The p53 tumour suppressor gene: A mediator of a G1 growth arrest and of apoptosis

Experientia

Volumn 52, Issue 10-11, 1996, Pages 1001-1007

  Yonish Rouach, Elisheva ^a  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

Author keywords

Apoptosis; G1 arrest; p53; Tumour suppression

Indexed keywords

PROTEIN P53;

APOPTOSIS; CELL CYCLE; CELL CYCLE G1 PHASE; DNA DAMAGE; GENOTOXICITY; GROWTH DISORDER; HUMAN; HUMAN CELL; IRRADIATION; REVIEW; SIGNAL TRANSDUCTION; TRANSACTIVATION; TUMOR SUPPRESSOR GENE;

ANIMALS; APOPTOSIS; CELL CYCLE; G1 PHASE; GENES, P53; HUMANS; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0029862307     PISSN: 00144754     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF01920109     Document Type: Review

References (73)

1. Williams B. O., Remington L., Albert D. M., Mukai S., Bronson R. T. and Jacks T. (1994) Cooperative tumorigenic effects of germline mutations in Rb and p53. Nature Genet. 7: 480-484
2. Harvey M., Vogel H., Moris D., Bradeley A., Bernstein A. and Donehower L. A. (1995) A mutant p53 transgene accelerates tumour development in heterozygous but not nullizygous p53-deficient mice. Nature Genet. 9: 305-311
3. Donehower L. A and Bradley A. (1993) The tumor suppressor p53. Biochim. Biophys. Acta 1155: 181-205
4. Farmer G., Bargonetti J., Zhu H., Friedman P., Prywes R. and Prives C. (1992) Wild-type p53 activates transcription in vitro. Nature 358: 83-86
5. 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 Genetics 1: 45-49
6. Kern S. E., Kinzler K. W., Bruskin A., Jarosz D., Friedman P., Prives C. and Vogelstein B. (1991) Identification of p53 as a sequence-specific DNA binding protein. Science 252: 1708-1711
7. 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
8. Pavletich N. P., Chambers K. A. and Pabo C. O. (1993) The DNA-binding domain of p53 contains the four conserved regions and the major mutation hot spots. Genes Dev 7: 2556-2564
9. Bargonetti J., Manfredi J. J., Chen X., Marshak D. R. and Prives C. A. (1993) Proteolytic fragment from the central region of p53 has marked sequence-specific DNA-binding activity when generated from wild-type but not from oncogenic mutant p53 protein. Genes Dev. 7: 2565-2574
10. Wang Y., Reed M., Wang P., Stenger J. E., Mayr G., Anderson M. E., Schweded J. F. and Tegtmeyer P. (1993) p53 domains: identification and characterization of two autonomous DNA-binding regions. Genes Dev. 7: 2575-2586
11. Cho Y., Gorina S., Jeffrey P. D. and Pavletich N. P. (1994) Crystal structure of a p53 tumour suppressor-DNA complex: understanding tumourigenic mutations. Science 265: 346-355
12. Raycroft L., Wu H. and Lozano G. (1990) Transcriptional activation by wild-type but not transforming mutants of the p53 anti-oncogene. Science 249: 1049-1051
13. Unger T., Nau M. M., Segal S. and Minna J. D. (1992) p53: a trans-dominant regulator of transcription whose function is ablated by mutations occurring in human cancer EMBO J. 11: 1383-1390
14. Stürzbecher H.-W., Brain R., Addison C., Rudge K., Remm M., Grimaldi M., Keenan E. and Jenkins J. R. (1992) A C-terminal x-helix plus basic region is the major structural determinant of p53 tetramerization. Oncogene 71: 513-1523
15. Shaulian E., Zauberman A., Milner J., Davies E. A. and Oren M. (1993) Tight DNA binding and oligomerization are dispensable for the ability of p53 to transactivate target genes and suppress transformation. EMBO J. 12: 2789-2797
16. Tarunina M. and Jenkins J. R. (1993) Human p53 binds DNA as a protein homodimer but monomeric variants retain full transcription transactivation activity. Oncogene 8: 3165-3173
17. Wu L., Bayle J. H., Elenbaas B., Pavletich N. P. and Levine A. J. (1995) Alternatively spliced forms in the carboxy-terminal domain of the p53 protein regulate its ability to promote annealing of complementary single strands of nucleic acids. Mol Cell. Biol. 15: 497-504
18. Lee S., Elenbaas B., Levine A. and Griffith J. (1995) p53 and its 14 kDa C-terminal domain recognize primary DNA damage in the form of insertion/deletion mismatches. Cell 81: 1013-1020
19. Hupp T. R., Meek D. W., Midgley C. A. and Lane D. P. (1993) Activation of the cryptic DNA binding function of mutant forms of p53. Nucl. Acids Res. 21: 3167-3174
20. Kulesz-Martin M. F., Lisafeld B., Huang H., Kisiel N. D. and Lee L. (1994) Endogenous p53 protein generated from wild-type alternatively spliced p53 RNA in mouse epidermal cells. Mol. Cell. Biol. 14: 1698-708
21. Pietenpol J. A. and Vogelstein B. (1993) No room at the p53 inn. Nature 365: 17-18
22. Ginsberg D., Mechta F., Yaniv M. and Oren M. (1991) Wild-type p53 can down-modulate the activity of various promoters. Proc. Natl Acad. Sci. USA 88: 9979-9983
23. Subler M. A., Martin D. W. and Deb S. (1992) Inhibition of viral and cellular promoters by human wild-type p53. J Virol. 66: 4757-4762
24. Mack D. H., Vartikar J., Pipas J. M. and Laimins L. A. (1993) Specific repression of TATA-mediated but not initiator-mediated transcription by wild type p53. Nature 363: 281-283
25. Liu X., Miller C. W., Koeffler P. H. and Berk A. J. (1993) The p53 activation domain binds the TATA box-binding polypeptide in Holo-TFIID. and a neighboring p53 domain inhibits transcription. Mol. Cell. Biol. 13: 3291-3300
26. Ragimov N., Krauskopf A., Navot N., Rotter V., Oren M. and Aloni Y. (1993) Wild-type but not mutant p53 can repress transcription initiation in vitro by interfering with the binding of basal transcription factors to the TATA motif. Oncogene 8: 1183-1193
27. Kastan M. B., Onyekwere O., Sidransky D., Vogelstein B. and Craig R. W. (1991) Participation of p53 protein in the cellular response to DNA damage. Cancer Res. 51: 6304-6311
28. Kuerbitz S. J., Plunkett B. S., Walsh W. V. and Kastan M. B. (1992) Wild-type p53 is a cell cycle checkpoint determinant following irradiation. Proc. Natl Acad. Sci. USA 89: 7491-7495
29. 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
30. Lu X. and Lane D. P. (1993) Differential induction of transcriptionally active p53 following UV or ionizing radiation: defects in chromosome instability syndromes? Cell 75: 765-778
31. Zhan Q., Carrier F. and Forance A. J. (1993) Induction of cellular p53 activity by DNA-damaging agents and growth arrest. Mol. Cell. Biol. 13: 4242-4250
32. 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. (1992) A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxia-telangiectasia. Cell 71: 587-597
33. Maltzman W. and Czyzyk L. (1984) UV irradiation stimulates levels of p53 cellular tumour antigen in nontransformed mouse cells. Mol. Cell. Biol. 4: 1689-1694
34. Sun X., Shimizu H. and Yamamoto K. (1995) Identification of a novel p53 promoter element involved in genotoxic stress-inducible p53 gene expression. Mol. Cell. Biol. 15: 4489- 4496
35. Aloni-Grinstein R., Schwartz D. and Rotter V. (1995) Accumulation of wild-type p53 protein upon γ-irradiation induces a G2 arrest-dependent immunoglobulin κ light chain gene expression. EMBO J. 14: 1393-1401
36. Atadja P., Wong I., Garkavtsev H., Veillette C. and Riabowol K. (1995) Increased activity of p53 in senescing fibroblasts. Proc. Natl Acad. Sci. USA 92: 8348-8352
37. Dameron K. M., Volpert O. V., Tainsky M. A. and Bouck N. (1994) Control of angiogenesis in fibroblasts by p53 reglation of thrombospondin-l. Science 265: 1582-1584
38. Diller L., Kassel J., Nelson C. E., Gryka M. A., Litwak G., Gebhardt M., Bressac B., Ozturk M., Baker S. J., Vogelstein B. and Friend S. H. (1990) p53 functions as a cell cycle control protein in osteosarcomas. Mol. Cell. Biol. 10: 5772-5781
39. Mercer W. E., Shields M. T., Amin M., Sauve M. G. J., Apella E., Romano J. W. and Ullrich S. J. (1990) Negative growth regulation in a glioblastoma tumor cell line that conditionally expresses human wild-type p53. Proc. Natl Acad. Sci. USA 87: 6166-6170
40. Smith M. L., Chen I.-T., Zhan Q., Bae I., Chen C.-Y., Glimer T. M., Kastan M. B., O'Conner P. M. and Forance A. J. (1995) Interaction of the p53-rcgulated protein Gadd45 with proliferating cell nuclear antigen. Science 266: 1376-1380
41. Kearsey J. M., Coates P. J., Prescott A. R., Warbrick E. and Hall P. A. (1995) Gadd45 is a nuclear cell cycle regulated protein which interacts with p21Cip1. Oncogene 11: 1675-1683
42. Chen I. T., Smith M. L., O'Connor P. M. and Fornace A. J. (1995) Direct interaction of Gadd45 with PCNA and evidence for competitive interaction of Gadd45 and p21Waf1/Cip1 with PCNA. Oncogene 11: 1931-1937
43. Okamoto K. and Beach D. (1994) Cyclin G is a transcriptional target of the p53 tumor suppressor protein. EMBO J. 13: 4816-4822
44. Zauberman A., Lupo A. and Oren M. (1995) Identification of p53 target genes through immune selection of genomic DNA: the cyclin G gene contains two distinct p53 binding sites. Oncogene 10: 2361-2366
45. Barak Y., Juven T., Haffner R. and Oren M. (1993) mdm-2 expression is induced by wild-type p53 activity EMBO J. 12: 461-468
46. Chen C. Y., Oliner J. D., Zhan Q., Forance A. J., Vogelstein B. and Kastan M. B. (1994) Interactions between p53 and MDM2 in a mammalian cell cycle checkpoint pathway. Proc. Natl Acad. Sci. USA 91: 2684-2688
47. Caelles C., Helmberg A. and Karin M. (1994) p53-dependent apoptosis in the absence of transcriptional activation of p53-target genes. Nature 370: 220-223
48. waf1/cip1. Genes Dev. 8: 2817-2830
49. Haupt Y., Rowan, S., Shaulian K., Vousden K. H. and Oren M. (1995) Induction of apoptosis in HeLa cells by trans-activation deficient p53. Genes Dev. 9: 2170-2183
50. Sabbatini P., Lin J., Levine A. J. and White E. (1995) Essential role for p53-mediated transcription in E1A-induced apoptosis. Genes Dev. 9: 2184-2192.
51. Oltvai Z., Milliman C. and Korsmeyer S. J. (1993) Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74: 609-619
52. Selvakumaran M., Lin H. K., Miyashita T., Wang H. G., Krajewski S., Reed J. C., Huffman B. and Liebermann D. (1994) Immediate early up-regulation of bax expression by p53 but not TGF-beta 1: a paradigm for distinct apoptotic pathways. Oncogene 9: 1791-1798
53. Zhan Q., Fan S., Bae, I. Guillouf C., Liebermann D. A., O'Connor P. M. and Forance A. J. Jr. (1994) Induction of bax by genotoxic stress in human cells correlates with normal p53 status and apoptosis. Oncogene 9: 3743-3751
54. Miyashita T. and Reed J. C. (1995) Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80: 293-299
55. 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
56. Knudson C., Tunk K., Tourtellotte W., Brown G. and Korsmeyer S. (1995) Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270: 96-99
57. Miyashita T., Krajewski S., Krajewska M., Wang H. G., Lin H. K., Huffman B., Lieberman D. and Reed J. C. (1994) tumour suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene 9: 1799-1805
58. Hadlar S., Negrini M., Monne M., Sabbioni S. and Croce C. M. (1994) Down regulation of bcl-2 by p53 in breast cancer cells. Cancer Res. 54: 2095-2097
59. Nagata S. and Golstein P. (1995) The Fas death factor. Science 267:1449-1456
60. Owen-Schaub L. B., Zhang W., Cusack J. C., Angelo L. S., Santee S. M., Fujiwara T., Roth J. A., Deiseroth A. B., Zhang W.-W., Kruzel E. and Radinsky R. (1995) Wild-type human p53 and a temperature-sensitive mutant induce Fas/APO-1 expression. Mol. Cell Biol. 15: 3032-3040
61. Morimoto H., Yonehara S. and Bonavida B. (1993) Overcoming tumor necrosis factor and drug resistance of human tumor cell lines by combination treatment with anti-Fas antibody and drugs and toxins. Cancer Res. 53: 2591-2596
62. Di Leonardo A., Linke S. P., Clarkin K. and Wahl G. M. (1994) DNA damage triggers a prolonged p53-dependent G1 arrest and long-term induction of Cip1 in normal human fibroblasts. Genes Dev. 8: 2540-2551
63. Lowe S. W., Ruley H. E., Jacks T. and Huosman D. E. (1993) p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell 74: 957-967
64. Demers G. W., Foster S. A., Halbert C. L. and Galloway D. A. (1994) Growth arrest by induction of p53 in DNA damaged keratinocytes is bypassed by human papillomavirus 16 E7. Proc. Natl Acad. Sci. USA 91: 4382-4386
65. Slebos R. J, Lee M. H., Plunkett B. S., Kessis T. D., Williams B. O., Jacks T., Hedrick L., Kastan M. B. and Cho K. R. (1994) p53-dependent G1 arrest involves pRB-related proteins and is disrupted by the human papillomavirus 16 E7 oncoprotein. Proc. Natl Acad. Sci. USA 91: 5320-5324
66. Hickman E. S., Picksley S. M. and Vousden K. H. (1994) Cells expressing HPV16 E7 continue cell cycle progression following DNA damage induced p53 activation. Oncogene 9: 2177-2181
67. White A. E., Livanos E. M. and Tlsty T. D. (1994) Differential disruption of genomic integrity and cell cycle regulation in normal human fibroblasts by the HPV oncoproteins. Genes Dev. 8: 666-677
68. Qin X. Q., Livingston D. M., Kaelin W. G. and Adams P. D. (1994) Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc. Natl Acad. Sci. USA 91: 10918-10922
69. Almasan A., Yin Y., Kelly R. E., Lee E. Y., Bradley A., Li W., Bertino J. R. and Wahl G. M. (1995) Deficiency of retinoblastoma protein leads to inappropriate S-phase entry, activation of E2F-responsive genes and apoptosis. Proc. Natl Acad. Sci. USA 92: 5436-5440
70. Shan B. and Lee W. H. (1994) Deregulated expression of E2F-1 induces S-phase entry and leads to apoptosis. Mol. Cell. Biol. 14: 8166-8173
71. Logan T. J., Evans D. L., Mercer W. E., Bjornsti M. A. and Hall D. J. (1995) Expression of a deletion mutant of the E2F1 transcription factor in fibroblasts lengthens S phase and increases sensitivity to S phase-specific toxins. Cancer Res. 55: 2883-2891
72. Howes K. A., Ransom L. N., Papermaster D. S., Lasudry J. G. H., Albert D. M. and Windle J. J. (1994) Analysis or retinoblastoma: alternative fates of photoreceptors expressing the HPV-16 E7 gene in the presence or absence of p53. Genes Dev. 8: 1300-1310
73. Pan H. and Griep A. E. (1994) Altered cell cycle regulation in the lens of HPV-16 E6 or E7 transgenic mice: implications for tumour suppressor gene function in development. Genes Dev. 8: 1285-1299