The sex-determining factors SRY and SOX9 regulate similar target genes and promote testis cord formation during testicular differentiation

Cell Reports

Volumn 8, Issue 3, 2014, Pages 723-733

  Li, Yunmin ^a,b   Zheng, Ming ^c   Lau, Yun Fai Chris ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; TESTIS DETERMINING FACTOR; TRANSCRIPTION FACTOR SOX9; WNT PROTEIN; SOX9 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL JUNCTION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; FETUS; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENE FREQUENCY; GENE INTERACTION; GENE REPRESSION; GENE TARGETING; GENETIC SIMILARITY; GERM CELL; GONAD DEVELOPMENT; INTRACELLULAR SIGNALING; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN INTERACTION; SERTOLI CELL; SEX DETERMINATION; TESTIS CORD DEVELOPMENT; TESTIS DEVELOPMENT; UPREGULATION; WNT SIGNALING PATHWAY; ANIMAL; CYTOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; SEX DETERMINATION PROCESS;

ANIMALS; CELL DIFFERENTIATION; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MICE; SERTOLI CELLS; SEX DETERMINATION PROCESSES; SEX-DETERMINING REGION Y PROTEIN; SOX9 TRANSCRIPTION FACTOR; WNT SIGNALING PATHWAY;

EID: 84924619591     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.06.055     Document Type: Article

References (38)

1. Bergstrom, D.E., Young, M., Albrecht, K.H., and Eicher, E.M. (2000). Related function of mouse SOX3, SOX9, and SRY HMG domains assayed by male sex determination. Genesis 28, 111-124.
2. Bishop, C.E., Whitworth, D.J., Qin, Y., Agoulnik, A.I., Agoulnik, I.U., Harrison, W.R., Behringer, R.R., and Overbeek, P.A. (2000). A transgenic insertion upstream of sox9 is associated with dominant XX sex reversal in the mouse. Nat. Genet. 26, 490-494.
3. Bowles, J., Knight, D., Smith, C., Wilhelm, D., Richman, J., Mamiya, S., Yashiro, K., Chawengsaksophak, K., Wilson, M.J., Rossant, J., et al. (2006). Retinoid signaling determines germ cell fate in mice. Science 312, 596-600.
4. Bradford, S.T., Hiramatsu, R., Maddugoda, M.P., Bernard, P., Chaboissier, M.C., Sinclair, A., Schedl, A., Harley, V., Kanai, Y., Koopman, P., and Wilhelm, D. (2009). The cerebellin 4 precursor gene is a direct target of SRY and SOX9 in mice. Biol. Reprod. 80, 1178-1188.
5. Cai, S., Lee, C.C., and Kohwi-Shigematsu, T. (2006). SATB1 packages densely looped, transcriptionally active chromatin for coordinated expression of cytokine genes. Nat. Genet. 38, 1278-1288.
6. Chaboissier, M.C., Kobayashi, A., Vidal, V.I., Lützkendorf, S., van de Kant, H.J., Wegner, M., de Rooij, D.G., Behringer, R.R., and Schedl, A. (2004). Functional analysis of Sox8 and Sox9 during sex determination in the mouse. Development 131, 1891-1901.
7. Chawengsaksophak, K., Svingen, T., Ng, E.T., Epp, T., Spiller, C.M., Clark, C., Cooper, H., and Koopman, P. (2012). Loss of Wnt5a disrupts primordial germ cell migration and male sexual development in mice. Biol. Reprod. 86, 1-12.
8. Cheng, C.Y., and Mruk, D.D. (2012). The blood-testis barrier and its implications for male contraception. Pharmacol. Rev. 64, 16-64.
9. Clark, A.M., Garland, K.K., and Russell, L.D. (2000). 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. 63, 1825-1838.
10. Colvin, J.S., Green, R.P., Schmahl, J., Capel, B., and Ornitz, D.M. (2001). Male-to-female sex reversal in mice lacking fibroblast growth factor 9. Cell 104, 875-889.
11. Cool, J., DeFalco, T., and Capel, B. (2012). Testis formation in the fetal mouse: dynamic and complex de novo tubulogenesis. Wiley Interdiscip Rev Dev Biol 1, 847-859.
12. Foster, J.W. (1996). Mutations in SOX9 cause both autosomal sex reversal and campomelic dysplasia. Acta Paediatr. Jpn. 38, 405-411.
13. Gubbay, J., Collignon, J., Koopman, P., Capel, B., Economou, A., Münsterberg, A., Vivian, N., Goodfellow, P., and Lovell-Badge, R. (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.
14. Jameson, S.A., Natarajan, A., Cool, J., DeFalco, T., Maatouk, D.M., Mork, L., Munger, S.C., and Capel, B. (2012). Temporal transcriptional profiling of somatic and germ cells reveals biased lineage priming of sexual fate in the fetal mouse gonad. PLoS Genet. 8, e1002575.
15. Karolchik, D., Hinrichs, A.S., and Kent, W.J. (2011). The UCSC Genome Browser. Curr. Protoc. Hum. Genet. Chapter 18, Unit 18 16.
16. Lau, Y.F., and Li, Y. (2009). The human and mouse sex-determining SRY genes repress the Rspol/beta-catenin signaling. J. Genet. Genomics 36, 193-202.
17. Li, Y., Oh, H.J., and Lau, Y.F. (2006). The poly(ADP-ribose) polymerase 1 interacts with Sry and modulates its biological functions. Mol. Cell. Endocrinol. 257-258, 35-46.
18. Li, Y., Taketo, T., and Lau, Y.F. (2012). Isolation of fetal gonads from embryos of timed-pregnant mice for morphological and molecular studies. Methods Mol. Biol. 825, 3-16.
19. Maatouk, D.M., DiNapoli, L., Alvers, A., Parker, K.L., Taketo, M.M., and Capel, B. (2008). Stabilization of beta-catenin in XY gonads causes male-to-female sex-reversal. Hum. Mol. Genet. 17, 2949-2955.
20. McGuinness, M.P., Linder, C.C., Morales, C.R., Heckert, L.L., Pikus, J., and Griswold, M.D. (1994). Relationship of a mouse Sertoli cell line (MSC-1) to normal Sertoli cells. Biol. Reprod. 51, 116-124.
21. McLaren, A. (1991). Development of the mammalian gonad: the fate of the supporting cell lineage. BioEssays 13, 151-156.
22. Oatley, J.M., and Brinster, R.L. (2008). Regulation of spermatogonial stem cell self-renewal in mammals. Annu. Rev. Cell Dev. Biol. 24, 263-286.
23. Oh, H.J., and Lau, Y.F. (2006). KRAB: a partner for SRY action on chromatin. Mol. Cell. Endocrinol. 247, 47-52.
24. Oh, H.J., Li, Y., and Lau, Y.F. (2005). Sry associates with the heterochromatin protein 1 complex by interacting with a KRAB domain protein. Biol. Reprod. 72, 407-415.
25. Peng, H., Ivanov, A.V., Oh, H.J., Lau, Y.F., and Rauscher, F.J., 3rd. (2009). Epigenetic gene silencing by the SRY protein is mediated by a KRAB-O protein that recruits the KAP1 co-repressor machinery. J. Biol. Chem. 284, 35670-35680.
26. Qin, Y., Kong, L.K., Poirier, C., Truong, C., Overbeek, P.A., and Bishop, C.E. (2004). Long-range activation of Sox9 in Odd Sex (Ods) mice. Hum. Mol. Genet. 13, 1213-1218.
27. Sekido, R., and Lovell-Badge, R. (2008). Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453, 930-934.
28. Sekido, R., and Lovell-Badge, R. (2009). Sex determination and SRY: down to a wink and a nudge? Trends Genet. 25, 19-29.
29. Sinclair, A.H., Berta, P., Palmer, M.S., Hawkins, J.R., Griffiths, B.L., Smith, M.J., Foster, J.W., Frischauf, A.M., Lovell-Badge, R., and Goodfellow, P.N. (1990). A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346, 240-244.
30. Svingen, T., and Koopman, P. (2013). Building the mammalian testis: origins, differentiation, and assembly of the component cell populations. Genes Dev. 27, 2409-2426.
31. Taketo, T., Lee, C.H., Zhang, J., Li, Y., Lee, C.Y., and Lau, Y.F. (2005). Expression of SRY proteins in both normal and sex-reversed XY fetal mouse gonads. Dev. Dyn. 233, 612-622.
32. Vidal, V.P., Chaboissier, M.C., de Rooij, D.G., and Schedl, A. (2001). Sox9 induces testis development in XX transgenic mice. Nat. Genet. 28, 216-217.
33. Wilhelm, D., Martinson, F., Bradford, S., Wilson, M.J., Combes, A.N., Beverdam, A., Bowles, J., Mizusaki, H., and Koopman, P. (2005). Sertoli cell differentiation is induced both cell-autonomously and through prostaglandin signaling during mammalian sex determination. Dev. Biol. 287, 111-124.
34. Wilhelm, D., Hiramatsu, R., Mizusaki, H., Widjaja, L., Combes, A.N., Kanai, Y., and Koopman, P. (2007). SOX9 regulates prostaglandin D synthase gene transcription in vivo to ensure testis development. J. Biol. Chem. 282, 10553-10560.
35. Wissmüller, S., Kosian, T., Wolf, M., Finzsch, M., and Wegner, M. (2006). The high-mobility-group domain of Sox proteins interacts with DNA-binding domains of many transcription factors. Nucleic Acids Res. 34, 1735-1744.
36. Wu, J.B., Chen, K., Li, Y., Lau, Y.F., and Shih, J.C. (2009). Regulation of monoamine oxidase A by the SRY gene on the Y chromosome. FASEB J. 23, 4029-4038.
37. Yao, H.H., Whoriskey, W., and Capel, B. (2002). Desert Hedgehog/Patched 1 signaling specifies fetal Leydig cell fate in testis organogenesis. Genes Dev. 16, 1433-1440.
38. Zheng, M., Li, Y.M., and Lau, Y.-F.C. (2013). Application of the simple and efficient Mpeak modeling in binding peak identification in ChIP-chip studies. In Tiling Arrays: Methods and Protocols, T.L. Lee and A.C.S. Luk, eds. (New York: Humanna Press).