Covalent and noncovalent modifiers of the p53 protein

Cellular and Molecular Life Sciences

Volumn 55, Issue 1, 1999, Pages 76-87

  Jayaraman, L ^a,b   Prives, C ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

C terminus; DNA bending; DNA binding; Modification; N terminus; Phosphorylation; Redox; Signalling; Stabilization

Indexed keywords

PROTEIN P53;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; DNA BINDING; HUMAN; PROTEIN METABOLISM; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE;

DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; NUCLEAR PROTEINS; NUCLEIC ACID CONFORMATION; OXIDATION-REDUCTION; PHOSPHORYLATION; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-MDM2; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0033027346     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s000180050271     Document Type: Review

References (133)

1. 1 Ko L. and Prives C. (1996) p53: puzzle and paradigm. Genes Dev. 10: 1054-1072
2. 2 Gottlieb M. T. and Oren M. (1996) p53 in growth control and neoplasia. Biochim. Biophys. Acta 1287: 77-102
3. 3 Levine A. J. (1997) p53, the cellular gatekeeper for growth and division. Cell 88: 323-331
4. 4 Unger T., Mietz J. A., Scheffner M., Yee C. L. and Howley P. M. (1993) Functional domains of wild-type and mutant p53 proteins involved in transcriptional regulation, transdominant inhibition and transformation suppression. Mol. Cell. Biol. 13: 5186-5194
5. 5 Chang J., Kim D.-H., Lee S. W., Choi K. Y. and Sung Y. C. (1995) Transactivation ability of p53 transcriptional activation domain is directly related to the binding affinity to TATA-binding protein. J. Biol. Chem. 270: 25014-25019
6. 6 Candau R, Scolnick D. M., Darpino P., Ying C. Y., Halazonetis T. D. and Berger S. L. (1997) Two tandem and independent sub-activation domains in the amino terminus of p53 require the adaptor complex for activity. Oncogene 15: 807-816
7. 7 Walker K. K. and Levine A. J. (1996) Identification of a novel p53 functional domain that is necessary for efficient growth suppression. Proc. Natl. Acad. Sci. USA 93: 15335-15340
8. 8 Ruaro E. M., Collavin L., Del Sal G., Haffner R., Oren M., Levine A. J. et al. (1997) A proline-rich motif in p53 is required for transactivation-independent growth arrest as induced by Gasl. Proc. Natl. Acad. Sci. USA 94: 4675-4680
9. 9 Sakamuro D., Sabbatini P., White E. and Prendergast G. C. (1997) The polyproline region of p53 is required to activate apoptosis but not growth arrest. Oncogene 15: 887-898
10. 10 Meek D. (1994) Post-translational modification of p53. Sem. Cancer Biol. 5: 203-207
11. 11 Ko L. J., Chen X., Shieh S.-Y., Jayaraman L., Tamai K., Taya Y. et al. (1997) p53 is phosphorylated by CDK7/cyclin H in a p36/MAT1 dependent manner. Mol. Cell. Biol. 17: 7220-7229
12. 12 Milne D. M., Campbell L. E., Campbell D. G. and Meek D. W. (1995) p53 is phosphorylated in vitro and in vivo by an ultraviolet radiation-induced protein kinase characteristic of the c-Jun kinase, JNK1. J. Biol. Chem. 270: 5511-5518
13. 13 Adler V., Pincus M. R., Minamoto T., Fuchs S. Y., Bluth M. J., Brandt-Rauf P. W. et al. (1997) Conformation-dependent phosphorylation of p53. Proc. Natl. Acad. Sci. USA 94, 1686-1691
14. 14 Milne D. M., Campbell D. G., Caudwell F. B. and Meek D. W. (1994) Phosphorylation of the tumour suppressor protein p53 by mitogen-activated protein kinases. J. Biol. Chem. 269: 9253-9260
15. 15 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
16. 16 Siliciano J. D., Canman C. E., Taya Y., Sakaguchi K., Appella E. and Kastan M. B. (1997) DNA damage induces phosphorylation of the amino terminus of p53. Genes Dev. 11: 3471-3481
17. 17 Chen J., Marechal V. and Levine A. J. (1993) Mapping of the p53 and mdm-2 interaction domains. Mol. Cell. Biol. 13: 4107-4114
18. 18 Oliner J. D., Pietenpol J. A., Thiagalingam S., Gyuris J., Kinzler K. W. and Vogelstein B. (1993) Oncoprotein MDM2 conceals the activation domain of tumour suppressor p53. Nature 362: 857-860
19. 19 Picksley S. M., Vojtesek B., Sparks A. and Lane D. P. (1994) Immunochemical analysis of the interaction of p53 with MDM2; fine mapping of the MDM2 binding site on p53 using synthetic peptides. Oncogene 9: 2523-2529
20. 20 Kussie P. H., Gorina S., Marechal V., Elenbaas B., Moreau J., Levine A. J. et al. (1996) Structure of the MDM2 onco-protein bound to the p53 tumour suppressor transactivation domain. Science 274: 948-953
21. 21 Lane D. P. and Hall P. A. (1997) MDM2-arbiter of p53's destruction. Trends Biochem. Sci. 22: 372-374
22. 22 de Oca Luna R. M., Wagner D. S. and Lozano G. (1995) Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53. Nature 378: 203-206
23. 23 Jones S. N., Roe A. E., Donehower L. A. and Bradley A. (1995) Rescue of embryonic lethality in Mdm2-deficient mice by absence of p53. Nature 378: 206-208
24. 24 Haupt Y., Maya R., Kazaz A. and Oren M. (1997) Mdm2 promotes the rapid degradation of p53. Nature 387: 296-299
25. 25 Kubbutat M. H. G., Jones S. N. and Vousden K. H. (1997) Regulation of p53 stability by Mdm2. Nature 387: 299-303
26. 26 Bottger A., Bottger V., Sparks A., Liu W. L., Howard S. F. and Lane D. P. (1997) Design of a synthetic Mdm2-binding mini protein that activates the p53 response in vivo. Curr. Biol. 7: 860-869
27. 27 Honda R., Tanaka H. and Yasuda H. (1997) Oncoprotein MDM2 is a ubiquitin ligase E3 for tumour suppressor p53. FEBS Lett. 420: 25-27
28. 28 Gu W., Shi X. L. and Roeder R. G. (1997) Synergistic activation of transcription by CBP and p53. Nature 387: 819-823
29. 29 Lill N. L., Grossman S. R., Ginsberg D., DeCaprio J. and Livingston D. M. (1997) Binding and modulation of p53 by p300/CBP coactivators. Nature 387: 823-827
30. 30 Avantaggiati M. L., Ogryzko V., Gardner K., Giordano A., Levine A. S. and Kelly K. (1997) Recruitment of p300/CBP in p53-dependent signal pathways. Cell 89: 1175-1184
31. 31 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
32. 32 Wu X., Bayle J. H., Olson D. and Levine A. J. (1993) The p53-mdm-2 autoregulatory feedback loop. Genes Dev. 7: 1126-1132
33. 33 Barak Y., Juven T., Haffner R. and Oren M. (1993) mdm2 expression is induced by wild type p53 activity. EMBO J. 12: 461-468
34. 34 Thut C. J., Goodrich J. A. and Tjian R. (1997) Repression of p53-mediated transcription by MDM2: a dual mechanism. Genes Dev. 11: 1974-1986
35. 35 Zauberman A., Barak Y., Ragimov N., Levy N. and Oren M. (1993) Sequence-specific DNA binding by p53: identification of target sites and lack of binding to p53-MDM2 complexes. EMBO J. 12: 2799-2808
36. 36 Bottger A., Bottger V., Garcia-Echeverria C., Chene P., Hochkeppel H. K., Sampson W. et al. (1997) Molecular characterization of the hdm2-p53 interaction. J. Mol. Biol. 269: 744-756
37. 37 Dutta A., Ruppert J. M., Aster J. C. and Winchester E. (1993) Inhibition of DNA replication factor RPA by p53. Nature 365: 79-82
38. 38 Miller S. D., Moses K., Jayaraman L. and Prives C. (1997) Complex formation between p53 and RP-A inhibits the sequence specific DNA binding of p53 and is regulated by single stranded DNA. Mol. Cell. Biol. 17: 2194-2201
39. 39 Chen X., Zhu H., Farmer G., Prywes R. and Prives C. (1993) p53 and TATA binding protein cooperate to bind to DNA. Genes Dev. 7: 1837-1849
40. 40 Martin M. E. and Berk A. J. (1998) Adenovirus E1B 55K represses p53 activation in vitro. J. Virol. 72: 3146-3154
41. 41 Hansen S., Hupp T. R. and Lane D. P. (1996) Allosteric regulation of the thermosensitivity and DNA binding activity of human p53 by specific interacting proteins. J. Biol. Chem. 271: 3917-3924
42. 42 Friedlander P., Legros Y., Soussi T. and Prives C. (1996) Regulation of mutant p53 temperature sensitive DNA binding. J. Biol. Chem. 271: 25468-25478
43. 43 Knippschild U., Milne D. M., Campbell L. E., DeMaggio A. J., Christenson E., Hoekstra M. F. et al. (1997) p53 is phosphorylated in vitro and in vivo by the delta and epsilon isoforms of casein kinase 1 and enhances the level of casein kinase 1 delta in response to topoisomerase-directed drugs. Oncogene 15: 1727-1736
44. 44 Pomerantz J., Schreiber-Agus N., Liegeois N. J., Silverman A., Alland L., Chin L. et al. (1998) The Ink4a tumour suppressor gene product. p19Arf, interacts with MDM2 and neutralizes MDM2's inhibition of p53. Cell 92: 713-723
45. 45 Zhang Y., Xiong Y. and Yarbrough W. (1998) GARF promotes MDM2 degradation and stabilizes p53: ARF-INK4a locus deletion impairs both the Rb and p53 tumour suppression pathways. Cell 92: 725-734
46. 46 Soussi T. and May P. (1996) Structural aspects of the p53 protein in relation to gene evolution: a second look. J. Mol. Biol. 260: 623-637
47. 47 Hainaut P., Soussi T., Shomer B., Hollstein M., Greenblatt M., Hovig E. et al. (1997) Database of p53 gene somatic mutations in human tumours and cell lines: updated compilation and future prospects. Nucleic Acids Res. 25: 151-157
48. 48 Vogelstein B. and Kinzler K. W. (1992) p53 function and disfunction. Cell 70: 5236-5238
49. 49 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
50. 50 Wang Y., Schwedes J. F., Parks D., Mann K. and Tegtmeyer P. (1995) Interaction of p53 with its consensus DNA-binding site. Mol. Cell. Biol. 15: 2157-2165
51. 51 Balagurumoorthy P., Sakamoto H., Lewis M. S., Zambrano N., Clore G. M., Gronenborn A. M. et al. (1995) Four p53 DNA binding domain peptides bind natural p53 response elements and bend the DNA. Proc. Natl. Acad. Sci. USA 92: 8591-8595
52. 52 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
53. 53 Jayaraman L., Freulich E. and Prives C. (1997) Functional dissection of the p53 tumour suppressor protein. Methods Enzymol. 283: 245-256
54. 54 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
55. 55 Wang Y., Reed M., Wang P., Stenger J. E., Mayr G., Anderson M. E. et al. (1993) p53 domains: identification and characterization of two autonomous DNA-binding regions. Genes Dev. 7: 2575-2586
56. 56 Sun Y. and Oberley L. W. (1996) Redox regulation of transcriptional activators. Free Radical Biol. Med. 21: 335-348
57. 57 Hainaut P. and Milner J. (1992) Interaction of heat-shock protein 70 with p53 translated in vitro: evidence for interaction with dimeric p53 and for a role in the regulation of p53 conformation. EMBO J. 10: 3513-3520
58. 58 Hainaut P. and Milner J. (1993) Redox modulation of p53 conformation and sequence-specific DNA binding in vitro. Cancer Res. 53: 4469-4473
59. 59 Hainaut P., Rolley N., Davies M. and Milner J. (1995) Modulation by copper of p53 conformation and sequence specific DNA binding: Role for Cu(II) Cu(I) redox mechanism. Oncogene 10: 27-32
60. 60 Bullock A. N., Henckel J., DeDecker B. S., Johnson C. M., Nikolova P. V., Proctor M. R. et al. (1997) Thermodynamic stability of wild-type and mutant p53 core domain. Proc. Natl. Acad. Sci. USA 94: 14338-14342
61. 61 Verhaegh G. W., Richard M. J. and Hainaut P. (1997) Regulation of p53 by metal ions and by antioxidants: dithiocarbamate down-regulates p53 DNA-binding activity by increasing the intracellular level of copper. Mol. Cell. Biol. 17: 5699-5706
62. 62 Hupp T. R., Meek C. A., Midgley C. A. and Lane D. P. (1993) Activation of the cryptic DNA binding function of mutant forms of p53. Nucleic Acids Res. 21: 3167-3174
63. 63 Delphin C., Cahen P., Lawrence J. J. and Baudier J. (1994) Characterization of baculovirus recombinant wild-type p53. Dimerization of p53 is required for high-affinity DNA binding and cysteine oxidation inhibits p53 DNA binding. Eur. J. Biochem. 223: 683-692
64. 64 Rainwater R., Parks D., Anderson M. E., Tegtmeyer P. and Mann K. (1995) Role of cysteine residues in regulation of p53 function. Mol. Cell. Biol. 15: 3892-3903
65. 65 Jayaraman L., Murthy K. G. K., Curran T., Xanthoudakis S. and Prives C. (1997) Identification of redox/repair protein Ref-1 as an activator of p53. Genes Dev. 11: 558-570
66. 66 Casso D. and Beach D. A. (1996) Mutation in a thioredoxin reductase homolog suppresses p53-induced growth inhibition in the fission yeast Schizosaccharomyces pombe. Mol. Gen. Genet. 252: 518-529
67. 67 Pearson G. D. and Merrill G. F. (1998) Deletion of the Saccharomyces cerevisiae TRR1 gene encoding thioredoxin reductase inhibits p53-dependent reporter gene expression. J. Biol. Chem. 273: 5431-5434
68. 68 Meira L. B., Cheo D. L., Hammer R. E., Burns D. K., Reis A. and Friedberg E. C. (1997) Genetic interaction between HAPI/REF-1 and p53. Nature Genet. 17: 145
69. 69 Graeber T. G., Osmanian C., Jacks T., Housman D. E., Koch C. J., Lowe S. W. et al. (1996) Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 379: 88-91
70. 70 Yao K.-S., Xanthoudakis S., Curran T. and O'Dwyer P. J. (1994) Activation of AP-1 and of a nuclear redox factor, Ref-1, in the response of HT29 colon cancer cells to hypoxia. Mol. Cell. Biol. 14: 5997-6003
71. 70a Yin Y., Terauchi Y., Solomon G. G., Aizawa S., Rangarajan P. N., Yazaki Y. et al. (1998) Involvement of p85 in p53-dependent response to oxidative stress. Nature 391: 707-710
72. 71 Nagaich A. K., Zhurkin V. B., Sakamoto H., Gorin A. A., Clore G. M., Gronenborn A. M. et al. (1997) Architectural accommodation in the complex of four p53 DNA binding domain peptides with the p21/waf1/cip1 DNA response element. J. Biol. Chem. 272: 14830-14841
73. 72 Nagaich A. K., Appella E. and Harrington R. E. (1997) DNA bending is essential for the site-specific recognition of DNA response elements by the DNA binding domain of the tumour suppressor protein p53. J. Biol. Chem. 272: 14842-14849
74. 73 Jayaraman L., Murthy K. G. K., Manley J. L., Bustin M. and Prives C. (1998) Identification of HMG-1 as a unique activator of p53. Genes Dev. 12: 462-472
75. 74 Bustin M. and Reeves R. (1996) High mobility group proteins. Progress Nucleic Acid Res. Mol. Biol. 54: 35-100
76. 75 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
77. 76 Wang Y., Reed M., Wang P., Stenger J. E., Mayr G., Anderson M. E. et al. (1993) p53 domains: identification and characterization of two autonomous DNA-binding regions. Genes Dev. 7: 2575-2586
78. 77 Brain R. and Jenkins J. R. (1994) Human p53 directs DNA strand reassociation and is photolabelled by 8-azido ATP. Oncogene 9: 1775-1780
79. 78 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
80. 79 Balkalkin G., Yakovleva T., Selivanova G., Magnusson K. P., Szekely L., Kiseleva E. et al. (1994) p53 binds single-stranded DNA ends and catalyzes DNA renaturation and strand transfer. Proc. Natl. Acad. Sci. USA 91: 413-417
81. 80 Waterman J. L., Shenk J. L. and Halazonetis T. D. (1995) The dihedral symmetry of the p53 tetramerization domain mandates a conformational switch upon DNA binding. EMBO J. 14: 512-519
82. 81 Clore G. M., Ernst J., Clubb R., Omichinski J. G., Kennedy W. M. P., Sakaguchi K. et al. (1995) Refined solution structure of the oligomerization domain of the tumour suppressor p53. Struct. Biol. 2: 321-332
83. 82 Lee W., Harvey T. S., Yin Y., Yau P., Litchfield D. and Arrowsmith C. H. (1994) Solution structure of the tetrameric minimum transforming domain of p53. Nature Struct. Biol. 1: 877-90
84. 83 Jeffrey P. D., Gorina S. and Pavletich N. P. (1995) Crystal structure of the tetramerization domain of the p53 tumour suppressor at 1.7 angstroms. Science 267: 1498-1502
85. 84 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
86. 85 Waterman M. J., Waterman J. L. and Halazonetis T. D. (1996) An engineered four-stranded coiled coil substitutes for the tetramerization domain of wild-type p53 and alleviates transdominant inhibition by tumour-derived p53 mutants. Cancer Res. 56: 158-163
87. 86 Chene P., Mittl P. and Grutter M. (1997) In vitro structure-function analysis of the beta-strand 326 333 of human p53. J. Mol. Biol. 273: 873-881
88. 87 McCoy M., Slavridi E. S., Waterman J. L., Wieczorek A. M., Opella S. J. and Halazonetis T. D. (1997) Hydrophobic side-chain size is a determinant of the three-dimensional structure of the p53 oligomerization domain. EMBO J. 16: 6230-6236
89. 88 Ishioka C., Englert C., Winge P., Yan V. X., Engelstein M. and Friend S. H. (1995) Mutational analysis of the carboxy-terminal portion of p53 using both yeast and mammalian cell assays in vivo. Oncogene 10: 1485-1492
90. 89 Pellegata N. S., Cajot J. F. and Stanbridge E. J. (1995) The basic carboxy-terminal domain of human p53 is dispensable for both transcriptional regulation and inhibition of tumour cell growth. Oncogene 11: 337-349
91. 90 Jayaraman L. and Prives C. (1995) Activation of p53 sequence-specific DNA binding by short single strands of DNA requires the p53 C-terminus. Cell 81: 1021-1029
92. 91 Hupp T. R., Sparks A. and Lane D. P. (1995) Small peptides activated the latent sequence-specific DNA binding function of p53. Cell 83: 237-245
93. 92 Shaw P., Freeman J., Bovey R. and Iggo R. (1996) Regulation of specific DNA binding by p53: evidence for a role for O-glycosylation and charged residues at the carboxy-terminus. Oncogene 12: 20797-20802
94. 93 Halazonetis T. D., Davis L. J. and Kandil A. N. (1993) Wild-type p53 adopts a 'mutant'-like conformation when bound to DNA. EMBO J. 12: 1021-1028
95. 94 Hupp T. R. and Lane D. P. (1994) Allosteric activation of latent p53 tetramers. Curr. Biol. 4: 865-875
96. 95 Bayle J. H., Elenbaas B. and Levine A. J. (1995) The carboxyl-terminal domain of the p53 protein regulates sequence-specific DNA binding through its non-specific nucleic acid binding activity. Proc. Natl. Acad. Sci. USA 92: 5729-5733
97. 96 Anderson M. E., Woelker B., Reed M., Wang P. and Tegtmeyer P. (1997) Reciprocal interference between the sequence-specific core and nonspecific C-terminal DNA binding domains of p53: implications for regulation. Mol. Cell. Biol. 17: 6255-6264
98. 97 Fiscella M., Ullrich S. J., Zambrano N., Shields M. T., Lin D., Lees-Miller S. P. et al. (1993) Mutation of the serine 15 phosphorylation site of human p53 reduces the ability of p53 to inhibit cell cycle progression. Oncogene 8: 1519-1528
99. 98 Fuchs B., O'Connor D., Fallis L., Scheidtmann K. H. and Lu X. (1995) p53 phosphorylation mutants retain transcription activity. Oncogene 10: 789-793
100. 99 Mayr G. A., Reed M., Wang P., Wang Y., Schwedes J. F. and Tegtmeyer P. (1995) Serine phosphorylation in the NH2 terminus of p53 facilitates transactivation. Cancer Res. 55: 2410-2417
101. 100 Fiscella M., Zambrano N., Ullrich S. J., Unger T., Lin D., Cho B. et al. (1994) The carboxy-terminal serine 392 phosphorylation site of human p53 is not required for wild-type activities. Oncogene 9: 3249-3257
102. 101 Marston N. J., Crook T. and Vousden K. H. (1994) Interaction of p53 with MDM2 is independent of E6 and does not mediate wild type transformation suppressor function. Oncogene 9: 2707-2716
103. 102 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
104. 103 Hao M., Lowy A. M., Kapoor M., Deffie A., Liu G. and Lozano G. (1996) Mutation of phosphoserine 389 affects p53 function in vivo. J. Biol. Chem. 271: 29380-29385
105. 104 Hall S. R., Campbell L. E. and Meek D. W. (1996) Phosphorylation of p53 at the casein kinase II site selectively regulates p53-dependent transcriptional repression but not transactivation. Nucleic Acids Res. 24: 1119-1126
106. 105 Horikoshi N., Usheva A., Chen J., Levine A. J., Weinmann R. and Shenk T. (1995) Two domains of p53 interact with the TATA-binding protein, and the adenovirus 13S E1A protein disrupts the association, relieving p53-mediated transcriptional repression. Mol. Cell. Biol. 15: 227-234
107. 106 Shaulian E., Haviv I., Shaul Y. and Oren M. (1995) Transcriptional repression by the C-terminal domain of p53. Oncogene 10: 671-680
108. 107 Filhol O., Baudier J., Chambaz E. M. and Cochet C. (1996) Casein kinase 2 inhibits the renaturation of complementary DNA strands mediated by p53 protein. Biochem. J. 316: 331-335
109. 108 Appel K., Wagner P., Boldyreff B., Issinger O. G. and Montenarh M. (1995) Mapping of the interaction sites of the growth suppressor protein p53 with the regulatory beta-subunit of protein kinase CK2. Oncogene 11: 1971-1978
110. 109 Sakaguchi K., Sakamoto H., Lewis M. S., Anderson C. W., Erickson J. W., Appella E. et al. (1997) Phosphorylation of serine 392 stabilizes the tetramer formation of tumour suppressor protein p53. Biochemistry 36: 10117-10124
111. 110 Kapoor M. and Lozano G. (1998) Functional activation of p53 via phosphorylation following DNA damage by UV but not gamma radiation. Proc. Natl. Acad. Sci. USA 95: 2834-2837
112. 111 Takenaka I., Morin F., Seizinger B. R. and Kley N. (1995) Regulation of the sequence-specific DNA binding function of p53 by protein kinase C and protein phosphatases. J. Biol. Chem. 270: 5405-5411
113. 112 Baudier J., Delphin C., Grunwald D., Khochbin S. and Lawrence J. J. (1992) Characterization of the tumour suppressor protein p53 as a protein kinase C substrate and a S100b-binding protein. Proc. Natl. Acad. Sci. USA 89: 11627-11631
114. 113 Milne D. M., McKendrick L., Jardine L. J., Deacon E., Lord J. M. and Meek D. W. (1996) Murine p53 is phosphorylated within the PAb421 epitope by protein kinase C in vitro, but not in vivo, even after stimulation with the phorbol ester o-tetradecanoylphorbol 13-acetate. Oncogene 13: 205-211
115. 114 Delphin C., Huang K. P., Scotto C., Chapel A., Vincon M., Chambaz E. et al. (1997) The in vitro phosphorylation of p53 by calcium-dependent protein kinase C-characterization of a protein-kinase-C-binding site on p53. Eur. J. Biochem. 245: 684-692
116. 115 Chernov M. V., Ramana C. V., Adler V. V. and Stark G. R. (1998) Stabilization and activation of p53 are regulated independently by different phosphorylation events. Proc. Natl. Acad. Sci. USA 95: 2284-2289
117. 116 Pitkanen K., Haapajarvi T. and Laiho M. (1998) U.V.C.-induction of p53 activation and accumulation is dependent on cell cycle and pathways involving protein synthesis and phosphorylation. Oncogene 16: 459-469
118. 117 Wang Y. and Prives C. (1995) Increased and altered DNA binding of human p53 by S and G2/M but not G1 cyclin-dependent kinases. Nature 376: 88-91
119. 118 Hansen S., Midgley C. A., Lane D. P., Freeman B. C., Morimoto R. I. and Hupp T. R. (1996) Modification of two distinct COOH-terminal domains is required for murine p53 activation by bacterial Hsp70. J. Biol. Chem. 271: 30922-30928
120. 119 Wagner P., Fuchs A., Gotz C., Nastainczyk W. and Montenarh M. (1998) Fine mapping and regulation of the association of p53 with p34cdc2. Oncogene 16: 105-111
121. 120 Lu H., Fisher R. P., Bailey P. and Levine A. J. (1997) The CDK7-cycH-p36 complex of transcription factor IIH phosphorylates p53, enhancing its sequence-specific DNA binding activity in vitro. Mol. Cell. Biol. 17: 5923-5934
122. 121 Wang X., Vermeulen W., Coursen J. D., Gibson M., Lupold S. E., Forrester K. et al. (1996) The XPB and XPD DNA helicases are components of the p53-mediated apoptosis pathway. Genes Dev. 10: 1219-1232
123. 122 Xiao H., Pearson A., Coulombe B., Truant R., Zhang S., Regier J. L. et al. (1994) Binding of basal transcription factor TFIIH to the acidic activation domains of VP16 and p53. Mol. Cell. Biol. 14: 7013-7024
124. 123 Fontoura B. M., Sorokina E. A., David E. and Carroll R. B. (1992) p53 is covalently linked to 5.8S rRNA. Mol. Cell. Biol. 12: 5145-5151
125. 124 Gu W. and Roeder R. G. (1997) Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90: 595-606
126. 125 Balkalkin G., Selivanova G., Yakovleva T., Kiseleva E., Kashuba E., Magnusson K. P. et al. (1995) p53 binds single-stranded DNA ends through the C-terminal domain and internal DNA segments via the middle domain. Nucleic Acids Res. 23: 362-369
127. 126 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
128. 127 Lee S., Cavallo L. and Griffith J. (1997) Human p53 binds Holliday junctions strongly and facilitates their cleavage. J. Biol. Chem. 272: 7532-7539
129. 128 Reed M., Woelker B., Wang P., Wang Y., Anderson M. E. and Tegtmeyer P. (1995) The C-terminal domain of p53 recognizes DNA damaged by ionizing radiation. Proc. Natl. Acad. Sci. USA 92: 9455-9459
130. 129 Buchhop S., Gibson M. K., Wang X. W., Wagner P., Sturzbecher H. W. and Harris C. C. (1997) Interaction of p53 with the human Rad51 protein. Nucleic Acids Res. 25: 3868-3874
131. 130 Abarzua P., LoSardo J. E., Gubler M. L., Spathis R., Lu Y. A., Felix A. et al. (1996) Restoration of the transcription activation function to mutant p53 in human cancer cells. Oncogene 13: 2477-2482
132. 131 Abarzua P., LoSardo J. E., Gubler M. L. and Neri A. (1995) Microinjection of monoclonal antibody Pab421 into human SW480 colorectal carcinoma cells restores the transcription activation function to mutant p53. Cancer Res. 55: 3490-3494
133. 132 Selivanova G., Iotsova V., Okan I., Fritsche M., Strom M., Groner B. et al. (1997) Restoration of the growth suppression function of mutant p53 by a synthetic peptide derived from the p53 C-terminal domain. Nature Med. 3: 632-638