The Wilms' tumor suppressor gene (wt1) product regulates Dax-1 gene expression during gonadal differentiation

Molecular and Cellular Biology

Volumn 19, Issue 3, 1999, Pages 2289-2299

  Kim, Jungho ^a   Prawitt, Dirk ^c   Bardeesy, Nabeel ^a   Torban, Elena ^a   Vicaner, Caroline ^a   Goodyer, Paul ^a   Zabel, Bernard ^c   Pelletier, Jerry ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS RECEPTOR; GENE PRODUCT;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GONAD DEVELOPMENT; NEPHROBLASTOMA; NONHUMAN; OVARY DEVELOPMENT; PRIORITY JOURNAL; PROMOTER REGION; RECEPTOR GENE; SEX DETERMINATION; TESTIS DEVELOPMENT; TUMOR SUPPRESSOR GENE;

ANIMALIA; MAMMALIA; MURINAE;

EID: 0032981181     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.19.3.2289     Document Type: Article

References (55)

1. Armstrong, J. F., K. Pritchard-Jones, W. A. Bickmore, N. D. Hastie, and J. B. L. Bard. 1992. The expression of the Wilms' tumour gene, WT1, in the developing mammalian embryo. Mech. Dev. 40:85-97.
2. Barbaux, S., P. Niaudet, M. C. Gubler, J. P. Grunfeld, F. Jaubert, F. Kuttenn, C. N. Fekete, N. Souleyreau-Therville, E. Thibaud, M. Fellous, and K. McElreavey. 1997. Donor splice-site mutations in WT1 are responsible for Fraiser syndrome. Nat. Genet. 17:467-470.
3. Bardoni, B., E. Zanaria, S. Guioli, G. Floridia, K. Worley, G. Tonini, E. Ferrante, G. Chiumello, E. McCabe, M. Fraccaro, O. Zuffardi, and G. Camerino. 1994. A dosage sensitive locus at chromosome Xp21 is involved in male to female sex reversal. Nat. Genet. 7:497-501.
4. Behringer, R. R., M. J. Finegold, and R. L. Cate. 1994. Müllerian-inhibiting substance function during mammalian sexual development. Cell 79:415-425.
5. Berta, P., J. R. Hawkins, A. H. Sinclair, A. Taylor, B. L. Griffiths, P. N. Goodfellow, and M. Fellous. 1990. Genetic evidence equating SRY and the testis-determining factor. Nature 348:448-450.
6. Bruening, W., N. Bardeesy, B. L. Silverman, R. A. Cohn, G. A. Machin, A. J. Aronson, D. Housman, and J. Pelletier. 1992. Germline intronic and exonic mutations in the Wilms' tumour gene (WT1) affecting urogenital development. Nat. Genet. 1:144-148.
7. Bruening, W., and J. Pelletier. 1994. Denys-Drash syndrome: a role for the WT1 tumor suppressor gene in urogenital development. Semin. Dev. Biol. 5: 333-343.
8. Bruening, W., P. Moffett, S. Chia, G. Heinrich, and J. Pelletier. 1996. Identification of nuclear localization signals within the zinc fingers of the WT1 tumor suppressor gene product. FEBS Lett. 393:41-47.
9. Burris, T. P., W. Guo, T. Le, and E. R. B. McCabe. 1995. Identification of a putative steroidogenic factor-1 response element in the DAX-1 promoter. Biochem. Biophys. Res. Commun. 214:576-581.
10. Cate, R. L., R. J. Mattaliano, C. Hession, R. Tizard, N. M. Farber, A. Cheung, E. G. Ninfa, A. Z. Frey, D. J. Gash, E. P. Chow, R. A. Fisher, J. M. Bertonis, G. Torres, B. P. Wallner, K. L. Ramachandran, R. C. Ragin, T. F. Manganaro, D. T. MacLaughlin, and P. K. Donahoe. 1986. Isolation of the bovine and human genes for Müllerian inhibiting substance and expression of the human gene in animal cells. Cell 45:685-698.
11. Clarkson, T., D. Gussow, and P. T. Jones. 1992. General application of PCR to gene cloning and manipulation, p. 187-214. In M. J. McPherson, P. Quirke, and G. R. Taylor (ed.), PCR - a practical approach. IRL Press, New York, N.Y.
12. Cook, D. M., M. T. Hinkes, M. Bernfied, and F. J. Rauscher III. 1996. Transcriptional activation of the syndecan-1 promoter by the Wilms' tumor protein WT1. Oncogene 13:1789-1799.
13. 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.
14. Englert, C., S. Maheswaran, A. J. Garvin, J. Kreidberg, and D. A. Haber. 1997. Induction of p21 by the Wilms' tumor suppressor gene wt1. Cancer Res. 57:1429-1434.
15. Foster, J. W., S. M. Dominguez, S. Guioli, G. Kowk, 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.
16. Gossen, M., and H. Bujard. 1992. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. USA 89:5547-5551.
17. Ikeda, Y., W.-H. Shen, H. Ingraham, and K. Parker. 1994. Developmental expression of mouse steroidogenic factor-1, an essential regulator of the steroid hydroxylases. Mol. Endocrinol. 8:654-662.
18. Ito, M., R. Yu, and J. L. Jameson. 1997. DAX-1 inhibits SF-1-mediated transactivation via a carboxy-terminal domain that is deleted in adrenal hypoplasia congenita. Mol. Cell. Biol. 17:1476-1483.
19. Jäger, R. J., M. Anvret, K. Hall, and G. Scherer. 1990. A human XY female with a frame shift mutation in the candidate testis-determining gene SRY. Nature 348:452-454.
20. Johnstone, R. W., R. H. See, S. F. Sells, J. Wang, S. Muthukkumar, C. Englert, D. A. Haber, J. D. Licht, S. P. Sugrue, T. Roberts, V. M. Rangnekar, and Y. Shi. 1996. A novel repressor, par-4, modulates transcription and growth suppression functions of the mouse Wilms' tumor suppressor WT1. Mol. Cell. Biol. 16:6945-6956.
21. Katoh-Fukui, Y., R. Tsuchiya, T. Shiroishi, Y. Nakahara, N. Hashimoto, K. Noguchi, and T. Higashinakagawa. 1998. Male-to-female sex reversal in M33 mutant mice. Nature 393:688-692.
22. Kikuchi, H., A. Takata, Y. Akasaka, R. Fukuzawa, H. Yoneyama, Y. Kurosawa, M. Honda, Y. Kamiyama, and J. Hata. 1997. Do intronic mutations affecting splicing of WT1 exon 9 cause Frasier syndrome? J. Med. Genet. 35: 45-48.
23. Kim, J., and J. Pelletier. Unpublished data.
24. Klamt, B., A. Koziell, F. Poulat, P. Wieacker, P. Scambler, P. Berta, and M. Gessler. 1998. Frasier syndrome is caused by defective alternative splicing of WT1 leading to an altered ratio of WT1 +/-KTS splice isoforms. Hum. Mol. Genet. 7:709-714.
25. Koopman, P., J. Gubbay, N. Vivian, P. Goodfellow, and R. Lovell-Badge. 1991. Male development of chromosomally female mice transgenic for Sry. Nature 351:117-121.
26. Kreidberg, J. A., H. Sariola, J. M. Loring, M. Maeda, J. Pelletier, D. Housman, and R. Jaenich. 1993. WT-1 is required for early kidney development. Cell 74:676-691.
27. Larsson, S. H., J.-P. Charlieu, K. Miyagawa, D. Engelkamp, M. Rassoulzadegan, A. Ross, F. Cuzin, V. van Heyningen, and N. D. Hastie. 1995. Subnuclear localization of WT1 in splicing or transcription factor domains is regulated by alternative splicing. Cell 81:391-401.
28. Luo, X., Y. Ikeda, and K. L. Parker. 1994. A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell 77:481-490.
29. Madden, S. L., D. M. Cook, and F. J. Rauscher III. 1993. A structure-function analysis of transcriptional repression mediated by the WT1, Wilms' tumor suppressor protein. Oncogene 8:1713-1720.
30. Moffett, P., W. Bruening, H. Nakagama, N. Bardeesy, D. Housman, D. Housman, and J. Pelletier. 1995. Antagonism of WT1 activity by protein self-association. Proc. Natl. Acad. Sci. USA 92:11105-11109.
31. Mundlos, S., J. Pelletier, A. Darveau, M. Bachmann, A. Winterpacht, and B. Zabel. 1993. Nuclear localization of the protein encoded by the Wilms' tumor gene WT1 in embryonic and adult tissues. Development 119:1329-1341.
32. Muscatelli, F., T. M. Strom, A. P. Walker, E. Zanaria, D. Recan, A. Meindl, B. Bardoni, S. Guioli, G. Zehetner, W. Rabl, H. P. Achwart, J.-C. Kaplan, G. Camerino, T. Meitinger, and A. P. Monaco. 1994. Mutations in the DAX-1 gene give rise to both X-linked adrenal hypoplasia congenita and hypogonadotropic hypogonadism. Nature 372:672-676.
33. 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.
34. Nakagama, H., G. Heinrich, J. Pelletier, and D. Housman. 1995. Sequence and structural requirements for high-affinity DNA binding by the WT1 gene product. Mol. Cell. Biol. 15:1489-1498.
35. Parker, K. L., and B. P. Schimmer. 1997. Steroidogenic factor 1: a key determinant of endocrine development and function. Endocr. Rev. 18:361-377.
36. Pelletier, J., W. Bruening, C. E. Kashtan, S. M. Mauer, J. C. Manivel, J. Striegel, D. C. Houghton, C. Junien, R. Habib, L. Fouser, R. N. Fine, B. L. Silverman, D. Haber, and D. Housman. 1991. Germline mutations in the Wilms' tumor suppressor gene are associated with abnormal urogenital development in Denys-Drash syndrome. Cell 67:437-447.
37. Pelletier, J., W. Bruening, F. P. Li, D. A. Haber, T. Glaser, and D. Housman. 1991. WT1 mutations contribute to abnormal genital system development and hereditary Wilms' tumour. Nature 353:431-434.
38. Pelletier, J., M. Schalling, A. J. Buckler, A. Rogers, D. A. Haber, and D. Housman. 1991. Expression of the Wilms' tumor gene WT1 in the murine urogenital system. Genes Dev. 5:1345-1356.
39. Pritchard-Jones, K., S. Fleming, D. Davidson, W. Bickmore, D. Porteous, C. Gosden, J. Bard, A. Buckler, J. Pelletier, D. E. Housman, V. van Heyningen, and N. Hastie. 1990. The candidate Wilms' tumor gene is involved in genitourinary development. Nature 346:194-197.
40. Rackley, R. R., A. M. Flenniken, N. P. Kuriyan, P. M. Kessler, M. H. Stoler, and B. R. G. Williams. 1993. Expression of the Wilms' tumor suppressor gene wt1 during mouse embryogenesis. Cell Growth Diff. 4:1023-1031.
41. Rauscher, F. J., III, J. F. Morris, O. E. Tournay, D. M. Cook, and T. Curran. 1990. Binding of the Wilms' tumor locus zinc finger protein to the EGR-1 consensus sequence. Science 250:1259-1262.
42. Reddy, J. C., and J. D. Licht. 1996. The WT1 Wilms' tumor suppressor gene: how much do we really know? Biochem. Biophys. Acta 1287:1-28.
43. Reddy, J. C., J. C. Morris, J. Wang, M. A. English, D. A. Haber, Y. Shi, and J. D. Licht. 1995. WT1-mediated transcriptional activation is inhibited by dominant negative mutant proteins. J. Biol. Chem. 270:10878-10884.
44. Sakamoto, Y., M. Yoshida, K. Semba, and T. Hunter. 1997. Inhibition of the DNA-binding and transcriptional repression activity of the Wilms' tumor gene product, WT1, by cAMP-dependent protein kinase-mediated phosphorylation of Ser-365 and Ser-393 in the zinc finger domain. Oncogene 15: 2001-2012.
45. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
46. 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 77:1-20.
47. Swain, A., V. Narvaez, P. Burgoyne, G. Camerino, and R. Lovell-Badge. 1998. Dax1 antagonizes Sry action in mammalian sex determination. Nature 391: 761-767.
48. Swain, A., E. Zanaria, A. Hacker, R. Lovell-Badge, and G. Camerino. 1996. Mouse Dax-1 expression is consistent with a role in sex determination as well as in adrenal and hypothalamus function. Nat. Genet. 12:404-409.
49. Tamai, K. T., L. Monaco, T.-P. Alastalo, E. Lalli, M. Parvinen, and P. Sassone-Corsi. 1996. Hormonal and developmental regulation of DAX-1 expression in Sertoli cells. Mol. Endocrinol. 10:1561-1569.
50. 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.
51. Wang, Z.-Y., Q.-Q. Qiu, and T. F. Deuel. 1993. The Wilms' tumor gene product WT1 activates or suppresses transcription through separate functional domains. J. Biol. Chem. 268:9172-9175.
52. Wang, Z. Y., Q.-Q. Qiu, K. T. Enger, and T. F. Deuel. 1993. A second transcriptionally active DNA-binding site for the Wilms tumor gene product, WT1. Proc. Natl. Acad. Sci. USA 90:8896-8900.
53. Ye, Y., B. Raychaudhuri, A. Gurney, C. E. Campbell, and B. R. G. Williams. 1996. Regulation of WT1 by phosphorylation: inhibition of DNA binding, alteration of transcriptional activity, and cellular translocation. EMBO J. 15: 5606-5615.
54. Zanaria, E., F. Muscatelli, B. Bardoni, T. M. Strom, S. Guioli, W. Guo, E. Lalli, C. Moser, A. P. Walker, E. R. McCabe, T. Meitinger, A. P. Monaco, P. Sassone-Corsi, and G. Camerino. 1994. An unusual member of the nuclear hormone receptor superfamily responsible for X-linked adrenal hypoplasia congenita. Nature 372:635-641.
55. Zazopoulos, E., E. Lalli, D. M. Stocco, and P. Sassone-Corsi. 1997. DNA binding and transcriptional repression by DAX-1 blocks steroidogenesis. Nature 390:311-315.