Mutant p53: Gain-of-function oncoproteins and wild-type p53 inactivators

Biological Chemistry

Volumn 380, Issue 7-8, 1999, Pages 879-887

  Roemer, Klaus ^a  

^a SAARLAND UNIVERSITY   (Germany)

Author keywords

Conformation; Dominant negative; Gain of function; Mutant p53; Transcription

Indexed keywords

AMINO ACID; MUTANT PROTEIN; ONCOPROTEIN; PROTEIN P53; TETRAMER; TRANSCRIPTION FACTOR;

CANCER; CARCINOGENICITY; CELL CULTURE; CELL IMMORTALIZATION; CELL SURVIVAL; METASTASIS POTENTIAL; PHENOTYPE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN CONFORMATION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN TERTIARY STRUCTURE; REVIEW; THERAPY RESISTANCE;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; GENES, DOMINANT; MUTATION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0032853774     PISSN: 14316730     EISSN: None     Source Type: Journal    
DOI: 10.1515/BC.1999.108     Document Type: Review

References (86)

1. Aaltonen, L.A., Peltomäki, P., Leach, F.S., Sistonen, P., Pylkkänen, L. et al. (1993). Clues to the pathogenesis of familial colorectal cancer. Science 260, 812-816.
2. Aas, T., Borresen, A.-L., Geisler, S., Smith-Sorensen, B., Johnsen, H. et al. (1996). Specific p53 mutations are associated with de novo resistance to doxorubicin in breast cancer patients. Nature Genet. 2, 811-814.
3. Albor, A., Kaku, S., and Kulesz-Martin, M. (1998). Wild-type and mutant forms of p53 activate human topoisomerase I: a possible mechanism for gain of function in mutants. Cancer Res. 58, 2091-2094.
4. Attardi, L.D., and Jacks, T. (1999). The role of p53 in tumour suppression: lessons from mouse models. Cell. Mol. Life Sci. 55, 48-63.
5. Bargonetti, J., Reynisdóttir, I., Friedman, P.N., and Prives, C. (1992). Site-specific binding of wild-type p53 to cellular DNA is inhibited by SV40 T antigen and mutant p53. Genes Dev. 6, 1886-1898.
6. Bates, S., and Vousden, K.H. (1999). Mechanisms of p53-mediated apoptosis. Cell. Mol. Life Sci. 55, 28-37.
7. Birch, L.M., Blair, V., Kelsey, A.M., Evans, D.G., Harris, M. et al. (1998). Cancer phenotype correlates with constitutional TP53 genotype in families with Li-Fraumeni syndrome. Oncogene 17, 1061-1068.
8. Bischoff, F.Z., Yim, S.O., Pathak, S., Grant, G., Siliciano, M.J. et al. (1990). Spontaneous abnormalities in normal fibroblasts from patients with Li-Fraumeni cancer syndrome: aneuploidy and immortalization. Cancer Res. 50, 7979-7984.
9. Bischoff, F.Z., Strong, L.C., Yim, S.O., Pratt, D.R., Siliciano, M.J. et al. (1991). Tumorigenic transformation of spontaneously immortalized fibroblasts from patients with a familial cancer syndrome. Oncogene 6, 183-186.
10. Blandino, G., Levine, A.J., and Oren, M. (1999). Mutant p53 gain of function: differential effects of different p53 mutants on resistance of cultured cells to chemotherapy. Oncogene 18, 477-485.
11. Bond, J.A., Wyllie, F.S., and Wynford-Thomas, D. (1994). Escape from senescence in human diploid fibroblasts induced directly by mutant p53. Oncogene 9, 1885-1889.
12. Borresen, A.-L., Anderson, T.I., Eyfjord, J.E., Cornelis, R.S., Thorlacius, S. et al. (1995). TP53 mutations and breast cancer prognosis: particularly poor survival rates for cases with mutations in the zinc-binding domains. Genes Chromosom. Cancer 14, 71-75.
13. Brachmann, R.K., Vidal, M., and Boeke, J.D. (1996). Dominant-negative p53 mutants selected in yeast hit cancer hot spots. Proc. Natl. Acad. Sci. USA 93, 4091-4095.
14. Chene, P. (1998). In vitro analysis of the dominant negative effect of p53 mutants. J. Mol. Biol. 281, 205-209.
15. Chene, P. (1999). p53 mutants without a functional tetramerization domain are not oncogenic. J. Mol. Biol. 286, 1269-1274.
16. Chin, K.-V., Ueda, K., Pastan, I., and Gottesman, M.M. (1992). Modulation of activity of the promoter of the human MDR1 gene by ras and p53. Science 255, 459-462.
17. 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.
18. Choi, J., and Donehower, L.A. (1999). p53 in embryonic development: maintaining a fine balance. Cell. Mol. Life Sci. 55, 38-47.
19. Cross, S.M., Sanchez, C.A., Morgan, C.A., Schimke, M.K., Ramel, S. et al. (1995). A p53-dependent mouse spindle checkpoint. Science 267, 1353-1356.
20. Deb, S.P., Munoz, R.M., Brown, D.R., Subler, M.A., and Deb, S. (1994). Wild-type human p53 activates the human epidermal growth factor receptor promoter. Oncogene 9, 1341-1349.
21. Di Como, C.J., Gaiddon, C., and Prives, C. (1999). p73 function is inhibited by tumor-derived p53 mutants in mammalian cells. Mol. Cell. Biol. 19, 1438-1449.
22. DiLeonardo, A., Khan, S.H., Linke, S.P., Greco, V., Seidita, G. et al. (1997). DNA rereplication in the presence of mitotic spindle inhibitors in human and mouse fibroblasts lacking either p53 or pRb function. Cancer Res. 57, 1013-1019.
23. Dittmer, D., Pati, S., Zambetti, G., Chu, S., Teresky, A.K. et al. (1993). Gain of function mutations in p53. Nature Genet 4, 42-46.
24. Eliyahu, D., Raz, A., Gruss, P., Givol, D., and Oren, M. (1984). Participation of p53 cellular tumor antigen in transformation of normal embryonic cells. Nature 312, 646-649.
25. Eliyahu, D., Goldfinger, N., Pinhasi-Kimhi, O., Shaulsky, G., Skurnik, Y. et al. (1988). Meth A fibrosarcoma cells express two transforming mutant p53 species. Oncogene 3, 313-321.
26. Eshleman, J.R., Casey, G., Kochera, M.E., Sedwick, W.D., Swinler, S.E. et al. (1998). Chromosome number and structure both are markedly stable in RER colorectal cancers and are not destabilized by mutation of p53. Oncogene 17, 719-725.
27. Finlay, C.A., Hinds, P.W., Tan, T.-H., Eliyahu, D., Oren, M. et al. (1988). Activating mutations for transformation by p53 produce a gene product that forms an hsc70-p53 complex with an altered half-life. Mol. Cell. Biol. 8, 531-539.
28. Finlay, C.A., Hinds, P.W., and Levine, A.J. (1989). The p53 protooncogene can act as a suppressor of transformation. Cell 57, 1083-1093.
29. Frazier, M.W., He, X., Wang, J., Gu, Z., Cleveland, J.L. et al. (1998). Activation of c-myc gene expression by tumor-derived p53 mutants requires a discrete C-terminal domain. Mol. Cell. Biol. 18, 3735-3743.
30. Frebourg, T., Sadelain, M., Ng, Y.-S., Kassel, J., and Friend, S.H. (1994). Equal transcription of wild-type and mutant p53 using bicistronic vectors result in the wild-type phenotype. Cancer Res. 54, 878-881.
31. Friedman, P.N., Chen, X., Bargonetti, J., and Prives, C. (1993). The p53 protein is an unusually shaped tetramer that binds directly to DNA. Proc. Natl. Acad. Sci. USA 90, 3319-3323.
32. Greenblatt, M.S., Bennett, W.P., Hollstein, M., and Harris, C.C. (1994). Mutations in the p53 tumor suppressor gene: clues to cancer etiology and molecular pathogenesis. Cancer Res. 54, 4855-4878.
33. Gualberto, A., Aldape, K., Kozakiewicz, K., and Tlsty, T.D. (1998). An oncogenic form of p53 confers a dominant, gain-of-function phenotype that disrupts spindle checkpoint control. Proc. Natl. Acad. Sci. USA 95, 5166-5171.
34. Halazonetis, T.D., and Kandil, A.N. (1993). Conformational shifts propagate from the oligomerization domain of p53 to its tetrameric DNA binding domain and restore DNA binding to select p53 mutants. EMBO J. 12, 5057-5064.
35. Halevy, O., Michalovitz, D., and Oren, M. (1990). Different tumorderived p53 mutants exhibit distinct biological activities. Science 250, 113-116.
36. Hara, E., Tsurui, H., Shinozaki, A., Nakada, S., and Oda, K. (1991). Cooperative effect of antisense-Rb and antisense-p53 oligomers on the extension of life span in human diploid fibroblasts, TIG-1. Biochem. Biophys. Res. Commun. 179, 528-534.
37. Harris, C.C. (1996). p53 tumor suppressor gene: from the basic research laboratory to the clinic - an abridged historical perspective. Carcinogenesis 17, 1187-1198.
38. Harvey, D.M., and Levine, A.J. (1991). p53 Alteration is a common event in the spontaneous immortalization of primary BALB/c murine embryo fibroblasts. Genes Dev. 5, 2375-2385.
39. Harvey, M., Vogel, H., Morris, D., Bradley, A., Bernstein, A. et al. (1995). A mutant p53 transgene accelerates tumour development in heterozygous but not nullizygous p53-deficient mice. Nature Genet. 9, 305-311.
40. Herskowitz, I. (1987). Functional interaction of genes by dominant negative mutations. Nature 329, 212-222.
41. Hinds, P., Findlay, C., and Levine, A.J. (1989). Mutation is required to activate the p53 gene for cooperation with the ras oncogene and transformation. J. Virol. 63, 739-746.
42. Hinds, P.W., Finlay, C.A., Quartin, R.S., Baker, S.J., Fearon, E.R. et al. (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 Diff. 1, 571-580.
43. Hollstein, M., Shimer, B., Greenblatt, M., Soussi, T., Hovig, E. et al. (1996). Somatic point mutations in the p53 gene of human tumors and cell lines: updated compilation. Nucl. Acids Res. 24, 141-146.
44. Iwamoto, K.S., Mizuno, T., Ito, T., Tsuyama, N., Kyoizumi, S. et al. (1996). Gain-of-function p53 mutations enhance alteration of the T-cell receptor following X-irradiation, independently of the cell cycle and cell survival. Cancer Res. 56, 3862-3865.
45. Jenkins, J.R., Rudge, K., and Currie, G.A. (1984). Cellular immortalization by a cDNA clone encoding the transformation-association phosphoprotein p53. Nature 312, 651-654.
46. Kern, S.E., Pietenpol, J.A., Thiagalingam, S., Seymour, A., Kinzler, K.W. et al. (1992). Oncogenic forms of p53 inhibit p53-regulated gene expression. Science 256, 827-830.
47. Kieser, A., Weich, H.A., Brandner, G., Marme, D., and Kolch, W. (1994). Mutant p53 potentiates protein kinase C induction of vascular endothelial growth factor expression. Oncogene 9, 963-969.
48. Lanni, J.S., and Jacks, T. (1998). Characterization of the p53-dependent postmitotic checkpoint following spindle disruption. Mol. Cell. Biol. 18, 1055-1064.
49. Lanyi, A., Deb, D., Seymour, R.C., Ludes-Meyer, J.H., Subler, M.A. et al. (1998). 'Gain of function' phenotype of tumor-derived mutant p53 requires the oligomerization/nonsequence-specific nucleic acid-binding domain. Oncogene 16, 3169-3176.
50. Lavigueur, A., Maltby, V., Mock, D., Rossant, J., Pawson, T. et al. (1989). High incidence of lung, bone and lymphoid tumors in transgenic mice overexpressing mutant alleles of the p53 oncogene. Mol. Cell. Biol. 9, 3982-3991.
51. Lengauer, C., Kinzler, K.W., and Vogelstein, B. (1998). Genetic instabilities in human cancers. Nature 396, 643-649.
52. Levine, A.J. (1997). p53, the cellular gatekeeper for growth and division. Cell 88, 323-331.
53. Li, R., Sutphin, P.D., Schwartz, D., Matas, D., Almog, N. et al. (1998). Mutant p53 protein expression interferes with p53-independent apoptotic pathways. Oncogene 16, 3269-3277.
54. Lin, J., Teresky, A.K., and Levine, A.J. (1995). Two critical hydrophobic amino acids in the N-terminal domain of the p53 protein are required for the gain of function phenotypes of human p53 mutants. Oncogene 10, 2387-2390.
55. Liu, P.K., Kraus, E., Wu, T.A., Strong, L.C., and Tainsky, M.A. (1996). Analysis of genomic instability in Li-Fraumeni fibroblasts with germline p53 mutations. Oncogene 12, 2267-2278.
56. Livingstone, L.R., White, A., Sprouse, J., Livanos, E., Jacks, T. et al. (1992). Altered cell cycle arrest and gene amplification potential accompany loss of wild-type p53. Cell 70, 923-935.
57. Lowe, S.W., Bodis, S., McClatchey, A., Remington, L., Ruley, H.E. et al. (1994). p53 status and efficacy of cancer therapy in vivo. Science 266, 807-810.
58. McLure, K.G., and Lee, P.W. (1998). How p53 binds DNA as a tetramer. EMBO J. 17, 3342-3350.
59. Midgley, C.A., and Lane, D.P. (1997). p53 protein stability in tumour cells is not determined by mutation but is dependent on Mdm2 binding. Oncogene 15, 1179-1189.
60. Milner, J. (1995). Flexibility: the key to p53 function? Trends Biochem. Sci. 20, 49-51.
61. Milner, J., and Medcalf, E.A. (1991). Cotranslation of activated mutant p53 with wild-type drives the wild-type p53 protein into the mutant conformation. Cell 65, 765-774.
62. Parada, L.F., Land, H., Weinberg, R.A., Wolf, D., and Rotter, V. (1984). Cooperation between gene encoding p53 tumor antigen and ras in cellulartransformation. Nature 312, 649-651.
63. Picksley, S.M., Spicer, J.F., Barnes, D.M., and Lane, D.P. (1996). The p53-MDM2 interaction in a cancer-prone family, and the identification of a novel therapeutic target. Acta Oncologica 35, 429-434.
64. Pietenpol, J.A., Tokino, T., Thiagalingam, S., El-Deiry, W.S., Kinzler, K.W. et al. (1994). Sequence-specific transcriptional activation is essential for growth suppression by p53. Proc. Natl. Acad. Sci. USA 91, 1998-2002.
65. Pohl, J., Goldfinger, N., Radler-Pohl, A., Rotter, V., and Schirrmacher, V. (1988). p53 increases experimental metastatic capacity of murine carcinoma cells. Mol. Cell. Biol 8, 2078-2081.
66. Prives, C. (1994). How loops, β-sheets, and α-helices help us understand p53. Cell 78, 543-546.
67. Rolley, N., Butcher, S., and Milner, J. (1995). Specific DNA binding by different classes of human p53 mutants. Oncogene 11, 763-770.
68. Rovinsky, B., and Benchimol, S. (1988). Immortalization of rat embryo fibroblasts by the cellular p53 oncogene. Oncogene 2, 445-452.
69. Shaulsky, G., Goldfinger, N., Rotter, V. (1991). Alterations in tumor development in vivo mediated by expression of wild type or mutant p53 proteins. Cancer Res. 51, 5232-5237.
70. Slingerland, J.M., Jenkins, J.R., and Benchimol, S. (1993). The transforming and suppressor functions of p53 alleles: effects of mutations that disrupt phosphorylation, oligomerization and nuclear translocation. EMBO J. 12, 1029-1037.
71. Srivastava, S., Wang, S., Tong, Y.A., Pirollo, K., Chang, E.H. (1993). Several mutant p53 proteins detected in cancer-prone families with Li-Fraumeni syndrome exhibit transdominat effects on the biochemical properties of wild-type p53. Oncogene 8, 2449-2456.
72. Taubert, H., Meye, A., and Wurl, P. (1996). Prognosis is correlated with p53 mutation type for soft tissue sarcoma patients. Cancer Res. 56, 4134-4136.
73. Thottassery, J.V., Zambetti, G.P., Arimori, K., Schuetz, E.G., and Schuetz, J.D. (1997). p53-dependent regulation of MDR1 gene expression causes selective resistance to chemotherapeutic agents. Proc. Natl. Acad. Sci. USA 94, 11037-11042.
74. Tsutsumi-Ishi, Y., Tadokoro, K., Hanaoka, F., and Tsuchida, N. (1995). Response of heat shock element within the human HSP70 promoter to mutated p53. Cell Growth Diff. 6, 1-8.
75. Ueba, T., Nosaka, T., Takahashi, J.A., Shibata, F., Florkiewicz, R.Z. et al. (1994). Transcriptional regulation of basis fibroblast growth factor gene by p53 in human glioblastoma and hepatocellular carcinoma cells. Proc. Natl. Acad. Sci. USA 91, 9009-9013.
76. Varley, J.M., Evans, D.G.R., and Birch, J.M. (1997a). Li-Fraumeni syndrome - a molecular and clinical review. Br. J. Cancer 76, 1-14.
77. Varley, J.M., Thorncroft, M., McGown, G., Appleby, J., Kelsey, A.M. et al. (1997b). A detailed study of loss of heterozygosity on chromosome 17 in tumours from Li-Fraumeni patients carrying a mutation in the TP53 gene. Oncogene 14, 865-872.
78. Vega, F.J., Iniesta, P., Caldes, T., Sanchez, A., Lopez, J.A. et al. (1997). p53 exon 5 mutations as a prognostic indicator of shortened survival in non-small-cell lung cancer. Br. J. Cancer 76, 44-51.
79. Venkatachalam, S., Shi, Y.-P., Jones, S.N., Vogel, H., Bradley, A. et al. (1998). Retention of wild-type p53 in tumors from p53 heterozygous mice: reduction of p53 dosage can promote cancer formation. EMBO J. 17, 4657-4667.
80. Wallace-Brodeur, R.R., and Lowe, S.W. (1999). Clinical implications of p53 mutations. Cell Mol Life Sci 55, 64-75.
81. Wang, L.-H., Okaichi, K., Ihara, M., Okamura, Y. (1998a). Sensitivity of anticancer drugs in Saos-2 cells transfected with mutant p53 varied with mutation point. Anticancer Res. 18, 321-326.
82. Wang, X.-J., Greenhalgh, D.A., Jiang, A., He, D., Zhong, L. et al. (1998b). Analysis of centrosome abnormalities and angiogenesis in epidermal-targeted p53-172H mutant and p53-knockout mice after chemical carcinogenesis: evidence for a gain of function. Mol. Carcinogen. 23, 185-192.
83. Weinstein, J.N., Myers, T.G., O'Connor, P.M., Friend, S.H., Fornace, A.J., Jr. et al. (1997). An information-intensive approach to the molecular pharmacology of cancer. Science 275, 343-349.
84. Will, K., Warnecke, G., Albrechtsen, N., Boulikas, T., and Deppert, W. (1998). High affinity MAR-DNA binding is a common property of murine and human mutant p53. J. Cell. Biochem. 69, 260-270.
85. Wolf, D., Harris, N., and Rotter, V. (1984). Reconstitution of p53 expression in a non-producer Ab-MuLV-transformed cell line by transfection of a functional p53 gene. Cell 38, 119-126.
86. Yin, Y., Tainsky, M.A., Bischoff, F.Z., Strong, L.C., and Wahl, G.M. (1992). Wild-type p53 restores cell cycle control and inhibits gene amplification in cells with mutant p53 alleles. Cell 70, 937-948.