Direct Interaction of SRY-Related Protein SOX9 and Steroidogenic Factor 1 Regulates Transcription of the Human Anti-Müllerian Hormone Gene

REFERENCES

• Ambrosetti, D.-C., C. Basilico, and L. Dailey 1997. Synergistic activation of the fibroblast growth factor 4 enhancer by Sox2 and Oct-3 depends on protein-protein interactions facilitated by a specific spatial arrangement of factor binding sites. Mol. Cell. Biol. 17: 6321–6329.
   PubMedGoogle Scholar
• Bell, D. M., K. K. H. Leung, S. C. Wheatley, L. J. Ng, S. Zhou, K. W. Ling, M. H. Sham, P. Koopman, P. P. L. Tam, and K. S. E. Cheah 1997. SOX9 directly regulates the type-II collagen gene. Nat. Genet. 16: 174–178.
   PubMed Web of Science ®Google Scholar
• Carré-Eusèbe, D., N. Di Clemente, R. Rey, C. Pieau, B. Vigier, N. Josso, and J.-Y. Picard 1996. Cloning and expression of the chick anti-Müllerian hormone gene. J. Biol. Chem. 271: 4798–4804.
   PubMedGoogle Scholar
• Clépet, C., A. J. Schafer, A. H. Sinclair, M. S. Palmer, R. Lovell-Badge, and P. N. Goodfellow 1993. The human SRY transcript. Hum. Mol. Genet. 2: 2007–2012.
   PubMed Web of Science ®Google Scholar
• Crawford, P. A., C. Dorn, Y. Sadovsky, and J. Milbrandt 1998. Nuclear receptor DAX-1 recruits nuclear receptor corepressor N-CoR to steroidogenic factor 1. Mol. Cell. Biol. 18: 2949–2956.
   PubMed Web of Science ®Google Scholar
• Crawford, P. A., J. A. Polish, G. Ganpule, and Y. Sadovski 1997. The activation function-2 hexamer is required, but not sufficient, for potentiation by SRC-1. Mol. Endocrinol. 11: 1626–1635.
   PubMedGoogle Scholar
• Denny, P., S. Swift, F. Connor, and A. Ashworth 1992. An SRY-related gene expressed during spermatogenesis in the mouse encodes a sequence-specific DNA-binding protein. EMBO J. 11: 3705–3712.
   PubMedGoogle Scholar
• Desclozeaux, M., F. Poulat, P. de Santa Barbara, J.-P. Capony, P. Turowski, P. Jay, C. Mejean, B. Moniot, B. Boizet, and P. Berta 1997. Phosphorylation of an N-terminal motif enhances DNA-binding activity of the human SRY protein. J. Biol. Chem. 273: 7988–7995.
   Google Scholar
• Dubin, R. A., and H. Ostrer 1994. Sry is a transcriptional activator. Mol. Endocrinol. 8: 1182–1192.
   PubMedGoogle Scholar
• Foster, J. W., M. A. Dominguez-Steglich, S. Guioli, C. Kwok, P. A. Weller, M. Stevanovic, J. Weissenbach, S. Mansour, I. D. Young, P. N. Goodfellow, J. D. Brook, and A. J. Schafer 1994. Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature 372: 525–530.
   PubMed Web of Science ®Google Scholar
• Fromont-Racine, M., J.-C. Rain, and P. Legrain 1997. Toward a functional analysis of the yeast genome through exhaustive two-hybrid screens. Nat. Genet. 16: 277–282.
   PubMed Web of Science ®Google Scholar
• Giese, K., J. Cox, and R. Grosschedl 1992. The HMG domain of lymphoid enhancer factor-1 bends DNA and facilitates assembly of functional nucleoprotein structures. Cell 69: 185–195.
   PubMed Web of Science ®Google Scholar
• Giuili, G., W.-H. Shen, and H. A. Ingraham 1997. The nuclear receptor SF-1 mediates sexually dimorphic expression of Müllerian inhibiting substance, in vivo. Development 124: 1799–1807.
   PubMedGoogle Scholar
• Greenfield, A., and P. Koopman 1996. SRY and mammalian sex determination. Curr. Top. Dev. Biol. 34: 1–23.
   PubMedGoogle Scholar
• Gubbay, J., J. Collignon, P. Koopman, B. Capel, A. Economou, A. Munsterberg, N. Vivian, P. Goodfellow, and R. Lovell-Badge 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.
   PubMed Web of Science ®Google Scholar
• Guerrier, D., L. Boussin, S. Mader, N. Josso, A. Khan, and J.-Y. Picard 1990. Expression of the gene for anti-Müllerian hormone. J. Reprod. Fertil. 88: 695–706.
   PubMedGoogle Scholar
• Guerrier, D., D. Tran, J. M. Vanderwinden, S. Hideux, L. Van Outryve, L. Legeai, M. Bouchard, G. Van Vliet, M. H. De Laet, J. Y. Picard, and N. Josso 1989. The persistent Müllerian duct syndrome: a molecular approach. J. Clin. Endocrinol. Metab. 68: 46–52.
   PubMed Web of Science ®Google Scholar
• Hacker, A., B. Capel, P. Goodfellow, and R. Lovell-Badge 1995. Expression of Sry, the mouse sex determining gene. Development 121: 1603–1614.
   PubMedGoogle Scholar
• Haqq, C. M., C. Y. King, P. K. Donahoe, and M. A. Weiss 1993. SRY recognizes conserved DNA sites in sex-specific promoters. Proc. Natl. Acad. Sci. USA 90: 1097–1101.
   PubMed Web of Science ®Google Scholar
• Haqq, C. M., C.-Y. King, E. Ukiyama, S. Falsafi, T. N. Haqq, P. K. Donahoe, and M. A. Weiss 1994. Molecular basis of mammalian sexual determination: activation of Müllerian inhibiting substance gene expression by SRY. Science 266: 1494–1500.
   PubMed Web of Science ®Google Scholar
• Harley, V. R., and P. N. Goodfellow 1994. The biochemical role of SRY in sex determination. Mol. Reprod. Dev. 39: 184–193.
   PubMedGoogle Scholar
• Harley, V. R., D. Jackson, P. Hextall, J. R. Hawkins, G. D. Berkovitz, S. Sockanathan, R. Lovell-Badge, and P. N. Goodfellow 1992. DNA binding activity of recombinant SRY from normal males and XY females. Science 255: 453–456.
   PubMed Web of Science ®Google Scholar
• Honda, S., K. Morohashi, M. Nomura, H. Takeya, M. Kitajima, and T. Omura 1993. Ad4BP regulating steroidogenic P-450 gene is a member of steroid hormone receptor superfamily. J. Biol. Chem. 268: 7494–7502.
   PubMed Web of Science ®Google Scholar
• Jay, P., S. Diriong, S. Taviaux, N. Roeckel, M.-G. Mattéi, M. Audit, J.-L. Bergé-Lefranc, M. Fontes, and P. Berta 1996. Isolation and regional mapping of cDNAs expressed during early human development. Genomics 39: 104–108.
   Google Scholar
• Josso, N., R. L. Cate, J.-Y. Picard, B. Vigier, N. Di Clemente, C. Wilson, S. Imbeaud, R. B. Pepinsky, D. Guerrier, L. Boussin, L. Legeai, and D. Carré-Eusèbe 1993. Anti-Müllerian hormone the Jost factor. Recent Prog. Horm. Res. 8: 379–418.
   Google Scholar
• Kent, J., S. C. Wheatley, J. E. Andrews, A. H. Sinclair, and P. Koopman 1996. A male-specific role for SOX9 in vertebrate sex determination. Development 122: 2813–2822.
   PubMed Web of Science ®Google Scholar
• Lai, J.-S., and W. Herr 1992. EtBr provides a simple tool for identifying genuine DNA-independent protein associations. Proc. Natl. Acad. Sci. USA 89: 6958–6962.
   PubMed Web of Science ®Google Scholar
• Lala, D. S., D. A. Rice, and K. L. Parker 1992. Steroidogenic factor 1, a key regulator of steroidogenic enzyme expression, is the mouse homolog of fushi tarazu-factor 1. Mol. Endocrinol. 6: 1249–1258.
   PubMedGoogle Scholar
• Lala, D. S., P. M. Syka, S. B. Lazarchik, D. J. Mangelsdorf, K. L. Parker, and R. A. Heyman 1997. Activation of orphan nuclear receptor steroidogenic factor 1 by oxysterols. Proc. Natl. Acad. Sci. USA 94: 4895–4900.
   PubMed Web of Science ®Google Scholar
• Lefebvre, V., W. Huang, V. R. Harley, P. N. Goodfellow, and B. de Crombrugghe 1997. SOX9 is a potent activator of the chondrocyte-specific enhancer of the proα1(II) collagen gene. Mol. Cell. Biol. 17: 2336–2346.
   PubMed Web of Science ®Google Scholar
• Meyer, J., P. Südbeck, M. Held, T. Wagner, M. L. Schmitz, F. D. Bricarelli, E. Eggermont, U. Friedrich, O. A. Hass, A. Kobelt, J. G. Leroy, L. van Maldergem, E. Michel, B. Mitulla, R. A. Pfeiffer, A. Schinzel, H. Schmidt, and G. Scherer 1997. Mutational analysis of the SOX9 gene in campomelic dysplasia and autosomal sex reversal: lack of genotype/phenotype correlations. Hum. Mol. Genet. 6: 91–98.
   PubMedGoogle Scholar
• Morais da Silva, S., A. Hacker, V. Harley, P. Goodfellow, A. Swain, and R. Lovell-Badge 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.
   PubMed Web of Science ®Google Scholar
• Morohashi, K. I., S. L. Honda, Y. Inamata, H. Handa, and T. Omura 1992. A common trans-acting factor, Ad4-binding protein, to the promoters of steroidogenic P-450s. J. Biol. Chem. 267: 17913–17919.
   PubMed Web of Science ®Google Scholar
• Münsterberg, A., and R. Lovell-Badge 1991. Expression of the mouse anti-Müllerian hormone gene suggests a role in both female and male sexual differentiation. Development 113: 613–624.
   PubMed Web of Science ®Google Scholar
• Nachtigal, M. W., Y. Hirokawa, D. L. Enyeart-VanHouten, J. N. Flanagan, G. D. Hammer, and H. A. Ingraham 1998. Wilms’ tumor 1 and Dax-1 modulate the orphan nuclear receptor SF-1 in sex-specific gene expression. Cell 93: 445–454.
   PubMed Web of Science ®Google Scholar
• Nasrin, N., C. Buggs, X. F. Kong, J. Carnazza, M. Goebl, and M. Alexander-Bridges 1991. DNA-binding properties of the product of the testis-determining gene related protein. Nature 354: 317–320.
   PubMed Web of Science ®Google Scholar
• Nielsen, D. A., T. C. Chang, and D. J. Shapiro 1989. A highly sensitive, mixed-phase assay for chloramphenicol acetyl transferase activity in transfected cells. Anal. Biochem. 179: 19–23.
   PubMedGoogle Scholar
• Onodera, K., K. Yomogida, N. Suwabe, S. Takahashi, Y. Muraosa, N. Hayashi, E. Ito, L. Gu, M. Rassoulzadegan, J. D. Engel, and M. Yamamoto 1997. Conserved structure, regulatory elements, and transcriptional regulation from the GATA-1 gene testis promoter. J. Biochem. 121: 251–263.
   PubMed Web of Science ®Google Scholar
• Pevny, L. H., and R. Lovell-Badge 1997. Sox genes find their feet. Curr. Opin. Genet. Dev. 7: 338–344.
   PubMed Web of Science ®Google Scholar
• Poulat, F., P. de Santa Barbara, M. Desclozeaux, S. Soullier, B. Moniot, N. Bonneaud, B. Boizet, and P. Berta 1997. The human testis determining factor SRY binds a nuclear factor containing PDZ protein interaction domains. J. Biol. Chem. 272: 7167–7172.
   PubMedGoogle Scholar
• Poulat, F., F. Girard, M.-P. Chevron, C. Gozé, X. Rebillard, B. Calas, N. Lamb, and P. Berta 1995. Nuclear localization of the testis determining gene product SRY. J. Cell Biol. 5: 737–748.
   Google Scholar
• Schafer, A. J., and P. N. Goodfellow 1996. Sex determination in humans. Bioessays 18: 955–963.
   PubMedGoogle Scholar
• Shen, W. H., C. C. D. Moore, Y. Ikeda, K. L. Parker, and H. A. Ingraham 1994. Nuclear receptor steroidogenic factor 1 regulates the Müllerian inhibiting substance gene: a link to the sex determination cascade. Cell 77: 651–661.
   PubMed Web of Science ®Google Scholar
• Sinclair, A. H., P. Berta, M. S. Palmer, J. R. Hawkins, B. L. Griffiths, M. J. Smith, J. W. Foster, A. M. Frischauf, R. Lovell-Badge, and P. N. Goodfellow 1990. A gene from the human sex-determining region encoding a protein with homology to a conserved DNA-binding motif. Nature 346: 240–244.
   PubMed Web of Science ®Google Scholar
• Südbeck, P., and G. Scherer 1997. Two independent nuclear localization signals are present in the DNA-binding high mobility group domains of SRY and SOX9. J. Biol. Chem. 272: 27848–27852.
   PubMed Web of Science ®Google Scholar
• Südbeck, P., M. L. Schmitz, P. A. Baeuerle, and G. Scherer 1996. Sex reversal by loss of the C-terminal transactivation domain of human SOX9. Nat. Genet. 13: 230–232.
   PubMed Web of Science ®Google Scholar
• Wagner, T., J. Wirth, J. Meyer, B. Zabel, M. Held, J. Zimmer, J. Pasantes, F. D. Bricarelli, J. Keutel, E. Hustert, U. Wolf, N. Tommerup, W. Schempp, and G. Scherer 1994. Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY related gene SOX9. Cell 79: 1111–1120.
   PubMed Web of Science ®Google Scholar
• Waterman, M., and K. Jones 1990. Purification of TCF-1α, a T-cell-specific transcription factor that activates the T-cell receptor gene enhancer in a context-dependent manner. New Biol. 2: 621–636.
   PubMedGoogle Scholar
• Wen, W., J. L. Meinkoth, R. Y. Tsien, and S. S. Taylor 1995. Identification of a signal for rapid export of proteins from the nucleus. Cell 82: 463–473.
   PubMed Web of Science ®Google Scholar
• Werner, M. H., J. R. Huth, A. M. Gronenborg, and G. M. Clore 1995. Molecular basis of human 46X,Y sex reversal revealed from the three dimensional solution structure of the human SRY-DNA complex. Cell 81: 705–714.
   PubMed Web of Science ®Google Scholar
• Yomogida, K., H. Ohtani, H. Harigae, E. Ito, Y. Nishume, J. D. Engel, and M. Yamamoto 1994. Developmental stage- and spermatogenic cycle-specific expression of transcription factor GATA-1 in mouse Sertoli cells. Development 120: 1759–1766.
   PubMed Web of Science ®Google Scholar
• Yuan, H., N. Corbi, C. Basilico, and L. Dailey 1995. Developmental-specific activity of the FGF-4 enhancer requires the synergistic action of Sox2 and Oct-3. Genes Dev. 9: 2635–2645.
   PubMed Web of Science ®Google Scholar