Abstract
The mammalian gonad develops within the urogenital ridge as a thickening along the ventromedial cranial area of the mesonephros. In mice, this occurs at day 10.0–10.5 post coitus (dpc) (Byskov 1986; Brennan and Capel 2004; Kim and Capel 2006; Wilhelm et al. 2007; Tang et al. 2008). This thickening results from both the proliferation of the coelomic epithelium and the allocation of cells from the mesonephros (Yao and Capel 2002; Ross and Capel 2005; Cool et al. 2008). At the beginning, the structure of this gonad anlage is identical in XX and XY mice embryos, and either ovary or testis can develop from this bipotential primordium. For testis development, a member of the Sox (Sry-related high-mobility group box) family of transcription factors, SRY (sex-determining region of the Y chromosome; Sry in mice) is expressed as a primary trigger by the supporting cell lineage, the precursor cells to the Sertoli cell lineage (DiNapoli and Capel 2008). Between 11.5 and 12.5 dpc in mice, the following events were established in the XY gonad: increased proliferation of coelomic epithelial cells, migration of cells from the mesonephros, structural organization of the testis cords, appearance of a male-specific coelomic vessel and differentiation of the steroidogenic Leydig cells (Brennan and Capel 2004).
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Adams IR, McLaren A (2002) Sexually dimorphic development of mouse primordial germ cells: switching from oogenesis to spermatogenesis. Development 129:1155–1164
Behringer RR, Finegold MJ, Cate RL (1994) Mullerian inhibiting substanece function during mammalian sexual development. Cell 79:415–425
Bendsen E, Byskov AG, Laursen SB, Larsen H-PE, Andersen CY, Westergaaed LG (2003) Number of germ cells and somatic cells in human fetal testes during the first weeks after sex differentiation. Hum Reprod 18:13–18
Bishop CE, Whitworth DJ, Qin Y, Agoulnik AI, Agoulnik IU, Harison WR, Behringer RR, Oberbeek RA (2000) A transgenic insertion upstream of Sox9 is associated with dominant XX sex reversal in the mouse. Nat Genet 26:490–494
Bitgood MJ, Shen L, McMahon AP (1996) Sertoli cell signaling by Desert hedgehog regulates the male germline. Curr Biol 6:298–304
Bowles J, Knight D, Smith C, Wilhelm D, Richman J, Mamiya S, Yashiro H, Chawengsaksophak K, Wilson MJ, Rossant J, Hamada H, Koopman P (2006) Retinoic signalling determines germ cell fate in mice. Science 312:596–600
Brennan J, Capel B (2004) One tissue, two fates: molecular genetic events that underlie testis versus ovary development. Nat Rev Gen 5:509–521
Brennan J, Karl J, Capel B (2002) Divergent vascular mechanisms downstream of Sry establish the arterial system in the XY gonad. Dev Biol 244:418–428
Brennan J, Tilmannn C, Capel B (2003) Pdgfr- a mediates testis cord organization and fetal Leydig cell development in the XY gonad. Genes Dev 17:800–810
Buehr M, Gu S, McLaren A (1993) Mesonephric contribution to testis differentiation in the fetal mouse, Development 117:273–281
Byskov AG (1986) Differentiation of mammalian embryonic gonad. Phys Rev 66:71–117
Capel B, Albrecht KH, Washburn LL, Eicher EM (1999) Migration of mesonephric cells into mammalian gonad depends on Sry. Mech Dev 84:127–131
Chiquoine AD (1954) The identification, origin, and migration of the primordial germ cells in the mouse embryo. Anat Rec 118:135–146
Colvin JS, Green RP, Schmahl J, Capel B, Ornitz DM (2001) Male-to-female sex reversal in mice lacking fibroblast growth factor 9. Cell 104:875–889
Cool J, Carmona FD, Szucsik JC, Capel B (2008) Peritubular myoid cells are not the migrating population required for testis cord formation in the XY gonad. Sex Dev 2:128–133
Coveney D, Cool J, Capel B (2008) Four-dimensional analysis of vascularization during primary development of an organ, the gonad. Proc Natl Acad Sci USA 105:7212–7217
DiNapoli L, Capel B (2008) SRY and the standoff in sex determination. Mol Endocrinol 22:1–9
DiNapoli L, Batchvarov J, Capel B (2006) FGF9 promotes survival of germ cells in the fetal testis. Development 133:1519–1527
Durcova-Hills G, Adams IR, Barton SC, Surani MA, McLaren A (2006) The role of exogenous fibroblast growth factor-2 on the reprogramming of primordial germ cells into pluripotent stem cells. Stem Cells 24:1441–1449
Ginsburg M, Snow MH, McLaren A (1990) Primordial germ cells in the mouse embryo during gastrulation. Development 110:521–528
He J, Wang Y, Li YL (2007) Fibroblast-like cells derived from gonadal ridges and dorsal mesenteries of human embryos as feeder cells for culture of human embryonic germ cells. J Biomed Sci 14:617–628
Jeanes A, Wilhelm D, Wilson MJ, Bowles J, McClive PJ, Sinclair AH, Koopman P (2005) Evaluation of candidate markers for peritubular myoid cell lineage in the developing mouse testis. R eproduction 130: 509–516
Karl J, Capel B (1998) Sertoli cells of the mouse testis originate from coelomic epithelium. Dev Biol 203:323–333
Kim Y, Capel B (2006) Balancing the bipotential gonad between alternative organ fates: a new perspective on an old problem. Dev Dyn 235:2292–2300
Kim Y, Kobayashi A, Sekido R, DiNapoli L, Brennan J, Chaboissier M-C, Poulat F, Behringer RR, Lovell-Badge R, Capel B (2006) Fgf9 and Wnt4 act as antagonistic signals to regulate mammalian sex determination. PLoS Biol 4(6):e187. doi:10.1371/journal.pbio.0040187
Martineau J, Nordqvist K, Tilmann C, Lovell-Badge R, Capel B (1997) Male-specific cell migration into the developing gonad. Curr Biol 7:958–968
McLaren A (1991) Development of the mammalian gonad: the fate of the supporting lineage. Bioessays 13:151–156
McLaren A (2000) Germ and somatic cell lineages in the developing gonad. Mol Cell Endocrinol 163:3–9
Park SY, Jameson JL (2005) Transcriptional regulation of gonadal development and differentiation . Endocrinology 146:1035–1042
Park SY, Tong M, Jameson JL (2007) Distinct roles for steroidogenic factor 1 and desert hedgehog pathways in fetal and adult Leydig cell development. Endicrinology 148:3704–3710
Ross AJ, Capel B (2005) Signaling at the crossroads of gonad development. Trends Endocrinol Metab 16:19–25
Schmahl J, Eicher EM, Washburn LL, Capel B (2000) Sry induces cell proliferation in the mouse gonad. Development 127:65–73
Sekido R, Lovell-Badge R (2008) Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453:930–934
Shovlin TC, Durcova-Hills G, Surani A, McLaren A (2008) Heterogeneity in imprinted methylation patterns of pluripotent embryonic germ cells derived from pre-migratory mouse germ cells. Dev Biol 313:674–681
Tam PP, Snow MH (1981) Proliferation and migration of primordial germ cells during compensatory growth in mouse embryos. J Embryol Exp Morphol 64:133–147
Tang H, Brennan J, Karl J, Hamada Y, Raetzman L, Capel B (2008) Notch signalling maintains Leydig progenitor cells in the mouse testis. Development 135:3745–3753
Tilmann C, Capel B (1999) Mesonephric cell migration induces testis cord formation and Sertoli cell differentiation in the mammalian gonad. Development 126:2883–2890
Vidal VP, Chaboissier M-C, de Rooij DG, Schedl A (2001) Sox9 induces testis development in XX transgenic mice. Nat Genet 28:216–217
Wilhelm D, Martinson F, Bradford S, Wilson MJ, Combes AN, Beverdam A, Bowles J, Mizusaki H, Koopman P (2005) Sertoli cell differentiation is induced both cell-autonomously and trough prostaglandin signaling during mammalaian sex determination. Dev Biol 287:111–124
Wilhelm D, Palmer S, Koopman P (2007) Sex determination and gonadal development in mammals. Physiol Rev 87:1–28
Wilson MJ, Bowles J, Koopman P (2006) The matricellular protein SPARC is internalized in Sertoli, Leydig, and germ cells during testis differentiation. Mol Reprod Dev 73:531–539
Wright E, Hargrave MR, Christiansen J, Cooper L, Kum J, Evans T, Gangadharan U, Greenfeld A, Koopman R (1995) The Sry-related gene Sox9 is expressed during chondrogenesis in mouse embryos. Nat Genet 9:15–20
Yamazaki Y, Mann MRW, Lee SS, Marh J, McCarrey JR, Yanagomachi R, Bartolomei MS (2003) Reprogramming of primordial germ cells begins before migration into the genital ridge, making these cells inadequate donors for reproductive cloning. Proc Natl Acad Sci USA 100:12207–12212
Yao HH-C, Capel B (2002) Disruption of testis cords by cyclopamine or forskolin reveals independent cellular pathways in testis organogenesis. Dev Biol 246:356–365
Yao HH-C, Whoriskey W, Capel B (2002) Desert Hedgehog/Patched 1 signaling specifies fetal Leydig cell fate in testis organogenesis. Genes Dev 16:1433–1440
Yao HH-C, Aardema J, Holthusen K (2006) Sexually dimorphic regulation of inhibin B in establishing gonatal vasculature in mice. Biol Reprod 74:978–983
McLaren A (1998) Gonad development: assembling the mammalian testis. Curr Biol 8:R175 – R177
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
Copyright information
© 2009 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Davidoff, M.S., Middendorff, R., Müller, D., Holstein, A.F. (2009). Development of the Testis. In: The Neuroendocrine Leydig Cells and their Stem Cell Progenitors, the Pericytes. Advances in Anatomy, Embryology and Cell Biology, vol 205. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-00513-8_6
Download citation
DOI: https://doi.org/10.1007/978-3-642-00513-8_6
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-00512-1
Online ISBN: 978-3-642-00513-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)