New inhibitor targeting human transcription factor HSF1: Effects on the heat shock response and tumor cell survival

Nucleic Acids Research

Volumn 45, Issue 10, 2017, Pages 5797-5817

  Vilaboa, Nuria ^a,b   Boré, Alba ^a,b   Martin Saavedra, Francisco ^a,b   Bayford, Melanie ^c   Winfield, Natalie ^c   Firth Clark, Stuart ^c   Kirton, Stewart B ^d   Voellmy, Richard ^e  

^a HOSPITAL UNIVERSITARIO LA PAZ IDIPAZ   (Spain)

^b BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^c Domainex Ltd   (United Kingdom)

^d UNIVERSITY OF HERTFORDSHIRE   (United Kingdom)

^e HSF Pharmaceuticals SA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

COMPOUND 115; DNA; HEAT SHOCK TRANSCRIPTION FACTOR 1; PROTEIN INHIBITOR; SHORT HAIRPIN RNA; TRANSCRIPTOME; UNCLASSIFIED DRUG; ACRYLAMIDE DERIVATIVE; ACTIVATING TRANSCRIPTION FACTOR 1; ANTINEOPLASTIC AGENT; ATF1 PROTEIN, HUMAN; DNA BINDING PROTEIN; HEAT SHOCK TRANSCRIPTION FACTOR; I(HSF)115 COMPOUND; LIGAND; MOLECULAR LIBRARY; PROTEIN BINDING; THIAZOLE DERIVATIVE; TRANSCRIPTION FACTOR;

ARTICLE; CANCER CELL CULTURE; CANCER CELL LINE; CELL ISOLATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DRUG DNA BINDING; DRUG TARGETING; FLOW CYTOMETRY; GENE EXPRESSION; GENE REPRESSION; GENETIC TRANSFECTION; HEAT SHOCK RESPONSE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MICROARRAY ANALYSIS; NUCLEAR LOCALIZATION SIGNAL; OLIGOMERIZATION; PLASMID; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN PURIFICATION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STRUCTURE ACTIVITY RELATION; SURFACE PLASMON RESONANCE; TUMOR CELL; A-549 CELL LINE; ANTAGONISTS AND INHIBITORS; BINDING SITE; CELL LINE; CHEMISTRY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HEAT; HELA CELL LINE; HEP-G2 CELL LINE; HIGH THROUGHPUT SCREENING; METABOLISM; MOLECULAR DOCKING; MOLECULAR LIBRARY; PHARMACOLOGY; PROTEIN DOMAIN; STRUCTURAL HOMOLOGY; TUMOR CELL LINE;

A549 CELLS; ACRYLAMIDES; ACTIVATING TRANSCRIPTION FACTOR 1; ANTINEOPLASTIC AGENTS; BINDING SITES; CELL LINE; CELL LINE, TUMOR; CELL SURVIVAL; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, NEOPLASTIC; HEAT-SHOCK RESPONSE; HELA CELLS; HEP G2 CELLS; HIGH-THROUGHPUT SCREENING ASSAYS; HOT TEMPERATURE; HUMANS; LIGANDS; MOLECULAR DOCKING SIMULATION; PROTEIN BINDING; PROTEIN DOMAINS; SMALL MOLECULE LIBRARIES; STRUCTURAL HOMOLOGY, PROTEIN; STRUCTURE-ACTIVITY RELATIONSHIP; THIAZOLES; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

EID: 85021359678     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkx194     Document Type: Article

References (65)

1. Richter, K., Haslbeck, M. and Buchner, J. (2010) The heat shock response: Life on the verge of death. Mol. Cell, 40, 253-266.
2. Hartl, F.U., Bracher, A. and Hayer-Hartl, M. (2011) Molecular chaperones in protein folding and proteostasis. Nature, 475, 324-332.
3. Ananthan, J., Goldberg, A.L. and Voellmy, R. (1986) Abnormal proteins serve as eukaryotic stress signals and trigger the activation of heat shock genes. Science, 232, 522-524.
4. Hightower, L.E. (1980) Cultured animal cells exposed to amino acid analogues or puromycin rapidly synthesize several polypeptides. J. Cell. Physiol., 102, 407-427.
5. McMillan, D.R., Xiao, X., Shao, L., Graves, K. and Benjamin, I.J. (1998) Targeted disruption of heat shock transcription factor 1 abolishes thermotolerance and protection against heat-inducible apoptosis. J. Biol. Chem., 273, 7523-7528.
6. Akerfelt, M., Morimoto, R.I. and Sistonen, L. (2010) Heat shock factors: Integrators of cell stress, development and life span. Nat. Rev. Mol. Cell Biol., 11, 545-555.
7. Zou, J., Guo, Y., Guettouche, T., Smith, D.O. and Voellmy, R. (1998) Repression of heat shock transcription factor HSF1 by Hsp90 (Hsp90 complex) that forms a stress-sensitive complex with HSF1. Cell, 94, 471-480.
8. Ali, A., Bharadwaj, S., O'Carroll, R. and Ovsenek, N. (1998) Hsp90 interacts with and regulates the activity of heat shock factor 1 in Xenopus oocytes. Mol. Cell. Biol., 18, 4949-4960.
9. Duina, A.A., Kalton, H.M. and Gaber, R.F. (1998) Requirement for Hsp90 and a Cyp-40-type cyclophilin in negative regulation of the heat shock response. J. Biol. Chem., 273, 18974-18978.
10. Voellmy, R. and Boellmann, F. (2007) Chaperone regulation of the heat shock protein response. Adv. Exp. Med. Biol., 594, 89-99.
11. Dai, Q., Zhang, C., Wu, Y., McDonough, H., Whaley, R.A., Godfrey, V., Li, H.H., Madamanchi, N., Xu, W., Neckers, L. et al. (2003) CHIP activates HSF1 and confers protection against apoptosis and cellular stress. EMBO J., 22, 5446-5458.
12. Boyault, C., Zhang, Y., Fritah, S., Caron, C., Gilquin, B., Kwon, S.H., Garrido, C., Yao, T-P., Vourc'h, C., Matthias, P. et al. (2007) HDAC6 controls major cell response pathways to cytotoxic accumulation of protein aggregates. Genes Dev., 21, 2172-2181.
13. Pernet, L., Faure, V., Gilquin, B., Dufour-Guérin, S., Khochbin, S. and Vourc'h, C. (2014) HDAC6-ubiquitin interaction controls the duration of HSF1 activation after heat shock. Mol. Biol. Cell, 25, 4187-4194.
14. Boellmann, F., Guettouche, T., Guo, Y., Fenna, M., Mnayer, L. and Voellmy, R. (2004) DAXX interacts with heat shock factor 1during stress activation and enhances its transcriptional activity. Proc. Natl. Acad. Sci. U.S.A.., 101, 4100-4105.
15. Wang, X.Z., Grammatikakis, N., Siganou, A., Stevenson, M.A. and Calderwood, S.K. (2004) Interactions between extracellular signal-regulated protein kinase 1, 14-3-3e, and heat shock factor 1 during stress. J. Biol. Chem., 279, 49460-49469.
16. Hu, Y. and Mivechi, N.F. (2011) Promotion of heat shock factor Hsf1 degradation via adaptor protein filamin A-interacting protein 1-like (FILIP-1L). J. Biol. Chem., 286, 31397-31408.
17. Satyal, S.H., Chen, D., Fox, S.G., Kramer, J.M. and Morimoto, R.I. (1998) Negative regulation of the heat shock transcriptional response by HSBP1. Genes Dev., 12, 1962-1974.
18. Fujimoto, M., Takaki, E., Takii, R., Tan, K., Prakasam, R., Hayashida, N., Iemura, S.-I., Natsume, T. and Nakai, A. (2012) RPA assists HSF1 access to nucleosomal DNA by recruiting histone chaperone FACT. Mol. Cell, 48, 182-194.
19. Takii, R., Fujimoto, M., Tan, K., Takaki, E., Hayashida, N., Nakato, R., Shirahige, K. and Nakai, A. (2015) ATF1 modulates the heat shock response by regulating the stress-inducible heat shock factor 1 transcription complex. Mol. Cell. Biol., 35, 11-25.
20. Rabindran, S.K., Haroun, R.I., Clos, J., Wisniewski, J. and Wu, C. (1993) Regulation of heat shock factor trimer formation: Role of a conserved leucine zipper. Science, 259, 230-234.
21. Guo, Y., Guettouche, T., Fenna, M., Boellmann, F., Pratt, W.B., Toft, D.O., Smith, D.F. and Voellmy, R. (2001) Evidence for a mechanism of repression of heat shock factor 1 transcriptional activity by a multichaperone complex. J. Biol. Chem., 276, 45791-45799.
22. Shi, Y., Mosser, D.D. and Morimoto, R.I. (1998) Molecular chaperones as HSF1-specific transcriptional repressors. Genes Dev., 12, 654-666.
23. Guettouche, T., Boellmann, F., Lane, W.S. and Voellmy, R. (2005) Analysis of phosphorylation of human heat shock factor 1 in severely heat-stressed cells. BMC Biochem., 6, 4.
24. Chou, S.-D., Prince, T., Gong, J. and Calderwood, S.K. (2012) mTOR is essential for the proteotoxic stress response, HSF1 activation and heat shock protein synthesis. PLoS One, 7, e39679.
25. Hietakangas, V., Ahlskog, J.K., Jakobsson, A.M., Hellesuo, M., Sahlberg, N.M., Holmberg, C.I., Mikhailov, A., Palvimo, J.J., Pirkkala, L. and Sistonen, L. (2003) Phosphorylation of serine 303 is a prerequisite for the stress-inducible SUMO modification of heat shock factor 1. Mol. Cell. Biol., 23, 2953-2968.
26. Raychaudhuri, S., Loew, C., Körner, R., Pinkert, S., Theis, M., Hayer-Hartl, M., Buchholz, F. and Hartl, F.U. (2014) Interplay of acetyltransferase EP300 and the proteasome system in regulating heat shock transcription factor 1. Cell, 156, 975-985.
27. Westerheide, S.D., Anckar, J., Stevens, S.M. Jr, Sistonen, L and Morimoto, R.I. (2009) Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science, 323, 1063-1066.
28. Trinklein, N.D., Murray, J.I., Hartman, S.J., Botstein, D. and Myers, R.M. (2004) The role of heat shock transcription factor 1 in the genome-wide regulation of the mammalian heat shock response. Mol. Biol. Cell, 15, 1254-1261.
29. Page, T.J., Sikder, D., Yang, L., Pluta, L., Wolfinger, R.D., Kodadek, T. and Thomas, R.S. (2006) Genome-wide analysis of human HSF1 signaling reveals a transcriptional program linked to cellular adaptation and survival. Mol. Biosyst., 2, 627-639.
30. 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.
31. 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.
32. Zhao, Y.H., Zhou, M., Liu, H., Ding, Y., Khong, H.T., Yu, D., Fodstad, O. and Tan, M. (2009) Upregulation of lactate dehydrogenase A by ErbB2 through heat shock factor 1 promotes breast cancer cell glycolysis and growth. Oncogene, 28, 3689-3701.
33. Ciocca, D.R., Arrigo, A.P. and Calderwood, S.K. (2013) Heat shock proteins and heat shock factor 1 in carcinogenesis and tumor development: An update. Arch. Toxicol., 87, 19-48.
34. Khaleque, M.A., Bharti, A., Sawyer, D., Gong, J., Benjamin, I.J., Stevenson, M.A. and Calderwood, S.K. (2005) Induction of heat shock proteins by heregulin β1 leads to protection from apoptosis and anchorage-independent growth. Oncogene, 24, 6564-6573.
35. Nakamura, Y., Fujimoto, M., Hayashida, N., Takii, R., Nakai, A. and Muto, M. (2010) Silencing HSF1 by short hairpin RNA decreases cell proliferation and enhances sensitivity to hyperthermia in human melanoma cell lines. J. Derm. Sci., 60, 187-192.
36. Meng, L., Gabai, V.L. and Sherman, M.Y. (2010) Heat-shock transcription factor HSF1 has a critical role in human epidermal growth factor receptor-2-induced cellular transformation and tumorigenesis. Oncogene, 29, 5204-5213.
37. Gabai, V.L., Meng, L., Kim, G., Mills, T.A., Benjamin, I.J. and Sherman, M.Y. (2012) Heat shock transcription factor Hsf1 is involved in tumor progression via regulation of hypoxia-inducible factor 1 and RNA-binding protein HuR. Mol. Cell. Biol., 32, 929-940.
38. Santagata, S., Hu, R., Lin, N.U., Mendillo, M.L., Collins, L.C., Hankinso, S.E., Schnitt, S.J., Whitesell, L., Tamimi, R.M., Lindquist, S. et al. (2011) High levels of nuclear heat-shock factor 1 (HSF1) are associated with poor prognosis in breast cancer. Proc. Natl. Acad. Sci. U.S.A., 108, 18378-18383.
39. Yoon, Y.J., Kim, J.A., Shin, K.D., Shin, D.-S., Han, Y.M., Lee, Y.J., Lee, J.S., Kwon, B.-M. and Han, D.C. (2011) KRIBB11 inhibits Hsp70 synthesis through inhibition of heat shock factor 1 function by impairing the recruitment of positive transcription elongation factor b to the hsp70 promoter. J. Biol. Chem., 286, 1737-1747.
40. Yoon, S.J., Lee, S.W., Kim, N.D., Park, Y.K., Lee, G.H., Kim, J.W., Park, S.J., Park, H.J. and Shin, D.H. (2001) Novel 3-nitropyridine derivatives and the pharmaceutical composition containing said derivatives. International Patent Application Publication WO 01/38306, May 31 2001.
41. Salamanca, H.H., Antonyak, M.A., Cerione, R.A., Shi, H. and Lis, J.T. (2014) Inhibiting heat shock factor 1 in human cancer cells with a potent RNA aptamer. PLoS One, 9, e96330.
42. Vilaboa, N., Fenna, M., Munson, J., Roberts, S.M. and Voellmy, R. (2005) Novel gene switches for targeted and timed expression of proteins of interest. Mol. Ther., 12, 290-298.
43. Zuo, J., Baler, R., Dahl, G. and Voellmy, R. (1994) Activation of the DNA-binding ability of human heat shock transcription factor 1 may involve the transition from an intramolecular to an intermolecular triple-stranded coiled-coil structure. Mol. Cell. Biol., 14, 7557-7568.
44. Zuo, J., Rungger, D. and Voellmy, R. (1995) Multiple layers of regulation of human heat shock transcription factor 1. Mol. Cell. Biol., 15, 4319-4330.
45. Loughran, S.T., Loughran, N.B., Ryan, B.J., D'Souza, B.N. and Walls, D. (2006) Modified His-tag fusion vector for enhanced protein purification by immobilized metal affinity chromatography. Anal. Biochem., 355, 148-150.
46. Goldenberg, C.J., Luo, Y., Fenna, M., Baler, R., Weinmann, R. and Voellmy, R. (1988) Purified human factor activates heat shock promoter in a HeLa cell-free transcription system. J. Biol. Chem., 263, 19734-19739.
47. Vilaboa, N.E., Calle, C., Pérez, C., De Blas, E., García-Bermejo, L. and Aller, P. (1995) cAMP increasing agents prevent the stimulation of heat-shock protein 70 (HSP70) gene expression by cadmium chloride in human myeloid cell lines. J. Cell Sci., 108, 2877-2893.
48. Huang, D.W., Sherman, B.T. and Lempicki, R.A. (2009) Systematic and integrative analysis of large gene lists using David bioinformatics resources. Nat. Protoc., 4, 44-57.
49. Ritchie, M.E., Phipson, B., Wu, D., Hu, Y., Law, C.W., Shi, W. and Smyth, G.K. (2015) limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res., 43, e47.
50. Mahalingam, P., Takrouri, K., Chen, T., Sahoo, R., Papadopoulos, E., Chen, L., Wagner, G., Aktas, B.H., Halperin, J.A. and Chorev, M. (2014) Synthesis of rigidified eIF4E/eIF4G inhibitor-1 (4EGI-1) mimetic and their in vitro characterization as inhibitors of protein-protein interaction. J. Med. Chem., 57, 5094-5111.
51. Jones, G., Willet, P. and Glenh, R.C. (1995) Molecular recognition of receptor sites using a genetic algorithm with a description of desolvation. J. Mol. Biol., 245, 43-53.
52. Mahat, D.B., Salamanca, H.H., Duarte, F.M., Danko, C.G. and Lis, J.T. (2016) Mammalian heat shock response and mechanisms underlying its genome-wide transcriptional regulation. Mol. Cell, 62, 63-78.
53. Vihervaara, A., Sergelius, C., Vasara, J., Blom, M.A., Elsing, A.N., Roos-Mattjus, P. and Sistonen, L. (2013) Transcriptional response to stress in the dynamic chromatin environment of cyclin and mitotic cells. Proc. Natl. Acad. Sci. U.S.A., 110, E3388-E3397.
54. Sandqvist, A., Björk, J.K., Akerfelt, M., Chitikova, Z., Frichine, A., Vourc'h, C., Jolly, C., Salminen, T.A., Nymalm, Y. and Sistonen, L. (2009) Heterotrimerization of heat shock factors 1 and 2 provides a transcriptional switch in response to distinct stimuli. Mol. Biol. Cell, 20, 1340-1347.
55. He, H., Soncin, F., Grammatikakis, N., Li, Y., Siganou, A., Gong, J., Brown, S.A., Kingston, R.E. and Calderwood, S.K. (2003) Elevated expression of heat shock factor (HSF) 2A stimulates HSF1-induced transcription during stress. J. Biol. Chem., 278, 35465-35475.
56. Oestling, P., Björk, J.K., Roos-Mattjus, P., Mezger, V. and Sistonen, L. (2007) Heat shock factor 2 (HSF2) contributes to inducible expression of hsp genes through interplay with HSF1. J. Biol. Chem., 282, 7077-7086.
57. Logan, I.R., McNeil, H.V., Cook, S., Lu, X., Meek, D.W., Fuller-Pace, F.V., Lunec, J. and Robson, C.N. (2009) Heat shock factor-1 modulates p53 activity in the transcriptional response to DNA damage. Nucleic Acids Res., 37, 2962-2971.
58. Hideshima, T., Richardsom, P., Chaudhan, D., Palombella, V.J., Elliott, P.J., Adams, J. and Anderson, K.C. (2001) The proteasome inhibitor PS-341 inhibits growth, induces apoptosis and overcomes drug resistance in human multiple myeloma cells. Cancer Res., 61, 3071-3076.
59. Darnell, J.E. Jr (2002) Transcription factors as targets for cancer therapy. Nat. Rev. Cancer, 2, 740-749.
60. Vazquez, A., Bond, E.E., Levine, A.J. and Bond, G.L. (2008) The genetics of the p53 pathway, apoptosis and cancer. Nat. Rev. Drug Discov., 7, 979-987.
61. Zhao, Y., Bernard, D. andWang, S. (2013) Small molecule inhibitors of MDM2-p53 and MDMX-p53 interactions as new cancer therapeutics. Biodiscovery, 8, 4.
62. Westwood, J.T., Clos, J. and Wu, C. (1991). Stress-induced oligomerization and chromosomal relocalization of heat-shock factor. Nature, 353, 822-827.
63. Guertin, M.J. and Lis, J.T. (2010). Chromatin landscape dictates HSF binding to target DNA elements. PLoS Genet., 6, e1001114.
64. Neudegger, T., Verghese, J., Hayer-Hartl, M., Hartl, F.U. and Bracher, A. (2016) Structure of human heat-shock transcription factor 1 in complex with DNA. Nat. Struct. Mol. Biol., 23, 140-146.
65. Jaeger, A.M., Pemble, C.W., Sistonen, L. and Thiele, D.J. (2016) Structures of HSF2 reveal mechanisms for differential regulation of human heat-shock factors. Nat. Struct. Mol. Biol., 23, 147-154.