Increased apoptosis induction by 121F mutant p53

EMBO Journal

Volumn 18, Issue 16, 1999, Pages 4424-4437

  Saller, Elisabeth ^a   Tom, Edward ^b   Brunori, Michele ^a   Otter, Michèle ^a   Estreicher, Anne ^a   Mack, David H ^b   Iggo, Richard ^a  

^a SWISS INST FOR EXP CANCER RESEARCH   (Switzerland)

^b Eos Biotechnology   (United States)

Author keywords

Apoptosis; MDM2; p53; PIR121; Rad

Indexed keywords

DNA; MUTANT PROTEIN; ONCOPROTEIN; PROTEIN P53; RNA;

APOPTOSIS; ARTICLE; BINDING AFFINITY; FIBROBLAST; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; TUMOR CELL;

ANIMALS; APOPTOSIS; BASE SEQUENCE; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLINS; DNA, COMPLEMENTARY; GENE EXPRESSION REGULATION; HUMANS; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS; NUCLEAR PROTEINS; PHENOTYPE; PROMOTER REGIONS (GENETICS); PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-MDM2; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0033575732     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.16.4424     Document Type: Article

References (87)

1. Cip1/WAF1 in monocytic differentiation. EMBO J., 18, 1223-1234.
2. Banin, S. et al. (1998) Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science, 281, 1674-1677.
3. Barak, Y., Juven, T., Haffner, R. and Oren, M. (1993) mdm2 expression is induced by wild-type p53 activity. EMBO J., 12, 461-468.
4. Buckbinder, L., Talbott, R., Velasco-Miguel, S., Takenaka, I., Faha, B., Seizinger, B.R. and Kley, N. (1995) Induction of the growth inhibitor IGF-binding protein 3 by p53. Nature, 377, 646-649.
5. Buckbinder, L. et al. (1997) The p53 tumor suppressor targets a novel regulator of G protein signaling. Proc. Natl Acad. Sci. USA, 94, 7868-7872.
6. Bunz, F., Dutriaux, A., Lengauer, C., Waldman, T., Zhou, S., Brown, J.P., Sedivy, J.M., Kinzler, K.W. and Vogelstein, B. (1998) Requirement for p53 and p21 to sustain G (2) arrest after DNA damage. Science, 282, 1497-1501.
7. Canman, C.E., Lim, D.S., Cimprich, K.A., Taya, Y. Tamai, K., Sakaguchi, K., Appella, E., Kastan, M.B. and Siliciano, J.D. (1998) Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science, 281, 1677-1679.
8. Chen, X., Ko, L.J., Jayaraman, L. and Prives, C. (1996) p53 levels, functional domains and DNA damage determine the extent of the apoptotic response of tumor cells. Genes Dev., 10, 2438-2451.
9. Cho, Y., Gorina, S., Jeffrey, P.D. and Pavletich, N.P. (1994) Crystal structure of a p53 tumor suppressor-DNA complex: understanding tumorigenic mutations. Science, 265, 346-355.
10. Clayman, G.L. et al. (1998) Adenovirus-mediated p53 gene transfer in patients with advanced recurrent head and neck squamous cell carcinoma. J. Clin. Oncol., 16, 2221-2232.
11. Comer, K.A., Dennis, P.A., Armstrong, L., Catino, J.J., Kastan, M.B. and Kumar, C.C. (1998) Human smooth muscle alpha-actin gene is a transcriptional target of the p53 tumor suppressor protein. Oncogene, 16, 1299-1308.
12. de Stanchina, E. et al. (1998) E1A signaling to p53 involves the p19 (ARF) tumor suppressor. Gene Dev., 12, 2434-2442.
13. Di Como, C.J. and Prives, C. (1998) Human tumor-derived p53 proteins exhibit binding site selectivity and temperature sensitivity for transactivation in a yeast-based assay. Oncogene, 16, 2527-2539.
14. 1 arrest. Cell, 76, 1013-1023.
15. el-Deiry, W.S., Kern, S.E., Pietenpol, J.A., Kinzler, K.W. and Vogelstein, B. (1992) Definition of a consensus binding site for p53. Nature Genet., 1, 45-49.
16. el-Deiry, W.S. et al. (1993) p21, a potential mediator of p53 tumor suppression. Cell, 75, 817-825.
17. Feinberg, A.P. and Vogelstein, B. (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem., 132, 6-13.
18. Flaman, J.M., Frebourg, T., Moreau, V., Charbonnier, F., Martin, C., Ishioka, C., Friend, S.H. and Iggo, R. (1994) A rapid PCR fidelity assay. Nucleic Acids Res., 22, 3259-3260.
19. Flaman, J.M., Robert, V., Lenglet, S., Moreau, V., Iggo, R. and Frebourg, T. (1998) Identification of human p53 mutations with differential effects on the bax and p21 promoters using functional assays in yeast. Oncogene, 16, 1369-1372.
20. Freeman, J., Schmidt, S., Scharer, E. and Iggo, R. (1994) Mutation of conserved domain II alters the sequence specificity of DNA binding by the p53 protein. EMBO J., 13, 5393-5400.
21. Friedlander, P., Haupt, Y., Prives, C. and Oren, M. (1996) A mutant p53 that discriminates between p53-responsive genes cannot induce apoptosis. Mol. Cell. Biol., 16, 4961-4971.
22. Funk, W.D., Pak, D.T., Karas, R.H., Wright, W.E. and Shay, J.W. (1992) A transcriptionally active DNA-binding site for human p53 protein complexes. Mol. Cell. Biol., 12, 2866-2871.
23. Gagnebin, J., Brunori, M., Otter, M., Juillerat-Jeaneret, L., Monnier, P. and Iggo, R. (1999) A photosensitising adenovirus for photodynamic therapy. Gene Therapy, in press.
24. Gomez-Manzano, C., Fueyo, J., Kyritsis, A.P., McDonnell, T.J., Steck, P.A., Levin, V.A. and Yung, W.K. (1997) Characterization of p53 and p21 functional interactions in glioma cells en route to apoptosis. J. Natl Cancer Inst., 89, 1036-1044.
25. Gossen, M. and Bujard, H. (1992) Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl Acad. Sci. USA, 89, 5547-5551.
26. Grossman, S.R., Perez, M., Kung, A.L., Joseph, M., Mansur, C., Xiao, Z.X., Kumar, S., Howley, P.M. and Livingston, D.M. (1998) p300/MDM2 complexes participate in MDM2-mediated p53 degradation. Mol. Cell, 2, 405-415.
27. Harlow, E. and Lane, D.P. (1988) Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
28. Haupt, Y., Maya, R., Kazaz, A. and Oren, M. (1997) Mdm2 promotes the rapid degradation of p53. Nature, 387, 296-299.
29. Hengstermann, A., Whitaker, N.J., Zimmer, D., Zentgraf, H. and Scheffner, M. (1998) Characterization of sequence elements involved in p53 stability regulation reveals cell type dependence for p53 degradation. Oncogene, 17, 2933-2941.
30. Hinds, P.W., Finlay, C.A., Quartin, R.S., Baker, S.J., Fearon, E.R., Vogelstein, B. and Levine, A.J. (1990) Mutant p53 DNA clones from human colon carcinomas cooperate with ras in transforming primary rat cells: a comparison of the 'hot spot' mutant phenotypes. Cell Growth Differ., 1, 571-580.
31. Honda, R. and Yasuda, H. (1999) Association of p19 (ARF) with Mdm2 inhibits ubiquitin ligase activity of Mdm2 for tumor suppressor p53. EMBO J., 18, 22-27.
32. Ichijo, H. et al. (1997) Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science, 275, 90-94.
33. Israeli, D., Tessler, E., Haupt, Y., Elkeles, A., Wilder, S., Amson, R., Telerman, A. and Oren, M. (1997) A novel p53-inducible gene, PAG608, encodes a nuclear zinc finger protein whose overexpression promotes apoptosis. EMBO J., 16, 4384-4392.
34. Juven, T., Barak, Y., Zauberman, A., George, D.L. and Oren, M. (1993) Wild-type p53 can mediate sequence-specific transactivation of an internal promoter within the mdm2 gene. Oncogene, 8, 3411-3416.
35. Kastan, M.B., Zhan, Q., el-Deiry, W.S., Carrier, F., Jacks, T., Walsh, W.V., Plunkett, B.S., Vogelstein, B. and Fornace, A.J., Jr (1992) A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxia-telangiectasia. Cell, 71, 587-597.
36. Ketner, G., Spencer, F., Tugendreich, S., Connelly, C. and Hieter, P. (1994) Efficient manipulation of the human adenovirus genome as an infectious yeast artificial chromosome clone. Proc. Natl Acad. Sci. USA, 91, 6186-6190.
37. Ko, L.J. and Prives, C. (1996) p53: puzzle and paradigm. Genes Dev., 10, 1054-1072.
38. Koster, F., Schinke, B., Niemann, S. and Hermans-Borgmeyer, I. (1998) Identification of shyc, a novel gene expressed in the murine developing and adult nervous system. Neurosci. Lett., 252, 69-71.
39. Kubbutat, M.H., Jones, S.N. and Vousden, K.H. (1997) Regulation of p53 stability by Mdm2. Nature, 387, 299-303.
40. Laborda, J. (1991) 36B4 cDNA used as an estradiol-independent mRNA control is the cDNA for human acidic ribosomal phosphoprotein PO. Nucleic Acids Res., 19, 3998.
41. Larionov, V., Kouprina, N., Graves, J., Chen, X.N., Korenberg, J.R. and Resnick, M.A. (1996) Specific cloning of human DNA as yeast artificial chromosomes by transformation-associated recombination. Proc. Natl Acad. Sci. USA, 93, 491-496.
42. Levine, A.J. (1997) p53, the cellular gatekeeper for growth and division. Cell, 88, 323-331.
43. Lin, J., Chen, J., Elenbaas, B. and Levine, A.J. (1994) Several hydrophobic amino acids in the p53 amino-terminal domain are required for transcriptional activation, binding to mdm-2 and the adenovirus 5 E1B 55-kD protein. Genes Dev., 8, 1235-1246.
44. Lowe, S.W., Schmitt, E.M., Smith, S.W., Osborne, B.A. and Jacks, T. (1993) p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature, 362, 847-849.
45. Lu, H. and Levine, A.J. (1995) Human TAFII31 protein is a transcriptional coactivator of the p53 protein. Proc. Natl Acad. Sci. USA, 92, 5154-5158.
46. Ludwig, R.L., Bates, S. and Vousden, K.H. (1996) Differential ctivation of target cellular promoters by p53 mutants with impaired apoptotic function. Mol. Cell Biol., 16, 4952-4960.
47. Madden, S.L., Galella, E.A., Zhu, J., Bertelsen, A.H. and Beaudry, G.A. (1997) SAGE transcript profiles for p53-dependent growth regulation. Oncogene, 15, 1079-1085.
48. Mayo, L.D., Turchi, J.J. and Berberich, S.J. (1997) Mdm-2 phosphorylation by DNA-dependent protein kinase prevents interaction with p53. Cancer Res., 57, 5013-5016.
49. McCurrach, M.E., Connor, T.M., Knudson, C.M., Korsmeyer, S.J. and Lowe, S.W. (1997) bax-deficiency promotes drug resistance and oncogenic transformation by attenuating p53-dependent apoptosis. Proc. Natl Acad. Sci. USA, 94, 2345-2349.
50. Miyashita, T. and Reed, J.C. (1995) Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell, 80, 293-299.
51. Montes de Oca Luna, R., Wagner, D.S. and Lozano, G. (1995) Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53. Nature, 378, 203-206.
52. Morgenstern, J.P. and Land, H. (1990) Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res., 18, 3587-3596.
53. Moyers, J.S., Bilan, P.J., Zhu, J. and Kahn, C.R. (1997) Rad and Rad-related GTPases interact with calmodulin and calmodulin-dependent protein kinase II. J. Biol. Chem., 272, 11832-11839.
54. Ogawa, N. et al. (1997) Novel combination therapy for human colon cancer with adenovirus-mediated wild-type p53 gene transfer and DNA-damaging chemotherapeutic agent. Int. J. Cancer, 73, 367-370.
55. Okamoto, K. and Beach, D. (1994) Cyclin G is a transcriptional target of the p53 tumor suppressor protein. EMBO J., 13, 4816-4822.
56. Owen-Schaub, L.B. et al. (1995) Wild-type human p53 and a temperature-sensitive mutant induce Fas/APO-1 expression. Mol. Cell Biol., 15, 3032-3040.
57. Palmero, I., Pantoja, C. and Serrano, M. (1998) p19ARF links the tumour suppressor p53 to Ras. Nature, 395, 125-126.
58. Polyak, K., Waldman, T., He, T.C., Kinzler, K.W. and Vogelstein, B. (1996) Genetic determinants of p53-induced apoptosis and growth arrest. Genes Dev., 10, 1945-1952.
59. Polyak, K., Xia, Y., Zweier, J.L., Kinzler, K.W. and Vogelstein, B. (1997) A model for p53-induced apoptosis. Nature, 389, 300-305.
60. Ponten, J. and Macintyre, E.H. (1968) Long term culture of normal and neoplastic human glia. Acta Pathol. Microbiol. Scand., 74, 465-486.
61. Rampino, N., Yamamoto, H., Ionov, Y., Li, Y., Sawai, H., Reed, J.C. and Perucho, M. (1997) Somatic frameshift mutations in the BAX gene in colon cancers of the microsatellite mutator phenotype. Science, 275, 967-969.
62. Reinke, V. and Lozano, G. (1997) The p53 targets mdm2 and Fas are not required as mediators of apoptosis in vivo. Oncogene, 15, 1527-1534.
63. Resnick-Silverman, L., St Clair, S., Maurer, M., Zhao, K. and Manfredi, J.J. (1998) Identification of a novel class of genomic DNA-binding sites suggests a mechanism for selectivity in target gene activation by the tumor suppressor protein p53. Genes Dev., 12, 2102-2107.
64. Reynet, C. and Kahn, C.R. (1993) Rad: a member of the Ras family overexpressed in muscle of type II diabetic humans. Science, 262, 1441-1444.
65. Roemer, K. and Mueller-Lantzsch, N. (1996) p53 transactivation domain mutant Q22, S23 is impaired for repression of promoters and mediation of apoptosis. Oncogene, 12, 2069-2079.
66. Roth, J., Dobbelstein, M., Freedman, D.A., Shenk, T. and Levine, A.J. (1998) Nucleo-cytoplasmic shuttling of the hdm2 oncoprotein regulates the levels of the p53 protein via a pathway used by the human immunodeficiency virus rev protein. EMBO J., 17, 554-564.
67. Rowan, S., Ludwig, R.L., Haupt, Y., Bates, S., Lu, X., Oren, M. and Vousden, K.H. (1996) Specific loss of apoptotic but not cell-cycle arrest function in a human tumor derived p53 mutant. EMBO J., 15, 827-838.
68. Sambrook, J., Fritsch, E. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
69. Scharer, E. and Iggo, R. (1992) Mammalian p53 can function as a transcription factor in yeast. Nucleic Acids Res., 20, 1539-1545.
70. Scolnick, D.M., Chehab, N.H., Stavridi, E.S., Lien, M.C., Caruso, L., Moran, E., Berger, S.L. and Halazonetis, T.D. (1997) CREB-binding protein and p300/CBP-associated factor are transcriptional coactivators of the p53 tumor suppressor protein. Cancer Res., 57, 3693-3696.
71. Sheikh, M.S., Carrier, F., Johnson, A.C., Ogdon, S.E. and Fornace, A.J., Jr. (1997) Identification of an additional p53-responsive site in the human epidermal growth factor receptor gene promotor. Oncogene, 15, 1095-1101.
72. Sherr, C.J. (1998) Tumor surveillance via the ARF-p53 pathway. Genes Dev., 12, 2984-2991.
73. Shieh, S.Y., Ikeda, M., Taya, Y. and Prives, C. (1997) DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell, 91, 325-334.
74. Shieh, S.Y., Taya, Y. and Prives, C. (1999) DNA damage-inducible phosphorylation of p53 at N-terminal sites including a novel site, Ser20, requires tetramerization. EMBO J., 18, 1815-1823.
75. Shivakumar, C.V., Brown, D.R., Deb, S. and Deb, S.P. (1995) Wild-type human p53 transactivates the human proliferating cell nuclear antigen promoter. Mol. Cell Biol., 15, 6785-6793.
76. Tada, M., Iggo, R.D., Ishii, N., Shinohe, Y., Sakuma, S., Estreicher, A., Sawamura, Y. and Abe, H. (1996) Clonality and stability of the p53 gene in human astrocytic tumor cells: quantitative analysis of p53 gene mutations by yeast functional assay. Int. J. Cancer, 67, 447-450.
77. Thut, C.J., Chen, J.L., Klemm, R. and Tjian, R. (1995) p53 transcriptional activation mediated by coactivators TAFII40 and TAFII60. Science, 267, 100-104.
78. Unger, T., Juven-Gershon, T., Moallem, E., Berger, M., Sionov, R.V., Lozano, G., Oren, M. and Haupt, Y. (1999) Critical role for Ser20 of human p53 in the negative regulation of p53 by Mdm2. EMBO J., 18, 1805-1814.
79. Varmeh-Ziaie, S., Okan, I., Wang, Y., Magnusson, K.P., Warthoe, P., Strauss, M. and Wiman, K.G. (1997) Wig-1, a new p53-induced gene encoding a zinc finger protein. Oncogene, 15, 2699-2704.
80. Vojtesek, B., Bartek, J., Midgley, C.A. and Lane, D.P. (1992) An immunochemical analysis of the human nuclear phosphoprotein p53. New monoclonal antibodies and epitope mapping using recombinant p53. J. Immunol. Methods, 151, 237-244.
81. Waldman, T., Zhang, Y., Dillehay, L., Yu, J., Kinzler, K., Vogelstein, B. and Williams, J. (1997) Cell-cycle arrest versus cell death in cancer therapy. Nature Med., 3, 1034-1036.
82. Weber, J.D., Taylor, L.J., Roussel, M., Sherr, C. and Bar-Sagi, D. (1999) Nucleolar Arf sequesters Mdm2 and activates p53. Nature Cell Biol., 1, 20-26.
83. Wodicka, L., Dong, H., Mittmann, M., Ho, M.H. and Lockhart, D.J. (1997) Genome-wide expression monitoring in Saccharomyces cerevisiae. Nature Biotechnol., 15, 1359-1367.
84. Wu, G.S. et al. (1997) KILLER/DR5 is a DNA damage-inducible p53-regulated death receptor gene. Nature Genet., 17, 141-143.
85. Wu, X., Bayle, J.H., Olson, D. and Levine, A.J. (1993) The p53-mdm-2 autoregulatory feedback loop. Genes Dev., 7, 1126-1132.
86. Zhu, J., Bilan, P.J., Moyers, J.S., Antonetti, D.A. and Kahn, C.R. (1996) Rad, a novel Ras-related GTPase, interacts with skeletal muscle betatropomyosin. J. Biol. Chem., 271, 768-773.
87. Zindy, F., Eischen, C.M., Randle, D.H., Kamijo, T., Cleveland, J.L., Sherr, C.J. and Roussel, M.F. (1998) Myc signaling via the Arf tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev., 12, 2424-2433.