A novel repressor, par-4, modulates transcription and growth suppression functions of the Wilms' tumor suppressor WT1

Molecular and Cellular Biology

Volumn 16, Issue 12, 1996, Pages 6945-6956

  Johnstone, Ricky W ^a   See, Raymond H ^a   Sells, Stephen F ^b   Wang, Jing ^a,c   Muthukkumar, Sumathi ^b   Englert, Christoph ^d   Haber, Daniel A ^d   Light, Jon D ^e   Sugrue, Stephen P ^f   Roberts, Tom ^a,c   Rangnekar, Vivek M ^b   Shi, Yang ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c DANA FARBER CANCER INSTITUTE   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

^e MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR GATA 1; ZINC FINGER PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; GENE EXPRESSION REGULATION; GENE REPRESSION; GROWTH INHIBITION; HELA CELL; HUMAN; HUMAN CELL; NEPHROBLASTOMA; NONHUMAN; PRIORITY JOURNAL; PROSTATE; PROTEIN PROTEIN INTERACTION; RAT; TRANSCRIPTION REGULATION; TUMOR GROWTH; TUMOR SUPPRESSOR GENE;

ANIMALIA;

EID: 10544225383     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.16.12.6945     Document Type: Article

References (71)

1. Altura, R. A., M. Valentine, H. Li, J. M. Boyett, P. Shearer, P. Grundy, D. N. Shapiro, and A. T. Look. 1996. Identification of novel regions of deletion in familial Wilms tumor by comparative genomic hybridization. Cancer Res. 56:3837-3841.
2. Armstrong, J. F., K. Pritchard-Jones, W. A. Bickmore, N. D. Hastie, and J. B. Bard. 1992. The expression of the Wilms' tumour gene, WT1, in the developing mammalian embryo. Mech. Dev. 40:85-97.
3. Austruy, E., S. Candon, I. Henry, G. Gyapay, M. F. Tournade, M. Mannens, D. Callen, C. Junien, and C. Jeanpierre. 1995. Characterization of regions of chromosomes 12 and 16 involved in nephroblastoma tumorigenesis. Genes Chromosomes Cancer 14:285-294.
4. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Strahl (ed.). 1993. Current protocols in molecular biology, vol. 2. John Wiley & Sons, Inc., New York.
5. Bardeesy, N., D. Falkoff, M.-J. Petruzzi, N. Nowak, B. Zabel, M. Adam, M. C. Aguiar, P. Grundy, T. Shows, and J. Pelletier. 1994. Anaplastic Wilms' tumor, a subtype displaying poor prognosis, harbors p53 gene mutations. Nat. Genet. 7:91-96.
6. Blobel, G. A., M. C. Simon, and S. H. Orkin. 1995. Rescue of GATA-1-deficient embryonic stem cells by heterologous GATA-hinding proteins. Mol. Cell. Biol. 15:626-633.
7. Call, K. M., T. Glaser, C. Y. Ito, A. J. Buckler, J. Pelletier, D. A. Haber, E. A. Rose, A. Kral, H. Yeger, W. H. Lewis, C. Jones, and D. E. Housman. 1990. Isolation and characterization of a zinc finger polypeptide gene at the human chromosome 11 Wilms' tumor locus. Cell 60:509-520.
8. Coppes, M. J., L. Bonetta, A. Huang, P. Hoban, S. Chilton-MacNeill, C. E. Campbell, R. Weksberg, H. Yeger, A. E. Reeve, and B. R. Williams. 1992. Loss of heterozygosity mapping in Wilms' tumor indicates the involvement of three distinct regions and a limited role for nondisjunction or mitotic recombination. Genes Chromosomes Cancer 5:326-334.
9. Coppes, M. J., C. E. Campbell, and B. R. Williams. 1993. The role of WT1 in Wilms tumorigenesis. FASEB J. 7:886-895.
10. Deluca, N. A., M. Harvey, B. L. Slagel, M. J. McArthur, C. A. Montgomery, Jr., J. S. Butel, and A. Bradley. 1992. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumors. Nature (London) 56:215-221.
11. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation of RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
12. Drummond, I. A., S. L. Madden, P. Rohwer-Nutter, G. I. Bell, V. P. Sukhatme, and F. J. Rauscher. 1992. Repression of the insulin-like growth factor II gene by the Wilms tumor suppressor WT1. Science 257:674-678.
13. Drummond, I. A., H. D. Ruppercht, P. Rohwer-Nutter, J. M. Lopez-Guisa, S. L. R. I. Madden, F. J. Rauscher, and V. P. Sukhatme. 1994. DNA recognition by splicing variants of the Wilms' tumor suppressor, WT1. Mol. Cell. Biol. 14:3800-3809.
14. Endo, Y., K. Matsushima, K. Onozaki, and J. J. Oppenhiem. 1988. Role of ornithine decarboxylase in the regulation of cell growth by IL-1 and tumor necrosis factor. J. Immunol. 141:2342-2348.
15. Englert, C, M. Vidal, S. Maheswaran, Y. Ge, M. Ezzell, K. J. Isselbacher, and D. A. Haber. 1995. Truncated WT1 mutants alter the subnuclear localization of the wild-type protein. Proc. Natl. Acad. Sci. USA 92:11960-11964.
16. Fields, S., and O. Song. 1989. A novel genetic system to detect protein-protein interactions. Nature (London) 340:245-246.
17. Flanagan, J. R., K. Becker, D. Ennist, S. L. Gleason, P. H. Driggers, B.-Z. Levi, E. Appella, and K. Ozato. 1992. Cloning of a negative transcription factor that binds to the upstream region of Moloney murine leukemia virus. Mol. Cell. Biol. 12:38-44.
18. Galvin, K., and Y. Shi. Unpublished data.
19. Gashler, A. L., D. T. Bonthron, S. L. Madden, F. J. Rauscher, T. Collins, and V. P. Sukhatme. 1992. Human platelet-derived growth factor A chain is transcriptionally repressed by the Wilms tumor suppressor WT1. Proc. Natl. Acad. Sci. USA 89:10984-10988.
20. Gessler, M., A. Poustka, W. Cavenee, R. L. Neve, S. H. Orkin, and G. A. P. Bruns. 1990. Homozygous deletion in Wilms tumours of a gene identified by chromosome jumping. Nature (London) 343:774-778.
21. Graham, F. L., J. Smiley, W. C. Russell, and R. Nairn. 1977. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J. Gen. Virol. 36:59-72.
22. Haber, D., and D. Housman. 1992. The genetics of Wilms' tumor. Adv. Cancer Res. 59:41-68.
23. Haber, D. A., and A. J. Buckler. 1992. WT1: a novel tumor suppressor gene inactivated in Wilms' tumor. New Biol. 4:97-106.
24. Haber, D. A., S. Park, S. Maheswaran, C. Englert, G. G. Re, D. J. Hazen-Martin, D. A. Sens, and A. J. Garvin. 1993. WT1-medialed growth suppression of Wilms tumor cells expressing a WT1 splicing variant. Science 262: 2057-2059.
25. Haber, D. A, R. L. Sohn, A. J. Buckler, J. Pelletier, K. M. Call, and D. E. Housman. 1991. Alternative splicing and genomic structure of the Wilms' tumor gene WT1. Proc. Natl. Acad. Sci. USA 88:9618-9622.
26. Hariharan, N., D. Kelley, and R. P. Perry. 1991. δ, a transcription factor that binds to downstream elements in several polymerase II promoters, is a functionally versatile zinc finger protein. Proc. Natl. Acad. Sci. USA 88: 9799-9803.
27. Harlow, E., and D. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
28. Johnson, P. F., and S. L. McKnight. 1989. Eukaryotic transcriptional regulatory proteins. Annu. Rev. Biochem. 58:799-839.
29. Johnstone, R., and Y. Shi. Unpublished data.
30. Kaelin, W. G., Jr., D. C. Pallas, J. A. DeCaprio, F. J. Kaye, and D. M. Livingston. 1991. Identification of cellular proteins that can interact specifically with the T/E1A-binding region of the retinoblastoma gene product. Cell 64:521-531.
31. Kreidberg, J. A., H. Sariola, J. M. Loring, M. Maeda, J. Pelletier, D. Housman, and R. Jaenisch. 1993. WT-1 is required for early kidney development. Cell 74:679-691.
32. Kudoh, T., T. Ishidate, M. Moriyama, K. Toyoshima, and T. Akiyama. 1995. G1 phase arrest induced by Wilms tumor protein WT1 is abrogated by cyclin/CDK. complexes. Proc. Natl. Acad. Sci. USA 92:4517-4521.
33. Larsson, S. H., J.-P. Charlieu, K. Miyagawa, D. Engelkamp, M. Rassoulzadegan, A. Ross, F. Cuzin, V. van Heyningen, and N. D. Hastie. 1995. Sub-nuclear localization of WT1 in splicing or transcription factor domains is regulated by alternative splicing. Cell 81:391-401.
34. Lee, J.-S., K. M. Galvin, R. H. See, R. Eckner, D. Livingston, E. Moran, and Y. Shi. 1995. Relief of YY1 transcriptional repression by adenovirus E1A is mediated by E1A-associated protein p300. Genes Dev. 9:1188-1198.
35. Lee, J.-S., K. M. Galvin, and Y. Shi. 1993. Evidence for physical interaction between the zinc finger transcription factors YY1 and Sp1. Proc. Natl. Acad. Sci. USA 90:6145-6149.
36. Luo, X.-N., J. C. Reddy, P. L. Yeyati, A. H. Idris, D. Hosono, A. Haber, J. D. Licht, and G. F. Atweh. 1995. The tumor suppressor gene WT1 inhibits ras-mediated transformation. Oncogene 11:734-750.
37. Madden, S., D. M. Cook, J. F. Morris, A. Cashler, V. Sukhatme, and F. J. Rauscher III. 1991. Transcriptional repression mediated by the WT1 Wilms tumor gene product. Science 253:1550-1553.
38. Madden, S. L., D. M. Cook, and F. J. I. Rauscher. 1993. A structure-function analysis of transcriptional repression mediated by the WT1, Wilms' tumor suppressor protein. Oncogene 8:1713-1720.
39. Maheswaran, S., C. Englert, P. Bennett, G. Heinrich, and A. D. Haber. 1995. The WT1 gene product stabilizes p53 and inhibits p53-mediated apoptosis. Genes Dev. 9:2143-2156.
40. Maheswaran, S., S. Park, A. Bernard, J. F. Morris, F. J. Rauscher III, D. E. Hill, and D. A. Haber. 1993. Physical and functional interaction between WT1 and p53 proteins. Proc. Natl. Acad. Sci. USA 90:5100-5104.
41. Malkin, B., E. Sexsmith, H. Yeger, B. R. G. Williams, and M. J. Coppes. 1994. Mutations of the p53 tumor suppressor gene occur infrequently in Wilms' tumor. Cancer Res. 54:2077-2079.
42. Maw, M. A., P. E. Gundy, L. J. Millow, M. R. Eccles, R. S. Dunn, P. J. Smith, A. P. Feinberg, D. J. Law, M. C. Paterson, P. E. Telzerow, D. F. Callen, A. D. Thompson, R. I. Richards, and A. E. Reeve. 1992. A third Wilms' tumor locus on chromosome 16q. Cancer Res. 52:3094-3098.
43. Moffett, P., W. Bruening, H. Nakagama, D. Bardeesy, D. Housman, E. Housman, and J. Pelletier. 1995. Antagonism of WT1 activity by protein self-association. Proc. Natl. Acad. Sci. USA 92:11105-11109.
44. 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.
45. Park, K., and M. Atchison. 1991. Isolation of a candidate repressor/activator, NF-E1 (YY1, δ), that binds to the immunoglobulin k 3′ enhancer and the immunoglobulin heavy-chain uE1 site. Proc. Natl. Acad. Sci. USA 88:9804-9808.
46. Park, S., G. Tomlinson, P. Nisen, and D. A. Haber. 1993. Altered transactivational properties of a mutated WT1 gene product in a WAGR-associated Wilms' tumor. Cancer Res. 53:4757-4760.
47. Parwardhan, S., A. Gashler, M. G. Siegel, L. C. Chang, J. Joseph, T. W. Shows, M. M. Le Beau, and V. P. Sukhatme. 1991. EGR3, a novel member of the Egr family of genes encoding immediate-early transcription factors. Oncogene 6:917-928.
48. Pelletier, J., M. Schalling, A. J. Buckler, A. Roger, D. A. Haber, and D. E. Housman. 1991. Expression of the Wilms' tumor gene WT1 in the murine urogenital system. Genes Dev. 5:1345-1356.
49. Pritchard-Jones, K., S. Fleming, D. Davidson, W. Bickmore, D. Porteus, C. Gosden, J. Bard, A. Buckler, J. Pelletier, D. Housman, V. van Heyningen, and N. Hastie. 1990. The candidate Wilms' tumor gene is involved in genitourinary development. Nature (London) 346:194-197.
50. Pu, W. T., and K. Struhl. 1991. Highly conserved residues in the bZIP domains of yeast GCN4 are not essential for DNA binding. Mol. Cell. Biol. 11:4918-4926.
51. Rauscher F., III, J. F. Morris, O. E. Tournay, D. M. Cook, and T. Curran. 1990. Binding of the Wilm's tumor locus zinc linger protein to the EGR-1 consensus sequence. Science 250:1259-1263.
52. Rauscher, F. J. 1993. The WT1 Wilms tumor gene product: a developmentally regulated transcription factor in the kidney that functions as a tumor suppressor. FASEB J. 7:896-903.
53. Reddy, J. C., and J. D. Licht. 1996. The WT1 Wilms' tumor suppressor gene: how much do we really know? Biochim. Biophys. Acta 1287:1-28.
54. Reddy, J. C., J. C. Morris, J. Wang, M. A. English, X.-N. Luo, G. F. Atweh, 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.
55. Reeve, A. E., S. A. Shi, A. M. Raisiz, and A. P. Feinberg. 1989. Loss of allelic heterozygosity at a second locus on chromosome 11 in sporadic Wilms tumor cells. Mol. Cell. Biol. 9:1799-1803.
56. Reinhard, C., A. Fernandez, N. J. C. Lamb, and G. Thomas. 1994. Nuclear localization of p85s6k: functional requirement for entry into S phase. EMBO J. 13:1557-1565.
57. See, R., and Y. Shi. Unpublished data.
58. Sells, S. F., S.-S. Han, S. Muthukkumar, N. Maddiwar, R. Johnstone, E. Boghaert, D. Gillis, G. Liu, P. Nair, S. Monning, P. Collini, M. P. Mattson, V. P. Sukhatme, S. Zimmer, D. P. Wood, Jr., J. W. McRoberts, Y. Shi, and V. M. Rangnekar. Expression and function of the leucine zipper protein par-4 in apoptosis. Submitted for publication.
59. Sells, S. F., S. Muthukkumar, V. P. Sukhatme, S. A. Crist, and V. M. Rangnekar. 1995. The zinc finger transcription factor EGR-1 impedes interleukin-1-inducible tumor growth arrest. Mol. Cell. Biol. 15:682-692.
60. Sells, S. F., D. P. Wood, Jr., S. S. Joshi-Barve, S. Muthukkumar, R. J. Jacob, S. A. Crist, S. Humphreys, and V. M. Rangnekar. 1994. Commonality of the gene programs induced by effectors of apoptosis in androgen-dependent and -independent prostate cells. Cell Growth Differ. 5:457-466.
61. Seto, E., B. Lewis, and T. Shenk. 1993. Interaction between transcription factors Sp1 and YY1. Nature (London) 365:462-464.
62. Sharma, P. M., X. Yang, M. Bowman, V. Roberts, and S. Sukumar. 1992. Molecular cloning of rat Wilms' tumor complementary DNA and a study of messenger RNA expression in the urogenital system and the brain. Cancer Res. 52:6407-6412.
63. Shi, Y., E. Selo, L. S. Chang, and T. Shenk. 1991. Transcriptional repression by YY1, a human GL1-Kruppel related protein, and relief of repression by adenovirus E1A protein. Cell 67:377-388.
64. Skolnik, F. Y., B. Margolis, M. Mohammadi, E. Lowenstein, R. Fischer, A. Drepps, A. Ulrich, and J. Schlessinger. 1991. Cloning of P13 kinase-associated p85 utilizing a novel method for expression/cloning of target proteins for receptor tyrosine kinases. Cell 65:83-90.
65. Visvader, J. E., M. Crossley, J. Hill, S. H. Orkin, and J. M. Adams. 1995. The C-terminal zinc finger of GATA-1 or GATA-2 is sufficient to induce megakaryocytic differentiation of an early myeloid cell line. Mol. Cell. Biol. 15:634-641.
66. Wang, Z.-Y., S. L. Madden, T. F. Deuel, and F. J. Rauscher. 1992. The Wilms' tumor gene product, WT1, represses transcription of the platelet-derived growth factor A-chain gene. J. Biol. Chem. 267:21999-22002.
67. Wang, Z.-Y., Q.-Q. Qiu, and T. E. Deuel. 1993. The Wilms' tumor gene product WT1 activates or represses transcription through separate functional domains. J. Biol. Chem. 268:9972-9975.
68. Wang, Z.-Y., Q.-Q. Qiu, J. Huang, M. Gurrieri, and T. F. Deuel. 1995. Products of alternatively spliced transcripts of the Wilms' tumor suppressor gene, wt1, have altered DNA binding specificity and regulate transcription in different ways. Oncogene 10:415-422.
69. Werner, H., G. G. Re, I. A. Drummond, V. P. Sukhatme, F. J. Rauscher, D. A. Sens, A. J. Garvin, D. DeRoith, and C. T. Roberts. 1993. Increased expression of the insulin-like growth factor 1 receptor gene, IGF1R, in Wilms tumor is correlated with modulation of IGF1R promoter activity by the WT1 Wilms tumor gene product. Proc. Natl. Acad. Sci. USA 90:5828-5832.
70. Zervos, A. S., J. Gyuris, and R. Brent. 1993. Mxi1, a protein that specifically interacts with Max to bind Myc-Max recognition sites. Cell 72:223-232.
71. Zhou, Q., R. W. Gedrich, and D. A. Engel. 1995. Transcriptional repression of the c-fos gene by YY1 is mediated by a direct interaction with ATF/ CREB. J. Virol. 69:4323-4330.