Molecular aspects of female and male gonadal development in mammals

Pediatric Endocrinology Reviews

Volumn 1, Issue 3, 2004, Pages 274-287

  Pannetier, Maëlle ^a   Mandon Pépin, Béatrice ^a   Copelli, Silvia ^c   Fellous, Marc ^b  

^a INRA Institut National de la Recherche Agronomique   (France)

^b Hôpital Cochin ^*  (France)

^c Universidad CAECE   (Argentina)

Author keywords

Ovary differentiation; Sex determination; Sex reversal; Testis differentiation

Indexed keywords

BONE MORPHOGENETIC PROTEIN 15; FACTOR IN THE GERMLINE ALPHA PROTEIN; FIBROBLAST GROWTH FACTOR 9; FORKHEAD BOX TRANSCRIPTION FACTOR L2; GENE PRODUCT; GROWTH DIFFERENTIATION FACTOR 9; HELIX LOOP HELIX PROTEIN; MESSENGER RNA; NUCLEAR RECEPTOR DAX 1; PIS REGULATED TRANSCRIPT 1 PROTEIN; PROTEIN OVOL1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR SOX9; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; WNT PROTEIN; WNT4 PROTEIN;

AUTOSOME ABERRATION; BLEPHAROPHIMOSIS; BLEPHAROPHIMOSIS PTOSIS EPICANTHUS INVERSUS SYNDROME; CELL DIFFERENTIATION; CELL INTERACTION; CELL SURVIVAL; CHROMOSOME DELETION; CHROMOSOME TRANSLOCATION; CHROMOSOME XQ; DELETED IN AZOOSPERMIA GENE; DELETED IN AZOOSPERMIA LIKE GENE; EMBRYO DEVELOPMENT; EMX2 GENE; FEMALE; GENE EXPRESSION; GENE INACTIVATION; GENE LOCATION; GENE MAPPING; GENE MUTATION; GENE OVEREXPRESSION; GENE TARGETING; GENETIC ANALYSIS; GENETIC CONSERVATION; GERM CELL; GOAT; GONAD DEVELOPMENT; HERMAPHRODITISM; HOMEOBOX; HUMAN; IMMUNOHISTOCHEMISTRY; KARYOTYPE 46,XX; KARYOTYPE 46,XY; KNOCKOUT MOUSE; LEYDIG CELL; LHX9 GENE; LIM1 GENE; M33 GENE; MALE; MAMMAL; MULTIGENE FAMILY; NONHUMAN; ORGANOGENESIS; OVARY DEVELOPMENT; OVARY FOLLICLE DEVELOPMENT; OVARY INSUFFICIENCY; PTOSIS; REVIEW; SEX DETERMINATION; SEX TRANSFORMATION; SEXUAL DEVELOPMENT; SPECIES DIFFERENCE; SRY GENE; TESTIS DEVELOPMENT; TISSUE DIFFERENTIATION; X CHROMOSOME ABERRATION; Y CHROMOSOME;

ANIMALS; FEMALE; HUMANS; MALE; MOLECULAR BIOLOGY; OVARY; TESTIS;

EID: 13444311624     PISSN: 15654753     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (140)

1. Byskov AG. Differentiation of mammalian embryonic gonad. Physiol Rev 1986;66(1):71-117.
2. Buehr M, McLaren A, Bartley A, Darling S. Proliferation and migration of primordial germ cells in We/We mouse embryos. Dev Dyn 1993;198(3):182-189.
3. Josso N. The intersex child. Pediatr Adolesc Endocr 1981;8:1-13.
4. Gessler M, Poustka A, Cavenee W, Neve RL, Orkin SH, Bruns GA. Homozygous deletion in Wilms tumours of a zinc-finger gene identified by chromosome jumping. Nature 1990;343(6260):774-778.
5. Pelletier J, Bruening W, Li FP, Haber DA, Glaser T, Housman DE. WT1 mutations contribute to abnormal genital system development and hereditary Wilms' tumour. Nature 1991;353(6343):431-434.
6. Englert C. WT1-more than a transcription factor? Trends Biochem Sci 1998;23(10):389-393.
7. Denys P, Malvaux P, Van Den Berghe H, Tanghe W, Proesmans W. Association d'un syndrome anatomo-pathologique de pseudo-hermaphrodisme masculin, d'une tumeur de Wilms, d'une nephropathie parenchymateuse et d'un mosaicisme XX/XY. Arch Fr Pediatr 1967;24(7):729-739.
8. Drash A, Sherman F, Hartmann WH, Blizzard RM. A syndrome of pseudohermaphroditism, Wilms' tumor, hypertension and degenerative renal disease. J Pediatr 1970;76(4):585-593.
9. Jadresic L, Leake J, Gordon I, Dillon MJ, Grant DB, Pritchard J, Risdon RA, Barratt TM. Clinicopathologic review of twelve children with nephropathy, Wilms tumor and genital abnormalities (Drash syndrome). J Pediatr 1990;117(5):717-725
10. Habib R, Loirat C, Gubler MC, Niaudet P, Bensman A, Levy M, Broyer M. The nephropathy associated with male pseudohermaphroditism and Wilms' tumor (Drash syndrome): a distinctive glomerular lesion-report of 10 cases. Clin Nephrol 1985;24(6):269-278
11. Frasier S, Bashore RA and Mosier HD. Gonadoblastoma associated with pure gonadal dysgenesis in monozygotic twins. J Pediatr 1964;64:740-745
12. Haning RV Jr, Chesney RW, Moorthy AV, Gilbert EF. A syndrome of chronic renal failure and XY gonadal dysgenesis in young phenotypic females without genital ambiguity. Am J Kidney Dis 1985;6(1):40-48
13. Kinberg JA, Angle CR, Wilson RB. Nephropathy-gonadal dysgenesis, type 2: renal failure in three siblings with XY dysgenesis in one. Am J Kidney Dis 1987;9(6):507-510
14. Moorthy AV, Chesney RW, Lubinsky M. Chronic renal failure and XY gonadal dysgenesis: "Frasier" syndrome-a commentary on reported cases. Am J Med Genet Suppl 1987;3:297-302
15. Kreidberg JA, Sariola H, Loring JM, Maeda M, Pelletier J, Housman D, Jaenisch R. WT-1 is required for early kidney development. Cell 1993;74(4):679-691
16. Menke AL, van der Eb AJ, Jochemsen AC. The Wilms' tumor 1 gene: oncogene or tumor suppressor gene? Int Rev Cytol 1998;181:151-212
17. Lee SB, Huang K, Palmer R, Truong VB, Herzlinger D, Kolquist KA, Wong J, Paulding C, Yoon SK, Gerald W, Oliner JD, Haber DA. The Wilms tumor suppressor WT1 encodes a transcriptional activator of amphiregulin. Cell 1999;98(5):663-673
18. Hastie ND. Life, sex and WT1 isoforms-three amino acids can make all the difference. Cell. 2001;106(4):391-394
19. Larsson SH, Charlieu JP, Miyagawa K, Engelkamp D, Rassoulzadegan M, Ross A, Cuzin F, van Heyningen V, Hastie ND. Subnuclear localization of WT1 in splicing or transcription factor domains is regulated by alternative splicing. Cell 1995;81(3):391-401
20. Ladomery MR, Slight J, McGhee S, Hastie ND. Presence of WT1, the Wilm's tumor suppressor gene product, in nuclear poly(A)(+) ribonucleoprotein. J Biol Chem 1999;274(51):36520-36526
21. Englert C, Vidal M, Maheswaran S, Ge Y, Ezzell RM, Isselbacher KJ, Haber DA. Truncated WT1 mutants alter the subnuclear localization of the wild-type protein. Proc Natl Acad Sci USA 1995;92(26): 11960-11964.
22. Hammes A, Guo JK, Lutsch G, Leheste JR, Landrock D, Ziegler U, Gubler MC, Schedl A. Two splice variants of the Wilms' tumor 1 gene have distinct functions during sex determination and nephron formation. Cell 2001;106(3):319-329.
23. Barbaux S, Niaudet P, Gubler MC, Grunfeld JP, Jaubert F, Kuttenn F, Fekete CN, Souleyreau-Therville N, Thibaud E, Fellous M, McElreavey Donor splice-site mutations in WT1 are responsible for Frasier syndrome. Nat Genet 1997;17(4):467-470
24. Kikuchi H, Takata A, Akasaka Y, Fukuzawa R, Yoneyama H, Kurosawa Y, Honda M, Kamiyama Y, Hata J. Do intronic mutations affecting splicing of WT1 exon 9 cause Frasier syndrome? J Med Genet 1998;35(1):45-48
25. Barbosa AS, Hadjiathanasiou CG, Theodoridis C, Papathanasiou A, Tar A, Merksz M, Gyorvari B, Sultan C, Dumas R, Jaubert F, Niaudet P, Moreira-Filho CA, Cotinot C, Fellous M. The same mutation affecting the splicing of WT1 gene is present on Frasier syndrome patients with or without Wilms' tumor. Hum Mutat 1999;13(2):146-153
26. Lala DS, Rice DA, Parker KL. Steroidogenic factor I, a key regulator of steroidogenic enzyme expression, is the mouse homolog of fushi tarazu-factor I. Mol Endocrinol 1992;6(8):1249-1258
27. Morohashi K, Honda S, Inomata Y, Handa H, Omura T. A common trans-acting factor, Ad4-binding protein, to the promoters of steroidogenic P-450s. J Biol Chem 1992;267(25):17913-17919
28. Ikeda Y, Shen WH, Ingraham HA, Parker KL. Developmental expression of mouse steroidogenic factor-1, an essential regulator of the steroid hydroxylases. Mol Endocrinol 1994;8(5):654-662
29. Hatano O, Takayama K, Imai T, Waterman MR, Takakusu A, Omura T, Morohashi K. Sex-dependent expression of a transcription factor, Ad4BP, regulating steroidogenic P-450 genes in the gonads during prenatal and postnatal rat development. Development 1994;120(10):2787-2797
30. Ingraham HA, Lala DS, Ikeda Y, Luo X, Shen WH, Nachtigal MW, Abbud R, Nilson JH, Parker KL. The nuclear receptor steroidogenic factor 1 acts at multiple levels of the reproductive axis. Genes Dev 1994;8(19):2302-2312
31. Morohashi K, Iida H, Nomura M, Hatano O, Honda S, Tsukiyama T, Niwa O, Hara T, Takakusu A, Shibata Y, et al. Functional difference between Ad4BP and ELP and their distributions in steroidogenic tissues. Mol Endocrinol 1994;8(5):643-653
32. Luo X, Ikeda Y, Parker KL. A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell 1994;77(4):481-490
33. Ikeda Y, Luo X, Abbud R, Nilson JH, Parker KL. The nuclear receptor steroidogenic factor 1 is essential for the formation of the ventromedial hypothalamic nucleus. Mol Endocrinol 1995;9(4):478-486
34. Achermann JC, Ito M, Ito M, Hindmarsh PC, Jameson JL. A mutation in the gene encoding steroidogenic factor-1 causes XY sex reversal and adrenal failure in humans. Nat Genet 1999;22(2):125-126
35. Birk OS, Casiano DE, Wassif CA, Cogliati T, Zhao L, Zhao Y, Grinbersg A, Huang S, Kreidberg JA, Parker KL, Porter FD, Westphal H. The LIM homeobox gene Lhx9 is essential for mouse gonad formation. Nature 2000;403(6772):909-913.
36. Wilhelm D, Englert C. The Wilms tumor suppressor WT1 regulates early gonad development by activation of SF1. Genes Dev 2002;16(14):1839-1851
37. Shawlot W, Behringer RR. Requirement for Lim1 in head-organizer function. Nature 1995;374(6521):425-430
38. Miyamoto N, Yoshida M, Kuratani S, Matsuo I, Aizawa S. Defects of urogenital development in mice lacking Emx2. Development 1997;124(9):1653-1664
39. Katoh-Fukui Y, Tsuchiya R, Shiroishi T, Nakahara Y, Hashimoto N, Noguchi K, Higashinakagawa T. Male-to-female sex reversal in M33 mutant mice. Nature 1998;393(6686):688-692
40. Capel B, Albrecht KH, Washburn LL, Eicher EM. Migration of mesonephric cells into the mammalian gonad depends on SRY. Mech Dev 1999;84(1-2):127-131
41. Buehr M, Gu S, McLaren A. Mesonephric contribution to testis differentiation in the fetal mouse. Development 1993;117(1):273-281
42. Merchant-Larios H, Moreno-Mendoza N, Buehr M. The role of the mesonephros in cell differentiation and morphogenesis of the mouse fetal testis. Int J Dev Biol 1993;37(3):407-415
43. Martineau J, Nordqvist K, Tilmann C, Lovell-Badge R, Capel B. Male-specific cell migration into the developing gonad. Curr Biol 1997;7(12):958-968
44. Tilmann C, Capel B. Mesonephric cell migration induces testis cord formation and Sertoli cell differentiation in the mammalian gonad. Development 1999;126(13):2883-2890
45. Berta P, Hawkins JR, Sinclair AH, Taylor A, Griffiths BL, Goodfellow PN, Fellous M. Genetic evidence equating SRY and the testis-determining factor. Nature 1990;348(6300):448-450
46. Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovell-Badge R. Male development of chromosomally female mice transgenic for SRY. Nature 1991;351(6322):117-121
47. Wegner M. From head to toes: the multiple facets of Sox proteins. Nucleic Acids Res 1999;27(6):1409-1420
48. Kamachi Y, Uchikawa M, Kondoh H. Pairing SOX off: with partners in the regulation of embryonic development. Trends Genet 2000;16(4): 182-187
49. McElreavey K, Vilain E, Abbas N, Herskowitz I, Fellous M. A regulatory cascade hypothesis for mammalian sex determination: SRY represses a negative regulator of male development. Proc Natl Acad Sci USA 1993;90(8):3368-3372
50. Foster JW, Dominguez-Steglich MA, Guioli S, Kowk G, Weller PA, Stevanovic M, Weissenbach J, Mansour S, Young ID, Goodfellow PN, et al. Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature 1994;372(6506):525-530
51. Wagner T, Wirth J, Meyer J, Zabel B, Held M, Zimmer J, Pasantes J, Bricarelli FD, Keutel J, Hustert E, et al. Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 1994;79(6):1111-1120
52. Huang B, Wang S, Ning Y, Lamb AN, Bartley J. Autosomal XX sex reversal caused by duplication of SOX9. Am J Med Genet 1999;87(4):349-353
53. Bishop CE, Whitworth DJ, Qin Y, Agoulnik AI, Agoulnik IU, Harrison WR, Behringer RR, Overbeek PA. A transgenic insertion upstream of SOX9 is associated with dominant XX sex reversal in the mouse. Nat Genet 2000;26(4):490-494
54. Wright E, Hargrave MR, Christiansen J, Cooper L, Kun J, Evans T, Gangadharan U, Greenfield A, Koopman P. The SRY-related gene SOX9 is expressed during chondrogenesis in mouse embryos. Nat Genet 1995;9(1):15-20
55. Sudbeck P, Schmitz ML, Baeuerle PA, Scherer C. Sex reversal by loss of the C-terminal transactivation domain of human SOX9. Nat Genet 1996;13(2):230-232
56. Ng LJ, Wheatley S, Muscat CE, Conway-Campbell J, Bowles J, Wright E, Bell DM, Tam PP, Cheah KS, Koopman P. SOX9 binds DNA, activates transcription and coexpresses with type II collagen during chondrogenesis in the mouse. Dev Biol 1997;183(1):108-121
57. McDowall S, Argentaro A, Ranganathan S, Weller P, Mertin S, Mansour S, Tolmie J, Harley V. Functional and structural studies of wild type SOX9 and mutations causing campomelic dysplasia. J Biol Chem 1999;274(34):24023-24030
58. Bernard P, Tang P, Liu S, Dewing P, Harley VR, Vilain E. Dimerization of SOX9 is required for chondrogenesis, but not for sex determination. Hum Mol Genet 2003;12(14):1755-1765
59. de Santa Barbara P, Bonneaud N, Boizet B, Desclozeaux M, Moniot B, Sudbeck P, Scherer G, Poulat F, Berta P. Direct interaction of SRY-related protein SOX9 and steroidogenic factor 1 regulates transcription of the human anti-Mullerian hormone gene. Mol Cell Biol 1998;18(11):6653-6665
60. Arango NA, Lovell-Badge R, Behringer RR. Targeted mutagenesis of the endogenous mouse Mis gene promoter: in vivo definition of genetic pathways of vertebrate sexual development. Cell 1999;99(4)409-419
61. Morais da Silva S, Hacker A, Harley V, Goodfellow P, Swain A, Lovell-Badge R. SOX9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nat Genet 1996;14(1):62-68
62. de Santa Barbara P, Moniot B, Poulat F, Berta P. Expression and subcellular localization of SF-1, SOX9, WT1 and AMH proteins during early human testicular development. Dev Dyn 2000;217(3):293-298
63. Sudbeck P, Scherer G. Two independent nuclear localization signals are present in the DNA-binding high-mobility group domains of SRY and SOX9. J Biol Chem 1997;272(44):27848-27852
64. Gasca S, Canizares J, De Santa Barbara P, Mejean C, Poulat F, Berta P, Boizet-Bonhoure B. A nuclear export signal within the high mobility group domain regulates the nucleocytoplasmic translocation of SOX9 during sexual determination. Proc Natl Acad Sci USA 2002;99(17):11199-11204
65. Ohe K, Lalli E, Sassone-Corsi P. A direct role of SRY and SOX proteins in pre-mRNA splicing. Proc Natl Acad Sci USA 2002;99(3):1146-1151
66. Bernard P, Tang P, Liu S, Dewing P, Harley VR, Vilain. Dimerization of SOX9 is required for chondrogenesis, but not for sex determination. Hum Mol Genet 2003;12(14):1755-1765
67. Schepers G, Wilson M, Wilhem D, Koopman P. SOX8 Is Expressed during Testis Differentiation in Mice and Synergiies with SF1 to Activate the Amh Promoter in Vitro. J Biol Chem 2003;278(30):28101-28108
68. Bardoni B, Zanaria E, Guioli S, Floridia G, Worley KC, Tonini G, Ferrante E, Chiumello G, McCabe ER, Fraccaro M, Zuffardi O, Camerino G. A dosage sensitive locus at chromosome Xp21 is involved in male to female sex reversal. Nat Genet 1994;7(4):497-501
69. Ikeda Y, Swain A, Weber TJ, Weniges KE, Zanaria E, Lalli E, Tamai KT, Sassone-Corsi P, Lovell-Badge R, Camerino G, Parker KL. Steroidogenic factor 1 and Dax-1 colocalize in multiple cell lineages: potential links in endocrine development. Mol Endocrinol 1996;10(10):1261-1272
70. Ikeda Y, Takeda Y, Shikayama T, Mukai T, Hisano S, Morohashi KI. Comparative localization of Dax-1 and Ad4BP/SF-1 during development of the hypothalamic-pituitary-gonadal axis suggests their closelyrelated and distinct functions. Dev Dyn 2001;220(4):363-376
71. Muscatelli F, Strom TM, Walker AP, Zanaria E, Recan D, Meindl A, Bardoni B, Guioli S, Zehetner C, Rabl W, et al. Mutations in the DAX-1 gene give rise to both X-linked adrenal hypoplasia congenita and hypogonadotropic hypogonadism. Nature 1994;372(6507):672-676
72. Swain A, Narvaez V, Burgoyne P, Camerino G, Lovell-Badge R. DAX1 antagonizes SRY action in mammalian sex determination. Nature 1998;391(6669):761-767
73. Yu RN, Ito M, Saunders TL, Camper SA, Jameson JL. Role of Ahch in gonadal development and gametogenesis. Nat Genet 1998;20(4):353-357
74. Meeks JJ, Crawford SE, Russell TA, Morohashi K, Weiss J, Jameson JL. DAX1 regulates testis cord organization during gonadal differentiation. Development 2003;130(5):1029-1036
75. Meeks JJ, Weiss J, Jameson JL. DAX1 is required for testis determination. Nat Genet 2003;34(1):32-33
76. Swain A, Zanaria E, Hacker A, Lovell-Badge R, Camerino G. Mouse DAX1 expression is consistent with a role in sex determination as well as in adrenal and hypothalamus function. Nat Genet 1996;12(4):404-409
77. Crawford PA, Dorn C, Sadovsky Y, Milbrandt J. Nuclear receptor DAX-1 recruits nuclear receptor corepressor N-CoR to steroidogenic factor 1. Mol Cell Biol 1998;18(5):2949-2956
78. Raymond CS, Shamu CE, Shen MM, Seifert KJ, Hirsch B, Hodgkin J, Zarkower D. Evidence for evolutionary conservation of sex-determining. Nature 1998;391(6668):691-695
79. Veitia RA, Nunes M, Quintana-Murci L, Rappaport R, Thibaud E, Jaubert F, Fellous M, McElreavey K, Goncalves J, Silva M, Rodrigues JC, Caspurro M, Boieiro F, Marques R, Lavinha J. Swyer syndrome and 46,XY partial gonadal dysgenesis associated with 9p deletions in the absence of monosomy-9p syndrome. Am J Hum Genet 1998;63(3):901-905
80. Ottolenghi C, Veitia R, Quintana-Murci L, Torchard D, Scapoli L, Souleyreau-Therville N, Beckmann J, Fellous M, McElreavey K. The region on 9p associated with 46,XY sex reversal contains several transcripts expressed in the urogenital system and a novel doublesex-related domain. Genomics 2000;64(2):170-178
81. Raymond CS, Kettlewell JR, Hirsch B, Bardwell VJ, Zarkower D. Expression of Dmrt1 in the genital ridge of mouse and chicken embryos suggests a role in vertebrate sexual development. Dev Biol 1999;215(2):208-220
82. Raymond CS, Murphy MW, O'Sullivan MG, Bardwell VJ, Zarkower D. Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev 2000;14(20):2587-2595
83. Colvin JS, Green RP, Schmahl J, Capel Bornitz DM. Male-to-female sex reversal in mice lacking fibroblast growth factor 9. Cell 2001;104(6):875-889
84. Brennan J, Tilmann C, Capel B. Pdgfr-alpha mediates testis cord organization and fetal Leydig cell development in the XY gonad. Genes Dev 2003;17(6):800-810
85. Clark AM, Garland KK, Russell LD. Desert hedgehog (Dhh) gene is required in the mouse testis for formation of adult-type Leydig cells and normal development of peritubular cells and seminiferous tubules. Biol Reprod 2000;63(6):1825-1838
86. Pierucci-Alves F, Clark AM, Russell LD. A developmental study of the Desert hedgehog-null mouse testis. Biol Reprod 2001;65(5):1392-1402
87. Yao HH, Whoriskey W, Capel B. Desert Hedgehog/Patched 1 signalling specifies fetal Leydig cell fate in testis organogenesis. Genes Dev 2002;16(11):1433-1440
88. Umehara F, Tate G, Itoh K, Osame M. Minifascicular neuropathy: a new concept of the human disease caused by desert hedgehog gene mutation. Cell Mol Biol (Noisy-le-grand) 2002;48(2):187-189
89. Albrecht KH, Eicher EM. Evidence that SRY is expressed in pre-Sertoli cells and Sertoli and granulosa cells have a common precursor. Dev Biol 2001;240(1):92-107
90. McLaren A, Southee D. Entry of mouse embryonic germ cells into meiosis. Dev Biol 1997;187(1):107-113
91. Kuroda H, Terada N, Nakayama H, Matsumoto K, Kitamura Y. Infertility due to growth arrest of ovarian follicles in Sl/Slt mice. Dev Biol 1988;126(1):71-79
92. Chabot B, Stephenson DA, Chapman VM, Besmer P, Bernstein A. The proto-oncogene c-kit encoding a transmembrane tyrosine kinase receptor maps to the mouse W locus. Nature 1988;335(6185):88-89
93. Wylie C.C., Heasman J. Migration, proliferation and potency of primordial germ cells. Semin Dev Biol 1993;4:161-170
94. McLaren A. Germ cells and germ cell sex. Philos Trans R Soc Lond B Biol Sci 1995;350(1333):229-233
95. Frojdman K, Paranko J, Virtanen I, Pelliniemi LJ. Intermediate filament proteins and epithelial differentiation in the embryonic ovary of the rat. Differentiation 1993;55(1):47-55
96. Sawyer HR, Smith P, Heath DA, Juengel JL, Wakefield SJ, McNatty KP. Formation of ovarian follicles during fetal development in sheep. Biol Reprod 2002;66(4):1134-1150
97. Richards JS. Perspective: the ovarian follicle - a perspective in 2001. Endocrinology 2001;142(6):2184-2193
98. Jost A. Recherches sur la différenciation sexuelle de l'embryon de lapin. Arch Anat Microsc Morphol Exp 1947;36:271-315
99. Crisponi L, Deiana M, Loi A, Chiappe F, Uda M, Amati P, Bisceglia L, Zelante L, Nagaraja R, Porcu S, Ristaldi MS, Marzella R, Rocchi M, Nicolino M, Lienhardt-Roussie A, Nivelon A, Verloes A, Schlessinger D, Gasparini P, Bonneau D, Cao A, Pilia G. The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ptosis/epicanthus inversus syndrome. Nat Genet 2001;27(2):159-166
100. Zlotogora J, Sagi M, Cohen T. The blepharophimosis, ptosis and epicanthus inversus syndrome: delineation of two types. Am J Hum Genet 1983;35(5):1020-1027
101. Cocquet J, Pailhoux E, Jaubert F, Servel N, Xia X, Pannetier M, De Caere E, Messiaen L, Cotinot C, Fellous M, Veitia RA. Evolution and expression of FOXL2. J Med Genet 2002;39(12):916-921
102. Pannetier M, Servel H, Cocquet J, Besnard H, Cotinot C, Pailhoux E. Expressional studies of the PIS-regulated genes suggest different mechanisms of sex determination within mammals. Cyto Genet Genome Res 2003;101:199-205
103. Loffler KA, Zarkower D, Koopman P. Etiology of Ovarian Failure in Blepharophimosis Ptosis Epicanthus Inversus Syndrome: FOXL2 Is a Conserved, Early-Acting Gene in Vertebrate Ovarian Development. Endocrinology 2003;144(7):3237-3243
104. Pailhoux E, Vigier B, Chaffaux S, Servel N, Taourit S, Furet JP, Fellous M, Grosclaude F, Cribiu EP, Cotinot C, Vaiman D. A 11.7-kb deletion triggers intersexuality and polledness in goats. Nat Genet 2001;29(4):453-458
105. Castrillon D, Miao L, Kollipara R, Hornet J, DePinho R. Suppresion of Ovarian follicle Activation in Mice by the transcription Factor Foxo3a. Science 2003;301:215-218
106. Brunei A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS Anderson MJ, Arden KC, Blenis J, Greenberg ME. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 1999;96:857-868
107. Vainio S, Heikkila M, Kispert A, Chin N, McMahon AP. Female development in mammals is regulated by Wnt-4 signalling. Nature 1999;397(6718):405-409
108. Stark K, Vainio S, Vassileva G, McMahon AP. Epithelial transformation of metanephric mesenchyme in the developing kidney regulated by Wnt-4. Nature 1994;372(6507):679-683
109. Jordan BK, Mohammed M, Ching ST, Delot E, Chen XN, Dewing P, Swain A, Rao PH, Elejalde BR, Vilain E. Up-regulation of WNT-4 signalling and dosage-sensitive sex reversal in humans. Am J Hum Genet 2001;68(5):1102-1109
110. Jeays-Ward K, Hoyle C, Brennan J, Dandonneau M, Alldus G, Capel B, Swain A. Endothelial and steroidogenic cell migration are regulated by WNT4 in the developing mammalian gonad. Development 2003;130(16):3663-3670
111. Menke DB, Page DC. Sexually dimorphic gene expression in the developing mouse gonad. Gene Expr Patterns 2002;2(3-4):359-367
112. Yao HHC, Brennan J, Matzuk M, Capel B. Follistatin operates one branch of the Wnt4 signalling cascade in development of the mammalian ovary. Third International Symposium on the Biology of Vertebrate Sex Determination, 2003; Hawaii.
113. McLaren A. Development of the mammalian gonad: the fate of the supporting cell lineage. Bioessays 1991;13(4):151-156
114. Prepin J, Hida H. Influence of age and medium on formation of epithelial cords in the rat fetal ovary in vitro. J Reprod Fertil 1989;87(1):375-382
115. Crumeyrolle-Arias M, Scheib D, Aschheim P. Light and electron microscopy of the ovarian interstitial tissue in the senile rat: normal aspect and response to HCG of deficiency cells and epithelial cords. Gerontology 1976;22(3):185-204
116. Ruggiu M, Speed R, Taggart M, McKay SJ, Kilanowski F, Saunders P, Dorin J, Cooke HJ. The mouse DAZLA gene encodes a cytoplasmic protein essential for gametogenesis. Nature 1997;389(6646):73-77
117. Xu EY, Moore FL, Pera RA. A gene family required for human germ cell development evolved from an ancient meiotic gene conserved in metazoans. Proc Natl Acad Sci USA 2001;98(13):7414-7419
118. Reijo R, Lee TY, Salo P, Alagappan R, Brown LG, Rosenberg M, Rozen S, Jaffe T, Straus D, Hovatta O, de la Chapelle A, Silber S, Page DC. Diverse spermatogenic defects in humans caused by Y chromosome deletions encompassing a novel RNA-binding protein gene. Nat Genet 1995;10(4):383-393
119. Nishi S, Hoshi N, Kasahara M, Ishibashi T, Fujimoto S. Existence of human DAZLA protein in the cytoplasm of human oocytes. Mol Hum Reprod 1999;5(6):495-497
120. Brekhman V, Itskovitz-Eldor J, Yodko E, Deutsch M, Seligman J. The DAZL1 gene is expressed in human male and female embryonic gonads before meiosis. Mol Hum Reprod 2000;6(5):465-468
121. Mandon-Pepin B, Oustry-Vaiman A, Vigier B, Piumi F, Cribiu E, Cotinot C. Expression profiles and chromosomal localization of genes controlling meiosis and follicular development in the sheep ovary. Biol Reprod. 2003;68(3):985-995
122. Liang L, Soyal SM, Dean J. FIGalpha, a germ cell specific transcription factor involved in the coordinate expression of the zona pellucida genes. Development 1997;124(24):4939-4947
123. Soyal SM, Amleh A, Dean J. FIGalpha, a germ cell-specific transcription factor required for ovarian follicle formation. Development 2000;127(21):4645- 4654
124. Huntriss J, Gosden R, Hinkins M, Oliver B, Miller D, Rutherford AJ, Picton HM. Isolation, characterization and expression of the human Factor In the Germline alpha (FIGLA) gene in ovarian follicles and oocytes. Mol Hum Reprod 2002;8(12):1087-1095
125. Kol S, Adashi EY. Intraovarian factors regulating ovarian function. Curr Opin Obstet Gynecol 1995;7(3):209-213
126. Dube JL, Wang P, Elvin, Lyons KM, Celeste AJ, Matzuk MM. The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Mol Endocrinol 1998;12(12):1809-1817.
127. McGrath SA, Esquela AF, Lee SJ. Oocyte-specific expression of growth/differentiation factor-9. Mol Endocrinol 1995;9(1):131-136
128. Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk MM. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 1996;383(6600):531-553
129. Yan C, Wang P, DeMayo J, DeMayo FJ, Elvin JA, Carino C, Prasad SV, Skinner SS, Dunbar BS, Dube JL, Celeste AJ, Matzuk MM. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol Endocrinol 2001;15(6):854-866
130. Davis GH, McEwan JC, Fennessy PF, Dodds KC, McNatty KP, O WS. Infertility due to bilateral ovarian hypoplasia in sheep homozygous (FecXI) for the Inverdale prolificacy gene located on the X chromosome. Biol Reprod 1992;46(4):636-640
131. Braw-Tal R, McNatty KP, Smith P, Heath DA, Hudson HL, Phillips DJ, McLeod BJ, Davis GH. 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 1993;49(5):895-907
132. Juengel JL, Quirke LD, Tisdall DJ, Smith P, Hudson NL, McNatty KP. Gene expression in abnormal ovarian structures of ewes homozygous for the inverdale prolificacy gene. Biol Reprod 2000;62(6):1467-1478
133. Rajpert-De Meyts E, Jorgensen N, Graem N, Muller J, Cate RL, Skakkebaek NE. Expression of anti-Mullerian hormone during normal and pathological gonadal development: association with differentiation of Sertoli and granulosa cells. J Clin Endocrinol Metab 1999;84(10):3836-3844
134. Ueno S, Kuroda T, Maclaughlin DT, Ragin RC, Manganaro TF, Donahoe PK. Mullerian inhibiting substance in the adult rat ovary during various stages of the estrous cycle. Endocrinology 1989;125(2):1060-1066
135. Hirobe S, He WW, Lee MM, Donahoe PK. Mullerian inhibiting substance messenger ribonucleic acid expression in granulosa and Sertoli cells coincides with their mitotic activity. Endocrinology 1992;131(2):854-862
136. Durlinger AL, Kramer P, Karels B, de Jong FH, Uilenbroek JT, Grootegoed JA, Themmen AP. Control of primordial follicle recruitment by anti-Mullerian hormone in the mouse ovary. Endocrinology 1999;140(12):5789-5796
137. Garfinkel MD, Lohe AR, Mahowald AP. Molecular genetics of the Drosophila melanogaster ovo locus, a gene required for sex determination of germline cells. Genetics 1992;130(4):791-803
138. Mevel-Ninio M, Terracol R, Salles C, Vincent A, Payre F. ovo, a Drosophila gene required for ovarian development, is specifically expressed in the germline and shares most of its coding sequences with shaven baby, a gene involved in embryo patterning. Mech Dev 1995;49(1-2):83-95
139. Marozzi A, Manfredini E, Tibiletti MG, Furlan D, Villa N, Vegetti W, Crosijnoni PG, Ginelli E, Meneveri R, Dalpra L. Molecular definition of Xq common-deleted region in patients affected by premature ovarian failure. Hum Genet 2000;107:304-311
140. Bione S, Sala C, Manzini C, Arrigo G, Zuffardi O, Banfi S, Borsani G, Jonveaux P, Philippe C, Zuccotti M, Ballabio A, Toniolo D. A human homologue of the Drosophila melanogaster diaphanous gene is disrupted in a patient with premature ovarian failure: evidence for conserved function in oogenesis and implications for human sterility. Am J Hum Genet 1998;62(3):533-541