Mutant p53 rescue and modulation of p53 redox state

Cell Cycle

Volumn 8, Issue 16, 2009, Pages 2509-2517

  Bykov, Vladimir J N ^a   Lambert, Jeremy M R ^a,c   Hainaut, Pierre ^b   Wiman, Klas G ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

^c UNIVERSITÉ DE LYON   (France)

Author keywords

Apoptosis; Cancer therapy; Mutant p53 rescue; p53; PRIMA 1; Redox regulation

Indexed keywords

BAG 1 PROTEIN; CISPLATIN; CYSTEINE; DOXORUBICIN; ETOPOSIDE; FLUOROURACIL; MULTIDRUG RESISTANCE PROTEIN 1; MUTANT PROTEIN; MYC PROTEIN; PROTEIN P53; PROTEIN P63; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR;

APOPTOSIS; DNA BINDING; DRUG MECHANISM; DRUG TARGETING; GENE MUTATION; HUMAN; INTRACELLULAR TRANSPORT; NONHUMAN; OXIDATION REDUCTION STATE; PROTEIN DOMAIN; PROTEIN EXPRESSION; REGULATOR GENE; REVIEW; TUMOR GROWTH;

EID: 69249202595     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.8.16.9382     Document Type: Review

References (65)

1. Riley T, Sontag E, Chen P, Levine A. Transcriptional control of human p53 - regulated genes. Nat Rev Mol Cell Biol 2008; 9:402-412 (Pubitemid 351574202)
2. Raver-Shapira N, Oren M. Tiny actors, great roles: microRNAs in p53's service. Cell Cycle 2007; 6:2656-2661 (Pubitemid 350224049)
3. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P, et al. p53 has a direct apoptogenic role at the mitochondria. Mol Cell 2003; 11:577-590 (Pubitemid 36385115)
4. Green DR, Kroemer G. Cytoplasmic functions of the tumour suppressor p53. Nature 2009; 458:1127-1130
5. Olivier M, Eeles R, Hollstein M, Khan MA, Harris CC, Hainaut P. The IARC TP53 database: new online mutation analysis and recommendations to users. Hum Mutat 2002; 19:607-614 (Pubitemid 34556481)
6. Cho Y, Gorina S, Jeffrey PD, Pavletich NP. Crystal structure of a p53 tumor suppressor- DNA complex: understanding tumorigenic mutations. Science 1994; 265:346-355 (Pubitemid 24259959)
7. Vousden KH, Lu X. Live or let die: the cell's response to p53. Nat Rev Cancer 2002; 2:594-604. (Pubitemid 37328926)
8. Soussi T, Beroud C. Assessing TP53 status in human tumours to evaluate clinical outcome. Nat Rev Cancer 2001; 1:233-240 (Pubitemid 33741898)
9. Bressac B, Kew M, Wands J, Ozturk M. Selective G to T mutations of p53 gene in hepatocellular carcinoma from Southern Africa. Nature 1991; 350:429-431 (Pubitemid 21912246)
10. Pfeifer GP, Denissenko MF, Olivier M, Tretyakova N, Hecht SS, Hainaut P. Tobacco smoke carcinogens, DNA damage and p53 mutations in smoking-associated cancers. Oncogene 2002; 21:7435-7451
11. Scian MJ, Stagliano KE, Ellis MA, Hassan S, Bowman M, Miles MF, et al. Modulation of gene expression by tumor-derived p53 mutants. Cancer Res 2004; 64:7447-7454 (Pubitemid 39372087)
12. Sigal A, Rotter V. Oncogenic mutations of the p53 tumor suppressor: the demons of the guardian of the genome. Cancer Res 2000; 60 6788-6793 (Pubitemid 32059139)
13. Gaiddon C, Lokshin M, Ahn J, Zhang T, Prives C. A subset of tumor-derived mutant forms of p53 down-regulate p63 and p73 through a direct interaction with the p53 core domain. Mol Cell Biol 2001; 21:1874-1887 (Pubitemid 32156407)
14. Hainaut P, Mann K. Zinc binding and redox control of p53 structure and function. Antioxid Redox Signal 2001; 3:611-623 (Pubitemid 32785984)
15. Liu B, Chen Y, St. Clair DK. ROS and p53: a versatile partnership. Free Radic Biol Med 2008; 44:1529-1535
16. Bensaad K, Tsuruta A, Selak MA, Vidal MN, Nakano K, Bartrons R, et al. TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell 2006; 126:107-120 (Pubitemid 44040989)
17. Hainaut P, Milner J. Redox modulation of p53 conformation and sequence-specific DNA binding in vitro. Cancer Res 1993; 53:4469-4473 (Pubitemid 23304364)
18. Hupp TR, Meek DW, Midgley CA, Lane DP. Regulation of the specific DNA binding function of p53. Cell 1992; 71:875-886
19. Rainwater R, Parks D, Anderson ME, Tegtmeyer P, Mann K. Role of cysteine residues in regulation of p53 function. Mol Cell Biol 1995; 15:3892-3903
20. Verhaegh GW, Richard MJ, Hainaut P. Regulation of p53 by metal ions and by antioxidants: dithiocarbamate downregulates p53 DNA-binding activity by increasing the intracellular level of copper. Mol Cell Biol 1997; 17:5699-5706 (Pubitemid 27411077)
21. Meplan C, Richard MJ, Hainaut P. Metalloregulation of the tumor suppressor protein p53: zinc mediates the renaturation of p53 after exposure to metal chelators in vitro and in intact cells. Oncogene 2000; 19:5227-5236
22. Seemann S, Hainaut P. Roles of thioredoxin reductase 1 and APE/Ref-1 in the control of basal p53 stability and activity. Oncogene 2005; 24:3853-3863 (Pubitemid 40896397)
23. Pearson GD, Merrill GF. Deletion of the Saccharomyces cerevisiae TRR1 gene encoding thioredoxin reductase inhibits p53-dependent reporter gene expression. J Biol Chem 1998; 273:5431-5434
24. Jayaraman L, Prives C. Covalent and noncovalent modifiers of the p53 protein. Cell Mol Life Sci 1999; 55:76-87. (Pubitemid 29077856)
25. Puca R, Nardinocchi L, Bossi G, Sacchi A, Rechavi G, Givol D, et al. Restoring wtp53 activity in HIPK2 depleted MCF7 cells by modulating metallothionein and zinc. Exp Cell Res 2009; 315:67-75.
26. Puca R, Nardinocchi L, Gal H, Rechavi G, Amariglio N, Domany E, et al. Reversible dysfunction of wild-type p53 following homeodomain-interacting protein kinase-2 knockdown. Cancer Res 2008; 68:3707-3714
27. Friedler A, DeDecker BS, Freund SM, Blair C, Rudiger S, Fersht AR. Structural distortion of p53 by the mutation R249S and its rescue by a designed peptide: implications for "mutant conformation". J Mol Biol 2004; 336:187-196
28. Martin AC, Facchiano AM, Cuff AL, Hernandez-Boussard T, Olivier M, Hainaut P, et al. Integrating mutation data and structural analysis of the TP53 tumor-suppressor protein. Hum Mutat 2002; 19:149-164 (Pubitemid 34121806)
29. Bullock AN, Henckel J, DeDecker BS, Johnson CM, Nikolova PV, Proctor MR, et al. Thermodynamic stability of wild-type and mutant p53 core domain. Proc Natl Acad Sci USA 1997; 94:14338-14342 (Pubitemid 28041374)
30. Lowe SW, Ruley HE, Jacks T, Housman DE. p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell 1993; 74:957-967 (Pubitemid 23289454)
31. Vasey PA, Jones NA, Jenkins S, Dive C, Brown R. Cisplatin, camptothecin and taxol sensitivities of cells with p53-associated multidrug resistance. Mol Pharmacol 1996; 50:1536-1540 (Pubitemid 26425109)
32. Bunz F, Hwang PM, Torrance C, Waldman T, Zhang Y, Dillehay L, et al. Disruption of p53 in human cancer cells alters the responses to therapeutic agents. J Clin Invest 1999; 104:263-269
33. Weller M. Predicting response to cancer chemotherapy: the role of p53. Cell Tissue Res 1998; 292:435-445 (Pubitemid 28282455)
34. Blandino G, Levine AJ, Oren M. Mutant p53 gain of function: differential effects of different p53 mutants on resistance of cultured cells to chemotherapy. Oncogene 1999; 18:477-485 (Pubitemid 29060623)
35. Berns EM, van Staveren IL, Look MP, Smid M, Klijn JG, Foekens JA. Mutations in residues of TP53 that directly contact DNA predict poor outcome in human primary breast cancer. Br J Cancer 1998; 77:1130-1136 (Pubitemid 28116285)
36. Borresen-Dale AL, Lothe RA, Meling GI, Hainaut P, Rognum TO, Skovlund E. TP53 and long-term prognosis in colorectal cancer: mutations in the L3 zinc-binding domain predict poor survival. Clin Cancer Res 1998; 4:203-210 (Pubitemid 28062897)
37. Girgin C, Tarhan H, Hekimgil M, Sezer A, Gurel G. p53 mutations and other prognostic factors of renal cell carcinoma. Urol Int 2001; 66:78-83. (Pubitemid 32172972)
38. Petitjean A, Achatz MI, Borresen-Dale AL, Hainaut P, Olivier M. TP53 mutations in human cancers: functional selection and impact on cancer prognosis and outcomes. Oncogene 2007; 26:2157-2165 (Pubitemid 46536647)
39. Ventura A, Kirsch DG, McLaughlin ME, Tuveson DA, Grimm J, Lintault L, et al. Restoration of p53 function leads to tumour regression in vivo. Nature 2007; 445:661-665 (Pubitemid 46232887)
40. Xue W, Zender L, Miething C, Dickins RA, Hernando E, Krizhanovsky V, et al. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 2007; 445:656-660 (Pubitemid 46232886)
41. Martins CP, Brown-Swigart L, Evan GI. Modeling the Therapeutic Efficacy of p53 Restoration in Tumors. Cell 2006; 127:1323-1334 (Pubitemid 44960417)
42. Selivanova G, Iotsova V, Okan I, Fritsche M, Strom M, Groner B, et al. Restoration of the growth suppression function of mutant p53 by a synthetic peptide derived from the p53 C-terminal domain. Nat Med 1997; 3:632-638 (Pubitemid 27264972)
43. Friedler A, Hansson LO, Veprintsev DB, Freund SM, Rippin TM, Nikolova PV, et al. A peptide that binds and stabilizes p53 core domain: chaperone strategy for rescue of oncogenic mutants. Proc Natl Acad Sci USA 2002; 99:937-942 (Pubitemid 34106614)
44. Foster BA, Coffey HA, Morin MJ, Rastinejad F. Pharmacological rescue of mutant p53 conformation and function. Science 1999; 286:2507-2510 (Pubitemid 30026339)
45. North S, Pluquet O, Maurici D, El-Ghissassi F, Hainaut P. Restoration of wild-type conformation and activity of a temperature-sensitive mutant of p53 (p53(V272M)) by the cytoprotective aminothiol WR1065 in the esophageal cancer cell line TE-1. Mol Carcinog 2002; 33:181-188 (Pubitemid 34195199)
46. Bykov VJ, Issaeva N, Shilov A, Hultcrantz M, Pugacheva E, Chumakov P, et al. Restoration of the tumor suppressor function to mutant p53 by a low-molecular-weight compound. Nat Med 2002; 8:282-288 (Pubitemid 34250107)
47. Bykov VJ, Issaeva N, Zache N, Shilov A, Hultcrantz M, Bergman J, et al. Reactivation of mutant p53 and induction of apoptosis in human tumor cells by maleimide analogs. J Biol Chem 2005; 280:30384-30391 (Pubitemid 41216221)
48. Zache N, Lambert JMR, Rökaeus N, Shen J, Hainaut P, Bergman J, et al. Mutant p53 targeting by the low molecular weight compound STIMA-1. Mol Oncol 2008; 2:70-80.
49. Bykov VJ, Zache N, Stridh H, Westman J, Bergman J, Selivanova G, et al. PRIMA- 1(MET) synergizes with cisplatin to induce tumor cell apoptosis. Oncogene 2005; 24:3484-3491 (Pubitemid 40756249)
50. MET inhibits growth of mouse tumors carrying mutant p53. Cell Oncol 2008; 30:411-418
51. MET induces mitochondrial apoptosis through activation of caspase-2. Oncogene 2008; 27:6571-6580
52. Lambert JM, Gorzov P, Veprintsev DB, Soderqvist M, Segerback D, Bergman J, et al. PRIMA-1 reactivates mutant p53 by covalent binding to the core domain. Cancer Cell 2009; 15:376-388
53. Zache N, Lambert JM, Rokaeus N, Shen J, Hainaut P, Bergman J, et al. Mutant p53 targeting by the low molecular weight compound STIMA-1. Mol Oncol 2008; 2:70-80.
54. Kouvaris JR, Kouloulias VE, Vlahos LJ. Amifostine: the first selective-target and broadspectrum radioprotector. Oncologist 2007; 12:738-747
55. Shen H, Chen ZJ, Zilfou JT, Hopper E, Murphy M, Tew KD. Binding of the aminothiol WR-1065 to transcription factors influences cellular response to anticancer drugs. J Pharmacol Exp Ther 2001; 297:1067-1073 (Pubitemid 32472505)
56. Thomas JA, Poland B, Honzatko R. Protein sulfhydryls and their role in the antioxidant function of protein S-thiolation. Arch Biochem Biophys 1995; 319:1-9.
57. Sun XZ, Vinci C, Makmura L, Han S, Tran D, Nguyen J, et al. Formation of disulfide bond in p53 correlates with inhibition of DNA binding and tetramerization. Antioxid Redox Signal 2003; 5:655-665 (Pubitemid 37315155)
58. Shi LM, Fan Y, Myers TG, O'Connor PM, Paull KD, Friend SH, et al. Mining the NCI anticancer drug discovery databases: genetic function approximation for the QSAR study of anticancer ellipticine analogues. J Chem Inf Comput Sci 1998; 38:189-199 (Pubitemid 128591236)
59. Sugikawa E, Hosoi T, Yazaki N, Gamanuma M, Nakanishi N, Ohashi M. Mutant p53 mediated induction of cell cycle arrest and apoptosis at G1 phase by 9-hydroxyellipticine. Anticancer Res 1999; 19:3099-3108 (Pubitemid 30042597)
60. Stiborova M, Sejbal J, Borek-Dohalska L, Aimova D, Poljakova J, Forsterova K, et al. The anticancer drug ellipticine forms covalent DNA adducts, mediated by human cytochromes P450, through metabolism to 13-hydroxyellipticine and ellipticine N2-oxide. Cancer Res 2004; 64:8374-8380 (Pubitemid 39496831)
61. Stiborova M, Arlt VM, Henderson CJ, Wolf CR, Kotrbova V, Moserova M, et al. Role of hepatic cytochromes P450 in bioactivation of the anticancer drug ellipticine: studies with the hepatic NADPH:cytochrome P450 reductase null mouse. Toxicol Appl Pharmacol 2008; 226:318-327 (Pubitemid 351172414)
62. Pasetto LM, D'Andrea MR, Brandes AA, Rossi E, Monfardini S. The development of platinum compounds and their possible combination. Crit Rev Oncol Hematol 2006; 60:59-75. (Pubitemid 44404105)
63. Bykov VJ, Issaeva N, Selivanova G, Wiman KG. Mutant p53-dependent growth suppression distinguishes PRIMA-1 from known anticancer drugs: a statistical analysis of information in the National Cancer Institute database. Carcinogenesis 2002; 23:2011-2018 (Pubitemid 36104953)
64. Weinstein JN, Myers TG, O'Connor PM, Friend SH, Fornace AJ Jr, Kohn KW, et al. An information-intensive approach to the molecular pharmacology of cancer. Science 1997; 275:343-349 (Pubitemid 27051604)
65. Matas D, Sigal A, Stambolsky P, Milyavsky M, Weisz L, Schwartz D, et al. Integrity of the N-terminal transcription domain of p53 is required for mutant p53 interference with drug-induced apoptosis. EMBO J 2001; 20:4163-4172 (Pubitemid 32751832)