Abstract
The earliest manifestation of gonadogenesis in vertebrates is the formation of the genital ridges. The genital ridges form through the transformation of monolayer coelomic epithelium into a cluster of somatic cells. This process depends on increased proliferation of coelomic epithelium and disintegration of its basement membrane, which is foreshadowed by the expression of series of regulatory genes. The earliest expressed gene is Gata4, followed by Sf1, Lhx9, Emx2, and Cbx2. The early genital ridge is a mass of somatic SF1-positive cells (gonadal precursor cells) that derive from proliferating coelomic epithelium. Primordial germ cells (PGCs) immigrate to the coelomic epithelium even in the absence of genital ridges, e.g., in mouse null mutants for Gata4. And conversely, the PGCs are not required for the formation of the genital ridges. After reaching genital ridges, the PGCs become enclosed by somatic cells derived from coelomic epithelium. Subsequently, the expression of sex-determining genes begins and the bipotential gonads differentiate into either testes or ovaries. Gonadal precursor cells, derived from coelomic epithelium, give rise to the somatic supporting cells such as Sertoli cells, follicular cells, and probably also peritubular myoid and steroidogenic cells.
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References
Albrecht KH, Eicher EM (2001) Evidence that Sry is expressed in pre-Sertoli cells and Sertoli and granulosa cells have a common precursor. Dev Biol 240:92–107
Bandiera R, Vidal VPI, Motamedi FJ (2013) WT1 maintains adrenal-gonadal primordium identity and marks a population of AGP-like progenitors within the adrenal gland. Dev Cell 27:5–18
Barske LA, Capel B (2010) Estrogen represses SOX9 during sex determination in the red-eared slider turtle Trachemys scripta. Dev Biol 341:305–314
Barsoum IB, Kaur J, Ge RS, Cooke PS, Yao HH (2013) Dynamic changes in fetal Leydig cell populations influence adult Leydig cell populations in mice. FASEB J 27:2657–2666
Birk OS, Casiano DE, Wassif CA, Cogliati T, Zhao L, Grinberg A, Huang S, Kreidberg JA, Parker KL, Porter FD, Westphal H (2000) The LIM homeobox gene Lhx9 is essential for mouse gonad formation. Nature 403:909–913
Bland ML, Fowkes RC, Ingraham HA (2004) Differential requirement for steroidogenic factor-1 gene dosage in adrenal development versus endocrine function. Mol Endocrinol 18:941–952
Brambell FWR (1927) The development and morphology of the gonads of the mouse—Part I. The morphogenesis of the indifferent gonad and of the ovary. Proc R Soc Lond B Biol Sci 101:391–409
Brennan J, Tilmann C, Capel B (2003) Pdgfr-α 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
Capel B, Albrecht KH, Washburn LL, Eicher EM (1999) Migration of mesonephric cells into the mammalian gonad depends on Sry. Mech Dev 84:127–131
Chen H, Palmer JS, Thiagarajan RD, Dinger ME, Lesieur E, Chiu H, Schulz A, Spiller C, Grimmond SM, Little MH, Koopman P, Wilhelm D (2012) Identification of novel markers of mouse fetal ovary development. PLoS One 7(7):e41683
Combes AN, Wilhelm D, Davidson T, Dejana E, Harley V, Sinclair A, Koopman P (2009) Endothelial cell migration directs testis cord formation. Dev Biol 326:112–120
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
Cui S, Ross A, Stallings N, Parker KL, Capel B, Quaggin SE (2004) Disrupted gonadogenesis and male-to-female sex reversal in Pod1 knockout mice. Development 131:4095–4105
Doitsidou M, Reichman-Fried M, Stebler J, Koprunner M, Dorries J, Meyer D, Esguerra CV, Leung T, Raz E (2002) Guidance of primordial germ cell migration by the chemokine SDF-1. Cell 111:647–659
Falconi R, Dalpiaz D, Zaccanti F (2004) Ultrastructural aspects of gonadal morphogenesis in Bufo bufo (Amphibia Anura) 1. Sex differentiation. J Exp Zool A 301:378–388
Flesken-Nikitin A, Hwang CI, Cheng CY, Michurina TV, Enikolopov G, Nikitin AY (2013) Ovarian surface epithelium at the junction area contains a cancer-prone stem cell niche. Nature 495:241–245
Francavilla S, Cordeschi G, Properzi G, Concordia N, Cappa F, Pozzi V (1990) Ultrastructure of fetal human gonad before sexual differentiation and during early testicular and ovarian development. J Submicrosc Cytol Pathol 22:389–400
Fujimoto Y, Tanaka SS, Yamaguchi YL, Kobayashi H, Kuroki S, Tachibana M, Shinomura M, Kanai Y, Morohashi K, Kawakami K, Nishinakamura R (2013) Homeoproteins Six1 and Six4 regulate male sex determination and mouse gonadal development. Dev Cell 26:416–430
Gomperts M, Wylie C, Heasman J (1994) Primordial germ cell migration. Ciba Found Symp 182:121–134
Gropp A, Ohno S (1966) The presence of a common embryonic blastema for ovarian and testicular parenchymal (follicular, interstitial and tubular) cells in cattle Bos taurus. Z Zellforsch Mikrosk Anat 74:505–528
Hacker A, Capel B, Goodfellow P, Lovell-Badge R (1995) Expression of Sry, the mouse sex determining gene. Development 121:1603–1614
Hammes A, Guo JK, Lutsch G, Leheste JR, Landrock D, Ziegler U, Gubler MC, Schedl A (2001) Two splice variants of the Wilms’ tumor 1 gene have distinct functions during sex determination and nephron formation. Cell 106:319–329
Hatano O, Takakusu A, Nomura M, Morohashi K (1994) Identical origin of adrenal cortex and gonad revealed by expression profiles of Ad4BP/SF-1. Genes Cells 1:663–671
Hsieh-Li HM, Witte DP, Weinstein M, Branford W, Li H, Small K, Potter SS (1995) Hoxa 11 structure, extensive antisense transcription, and function in male and female fertility. Development 121:1373–1385
Hu YC, Okumura LM, Page DC (2013) Gata4 is required for formation of the genital ridge in mice. PLoS Genet 9(7):e1003629
Hummitzsch K, Irving-Rodgers HF, Hatzirodos N et al (2013) A new model of development of the mammalian ovary and follicles. PLoS ONE 8(2), e55578
Ikeda Y (1996) SF-1: a key regulator of development and function in the mammalian reproductive system. Acta Paediatr Jpn 38:412–419
Ikeda Y, Shen WH, Ingraham HA, Parker KL (1994) Developmental expression of mouse steroidogenic factor-1, an essential regulator of the steroid hydroxylases. Mol Endocrinol 8:654–662
Iwasawa H, Yamaguchi K (1984) Ultrastructural study of gonadal development in Xenopus laevis. Zool Sci 1:591–600
Karl J, Capel B (1995) Three-dimensional structure of the developing mouse genital ridge. Philos Trans R Soc Lond B Biol Sci 350:235–242
Karl J, Capel B (1998) Sertoli cells of the mouse testis originate from the coelomic epithelium. Dev Biol 203:323–333
Katoh-Fukui Y, Miyabayashi K, Komatsu T, Owaki A, Baba T, Shima Y, Kidokoro T, Kanai Y, Schedl A, Wilhelm D, Koopman P, Okuno Y, Morohashi K (2012) Cbx2, a polycomb group gene, is required for Sry gene expression in mice. Endocrinology 153:913–924
Kawano K, Furusawa S, Matsuda H, Takase M, Nakamura M (2001) Expression of steroidogenic factor-1 in frog embryo and developing gonad. Gen Comp Endocrinol 123:13–22
Kent J, Coriat AM, Sharpe PT, Hastie ND, van Heyningen V (1995) The evolution of WT1 sequence and expression pattern in the vertebrates. Oncogene 11:1781–1792
Kim Y, Bingham N, Sekido R, Parker KL, Lovell-Badge R, Capel B (2007) Fibroblast growth factor receptor 2 regulates proliferation and Sertoli differentiation during male sex determination. Proc Natl Acad Sci U S A 104:16558–16563
Kreidberg JA, Sariola H, Loring JM, Maeda M, Pelletier J, Housman D, Jaenisch R (1993) WT-1 is required for early kidney development. Cell 74:679–691
Kusaka M, Katoh-Fukui Y, Ogawa H, Miyabayashi K, Baba T, Shima Y, Sugiyama N, Sugimoto Y, Okuno Y, Kodama R, Iizuka-Kogo A, Senda T, Sasaoka T, Kitamura K, Aizawa S, Morohashi K (2010) Abnormal epithelial cell polarity and ectopic epidermal growth factor receptor (EGFR) expression induced in Emx2 KO embryonic gonads. Endocrinology 151:5893–5904
Li J, Chen W, Wang D, Zhou L, Sakai F et al (2012) GATA4 is involved in the gonadal development and maturation of the teleost fish tilapia, Oreochromis niloticus. J Reprod Dev 58:237–242
Liu C, Peng J, Matzuk MM, Yao HH (2015) Lineage specification of ovarian theca cells requires multicellular interactions via oocyte and granulosa cells. Nat Commun 6:6934
Luo X, Ikeda Y, Parker KL (1994) A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell 77:481–490
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
Mazaud S, Oreal E, Guigon CJ, Carre-Eusebe D, Magre S (2002) Lhx9 expression during gonadal morphogenesis as related to the state of cell differentiation. Gene Expr Patterns 2:373–377
McLaren A (1991) Development of the mammalian gonad: the fate of the supporting cell lineage. Bioessays 13:151–156
Merchant-Larios H (1979) Origin of the somatic cells in the rat gonad: an autoradiographic approach. Ann Biol Anim Biochim Biophys 19:1219–1229
Merchant-Larios H, Villalpando I (1981) Ultrastructural events during early gonadal development in Rana pipiens and Xenopus laevis. Anat Rec 199:349–360
Merchant-Larios H, Moreno-Mendoza N, Buehr M (1993) The role of the mesonephros in cell differentiation and morphogenesis of the mouse fetal testis. Int J Dev Biol 37:407–415
Miyamoto N, Yoshida M, Kuratani S, Matsuo I, Aizawa S (1997) Defects of urogenital development in mice lacking Emx2. Development 124:1653–1664
Miyamoto Y, Taniguchi H, Hamel F, Silversides DW, Viger RS (2008) A GATA4/WT1 cooperation regulates transcription of genes required for mammalian sex determination and differentiation. BMC Mol Biol 9:44
Molyneaux KA, Stallock J, Schaible K, Wylie C (2001) Time-lapse analysis of living mouse germ cell migration. Dev Biol 240:488–498
Molyneaux KA, Zinszner H, Kunwar PS, Schaible K, Stebler J, Sunshine MJ, O’Brien W, Raz E, Littman D, Wylie C, Lehmann R (2003) The chemokine SDF1/CXCL12 and its receptor CXCR4 regulate mouse germ cell migration and survival. Development 130:4279–4286
Mork L, Maatouk DM, McMahon JA, Guo JJ, Zhang P, McMahon AP, Capel B (2012) Temporal differences in granulosa cell specification in the ovary reflect distinct follicle fates in mice. Biol Reprod 86:37
Nef S, Parada LF (2000) Hormones in male sexual development. Genes Dev 14:3075–3086
Oreal E, Mazaud S, Picard JY, Magre S, Carre-Eusebe D (2002) Different patterns of anti-Mullerian hormone expression, as related to DMRT1, SF-1, WT1, GATA-4, Wnt-4, and Lhx9 expression, in the chick differentiating gonads. Dev Dyn 225:221–232
Paranko J (1987) Expression of type I and III collagen during morphogenesis of fetal rat testis and ovary. Anat Rec 219:91–101
Pelliniemi LJ (1975) Ultrastructure of gonadal ridge in male and female pig embryos. Anat Embryol (Berl) 147:20–34
Pelliniemi LJ, Frojdman K, Sundstrom J, Pollanen P, Kuopio T (1998) Cellular and molecular changes during sex differentiation of embryonic mammalian gonads. J Exp Zool 281:482–493
Pereda J, Pozo J, Motta PM (2001) Is there a mesonephric cell contribution to the gonadal primordium before sexual differentiation in humans?: an ultrastructural study. Ital J Anat Embryol 106:143–154
Piprek RP (2009a) Genetic mechanisms underlying male sex determination in mammals. J Appl Genet 50:347–360
Piprek RP (2009b) Molecular mechanisms underlying female sex determination—antagonism between female and male pathway. Folia Biol 57:105–113
Piprek RP (2010) Molecular machinery of gonadal differentiation in mammals. Int J Dev Biol 54:779–786
Piprek RP, Pecio A, Szymura JM (2010) Differentiation and development of gonads in the yellow-bellied toad, Bombina variegata L. 1758 (Amphibia: Anura: Bombinatoridae). Zool Sci 27:47–55
Pitetti JL, Calvel P, Romero Y, Conne B, Truong V, Papaioannou MD, Schaad O, Docquier M, Herrera PL, Wilhelm D, Nef S (2013) Insulin and IGF1 receptors are essential for XX and XY gonadal differentiation and adrenal development in mice. PLoS Genet 9:e1003160
Satoh M (1991) Histogenesis and organogenesis of the gonad in human embryos. J Anat 177:85–107
Schmahl J, Capel B (2003) Cell proliferation is necessary for the determination of male fate in the gonad. Dev Biol 258:264–276
Schmahl J, Eicher EM, Washburn LL, Capel B (2000) Sry induces cell proliferation in the mouse gonad. Development 127:65–73
Schnabel CA, Selleri L, Cleary ML (2003) Pbx1 is essential for adrenal development and urogenital differentiation. Genesis 37:123–130
Smith CA, Sinclair AH (2004) Sex determination: insights from the chicken. Bioessays 26:120–132
Smith CA, Smith MJ, Sinclair AH (1999) Expression of chicken steroidogenic factor-1 during gonadal sex differentiation. Gen Comp Endocrinol 113:187–196
Tamura M, Kanno Y, Chuma S et al (2001) Pod-1/Capsulin shows a sex- and stage-dependent expression pattern in the mouse gonad development and represses expression of Ad4BP/SF-1. Mech Dev 102:135–144
Tanaka SS, Nishinakamura R (2014) Regulation of male sex determination: genital ridge formation and Sry activation in mice. Cell Mol Life Sci 71:4781–4802
Tanimura A, Iwasawa H (1988) Ultrastructural observations on the origin and differentiation of somatic cells during gonadal development in the frog Rana nigromaculata. Dev Growth Differ 30:681–691
Tanimura A, Iwasawa H (1989) Origin of somatic cells and histogenesis in the primordial gonad of the Japanese tree frog Rhacophorus arboreus. Anat Embryol 180:165–173
Taylor H, Vanden Heuvel GB, 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 57:1338–1345
Tilmann C, Capel B (1999) Mesonephric cell migration induces testis cord formation and Sertoli cell differentiation in the mammalian gonad. Development 126:2883–2890
Wartenberg H, Kinsky I, Viebahn C, Schmolke C (1991) Fine structural characteristics of testicular cord formation in the developing rabbit gonad. J Electron Microsc Tech 19:133–157
Wilhelm D, Englert C (2002) The Wilms tumor suppressor WT1 regulates early gonad development by activation of Sf1. Genes Dev 16:1839–1851
Wylie CC, Heasman J (1976) The formation of the gonadal ridge in Xenopus laevis. I. A light and transmission electron microscope study. J Embryol Exp Morphol 35:125–138
Yao HH, DiNapoli L, Capel B (2004) Cellular mechanisms of sex determination in the red-eared slider turtle, Trachemys scripta. Mech Dev 121:1393–1401
Yoshinaga K, Hess DL, Hendrickx AG, Zamboni L (1988) The development of the sexually indifferent gonad in the prosimian, Galago crassicaudatus crassicaudatus. Am J Anat 181:89–105
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RPP was supported by the project financed by the National Science Centre assigned on the basis of the decision number DEC-2013/11/D/NZ3/00184.
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Piprek, R.P., Kloc, M., Kubiak, J.Z. (2016). Early Development of the Gonads: Origin and Differentiation of the Somatic Cells of the Genital Ridges. In: Piprek, R. (eds) Molecular Mechanisms of Cell Differentiation in Gonad Development. Results and Problems in Cell Differentiation, vol 58. Springer, Cham. https://doi.org/10.1007/978-3-319-31973-5_1
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