Gonadal identity in the absence of pro-testis factor SOX9 and pro-ovary factor beta-catenin in mice

Biology of Reproduction

Volumn 93, Issue 2, 2015, Pages

  Nicol, Barbara ^a   Yao, Humphrey H C ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

Beta catenin; Sex determination; Sox9; Sry; Testis

Indexed keywords

BETA CATENIN; TRANSCRIPTION FACTOR SOX9; TRANSCRIPTOME; CTNNB1 PROTEIN, MOUSE; CYP26B1 PROTEIN, HUMAN; CYP26B1 PROTEIN, MOUSE; CYTOCHROME P450; CYTOCHROME P450 FAMILY 26; SOX9 PROTEIN, MOUSE; SRY PROTEIN, MOUSE; TESTIS DETERMINING FACTOR;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYP26B1 GENE; DISORDER OF SEX DEVELOPMENT; FEMALE; FETUS; GENE; GENE EXPRESSION; GONAD DEVELOPMENT; KARYOTYPE 46,XX; KARYOTYPE 46,XY; MALE; MORPHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEX DETERMINATION; SEX TRANSFORMATION; SOMATIC CELL; SOX8 GENE; SOX9 GENE; SRY GENE; VIRILIZATION; ANIMAL; EMBRYOLOGY; GENETICS; GONAD; GROWTH, DEVELOPMENT AND AGING; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; PREGNANCY; SEX DETERMINATION PROCESS; SEX DIFFERENTIATION; TESTIS; X CHROMOSOME; Y CHROMOSOME;

ANIMALS; BETA CATENIN; CYTOCHROME P-450 ENZYME SYSTEM; FEMALE; GONADS; MALE; MICE; MICE, KNOCKOUT; PREGNANCY; RETINOIC ACID 4-HYDROXYLASE; SEX DETERMINATION PROCESSES; SEX DIFFERENTIATION; SEX-DETERMINING REGION Y PROTEIN; SOX9 TRANSCRIPTION FACTOR; TESTIS; TRANSCRIPTOME; X CHROMOSOME; Y CHROMOSOME;

EID: 84941559891     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.115.131276     Document Type: Article

References (49)

1. Svingen T, Koopman P. Building the mammalian testis: origins, differentiation, and assembly of the component cell populations. Genes Dev 2013; 27:2409-2426.
2. Sinclair AH, Berta P, Palmer MS, Hawkins JR, Griffiths BL, Smith MJ, Foster JW, Frischauf AM, Lovell-Badge R, Goodfellow PN. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 1990; 346:240-244.
3. Gubbay J, Collignon J, Koopman P, Capel B, Economou A, Munsterberg A, Vivian N, Goodfellow P, Lovellbadge RA. Gene-mapping to the sexdetermining region of the mouse Y-chromosome is a member of a novel family of embryonically expressed genes. Nature 1990; 346:245-250.
4. Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovell-Badge R. Male development of chromosomally female mice transgenic for Sry. Nature 1991; 351:117-121.
5. Hacker A, Capel B, Goodfellow P, Lovell-Badge R. Expression of Sry, the mouse sex determining gene. Development 1995; 121:1603-1614.
6. Hiramatsu R, Matoba S, Kanai-Azuma M, Tsunekawa N, Katoh-Fukui Y, Kurohmaru M, Morohashi K, Wilhelm D, Koopman P, Kanai Y. A critical time window of Sry action in gonadal sex determination in mice. Development 2009; 136:129-138.
7. Sekido R, Lovell-Badge R. Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 2008; 453:930-934.
8. Foster JW, Dominguez-Steglich MA, Guioli S, Kwok C, Weller PA, Stevanovic M, Weissenbach J, Mansour S, Young ID, Goodfellow PN, Brook JD, Schafer AJ. Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature 1994; 372:525-530.
9. Chaboissier MC, Kobayashi A, Vidal VI, Lutzkendorf S, van de Kant HJ, Wegner M, de Rooij DG, Behringer RR, Schedl A. Functional analysis of Sox8 and Sox9 during sex determination in the mouse. Development 2004; 131:1891-1901.
10. Barrionuevo F, Bagheri-Fam S, Klattig J, Kist R, Taketo MM, Englert C, Scherer G. Homozygous inactivation of Sox9 causes complete XY sex reversal in mice. Biol Reprod 2006; 74:195-201.
11. 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: 349-353.
12. Vidal VP, Chaboissier MC, de Rooij DG, Schedl A. Sox9 induces testis development in XX transgenic mice. Nat Genet 2001; 28:216-217.
13. Nicol B, Yao HH. Building an ovary: insights into establishment of somatic cell lineages in the mouse. Sex Dev 2014; 8:243-251.
14. Vainio S, Heikkila M, Kispert A, Chin N, McMahon AP. Female development in mammals is regulated by Wnt-4 signalling. Nature 1999; 397:405-409.
15. 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: 3663-3670.
16. Chassot AA, Ranc F, Gregoire EP, Roepers-Gajadien HL, Taketo MM, Camerino G, de Rooij DG, Schedl A, Chaboissier MC. Activation of betacatenin signaling by Rspo1 controls differentiation of the mammalian ovary. Hum Mol Genet 2008; 17:1264-1277.
17. Tomizuka K, Horikoshi K, Kitada R, Sugawara Y, Iba Y, Kojima A, Yoshitome A, Yamawaki K, Amagai M, Inoue A, Oshima T, Kakitani M. R-spondin1 plays an essential role in ovarian development through positively regulating Wnt-4 signaling. Hum Mol Genet 2008; 17: 1278-1291.
18. Manuylov NL, Smagulova FO, Leach L, Tevosian SG. Ovarian development in mice requires the GATA4-FOG2 transcription complex. Development 2008; 135:3731-3743.
19. Liu CF, Bingham N, Parker K, Yao HH. Sex-specific roles of beta-catenin in mouse gonadal development. Hum Mol Genet 2009; 18:405-417.
20. Maatouk DM, Mork L, Chassot AA, Chaboissier MC, Capel B. Disruption of mitotic arrest precedes precocious differentiation and transdifferentiation of pregranulosa cells in the perinatal Wnt4 mutant ovary. Dev Biol 2013; 383:295-306.
21. Maatouk DM, DiNapoli L, Alvers A, Parker KL, Taketo MM, Capel B. Stabilization of beta-catenin in XY gonads causes male-to-female sexreversal. Hum Mol Genet 2008; 17:2949-2955.
22. Jameson SA, Lin Y-T, Capel B. Testis development requires the repression of Wnt4 by Fgf signaling. Dev Biol 2012; 370:24-32.
23. Lavery R, Chassot AA, Pauper E, Gregoire EP, Klopfenstein M, de Rooij DG, Mark M, Schedl A, Ghyselinck NB, Chaboissier MC. Testicular differentiation occurs in absence of R-spondin1 and Sox9 in mouse sex reversals. PLoS Genet 2012; 8:e1003170.
24. Bingham NC, Verma-Kurvari S, Parada LF, Parker KL. Development of a steroidogenic factor 1/Cre transgenic mouse line. Genesis 2006; 44: 419-424.
25. Jameson SA, Natarajan A, Cool J, DeFalco T, Maatouk DM, Mork L, Munger SC, Capel B. Temporal transcriptional profiling of somatic and germ cells reveals biased lineage priming of sexual fate in the fetal mouse gonad. PLoS Genet 2012; 8:e1002575.
26. Lavery R, Lardenois A, Ranc-Jianmotamedi F, Pauper E, Gregoire EP, Vigier C, Moreilhon C, Primig M, Chaboissier MCXY. Sox9 embryonic loss-of-function mouse mutants show complete sex reversal and produce partially fertile XY oocytes. Dev Biol 2011; 354:111-122.
27. Li Y, Zheng M, Lau YF. The sex-determining factors SRY and SOX9 regulate similar target genes and promote testis cord formation during testicular differentiation. Cell Rep 2014; 8:723-733.
28. Bradford ST, Hiramatsu R, Maddugoda MP, Bernard P, Chaboissier MC, Sinclair A, Schedl A, Harley V, Kanai Y, Koopman P, Wilhelm D. The cerebellin 4 precursor gene is a direct target of SRY and SOX9 in mice. Biol Reprod 2009; 80:1178-1188.
29. Yamauchi Y, Riel JM, Stoytcheva Z, Ward MA. Two Y genes can replace the entire Y chromosome for assisted reproduction in the mouse. Science 2014; 343:69-72.
30. Barrionuevo F, Georg I, Scherthan H, Lecureuil C, Guillou F, Wegner M, Scherer G. Testis cord differentiation after the sex determination stage is independent of Sox9 but fails in the combined absence of Sox9 and Sox8. Dev Biol 2009; 327:301-312.
31. Bullejos M, Koopman P. Delayed Sry and Sox9 expression in developing mouse gonads underlies B6-Y(DOM) sex reversal. Dev Biol 2005; 278: 473-481.
32. Schepers G, Wilson M, Wilhelm D, Koopman P. SOX8 is expressed during testis differentiation in mice and synergizes with SF1 to activate the Amh promoter in vitro. J Biol Chem 2003; 278:28101-28108.
33. Bowles J, Knight D, Smith C, Wilhelm D, Richman J, Mamiya S, Yashiro K, Chawengsaksophak K, Wilson MJ, Rossant J, Hamada H, Koopman P. Retinoid signaling determines germ cell fate in mice. Science 2006; 312: 596-600.
34. Magnan DR, Spacek DV, Ye N, Lu YC, King TR. The male sterility and histoincompatibility (mshi) mutation in mice is a natural variant of microtubule-associated protein 7 (Mtap7). Mol Genet Metab 2009; 97: 155-162.
35. Yao HHC, Whoriskey W, Capel B. Desert Hedgehog/Patched 1 signaling specifies fetal Leydig cell fate in testis organogenesis. Genes Dev 2002; 16:1433-1440.
36. Wilhelm D, Martinson F, Bradford S, Wilson MJ, Combes AN, Beverdam A, Bowles J, Mizusaki H, Koopman P. Sertoli cell differentiation is induced both cell-autonomously and through prostaglandin signaling during mammalian sex determination. Dev Biol 2005; 287:111-124.
37. Moniot B, Declosmenil F, Barrionuevo F, Scherer G, Aritake K, Malki S, Marzi L, Cohen-Solal A, Georg I, Klattig J, Englert C, Kim Y, et al. The PGD2 pathway, independently of FGF9, amplifies SOX9 activity in Sertoli cells during male sexual differentiation. Development 2009; 136: 1813-1821.
38. Munger SC, Natarajan A, Looger LL, Ohler U, Capel B. Fine time course expression analysis identifies cascades of activation and repression and maps a putative regulator of mammalian sex determination. PLoS Genet 2013; 9:e1003630.
39. Yao HH, Aardema J, Holthusen K. Sexually dimorphic regulation of inhibin beta B in establishing gonadal vasculature in mice. Biol Reprod 2006; 74:978-983.
40. Bernard P, Ryan J, Sim H, Czech DP, Sinclair AH, Koopman P, Harley VR. Wnt signaling in ovarian development inhibits Sf1 activation of Sox9 via the Tesco enhancer. Endocrinology 2012; 153:901-912.
41. Kormish JD, Sinner D, Zorn AM. Interactions between SOX factors and Wnt/beta-catenin signaling in development and disease. Dev Dyn 2010; 239:56-68.
42. Pierucci-Alves F, Clark AM, Russell LD. A developmental study of the Desert hedgehog-null mouse testis. Biol Reprod 2001; 65:1392-1402.
43. Wilhelm D, Hiramatsu R, Mizusaki H, Widjaja L, Combes AN, Kanai Y, Koopman P. SOX9 regulates prostaglandin D synthase gene transcription in vivo to ensure testis development. J Biol Chem 2007; 282: 10553-10560.
44. 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; 18:6653-6665.
45. Sekido R, Lovell-Badge R. Genetic control of testis development. Sex Dev 2013; 7:21-32.
46. Bhandari RK, Haque MM, Skinner MK. Global genome analysis of the downstream binding targets of testis determining factor SRY and SOX9. PLoS One 2012; 7:e43380.
47. Sock E, Schmidt K, Hermanns-Borgmeyer I, Bosl MR, Wegner M. Idiopathic weight reduction in mice deficient in the high-mobility-group transcription factor Sox8. Mol Cell Biol 2001; 21:6951-6959.
48. Chalmel F, Lardenois A, Georg I, Barrionuevo F, Demougin P, Jegou B, Scherer G, Primig M. Genome-wide identification of Sox8-, and Sox9-dependent genes during early post-natal testis development in the mouse. Andrology 2013; 1:281-292.
49. Ohnesorg T, Vilain E, Sinclair AH. The genetics of disorders of sex development in humans. Sex Dev 2014; 8:262-272.