Developmental genetics of the female reproductive tract in mammals

Nature Reviews Genetics

Volumn 4, Issue 12, 2003, Pages 969-980

  Kobayashi, Akio ^a   Behringer, Richard R ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

CONGENITAL MALFORMATION; DEVELOPMENTAL GENETICS; DEVELOPMENTAL STAGE; EMBRYOLOGY; EPITHELIUM; EVOLUTION; FEMALE; FEMALE GENITAL SYSTEM; GENE CONTROL; HUMAN; INVERTEBRATE; MAMMAL; MESENCHYME; MOLECULAR GENETICS; MOLECULAR INTERACTION; MUELLERIAN DUCT; NIDATION; NONHUMAN; ORGANOGENESIS; PERINATAL PERIOD; PRIORITY JOURNAL; REVIEW;

ANIMALS; EVOLUTION, MOLECULAR; FEMALE; GENITALIA, FEMALE; MICE; SEX DIFFERENTIATION;

INVERTEBRATA; MAMMALIA;

EID: 0344010195     PISSN: 14710056     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrg1225     Document Type: Review

References (109)

1. Gidwani, G. & Falcone, T. Congenital Malformations of the Female Genital Tract: Diagnosis and Management (Lippincott Williams & Wilkins, Philadelphia, 1999).
2. National Cancer Institute. Surveillance, Epidemiology, and End Results SEER) Program. [online], (cited 8 Oct. 2003), 〈 http://www.seer.cancer.gov〉 (2003).
3. Paria, B. C., Reese, J., Das, S. K. & Dey, S. K. Deciphering the cross-talk of implantation: advances and challenges. Science 296, 2185-2188 (2002).
4. Couse, J. F. & Korach, K. S. Estrogen receptor null mice: what have we learned and where will they lead us? Endocr. Rev. 20, 358-417 (1999).
5. Feldhamer G., Drickamer, L., Vessey, S. & Merritt, J. Mammalogy: Adaptation, Diversity, and Ecology (McGraw-Hill, New York, 2003).
6. Hill, J. E. & Smith, J. D. Bats: a Natural History (Univ. of Texas Press, Austin, 1984).
7. Chi, N. & Epstein, J. A. Getting your Pax straight: Pax proteins in development and disease. Trends Genet. 18, 41-47 (2002).
8. Torres, M., Gomez-Pardo, E., Dressler, G. R. & Gruss, P. Pax-2 controls multiple steps of urogenital development. Development 121, 4057-4065 (1995).
9. Mansouri, A., Chowdhury, K. & Gruss, P. Follicular cells of the thyroid gland require Pax8 gene function. Nature Genet. 19, 87-90 (1998).
10. Bouchard, M., Souabni, A., Mandler, M., Neubuser A. & Busslinger, M. Nephric lineage specification by Pax2 and Pax8. Genes Dev. 16, 2958-2970 (2002).
11. Kobayashi, A., Shawlot, W., Kania, A. & Behringer, R. R. Requirement of Lim1 for female reproductive tract development. Development (in the press). This study describes the visualization of reproductive tract development in embryos and a new chimaera analysis for female organs is used to identify a cell-autonomous requirement of Lim1 in Müllerian duct formation.
12. Miyamoto, N., Yoshida, M., Kuratani, S., Matsuo, I. & Aizawa, S. Defects of urogenital development in mice lacking Emx2. Development 124, 1653-1664 (1997).
13. Mendelsohn, C. et al. Function of the retinoic acid receptors (RARs) during development (II). Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development 120, 2749-2771 (1994).
14. Kastner, P. et al. Genetic evidence that the retinoid signal is transduced by heterodimeric RXR/RAR functional units during mouse development. Development 124, 313-326 (1997).
15. Miller, C., Pavlova, A. & Sassoon, D. A. Differential expression patterns of Writ genes in the murine female reproductive tract during development and the estrous cycle. Mech. Dev. 76, 91-99 (1998).
16. Jeays-Ward, K. et al. Endothelial and steriodogenic cell migration are regulated by WNT4 in the developing mammalian gonad. Development 130, 3663-3670 (2003)
17. Vainio, S., Heikkila, M., Kispert, A., Chin, N. & McMahon, A. P. Female development in mammals is regulated by Wnt-4 signalling. Nature 397, 405-409 (1999). This study identifies the involvement of a Wnt pathway in Müllerian duct formation.
18. Kuure, S., Vuolteenaho, R. & Vainio, S. Kidney morphogenesis: cellular and molecular regulation. Mech. Dev. 92, 31-45 (2000).
19. Vainio, S. & Lin, Y. Coordinating early kidney development: lessons from gene targeting. Nature Rev. Genet 3, 533-543 (2002).
20. Stark, K., Vainio, S., Vassileva, G. & McMahon, A. P. Epithelial transformation of metanephric mesenchyme in the developing kidney regulated by Wnt-4. Nature 372, 679-683 (1994).
21. Rothenpieler, U. W. & Dressler, G. R. Pax-2 is required for mesenchyme-to-epithelium conversion during kidney development. Development 119, 711-720 (1993).
22. Strong, L. C. & Hollander, W. F. Hereditary loop-tail in the house mouse accompanied by inperforate vagina and craniorachischisis when homozygous. J. Hered. 40, 329-334 (1949).
23. Kibar, Z. et al. Ltap, a mammalian homologue of Drosophila Strabismus/ Van Gogh, is altered in the mouse neural tube mutant Loop-tail. Nature Genet. 28, 251-255 (2001).
24. Montcouquiol, M. et al. Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 423, 173-177 (2003).
25. Heisenberg, C. P. & Tada, M. Wnt signalling: a moving picture emerges from van gogh. Curr. Biol. 12, 126-128 (2002).
26. Josso, N. et al. Anti-mullerian hormone: the Jost factor. Recent Prog. Horm. Res. 4B, 1-59 (1993).
27. Behringer, R. R., Finegold, M. J. & Cate, R. L. Mullerian-inhibiting substance function during mammalian sexual development Cell 79, 415-425 (1994). This study provides evidence that MIS is essential for Mullerian duct regression.
28. Behringer, R. R., Cate, R. L., Froelick, G. J., Palmiter, R. D. & Brinster, R. L. Abnormal sexual development in transgenic mice chronically expressing mullerian inhibiting substance. Nature 345, 167-170 (1990).
29. Shen, W. H., Moore, C. C., Ikeda, Y., Parker, K. L. & Ingraham, H. A. Nuclear receptor steroidogenic factor 1 regulates the mullerian inhibiting substance gene: a link to the sex determination cascade. Cell 77, 651-661 (1994).
30. De Santa Barbara, P. et al. Direct interaction of SRY-related protein SOX9 and steroidogenic factor 1 regulates transcription of the human anti-Mullerian hormone gene. Mol. Cell Biol. 18, 6653-6665 (1998).
31. Nachtigal, M. W. et al. Wilms' tumor 1 and Dax-1 modulate the orphan nuclear receptor SF-1 in sex-specific gene expression. Cell 93, 445-454 (1998).
32. Arango, N. A., Lovell-Badge, R. & Behringer, R. R. Targeted mutagenesis of the endogenous mouse Mis gene promoter: in vivo definition of genetic pathways of vertebrate sexual development. Cell 99, 409-419 (1999).
33. Roberts, L. M., Visser, J. A. & Ingraham, H. A. Involvement of a matrix metalloproteinase in MIS-induced cell death during urogenital development. Development 129, 1487-1496 (2002)
34. Dyche, W. J. A comparative study of the differentiation and involution of the Mullerian duct and Wolffian duct in the male and female fetal mouse. J. Morphol. 162, 175-209 (1979).
35. Mishina, Y. et al. Genetic analysis of the Mullerian-inhibiting substance signal transduction pathway in mammalian sexual differentiation. Genes Dev. 10, 2577-2587 (1996).
36. Mishina, Y., Whitworth, D. J., Racine, C. & Behringer, R. R. High specificity of Mullerian-inhibiting substance signaling in vivo. Endocrinology 140, 2084-2088 (1999).
37. Gouedard, L. et al. Engagement of bone morphogenetic protein type IB receptor and Smad1 signaling by anti-Mullerian hormone and its type II receptor. J. Biol. Chem. 275, 27973-27978 (2000).
38. Clarke, T. R. et al. Mullerian inhibiting substance signaling uses a bone morphogenetic protein (BMP)-like pathway mediated by ALK2 and induces SMAD6 expression. Mol. Endocrinol. 15, 946-959 (2001).
39. Visser, J. A. et al. The serine/threonine transmembrane receptor ALK2 mediates Mullerian inhibiting substance signaling. Mol. Endocrinol. 15, 936-945 (2001)
40. Mishina, Y., Suzuki, A., Ueno, N. & Behringer, R. R. Bmpr encodes a type I bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes Dev. 9, 3027-3037 (1995)
41. Jamin, S. P., Arango, N. A., Mishina, Y., Hanks, M. C. & Behringer, R. R. Requirement of Bmpr1a for Mullerian duct regression during male sexual development. Nature Genet. 32, 408-419 (2002).
42. Parr B. A., & McMahon, A. P. Sexually dimorphic development of the mammalian reproductive tract requires Wnt-7a. Nature 395, 707-710 (1998). This study identifies the involvement of a Wnt pathway in Müllerian duct regression: Wnt7a expression in the Müllerian duct epithelium is required for the activation of MIS type II receptor expression in the Müllerian duct mesenchyme.
43. Kawakami, Y., Wada, N., Nishimatsu, S. & Nohno, T. Involvement of frizzled-10 in Wnt-7a signaling during chick limb development. Dev. Growth Differ. 42, 561-569 (2000).
44. Parr, B. A. & McMahon, A. P. Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature 374, 350-353 (1995).
45. Allard, S. et al. Molecular mechanisms of hormone-mediated Mullerian duct regression: involvement of β-catenin. Development 127, 3349-3360 (2000).
46. Itoh, T. et al. Unaltered secretion of β-amyloid precursor protein in gelatinase A (matrix metalloproteinase 2)-deficient mice. J. Biol. Chem. 272, 22389-22392 (1997).
47. Kurita, T., Cooke, P. S. & Cunha, G. R. Epithelial-stromal tissue interaction in paramesonephric (Mullerian) epithelial differentiation. Dev. Biol. 240, 194-211 (2001).
48. Zhao, Y. & Potter, S. S. Functional specificity of the Hoxa13 homeobox. Development 128, 3197-3207 (2001).
49. Branford, W. W., Benson, G. V., Ma, L., Maas, R. L. & Potter, S. S. Characterization of Hoxa-10/Hoxa-11 transheterozygotes reveals functional redundancy and regulatory interactions. Dev. Biol. 224, 373-387 (2000).
50. Taylor, H. S., Vanden Heuvel, G. B. & 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. 57, 1336-1345 (1997).
51. Warot, X., Fromental-Ramain, C., Fraulob, V., Chambon, P. & Dolle, P. 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 (1997).
52. Benson, G. V. et al. Mechanisms of reduced fertility in Hoxa-10 mutant mice: uterine homeosis and loss of maternal Hoxa-10 expression. Development 122, 2687-2696 (1996). This study shows that a Hox gene is involved in patterning the anterior-posterior axis of the female reproductive tract.
53. Miller, C. & Sassoon, D. A. Wnt-7a maintains appropriate uterine patterning during the development of the mouse female reproductive tract. Development 125, 3201-3211 (1998). This paper nicely describes the function of Wnt7a in the differentiation of the oviduct and uterus along both the anterior-posterior and lateral axes.
54. Miller, C., Degenhardt, K. & Sassoon, D. A. Fetal exposure to DES results in de-regulation of Wnt7a during uterine morphogenesis. Nature Genet. 20, 228-230 (1998). This study points to phenotypic similarities between the uterus of Wnt7a-null mutants and those of prenatally DES-treated wild-type animals. The authors show that prenatal DES treatment inhibits Wnt7a expression in the uterine epithelium.
55. Mittendorf, R. Teratogen update: carcinogenesis and teratogenesis associated with exposure to diethastilbestrol (DES) in utero. Teratology 51, 435-445 (1995).
56. Ma, L., Benson, G. V., Lim, H., Dey, S. K. & Maas, R. L. Abdominal B (AbdB) Hoxa genes: regulation in adult uterus by estrogen and progesterone and repression in mullerian duct by the synthetic estrogen diethylstilbestrol (DES). Dev. Biol. 197, 141-154 (1998).
57. Block, K., Kardana, A., Igarashi, P. & Taylor, H. S. In utero diethylstilbestrol (DES) exposure alters Hox gene expression in the developing mullerian system. FASEB J. 14, 1101-1108 (2000).
58. Lindner, T. H. et al. A novel syndrome of diabetes mellitus, renal dysfunction and genital malformation associated with a partial deletion of the pseudo-POU domain of hepatocyte nuclear factor-1β. Hum. Mol. Genet. 8, 2001-2008 (1999).
59. Bingham, C., et al. Solitary functioning kidney and diverse genital tract malformations associated with hepatocyte nuclear factor-1β mutations. Kidney Int. 61, 1243-1251 (2002).
60. Coffinier, C., Barra, J., Babinet, C. & Yaniv, M. Expression of the vHNF1/HNF1β homeoprotein gene during mouse organogenesis. Mech. Dev. 89, 211-213 (1999).
61. Reber, M. & Cereghini, S. Variant hepatocyte nuclear factor 1 expression in the mouse genital tract. Mech. Dev. 100, 75-8 (2001).
62. Bai, Y., Pontoglio, M., Hiesberger, T., Sinclair, A. M. & Igarashi, P. Regulation of kidney-specific Ksp-cadherin gene promoter by hepatocyte nuclear factor-1β. Am. J. Physiol. Renal Physiol. 283, 839-851 (2002)
63. Wertz, K. & Herrmann, B. G. Kidney-specific cadherin (cdh16) is expressed in embryonic kidney, lung, and sex ducts. Mech. Dev. 84, 185-188 (1999).
64. Coffinier C., Thepot, D., Babinet, C., Yaniv, M. & Barra, J. Essential role for the homeoprotein vHNF1/HNF1β in visceral endoderm differentiation. Development 126, 4785-4794 (1999).
65. Barbacci, E. et al. Variant hepatocyte nuclear factor 1 is required for visceral endoderm specification. Development 126, 4795-4805 (1999).
66. Coffinier, C. et al. Bile system morphogenesis defects and liver dysfunction upon targeted deletion of HNF1β. Development 129, 1829-1838 (2002).
67. David, A. et al. Hydrometrecolpos and polydactyly: a common neonatal presentation of Bardet-Biedl and McKusick-Kaufman syndromes. J. Med. Genet. 36, 599-603 (1999)
68. Stone, D. L. et al. Mutation of a gene encoding a putative chaperonin causes McKusick-Kaufman syndrome. Nature Genet. 25, 79-82 (2000).
69. Belville, C., Josso, N. & Picard, J. Y. Persistence of Mullerian derivatives in males. Am. J. Med. Genet. 89, 218-223 (1999).
70. Urioste, M. et al. Persistence of mullerian derivatives, lymphangiectasis, hepatic failure, postaxial polydactyly, renal and craniofacial anomalies. Am. J. Med. Genet. 47, 494-503 (1993).
71. Hummel, K. P. Hypodactyly, a semidominant lethal mutation in mice. J. Hered. 61, 219-220 (1970)
72. Mortlock, D. P., Post, L. C. & Innis, J. W. The molecular basis of hypodactyly (Hd): a deletion in Hoxa 13 leads to arrest of digital arch formation. Nature Genet. 13, 284-289 (1996).
73. Fromental-Ramain, C. et al. Hoxa-13 and Hoxd-13 play a crucial role in the patterning of the limb autopod. Development 122, 2997-3011 (1996).
74. Post, L. C., Margulies, E. H., Kuo, A. & Innis, J. W. Severe limb defects in Hypodactyly mice result from the expression of a novel, mutant HOXA13 protein. Dev. Biol. 217, 290-300 (2000).
75. Mortlock, D. P. & Innis, J. W. Mutation of HOXA13 in hand-foot-genital syndrome. Nature Genet. 15, 179-180 (1997). Identification of the involvement of a HOX gene, HOXA13, in female reproductive-tract development in humans.
76. Wawersik, S. & Maas, R. L. Vertebrate eye development as modeled in Drosophila. Hum. Mol. Genet. 9, 917-925 (2000).
77. Capdevila, J. & Johnson, R. L. Hedgehog signaling in vertebrate and invertebrate limb patterning. Cell. Mol. Life Sci. 57, 1682-1694 (2000).
78. Hirth, F. & Reichert, H. Conserved genetic programs in insect and mammalian brain development. Bioessays 21, 677-684 (1999).
79. Newman, A. P. & Sternberg, P. W. Coordinated morphogenesis of epithelia during development of the Caenorhabditis elegans uterine-vulval connection. Proc. Natl Acad. Sci. USA 93, 9329-9333 (1996).
80. Kornfeld, K. Vulval development in Caenorhabditis elegans. Trends Genet. 13, 55-61 (1997)
81. Newman, A. P., Acton, G. Z., Hartwieg, E., Horvitz, H. R. & Sternberg, P. W. The lin-11 LIM domain transcription factor is necessary for morphogenesis of C. elegans uterine cells. Development 126, 5319-5326 (1999).
82. Chamberlin, H. M. et al. The PAX gene egl-38 mediates developmental patterning in Caenornabditis elegans. Development 124, 3919-3928 (1997).
83. Maloof, J. N. & Kenyon, C. The Hox gene lin-39 is required during C. elegans vulval induction to select the outcome of Ras signaling. Development 125, 181-190 (1998).
84. Gleason, J. E., Korswagen, H. C. & Eisenmann, D. M. Activation of Wnt signaling bypasses the requirement for RTK/Ras signaling during C. elegans vulval induction. Genes Dev. 16, 1281-1290 (2002).
85. Eisenmann, D. M., Maloof, J. N., Simske, J. S., Kenyon, C & Kim, S. K. The β-catenin homologue BAR-1 and LET-60 Ras coordinately regulate the Hox gene lin-39 during Caenorhabditis elegans vulval development. Development 125, 3667-3680 (1998).
86. Hoier, E. F., Mohler, W. A., Kim, S. K. & Hajnal, A. The Caenorhabditis elegans APC-related gene apr-1 is required for epithelial cell migration and Hox gene expression. Genes Dev. 14, 874-886 (2000).
87. Hogan, B. L. & Kolodziej, R. A. Organogenesis: molecular mechanisms of tubulogenesis. Nature Rev. Genet. 3, 513-523 (2002).
88. Lubarsky, B. & Krasnow, M. A. Tube morphogenesis: making and shaping biological tubes. Cell 112, 19-28 (2003).
89. Gruenwald, P. The relation of the growing Mullerian duct to the Wolffian duct and its importance for the genesis of malformations. Anat. Rec. 81, 1-19 (1941).
90. Igarashi, P. et al. Ksp-cadherin gene promoter. II. Kidney-specific activity in transgenic mice. Am. J. Physiol. 277, 599-610 (1999).
91. Shao, X., Somlo, S. & Igarashi, P. Epithelial-specific Cre/lox recombination in the developing kidney and genitourinary tract. J. Am. Soc. Nephrol. 13, 1837-1846 (2002).
92. Shao, X., Johnson, J. E., Richardson, J. A., Hiesberger, T. & Igarashi, P. A minimal Ksp-cadherin promoter linked to a green fluorescent protein reporter gene exhibits tissue-specific expression in the developing kidney and genitourinary tract. J. Am. Soc. Nephrol. 13, 1824-1836 (2002).
93. Nef, S. & Parada, L. F. Hormones in male sexual development. Genes Dev. 14, 3075-3086 (2000). This review nicely describes how male development is regulated by testis-secreted hormones, including testosterone, MIS and Insl3.
94. Forsberg, J. G. Cervicovaginal epithelium: its origin and development. Am. J. Obstet. Gynecol. 115, 1025-1043 (1973).
95. Cunha, G. R. The dual origin of vaginal epithelium. Am. J. Anat. 143, 387-392 (1975).
96. Drews, U., Sulak, O. & Schenck, P. A. Androgens and the development of the vagina. Biol. Reprod. 67, 1353-1359 (2002).
97. Carroll, T. J. & Vize, P. D. Synergism between Pax-8 and lim-1 in embryonic kidney development. Dev. Biol. 214, 46-59 (1999).
98. Roberts, L. M., Hirokawa, Y., Nachtigal, M. W. & Ingraham, H. A. Paracrine-mediated apoptosis in reproductive tract development. Dev. Biol. 208, 110-122 (1999).
99. Zhao, Y. & Potter, S. S. Functional comparison of the Hoxa 4, Hoxa 10, and Hoxa 11 homeoboxes. Dev. Biol. 244, 21-36 (2002).
100. Post, L. C. & Innis, J. W. Infertility in adult hypodactyly mice is associated with hypoplasia of distal reproductive structures. Biol. Reprod. 61, 1402-1408 (1999).
101. Dai, X. et al. The ovo gene required for cuticle formation and oogenesis in flies is involved in hair formation and spermatogenesis in mice. Genes Dev. 12, 3452-3463 (1998).
102. Katsanis, N. et al. Mutations in MKKS cause obesity, retinal dystrophy and renal malformations associated with Bardet-Biedl syndrome. Nature Genet. 28, 67-70 (2000).
103. Slavotinek, A. M. et al. Mutations in MKKS cause Bardet-Biedl syndrome. Nature Genet. 26, 15-16 (2000).
104. Griffin, J. E., Edwards, C., Madden, J. D., Harrod, M. J. & Wilson, J. D. Congenital absence of the vagina. The Mayer-Rokitansky-Kuster-Hauser syndrome. Ann. Intern. Med. 85, 224-236 (1976).
105. Duncan, P. A., Shapiro, L. R., Stangel, J. J., Klein, R. M. & Addonizio, J. C. The MURCS association: Mullerian duct aplasia, renal aplasia, and cervicothoracic somite dysplasia. J. Pediatr. 95, 399-402 (1979).
106. van Haelst, M. M. et al. Lymphangiectasia with persistent Mullerian derivatives: confirmation of autosomal recessive Urioste syndrome. Am J. Med. Genet. 104, 65-68 (2001).
107. Bellini, C. et al. Persistence of Mullerian derivatives and intestinal lymphangiectasis in two newborn brothers: confirmation of the Urioste syndrome. Am. J. Med. Genet. 104, 69-74 (2001).
108. Footz, T. K. et al. Analysis of the cat eye syndrome critical region in humans and the region of conserved synteny in mice: a search for candidate genes at or near the human chromosome 22 pericentromere. Genome Res. 11, 1053-1070 (2001).
109. Fryns, J. P., Moerman, F., Goddeeris, P., Bossuyt, C. & Van den Berghe, H. A new lethal syndrome with cloudy corneae, diaphragmatic defects and distal limb deformities. Hum. Genet. 50, 65-70 (1979).