Embryology of the uterus

The Endometrium: Molecular, Cellular and Clinical Perspectives, Second Edition

Volumn , Issue , 2008, Pages 1-18

  Kurita, Takeshi ^a   Nakamura, Hisae ^b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b BRITISH COLUMBIA CANCER AGENCY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 77957311347     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (100)

1. Ramsey EM. History. In: Wynn RM, ed. Biology of The Uterus. New York: Plenum Press, 1977: 1-18.
2. Bordemer CW. History of the mammalian oviduct. In: Hafez ESE, Blandau RJ, eds. The Mammalian Oviduct. Chicago, IL: The University of Chicago Press, 1969: 3-26.
3. Sadler TW. Langman’s Medical Embryology. Baltimore, MD: Lippincott, Williams and Wilkins, 2004.
4. Vize PD, Seufert DW, Carroll TJ et al. Model systems for the study of kidney development: use of the pronephros in the analysis of organ induction and patterning. Dev Biol 1997; 188: 189-204.
5. Ludwig KS, Landmann L. Early development of the human mesonephros. Anat Embryol (Berl) 2005; 209: 439-47.
6. Yu J, McMahon AP, Valerius MT. Recent genetic studies of mouse kidney development. Curr Opin Genet Dev 2004; 14: 550-7.
7. Witschi E. Development and differentiation of the uterus. In: Mack HC, ed. Prenatal Life. Detroit: Wayne State University Press, 1970: 11-34.
8. Koff AK. Development of the vagina in the human fetus. Contrib Embryol 1933; 24: 59-91.
9. O’Rahilly R. The embryology and anatomy of the uterus. In: Wynn RM, ed. The Uterus. Baltimore, MD: Williams & Wilkins, 1973: 17-39.
10. Grünwald P. The relation of the growing tip of the Müllerian duct to the Wolffian duct and its importance for the genesis of malformations. Anat Rec 1941; 81: 1-19.
11. Kobayashi A, Kwan KM, Carroll TJ et al. Distinct and sequential tissue-specific activities of the LIM-class homeobox gene Lim1 for tubular morphogenesis during kidney development. Development 2005; 132: 2809-23.
12. Cornish JA, Etkin LD. The formation of the pronephric duct in Xenopus involves recruitment of posterior cells by migrating pronephric duct cells. Dev Biol 1993; 159: 338-45.
13. Yu J, Carroll TJ, McMahon AP. Sonic hedgehog regulates proliferation and differentiation of mesenchymal cells in the mouse metanephric kidney. Development 2002; 129: 5301-12.
14. Jamin SP, Arango NA, Mishina Y et al. Requirement of Bmpr1a for Müllerian duct regression during male sexual development. Nat Genet 2002; 32: 408-10.
15. Lobe CG, Koop KE, Kreppner W et al. Z/AP, a double reporter for cre-mediated recombination. Dev Biol 1999; 208: 281-92.
16. Brennan J, Capel B. One tissue, two fates: molecular genetic events that underlie testis versus ovary development. Nat Rev Genet 2004; 5: 509-21.
17. Roberts LM, Hirokawa Y, Nachtigal MW et al. Paracrinemediated apoptosis in reproductive tract development. Dev Biol 1999; 208: 110-22.
18. Wilson JD, George FW, Griffin JE. The hormonal control of sexual development. Science 1981; 211: 1278-84.
19. Hashimoto R. Development of the human Müllerian duct in the sexually undifferentiated stage. Anat Rec A Discov Mol Cell Evol Biol 2003; 272: 514-19.
20. Forsberg JG. Cervicovaginal epithelium: its origin and development. Am J Obstet Gynecol 1973; 115: 1025-43.
21. Forsberg JG. Derivation and differentiation of the vaginal epithelium. Thesis, Lund, 1963.
22. Ludwig KS. The Mayer-Rokitansky-Kuster syndrome. An analysis of its morphology and embryology. Part II: Embryology. Arch Gynecol Obstet 1998; 262: 27-42.
23. Cunha GR. The dual origin of vaginal epithelium. Am J Anat 1975; 143: 387-92.
24. Quigley CA, De Bellis A, Marschke KB et al. Androgen receptor defects: historical, clinical, and molecular perspectives. Endocr Rev 1995; 16: 271-321.
25. Boutin EL, Battle E, Cunha GR. The germ layer origin of mouse vaginal epithelium restricts its responsiveness to mesenchymal inductors: uterine induction. Differentiation 1992; 49: 101-7.
26. Boutin EL, Cunha GR. Does sinus vaginal epithelium persist in the adult mouse vagina? Dev Dyn 1996; 206: 403-11.
27. Kurita T, Cunha GR, Robboy SJ et al. Differential expression of p63 isoforms in female reproductive organs. Mech Dev 2005; 122: 1043-55.
28. Cunha GR. Epithelio-mesenchymal interactions in primordial gland structures which become responsive to androgenic stimulation. Anat Rec 1972; 172: 179-96.
29. Drews U, Sulak O, Schenck PA. Androgens and the development of the vagina. Biol Reprod 2002; 67: 1353-9.
30. Mauch RB, Thiedemann KU, Drews U. The vagina is formed by downgrowth of Wolffian and Müllerian ducts. Graphical reconstructions from normal and Tfm mouse embryos. Anat Embryol (Berl) 1985; 172: 75-87.
31. Kobayashi A, Shawlot W, Kania A et al. Requirement of Lim1 for female reproductive tract development. Development 2004; 131: 539-49.
32. Vainio S, Heikkila M, Kispert A et al. Female development in mammals is regulated by Wnt-4 signalling. Nature 1999; 397: 405-9.
33. Carroll TJ, Park JS, Hayashi S, Majumdar A, McMahon AP. Wnt9b plays a central role in the regulation of mesenchymal to epithelial transitions underlying organogenesis of the mammalian urogenital system. Dev Cell 2005; 9: 283-92.
34. Torres M, Gomez-Pardo E, Dressler GR et al. Pax-2 controls multiple steps of urogenital development. Development 1995; 121: 4057-65.
35. Miyamoto N, Yoshida M, Kuratani S et al. Defects of urogenital development in mice lacking Emx2. Development 1997; 124: 1653-64.
36. Wilson JG, Warakany J. Malformation in the genitourinary tract induced by maternal vitamin A deficiency in the rat. Am J Anat 1948; 83: 357-408.
37. Mendelsohn C, Lohnes D, Decimo D et al. Function of the retinoic acid receptors (RARs) during development (II). Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development 1994; 120: 2749-71.
38. Kastner P, Mark M, Ghyselinck N et al. Genetic evidence that the retinoid signal is transduced by heterodimeric RXR/RAR functional units during mouse development. Development 1997; 124: 313-26.
39. Marshall H, Morrison A, Studer M, Popperl H, Krumlauf R. Retinoids and Hox genes. FASEB J 1996; 10: 969-78.
40. Ma L, Benson GV, Lim H et al. Abdominal B (AbdB) Hoxa genes: regulation in adult uterus by estrogen and progesterone and repression in Müllerian duct by the synthetic estrogen diethylstilbestrol (DES). Dev Biol 1998; 197: 141-54.
41. Izpisua-Belmonte JC, Dolle P, Renucci A et al. Primary structure and embryonic expression pattern of the mouse Hox-4.3 homeobox gene. Development 1990; 110: 733-45.
42. Warot X, Fromental-Ramain C, Fraulob V et al. Gene dosagedependent effects of the Hoxa-13 and Hoxd-13 mutations on morphogenesis of the terminal parts of the digestive and urogenital tracts. Development 1997; 124: 4781-91.
43. Schnabel CA, Selleri L, Cleary ML. Pbx1 is essential for adrenal development and urogenital differentiation. Genesis 2003; 37: 123-30.
44. Yamaguchi TP, Bradley A, McMahon AP et al. A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 1999; 126: 1211-23.
45. Mericskay M, Kitajewski J, Sassoon D. Wnt5a is required for proper epithelial-mesenchymal interactions in the uterus. Development 2004; 131: 2061-72.
46. Kurita T, Cooke PS, Cunha GR. Epithelial-stromal tissue interaction in paramesonephric (Müllerian) epithelial differentiation. Dev Biol 2001; 240: 194-211.
47. Komatsu M, Fujita H. Electron-microscopic studies on the development and aging of the epithelium of mice. Anat Embryol (Berl) 1978; 152: 243-59.
48. 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.
49. Bigsby RM, Li AX, Luo K et al. Strain differences in the ontogeny of estrogen receptors in murine uterine epithelium. Endocrinology 1990; 126: 2592-6.
50. Valdés-Dapena MA. The development of the uterus in late fetal life, infancy, and childhood. In: Norris HJ, Hertig AT, Abell MR, eds. The Uterus. Baltimore, MD: Williams and Wilkins, 1973.
51. Forsberg JG, Norell K. Differentiation of the epithelium in early grafts of the mouse Müllerian vaginal region. Experientia 1966; 22: 402-4.
52. Kurita T, Mills AA, Cunha GR. Roles of p63 in the diethylstilbestrol- induced cervicovaginal adenosis. Development 2004; 131: 1639-49.
53. Chan Y, Anton-Lamprecht I, Yu QC et al. A human keratin 14 “knockout”: the absence of K14 leads to severe epidermolysis bullosa simplex and a function for an intermediate filament protein. Genes Dev 1994; 8: 2574-87.
54. Rugg EL, McLean WH, Lane EB et al. A functional “knockout” of human keratin 14. Genes Dev 1994; 8: 2563-73.
55. Kurita T, Lee K, Cooke PS et al. Paracrine regulation of epithelial progesterone receptor by estradiol in the mouse female reproductive tract. Biol Reprod 2000; 62: 821-30.
56. Pixley E. Morphology of the fetal and prepubertal cervicovaginal epithelium. In: Jordan JA, Singer A, eds. The Cervix. London: WB Saunders, 1976.
57. Jernvall J, Thesleff I. Reiterative signaling and patterning during mammalian tooth morphogenesis. Mech Dev 2000; 92: 19-29.
58. Shannon JM, Hyatt BA. Epithelial-mesenchymal interactions in the developing lung. Annu Rev Physiol 2004; 66: 625-45.
59. Roberts DJ. Molecular mechanisms of development of the gastrointestinal tract. Dev Dyn 2000; 219: 109-20.
60. Cunha GR. Epithelial-stromal interactions in development of the urogenital tract. Int Rev Cytol 1976; 47: 137-94.
61. Cunha GR. Stromal induction and specification of morphogenesis and cytodifferentiation of the epithelia of the Müllerian ducts and urogenital sinus during development of the uterus and vagina in mice. J Exp Zool 1976; 196: 361-70.
62. Boutin EL, Sanderson RD, Bernfield M et al. Epithelial- mesenchymal interactions in uterus and vagina alter the expression of the cell surface proteoglycan, syndecan. Dev Biol 1991; 148: 63-74.
63. Cunha GR, Young P, Brody JR. Role of uterine epithelium in the development of myometrial smooth muscle cells. Biol Reprod 1989; 40: 861-71.
64. Kurita T, Medina R, Schabel AB et al. The activation function-1 domain of estrogen receptor alpha in uterine stromal cells is required for mouse but not human uterine epithelial response to estrogen. Differentiation 2005; 73: 313-22.
65. Miller C, Pavlova A, Sassoon DA. Differential expression patterns of Wnt genes in the murine female reproductive tract during development and the estrous cycle. Mech Dev 1998; 76: 91-9.
66. Miller C, Sassoon DA. Wnt-7a maintains appropriate uterine patterning during the development of the mouse female reproductive tract. Development 1998; 125: 3201-11.
67. Kmita M, Duboule D. Organizing axes in time and space; 25 years of colinear tinkering. Science 2003; 301: 331-3.
68. Taylor HS, Vanden Heuvel GB, Igarashi P. 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 1997; 57: 1338-45.
69. Benson GV, Lim H, Paria BC et al. Mechanisms of reduced fertility in Hoxa-10 mutant mice: uterine homeosis and loss of maternal Hoxa-10 expression. Development 1996; 122: 2687-96.
70. Zhao Y, Potter SS. Functional specificity of the Hoxa13 homeobox. Development 2001; 128: 3197-207.
71. Parr BA, Avery EJ, Cygan JA et al. The classical mouse mutant postaxial hemimelia results from a mutation in the Wnt 7a gene. Dev Biol 1998; 202: 228-34.
72. Patton PE, Novy MJ, Lee DM et al. The diagnosis and reproductive outcome after surgical treatment of the complete septate uterus, duplicated cervix and vaginal septum. Am J Obstet Gynecol 2004; 190: 1669-78.
73. Propst AM, Hill JA 3rd. Anatomic factors associated with recurrent pregnancy loss. Semin Reprod Med 2000; 18: 341-50.
74. Simpson JL. Genetics of the female reproductive ducts. Am J Med Genet 1999; 89: 224-39.
75. Lin PC, Bhatnagar KP, Nettleton GS et al. Female genital anomalies affecting reproduction. Fertil Steril 2002; 78: 899-915.
76. Acién P, Acién M, Sánchez-Ferrer M. Complex malformations of the female genital tract. New types and revision of classification. Hum Reprod 2004; 19: 2377-84.
77. Fedele L, Bianchi S, Agnoli B et al. Urinary tract anomalies associated with unicornuate uterus. J Urol 1996; 155: 847-8.
78. Duncan PA, Shapiro LR, Stangel JJ et al. The MURCS association: Müllerian duct aplasia, renal aplasia, and cervicothoracic somite dysplasia. J Pediatr 1979; 95: 399-402.
79. Behera M, Couchman G, Walmer D et al. Müllerian agenesis and thrombocytopenia absent radius syndrome: a case report and review of syndromes associated with Müllerian agenesis. Obstet Gynecol Surv 2005; 60: 453-61.
80. Gell JS. Müllerian anomalies. Semin Reprod Med 2003; 21: 375-88.
81. Rock JA, Zacur HA, Dlugi AM et al. Pregnancy success following surgical correction of imperforate hymen and complete transverse vaginal septum. Obstet Gynecol 1982; 59: 448-51.
82. Mortlock DP, Innis JW. Mutation of HOXA13 in hand-footgenital syndrome. Nat Genet 1997; 15: 179-80.
83. Lubahn DB, Moyer JS, Golding TS et al. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci USA 1993; 90: 11162-6.
84. Krege JH, Hodgin JB, Couse JF et al. Generation and reproductive phenotypes of mice lacking estrogen receptor β. Proc Natl Acad Sci USA 1998; 95: 15677-82.
85. Lydon JP, DeMayo FJ, Funk CR et al. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 1995; 9: 2266-78.
86. Couse JF, Curtis SW, Washburn TF et al. Disruption of the mouse oestrogen receptor gene: resulting phenotypes and experimental findings. Biochem Soc Trans 1995; 23: 929-35.
87. Giusti RM, Iwamoto K, Hatch EE. Diethylstilbestrol revisited: a review of the long-term health effects. Ann Intern Med 1995; 122: 778-88.
88. Herbst AL, Ulfelder H, Poskanzer DC. Adenocarcinoma of the vagina. Association of maternal stilbestrol therapy with tumor appearance in young women. N Engl J Med 1971; 284: 878-81.
89. Robboy SJ, Szyfelbein WM, Goellner JR et al. Dysplasia and cytologic findings in 4,589 young women enrolled in diethylstilbestrol- adenosis (DESAD) project. Am J Obstet Gynecol 1981; 140: 579-86.
90. Robboy SJ, Young RH, Welch WR et al. Atypical vaginal adenosis and cervical ectropion. Association with clear cell adenocarcinoma in diethylstilbestrol-exposed offspring. Cancer 1984; 54: 869-75.
91. Forsberg JG. Animal model of human disease: adenosis and clear-cell carcinomas of vagina and cervix. Am J Pathol 1976; 84: 669-72.
92. McLachlan JA, Newbold RR, Bullock BC. Long-term effects on the female mouse genital tract associated with prenatal exposure to diethylstilbestrol. Cancer Res 1980; 40: 3988-99.
93. Plapinger L, Bern HA. Adenosis-like lesions and other cervicovaginal abnormalities in mice treated perinatally with estrogen. J Natl Cancer Inst 1979; 63: 507-18.
94. Newbold RR, McLachlan JA. Vaginal adenosis and adenocarcinoma in mice exposed prenatally or neonatally to diethylstilbestrol. Cancer Res 1982; 42: 2003-11.
95. Couse JF, Dixon D, Yates M et al. Estrogen receptor-alpha knockout mice exhibit resistance to the developmental effects of neonatal diethylstilbestrol exposure on the female reproductive tract. Dev Biol 2001; 238: 224-38.
96. Miller C, Degenhardt K, Sassoon DA. Fetal exposure to DES results in de-regulation of Wnt7a during uterine morphogenesis. Nat Genet 1998; 20: 228-30.
97. Brody JR, Cunha GR. Histologic, morphometric, and immunocytochemical analysis of myometrial development in rats and mice: II. Effects of DES on development. Am J Anat 1989; 186: 21-42.
98. MacGregor SN, Tamura RK, Sabbagha RE et al. Underestimation of gestational age by conventional crown-rump length dating curves. Obstet Gynecol 1987; 70: 344-8.
99. Konishi I, Fujii S, Okamura H et al. Development of smooth muscle in the human fetal uterus: an ultrastructural study. J Anat 1984; 139(Pt 2): 239-52.
100. Sasaki C, Yamaguchi K, Akita K. Spatiotemporal distribution of apoptosis during normal cloacal development in mice. Anat Rec A Discov Mol Cell Evol Biol 2004; 279: 761-7.