J. and Nusse, R. (2004) Convergence of Wnt, β-catenin, and cadherin pathways. Science 303, 1483-1487
11. Vainio, S., Heikkila, M., Kispert, A., Chin, N., and McMahon, A.P. (1999) Female development in mammals is regulated by Wnt-4 signalling. Nature 397, 405-409
12. Tsang, T.E., Shawlot, W., Kinder, S.J., Kobayashi, A., Kwan, K.M., Schughart, K., Kania, A., Jessell, T.M., Behringer, R.R., and Tam, P.P. (2000) Lim1 activity is required for intermediate mesoderm differentiation in the mouse embryo. Dev. Biol. 223, 77-90
13. Koopman, P., Gubbay, J., Vivian, N., Goodfellow, P., and Lovell-Badge, R. (1991) Male development of chromosomally female mice transgenic for Sry. Nature 351, 117-121
14. Giese, K., Cox, J., and Grosschedl, R. (1992) The HMG domain of lymphoid enhancer factor 1 bends DNA and facilitates assembly of functional nucleoprotein structures. Cell 69, 185-195
15. Cate, R.L., Mattaliano, R.J., Hession, C., Tizard, R., Farber, N.M., Cheung, A., Ninfa, E.G., Frey, A.Z., Gash, D.J., Chow, E.P., et al. (1986) Isolation of the bovine and human genes for Mullerian inhibiting substance and expression of the human gene in animal cells. Cell 45, 685-698
16. Behringer, R.R., Finegold, M.J., and Cate, R.L. (1994) Mullerian-inhibiting substance function during mammalian sexual development. Cell 79, 415-425
17. Rey, R., Lukas-Croisier, C., Lasala, C., and Bedecarras, P. (2003) AMH/MIS, what we know already about the gene, the protein and its regulation. Mol. Cell. Endocrinol. 211, 21-31
18. Wrana, J.L., Attisano, L., Wieser, R., Ventura, F., and Massague, J. (1994) Mechanism of activation of the TGF-beta receptor. Nature 370, 341-347
19. Baarends, W.M., van Helmond, M.J., Post, M., van der, S.choot, P.J., Hoogerbrugge, J.W., de Winter, J.P., Uilenbroek, J.T., Karels, B., Wilming, L.G., Meijers, J.H., et al. (1994) A novel member of the transmembrane serine/threonine kinase receptor family is specifically expressed in the gonads and in mesenchymal cells adjacent to the mullerian duct. Development 120, 189-197
20. Teixeira, J., He, W.W., Shah, P.C., Morikawa, N., Lee, M.M., Catlin, E.A., Hudson, P.L., Wing, J., Maclaughlin, D.T., and Donahoe, P.K. (1996) Developmental expression of a candidate mullerian inhibiting substance type II receptor. Endocrinology 137, 160-165
21. di Clemente, N., Wilson, C., Faure, E., Boussin, L., Carmillo, P., Tizard, R., Picard, J.Y., Vigier, B., Josso, N., and Cate, R. (1994) Cloning, expression, and alternative splicing of the receptor for anti-Mullerian hormone. Mol. Endocrinol. 8, 1006-1020
22. Mishina, Y., Rey, R., Finegold, M.J., Matzuk, M.M., Josso, N., Cate, R.L., and Behringer, R.R. (1996) Genetic analysis of the Mullerian-inhibiting substance signal transduction pathway in mammalian sexual differentiation. Genes Dev. 10, 2577-2587
23. Imbeaud, S., Faure, E., Lamarre, I., Mattei, M.G., di Clemente, N., Tizard, R., Carre-Eusebe, D., Belville, C., Tragethon, L., Tonkin, C., et al. (1995) Insensitivity to anti-mullerian hormone due to a mutation in the human anti-mullerian hormone receptor. Nat. Genet. 11, 382-388
24. Imbeaud, S., Belville, C., Messika-Zeitoun, L., Rey, R., di Clemente, N., Josso, N., and Picard, J.Y. (1996) A 27 base-pair deletion of the anti-mullerian type II receptor gene is the most common cause of the persistent mullerian duct syndrome. Hum. Mol. Genet. 5, 1269-1277
25. Clarke, T.R., Hoshiya, Y., Yi, S.E., Liu, X., Lyons, K.M., and Donahoe, P.K. (2001) Mullerian inhibiting substance signaling uses a bone morphogenetic protein (BMP)-like pathway mediated by ALK2 and induces SMAD6 expression. Mol. Endocrinol. 15, 946-959
26. Jamin, S.P., Arango, N.A., Mishina, Y., Hanks, M.C., and Behringer, R.R. (2002) Requirement of Bmpr1a for Mullerian duct regression during male sexual development. Nat. Genet. 32, 408-410
27. Roberts, L.M., Visser, J.A., and Ingraham, H.A. (2002) Involvement of a matrix metalloproteinase in MIS-induced cell death during urogenital development. Development 129, 1487-1496
28. Parr, B.A. and McMahon, A.P. (1998) Sexually dimorphic development of the mammalian reproductive tract requires Wnt-7a. Nature 395, 707-710
29. Hossain, A. and Saunders, G.F. (2003) Synergistic cooperation between the beta-catenin signaling pathway and steroidogenic factor 1 in the activation of the Mullerian inhibiting substance type II receptor. J. Biol. Chem. 278, 26511-26516
30. Shen, W.H., Moore, C.C., Ikeda, Y., Parker, K.L., and Ingraham, H.A. (1994) Nuclear receptor steroidogenic factor 1 regulates the mullerian inhibiting substance gene, a link to the sex determination cascade. Cell 77, 651-661
31. Cunha, G.R (1976) Stromal induction and specification of morphogenesis and cytodifferentiation of the epithelia of the Mullerian ducts and urogenital sinus during development of the uterus and vagina in mice. J. Exp. Zool. 196, 361-370
32. Kurita, T., Cooke, P.S., and Cunha, G.R. (2001) Epithelial-stromal tissue interaction in paramesonephric (Mullerian) epithelial differentiation. Dev. Biol. 240, 194-211
33. Kmita, M. and Duboule, D. (2003) Organizing axes in time and space; 25 years of colinear tinkering. Science 301, 331-333
34. Dolle, P., Izpisua-Belmonte, J.C., Brown, J.M., Tickle, C., and Duboule, D. (1991) HOX-4 genes and the morphogenesis of mammalian genitalia. Genes Dev. 5, 1767-1767
35. Taylor, H.S., Vanden Heuvel, G.B., and Igarashi, P. (1997) A conserved Hox axis in the mouse and human female reproductive system, late establishment and persistent adult expression of the Hoxa cluster genes. Biol. Reprod. 57, 1338-4135
36. Benson, G.V., Lim, H., Paria, B.C., Satokata, I., Dey, S.K., and Maas, R.L. (1996) Mechanisms of reduced fertility in Hoxa-10 mutant mice, uterine homeosis and loss of maternal Hoxa-10 expression. Development 122, 2687-2696
37. Warot, X., Fromental-Ramain, C., Fraulob, V., Chambon, P., and Dolle, P. (1997) Gene dosage-dependent effects of the Hoxa-13 and Hoxd-13 mutations on morphogenesis of the terminal parts of the digestive and urogenital tracts. Development 124, 4781-4791
38. Zhao, Y. and Potter, S.S. (2001) Functional specificity of the Hoxa13 homeobox. Development 128, 3197-3207
39. Kurita, T., Mills, A.A., and Cunha, G.R. (2004) Roles of p63 in the diethylstilbestrol-induced cervicovaginal adenosis. Development 131, 1639-1649
40. Miller, C. and Sassoon, D.A. (1998) Wnt-7a maintains appropriate uterine patterning during the development of the mouse female reproductive tract. Development 125, 3201-3211
41. Mericskay, M., Kitajewski, J., and Sassoon, D. (2004) Wnt5a is required for proper epithelial-mesenchymal interactions in the uterus. Development 131, 2061-2072
42. Gray, C.A., Bartol, F.F., Tarleton, B.J., Wiley, A.A., Johnson, G.A., Bazer, F.W., and Spencer, T.E. (2001) Developmental biology of uterine glands. Biol. Reprod. 65, 1311-1323
43. Bartol, F.F., Wiley, A.A., Floyd, J.G., Ott, T.L., Bazer, F.W., Gray, C.A., and Spencer, T.E. (1999) Uterine differentiation as a foundation for subsequent fertility. J. Reprod. Fertil. Suppl. 54, 287-302
44. Zhu, L.J., Bagchi, M.K., and Bagchi, I.C. (1998) Attenuation of calcitonin gene expression in pregnant rat uterus leads to a block in embryonic implantation. Endocrinology 139, 330-339
45. Chen, J.R., Cheng, J.G., Shatzer, T., Sewell, L., Hernandez, L., and Stewart, C.L. (2000) Leukemia inhibitory factor can substitute for nidatory estrogen and is essential to inducing a receptive uterus for implantation but is not essential for subsequent embryogenesis. Endocrinology 141, 4365-4372
46. Zhou, H.E., Zhang, X., and Nothnick, W.B. (2004) Disruption of the TIMP-1 gene product is associated with accelerated endometrial gland formation during early postnatal uterine development. Biol. Reprod. 71, 534-539
47. Kheradmand, F., Rishi, K., and Werb, Z. (2002) Signaling through the EGF receptor controls lung morphogenesis in part by regulating MT1-MMP-mediated activation of gelatinase A/MMP2. J. Cell Sci. 115, 839-848
48. Simian, M., Hirai, Y., Navre, M., Werb, Z., Lochter, A., and Bissell, M.J. (2001) The interplay of matrix metalloproteinases, morphogens and growth factors is necessary for branching of mammary epithelial cells. Development 128, 3117-3131
49. Hu, J., Zhang, X., Nothnick, W.B., and Spencer, T.E. (2004) Matrix metalloproteinases and their tissue inhibitors in the developing neonatal mouse uterus. Biol. Reprod. 71, 1598-1604
50. Hulboy, D.L., Rudolph, L.A., and Matrisian, L.M. (1997) Matrix metalloproteinases as mediators of reproductive function. Mol. Hum. Reprod. 3, 27-45
51. Jones, J.I. and Clemmons, D.R. (1995) Insulin-like growth factors and their binding proteins, biological actions. Endocr. Rev. 16, 3-34
52. Gu, Y., Branham, W.S., Sheehan, D.M., Webb, P.J., Moland, C.L., and Streck, R.D. (1999) Tissue-specific expression of messenger ribonucleic acids for insulin-like growth factors and insulin-like growth factor-binding proteins during perinatal development of the rat uterus. Biol. Reprod. 60, 1172-1182
53. Baker, J., Hardy, M.P., Zhou, J., Bondy, C., Lupu, F., Bellve, A.R., and Efstratiadis, A. (1996) Effects of an Igf1 gene null mutation on mouse reproduction. Mol. Endocrinol. 10, 903-918
54. Taylor, K.M., Chen, C., Gray, C.A., Bazer, F.W., and Spencer, T.E. (2001) 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. 64, 1236-1246
55. Tarleton, B.J., Wiley, A.A., Spencer, T.E., Moss, A.G., and Bartol, F.F. (1998) Ovary-independent estrogen receptor expression in neonatal porcine endometrium. Biol. Reprod. 58, 1009-1019
56. Bartol, F.F., Wiley, A.A., Coleman, D.A., Wolfe, D.F., and Riddell, M.G. (1988) Ovine uterine morphogenesis, effects of age and progestin administration and withdrawal on neonatal endometrial development and DNA synthesis. J. Anim. Sci. 66, 3000-3009
57. Branham, W.S. and Sheehan, D.M. (1995) Ovarian and adrenal contributions to postnatal growth and differentiation of the rat uterus. Biol. Reprod. 53, 863-872
58. Allison, G.C., Bartol, F.F., Taylor, K.M., Wiley, A.A., Ramsey, W.S., Ott, T.L., Bazer, F.W., and Spencer, T.E. (2000) Ovine uterine gland knock-out model, effects of gland ablation on the estrous cycle. Biol. Reprod. 62, 448-456
59. Bartol, F.F., Wiley, A.A., Spencer, T.E., Ing, N.H., Ott, T.L., and Bazer, F.W. (1997) Progestin Exposure from birth, Epitenetic induction of a unique adult uterine phenotype in sheep-a glandless endometrium. Biol. Reprod. 56, 133
60. Tarleton, B.J., Wiley, A.A., and Bartol, F.F. (1999) Endometrial development and adenogenesis in the neonatal pig, effects of estradiol valerate and the antiestrogen ICI 182,780. Biol. Reprod. 61, 253-263
61. Curtis, S.W., Clark, J., Myers, P., and Korach, K.S. (1999) Disruption of estrogen signaling does not prevent progesterone action in the estrogen receptor alpha knockout mouse uterus. Proc. Natl Acad. Sci. USA 96, 3646-3651
62. Lubahn, D.B., Moyer, J.S., Golding, T.S., Couse, J.F., Korach, K.S., and Smithies, O. (1993) Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc. Natl Acad. Sci. USA 90, 11162-11166
63. Taylor, K.M., Gray, C.A., Joyce, M.M., Stewart, M.D., Bazer, F.W., and Spencer, T.E. (2000) Neonatal ovine uterine development involves alterations in expression of receptors for estrogen, progesterone, and prolactin. Biol. Reprod. 63, 1192-1204
64. Carpenter, K.D., Gray, C.A., Noel, S., Gertler, A., Bazer, F.W., and Spencer, T.E. (2003) Prolactin regulation of neonatal ovine uterine gland morphogenesis. Endocrinology 144, 110-120
65. Schwertfeger, K.L., Hunter, S., Heasley, L.E., Levresse, V., Leon, R.P., DeGregori, J., and Anderson, S.M. (2000) Prolactin stimulates activation of c-jun N-terminal kinase (JNK). Mol. Endocrinol. 14, 1592-1602
66. Gubbay, O., Critchley, H.O., Bowen, J.M., King, A., and Jabbour, H.N. (2002) Prolactin induces ERK phosphorylation in epithelial and CD56(+) natural killer cells of the human endometrium. J. Clin. Endocrinol. Metab. 87, 2329-2335
67. Mittendorf, R. (1995) Teratogen update, carcinogenesis and teratogenesis associated with exposure to diethylstilbestrol (DES) in utero. Teratology 51, 435-445
68. Herbst, A.L., Ulfelder, H., and Poskanzer, D.C. (1971) Adenocarcinoma of the vagina. Association of maternal stilbestrol therapy with tumor appearance in young women. N. Engl. J. Med. 284, 878-881
69. Haney, A.F., Hammond, C.B., Soules, M.R., and Creasman, W.T. (1979) Diethylstilbestrol-induced upper genital tract abnormalities. Fertil. Steril. 31, 142-146
70. Noller, K.L., O'Brien, P.C., Colton, T., Kaufman, R., and Melton, L.J. (1990) Medical and surgical diseases associated with in utero exposure to diethylstilbestrol in Clinical Practice of Gynecology (Noller, L.L., ed.) pp. 1-7, Elsevier Science Publishing, New York
71. Korach, K.S., Chae, K., Levy, L.A., Duax, W.L., and Sarver, P.J. (1989) Diethylstilbestrol metabolites and analogs. Stereochemical probes for the estrogen receptor binding site. J. Biol. Chem. 264, 5642-5647
72. Newbold, R.R. and McLachlan, J.A. (1982) Vaginal adenosis and adenocarcinoma in mice exposed prenatally or neonatally to diethylstilbestrol. Cancer Res. 42, 2003-2011
73. Huang, W.W., Yin, Y., Bi, Q., Chiang, T.C., Garner, N., Vuoristo, J., McLachlan, J.A., and Ma, L. (2004) Developmental diethylstilbestrol (DES) exposure alters genetic pathways of uterine cytodifferentiation. Mol. Endocrinol. In press
74. Gendron, R.L., Paradis, H., Hsieh-Li, H.M., Lee, D.W., Potter, S.S., and Markoff, E. (1997) Abnormal uterine stromal and glandular function associated with maternal reproductive defects in Hoxa-11 null mice. Biol. Reprod. 56, 1097-1105
75. Hsieh-Li, H.M., Witte, D.P., Weinstein, M., Branford, W., Li, H., Small, K., and Potter, S.S. (1995) Hoxa 11 structure, extensive antisense transcription, and function in male and female fertility. Development 121, 1373-1385
76. Ince, T.A., Cviko, A.P., Quade, B.J., Yang, A., McKeon, F.D., Mutter, G.L., and Crum, C.P. (2002) p63 Coordinates anogenital modeling and epithelial cell differentiation in the developing female urogenital tract. Amer. J. Pathol. 161, 1111-1117