Chaperoning of mutant p53 protein by wild-type p53 protein causes hypoxic tumor regression

Journal of Biological Chemistry

Volumn 287, Issue 4, 2012, Pages 2907-2914

  Gogna, Rajan ^a   Madan, Esha ^a   Kuppusamy, Periannan ^b   Pati, Uttam ^a  

^a JAWAHARLAL NEHRU UNIVERSITY   (India)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATION PROPENSITY; CANCER CELLS; CANCER THERAPEUTICS; CELLULAR EVENTS; CHAPERONE FUNCTIONS; CHEMORESISTANCE; CONFORMATIONAL CHANGE; DOMINANT NEGATIVE; IN-VIVO; MOLECULAR CHAPERONES; MUTANT PHENOTYPE; NEW DIMENSIONS; ONCOGENIC MUTANTS; P53 FUNCTION; P53 MUTANTS; P53 PROTEIN; SOLID TUMORS; TUMOR REGRESSION; TUMOR SUPPRESSION; TUMOR XENOGRAFTS; WILD TYPES;

BIOLOGICAL MATERIALS; CELL DEATH; DISEASES;

TUMORS;

CHAPERONE; MUTANT PROTEIN; OXYGEN; PROTEIN P53; PROTEOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL; CARCINOGENESIS; CELL STRAIN MCF 7; CONTROLLED STUDY; DRUG RESISTANCE; GENE INACTIVATION; GENETIC TRANSCRIPTION; HYPOXIA; IN VIVO STUDY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN STRUCTURE; SOLID TUMOR; TUMOR REGRESSION; TUMOR XENOGRAFT; WILD TYPE;

ANIMALS; CELL HYPOXIA; HEP G2 CELLS; HUMANS; MICE; MUTATION; NEOPLASM TRANSPLANTATION; NEOPLASMS; PROTEIN CONFORMATION; TRANSPLANTATION, HETEROLOGOUS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84856073049     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.317354     Document Type: Article

References (36)

1. Schnitzer, S. E., Schmid, T., Zhou, J., and Brüne, B. (2006) Hypoxia and HIF-1α protect A549 cells from drug-induced apoptosis. Cell Death Differ. 13, 1611-1613 (Pubitemid 44210362)
2. Ashcroft, M., Taya, Y., and Vousden, K. H. (2000) Stress signals utilize multiple pathways to stabilize p53. Mol. Cell. Biol. 20, 3224-3233 (Pubitemid 30215034)
3. Koumenis, C., Alarcon, R., Hammond, E., Sutphin, P., Hoffman, W., Murphy, M., Derr, J., Taya, Y., Lowe, S. W., Kastan, M., and Giaccia, A. (2001) Regulation of p53 by hypoxia: dissociation of transcriptional repression and apoptosis from p53-dependent transactivation. Mol. Cell. Biol. 21, 1297-1310 (Pubitemid 32114977)
4. Achison, M., and Hupp, T. R. (2003) Hypoxia attenuates the p53 response to cellular damage. Oncogene 22, 3431-3440 (Pubitemid 36713741)
5. Hammond, E. M., and Giaccia, A. J. (2006) Hypoxia-inducible factor-1 and p53: friends, acquaintances, or strangers? Clin. Cancer Res. 12, 5007-5009
6. Liu, T., Laurell, C., Selivanova, G., Lundeberg, J., Nilsson, P., and Wiman, K. G. (2007) Hypoxia induces p53-dependent transactivation and Fas/CD95-dependent apoptosis. Cell Death Differ. 14, 411-421
7. Pan, Y., Oprysko, P. R., Asham, A. M., Koch, C. J., and Simon, M. C. (2004) p53 cannot be induced by hypoxia alone but responds to the hypoxic microenvironment. Oncogene 23, 4975-4983 (Pubitemid 38938730)
8. Bourdon, J. C., Khoury, M. P., Diot, A., Baker, L., Fernandes, K., Aoubala, M., Quinlan, P., Purdie, C. A., Jordan, L. B., Prats, A. C., Lane, D. P., and Thompson, A. M. (2011) p53 mutant breast cancer patients expressing p53γ have as good a prognosis as wild-type p53 breast cancer patients. Breast Cancer Res. 13, R7
9. Martins, C. P., Brown-Swigart, L., and Evan, G. I. (2006) Modeling the therapeutic efficacy of p53 restoration in tumors. Cell 127, 1323-1334 (Pubitemid 44960417)
10. Sauter, E. R., Takemoto, R., Litwin, S., and Herlyn, M. (2002) p53 alone or in combination with antisense cyclin D1 induces apoptosis and reduces tumor size in human melanoma. Cancer Gene Ther. 9, 807-812
11. Senzer, N., Nemunaitis, J., Nemunaitis, M., Lamont, J., Gore, M., Gabra, H., Eeles, R., Sodha, N., Lynch, F. J., Zumstein, L. A., Menander, K. B., Sobol, R. E., and Chada, S. (2007) p53 therapy in a patient with Li-Fraumeni syndrome. Mol. Cancer Ther. 6, 1478-1482 (Pubitemid 46954014)
12. Ventura, A., Kirsch, D. G., McLaughlin, M. E., Tuveson, D. A., Grimm, J., Lintault, L., Newman, J., Reczek, E. E., Weissleder, R., and Jacks, T. (2007) Restoration of p53 function leads to tumour regression in vivo. Nature 445, 661-665 (Pubitemid 46232887)
13. Xue, W., Zender, L., Miething, C., Dickins, R. A., Hernando, E., Krizhanovsky, V., Cordon-Cardo, C., and Lowe, S. W. (2007) Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 445, 656-660 (Pubitemid 46232886)
14. Vazquez, A., Bond, E. E., Levine, A. J., and Bond, G. L. (2008) The genetics of the p53 pathway, apoptosis and cancer therapy. Nat. Rev. Drug Discov. 7, 979-987
15. 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 (Pubitemid 121001308)
16. Xu, J., Reumers, J., Couceiro, J. R., De Smet, F., Gallardo, R., Rudyak, S., Cornelis, A., Rozenski, J., Zwolinska, A., Marine, J. C., Lambrechts, D., Suh, Y. A., Rousseau, F., and Schymkowitz, J. (2011) Gain of function of mutant p53 by coaggregation with multiple tumor suppressors. Nat. Chem. Biol. 7, 285-295
17. Kuppusamy, P., Li, H., Ilangovan, G., Cardounel, A. J., Zweier, J. L., Yamada, K., Krishna, M. C., and Mitchell, J. B. (2002) Noninvasive imaging of tumor redox status and its modification by tissue glutathione levels. Cancer Res. 62, 307-312 (Pubitemid 34074020)
18. Vaupel, P., Höckel, M., and Mayer, A. (2007) Detection and characterization of tumor hypoxia using pO2 histography. Antioxid. Redox Signal. 9, 1221-1235 (Pubitemid 47080831)
19. Wang, P. L., Sait, F., and Winter, G. (2001) The "wild-type" conformation of p53: epitope mapping using hybrid proteins. Oncogene 20, 2318-2324 (Pubitemid 32531290)
20. Gannon, J. V., Greaves, R., Iggo, R., and Lane, D. P. (1990) Activating mutations in p53 produce a common conformational effect: a monoclonal antibody specific for the mutant form. EMBO J. 9, 1595-1602
21. Graeber, T. G., Peterson, J. F., Tsai, M., Monica, K., Fornace, A. J., Jr., and Giaccia, A. J. (1994) Hypoxia induces accumulation of p53 protein, but activation of a G1 phase checkpoint by low-oxygen conditions is independent of p53 status. Mol. Cell. Biol. 14, 6264-6277
22. Waldo, G. S., Standish, B. M., Berendzen, J., and Terwilliger, T. C. (1999) Rapid protein-folding assay using green fluorescent protein. Nat. Biotechnol. 17, 691-695 (Pubitemid 29316148)
23. Nollen, E. A., and Morimoto, R. I. (2002) Chaperoning signaling pathways: molecular chaperones as stress-sensing "heat shock" proteins. J. Cell Sci. 115, 2809-2816
24. Freeman, B. C., and Yamamoto, K. R. (2002) Disassembly of transcriptional regulatory complexes by molecular chaperones. Science 296, 2232-2235 (Pubitemid 34680310)
25. Tripathi, V., Ali, A., Bhat, R., and Pati, U. (2007) CHIP chaperones wildtype p53 tumor suppressor protein. J. Biol. Chem. 282, 28441-28454 (Pubitemid 47606015)
26. Walerych, D., Olszewski, M. B., Gutkowska, M., Helwak, A., Zylicz, M., and Zylicz, A. (2009) Hsp70 molecular chaperones are required to support p53 tumor suppressor activity under stress conditions. Oncogene 28, 4284-4294
27. Sharma, A. K., Ali, A., Gogna, R., Singh, A. K., and Pati, U. (2009) p53 amino terminus region (1-125) stabilizes and restores heat denatured p53 wild phenotype. PloS One 4, e7159
28. Lavrrar, J. L., and Farnham, P. J. (2004) Use of transient chromatin immunoprecipitation assays to test models for E2F1-specific transcriptional activation. J. Biol. Chem. 279, 46343-46349 (Pubitemid 39491630)
29. Somers, K. D., Merrick, M. A., Lopez, M. E., Incognito, L. S., Schechter, G. L., and Casey, G. (1992) Frequent p53 mutations in head and neck cancer. Cancer Res. 52, 5997-6000
30. Chandrachud, U., and Gal, S. (2009) Three assays show differences in binding of wild-type and mutant p53 to unique gene sequences. Technol. Cancer Res. Treat. 8, 445-453
31. Bajgelman, M. C., and Strauss, B. E. (2006) The DU145 human prostate carcinoma cell line harbors a temperature-sensitive allele of p53. Prostate 66, 1455-1462 (Pubitemid 44350371)
32. Goh, A. M., Coffill, C. R., and Lane, D. P. (2011) The role of mutant p53 in human cancer. J. Pathol. 223, 116-126
33. Joerger, A. C., and Fersht, A. R. (2008) Structural biology of the tumor suppressor p53. Annu. Rev. Biochem. 77, 557-582
34. Shangary, S., and Wang, S. (2009) Small-molecule inhibitors of the MDM2-p53 protein-protein interaction to reactivate p53 function: a novel approach for cancer therapy. Annu. Rev. Pharmacol. Toxicol. 49, 223-241
35. Wiman, K. G. (2010) Pharmacological reactivation of mutant p53: from protein structure to the cancer patient. Oncogene 29, 4245-4252
36. Kim, H., Kim, K., Choi, J., Heo, K., Baek, H. J., Roeder, R. G., and An, W. (2011) p53 requires an intact C-terminal domain for DNA binding and transactivation. J. Mol. Biol. 10.1016/j.jmb.2011.12.001