Chapter 5 Sexual Development of the Soma in the Mouse

Current Topics in Developmental Biology

Volumn 83, Issue , 2008, Pages 151-183

  Maatouk, Danielle M ^a   Capel, Blanche ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ARTICLE; BIOLOGICAL MODEL; CELL DIFFERENTIATION; CYTOLOGY; FEMALE; GENDER AND SEX; GENETICS; GONAD; GROWTH, DEVELOPMENT AND AGING; HUMAN; MALE; METABOLISM; MOUSE; PRENATAL DEVELOPMENT; SEX DIFFERENTIATION; SEXUAL DEVELOPMENT;

ANIMALS; CELL DIFFERENTIATION; FEMALE; GONADS; HUMANS; MALE; MICE; MODELS, BIOLOGICAL; SEX CHARACTERISTICS; SEX DETERMINATION (GENETICS); SEX DIFFERENTIATION; SEXUAL DEVELOPMENT;

EID: 57949115296     PISSN: 00702153     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0070-2153(08)00405-5     Document Type: Review

References (119)

1. Akiyama H., Lyons J.P., Mori-Akiyama Y., Yang X., Zhang R., Zhang Z., Deng J.M., Taketo M.M., Nakamura T., Behringer R.R., McCrea P.D., and de Crombrugghe B. Interactions between Sox9 and beta-catenin control chondrocyte differentiation. Genes Dev. 18 (2004) 1072-1087
2. Albrecht K.H., and Eicher E.M. DNA sequence analysis of Sry alleles (subgenus Mus) implicates misregulation as the cause of C57BL/6J-Y(POS) sex reversal and defines the SRY functional unit. Genetics 147 (1997) 1267-1277
3. Albrecht K.H., and Eicher E.M. Evidence that Sry is expressed in pre-Sertoli cells and Sertoli and granulosa cells have a common precursor. Dev. Biol. 240 (2001) 92-107
4. Bardoni B., Zanaria E., Guioli S., Floridia G., Worley K.C., Tonini G., Ferrante E., Chiumello G., McCabe E.R., Fraccaro M., Zuffardi O., and Camerino G. A dosage sensitive locus at chromosome Xp21 is involved in male to female sex reversal. Nat. Genet. 7 (1994) 497-501
5. Barrionuevo F.J., Zurita F., Burgos M., and Jimenez R. Testis-like development of gonads in female moles. New insights on mammalian gonad organogenesis. Dev. Biol. 268 (2004) 39-52
6. Barsoum I., and Yao H.H. The road to maleness: From testis to Wolffian duct. Trends Endocrinol. Metab. 17 (2006) 223-228
7. Behringer R.R., Finegold M.J., and Cate R.L. Mullerian-inhibiting substance function during mammalian sexual development. Cell 79 (1994) 415-425
8. Bergstrom D.E., Young M., Albrecht K.H., and Eicher E.M. Related function of mouse SOX3, SOX9, and SRY HMG domains assayed by male sex determination. Genesis 28 (2000) 111-124
9. Bouma G.J., Albrecht K.H., Washburn L.L., Recknagel A.K., Churchill G.A., and Eicher E.M. Gonadal sex reversal in mutant Dax1 XY mice: A failure to upregulate Sox9 in pre-Sertoli cells. Development 132 (2005) 3045-3054
10. Braw Tal R., McNatty K.P., Smith P., Heath D.A., Hudson N.L., Phillips D.J., McLeod B.J., and Davis G.H. Ovaries of ewes homozygous for the X-linked Inverdale gene (FecXI) are devoid of secondary and tertiary follicles but contain many abnormal structures. Biol. Reprod. 49 (1993) 895-907
11. Brennan J., and Capel B. One tissue, two fates: Molecular genetic events that underlie testis versus ovary development. Nat. Rev. Genet. 5 (2004) 509-521
12. Brennan J., Tilmann C., and Capel B. Pdgfr-alpha mediates testis cord organization and fetal Leydig cell development in the XY gonad. Genes Dev. 17 (2003) 800-810
13. Bridges C.B. Direct proof through non-disjunction that the sex-linked genes of Drosophila are borne by the X-chromosome. Science 40 (1914) 107-109
14. Britt K.L., and Findlay J.K. Regulation of the phenotype of ovarian somatic cells by estrogen. Mol. Cell Endocrinol. 202 (2003) 11-17
15. Bullejos M., and Koopman P. Spatially dynamic expression of Sry in mouse genital ridges. Dev. Dyn. 221 (2001) 201-205
16. Burgoyne P., and Palmer S. The genetics of XY sex reversal in the mouse and other mammals. Semin. Dev. Biol. 2 (1991) 277-284
17. Burgoyne P., and Palmer S. Cellular Basis of Sex Determination and Sex Reversal in Mammals from Gonadal Development and Function (1992), Raven Press, NY
18. Burgoyne P.S., Thornhill A.R., Boudrean S.K., Darling S.M., Bishop C.E., and Evans E.P. The genetic basis of XX-XY differences present before gonadal sex differentiation in the mouse. Philos. Trans. R. Soc. Lond. B Biol. Sci. 350 (1995) 253-260 discussion 260-261
19. Capel B. The role of Sry in cellular events underlying mammalian sex determination. Curr. Top Dev. Biol. 32 (1996) 1-37
20. Capel B., Rasberry C., Dyson J., Bishop C.E., Simpson E., Vivian N., Lovell-Badge R., Rastan S., and Cattanach B.M. Deletion of Y chromosome sequences located outside the testis determining region can cause XY female sex reversal. Nat. Genet. 5 (1993) 301-307
21. Carruth L.L., Reisert I., and Arnold A.P. Sex chromosome genes directly affect brain sexual differentiation. Nat. Neurosci. 5 (2002) 933-934
22. Chaboissier M.C., Kobayashi A., Vidal V.I., Lutzkendorf S., van de Kant H.J., Wegner M., de Rooij D.G., Behringer R.R., and Schedl A. Functional analysis of Sox8 and Sox9 during sex determination in the mouse. Development 131 (2004) 1891-1901
23. Chassot A.A., Ranc F., Gregoire E.P., Roepers-Gajadien H.L., Taketo M.M., Camerino G., de Rooij D.G., Schedl A., and Chaboissier M.C. Activation of beta-catenin signaling by Rspo1 controls differentiation of the mammalian ovary. Hum. Mol. Genet. 17 (2008) 1264-1277
24. Chiquoine A.D. The identification, origin, and migration of primordial germ cells in the mouse embryo. Anat. Rec. 118 (1954) 135-146
25. Choi Y., and Rajkovic A. Genetics of early mammalian folliculogenesis. Cell Mol. Life Sci. 63 (2006) 579-590
26. Cline T.W., and Meyer B.J. Vive la difference: Males vs females in flies vs worms. Annu. Rev. Genet. 30 (1996) 637-702
27. Cohn M.J. Developmental genetics of the external genitalia. Adv. Exp. Med. Biol. 545 (2004) 149-157
28. Cool J., Carmona F.D., Szucsik J.C., and Capel B. Peritubular myoid cells are not the migrating population required for testis cord formation in the XY gonad. Sex Dev. 2 (2008) 128-133
29. Couse J.F., Hewitt S.C., Bunch D.O., Sar M., Walker V.R., Davis B.J., and Korach K.S. Postnatal sex reversal of the ovaries in mice lacking estrogen receptors alpha and beta. Science 286 (1999) 2328-2331
30. Coveney D., Cool J., Oliver T., and Capel B. Four-dimensional analysis of vascularization during primary development of an organ, the gonad. Proc. Natl. Acad Sci. USA 105 (2008) 7212-7217
31. Crisponi L., Deiana M., Loi A., Chiappe F., Uda M., Amati P., Bisceglia L., Zelante L., Nagaraja R., Porcu S., Ristaldi M.S., Marzella R., et al. The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ptosis/epicanthus inversus syndrome. Nat. Genet. 27 (2001) 159-166
32. Davies W., and Wilkinson L.S. It is not all hormones: Alternative explanations for sexual differentiation of the brain. Brain Res. 1126 (2006) 36-45
33. Davies W., Humby T., Isles A.R., Burgoyne P.S., and Wilkinson L.S. X-monosomy effects on visuospatial attention in mice: A candidate gene and implications for Turner syndrome and attention deficit hyperactivity disorder. Biol. Psychiatry 61 (2007) 1351-1360
34. De Vries G.J., Rissman E.F., Simerly R.B., Yang L.Y., Scordalakes E.M., Auger C.J., Swain A., Lovell-Badge R., Burgoyne P.S., and Arnold A.P. A model system for study of sex chromosome effects on sexually dimorphic neural and behavioral traits. J. Neurosci. 22 (2002) 9005-9014
35. Deutscher E., and Hung-Chang Yao H. Essential roles of mesenchyme-derived beta-catenin in mouse Mullerian duct morphogenesis. Dev. Biol. 307 (2007) 227-236
36. Dewing P., Shi T., Horvath S., and Vilain E. Sexually dimorphic gene expression in mouse brain precedes gonadal differentiation. Brain Res. Mol. Brain Res. 118 (2003) 82-90
37. Dewing P., Chiang C.W., Sinchak K., Sim H., Fernagut P.O., Kelly S., Chesselet M.F., Micevych P.E., Albrecht K.H., Harley V.R., and Vilain E. Direct regulation of adult brain function by the male-specific factor SRY. Curr. Biol. 16 (2006) 415-420
38. DiNapoli L., and Capel B. SRY and the standoff in sex determination. Mol. Endocrinol. 22 (2008) 1-9
39. Eicher E.M., and Washburn L.L. Inherited sex reversal in mice: Identification of a new primary sex-determining gene. J. Exp. Zool. 228 (1983) 297-304
40. Eicher E.M., Beamer W.G., Washburn L.L., and Whitten W.K. A cytogenetic investigation of inherited true hermaphroditism in BALB/cWt mice. Cytogenet. Cell Genet. 28 (1980) 104-115
41. Eicher E.M., Washburn L.L., Whitney III J.B., and Morrow K.E. Mus poschiavinus Y chromosome in the C57BL/6J murine genome causes sex reversal. Science 217 (1982) 535-537
42. Elejalde B.R., Opitz J.M., de Elejalde M.M., Gilbert E.F., Abellera M., Meisner L., Lebel R.R., and Hartigan J.M. Tandem dup (1p) within the short arm of chromosome 1 in a child with ambiguous genitalia and multiple congenital anomalies. Am. J. Med. Genet. 17 (1984) 723-730
43. Foster J.W., Dominguez-Steglich M.A., Guioli S., Kowk G., Weller P.A., Stevanovic M., Weissenbach J., Mansour S., Young I.D., Goodfellow P.N., Brook J.D., and Schafer A.J. Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature 372 (1994) 525-530
44. Grobstein C. Mechanisms of organogenetic tissue interaction. Natl. Cancer Inst. Monogr. 26 (1967) 279-299
45. Gubbay J., Collignon J., Koopman P., Capel B., Economou A., Munsterberg A., Vivian N., Goodfellow P., and Lovell-Badge R. A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nature 346 (1990) 245-250
46. Gubbay J., Vivian N., Economou A., Jackson D., Goodfellow P., and Lovell Badge R. Inverted repeat structure of the Sry locus in mice. Proc. Natl. Acad. Sci. USA 89 (1992) 7953-7957
47. Guigon C.J., and Magre S. Contribution of germ cells to the differentiation and maturation of the ovary: Insights from models of germ cell depletion. Biol. Reprod. 74 (2006) 450-458
48. Guillette Jr. L.J., Pickford D.B., Crain D.A., Rooney A.A., and Percival H.F. Reduction in penis size and plasma testosterone concentrations in juvenile alligators living in a contaminated environment. Gen. Comp. Endocrinol. 101 (1996) 32-42
49. Guioli S., Sekido R., and Lovell-Badge R. The origin of the Mullerian duct in chick and mouse. Dev. Biol. 302 (2007) 389-398
50. Hacker A., Capel B., Goodfellow P., and Lovell-Badge R. Expression of Sry, the mouse sex determining gene. Development 121 (1995) 1603-1614
51. Hawkins J.R., Koopman P., and Berta P. Testis-determining factor and Y-linked sex reversal. Curr. Opin. Genet. Dev. 1 (1991) 30-33
52. Heard E., and Disteche C.M. Dosage compensation in mammals: Fine-tuning the expression of the X chromosome. Genes Dev. 20 (2006) 1848-1867
53. Jacobs P.A., and Strong J.A. A case of human intersexuality having a possible XXY sex-determining mechanism. Nature 183 (1959) 302-303
54. Jeays-Ward K., Hoyle C., Brennan J., Dandonneau M., Alldus G., Capel B., and Swain A. Endothelial and steroidogenic cell migration are regulated by WNT4 in the developing mammalian gonad. Development 130 (2003) 3663-3670
55. Jordan B.K., Mohammed M., Ching S.T., Delot E., Chen X.N., Dewing P., Swain A., Rao P.N., Elejalde B.R., and Vilain E. Up-regulation of WNT-4 signaling and dosage-sensitive sex reversal in humans. Am. J. Hum. Genet. 68 (2001) 1102-1109
56. Josso N., Cate R.L., Picard J.Y., Vigier B., di Clemente N., Wilson C., Imbeaud S., Pepinsky R.B., Guerrier D., Boussin L., Legeai L., and Carre-Eusebe D. Anti-mullerian hormone: The Jost factor. Recent Prog. Horm. Res. 48 (1993) 1-59
57. Jost A. Investigation of hormonal control of genesis of the sex organs in rabbit and notes on certain malformations of the genital apparatus in man. Ginecol. Obstet. Mex. 7 (1952) 477-492
58. Jost A. Hormonal factors in the sex differentiation of the mammalian foetus. Philos. Trans. R. Soc. Lond. B Biol. Sci. 259 (1970) 119-130
59. Karl J., and Capel B. Sertoli cells of the mouse testis originate from the coelomic epithelium. Dev. Biol. 203 (1998) 323-333
60. Kim Y., and Capel B. Balancing the bipotential gonad between alternative organ fates: A new perspective on an old problem. Dev. Dyn. 235 (2006) 2292-2300
61. Kim Y., Kobayashi A., Sekido R., DiNapoli L., Brennan J., Chaboissier M.C., Poulat F., Behringer R.R., Lovell-Badge R., and Capel B. Fgf9 and Wnt4 act as antagonistic signals to regulate mammalian sex determination. PLoS Biol. 4 (2006) e187
62. Koopman P., Munsterberg A., Capel B., Vivian N., and Lovell-Badge R. Expression of a candidate sex-determining gene during mouse testis differentiation. Nature 348 (1990) 450-452
63. Koopman P., Gubbay J., Vivian N., Goodfellow P., and Lovell-Badge R. Male development of chromosomally female mice transgenic for Sry. Nature 351 (1991) 117-121
64. Lovell-Badge R., Canning C., and Sekido R. Sex-determining genes in mice: Building pathways. Novartis Found. Symp. 244 (2002) 4-18 discussion 18-22, 35-42, 253-257
65. Lyon M.F. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190 (1961) 372-373
66. Lyon M.F. Sex chromatin and gene action in the mammalian X-chromosome. Am. J. Hum. Genet. 14 (1962) 135-148
67. Maatouk D.M., DiNapoli L., Alvers A., Parker K.L., Taketo M.M., and Capel B. Stabilization of beta-catenin in XY gonads causes male-to-female sex-reversal. Hum. Mol. Genet. 17 (2008) 2949-2955
68. Markham J.A., Jurgens H.A., Auger C.J., De Vries G.J., Arnold A.P., and Juraska J.M. Sex differences in mouse cortical thickness are independent of the complement of sex chromosomes. Neuroscience 116 (2003) 71-75
69. Martineau J., Nordqvist K., Tilmann C., Lovell-Badge R., and Capel B. Male-specific cell migration into the developing gonad. Curr. Biol. 7 (1997) 958-968
70. Mayer A., Lahr G., Swaab D.F., Pilgrim C., and Reisert I. The Y-chromosomal genes SRY and ZFY are transcribed in adult human brain. Neurogenetics 1 (1998) 281-288
71. Mayer A., Mosler G., Just W., Pilgrim C., and Reisert I. Developmental profile of Sry transcripts in mouse brain. Neurogenetics 3 (2000) 25-30
72. McElreavey K., Vilain E., Abbas N., Herskowitz I., and Fellous M. A regulatory cascade hypothesis for mammalian sex determination: SRY represses a negative regulator of male development. Proc. Natl. Acad. Sci. USA 90 (1993) 3368-3372
73. McLaren A. Somatic and germ-cell sex in mammals. Philos. Trans. R. Soc. Lond. B Biol. Sci. 322 (1988) 3-9
74. McLaren A. Development of the mammalian gonad: The fate of the supporting cell lineage. Bioessays 13 (1991) 151-156
75. Meeks J.J., Weiss J., and Jameson J.L. Dax1 is required for testis determination. Nat. Genet. 34 (2003) 32-33
76. Merchant Larios H., and Coello J. The effect of busulfan on rat primordial germ cells at the ultrastructural level. Cell Differ. 8 (1979) 145-155
77. Merchant-Larios H., and Centeno B. Morphogenesis of the ovary from the sterile W/Wv mouse. Prog. Clin. Biol. Res. 59B (1981) 383-392
78. Morais da Silva S., Hacker A., Harley V., Goodfellow P., Swain A., and Lovell-Badge R. Sox9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nat. Genet. 14 (1996) 62-68
79. Nagamine C.M., Capehart J., Carlisle C., and Chang D. Ovotestes in B6-XXSxr sex-reversed mice. Dev. Biol. 196 (1998) 24-32
80. Nef S., Schaad O., Stallings N.R., Cederroth C.R., Pitetti J.L., Schaer G., Malki S., Dubois-Dauphin M., Boizet-Bonhoure B., Descombes P., Parker K.L., and Vassalli J.D. Gene expression during sex determination reveals a robust female genetic program at the onset of ovarian development. Dev. Biol. 287 (2005) 361-377
81. Orvis G.D., and Behringer R.R. Cellular mechanisms of Mullerian duct formation in the mouse. Dev. Biol. 306 (2007) 493-504
82. Ottolenghi C., Omari S., Garcia-Ortiz J.E., Uda M., Crisponi L., Forabosco A., Pilia G., and Schlessinger D. Foxl2 is required for commitment to ovary differentiation. Hum. Mol. Genet. 14 (2005) 2053-2062
83. Pailhoux E., Vigier B., Chaffaux S., Servel N., Taourit S., Furet J.P., Fellous M., Grosclaude F., Cribiu E.P., Cotinot C., and Vaiman D. A 11.7-kb deletion triggers intersexuality and polledness in goats. Nat. Genet. 29 (2001) 453-458
84. Painter T.S. Further observations on the sex chromosomes of mammals. Science 58 (1923) 247-248
85. Palmer S.J., and Burgoyne P.S. In situ analysis of fetal, prepuberal and adult XX--XY chimaeric mouse testes: Sertoli cells are predominantly, but not exclusively, XY. Development 112 (1991) 265-268
86. Panning B., and Jaenisch R. RNA and the epigenetic regulation of X chromosome inactivation. Cell 93 (1998) 305-308
87. Parma P., Radi O., Vidal V., Chaboissier M.C., Dellambra E., Valentini S., Guerra L., Schedl A., and Camerino G. R-spondin1 is essential in sex determination, skin differentiation and malignancy. Nat. Genet. 38 (2006) 1304-1309
88. Pepling M.E., and Spradling A.C. Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev. Biol. 234 (2001) 339-351
89. Perriton C.L., Powles N., Chiang C., Maconochie M.K., and Cohn M.J. Sonic hedgehog signaling from the urethral epithelium controls external genital development. Dev. Biol. 247 (2002) 26-46
90. Phoenix C.H., Goy R.W., Gerall A.A., and Young W.C. Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 65 (1959) 369-382
91. Qin Y., Kong L.K., Poirier C., Truong C., Overbeek P.A., and Bishop C.E. Long-range activation of Sox9 in Odd Sex (Ods) mice. Hum. Mol. Genet. 13 (2004) 1213-1218
92. Russell D.W., and Wilson J.D. Steroid 5 alpha-reductase: Two genes/two enzymes. Annu. Rev. Biochem. 63 (1994) 25-61
93. Schmahl J., and Capel B. Cell proliferation is necessary for the determination of male fate in the gonad. Dev. Biol. 258 (2003) 264-276
94. Schmahl J., Eicher E.M., Washburn L.L., and Capel B. Sry induces cell proliferation in the mouse gonad. Development 127 (2000) 65-73
95. Schmahl J., Kim Y., Colvin J.S., Ornitz D.M., and Capel B. Fgf9 induces proliferation and nuclear localization of FGFR2 in Sertoli precursors during male sex determination. Development 131 (2004) 3627-3636
96. Scott W.J., and Holson J.F. Weight differences in rat embryos prior to sexual differentiation. J. Embryol. Exp. Morphol. 40 (1977) 259-263
97. Sekido R., Bar I., Narvaez V., Penny G., and Lovell-Badge R. SOX9 is up-regulated by the transient expression of SRY specifically in Sertoli cell precursors. Dev. Biol. 274 (2004) 271-279
98. Sekido R., and Lovell-Badge R. Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453 (2008) 930-934
99. Seller M.J., and Perkins-Cole K.J. Sex difference in mouse embryonic development at neurulation. J. Reprod. Fertil. 79 (1987) 159-161
100. Sinclair A.H., Berta P., Palmer M.S., Hawkins J.R., Griffiths B.L., Smith M.J., Foster J.W., Frischauf A.M., Lovell Badge R., and Goodfellow P.N. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif [see comments]. Nature 346 (1990) 240-244
101. Skinner M.K., Tung P.S., and Fritz I.B. Cooperativity between Sertoli cells and testicular peritubular cells in the production and deposition of extracellular matrix components. J. Cell Biol. 100 (1985) 1941-1947
102. Swain A., Narvaez V., Burgoyne P., Camerino G., and Lovell-Badge R. Dax1 antagonizes Sry action in mammalian sex determination. Nature 391 (1998) 761-767
103. Tilmann C., and Capel B. Mesonephric cell migration induces testis cord formation and Sertoli cell differentiation in the mammalian gonad. Development 126 (1999) 2883-2890
104. Tomizuka K., Horikoshi K., Kitada R., Sugawara Y., Iba Y., Kojima A., Yoshitome A., Yamawaki K., Amagai M., Inoue A., Oshima T., and Kakitani M. R-spondin1 plays an essential role in ovarian development through positively regulating Wnt-4 signaling. Hum. Mol. Genet. 17 (2008) 1278-1291
105. Tung P.S., Skinner M.K., and Fritz I.B. Cooperativity between Sertoli cells and peritubular myoid cells in the formation of the basal lamina in the seminiferous tubule. Ann. N. Y. Acad. Sci. 438 (1984) 435-446
106. Uhlenhaut N.H., and Treier M. Foxl2 function in ovarian development. Mol. Genet. Metab. 88 (2006) 225-234
107. Vainio S., Heikkila M., Kispert A., Chin N., and McMahon A.P. Female development in mammals is regulated by Wnt-4 signalling. Nature 397 (1999) 405-409
108. Vidal V.P., Chaboissier M.C., de Rooij D.G., and Schedl A. Sox9 induces testis development in XX transgenic mice. Nat. Genet. 28 (2001) 216-217
109. Wagner T., Wirth J., Meyer J., Zabel B., Held M., Zimmer J., Pasantes J., Bricarelli F.D., Keutel J., Hustert E., Wolf U., Tommerup N., et al. Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 79 (1994) 1111-1120
110. Welshons W.J., and Russell L.B. The Y-chromosome as the bearer of male determining factors in the mouse. Proc. Natl. Acad. Sci. USA 45 (1959) 560-566
111. Wilhelm D., Martinson F., Bradford S., Wilson M.J., Combes A.N., Beverdam A., Bowles J., Mizusaki H., and Koopman P. Sertoli cell differentiation is induced both cell-autonomously and through prostaglandin signaling during mammalian sex determination. Dev. Biol. 287 (2005) 111-124
112. Wilhelm D., Palmer S., and Koopman P. Sex determination and gonadal development in mammals. Physiol. Rev. 87 (2007) 1-28
113. Witschi E. I. Gonad development and function. Recent Prog. Horm. Res. 6 (1951) 1-27
114. Yamada G., Satoh Y., Baskin L.S., and Cunha G.R. Cellular and molecular mechanisms of development of the external genitalia. Differentiation 71 (2003) 445-460
115. Yamada G., Suzuki K., Haraguchi R., Miyagawa S., Satoh Y., Kamimura M., Nakagata N., Kataoka H., Kuroiwa A., and Chen Y. Molecular genetic cascades for external genitalia formation: An emerging organogenesis program. Dev. Dyn. 235 (2006) 1738-1752
116. Yao H.H., DiNapoli L., and Capel B. Meiotic germ cells antagonize mesonephric cell migration and testis cord formation in mouse gonads. Development 130 (2003) 5895-5902
117. Yao H.H., Matzuk M.M., Jorgez C.J., Menke D.B., Page D.C., Swain A., and Capel B. Follistatin operates downstream of Wnt4 in mammalian ovary organogenesis. Dev. Dyn. 230 (2004) 210-215
118. Yao H.H., Aardema J., and Holthusen K. Sexually dimorphic regulation of inhibin beta B in establishing gonadal vasculature in mice. Biol. Reprod. 74 (2006) 978-983
119. Yoshida S., Sukeno M., and Nabeshima Y. A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science 317 (2007) 1722-1726