Steroidogenic organ development and homeostasis: A WT1-centric view

Molecular and Cellular Endocrinology

Volumn 408, Issue , 2015, Pages 145-155

  Bandiera, Roberto ^a   Sacco, Sonia ^b,c,d   Vidal, Valerie P I ^b,c,d   Chaboissier, Marie Christine ^b,c,d   Schedl, Andreas ^b,c,d  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b CENTRE DE BIOCHIMIE   (France)

^c INSERM   (France)

^d CNRS   (France)

Author keywords

Adrenal development; Gonadal development; Progenitor cells; Steroidogenic differentiation; WT1; Catenin

Indexed keywords

STEROID; WT1 PROTEIN;

ANIMAL; BIOSYNTHESIS; CHEMISTRY; GONAD; HOMEOSTASIS; HUMAN; METABOLISM; ORGANOGENESIS; STRUCTURE ACTIVITY RELATION;

ANIMALS; GONADS; HOMEOSTASIS; HUMANS; ORGANOGENESIS; STEROIDS; STRUCTURE-ACTIVITY RELATIONSHIP; WT1 PROTEINS;

EID: 84926631095     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2015.01.009     Document Type: Review

References (120)

1. Andersen S.R., Geertinger P., Larsen H.W., Mikkelsen M., Parving A., Vestermark S., et al. Aniridia, cataract and gonadoblastoma in a mentally retarded girl with deletion of chromosome II. A clinicopathological case report. Ophthalmologica 1977, 176:171-177.
2. 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 1999, 99:409-419.
3. Bamforth S.D., Braganca J., Eloranta J.J., Murdoch J.N., Marques F.I., Kranc K.R., et al. Cardiac malformations, adrenal agenesis, neural crest defects and exencephaly in mice lacking Cited2, a new Tfap2 co-activator. Nat. Genet 2001, 29:469-474.
4. Bandiera R., Vidal V.P., Motamedi F.J., Clarkson M., Sahut-Barnola I., von Gise A., et al. WT1 maintains adrenal-gonadal primordium identity and marks a population of AGP-like progenitors within the adrenal gland. Dev. Cell 2013, 27:5-18.
5. Barbaux S., Niaudet P., Gubler M.C., Grunfeld J.P., Jaubert F., Kuttenn F., et al. Donor splice-site mutations in WT1 are responsible for Frasier syndrome. Nat. Genet 1997, 17:467-470.
6. Bernard P., Ryan J., Sim H., Czech D.P., Sinclair A.H., Koopman P., et al. Wnt signaling in ovarian development inhibits Sf1 activation of Sox9 via the Tesco enhancer. Endocrinology 2012, 153:901-912.
7. Berta P., Hawkins J.R., Sinclair A.H., Taylor A., Griffiths B.L., Goodfellow P.N., et al. Genetic evidence equating SRY and the testis-determining factor. Nature 1990, 348:448-450.
8. Berthon A., Sahut-Barnola I., Lambert-Langlais S., de Joussineau C., Damon-Soubeyrand C., Louiset E., et al. Constitutive beta-catenin activation induces adrenal hyperplasia and promotes adrenal cancer development. Hum. Mol. Genet 2010, 19:1561-1576.
9. Berthon A., Martinez A., Bertherat J., Val P. Wnt/beta-catenin signalling in adrenal physiology and tumour development. Mol. Cell. Endocrinol 2012, 351:87-95.
10. Berthon A., Drelon C., Ragazzon B., Boulkroun S., Tissier F., Amar L., et al. WNT/beta-catenin signalling is activated in aldosterone-producing adenomas and controls aldosterone production. Hum. Mol. Genet 2014, 23:889-905.
11. Biason-Lauber A., Konrad D., Navratil F., Schoenle E.J. A WNT4 mutation associated with Mullerian-duct regression and virilization in a 46,XX woman. N. Engl. J. Med 2004, 351:792-798.
12. Bielinska M., Parviainen H., Porter-Tinge S.B., Kiiveri S., Genova E., Rahman N., et al. Mouse strain susceptibility to gonadectomy-induced adrenocortical tumor formation correlates with the expression of GATA-4 and luteinizing hormone receptor. Endocrinology 2003, 144:4123-4133.
13. Bielinska M., Genova E., Boime I., Parviainen H., Kiiveri S., Leppaluoto J., et al. Gonadotropin-induced adrenocortical neoplasia in NU/J nude mice. Endocrinology 2005, 146:3975-3984.
14. Bingham N.C., Verma-Kurvari S., Parada L.F., Parker K.L. Development of a steroidogenic factor 1/Cre transgenic mouse line. Genesis 2006, 44:419-424.
15. Bland M.L., Desclozeaux M., Ingraham H.A. Tissue growth and remodeling of the embryonic and adult adrenal gland. Ann. N. Y. Acad. Sci 2003, 995:59-72.
16. Bor Y.C., Swartz J., Morrison A., Rekosh D., Ladomery M., Hammarskjold M.L. The Wilms' tumor 1 (WT1) gene (+KTS isoform) functions with a CTE to enhance translation from an unspliced RNA with a retained intron. Genes Dev 2006, 20:1597-1608.
17. Bradford S.T., Wilhelm D., Bandiera R., Vidal V., Schedl A., Koopman P. A cell-autonomous role for WT1 in regulating Sry in vivo. Hum. Mol. Genet 2009, 18:3429-3438.
18. Buganim Y., Itskovich E., Hu Y.C., Cheng A.W., Ganz K., Sarkar S., et al. Direct reprogramming of fibroblasts into embryonic Sertoli-like cells by defined factors. Cell Stem Cell 2012, 11:373-386.
19. Call K.M., Glaser T., Ito C.Y., Buckler A.J., Pelletier J., Haber D.A., et al. Isolation and characterization of a zinc finger polypeptide gene at the human chromosome 11 Wilms' tumor locus. Cell 1990, 60:509-520.
20. Caricasole A., Duarte A., Larsson S.H., Hastie N.D., Little M., Holmes G., et al. RNA binding by the Wilms tumor suppressor zinc finger proteins. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:7562-7566.
21. Carpenter B., Hill K.J., Charalambous M., Wagner K.J., Lahiri D., James D.I., et al. BASP1 is a transcriptional cosuppressor for the Wilms' tumor suppressor protein WT1. Mol. Cell. Biol 2004, 24:537-549.
22. Carre G.A., Greenfield A. Characterising novel pathways in testis determination using mouse genetics. Sex. Dev 2014, 8:199-207.
23. Chaboissier M.C., Kobayashi A., Vidal V.I., Lutzkendorf S., van de Kant H.J., Wegner M., et al. Functional analysis of Sox8 and Sox9 during sex determination in the mouse. Development 2004, 131:1891-1901.
24. Chang H., Gao F., Guillou F., Taketo M.M., Huff V., Behringer R.R. Wt1 negatively regulates beta-catenin signaling during testis development. Development 2008, 135:1875-1885.
25. Chassot A.A., Ranc F., Gregoire E.P., Roepers-Gajadien H.L., Taketo M.M., Camerino G., et al. Activation of {beta}-catenin signalling by Rspo1 controls differentiation of the mammalian ovary. Hum. Mol. Genet 2008, 17:1264-1277.
26. Chau Y.Y., Brownstein D., Mjoseng H., Lee W.C., Buza-Vidas N., Nerlov C., et al. Acute multiple organ failure in adult mice deleted for the developmental regulator wt1. PLoS Genet 2011, 7:e1002404.
27. Davies R.C., Calvio C., Bratt E., Larsson S.H., Lamond A.I., Hastie N.D. WT1 interacts with the splicing factor U2AF65 in an isoform-dependent manner and can be incorporated into spliceosomes. Genes Dev 1998, 12:3217-3225.
28. DeFalco T., Capel B. Gonad morphogenesis in vertebrates: divergent means to a convergent end. Annu. Rev. Cell Dev. Biol 2009, 25:457-482.
29. DeFalco T., Takahashi S., Capel B. Two distinct origins for Leydig cell progenitors in the fetal testis. Dev. Biol 2011, 352:14-26.
30. Discenza M.T., Pelletier J. Insights into the physiological role of WT1 from studies of genetically modified mice. Physiol. Genomics 2004, 16:287-300.
31. Essafi A., Webb A., Berry R.L., Slight J., Burn S.F., Spraggon L., et al. A wt1-controlled chromatin switching mechanism underpins tissue-specific wnt4 activation and repression. Dev. Cell 2011, 21:559-574.
32. Franca M.M., Ferraz-de-Souza B., Santos M.G., Lerario A.M., Fragoso M.C., Latronico A.C., et al. POD-1 binding to the E-box sequence inhibits SF-1 and StAR expression in human adrenocortical tumor cells. Mol. Cell. Endocrinol 2013, 371:140-147.
33. Freedman B.D., Kempna P.B., Carlone D.L., Shah M.S., Guagliardo N.A., Barrett P.Q., et al. Adrenocortical zonation results from lineage conversion of differentiated zona glomerulosa cells. Dev. Cell 2013, 26:666-673.
34. Fujimoto Y., Tanaka S.S., Yamaguchi Y.L., Kobayashi H., Kuroki S., Tachibana M., et al. Homeoproteins Six1 and Six4 regulate male sex determination and mouse gonadal development. Dev. Cell 2013, 26:416-430.
35. Gao F., Maiti S., Sun G., Ordonez N.G., Udtha M., Deng J.M., et al. The Wt1+/R394W mouse displays glomerulosclerosis and early-onset renal failure characteristic of human Denys-Drash syndrome. Mol. Cell. Biol 2004, 24:9899-9910.
36. Gao F., Maiti S., Alam N., Zhang Z., Deng J.M., Behringer R.R., et al. The Wilms tumor gene, Wt1, is required for Sox9 expression and maintenance of tubular architecture in the developing testis. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:11987-11992.
37. Gessler M., Poustka A., Cavenee W., Neve R.L., Orkin S.H., Bruns G.A. Homozygous deletion in Wilms tumours of a zinc-finger gene identified by chromosome jumping. Nature 1990, 343:774-778.
38. Gottschau M. Struktur und embryonale entwicklung der nebennieren bei säugetieren. Arch. Anat. Physiol 1883, 9:412-458.
39. Guasti L., Candy Sze W.C., McKay T., Grose R., King P.J. FGF signalling through Fgfr2 isoform IIIb regulates adrenal cortex development. Mol. Cell. Endocrinol 2013, 371:182-188.
40. Gubbay J., Collignon J., Koopman P., Capel B., Economou A., Munsterberg A., et al. 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 1990, 346:245-250.
41. Haber D.A., Buckler A.J., Glaser T., Call K.M., Pelletier J., Sohn R.L., et al. An internal deletion within an 11p13 zinc finger gene contributes to the development of Wilms' tumor. Cell 1990, 61:1257-1269.
42. Hammes A., Guo J.K., Lutsch G., Leheste J.R., Landrock D., Ziegler U., et al. Two splice variants of the Wilms' tumor 1 gene have distinct functions during sex determination and nephron formation. Cell 2001, 106:319-329.
43. Hatano O., Takakusu A., Nomura M., Morohashi K. Identical origin of adrenal cortex and gonad revealed by expression profiles of Ad4BP/SF-1. Genes Cells 1996, 1:663-671.
44. Hohenstein P., Hastie N.D. The many facets of the Wilms' tumour gene, WT1. Hum. Mol. Genet 2006, 15(Spec2):R196-R201.
45. Hu M.C., Chou S.J., Huang Y.Y., Hsu N.C., Li H., Chung B.C. Tissue-specific, hormonal, and developmental regulation of SCC-LacZ expression in transgenic mice leads to adrenocortical zone characterization. Endocrinology 1999, 140:5609-5618.
46. Hu Y.C., Okumura L.M., Page D.C. Gata4 is required for formation of the genital ridge in mice. PLoS Genet 2013, 9:e1003629.
47. Huang C.C., Miyagawa S., Matsumaru D., Parker K.L., Yao H.H. Progenitor cell expansion and organ size of mouse adrenal is regulated by sonic hedgehog. Endocrinology 2010, 151:1119-1128.
48. Iannaccone P.M., Weinberg W.C. The histogenesis of the rat adrenal cortex: a study based on histologic analysis of mosaic pattern in chimeras. J. Exp. Zool 1987, 243:217-223.
49. Ingle D.J., Higgins G.M. Autotransplantation and regeneration of the adrenal gland. Endocrinology 1938, 22:458-464.
50. Jaubert F., Vasiliu V., Patey-Mariaud de Serre N., Auber F., Jeanpierre C., Gubler M.C., et al. Gonad development in Drash and Frasier syndromes depends on WT1 mutations. Arkh. Patol 2003, 65:40-44.
51. Kennedy D., Ramsdale T., Mattick J., Little M. An RNA recognition motif in Wilms' tumour protein (WT1) revealed by structural modelling. Nat. Genet 1996, 12:329-331.
52. Kent J., Coriat A.M., Sharpe P.T., Hastie N.D., van Heyningen V. The evolution of WT1 sequence and expression pattern in the vertebrates. Oncogene 1995, 11:1781-1792.
53. Kero J., Poutanen M., Zhang F.P., Rahman N., McNicol A.M., Nilson J.H., et al. Elevated luteinizing hormone induces expression of its receptor and promotes steroidogenesis in the adrenal cortex. J. Clin. Invest 2000, 105:633-641.
54. Kikuchi H., Takata A., Akasaka Y., Fukuzawa R., Yoneyama H., Kurosawa Y., et al. Do intronic mutations affecting splicing of WT1 exon 9 cause Frasier syndrome?. J. Med. Genet 1998, 35:45-48.
55. Kim A.C., Hammer G.D. Adrenocortical cells with stem/progenitor cell properties: recent advances. Mol. Cell. Endocrinol 2007, 265-266:10-16.
56. Kim A.C., Reuter A.L., Zubair M., Else T., Serecky K., Bingham N.C., et al. Targeted disruption of beta-catenin in Sf1-expressing cells impairs development and maintenance of the adrenal cortex. Development 2008, 135:2593-2602.
57. Kim A.C., Barlaskar F.M., Heaton J.H., Else T., Kelly V.R., Krill K.T., et al. In search of adrenocortical stem and progenitor cells. Endocr. Rev 2009, 30:241-263.
58. Kim Y., Kobayashi A., Sekido R., DiNapoli L., Brennan J., Chaboissier M.C., et al. Fgf9 and Wnt4 act as antagonistic signals to regulate mammalian sex determination. PLoS Biol 2006, 4:e187.
59. Kim Y., Bingham N., Sekido R., Parker K.L., Lovell-Badge R., Capel B. Fibroblast growth factor receptor 2 regulates proliferation and Sertoli differentiation during male sex determination. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:16558-16563.
60. King P., Paul A., Laufer E. Shh signaling regulates adrenocortical development and identifies progenitors of steroidogenic lineages. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:21185-21190.
61. Klamt B., Koziell A., Poulat F., Wieacker P., Scambler P., Berta P., et al. Frasier syndrome is caused by defective alternative splicing of WT1 leading to an altered ratio of WT1+/-KTS splice isoforms. Hum. Mol. Genet 1998, 7:709-714.
62. Koziell A., Charmandari E., Hindmarsh P.C., Rees L., Scambler P., Brook C.G. Frasier syndrome, part of the Denys Drash continuum or simply a WT1 gene associated disorder of intersex and nephropathy?. Clin. Endocrinol. (Oxf) 2000, 52:519-524.
63. Kreidberg J.A., Sariola H., Loring J.M., Maeda M., Pelletier J., Housman D., et al. WT-1 is required for early kidney development. Cell 1993, 74:679-691.
64. Ladomery M., Sommerville J., Woolner S., Slight J., Hastie N. Expression in Xenopus oocytes shows that WT1 binds transcripts in vivo, with a central role for zinc finger one. J. Cell Sci 2003, 116:1539-1549.
65. Laity J.H., Dyson H.J., Wright P.E. Molecular basis for modulation of biological function by alternate splicing of the Wilms' tumor suppressor protein [In process citation]. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:11932-11935.
66. Larsson S.H., Charlieu J.P., Miyagawa K., Engelkamp D., Rassoulzadegan M., Ross A., et al. Subnuclear localization of WT1 in splicing or transcription factor domains is regulated by alternative splicing. Cell 1995, 81:391-401.
67. Lavery R., Chassot A.A., Pauper E., Gregoire E.P., Klopfenstein M., de Rooij D.G., et al. Testicular differentiation occurs in absence of R-spondin1 and Sox9 in mouse sex reversals. PLoS Genet 2012, 8:e1003170.
68. Little M.H., Williamson K.A., Mannens M., Kelsey A., Gosden C., Hastie N.D., et al. Evidence that WT1 mutations in Denys-Drash syndrome patients may act in a dominant-negative fashion. Hum. Mol. Genet 1993, 2:259-264.
69. Liu C.F., Liu C., Yao H.H. Building pathways for ovary organogenesis in the mouse embryo. Curr. Top. Dev. Biol 2010, 90:263-290.
70. Luo X., Ikeda Y., Parker K.L. A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell 1994, 77:481-490.
71. Maatouk D.M., DiNapoli L., Alvers A., Parker K.L., Taketo M.M., Capel B. Stabilization of beta-catenin in XY gonads causes male-to-female sex-reversal. Hum. Mol. Genet 2008, 17:2949-2955.
72. Madden S.L., Cook D.M., Morris J.F., Gashler A., Sukhatme V.P., Rauscher F.J.I.I.I. Transcriptional repression mediated by the WT1 Wilms tumor gene product. Science 1991, 253:1550-1553.
73. Mandel H., Shemer R., Borochowitz Z.U., Okopnik M., Knopf C., Indelman M., et al. SERKAL syndrome: an autosomal-recessive disorder caused by a loss-of-function mutation in WNT4. Am. J. Hum. Genet 2008, 82:39-47.
74. Manuylov N.L., Fujiwara Y., Adameyko I.I., Poulat F., Tevosian S.G. The regulation of Sox9 gene expression by the GATA4/FOG2 transcriptional complex in dominant XX sex reversal mouse models. Dev. Biol 2007, 307:356-367.
75. Matson C.K., Murphy M.W., Sarver A.L., Griswold M.D., Bardwell V.J., Zarkower D. DMRT1 prevents female reprogramming in the postnatal mammalian testis. Nature 2011, 476:101-104.
76. McNicol A.M., Duffy A.E. A study of cell migration in the adrenal cortex of the rat using bromodeoxyuridine. Cell Tissue Kinet 1987, 20:519-526.
77. Miles C.G., Slight J., Spraggon L., O'Sullivan M., Patek C., Hastie N.D. Mice lacking the 68-amino-acid, mammal-specific N-terminal extension of WT1 develop normally and are fertile. Mol. Cell. Biol 2003, 23:2608-2613.
78. Miyamoto Y., Taniguchi H., Hamel F., Silversides D.W., Viger R.S. A GATA4/WT1 cooperation regulates transcription of genes required for mammalian sex determination and differentiation. BMC Mol. Biol 2008, 9:44.
79. Molyneaux K.A., Stallock J., Schaible K., Wylie C. Time-lapse analysis of living mouse germ cell migration. Dev. Biol 2001, 240:488-498.
80. Moore A.W., McInnes L., Kreidberg J., Hastie N.D., Schedl A. YAC complementation shows a requirement for Wt1 in the development of epicardium, adrenal gland and throughout nephrogenesis. Development 1999, 126:1845-1857.
81. Mork L., Maatouk D.M., McMahon J.A., Guo J.J., Zhang P., McMahon A.P., et al. Temporal differences in granulosa cell specification in the ovary reflect distinct follicle fates in mice. Biol. Reprod 2012, 86:37.
82. Morley S.D., Viard I., Chung B.C., Ikeda Y., Parker K.L., Mullins J.J. Variegated expression of a mouse steroid 21-hydroxylase/beta-galactosidase transgene suggests centripetal migration of adrenocortical cells. Mol. Endocrinol 1996, 10:585-598.
83. Morohashi K. The ontogenesis of the steroidogenic tissues. Genes Cells 1997, 2:95-106.
84. Motamedi F.J., Badro D.A., Clarkson M., Rita Lecca M., Bradford S.T., Buske F.A., et al. WT1 controls antagonistic FGF and BMP-pSMAD pathways in early renal progenitors. Nat. Commun 2014, 5:4444.
85. Muzumdar M.D., Tasic B., Miyamichi K., Li L., Luo L. A global double-fluorescent Cre reporter mouse. Genesis 2007, 45:593-605.
86. Natoli T.A., McDonald A., Alberta J.A., Taglienti M.E., Housman D.E., Kreidberg J.A. A mammal-specific exon of WT1 is not required for development or fertility. Mol. Cell. Biol 2002, 22:4433-4438.
87. Nicol B., Yao H.H. Building an ovary: insights into establishment of somatic cell lineages in the mouse. Sex. Dev 2014, 8:243-251.
88. Nussmann T., Zwemer R.L. A study of the life history of cortico-adrenal gland cells of the rat by means of trypan blue injections. Anat. Rec 1941, 80:421-429.
89. Parma P., Radi O., Vidal V., Chaboissier M.C., Dellambra E., Valentini S., et al. R-spondin1 is essential in sex determination, skin differentiation and malignancy. Nat. Genet 2006, 38:1304-1309.
90. Pelletier J., Bruening W., Li F.P., Haber D.A., Glaser T., Housman D.E. WT1 mutations contribute to abnormal genital system development and hereditary Wilms' tumour. Nature 1991, 353:431-434.
91. Pitetti J.L., Calvel P., Romero Y., Conne B., Truong V., Papaioannou M.D., et al. Insulin and IGF1 receptors are essential for XX and XY gonadal differentiation and adrenal development in mice. PLoS Genet 2013, 9:e1003160.
92. Quinn A., Koopman P. The molecular genetics of sex determination and sex reversal in mammals. Semin. Reprod. Med 2012, 30:351-363.
93. Rao M.K., Pham J., Imam J.S., MacLean J.A., Murali D., Furuta Y., et al. Tissue-specific RNAi reveals that WT1 expression in nurse cells controls germ cell survival and spermatogenesis. Genes Dev 2006, 20:147-152.
94. Rastetter R.H., Bernard P., Palmer J.S., Chassot A.A., Chen H., Western P.S., et al. Marker genes identify three somatic cell types in the fetal mouse ovary. Dev. Biol 2014, 394:242-252.
95. Riccardi V.M., Sujansky E., Smith A.C., Francke U. Chromosomal imbalance in the Aniridia-Wilms' tumor association: 11p interstitial deletion. Pediatrics 1978, 61:604-610.
96. Richard D.J., Schumacher V., Royer-Pokora B., Roberts S.G. Par4 is a coactivator for a splice isoform-specific transcriptional activation domain in WT1. Genes Dev 2001, 15:328-339.
97. Schmahl J., Eicher E.M., Washburn L.L., Capel B. Sry induces cell proliferation in the mouse gonad. Development 2000, 127:65-73.
98. Schmahl J., Kim Y., Colvin J.S., Ornitz D.M., Capel B. Fgf9 induces proliferation and nuclear localization of FGFR2 in Sertoli precursors during male sex determination. Development 2004, 131:3627-3636.
99. Schmidt D., Ovitt C.E., Anlag K., Fehsenfeld S., Gredsted L., Treier A.C., et al. The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development 2004, 131:933-942.
100. Sekido R., Lovell-Badge R. Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 2008, 453:930-934.
101. Srichai M.B., Konieczkowski M., Padiyar A., Konieczkowski D.J., Mukherjee A., Hayden P.S., et al. A WT1 co-regulator controls podocyte phenotype by shuttling between adhesion structures and nucleus. J. Biol. Chem 2004, 279:14398-14408.
102. Suri M., Kelehan P., O'Neill D., Vadeyar S., Grant J., Ahmed S.F., et al. WT1 mutations in Meacham syndrome suggest a coelomic mesothelial origin of the cardiac and diaphragmatic malformations. Am. J. Med. Genet. A 2007, 143A:2312-2320.
103. Svingen T., Koopman P. Building the mammalian testis: origins, differentiation, and assembly of the component cell populations. Genes Dev 2013, 27:2409-2426.
104. Tamura M., Kanno Y., Chuma S., Saito T., Nakatsuji N. 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 2001, 102:135-144.
105. Tevosian S.G., Albrecht K.H., Crispino J.D., Fujiwara Y., Eicher E.M., Orkin S.H. Gonadal differentiation, sex determination and normal Sry expression in mice require direct interaction between transcription partners GATA4 and FOG2. Development 2002, 129:4627-4634.
106. Uhlenhaut N.H., Jakob S., Anlag K., Eisenberger T., Sekido R., Kress J., et al. Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 2009, 139:1130-1142.
107. Vainio S., Heikkila M., Kispert A., Chin N., McMahon A.P. Female development in mammals is regulated by Wnt-4 signalling. Nature 1999, 397:405-409.
108. Val P., Jeays-Ward K., Swain A. Identification of a novel population of adrenal-like cells in the mammalian testis. Dev. Biol 2006, 299:250-256.
109. Val P., Martinez-Barbera J.P., Swain A. Adrenal development is initiated by Cited2 and Wt1 through modulation of Sf-1 dosage. Development 2007, 134:2349-2358.
110. Vidal V.P., Chaboissier M.C., de Rooij D.G., Schedl A. Sox9 induces testis development in XX transgenic mice. Nat. Genet 2001, 28:216-217.
111. Walczak E.M., Hammer G.D. Regulation of the adrenocortical stem cell niche: implications for disease. Nat. Rev. Endocrinol 2015, 11:14-28.
112. Walczak E.M., Kuick R., Finco I., Bohin N., Hrycaj S.M., Wellik D.M., et al. Wnt signaling inhibits adrenal steroidogenesis by cell-autonomous and non-cell-autonomous mechanisms. Mol. Endocrinol 2014, 28:1471-1486.
113. Wang X.N., Li Z.S., Ren Y., Jiang T., Wang Y.Q., Chen M., et al. The Wilms tumor gene, Wt1, is critical for mouse spermatogenesis via regulation of sertoli cell polarity and is associated with non-obstructive azoospermia in humans. PLoS Genet 2013, 9:e1003645.
114. Wilhelm D., Englert C. The Wilms tumor suppressor WT1 regulates early gonad development by activation of Sf1. Genes Dev 2002, 16:1839-1851.
115. Woolley G.W., Dickie M.M., Little C.C. Adrenal tumors and other pathological changes in reciprocal crosses in mice. I. Strain DBA x strain CE and the reciprocal. Cancer Res 1952, 12:142-152.
116. Woolley G.W., Dickie M.M., Little C.C. Adrenal tumors and other pathological changes in reciprocal crosses in mice. II. An introduction to results of four reciprocal crosses. Cancer Res 1953, 13:231-245.
117. Zajicek G., Ariel I., Arber N. The streaming adrenal cortex: direct evidence of centripetal migration of adrenocytes by estimation of cell turnover rate. J. Endocrinol 1986, 111:477-482.
118. Zheng W., Zhang H., Gorre N., Risal S., Shen Y., Liu K. Two classes of ovarian primordial follicles exhibit distinct developmental dynamics and physiological functions. Hum. Mol. Genet 2014, 23:920-928.
119. Zhou B., Ma Q., Rajagopal S., Wu S.M., Domian I., Rivera-Feliciano J., et al. Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 2008, 454:109-113.
120. Zubair M., Ishihara S., Oka S., Okumura K., Morohashi K. Two-step regulation of Ad4BP/SF-1 gene transcription during fetal adrenal development: initiation by a Hox-Pbx1-Prep1 complex and maintenance via autoregulation by Ad4BP/SF-1. Mol. Cell. Biol 2006, 26:4111-4121.