Testicular Differentiation Occurs in Absence of R-spondin1 and Sox9 in Mouse Sex Reversals

PLoS Genetics

Volumn 8, Issue 12, 2012, Pages

  Lavery, Rowena ^a,b   Chassot, Anne Amandine ^a,b   Pauper, Eva ^a,b   Gregoire, Elodie P ^a,b   Klopfenstein, Muriel ^c   de Rooij, Dirk G ^d   Mark, Manuel ^c   Schedl, Andreas ^a,b   Ghyselinck, Norbert B ^c   Chaboissier, Marie Christine ^a,b  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b CENTRE DE BIOCHIMIE   (France)

^c INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^d ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR SOX10; TRANSCRIPTION FACTOR SOX8; TRANSCRIPTION FACTOR SOX9;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; FEMALE; GENE; GENE EXPRESSION; GERM CELL; MALE; MEIOSIS; MOUSE; NONHUMAN; OVARY DEVELOPMENT; R SPONDIN1 GENE; SEMINIFEROUS TUBULE; SERTOLI CELL; SEX DETERMINATION; SEX DIFFERENTIATION; SOX9 GENE; SRY GENE; TESTIS DEVELOPMENT;

ANIMALS; CELL DIFFERENTIATION; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, SRY; HUMANS; MALE; MICE; OVARY; SEX DETERMINATION PROCESSES; SEX DIFFERENTIATION; SIGNAL TRANSDUCTION; SOX9 TRANSCRIPTION FACTOR; TESTIS; THROMBOSPONDINS; WNT SIGNALING PATHWAY;

MAMMALIA; MUS;

EID: 84872038015     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003170     Document Type: Article

References (73)

1. DeFalco T, Capel B, (2009) Gonad morphogenesis in vertebrates: divergent means to a convergent end. Annu Rev Cell Dev Biol 25: 457-482.
2. Gubbay J, Collignon J, Koopman P, Capel B, Economou A, et al. (1990) 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 346: 245-250.
3. Sinclair AH, Berta P, Palmer MS, Hawkins JR, Griffiths BL, et al. (1990) A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346: 240-244.
4. Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovell-Badge R, (1991) Male development of chromosomally female mice transgenic for Sry. Nature 351: 117-121.
5. Sekido R, Lovell-Badge R, (2008) Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453: 930-934.
6. Barrionuevo F, Bagheri-Fam S, Klattig J, Kist R, Taketo MM, et al. (2006) Homozygous inactivation of Sox9 causes complete XY sex reversal in mice. Biol Reprod 74: 195-201.
7. Chaboissier MC, Kobayashi A, Vidal VI, Lutzkendorf S, van de Kant HJ, et al. (2004) Functional analysis of Sox8 and Sox9 during sex determination in the mouse. Development 131: 1891-1901.
8. Hiramatsu R, Harikae K, Tsunekawa N, Kurohmaru M, Matsuo I, et al. (2010) FGF signaling directs a center-to-pole expansion of tubulogenesis in mouse testis differentiation. Development 137: 303-312.
9. Yao HH, Whoriskey W, Capel B, (2002) Desert Hedgehog/Patched 1 signaling specifies fetal Leydig cell fate in testis organogenesis. Genes Dev 16: 1433-1440.
10. DeFalco T, Takahashi S, Capel B, (2011) Two distinct origins for Leydig cell progenitors in the fetal testis. Dev Biol 352: 14-26.
11. Barrios F, Filipponi D, Pellegrini M, Paronetto MP, Di Siena S, et al. (2010) Opposing effects of retinoic acid and FGF9 on Nanos2 expression and meiotic entry of mouse germ cells. J Cell Sci 123: 871-880.
12. Bowles J, Feng CW, Spiller C, Davidson TL, Jackson A, et al. (2010) FGF9 suppresses meiosis and promotes male germ cell fate in mice. Dev Cell 19: 440-449.
13. Berta P, Hawkins JR, Sinclair AH, Taylor A, Griffiths BL, et al. (1990) Genetic evidence equating SRY and the testis-determining factor. Nature 348: 448-450.
14. Wagner T, Wirth J, Meyer J, Zabel B, Held M, et al. (1994) Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 79: 1111-1120.
15. Lovell-Badge R, Robertson E, (1990) XY female mice resulting from a heritable mutation in the primary testis-determining gene, Tdy. Development 109: 635-646.
16. Lavery R, Lardenois A, Ranc-Jianmotamedi F, Pauper E, Gregoire EP, et al. (2011) XY Sox9 embryonic loss-of-function mouse mutants show complete sex reversal and produce partially fertile XY oocytes. Dev Biol 354: 111-122.
17. Vidal VP, Chaboissier MC, de Rooij DG, Schedl A, (2001) Sox9 induces testis development in XX transgenic mice. Nat Genet 28: 216-217.
18. Bishop CE, Whitworth DJ, Qin Y, Agoulnik AI, Agoulnik IU, et al. (2000) A transgenic insertion upstream of sox9 is associated with dominant XX sex reversal in the mouse. Nat Genet 26: 490-494.
19. Parma P, Radi O, Vidal V, Chaboissier MC, Dellambra E, et al. (2006) R-spondin1 is essential in sex determination, skin differentiation and malignancy. Nat Genet 38: 1304-1309.
20. Chassot AA, Ranc F, Gregoire EP, Roepers-Gajadien HL, Taketo MM, et al. (2008) Activation of beta-catenin signaling by Rspo1 controls differentiation of the mammalian ovary. Hum Mol Genet 17: 1264-1277.
21. Tomizuka K, Horikoshi K, Kitada R, Sugawara Y, Iba Y, et al. (2008) R-spondin1 plays an essential role in ovarian development through positively regulating Wnt-4 signaling. Hum Mol Genet 17: 1278-1291.
22. Vainio S, Heikkila M, Kispert A, Chin N, McMahon AP, (1999) Female development in mammals is regulated by Wnt-4 signalling. Nature 397: 405-409.
23. Maatouk DM, DiNapoli L, Alvers A, Parker KL, Taketo MM, et al. (2008) Stabilization of beta-catenin in XY gonads causes male-to-female sex-reversal. Hum Mol Genet 17: 2949-2955.
24. Manuylov NL, Smagulova FO, Leach L, Tevosian SG, (2008) Ovarian development in mice requires the GATA4-FOG2 transcription complex. Development 135: 3731-3743.
25. Schmidt D, Ovitt CE, Anlag K, Fehsenfeld S, Gredsted L, et al. (2004) The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development 131: 933-942.
26. Ottolenghi C, Omari S, Garcia-Ortiz JE, Uda M, Crisponi L, et al. (2005) Foxl2 is required for commitment to ovary differentiation. Hum Mol Genet 14: 2053-2062.
27. Uhlenhaut NH, Jakob S, Anlag K, Eisenberger T, Sekido R, et al. (2009) Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 139: 1130-1142.
28. Uda M, Ottolenghi C, Crisponi L, Garcia JE, Deiana M, et al. (2004) Foxl2 disruption causes mouse ovarian failure by pervasive blockage of follicle development. Hum Mol Genet 13: 1171-1181.
29. Raymond CS, Murphy MW, O'Sullivan MG, Bardwell VJ, Zarkower D, (2000) Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev 14: 2587-2595.
30. Joseph A, Yao H, Hinton BT, (2009) Development and morphogenesis of the Wolffian/epididymal duct, more twists and turns. Dev Biol 325: 6-14.
31. Auguste A, Chassot AA, Gregoire EP, Renault L, Pannetier M, et al. (2011) Loss of R-spondin1 and Foxl2 amplifies female-to-male sex reversal in XX mice. Sex Dev 5: 304-317.
32. Jeays-Ward K, Hoyle C, Brennan J, Dandonneau M, Alldus G, et al. (2003) Endothelial and steroidogenic cell migration are regulated by WNT4 in the developing mammalian gonad. Development 130: 3663-3670.
33. Jeays-Ward K, Dandonneau M, Swain A, (2004) Wnt4 is required for proper male as well as female sexual development. Dev Biol 276: 431-440.
34. Heikkila M, Prunskaite R, Naillat F, Itaranta P, Vuoristo J, et al. (2005) The partial female to male sex reversal in Wnt-4-deficient females involves induced expression of testosterone biosynthetic genes and testosterone production, and depends on androgen action. Endocrinology 146: 4016-4023.
35. Val P, Jeays-Ward K, Swain A, (2006) Identification of a novel population of adrenal-like cells in the mammalian testis. Dev Biol 299: 250-256.
36. Nel-Themaat L, Gonzalez G, Akiyama H, Behringer RR, (2010) Illuminating testis morphogenesis in the mouse. J Androl 31: 5-10.
37. Behringer RR, Finegold MJ, Cate RL, (1994) Mullerian-inhibiting substance function during mammalian sexual development. Cell 79: 415-425.
38. Bullejos M, Koopman P, (2001) Spatially dynamic expression of Sry in mouse genital ridges. Dev Dyn 221: 201-205.
39. Hacker A, Capel B, Goodfellow P, Lovell-Badge R, (1995) Expression of Sry, the mouse sex determining gene. Development 121: 1603-1614.
40. Jeske YW, Bowles J, Greenfield A, Koopman P, (1995) Expression of a linear Sry transcript in the mouse genital ridge. Nat Genet 10: 480-482.
41. 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.
42. Isotani A, Nakanishi T, Kobayashi S, Lee J, Chuma S, et al. (2005) Genomic imprinting of XX spermatogonia and XX oocytes recovered from XX<->XY chimeric testes. Proc Natl Acad Sci U S A 102: 4039-4044.
43. Chassot AA, Gregoire EP, Lavery R, Taketo MM, de Rooij DG, et al. (2011) RSPO1/beta-catenin signaling pathway regulates oogonia differentiation and entry into meiosis in the mouse fetal ovary. PLoS ONE 6: e25641 doi:10.1371/journal.pone.0025641.
44. Maldonado-Saldivia J, van den Bergen J, Krouskos M, Gilchrist M, Lee C, et al. (2007) Dppa2 and Dppa4 are closely linked SAP motif genes restricted to pluripotent cells and the germ line. Stem Cells 25: 19-28.
45. Li H, MacLean G, Cameron D, Clagett-Dame M, Petkovich M, (2009) Cyp26b1 expression in murine Sertoli cells is required to maintain male germ cells in an undifferentiated state during embryogenesis. PLoS ONE 4: e7501 doi:10.1371/journal.pone.0007501.
46. MacLean G, Li H, Metzger D, Chambon P, Petkovich M, (2007) Apoptotic extinction of germ cells in testes of Cyp26b1 knockout mice. Endocrinology 148: 4560-4567.
47. Baltus AE, Menke DB, Hu YC, Goodheart ML, Carpenter AE, et al. (2006) In germ cells of mouse embryonic ovaries, the decision to enter meiosis precedes premeiotic DNA replication. Nat Genet 38: 1430-1434.
48. Arango NA, Lovell-Badge R, Behringer RR, (1999) Targeted mutagenesis of the endogenous mouse Mis gene promoter: in vivo definition of genetic pathways of vertebrate sexual development. Cell 99: 409-419.
49. De Santa Barbara P, Bonneaud N, Boizet B, Desclozeaux M, Moniot B, et al. (1998) Direct interaction of SRY-related protein SOX9 and steroidogenic factor 1 regulates transcription of the human anti-Mullerian hormone gene. Mol Cell Biol 18: 6653-6665.
50. Schepers G, Wilson M, Wilhelm D, Koopman P, (2003) SOX8 is expressed during testis differentiation in mice and synergizes with SF1 to activate the Amh promoter in vitro. J Biol Chem 278: 28101-28108.
51. Polanco JC, Wilhelm D, Davidson TL, Knight D, Koopman P, (2010) Sox10 gain-of-function causes XX sex reversal in mice: implications for human 22q-linked disorders of sex development. Hum Mol Genet 19: 506-516.
52. Barrionuevo F, Georg I, Scherthan H, Lecureuil C, Guillou F, et al. (2009) Testis cord differentiation after the sex determination stage is independent of Sox9 but fails in the combined absence of Sox9 and Sox8. Dev Biol 327: 301-312.
53. Sutton E, Hughes J, White S, Sekido R, Tan J, et al. (2011) Identification of SOX3 as an XX male sex reversal gene in mice and humans. J Clin Invest 121: 328-341.
54. Matson CK, Murphy MW, Sarver AL, Griswold MD, Bardwell VJ, et al. (2011) DMRT1 prevents female reprogramming in the postnatal mammalian testis. Nature 476: 101-104.
55. Gao F, Maiti S, Alam N, Zhang Z, Deng JM, et al. (2006) 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 103: 11987-11992.
56. Kim Y, Kobayashi A, Sekido R, Dinapoli L, Brennan J, et al. (2006) Fgf9 and wnt4 act as antagonistic signals to regulate Mammalian sex determination. PLoS Biol 4: e187 doi:10.1371/journal.pbio.0040187.
57. Moniot B, Farhat A, Aritake K, Declosmenil F, Nef S, et al. (2011) Hematopoietic prostaglandin D synthase (H-Pgds) is expressed in the early embryonic gonad and participates to the initial nuclear translocation of the SOX9 protein. Dev Dyn 240: 2335-2343.
58. Adams IR, McLaren A, (2002) Sexually dimorphic development of mouse primordial germ cells: switching from oogenesis to spermatogenesis. Development 129: 1155-1164.
59. Wilhelm D, Martinson F, Bradford S, Wilson MJ, Combes AN, et al. (2005) Sertoli cell differentiation is induced both cell-autonomously and through prostaglandin signaling during mammalian sex determination. Dev Biol 287: 111-124.
60. Kim Y, Bingham N, Sekido R, Parker KL, Lovell-Badge R, et al. (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.
61. Jost A, (1947) Recherche sur la différenciation sexuelle de l'embryon de lapin. Arch Anat Microsc Morph Exp pp. 271-315.
62. McLaren A, (1991) Development of the mammalian gonad: the fate of the supporting cell lineage. Bioessays 13: 151-156.
63. Munger SC, Aylor DL, Syed HA, Magwene PM, Threadgill DW, et al. (2009) Elucidation of the transcription network governing mammalian sex determination by exploiting strain-specific susceptibility to sex reversal. Genes Dev 23: 2521-2536.
64. Bingham NC, Verma-Kurvari S, Parada LF, Parker KL, (2006) Development of a steroidogenic factor 1/Cre transgenic mouse line. Genesis 44: 419-424.
65. Hogan BL, Beddington RS, F C, E L (1994) Manipulating the Mouse Embryo. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
66. Bradford ST, Wilhelm D, Koopman P, (2007) Comparative analysis of anti-mouse SRY antibodies. Sex Dev 1: 305-310.
67. Wilkinson DG (1992) Whole mount in situ hybridization of vertebrate embryos. Whole mount in situ hybridization of vertebrate embryos Oxford: Oxford University Press: 75-83.
68. Morais da Silva S, Hacker A, Harley V, Goodfellow P, Swain A, et al. (1996) Sox9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nat Genet 14: 62-68.
69. Sock E, Schmidt K, Hermanns-Borgmeyer I, Bosl MR, Wegner M, (2001) Idiopathic weight reduction in mice deficient in the high-mobility-group transcription factor Sox8. Mol Cell Biol 21: 6951-6959.
70. Vernet N, Dennefeld C, Rochette-Egly C, Oulad-Abdelghani M, Chambon P, et al. (2006) Retinoic acid metabolism and signaling pathways in the adult and developing mouse testis. Endocrinology 147: 96-110.
71. DeBlock M, Debrouwer D, (1993) RNA-RNA in situ hybridization using digoxigenin-labeled probes: the use of high-molecular-weight polyvinyl alcohol in the alkaline phosphatase indoxyl-nitroblue tetrazolium reaction. Anal Biochem 215: 86-89.
72. Jameson SA, Lin YT, Capel B, (2012) Testis development requires the repression of Wnt4 by Fgf signaling. Dev Biol.
73. Hunt PA, Worthman C, Levinson H, Stallings J, LeMaire R, et al. (1998) Germ cell loss in the XXY male mouse: altered X-chromosome dosage affects prenatal development. Mol Reprod Dev 49: 101-111.