A gain-of-function mutant p53-HSF1 feed forward circuit governs adaptation of cancer cells to proteotoxic stress

Cell Death and Disease

Volumn 5, Issue 4, 2014, Pages

  Li, D ^a   Yallowitz, A ^a   Ozog, L ^a   Marchenko, N ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

EGFR; ErbB2; HSF1; Hsp90; Mutant p53; Ser326 HSF1

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; HEAT SHOCK PROTEIN 90; HEAT SHOCK TRANSCRIPTION FACTOR 1; MITOGEN ACTIVATED PROTEIN KINASE; MUTANT PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN P53; SERINE; DNA BINDING PROTEIN; HEAT SHOCK TRANSCRIPTION FACTOR; PHOSPHOSERINE; PROTEIN BINDING; TRANSCRIPTION FACTOR;

ADAPTATION; ARTICLE; CANCER CELL; CELL STRESS; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MALIGNANT TRANSFORMATION; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEOTOXIC STRESS; SIGNAL TRANSDUCTION; ANIMAL; BREAST TUMOR; CELL NUCLEUS; FEMALE; GENETIC TRANSCRIPTION; GENETICS; HEAT SHOCK RESPONSE; METABOLISM; MOUSE; MUTATION; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGICAL STRESS; TUMOR CELL LINE; UPREGULATION;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL NUCLEUS; DNA-BINDING PROTEINS; FEMALE; HEAT-SHOCK RESPONSE; HUMANS; MICE; MUTANT PROTEINS; MUTATION; PHOSPHORYLATION; PHOSPHOSERINE; PROTEIN BINDING; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 84901020936     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.158     Document Type: Article

References (37)

1. Freed-Pastor WA, Prives C. Mutant p53: one name, many proteins. Genes Deve 2012; 26: 1268-1286.
2. Lee MK, Teoh WW, Phang BH, Tong WM, Wang ZQ, Sabapathy K. Cell-type, dose, and mutation-type specificity dictate mutant p53 functions in vivo. Cancer Cell 2012; 22: 751-764.
3. Oren M, Rotter V. Mutant p53 gain-of-function in cancer. Cold Spring Harb Persp Biol 2010; 2: a001107.
4. Muller PA, Vousden KH. p53 mutations in cancer. Nat Cell Biol 2013; 15: 2-8.
5. Ciocca DR, Arrigo AP, Calderwood SK. Heat shock proteins and heat shock factor 1 in carcinogenesis and tumor development: an update. Arch Toxicol 2013; 87: 19-48.
6. Whitesell L, Lindquist S. Inhibiting the transcription factor HSF1 as an anticancer strategy. Exp Opin Ther Targets 2009; 13: 469-478.
7. Mendillo ML, Santagata S, Koeva M, Bell GW, Hu R, Tamimi RM et al. HSF1 drives a transcriptional program distinct from heat shock to support highly malignant human cancers. Cell 2012; 150: 549-562.
8. Dai C, Whitesell L, Rogers AB, Lindquist S. Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell 2007; 130: 1005-1018.
9. Li D, Marchenko ND, Schulz R, Fischer V, Velasco-Hernandez T, Talos F et al. Functional inactivation of endogenous MDM2 and CHIP by HSP90 causes aberrant stabilization of mutant p53 in human cancer cells. Mol Cancer Res 2011; 9: 577-588.
10. Li D, Marchenko ND, Moll UM. SAHA shows preferential cytotoxicity in mutant p53 cancer cells by destabilizing mutant p53 through inhibition of the HDAC6-Hsp90 chaperone axis. Cell Death Differ 2011; 18: 1904-1913.
11. Lang GA, Iwakuma T, Suh YA, Liu G, Rao VA, Parant JM et al. Gain of function of a p53 hot spot mutation in a mouse model of Li-Fraumeni syndrome. Cell 2004; 119: 861-872.
12. Olive KP, Tuveson DA, Ruhe ZC, Yin B, Willis NA, Bronson RT et al. Mutant p53 gain of function in two mouse models of Li-Fraumeni syndrome. Cell 2004; 119: 847-860.
13. Muller WJ, Sinn E, Pattengale PK, Wallace R, Leder P. Single-step induction of mammary adenocarcinoma in transgenic mice bearing the activated c-neu oncogene. Cell 1988; 54: 105-115.
14. Voellmy R. On mechanisms that control heat shock transcription factor activity in metazoan cells. Cell Stress Chaperones 2004; 9: 122-133.
15. Dai C, Santagata S, Tang Z, Shi J, Cao J, Kwon H et al. Loss of tumor suppressor NF1 activates HSF1 to promote carcinogenesis. J Clin Investig 2012; 122: 3742-3754.
16. Newton R, Cambridge L, Hart LA, Stevens DA, Lindsay MA, Barnes PJ. The MAP kinase inhibitors, PD098059, UO126 and SB203580, inhibit IL-1beta-dependent PGE(2) release via mechanistically distinct processes. Br J Pharmacol 2000; 130: 1353-1361.
17. Gharbi SI, Zvelebil MJ, Shuttleworth SJ, Hancox T, Saghir N, Timms JF et al. Exploring the specificity of the PI3K family inhibitor LY294002. Biochem J 2007; 404: 15-21.
18. Guo F, Letrent SP, Munster PN, Britten CD, Gelmon K, Tolcher AW et al. Pharmacokinetics of a HER2 tyrosine kinase inhibitor CP-724,714 in patients with advanced malignant HER2 positive solid tumors: correlations with clinical characteristics and safety. Cancer Chemother Pharmacol 2008; 62: 97-109.
19. Wu W, Graves LM, Gill GN, Parsons SJ, Samet JM. Src-dependent phosphorylation of the epidermal growth factor receptor on tyrosine 845 is required for zinc-induced Ras activation. J Biol Chem 2002; 277: 24252-24257.
20. Powers MV, Workman P. Targeting of multiple signalling pathways by heat shock protein 90 molecular chaperone inhibitors. Endocr Relat Cancer 2006; 13(Suppl 1): S125-S135.
21. Neckers L, Workman P. Hsp90 molecular chaperone inhibitors: are we there yet? Clin Cancer Res 2012; 18: 64-76.
22. Muller PA, Caswell PT, Doyle B, Iwanicki MP, Tan EH, Karim S et al. Mutant p53 drives invasion by promoting integrin recycling. Cell 2009; 139: 1327-1341.
23. Luo J, Solimini NL, Elledge SJ. Principles of cancer therapy: oncogene and non-oncogene addiction. Cell 2009; 136: 823-837.
24. Santagata S, Hu R, Lin NU, Mendillo ML, Collins LC, Hankinson SE et al. High levels of nuclear heat-shock factor 1 (HSF1) are associated with poor prognosis in breast cancer. Proc Natl Acad Sci USA 2011; 108: 18378-18383.
25. Cancer Genome Atlas N. Comprehensive molecular portraits of human breast tumours. Nature 2012; 490: 61-70.
26. Terzian T, Suh YA, Iwakuma T, Post SM, Neumann M, Lang GA et al. The inherent instability of mutant p53 is alleviated by Mdm2 or p16INK4a loss. Genes Dev 2008; 22: 1337-1344.
27. Yan W, Liu G, Scoumanne A, Chen X. Suppression of inhibitor of differentiation 2, a target of mutant p53, is required for gain-of-function mutations. Cancer Res 2008; 68: 6789-6796.
28. 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.
29. Kim G, Meriin AB, Gabai VL, Christians E, Benjamin I, Wilson A et al. The heat shock transcription factor Hsf1 is downregulated in DNA damage-associated senescence, contributing to the maintenance of senescence phenotype. Aging Cell 2012; 11: 617-627.
30. Yarden Y, Pines G. The ERBB network: at last, cancer therapy meets systems biology. Nature Rev Cancer 2012; 12: 553-563.
31. Ahsan A, Ramanand SG, Whitehead C, Hiniker SM, Rehemtulla A, Pratt WB et al. Wildtype EGFR is stabilized by direct interaction with HSP90 in cancer cells and tumors. Neoplasia 2012; 14: 670-677.
32. Powers MV, Clarke PA, Workman P. Dual targeting of HSC70 and HSP72 inhibits HSP90 function and induces tumor-specific apoptosis. Cancer Cell 2008; 14: 250-262.
33. Denissov S, van Driel M, Voit R, Hekkelman M, Hulsen T, Hernandez N et al. Identification of novel functional TBP-binding sites and general factor repertoires. EMBO J 2007; 26: 944-954.
34. Adachi M, Liu Y, Fujii K, Calderwood SK, Nakai A, Imai K et al. Oxidative stress impairs the heat stress response and delays unfolded protein recovery. PLoS One 2009; 4: e7719.
35. Masciari S, Dillon DA, Rath M, Robson M, Weitzel JN, Balmana J et al. Breast cancer phenotype in women with TP53 germline mutations: a Li-Fraumeni syndrome consortium effort. Breast Cancer Res Treat 2012; 133: 1125-1130.
36. Rahko E, Blanco G, Soini Y, Bloigu R, Jukkola A. A mutant TP53 gene status is associated with a poor prognosis and anthracycline-resistance in breast cancer patients. Eur J Cancer 2003; 39: 447-453.
37. Yamashita H, Nishio M, Toyama T, Sugiura H, Zhang Z, Kobayashi S et al. Coexistence of HER2 over-expression and p53 protein accumulation is a strong prognostic molecular marker in breast cancer. Breast Cancer Res 2004; 6: R24-R30.