The stress protein BAG3 stabilizes MCL-1 protein and promotes survival of cancer cells and resistance to antagonist ABT-737

Journal of Biological Chemistry

Volumn 288, Issue 10, 2013, Pages 6980-6990

  Boiani, Mariana ^a   Daniel, Cristina ^a   Liu, Xueyuan ^b   Hogarty, Michael D ^b   Marnett, Lawrence J ^a,c  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Children's Hospital   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIAPOPTOTIC ACTIVITIES; ANTICANCER DRUG DISCOVERY; CANCER CELLS; HUMAN CANCER; POTENTIAL TARGETS; PROTEASOMES; STRESS PROTEIN;

CELL DEATH;

PROTEINS;

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; BIM PROTEIN; CASPASE; CELL PROTEIN; HEAT SHOCK PROTEIN 70; MESSENGER RNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAD; PROTEIN BAG3; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL W; PROTEIN BCL XL; PROTEIN MCL 1; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER RESISTANCE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; GENE; GENE SILENCING; IMMUNOBLOTTING; IMMUNOPRECIPITATION; IN VITRO STUDY; MCL 1 GENE; NEUROBLASTOMA CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; TRIPLE NEGATIVE BREAST CANCER;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANTINEOPLASTIC AGENTS; APOPTOSIS; BIPHENYL COMPOUNDS; CELL LINE, TUMOR; CELL SURVIVAL; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; IMMUNOBLOTTING; NEOPLASMS; NITROPHENOLS; PIPERAZINES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN STABILITY; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-BCL-2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SULFONAMIDES; UBIQUITINATION;

EID: 84874817068     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.414177     Document Type: Article

References (69)

1. Green, D. R., and Evan, G. I. (2002) A matter of life and death. Cancer Cell 1, 19-30 (Pubitemid 41039172)
2. Hanahan, D., and Weinberg, R. A. (2000) The hallmarks of cancer. Cell 100, 57-70 (Pubitemid 30046295)
3. Reed, J. C., Cuddy, M., Slabiak, T., Croce, C. M., and Nowell, P. C. (1988) Oncogenic potential of bcl-2 demonstrated by gene transfer. Nature 336, 259-261 (Pubitemid 18264408)
4. Yip, K. W., and Reed, J. C. (2008) Bcl-2 family proteins and cancer. Oncogene 27, 6398-6406
5. Yang, J., Liu, X., Bhalla, K., Kim, C. N., Ibrado, A. M., Cai, J., Peng, T. I., Jones, D. P., and Wang, X. (1997) Prevention of apoptosis by Bcl-2: Release of cytochrome c from mitochondria blocked. Science 275, 1129-1132 (Pubitemid 27097312)
6. Lomonosova, E., and Chinnadurai, G. (2008) BH3-only proteins in apoptosis and beyond: An overview. Oncogene 27, Suppl. 1, S2-S19
7. Willis, S. N., Fletcher, J. I., Kaufmann, T., van Delft, M. F., Chen, L., Czabotar, P. E., Ierino, H., Lee, E. F., Fairlie, W. D., Bouillet, P., Strasser, A., Kluck, R. M., Adams, J. M., and Huang, D. C. (2007) Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 315, 856-859
8. Letai, A., Bassik, M. C., Walensky, L. D., Sorcinelli, M. D., Weiler, S., and Korsmeyer, S. J. (2002) Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2, 183-192 (Pubitemid 41043974)
9. Reed, J. C., Stein, C., Subasinghe, C., Haldar, S., Croce, C. M., Yum, S., and Cohen, J. (1990) Antisense-mediated inhibition of BCL2 protooncogene expression and leukemic cell growth and survival: Comparisons of phosphodiester and phosphorothioate oligodeoxynucleotides. Cancer Res. 50, 6565-6570 (Pubitemid 20348780)
10. Oltersdorf, T., Elmore, S. W., Shoemaker, A. R., Armstrong, R. C., Augeri, D. J., Belli, B. A., Bruncko, M., Deckwerth, T. L., Dinges, J., Hajduk, P. J., Joseph, M. K., Kitada, S., Korsmeyer, S. J., Kunzer, A. R., Letai, A., Li, C., Mitten, M. J., Nettesheim, D. G., Ng, S., Nimmer, P. M., O'Connor, J. M., Oleksijew, A., Petros, A. M., Reed, J. C., Shen, W., Tahir, S. K., Thompson, C. B., Tomaselli, K. J., Wang, B., Wendt, M. D., Zhang, H., Fesik, S. W., and Rosenberg, S. H. (2005) An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435, 677-681 (Pubitemid 40825512)
11. Konopleva, M., Contractor, R., Tsao, T., Samudio, I., Ruvolo, P. P., Kitada, S., Deng, X., Zhai, D., Shi, Y. X., Sneed, T., Verhaegen, M., Soengas, M., Ruvolo, V. R., McQueen, T., Schober, W. D., Watt, J. C., Jiffar, T., Ling, X., Marini, F. C., Harris, D., Dietrich, M., Estrov, Z., McCubrey, J., May, W. S., Reed, J. C., and Andreeff, M. (2006) Mechanisms of apoptosis sensitivity and resistance to the BH3 mimetic ABT-737 in acute myeloid leukemia. Cancer Cell 10, 375-388 (Pubitemid 44693472)
12. Tahir, S. K., Yang, X., Anderson, M. G., Morgan-Lappe, S. E., Sarthy, A. V., Chen, J., Warner, R. B., Ng, S. C., Fesik, S. W., Elmore, S. W., Rosenberg, S. H., and Tse, C. (2007) Influence of Bcl-2 family members on the cellular response of small-cell lung cancer cell lines to ABT-737. Cancer Res. 67, 1176-1183
13. Aichberger, K. J., Mayerhofer, M., Krauth, M. T., Skvara, H., Florian, S., Sonneck, K., Akgul, C., Derdak, S., Pickl, W. F., Wacheck, V., Selzer, E., Monia, B. P., Moriggl, R., Valent, P., and Sillaber, C. (2005) Identification of mcl-1 as a BCR/ABL-dependent target in chronic myeloid leukemia (CML): Evidence for cooperative antileukemic effects of imatinib and mcl-1 antisense oligonucleotides. Blood 105, 3303-3311
14. Derenne, S., Monia, B., Dean, N. M., Taylor, J. K., Rapp, M. J., Harousseau, J. L., Bataille, R., and Amiot, M. (2002) Antisense strategy shows that Mcl-1 rather than Bcl-2 or Bcl-xL is an essential survival protein of human myeloma cells. Blood 100, 194-199 (Pubitemid 35177447)
15. Cho-Vega, J. H., Rassidakis, G. Z., Admirand, J. H., Oyarzo, M., Ramalingam, P., Paraguya, A., McDonnell, T. J., Amin, H. M., and Medeiros, L. J. (2004) MCL-1 expression in B-cell non-Hodgkin's lymphomas. Hum. Pathol. 35, 1095-1100 (Pubitemid 39165341)
16. Sieghart, W., Losert, D., Strommer, S., Cejka, D., Schmid, K., Rasoul-Rockenschaub, S., Bodingbauer, M., Crevenna, R., Monia, B. P., Peck-Radosavljevic, M., and Wacheck, V. (2006) Mcl-1 overexpression in hepatocellular carcinoma: A potential target for antisense therapy. J. Hepatol. 44, 151-157 (Pubitemid 41772529)
17. Akgul, C. (2009) Mcl-1 is a potential therapeutic target in multiple types of cancer. Cell Mol. Life Sci. 66, 1326-1336
18. Yang, T., Kozopas, K. M., and Craig, R. W. (1995) The intracellular distribution and pattern of expression of Mcl-1 overlap with, but are not identical to, those of Bcl-2. J. Cell Biol. 128, 1173-1184
19. Hershko, A., and Ciechanover, A. (1998) The ubiquitin system. Annu. Rev. Biochem. 67, 425-479 (Pubitemid 28411135)
20. Ding, Q., Huo, L., Yang, J. Y., Xia, W., Wei, Y., Liao, Y., Chang, C. J., Yang, Y., Lai, C. C., Lee, D. F., Yen, C. J., Chen, Y. J., Hsu, J. M., Kuo, H. P., Lin, C. Y., Tsai, F. J., Li, L. Y., Tsai, C. H., and Hung, M. C. (2008) Downregulation of myeloid cell leukemia-1 through inhibiting Erk/Pin 1 pathway by sorafenib facilitates chemosensitization in breast cancer. Cancer Res. 68, 6109-6117
21. Domina, A. M., Vrana, J. A., Gregory, M. A., Hann, S. R., and Craig, R. W. (2004) MCL1 is phosphorylated in the PEST region and stabilized upon ERK activation in viable cells, and at additional sites with cytotoxic okadaic acid or taxol. Oncogene 23, 5301-5315 (Pubitemid 39005806)
22. Maurer, U., Charvet, C., Wagman, A. S., Dejardin, E., and Green, D. R. (2006) Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Mol. Cell 21, 749-760 (Pubitemid 43376126)
23. Inoshita, S., Takeda, K., Hatai, T., Terada, Y., Sano, M., Hata, J., Umezawa, A., and Ichijo, H. (2002) Phosphorylation and inactivation of myeloid cell leukemia 1 by JNK in response to oxidative stress. J. Biol. Chem. 277, 43730-43734 (Pubitemid 36157790)
24. Weng, C., Li, Y., Xu, D., Shi, Y., and Tang, H. (2005) Specific cleavage of Mcl-1 by caspase-3 in tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis in Jurkat leukemia T cells. J. Biol. Chem. 280, 10491-10500 (Pubitemid 40395908)
25. Zhong, Q., Gao, W., Du, F., and Wang, X. (2005) Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell 121, 1085-1095 (Pubitemid 40884398)
26. Stewart, D. P., Koss, B., Bathina, M., Perciavalle, R. M., Bisanz, K., and Opferman, J. T. (2010) Ubiquitin-independent degradation of antiapoptotic MCL-1. Mol. Cell Biol. 30, 3099-3110
27. Craig, R. W. (2002) MCL1 provides a window on the role of the BCL2 family in cell proliferation, differentiation and tumorigenesis. Leukemia 16, 444-454 (Pubitemid 34449724)
28. Clohessy, J. G., Zhuang, J., and Brady, H. J. (2004) Characterisation of Mcl-1 cleavage during apoptosis of haematopoietic cells. Br. J. Haematol. 125, 655-665 (Pubitemid 38747969)
29. Nijhawan, D., Fang, M., Traer, E., Zhong, Q., Gao, W., Du, F., and Wang, X. (2003) Elimination of Mcl-1 is required for the initiation of apoptosis following ultraviolet irradiation. Genes Dev. 17, 1475-1486 (Pubitemid 36734705)
30. Schwickart, M., Huang, X., Lill, J. R., Liu, J., Ferrando, R., French, D. M., Maecker, H., O'Rourke, K., Bazan, F., Eastham-Anderson, J., Yue, P., Dornan, D., Huang, D. C., and Dixit, V. M. (2010) Deubiquitinase USP9X stabilizes MCL1 and promotes tumour cell survival. Nature 463, 103-107
31. Jacobs, A. T., and Marnett, L. J. (2009) HSF1-mediated BAG3 expression attenuates apoptosis in 4-hydroxynonenal-treated colon cancer cells via stabilization of anti-apoptotic Bcl-2 proteins. J. Biol. Chem. 284, 9176-9183
32. Takayama, S., Sato, T., Krajewski, S., Kochel, K., Irie, S., Millan, J. A., and Reed, J. C. (1995) Cloning and functional analysis of BAG-1: A novel Bcl-2-binding protein with anti-cell death activity. Cell 80, 279-284
33. Takayama, S., Bimston, D. N., Matsuzawa, S., Freeman, B. C., Aime-Sempe, C., Xie, Z., Morimoto, R. I., and Reed, J. C. (1997) BAG-1 modulates the chaperone activity of Hsp70/Hsc70. EMBO J. 16, 4887-4896 (Pubitemid 27348398)
34. Doong, H., Vrailas, A., and Kohn, E. C. (2002) What's in the 'BAG'TNFαA functional domain analysis of the BAG-family proteins. Cancer Lett. 188, 25-32 (Pubitemid 35292325)
35. Lüders, J., Demand, J., and Höhfeld, J. (2000) The ubiquitin-related BAG-1 provides a link between the molecular chaperones Hsc70/Hsp70 and the proteasome. J. Biol. Chem. 275, 4613-4617 (Pubitemid 30108845)
36. Doong, H., Rizzo, K., Fang, S., Kulpa, V., Weissman, A. M., and Kohn, E. C. (2003) CAIR-1/BAG-3 abrogates heat shock protein-70 chaperone complex-mediated protein degradation: Accumulation of poly-ubiquitinated Hsp90 client proteins. J. Biol. Chem. 278, 28490-28500 (Pubitemid 36935751)
37. Gamerdinger, M., Hajieva, P., Kaya, A. M., Wolfrum, U., Hartl, F. U., and Behl, C. (2009) Protein quality control during aging involves recruitment of the macroautophagy pathway by BAG3. EMBO J. 28, 889-901
38. Gamerdinger, M., Kaya, A. M., Wolfrum, U., Clement, A. M., and Behl, C. (2011) BAG3 mediates chaperone-based aggresome-targeting and selective autophagy of misfolded proteins. EMBO Rep. 12, 149-156
39. Chen, H. Y., Liu, P., Sun, M., Wu, L. Y., Zhu, H. Y., Qiao, C., Dong, H. J., Zhu, D. X., Xu, W., and Li, J. Y. (2010) [Bag3 gene expression in chronic lymphocytic leukemia and its association with patients' prognosis]. Zhongguo Shi Yan Xue Ye Xue Za Zhi 18, 838-842
40. Chiappetta, G., Ammirante, M., Basile, A., Rosati, A., Festa, M., Monaco, M., Vuttariello, E., Pasquinelli, R., Arra, C., Zerilli, M., Todaro, M., Stassi, G., Pezzullo, L., Gentilella, A., Tosco, A., Pascale, M., Marzullo, L., Belisario, M. A., Turco, M. C., and Leone, A. (2007) The antiapoptotic protein BAG3 is expressed in thyroid carcinomas and modulates apoptosis mediated by tumor necrosis factor-related apoptosis-inducing ligand. J. Clin. Endocrinol. Metab. 92, 1159-1163 (Pubitemid 46465696)
41. Liao, Q., Ozawa, F., Friess, H., Zimmermann, A., Takayama, S., Reed, J. C., Kleeff, J., and Büchler, M. W. (2001) The anti-apoptotic protein BAG-3 is overexpressed in pancreatic cancer and induced by heat stress in pancreatic cancer cell lines. FEBS Lett. 503, 151-157 (Pubitemid 32763196)
42. Rosati, A., Ammirante, M., Gentilella, A., Basile, A., Festa, M., Pascale, M., Marzullo, L., Belisario, M. A., Tosco, A., Franceschelli, S., Moltedo, O., Pagliuca, G., Lerose, R., and Turco, M. C. (2007) Apoptosis inhibition in cancer cells: A novel molecular pathway that involves BAG3 protein. Int. J. Biochem. Cell Biol. 39, 1337-1342 (Pubitemid 47031037)
43. Schwab, M., Westermann, F., Hero, B., and Berthold, F. (2003) Neuroblastoma: Biology and molecular and chromosomal pathology. Lancet Oncol. 4, 472-480 (Pubitemid 37009955)
44. Landis, S. H., Murray, T., Bolden, S., and Wingo, P. A. (1999) Cancer statistics, 1999. CA Cancer J. Clin. 49, 8-31 (Pubitemid 29094959)
45. Goldsmith, K. C., and Hogarty, M. D. (2005) Targeting programmed cell death pathways with experimental therapeutics: Opportunities in highrisk neuroblastoma. Cancer Lett. 228, 133-141 (Pubitemid 41188435)
46. Lestini, B. J., Goldsmith, K. C., Fluchel, M. N., Liu, X., Chen, N. L., Goyal, B., Pawel, B. R., and Hogarty, M. D. (2009) Mcl1 downregulation sensitizes neuroblastoma to cytotoxic chemotherapy and small molecule Bcl2-family antagonists. Cancer Biol. Ther. 8, 1587-1595
47. Janoueix-Lerosey, I., Schleiermacher, G., Michels, E., Mosseri, V., Ribeiro, A., Lequin, D., Vermeulen, J., Couturier, J., Peuchmaur, M., Valent, A., Plantaz, D., Rubie, H., Valteau-Couanet, D., Thomas, C., Combaret, V., Rousseau, R., Eggert, A., Michon, J., Speleman, F., and Delattre, O. (2009) Overall genomic pattern is a predictor of outcome in neuroblastoma. J. Clin. Oncol. 27, 1026-1033
48. Mosse, Y. P., Greshock, J., Margolin, A., Naylor, T., Cole, K., Khazi, D., Hii, G., Winter, C., Shahzad, S., Asziz, M. U., Biegel, J. A., Weber, B. L., and Maris, J. M. (2005) High-resolution detection and mapping of genomic DNA alterations in neuroblastoma. Genes Chromosomes Cancer 43, 390-403 (Pubitemid 40946474)
49. Hackett, C. S., Hodgson, J. G., Law, M. E., Fridlyand, J., Osoegawa, K., de Jong, P. J., Nowak, N. J., Pinkel, D., Albertson, D. G., Jain, A., Jenkins, R., Gray, J. W., and Weiss, W. A. (2003) Genome-wide array CGH analysis of murine neuroblastoma reveals distinct genomic aberrations which parallel those in human tumors. Cancer Res. 63, 5266-5273 (Pubitemid 37139840)
50. Goldsmith, K. C., Lestini, B. J., Gross, M., Ip, L., Bhumbla, A., Zhang, X., Zhao, H., Liu, X., and Hogarty, M. D. (2010) BH3 response profiles from neuroblastoma mitochondria predict activity of small molecule Bcl-2 family antagonists. Cell Death Differ. 17, 872-882
51. Goldsmith, K. C., Gross, M., Peirce, S., Luyindula, D., Liu, X., Vu, A., Sliozberg, M., Guo, R., Zhao, H., Reynolds, C. P., and Hogarty, M. D. (2012) Mitochondrial Bcl-2 family dynamics define therapy response and resistance in neuroblastoma. Cancer Res. 72, 2565-2577
52. Certo, M., Del Gaizo Moore, V., Nishino, M., Wei, G., Korsmeyer, S., Armstrong, S. A., and Letai, A. (2006) Mitochondria primed by death signals determine cellular addiction to antiapoptotic BCL-2 family members. Cancer Cell 9, 351-365 (Pubitemid 43668734)
53. Lee, J. H., Takahashi, T., Yasuhara, N., Inazawa, J., Kamada, S., and Tsujimoto, Y. (1999) Bis, a Bcl-2-binding protein that synergizes with Bcl-2 in preventing cell death. Oncogene 18, 6183-6190
54. Akgul, C., Moulding, D. A., White, M. R., and Edwards, S. W. (2000) In vivo localisation and stability of human Mcl-1 using green fluorescent protein (GFP) fusion proteins. FEBS Lett. 478, 72-76 (Pubitemid 30462261)
55. Iwasaki, M., Homma, S., Hishiya, A., Dolezal, S. J., Reed, J. C., and Takayama, S. (2007) BAG3 regulates motility and adhesion of epithelial cancer cells. Cancer Res. 67, 10252-10259 (Pubitemid 350070798)
56. Takayama, S., Xie, Z., and Reed, J. C. (1999) An evolutionarily conserved family of Hsp70/Hsc70 molecular chaperone regulators. J. Biol. Chem. 274, 781-786
57. Gentilella, A., and Khalili, K. (2011) BAG3 expression in glioblastoma cells promotes accumulation of ubiquitinated clients in an Hsp70-dependent manner. J. Biol. Chem. 286, 9205-9215
58. Selcen, D., Muntoni, F., Burton, B. K., Pegoraro, E., Sewry, C., Bite, A. V., and Engel, A. G. (2009) Mutation in BAG3 causes severe dominant childhood muscular dystrophy. Ann. Neurol. 65, 83-89
59. Chen, S., Dai, Y., Harada, H., Dent, P., and Grant, S. (2007) Mcl-1 downregulation potentiates ABT-737 lethality by cooperatively inducing Bak activation and Bax translocation. Cancer Res. 67, 782-791 (Pubitemid 46192219)
60. van Delft, M. F., Wei, A. H., Mason, K. D., Vandenberg, C. J., Chen, L., Czabotar, P. E., Willis, S. N., Scott, C. L., Day, C. L., Cory, S., Adams, J. M., Roberts, A. W., and Huang, D. C. (2006) The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/ Bax if Mcl-1 is neutralized. Cancer Cell 10, 389-399 (Pubitemid 44711953)
61. Baou, M., Kohlhaas, S. L., Butterworth, M., Vogler, M., Dinsdale, D., Walewska, R., Majid, A., Eldering, E., Dyer, M. J., and Cohen, G. M. (2010) Role of NOXA and its ubiquitination in proteasome inhibitor-induced apoptosis in chronic lymphocytic leukemia cells. Haematologica 95, 1510-1518
62. Quinn, B. A., Dash, R., Azab, B., Sarkar, S., Das, S. K., Kumar, S., Oyesanya, R. A., Dasgupta, S., Dent, P., Grant, S., Rahmani, M., Curiel, D. T., Dmitriev, I., Hedvat, M., Wei, J., Wu, B., Stebbins, J. L., Reed, J. C., Pellecchia, M., Sarkar, D., and Fisher, P. B. (2011) Targeting Mcl-1 for the therapy of cancer. Expert Opin. Investig. Drugs 20, 1397-1411
63. Beroukhim, R., Mermel, C. H., Porter, D., Wei, G., Raychaudhuri, S., Donovan, J., Barretina, J., Boehm, J. S., Dobson, J., Urashima, M., Mc Henry, K. T., Pinchback, R. M., Ligon, A. H., Cho, Y. J., Haery, L., Greulich, H., Reich, M., Winckler, W., Lawrence, M. S., Weir, B. A., Tanaka, K. E., Chiang, D. Y., Bass, A. J., Loo, A., Hoffman, C., Prensner, J., Liefeld, T., Gao, Q., Yecies, D., Signoretti, S., Maher, E., Kaye, F. J., Sasaki, H., Tepper, J. E., Fletcher, J. A., Tabernero, J., Baselga, J., Tsao, M. S., Demichelis, F., Rubin, M. A., Janne, P. A., Daly, M. J., Nucera, C., Levine, R. L., Ebert, B. L., Gabriel, S., Rustgi, A. K., Antonescu, C. R., Ladanyi, M., Letai, A., Garraway, L. A., Loda, M., Beer, D. G., True, L. D., Okamoto, A., Pomeroy, S. L., Singer, S., Golub, T. R., Lander, E. S., Getz, G., Sellers, W. R., and Meyerson, M. (2010) The landscape of somatic copy-number alteration across human cancers. Nature 463, 899-905
64. Homma, S., Iwasaki, M., Shelton, G. D., Engvall, E., Reed, J. C., and Takayama, S. (2006) BAG3 deficiency results in fulminant myopathy and early lethality. Am. J. Pathol. 169, 761-773 (Pubitemid 44411944)
65. Krajewski, S., Bodrug, S., Krajewska, M., Shabaik, A., Gascoyne, R., Berean, K., and Reed, J. C. (1995) Immunohistochemical analysis of Mcl-1 protein in human tissues. Differential regulation of Mcl-1 and Bcl-2 protein production suggests a unique role for Mcl-1 in control of programmed cell death in vivo. Am. J. Pathol. 146, 1309-1319
66. Luo, J., Solimini, N. L., and Elledge, S. J. (2009) Principles of cancer therapy: Oncogene and non-oncogene addiction. Cell 136, 823-837
67. Dai, C., Whitesell, L., Rogers, A. B., and Lindquist, S. (2007) Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell 130, 1005-1018 (Pubitemid 47410269)
68. Hoang, A. T., Huang, J., Rudra-Ganguly, N., Zheng, J., Powell, W. C., Rabindran, S. K., Wu, C., and Roy-Burman, P. (2000) A novel association between the human heat shock transcription factor 1 (HSF1) and prostate adenocarcinoma. Am. J. Pathol. 156, 857-864 (Pubitemid 30626944)
69. Mendillo, M. L., Santagata, S., Koeva, M., Bell, G. W., Hu, R., Tamimi, R. M., Fraenkel, E., Ince, T. A., Whitesell, L., and Lindquist, S. (2012) HSF1 drives a transcriptional program distinct from heat shock to support highly malignant human cancers. Cell 150, 549-562