Differential recognition of response elements determines target gene specificity for p53 and p63

Molecular and Cellular Biology

Volumn 25, Issue 14, 2005, Pages 6077-6089

  Osada, Motonobu ^a   Park, Hannah Lui ^a   Nagakawa, Yuichi ^a   Yamashita, Keishi ^a   Fomenkov, Alexey ^a   Kim, Myoung Sook ^a   Wu, Guojun ^a   Nomoto, Shuji ^a   Trink, Barry ^a   Sidransky, David ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENVOPLAKIN; PROTEIN P53; PROTEIN P63; PROTEIN SMARCD3; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DNA MICROARRAY; DNA RESPONSIVE ELEMENT; EMBRYO; EPITHELIUM CELL; GEL MOBILITY SHIFT ASSAY; GENE ACTIVATION; GENE EXPRESSION; GENE INDUCTION; GENE TARGETING; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHARYNX; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; PROTEIN EXPRESSION; SKIN EPITHELIUM;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BONE DEVELOPMENT; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REPORTER; GENES, TUMOR SUPPRESSOR; HUMANS; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHARYNX; PHOSPHOPROTEINS; PROMOTER REGIONS (GENETICS); PROTEIN PRECURSORS; RESPONSE ELEMENTS; SKIN; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 21744448805     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.14.6077-6089.2005     Document Type: Article

References (61)

1. Amiel, J., G. Bougeard, C. Francannet, V. Raclin, A. Munnich, S. Lyonnet, and T. Frebourg. 2001. TP63 gene mutation in ADULT syndrome. Eur. J. Hum. Genet. 9:642-645.
2. Borradori, L., and A. Sonnenberg. 1999. Structure and function of hemidesmosomes: more than simple adhesion complexes. J. Investig. Dermatol. 112:411-418.
3. Celli, J., P. Duijf, B. C. Hamel, M. Bamshad, B. Kramer, A. P. Smits, R. Newbury-Ecob, R. C. Hennekam, G. Van Buggenhout, A. van Haeringen, C. G. Woods, A. J. van Essen, R. de Waal, G. Vriend, D. A. Haber, A. Yang, F. McKeon, H. G. Brunner, and H. van Bokhoven. 1999. Heterozygous germline mutations in the p53 homolog p63 are the cause of EEC syndrome. Cell 99:143-153.
4. Comer, K. A., P. A. Dennis, L. Armstrong, J. J. Catino, M. B. Kastan, and C. C. Kumar. 1998. Human smooth muscle α-actin gene is a transcriptional target of the p53 tumor suppressor protein. Oncogene 16:1299-1308.
5. Contente, A., A. Dittmer, M. C. Koch, J. Roth, and M. Dobbelstein. 2002. A polymorphic microsatellite that mediates induction of PIG3 by p53. Nat. Genet. 30:315-320.
6. Dohn, M., S. Zhang, and X. Chen. 2001. p63α and ΔNp63α can induce cell cycle arrest and apoptosis and differentially regulate p53 target genes. Oncogene 20:3193-3205.
7. Donehower, L. A., M. Harvey, B. L. Slagle, 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 tumours. Nature 356:215-221.
8. el-Deiry, W. S. 1998. Regulation of p53 downstream genes. Semin. Cancer Biol. 8:345-357.
9. el-Deiry, W. S., S. E. Kern, J. A. Pietenpol, K. W. Kinzler, and B. Vogelstein. 1992. Definition of a consensus binding site for p53. Nat. Genet. 1:45-49.
10. el-Deiry, W. S., T. Tokino, V. E. Velculescu, D. B. Levy, R. Parsons, J. M. Trent, D. Lin, W. E. Mercer, K. W. Kinzler, and B. Vogelstein. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
11. Ellisen, L. W., K. D. Ramsayer, C. M. Johannessen, A. Yang, H. Beppu, K. Minda, J. D. Oliner, F. McKeon, and D. A. Haber. 2002. REDD1, a developmentally regulated transcriptional target of p63 and p53, links p63 to regulation of reactive oxygen species. Mol. Cell 10:995-1005.
12. Flores, E. R., K. Y. Tsai, D. Crowley, S. Sengupta, A. Yang, F. McKeon, and T. Jacks. 2002. p63 and p73 are required for p53-dependent apoptosis in response to DNA damage. Nature 416:560-564.
13. Fontao, L., B. Favre, S. Riou, D. Geerts, F. Jaunin, J. H. Saurat, K. J. Green, A. Sonnenberg, and L. Borradori. 2003. Interaction of the bullous pemphigoid antigen 1 (BP230) and desmoplakin with intermediate filaments is mediated by distinct sequences within their COOH terminus. Mol. Biol. Cell 14:1978-1992.
14. Ghioni, P., F. Bolognese, P. H. Duijf, H. Van Bokhoven, R. Mantovani, and L. Guerrini. 2002. Complex transcriptional effects of p63 isoforms: identification of novel activation and repression domains. Mol. Cell. Biol. 22:8659-8668.
15. Hermeking, H., C. Lengauer, K. Polyak, T. C. He, L. Zhang, S. Thiagalingam, K. W. Kinzler, and B. Vogelstein. 1997. 14-3-3 σ Is a p53-regulated inhibitor of G2/M progression. Mol. Cell 1:3-11.
16. Hwang, P. M., F. Bunz, J. Yu, C. Rago, T. A. Chan, M. P. Murphy, G. F. Kelso, R. A. Smith, K. W. Kinzler, and B. Vogelstein. 2001. Ferredoxin reductase affects p53-dependent, 5-fluorouracil-induced apoptosis in colorectal cancer cells. Nat. Med. 7:1111-1117.
17. Ianakiev, P., M. W. Kilpatrick, I. Toudjarska, D. Basel, P. Beighton, and P. Tsipouras. 2000. Split-hand/split-foot malformation is caused by mutations in the p63 gene on 3q27. Am. J. Hum. Genet. 67:59-66.
18. Inga, A., F. Storici, T. A. Darden, and M. A. Resnick. 2002. Differential transactivation by the p53 transcription factor is highly dependent on p53 level and promoter target sequence. Mol. Cell. Biol. 22:8612-8625.
19. Juven, T., Y. Barak, A. Zauberman, D. L. George, and M. Oren. 1993. Wild type p53 can mediate sequence-specific transactivation of an internal promoter within the mdm2 gene. Oncogene 8:3411-3416.
20. King, K. E., R. M. Ponnamperuma, T. Yamashita, T. Tokino, L. A. Lee, M. F. Young, and W. C. Weinberg. 2003. ΔNp63α functions as both a positive and a negative transcriptional regulator and blocks in vitro differentiation of murine keratinocytes. Oncogene 22:3635-3644.
21. Klein, C., G. Georges, K. P. Kunkele, R. Huber, R. A. Engh, and S. Hansen. 2001. High thermostability and lack of cooperative DNA binding distinguish the p63 core domain from the homologous tumor suppressor p53. J. Biol. Chem. 276:37390-37401.
22. Kurata, S. I., T. Okuyama, M. Osada, T. Watanabe, Y. Tomimori, S. Sato, A. Iwai, T. Tsuji, Y. Ikawa, and I. Katoh. 2004. p51/p63 controls subunit α3 of the major epidermis integrin anchoring the stem cells to the niche. J. Biol. Chem. 279:50069-50077.
23. Liu, G., and X. Chen. 2002. The ferredoxin reductase gene is regulated by the p53 family and sensitizes cells to oxidative stress-induced apoptosis. Oncogene 21:7195-7204.
24. Maatta, A., T. DiColandrea, K. Groot, and F. M. Watt. 2001. Gene targeting of envoplakin, a cytoskeletal linker protein and precursor of the epidermal cornified envelope. Mol. Cell. Biol. 21:7047-7053.
25. Maatta, A., C. Ruhrberg, and F. M. Watt. 2000. Structure and regulation of the envoplakin gene. J. Biol. Chem. 275:19857-19865.
26. Malkin, D., F. P. Li, L. C. Strong, J. F. Fraumeni, Jr., C. E. Nelson, D. H. Kim, J. Kassel, M. A. Gryka, F. Z. Bischoff, M. A. Tainsky, et al. 1990. Germ line p53 mutations in a familial syndrome of breast cancer, sarcomas, and other neoplasms. Science 250:1233-1238.
27. Maxwell, S. A., and G. E. Davis. 2000. Differential gene expression in p53-mediated apoptosis-resistant vs. apoptosis-sensitive tumor cell lines. Proc. Natl. Acad. Sci. USA 97:13009-13014.
28. McGrath, J. A., P. H. Duijf, V. Doetsch, A. D. Irvine, R. de Waal, K. R. Vanmolkot, V. Wessagowit, A. Kelly, D. J. Atherton, W. A. Griffiths, S. J. Orlow, A. van Haeringen, M. G. Ausems, A. Yang, F. McKeon, M. A. Bamshad, H. G. Brunner, B. C. Hamel, and H. van Bokhoven. 2001. Hay-Wells syndrome is caused by heterozygous missense mutations in the SAM domain of p63. Hum. Mol. Genet. 10:221-229.
29. Mills, A. A., B. Zheng, X. J. Wang, H. Vogel, D. R. Roop, and A. Bradley. 1999. p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 398:708-713.
30. Nakagawa, T., M. Takahashi, T. Ozaki, K. Watanabe Ki, S. Todo, H. Mizuguchi, T. Hayakawa, and A. Nakagawara. 2002. Autoinhibitory regulation of p73 by ΔNp73 to modulate cell survival and death through a p73-specific target element within the ΔNp73 promoter. Mol. Cell. Biol. 22:2575-2585.
31. Nakamura, Y. 2004. Isolation of p53-target genes and their functional analysis. Cancer Sci. 95:7-11.
32. Nylander, K., B. Vojtesek, R. Nenutil, B. Lindgren, G. Roos, W. Zhanxiang, B. Sjostrom, A. Dahlqvist, and P. J. Coates. 2002. Differential expression of p63 isoforms in normal tissues and neoplastic cells. J. Pathol. 198:417-427.
33. Ongusaha, P. P., J. I. Kim, L. Fang, T. W. Wong, G. D. Yancopoulos, S. A. Aaronson, and S. W. Lee. 2003. p53 induction and activation of DDR1 kinase counteract p53-mediated apoptosis and influence p53 regulation through a positive feedback loop. EMBO J. 22:1289-1301.
34. Osada, M., R. Inaba, H. Shinohara, M. Hagiwara, M. Nakamura, and Y. Ikawa. 2001. Regulatory domain of protein stability of human P51/TAP63, a P53 homologue. Biochem. Biophys. Res. Commun. 283:1135-1141.
35. Osada, M., M. Ohba, C. Kawahara, C. Ishioka, R. Kanamaru, I. Katoh, Y. Ikawa, Y. Nimura, A. Nakagawara, M. Obinata, and S. Ikawa. 1998. Cloning and functional analysis of human p51, which structurally and functionally resembles p53. Nat. Med. 4:839-843.
36. Polyak, K., Y. Xia, J. L. Zweier, K. W. Kinzler, and B. Vogelstein. 1997. A model for p53-induced apoptosis. Nature 389:300-305.
37. Ruhrberg, C., M. A. Hajibagheri, M. Simon, T. P. Dooley, and F. M. Watt. 1996. Envoplakin, a novel precursor of the cornified envelope that has homology to desmoplakin. J. Cell Biol. 134:715-729.
38. Sakuma, S., H. Saya, M. Tada, M. Nakao, T. Fujiwara, J. A. Roth, Y. Sawamura, Y. Shinohe, and H. Abe. 1996. Receptor protein tyrosine kinase DDR is up-regulated by p53 protein. FEBS Lett. 398:165-169.
39. Sasaki, Y., S. Ishida, I. Morimoto, T. Yamashita, T. Kojima, C. Kihara, T. Tanaka, K. Imai, Y. Nakamura, and T. Tokino. 2002. The p53 family member genes are involved in the Notch signal pathway. J. Biol. Chem. 277:719-724.
40. Sasaki, Y., H. Mita, M. Toyota, S. Ishida, I. Morimoto, T. Yamashita, T. Tanaka, K. Imai, Y. Nakamura, and T. Tokino. 2003. Identification of the interleukin 4 receptor α gene as a direct target for p73. Cancer Res. 63:8145-8152.
41. Schmale, H., and C. Bamberger. 1997. A novel protein with strong homology to the tumor suppressor p53. Oncogene 15:1363-1367.
42. Senoo, M., J. P. Manis, F. W. Alt, and F. McKeon. 2004. p63 and p73 are not required for the development and p53-dependent apoptosis of T cells. Cancer Cell 6:85-89.
43. Senoo, M., N. Seki, M. Ohira, S. Sugano, M. Watanabe, S. Inuzuka, T. Okamoto, M. Tachibana, T. Tanaka, Y. Shinkai, and H. Kato. 1998. A second p53-related protein, p73L, with high homology to p73. Biochem. Biophys. Res. Commun. 248:603-607.
44. Serber, Z., H. C. Lai, A. Yang, H. D. Ou, M. S. Sigal, A. E. Kelly, B. D. Darimont, P. H. Duijf, H. Van Bokhoven, F. McKeon, and V. Dotsch. 2002. A C-terminal inhibitory domain controls the activity of p63 by an intramolecular mechanism. Mol. Cell. Biol. 22:8601-8611.
45. Shimada, A., S. Kato, K. Enjo, M. Osada, Y. Ikawa, K. Kohno, M. Obinata, R. Kanamaru, S. Ikawa, and C. Ishioka. 1999. The transcriptional activities of p53 and its homologue p51/p63: similarities and differences. Cancer Res. 59:2781-2786.
46. Shiraishi, K., S. Fukuda, T. Mori, K. Matsuda, T. Yamaguchi, C. Tanikawa, M. Ogawa, Y. Nakamura, and H. Arakawa. 2000. Identification of fractalkine, a CX3C-type chemokine, as a direct target of p53. Cancer Res. 60:3722-3726.
47. Simon, M., and H. Green. 1984. Participation of membrane-associated proteins in the formation of the cross-linked envelope of the keratinocyte. Cell 36:827-834.
48. Stappenbeck, T. S., E. A. Bornslaeger, C. M. Corcoran, H. H. Luu, M. L. Virata, and K. J. Green. 1993. Functional analysis of desmoplakin domains: specification of the interaction with keratin versus vimentin intermediate filament networks. J. Cell Biol. 123:691-705.
49. Takei, Y., S. Ishikawa, T. Tokino, T. Muto, and Y. Nakamura. 1998. Isolation of a novel TP53 target gene from a colon cancer cell line carrying a highly regulated wild-type TP53 expression system. Genes Chromosomes Cancer 23:1-9.
50. Tan, M., C. W. Heizmann, K. Guan, B. W. Schafer, and Y. Sun. 1999. Transcriptional activation of the human S100A2 promoter by wild-type p53. FEBS Lett. 445:265-268.
51. 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.
52. Trink, B., K. Okami, L. Wu, V. Sriuranpong, J. Jen, and D. Sidransky. 1998. A new human p53 homologue. Nat. Med. 4:747-748.
53. van Bokhoven, H., and H. G. Brunner. 2002. Splitting p63. Am. J. Hum. Genet. 71:1-13.
54. Vogelstein, B., and K. W. Kinzler. 1992. p53 function and dysfunction. Cell 70:523-526.
55. Westfall, M. D., D. J. Mays, J. C. Sniezek, and J. A. Pietenpol. 2003. The ΔNp63α phosphoprotein binds the p21 and 14-3-3 σ promoters in vivo and has transcriptional repressor activity that is reduced by Hay-Wells syndrome-derived mutations. Mol. Cell. Biol. 23:2264-2276.
56. Yang, A., M. Kaghad, Y. Wang, E. Gillett, M. D. Fleming, V. Dotsch, N. C. Andrews, D. Caput, and F. McKeon. 1998. p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominant-negative activities. Mol. Cell 2:305-316.
57. Yang, A., R. Schweitzer, D. Sun, M. Kaghad, N. Walker, R. T. Bronson, C. Tabin, A. Sharpe, D. Caput, C. Crum, and F. McKeon. 1999. p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 398:714-718.
58. Yu, J., L. Zhang, P. M. Hwang, K. W. Kinzler, and B. Vogelstein. 2001. PUMA induces the rapid apoptosis of colorectal cancer cells. Mol. Cell 7:673-682.
59. Zheng, X., and X. Chen. 2001. Aquaporin 3, a glycerol and water transporter, is regulated by p73 of the p53 family. FEBS Lett. 489:4-7.
60. Zhu, K., J. Wang, J. Zhu, J. Jiang, J. Shou, and X. Chen. 1999. p53 induces TAP1 and enhances the transport of MHC class I peptides. Oncogene 18:7740-7747.
61. Zou, Z., C. Gao, A. K. Nagaich, T. Connell, S. Saito, J. W. Moul, P. Seth, E. Appella, and S. Srivastava. 2000. p53 regulates the expression of the tumor suppressor gene maspin. J. Biol. Chem. 275:6051-6054.