Characterizing the altered cellular proteome induced by the stress-independent activation of heat shock factor 1

ACS Chemical Biology

Volumn 9, Issue 6, 2014, Pages 1273-1283

  Ryno, Lisa M ^a   Genereux, Joseph C ^a   Naito, Tadasuke ^b   Morimoto, Richard I ^b   Powers, Evan T ^a   Shoulders, Matthew D ^a,c   Wiseman, R Luke ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; DOXYCYCLINE; HEAT SHOCK PROTEIN 22; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 40; HEAT SHOCK TRANSCRIPTION FACTOR 1; MESSENGER RNA; PROTEOME; SMALL HEAT SHOCK PROTEIN; BIOLOGICAL MARKER; DNA BINDING PROTEIN; HEAT SHOCK TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR;

ARTICLE; CELL STRESS; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; GENE EXPRESSION; HEAT SHOCK RESPONSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN HOMEOSTASIS; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEOMICS; STEADY STATE; TRANSCRIPTION INITIATION; UNFOLDED PROTEIN RESPONSE; GENE REGULATORY NETWORK; GENETICS; HEK293 CELL LINE; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN GENOME; LIQUID CHROMATOGRAPHY; METABOLISM; PHYSIOLOGICAL STRESS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING;

BIOMARKERS; BLOTTING, WESTERN; CHROMATOGRAPHY, LIQUID; DNA-BINDING PROTEINS; GENE REGULATORY NETWORKS; GENOME, HUMAN; HEK293 CELLS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; PROTEOME; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STRESS, PHYSIOLOGICAL; TANDEM MASS SPECTROMETRY; TRANSCRIPTION FACTORS;

EID: 84903166300     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb500062n     Document Type: Article

References (48)

1. Calamini, B. and Morimoto, R. I. (2012) Protein homeostasis as a therapeutic target for diseases of protein conformation Curr. Top. Med. Chem. 12, 2623-2640
2. Powers, E. T., Morimoto, R. I., Dillin, A., Kelly, J. W., and Balch, W. E. (2009) Biological and chemical approaches to diseases of proteostasis deficiency Annu. Rev. Biochem. 78, 959-991
3. Anckar, J. and Sistonen, L. (2011) Regulation of HSF1 function in the heat stress response: implications in aging and disease Annu. Rev. Biochem. 80, 1089-1115
4. Akerfelt, M., Morimoto, R. I., and Sistonen, L. (2010) Heat shock factors: integrators of cell stress, development and lifespan Nat. Rev. Mol. Cell Biol. 11, 545-555
5. Raychaudhuri, S., Loew, C., Korner, 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
6. 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
7. 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 (Pubitemid 44772306)
8. 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 (Pubitemid 38316232)
9. de Billy, E., Powers, M. V., Smith, J. R., and Workman, P. (2009) Drugging the heat shock factor 1 pathway: exploitation of the critical cancer cell dependence on the guardian of the proteome Cell Cycle 8, 3806-3808
10. Gestwicki, J. E. and Garza, D. (2012) Protein quality control in neurodegenerative disease Prog. Mol. Biol. Transl. Sci. 107, 327-353
11. Whitesell, L. and Lindquist, S. (2009) Inhibiting the transcription factor HSF1 as an anticancer strategy Expert Opin. Ther. Targets 13, 469-478
12. Westerheide, S. D. and Morimoto, R. I. (2005) Heat shock response modulators as therapeutic tools for diseases of protein conformation J. Biol. Chem. 280, 33097-33100 (Pubitemid 41397104)
13. Fujimoto, M., Takaki, E., Hayashi, T., Kitaura, Y., Tanaka, Y., Inouye, S., and Nakai, A. (2005) Active HSF1 significantly suppresses polyglutamine aggregate formation in cellular and mouse models J. Biol. Chem. 280, 34908-34916 (Pubitemid 41504625)
14. Krobitsch, S. and Lindquist, S. (2000) Aggregation of huntingtin in yeast varies with the length of the polyglutamine expansion and the expression of chaperone proteins Proc. Natl. Acad. Sci. U.S.A. 97, 1589-1594 (Pubitemid 30118486)
15. Cohen, A., Ross, L., Nachman, I., and Bar-Nun, S. (2012) Aggregation of polyQ proteins is increased upon yeast aging and affected by Sir2 and Hsf1: novel quantitative biochemical and microscopic assays PLoS One 7, e44785
16. Chafekar, S. M. and Duennwald, M. L. (2012) Impaired heat shock response in cells expressing full-length polyglutamine-expanded huntingtin, PLoS One, 7, DOI: 10.1371/journal.pone.0037929.
17. Pierce, A., Podlutskaya, N., Halloran, J. J., Hussong, S. A., Lin, P. Y., Burbank, R., Hart, M. J., and Galvan, V. (2013) Over-expression of heat shock factor 1 phenocopies the effect of chronic inhibition of TOR by rapamycin and is sufficient to ameliorate Alzheimer's-like deficits in mice modeling the disease J. Neurochem. 124, 880-893
18. Scheper, W., Nijholt, D. A., and Hoozemans, J. J. (2011) The unfolded protein response and proteostasis in Alzheimer disease: preferential activation of autophagy by endoplasmic reticulum stress Autophagy 7, 910-911
19. Hartl, F. U., Bracher, A., and Hayer-Hartl, M. (2011) Molecular chaperones in protein folding and proteostasis Nature 475, 324-332
20. Cohen, E. (2012) Aging, protein aggregation, chaperones, and neurodegenerative disorders: mechanisms of coupling and therapeutic opportunities Rambam Maimonides Med. J. 3, e0021
21. Neef, D. W., Turski, M. L., and Thiele, D. J. (2010) Modulation of heat shock transcription factor 1 as a therapeutic target for small molecule intervention in neurodegenerative disease PLoS Biol. 8, e1000291
22. Calamini, B., Silva, M. C., Madoux, F., Hutt, D. M., Khanna, S., Chalfant, M. A., Saldanha, S. A., Hodder, P., Tait, B. D., Garza, D., Balch, W. E., and Morimoto, R. I. (2012) Small-molecule proteostasis regulators for protein conformational diseases Nat. Chem. Biol. 8, 185-196
23. Zhang, B., Au, Q., Yoon, I. S., Tremblay, M. H., Yip, G., Zhou, Y., Barber, J. R., and Ng, S. C. (2009) Identification of small-molecule HSF1 amplifiers by high content screening in protection of cells from stress induced injury Biochem. Biophys. Res. Commun. 390, 925-930
24. Bersuker, K., Hipp, M. S., Calamini, B., Morimoto, R. I., and Kopito, R. R. (2013) Heat shock response activation exacerbates inclusion body formation in a cellular model of Huntington disease J. Biol. Chem. 288, 23633-23638
25. Wu, L., Hu, C., Huang, M., Jiang, M., Lu, L., and Tang, J. (2013) Heat shock transcription factor 1 attenuates TNFalpha-induced cardiomyocyte death through suppression of NFkappaB pathway Gene 527, 89-94
26. Jolly, C. and Morimoto, R. I. (2000) Role of the heat shock response and molecular chaperones in oncogenesis and cell death J. Natl. Cancer Inst. 92, 1564-1572
27. Shoulders, M. D., Ryno, L. M., Cooley, C. B., Kelly, J. W., and Wiseman, R. L. (2013) Broadly applicable methodology for the rapid and dosable small molecule-mediated regulation of transcription factors in human cells J. Am. Chem. Soc. 135, 8129-8132
28. Shalgi, R., Hurt, J. A., Krykbaeva, I., Taipale, M., Lindquist, S., and Burge, C. B. (2013) Widespread regulation of translation by elongation pausing in heat shock Mol. Cell 49, 439-452
29. Vabulas, R. M., Raychaudhuri, S., Hayer-Hartl, M., and Hartl, F. U. (2010) Protein folding in the cytoplasm and the heat shock response Cold Spring Harbor Perspect. Biol. 2, a004390
30. Shoulders, M. D., Ryno, L. M., Genereux, J. C., Moresco, J. J., Tu, P. G., Wu, C., Yates, J. R., III., Su, A. I., Kelly, J. W., and Wiseman, R. L. (2013) Stress-independent activation of XBP1s and/or ATF6 reveals three functionally diverse ER proteostasis environments Cell Rep. 3, 1279-1292
31. Aldridge, J. E., Horibe, T., and Hoogenraad, N. J. (2007) Discovery of genes activated by the mitochondrial unfolded protein response (mtUPR) and cognate promoter elements PLoS One 2, e874
32. Kampinga, H. H. and Garrido, C. (2012) HSPBs: small proteins with big implications in human disease Int. J. Biochem. Cell Biol. 44, 1706-1710
33. Hageman, J., van Waarde, M. A. W. H., Zylicz, A., Walerych, D., and Kampinga, H. H. (2011) The diverse members of the mammalian HSP70 machine show distinct chaperone-like activities Biochem. J. 435, 127-142
34. Kampinga, H. H. and Craig, E. A. (2010) The HSP70 chaperone machinery: J proteins as drivers of functional specificity Nat. Rev. Mol. Cell Biol. 11, 579-592
35. Pratt, W. B., Morishima, Y., Peng, H. M., and Osawa, Y. (2010) Proposal for a role of the Hsp90/Hsp70-based chaperone machinery in making triage decisions when proteins undergo oxidative and toxic damage Exp Biol. Med. (Maywood, NJ, U.S.) 235, 278-289
36. Young, J. C., Agashe, V. R., Siegers, K., and Hartl, F. U. (2004) Pathways of chaperone-mediated protein folding in the cytosol Nat. Rev. Mol. Cell Biol. 5, 781-791 (Pubitemid 39336272)
37. Park, S. H., Kukushkin, Y., Gupta, R., Chen, T., Konagai, A., Hipp, M. S., Hayer-Hartl, M., and Hartl, F. U. (2013) PolyQ proteins interfere with nuclear degradation of cytosolic proteins by sequestering the Sis1p chaperone Cell 154, 134-145
38. Borges, J. C., Seraphim, T. V., Mokry, D. Z., Almeida, F. C., Cyr, D. M., and Ramos, C. H. (2012) Identification of regions involved in substrate binding and dimer stabilization within the central domains of yeast Hsp40 Sis1 PLoS One 7, e50927
39. Rauniyar, N., Gao, B., McClatchy, D. B., and Yates, J. R., III. (2013) Comparison of protein expression ratios observed by sixplex and duplex TMT labeling method J. Proteome Res. 12, 1031-1039
40. Washburn, M. P., Ulaszek, R., Deciu, C., Schieltz, D. M., and Yates, J. R., III. (2002) Analysis of quantitative proteomic data generated via multidimensional protein identification technology Anal. Chem. 74, 1650-1657 (Pubitemid 34297605)
41. Washburn, M. P., Ulaszek, R. R., and Yates, J. R., III. (2003) Reproducibility of quantitative proteomic analyses of complex biological mixtures by multidimensional protein identification technology Anal. Chem. 75, 5054-5061 (Pubitemid 37238557)
42. Kim, Y. H., Park, E. J., Han, S. T., Park, J. W., and Kwon, T. K. (2005) Arsenic trioxide induces Hsp70 expression via reactive oxygen species and JNK pathway in MDA231 cells Life Sci. 77, 2783-2793 (Pubitemid 41297864)
43. 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 (Pubitemid 28152777)
44. Song, X., Chen, Z., Wu, C., and Zhao, S. (2010) Abrogating HSP response augments cell death induced by As2O3 in glioma cell lines Can. J. Neurol. Sci. 37, 504-511
45. Gidalevitz, T., Ben-Zvi, A., Ho, K. H., Brignull, H. R., and Morimoto, R. I. (2006) Progressive disruption of cellular protein folding in models of polyglutamine diseases Science 311, 1471-1474 (Pubitemid 43376703)
46. Sittler, A., Lurz, R., Lueder, G., Priller, J., Lehrach, H., Hayer-Hartl, M. K., Hartl, F. U., and Wanker, E. E. (2001) Geldanamycin activates a heat shock response and inhibits huntingtin aggregation in a cell culture model of Huntington's disease Hum. Mol. Genet. 10, 1307-1315 (Pubitemid 32600484)
47. Neef, D. W., Jaeger, A. M., and Thiele, D. J. (2011) Heat shock transcription factor 1 as a therapeutic target in neurodegenerative diseases Nat. Rev. Drug Discovery 10, 930-944
48. Kim, S., Nollen, E. A., Kitagawa, K., Bindokas, V. P., and Morimoto, R. I. (2002) Polyglutamine protein aggregates are dynamic Nat. Cell Biol. 4, 826-831