Tumor suppressor p53 can participate in transcriptional induction of the GADD45 promoter in the absence of direct DNA binding

Molecular and Cellular Biology

Volumn 18, Issue 5, 1998, Pages 2768-2778

  Zhan, Qimin ^a   Chen, I Tsuen ^a,b   Antinore, Michael J ^a   Fornace Jr , Albert J ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P53;

ARTICLE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE;

EID: 0031946364     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.18.5.2768     Document Type: Article

References (65)

1. Ahmed, M. M., S. F. Sells, K. Venkatasubbarao, S. M. Fruitwala, S. Muthukkumar, C. Harp, M. Mohiuddin, and V. M. Rangnekar. 1997. Ionizing radiation-inducible apoptosis in the absence of p53 linked to transcription factor EGR-1. J. Biol. Chem. 272:33056-33061.
2. Avantaggiati, M. L., V. Ogryzko, K. Gardner, A. Giordano, A. S. Levine, and K. Kelly. 1997. Recruitment of p300/CBP in p53-dependent signal pathways. Cell 89:1175-1184.
3. Buckler, A. J., J. Pelletier, D. A. Haber, T. Glaser, and D. E. Housman. 1991. Isolation, characterization, and expression of the murine Wilms' tumor gene (WT1) during kidney development. Mol. Cell. Biol. 11:1707-1712.
4. Datta, R., N. Taneja, V. P. Sukhatme, S. A. Qureshi, R. Weichselbaum, and D. W. Kufe. 1993. Reactive oxygen intermediates target CC(A/T)6GG sequences to mediate activation of the early growth response 1 transcription factor gene by ionizing radiation. Proc. Natl. Acad. Sci. USA 90:2419-2422.
5. Day, M. L., T. J. Fahrner, S. Aykent, and J. Milbrandt. 1990. The zinc finger protein NGFI-A exists in both nuclear and cytoplasmic forms in nerve growth factor-stimulated PC12 cells. J. Biol. Chem. 265:15253-15260.
6. Dey, B. R., V. P. Sukhatme, A. B. Roberts, M. B. Sporn, F. J. Rauscher III, and S. J. Kim. 1994. Repression of the transforming growth factor-beta 1 gene by the Wilms' tumor suppressor WT1 gene product. Mol. Endocrinol. 8:595-602.
7. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
8. Drummond, I. A., S. L. Madden, P. Rohwer-Nutter, G. I. Bell, V. P. Sukhatme, and F. J. D. Rauscher. 1992. Repression of the insulin-like growth factor II gene by the Wilms tumor suppressor WT1. Science 257: 674-678.
9. Englert, C., X. Hou, S. Maheswaran, P. Bennett, C. Ngwu, G. G. Re, A. J. Garvin, M. R. Rosner, and D. A. Haber. 1995. WT1 suppresses synthesis of the epidermal growth factor receptor and induces apoptosis. EMBO J. 14: 4662-4675.
10. Englert, C., M. Vidal, S. Maheswaran, Y. Ge, R. 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.
11. Fan, S., M. L. Smith, D. J. Rivet II, D. Duba, Q. Zhan, K. W. Kohn, A. J. Fornace, Jr., and P. M. O'Connor. 1995. Disruption of p53 function sensitizes breast cancer MCF-7 cells to cisplatin and pentoxifylline. Cancer Res. 55:1649-1654.
12. Fornace, A. J., Jr., I. J. Alamo, and M. C. Hollander. 1988. DNA damage-inducible transcripts in mammalian cells. Proc. Natl. Acad. Sci. USA 85: 8800-8804.
13. Fornace, A. J., Jr., D. W. Nebert, M. C. Hollander, J. D. Luethy, M. Papathanasiou, J. Fargnoli, and N. J. Holbrook. 1989. Mammalian genes coordinately regulated by growth arrest signals and DNA-damaging agents. Mol. Cell. Biol. 9:4196-4203.
14. Goodyer, P., M. Dehbi, E. Torban, W. Bruening, and J. Pelletier. 1995. Repression of the retinoic acid receptor-alpha gene by the Wilms' tumor suppressor gene product, wt1. Oncogene 10:1125-1129.
15. Gu, W., X. L. Shi, and R. G. Roeder. 1997. Synergistic activation of transcription by CBP and p53. Nature 387:819-823.
16. Gujuluva, C. N., J. H. Baek, K. H. Shin, H. M. Cherrick, and N. H. Park. 1994. Effect of UV-irradiation on cell cycle, viability and the expression of p53, gadd153 and gadd45 genes in normal and HPV-immortalized human oral keratinocytes. Oncogene 9:1819-1827.
17. 16a. Haber, D. A. Personal communication.
18. 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-mediated growth suppression of Wilms tumor cells expressing a WT1 splicing variant. Science 262: 2057-2059.
19. 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.
20. Hallahan, D. E., V. P. Sukhatme, M. L. Sherman, S. Virudachalam, D. Kufe, and R. R. Weichselbaum. 1991. Protein kinase C mediates x-ray inducibility of nuclear signal transducers EGR1 and JUN. Proc. Natl. Acad. Sci. USA 88:2156-2160.
21. Harrington, M. A., B. Konicek, A. Song, X. L. Xia, W. J. Fredericks, and F. J. Rauscher. 1993. Inhibition of colony-stimulating factor-1 promoter activity by the product of the Wilms' tumor locus. J. Biol. Chem. 268:21271-21275.
22. Hewitt, S. M., S. Hamada, T. J. McDonnell, F. J. Rauscher III, and G. F. Saunders. 1995. Regulation of the proto-oncogenes bcl-2 and c-myc by the Wilms' tumor suppressor gene WT1. Cancer Res. 55:5386-5389.
23. Holbrook, N. J., and A. J. Fornace, Jr. 1991. Response to adversity: molecular control of gene activation following genotoxic stress. New Biol. 3:825-833.
24. Hollander, M. C., I. Alamo, J. Jackman, O. W. McBride, and A. J. Fornace, Jr. 1993. Sequence conservation and DNA damage-responsiveness of the mammalian gadd45 gene. J. Biol. Chem. 268:24385-24393.
25. Hollander, M. C., and A. J. Fornace, Jr. 1989. Induction of fos RNA by DNA-damaging agents. Cancer Res. 49:1687-1692.
26. Huang, R. P., and E. D. Adamson. 1995. A biological role for Egr-1 in cell survival following ultra-violet irradiation. Oncogene 10:467-475.
27. 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 Wilms' tumor suppressor WT1. Mol. Cell. Biol. 16:6945-6956.
28. Jones, K. A., K. R. Yamamoto, and R. Tjan. 1985. Two distinct transcription factors bind to the HSV thymidine kinase promoter in vitro. Cell 42:559-572.
29. Kastan, M. B., Q. Zhan, W. S. El-Deiry, F. Carrier, T. Jacks, W. V. Walsh, B. S. Plunkett, B. Vogelstein, and A. J. Fornace, Jr. 1992. A mammalian cell cycle checkpoint utilizing p53 and GADD45 is defective in ataxia telangiectasia. Cell 71:587-597.
30. Kedar, P. S., S. G. Widen, E. W. Englander, A. J. Fornace, Jr., and S. H. Wilson. 1991. The ATF/CREB transcription factor-binding site in the polymerase beta promoter mediates the positive effect of N-methyl-N′-nitro-N-nitrosoguanidine on transcription. Proc. Natl. Acad. Sci. USA 88:3729-3733.
31. Kessis, T. D., R. J. Slebos, W. G. Nelson, M. B. Kastan, B. S. Plunkett, S. M. Han, A. T. Lorincz, L. Hedrick, and K. R. Cho. 1993. Human papillomavirus 16 E6 expression disrupts the p53 mediated cellular response to DNA damage Proc. Natl. Acad. Sci. USA 90:3988-3992.
32. Khachigian, L. M., V. Lindner, A. J. Williams, and T. Collins. 1996. Egr-1-induced endothelial gene expression: a common theme in vascular injury. Science 271:1427-1431.
33. Ko, L. J., and C. Prives. 1996. p53: puzzle and paradigm. Genes Dev. 10:1054-1072.
34. 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.
35. Lill, N. L., S. R. Grossman, D. Ginsberg, J. DeCaprio, and D. M. Livingston. 1997. Binding and modulation of p53 by p300/CBP coactivators. Nature 387:823-827.
36. Luethy, J. D., J. Fargnoli, J. S. Park, A. J. Fornace, Jr., and N. J. Holbrook. 1990. Isolation and characterization of the hamster gadd153 gene. Activation of promoter activity by agents that damage DNA. J. Biol. Chem. 265:16521-16526.
37. Madden, S. L., D. M. Cook, J. F. Morris, A. Gashler, V. P. Sukhatme, and F. J. Rauscher III. 1991. Transcriptional repression mediated by the WT1 Wilms tumor gene product. Science 253:1550-1553.
38. Maheswaran, S., S. Park, A. Bernard, J. F. Morris, F. J. D. Rauscher, 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.
39. Morris, J. F., S. L. Madden, O. E. Tournay, D. M. Cook, V. P. Sukhatme, and F. J. Rauscher III. 1991. Characterization of the zinc finger protein encoded by the WT1 Wilms' tumor locus. Oncogene 6:2339-2348.
40. Murphy, M., A. Hinman, and A. J. Levine. 1996. Wild-type p53 negatively regulates the expression of a microtubule-associated protein. Genes Dev. 10:2971-2980.
41. Muzio, M., A. M. Chinnaiyan, F. C. Kischkel, K. O'Rourke, A. Shevchenko, J. Ni, C. Scaffidi, J. D. Bretz, M. Zhang, R. Gentz, M. Mann, P. H. Krammer, M. E. Peter, and V. M. Dixit. 1996. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell 85:817-827.
42. Nakagama, H., G. Heinrich, J. Pelletier, and D. E. Housman. 1995. Sequence and structural requirements for high-affinity DNA binding by the WT1 gene product. Mol. Cell. Biol. 15:1489-1498.
43. Nelson, W. G., and M. B. Kastan. 1994. DNA strand breaks: the DNA template alterations that trigger p53-dependent DNA damage response pathways. Mol. Cell. Biol. 14:1815-1823.
44. O'Connor, P. M., J. Jackman, I. Bae, T. G. Myers, S. Fan, M. Mutoh, D. Scudiero, A. Monks, E. A. Sausville, J. N. Weinstein, S. Friend, A. J. Fornace, Jr., and K. W. Kohn. 1997. Characterization of the p53 tumor suppressor pathway in cell lines of the NCI anticancer drug screen and correlations with the growth inhibitory potency of 123 anticancer agents. Cancer Res. 57:4285-4300.
45. Park, S., A. Bernard, K. E. Bove, D. A. Sens, D. J. Hazen-Martin, A. J. Garvin, and D. A. Haber. 1993. Inactivation of WT1 in nephrogenic rests, genetic precursors to Wilms' tumour. Nat. Genet. 5:363-367.
46. Pietenpol, J. A., T. Tokino, S. Thiagalingam, W. S. el-Deiry, K. W. Kinzler, and B. Vogelstein. 1994. Sequence-specific transcriptional activation is essential for growth suppression by p53. Proc. Natl. Acad. Sci. USA 91:1998-2002.
47. Prabhakar, N. R., B. C. Shenoy, M. S. Simonson, and N. S. Cherniack. 1995. Cell selective induction and transcriptional activation of immediate early genes by hypoxia. Brain Res. 697:266-270.
48. 46a. Rauscher, F. Personal communication.
49. 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.
50. Robertson, L. M., T. K. Kerppola, M. Vendrell, D. Luk, R. J. Smeyne, C. Bocchiaro, J. I. Morgan, and T. Curran. 1995. Regulation of c-fos expression in transgenic mice requires multiple interdependent transcription control elements. Neuron 14:241-252.
51. Schiestl, R. H., F. Khogali, and N. Carls. 1994. Revision of the mouse pink-eyed unstable mutation induced by low doses of x-rays. Science 266: 1573-1576.
52. Shiao, R. T., L. Miglietta, S. Y. Khera, A. Wolfson, and C. E. Freter. 1995. Dexamethasone and suramin inhibit cell proliferation and interleukin-6-mediated immunoglobulin secretion in human lymphoid and multiple myeloma cell lines. Leuk. Lymphoma 17:485-494.
53. Smith, M. L., I. Chen, Q. Zhan, I. Bae, C. Chen, T. Gilmer, M. B. Kastan, P. M. O'Connor, and A. J. Fornace, Jr. 1994. Interaction of the p53-regulated protein Gadd45 with proliferating cell nuclear antigen. Science 266: 1376-1380.
54. Smith, M. L., I. T. Chen, Q. Zhan, P. M. O'Connor, and A. J. Fornace, Jr. 1995. Involvement of the p53 tumor suppressor in repair of UV-type DNA damage. Oncogene 10:1053-1059.
55. Smith, M. L., H. U. Kontny, Q. Zhan, A. Sreenath, P. M. O'Connor, and A. J. Fornace, Jr. 1996. Antisense GADD45 expression results in decreased DNA repair and sensitizes cells to UV-irradiation or cisplatin. Oncogene 13:2255-2263.
56. Tokino, T., S. Thiagalingam, W. S. el-Deiry, T. Waldman, K. W. Kinzler, and B. Vogelstein. 1994. p53 tagged sites from human genomic DNA. Hum. Mol. Genet. 3:1537-1542.
57. 54a. Wang, X. W., et al. Unpublished data.
58. Wang, Z. Y., Q. Q. Qiu, M. Gurrieri, J. Huang, and T. F. Deuel. 1995. WT1, the Wilms' tumor suppressor gene product, represses transcription through an interactive nuclear protein. Oncogene 10:1243-1247.
59. 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.
60. Werner, H., Z. Shen-Orr, F. J. Rauscher III, J. F. Morris, C. T. Roberts, Jr., and D. LeRoith. 1995. Inhibition of cellular proliferation by the Wilms tumor suppressor WT1 is associated with suppression of insulin-like growth factor I receptor gene expression. Mol. Cell. Biol. 15:3516-3522.
61. 57a. Zhan, Q., et al. Unpublished data.
62. Zhan, Q., I. Bae, M. B. Kastan, and A. J. Fornace, Jr. 1994. The p53-dependent γ-ray response of GADD45. Cancer Res. 54:2755-2760.
63. Zhan, Q., F. Carrier, and A. J. Fornace, Jr. 1993. Induction of cellular p53 activity by DNA-damaging agents and growth arrest. Mol. Cell. Biol. 13: 4242-4250.
64. Zhan, Q., S. Fan, M. L. Smith, I. Bae, K. Yu, I. Alamo, Jr., P. M. O'Connor, and A. J. Fornace, Jr. 1996. Abrogation of p53 function affects the response of gadd genes to DNA base damaging agents and medium starvation. DNA Cell Biol. 15:805-815.
65. Zhan, Q., K. A. Lord, I. Alamo, Jr., M. C. Hollander, F. Carrier, D. Ron, K. W. Kohn, B. Hoffman, D. A. Liebermann, and A. J. Fornace, Jr. 1994. The gadd and MyD genes define a novel set of mammalian genes encoding acidic proteins that synergistically suppress cell growth. Mol. Cell. Biol. 14:2361-2371.