The tumour suppressor gene p53 as a regulator of proliferative life-span and tumour progression

NeuroSignals

Volumn 5, Issue 3, 1996, Pages 139-153

  Wynford Thomas, David ^a   Jones, Christopher J ^a   Wyllie, Fiona S ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Immortalisation; p53; Senescence; Telomeres; Tumour suppressor genes

Indexed keywords

PROTEIN P53; TRANSCRIPTION FACTOR;

ANIMAL CELL; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; DNA DAMAGE; HUMAN; HUMAN CELL; NONHUMAN; REVIEW; SENESCENCE; TELOMERE; TUMOR GROWTH; TUMOR SUPPRESSOR GENE;

CELL AGING; CELL DIVISION; DISEASE PROGRESSION; GENES, P53; HUMANS; NEOPLASMS;

ANIMALIA;

EID: 0029742458     PISSN: 1424862X     EISSN: 14248638     Source Type: Journal    
DOI: 10.1159/000109184     Document Type: Article

References (99)

1. Lane DP, Crawford LV:Tantigen is bound to a host protein in SV40-transfomicd cells. Nature 1979:278: 261-263.
2. Rotter V: p53, a transformation-related cellular-encodcd protein, can be used as a biochemical marker for the detection of primary mouse tumor cells. Proc Nall Acad Sci USA 1983;80:2613-2617.
3. Reich NC, Levine AJ: Growth regulation of a cellular tumour antigen. p53, in nontransformed cells. Nature 1984;308:199-201.
4. Wynford-Thomas D, LaMontagne A, Marin G, Prescott DM: The role of p53 in growth of mouse fibroblast lines. Exp Cell Res 1985; 159:191-200.
5. Williams NW, Wynford-Thomas D: Oncoprotein p53 expression in normal. immortalized and transformed mouse fibroblasts. Exp Cell Res 1989:184:316-328.
6. Eliyahu D, Raz A, Gruss P, Givol D, Oren M: Participation of p53 cellular tumour antigen in transformation of normal embryonic cells. Nature 1984;312:646-654.
7. Parada LF, Land H, Weinberg RA, Wolf D, Rotter V: Cooperation between gene encoding pS3 tumour antigen and ras in cellular transformation. Nature 1984;312:649-651.
8. Jenkins JR, Rudge K, Currie GA: Cellular immortalisation by a cDNA clone encoding the transformation-associated phosphoprotein p53. Nature 1984;312:651-654.
9. Hinds P, Finlay C, Levine AJ: Mutation is required to activate the p53 gene for cooperation with the ras oncogene and transformation. J Virol 1989;63:739-746.
10. Eliyahu D, Michalovitz D, Eliyahu S, Pinhasi-Kimhi O, Oren M: Wild-type p53 can inhibit oncogene-mediated focus formation. Proc Natl AcadSci USA 1989;86:8763-8767.
11. Finlay CA, Hinds PW, Levine AJ: The p53 proto-oncogene can act as a suppressor of transformation. Cell 1989;57:1083-1093.
12. Levine AJ, Momand J, Finlay CA: The p53 tumour suppressor gene. Nature 1991;351:453-456.
13. Baker SJ, Markovitz S, Fcaron ER, Willson JKV, Vogelstein B: Suppression of human colorectal carcinoma cell growth by wild-type p53. Science 1990;249:912-915.
14. Diller L, Kassel J, Nelson CE, Gryka MA, Litwak G, Gebhardt M, Brcs-sac B, Ozturk M, Baker SJ, Vogel-stcin B, Friend SH: p53 functions as a cell cycle control protein in osteosarcomas. Mol Cell Biol 1990; 10: 5772-5781.
15. Grecnblatl MS, Bennett WP, Holl-stein M, Harris CC: Mutations in the p53 tumor suppressor gene: Clues to cancer etiology and molecular pathogenesis. Cancer Res 1994; 54:4855-4878.
16. Vogelstein B, Kinzler KW: The multistep nature of cancer. Trends Genet 1993;9:138-141.
17. Wynford-Thomas D: Molecular genetics of thyroid cancer. Trends Endocrinol Metab 1993;4:224-232.
18. El-Deiry WS, Tokino T, Waldman T, Oliner JD, Velculescu VE, Burrell M, Hill DE, Healy E, Rees JL, Hamilton SR, Kinzler KW, Vogelstein B: Topological control of p21 WAF1/ CIP1 expression in normal and neoplastic tissues. Cancer Res 1995;55: 2910-2919.
19. Land H, Parada LF, Weinberg RA: Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature 1983;304:596-602.
20. Maltzman W, Czyzyk L: UV Irradiation stimulates levels of p53 cellular tumor antigen in nontransformed mouse cells. Mol Cell Biol 1984;4:1689-1694.
21. Kastan MB, Onyekwere O, Sidransky D, Vogelstein B, Craig RW: Participation of p53 protein in the cellular response to DNA damage. Cancer Res 1991;51:6304-6311.
22. Lane DP: p53, guardian of the genome. Nature 1992;358:15-16.
23. Cox LS, Lane DP: Tumour suppressors, kinases and clamps: How p53 regulates the cell cycle in response to DNA damage. Bioessays 1995;17: 501-508.
24. Meek DW: Post-translational modification of p53. Semin Cancer Biol 1994;5:203-210.
25. Milne DM, Palmer RH, Meek DW: Mutation of the casein kinase II phosphorylation site abolishes the anti-proliferative activity of p53. Nucleic Acids Res 1992;20:5565-5570.
26. Hupp TR, Lane DP: Two distinct signalling pathways activate the latent DNA binding function of p53 in a casein kinase II-independent manner. J Biol Chem 1995;270: 18165-18174.
27. Fiscella M, Ullrich SJ, Zambrano N, Shields MT, Lin D, Lees-Miller SP, Anderson CW, Mercer WE, Appella E: Mutation of the serine 15 phosphorylation site of human p53 reduces the ability of p53 to inhibit cell cycle progression. Oncogene 1993;8:1519-1528.
28. Enoch T, Norbury C: Cellular responses to DNA damage: Cell-cycle checkpoints, apoptosis and the roles of p53 and ATM. TIBS 1995;20: 426-430.
29. Chernova OB, Chernov MV, Agaaarwal ML, Taylr WR, Stark GR: The role of p53 in regulating genomic stability when DNA and RNA synthesis are inhibited. TIBS 1995;20:431-434.
30. Jones CJ, Wynford-Thomas D: Is TF11H an activator of the p53-me-diated Gl/S checkpoint? Trends Genet 1995;11:165-166.
31. Di Leonardo A, Linke SP, Clarkin K, Wahl GM: DNA damage triggers a prolonged p53-dependent Gl arrest and long-term induction of Cip 1 in normal human fibroblasts. Genes Dev 1994;8:2540-2551.
32. Hartwell L: Defects in a cell cycle checkpoint may be responsible for the genomic instability of cancer cells. Cell 1992;71:543-546.
33. Caelles C, Helmberg A, Karin M: p53-Depcndent apoptosis in the absence of transcriptional activation of p53-targct genes. Nature 1994;370: 220-223.
34. Cox LS, Hupp T. Midgley CA, Lane DP: A direct effect of activated human p53 on nuclear DNA replication. EMBOJ 1995;14:2099-2105.
35. Donehower LA, Bradley A: The tumor suppressor p53. Biochim Bio-physActa 1993;1155:181-205.
36. El-Deiry WS, Kem SE, Pietenpol JA, Kinzler KW, Vogelstein B: Definition of a consensus binding site for p53. Nature Genet 1992;1:45-49.
37. Sturzbecher H-W, Deppert W: The tumor suppressor protein p53: Relationship of structure to function. Oncol Rep 1994;1:301-307.
38. Thut CJ, Chen J-L, Klemm R, Tjian R: p53 transcriptional activation mediated by coactivators TAFII40 and TAFII60. Science 1995;267: 100-105.
39. Cho Y, Gorina S, Jeffrey PD, Pavle-tich NP: Crystal structure of a p53 tumor suppressor-DNA complex: Understanding tumorigenic mutations. Science 1994;265:346-355.
40. Wcintraub H, Hauschka S, Tapscott SJ: The MCK enhancer contains a p53 responsive element. Proc Natl AcadSci USA 1991;88:4570-4571.
41. El-Deiry WS, Tokino T, Velculescu VE, Trent JM, Lin D, Mercer WE, Kinzler KW, Vogelstein B: WAFKa potential mediator of p53 tumour suppression. Cell 1993;75:817-825.
42. Harper JW, Adami GR, Nan W, Keyomarsi K, Elledge SJ: The p21 Cdk-interacting protein Cipl is a potent inhibitor of Gl cyclin-depen-dent kinases. Cell 1993;75:805-816.
43. Noda A, Ning Y, Venable SF, Percira-Smith OM, Smith JR: Cloning of senescent cell-derived inhibitors of DNA synthesis using an expression screen. Exp Cell Res 1994;211:90-98.
44. Dullie V, Kaufmann WK, Wilson SJ, Tlsty TD, Lees E, Harper JW, Elledge SJ, Reed SI: p53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced Gl arrest. Cell 1994;76:1013-1023.
45. Waga S, Hannon GJ, Beach D, Stillman B: The p21 inhibitor of cyclin-dependent kinases controls DNA replication by interaction with PCNA. Nature 1994;369:574-578.
46. Johnson M, Dimitrov D, Vojta PJ, Barrett JC, Noda A, Pereira-Smith OM, Smith JR: Evidence for a p53-indepcndent pathway for upregulation of SD1 l/ClPl/WAFl/p21 RNA in human cells. Mol Carcinog 1994;11:59-64.
47. Bond JA, Blaydes JP, Rowson J, Haughton MF, Smith JR, Wynford-Thomas D: Mutant p53 rescues human diploid cells from senescence without inhibiting the induction of SD11/WAF1. Cancer Res I995;55: 2404-2409.
48. Nakanishi M, Adami GR, Robetoryc RS, Noda A, Venable SF, Dimitrov D, Pereira-Smith OM, Smith JR: Exit from GO and entry into the cell cycle of cells expressing p21 Sdil antisense RNA. Proc Natl Acad Sci USA 1995;92:4352-4356.
49. Deng C, Zhang P, Harper JW, El-ledge SJ, Leder P: Mice lacking p21 C1PIAVAF1 undergo normal development, but are defective in Gl checkpoint control. Cell 1995;82: 675-684.
50. Wales MM, Biel MA, El-Deiry W, Nelkin BD, Issa J-P, Cavcnce WK, Kuerbitz SJ, Baylin SB: p53 activates expression of HIC-I, a new candidate tumour suppressor gene on 17pl3.3. Nature Med 1995; 1: 570-577.
51. Yin Y, Tainsky MA, Bischoff FZ, Strong LC, Wahl GM: Wild-type p53 restores cel! cycle control and inhibits gene amplification in cells with mutant p53 alleles. Cell 1992; 70:937-948.
52. Nishino H, Knoll A, Bueltner VL, Frisk CS, Maruta Y, Haavik J, Sommer SS: p53 wild-type and p53 nulli-zygous Big Blue transgenic mice have similar frequencies and patterns of observed mutation in liver, spleen and brain. Oncogene 1995; 11:263-270.
53. Havre PA, Yuan J, Hedrick L, Cho KR, Glazer PM: p53 inactivation by HPV16 E6 results in increased mutagenesis in human cells. Cancer Res 1995;55:4420-4424.
54. White AE, Livanos EM, Tlsty TD: Differential disruption of genomic integrity and cell cycle regulation in normal human fibroblasts by the HPV oncoproteins. Genes Dev 1994;8:666-677.
55. Wu X, Levine AJ: p53 and E2F-1 cooperate to mediate apoptosis. Proc Natl Acad Sci USA 1994;91: 3602-3606.
56. Hcrmcking H, Eick D: Mediation of c-Myc-Induccd apoptosis by p53. Science 1994;265:2091-2093.
57. Symonds H, Krall L, Remington L, Saenz-Robles M, Lowe S, Jacks T, Van Dyke T: p53-dependent apoptosis suppresses tumor growth and progression in vivo. Cell 1994;78: 703-711.
58. Sidransky D, Millelsen T, Schwech-heimer K, Rosenblum ML, Cavanec W, Vogelstein B: Clonal expansion of p53 mutant cells is associated with brain tumour progression. Nature 1992;355:846-847.
59. Loeb LA: Microsatcllitc instability: Marker of a mutator phenotype in cancer. Cancer Res 1994;54:5059-5063.
60. Chen Q, Fischer A, Reagan JD, Yan L-J, Ames BN: Oxidative DNA damage and senescence of human diploid fibroblast cells. Proc Natl Acad Sci USA 1995;92:4337-4341.
61. Sanford KK, Price FM, Rhim JS, Stampfer MR, Parshad R: Role of DNA repair in malignant neoplastic transformation of human mammary epithelial cells in culture. Carcinogen 1992;13:1137-1141.
62. Bacchetti S, Counter CM: Telomeres and teiomerase in human cancer. Int J Oncol 1995;7:423-432.
63. Wright WE, Shay JW: Time, telomeres and tumours: Is cellular senescence more than an anticancer mechanism? Trends Cell Biol 1995; 5:293-297.
64. de Lange T: Telomere dynamics and genome instability in human cancer, in Blackbum E, Greider C (eds): Telomeres. Cold Spring Harbor Monographs. New York, Cold Spring Harbor Laboratory Press, in press.
65. Shay JW, Wright WE, Werbin H: Defining the molecular mechanism of human cell immortalisation. Bio-chim Biophys Acta 1991;1072:1-7.
66. Counter CM, Avillion AA, Le-Feuvre CE, Stewart NG, Greider CW, Harley CB, Bacchetti S: Telomere shortening associated with chromosome instability is arrested in immortal cells which express teiomerase activity. EMBO J 1992; 11: 1921-1929.
67. Kim NW, Piatyszck MA, Prowse KR, Harley CB. West MD, Ho PLC, Coviello GM, Wright WE, Weinrich SL, Shay JW: Specific association of human teiomerase activity with immortal cells and cancer. Science 1994;266:2011-2015.
68. Rogan EM, Bryan TM, Hukku B, Maclean K, Chang AC-M, Moy EL, Englezou A, Wamcford SG, Dalla-Pozza L, Reddel RR: Altrations in p53 and pi6ink4 expression and telomere length during spontaneous immortalization of Li-Fraumeni syndrome fibroblasts. Mol Cell Biol 1995;15:4745-4753.
69. Klingelhutz AJ, Barber SA, Smith PP, Dyer K, McDougall JK: Restoration of telomeres in human papillomavirus-immortalized human anogenital epithelial cells. Mol Cell Biol 1994;14:961-969.
70. Wynford-Thomas D: Docs telomere shortening drive selection for p53 mutation in human cancer? Mol Carcinog 1995;12:119-123.
71. Wright WE, Pereira-Smith OM, Shay JW: Reversible cellular senescence: Implications for immortalisation of normal human diploid fibroblasts. Mol Cell Biol 1989;9:3088-3092.
72. Shay JW, Van der Haegen BA, Ying Y, Wright WE: The frequency of immortalization of human fibroblasts and mammary epithelial cells transfected with SV40 large T-antigen. Exp Cell Res 1993;209:45-52.
73. Harley CB, Futcher AB, Greider CW: Telomeres shorten during ageing of human Fibroblasts. Nature 1990;345:458-460.
74. Allsopp RC, Chang E, Kashefi-Aazam M, Rogaev EI, Piatyszek MA, Shay JW, Harley CB: Telomere shortening is associated with cell division in vitro and in vivo. Exp Cell Res 1995;220:194-200.
75. Allsopp RC, Vaziri H, Patterson C, Goldstein S, Younglai EV, Futcher AB, Greider CW, Harley CB: Telomere length predicts replicative capacity of human fibroblasts. Proc Natl Acad Sci USA 1992;89:10114-10118.
76. Allsopp RC, Harley CB: Evidence for a critical telomere length in senescent human fibroblasts. Exp Cell Res 1995;219:130-136.
77. Benn PA: Specific chromosome aberrations in senescent fibroblast cell lines derived from human embryos. Am J Hum Genet 1976;28: 465-473.
78. Shay JW, Pereira-Smith OM, Wright WE: A role for both RB and p53 in the regulation of human cellular senescence. Exp Cell Res 1991; 196:33-39.
79. Shay JW, Wright WE, Brasiskyte D, Van der Hagen BA: E6 of human papillomavirus type 16 can overcome the Ml stage of immortalisation in human mammary epithelial cells but not human fibroblasts. Oncogene 1993;8:1407-1413.
80. Hara E, Tsurui H, Shinozaki A, Na-kada S, Oda K: Cooperative effect ofantisense-Rb and antisense-p53 oligomers on the extension of life span in human diploid fibroblasts, TIG-1. Biochem Biophys Res Communal; 179:528-534.
81. Bond JA, Wyllie FS, Wynford-Thomas D: Escape from senescence in human diploid fibroblasts induced directly by mutant p53. Oncogene 1994;9:1885-1889.
82. Kulju KS, Lehman JM: Increased p53 protein associated with aging in human diploid fibroblasts. Exp Cell Res 1995;217:336-345.
83. Afshari CA, Vojta PJ, Annab LA, Futreal PA, Willard TB, Barrett JC: Investigation of the role of G 1/S cell cycle mediators in cellular senescence. Exp Cell Res 1993;209:231-237.
84. Atadja P, Wong H, Garkavtsev I, Geillette C, Riabowol K: Increased activity of p53 in senescing fibroblasts. Proc Natl Acad Sci USA 1995;92:8348-8352.
85. Hupp TR, Sparks A, Lane DP: Small peptides activate the latent sequence-specific DNA binding function of p53. Cell 1995;83:237-245.
86. Vojta PJ, Carl Barrett J: Genetic analysis of cellular senescence. Bio-chim Biophys Acta 1995; 1242:29-41.
87. Parker SB, Eichele G, Zhang P. Rawls A, Sands AT, Bradley A, Olson EN, Harper JW, Elledge SJ: p53 independent expression ofp21 Cipl in muscle and other terminally differentiating cells. Science 1995;267: 1024-1027.
88. Band V, De Caprio JA, Delmolino L, Kulesa V, Sager R: Loss of p53 protein in human papillomavirus type 16 E6-immortalised human mammary epithelial cells. J Virol 1991;65:6671-6676.
89. Shay JW, Tomlinson G, Piatyszek MA, Gollahon LS: Spontaneous in vitro immortalization of breast epithelial cells from a patient with Li-Fraumeni syndrome. Mol Cell Biol 1995;15:425-432.
90. Halbert CL, Demers GW, Galloway DA: The E7 gene of human papillomavirus type 16 is sufficient for immortalization of human epithelial cells. J Virol 1991;65:473-478.
91. Demers GW, Halbert CL, Galloway DA: Elevated wild-type p53 protein levels in human epithelial cell lines immortalized by the human papillomavirus type 16 E7 gene. Virology 1994;198:169-174.
92. Wyllie F, Lemoine N, Barton C, Dawson T, Bond J, Wynford-Thomas D: Direct growth stimulation of normal human epithelial cells by mutant p53. Mol Carcinog 1993;7: 83-88.
93. Wazer DE, Liu X-L, Chu Q, Gao Q, Band V: Immortalization of distinct human mammary epithelial cell types by human papilloma virus 16 E6 or E7. Proc Natl Acad Sci USA 1995;92:3687-3691.
94. Van der Haegen BA, Shay JW: Immortalization of human mammary epithelial cells by SV40 large T-anti-gen involves a two step mechanism. In Vitro Cell Dev Biol 1993;29A: 180-182.
95. Bond JA, Wyllie FS, Ivan M, Dawson T, Wynford-Thomas D: A variant epithelial subpopulation in normal thyroid with high proliferative capacity in vitro. Mol Cell Endocrinol 1993;93:175-183.
96. Reznikoff CA, Belair C, Savelieva E, et al: Long-term genome stability and minimal genotypic and phenotypic alterations in HPV16 E7-, but not E6-, immortalized human uro-cpithelial cells. Genes Dev 1994;8: 2227-2240.
97. Williams DW, Williams ED: The pathology of follicular thyroid epithelial tumours; in Wynford-Thomas D, Williams ED (eds): Thyroid Tumours: Molecular Basis of Pathogenesis. Edingburgh, Churchill Livingstone, 1989, pp 57-65.
98. Hicks GG, Egan SE, Greenberg AH, Mowat M: Mutant p53 tumor suppressor alleles release ras-induccd cell cycle growth arrest. Mol Cell Biol 1991;11:1344-1352.
99. Denko NC, Giaccia AJ, Stringer JR, Stambrook PJ: The human Ha-ras oncogene induces genomic instability in murine fibroblasts within one cell cycle. Proc Natl Acad Sci USA 1994;91:5124-5128.