Interplay of acetyltransferase EP300 and the proteasome system in regulating heat shock transcription factor 1

Cell

Volumn 156, Issue 5, 2014, Pages 975-985

  Raychaudhuri, Swasti ^a,c   Loew, Christian ^a   Körner, Roman ^a   Pinkert, Stefan ^a   Theis, Mirko ^b   Hayer Hartl, Manajit ^a   Buchholz, Frank ^b   Hartl, F Ulrich ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLTRANSFERASE EP300; ACYLTRANSFERASE; HEAT SHOCK TRANSCRIPTION FACTOR 1; LYSINE; NUCLEAR PROTEIN; PROTEASOME; RNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; E1A ASSOCIATED P300 PROTEIN;

ARTICLE; ATTENUATION; CELL STRESS; CHROMATIN; DRUG SCREENING; FEMALE; HELA CELL; HISTONE ACETYLATION; HUMAN; HUMAN CELL; INTRACELLULAR SPACE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEOMICS; QUALITY CONTROL; RNA INTERFERENCE; ACETYLATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HEAT SHOCK RESPONSE; NUCLEAR LOCALIZATION SIGNAL; PROTEIN AGGREGATION; PROTEIN HOMEOSTASIS; REGULATORY MECHANISM;

ACETYLATION; ANIMALS; CELL NUCLEUS; DNA-BINDING PROTEINS; E1A-ASSOCIATED P300 PROTEIN; HEAT-SHOCK RESPONSE; HEK293 CELLS; HELA CELLS; HUMANS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN FOLDING; PROTEIN INTERACTION MAPS; PROTEOME; TRANSCRIPTION FACTORS;

EID: 84896843332     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.01.055     Document Type: Article

References (60)

1. J. Anckar, and L. Sistonen Regulation of HSF1 function in the heat stress response: implications in aging and disease Annu. Rev. Biochem. 80 2011 1089 1115
2. L. Batista-Nascimento, D.W. Neef, P.C. Liu, C. Rodrigues-Pousada, and D.J. Thiele Deciphering human heat shock transcription factor 1 regulation via post-translational modification in yeast PLoS ONE 6 2011 e15976
3. A. Ben-Zvi, E.A. Miller, and R.I. Morimoto Collapse of proteostasis represents an early molecular event in Caenorhabditis elegans aging Proc. Natl. Acad. Sci. USA 106 2009 14914 14919
4. S. Bharadwaj, A. Ali, and N. Ovsenek Multiple components of the HSP90 chaperone complex function in regulation of heat shock factor 1 In vivo Mol. Cell. Biol. 19 1999 8033 8041
5. G. Biamonti, and J.F. Caceres Cellular stress and RNA splicing Trends Biochem. Sci. 34 2009 146 153
6. G. Biamonti, and C. Vourc'h Nuclear stress bodies Cold Spring Harb. Perspect. Biol. 2 2010 a000695
7. S. Boulon, B.J. Westman, S. Hutten, F.M. Boisvert, and A.I. Lamond The nucleolus under stress Mol. Cell 40 2010 216 227
8. B. Calamini, M.C. Silva, F. Madoux, D.M. Hutt, S. Khanna, M.A. Chalfant, S.A. Saldanha, P. Hodder, B.D. Tait, and D. Garza et al. Small-molecule proteostasis regulators for protein conformational diseases Nat. Chem. Biol. 8 2012 185 196
9. C. Caron, C. Boyault, and S. Khochbin Regulatory cross-talk between lysine acetylation and ubiquitination: role in the control of protein stability Bioessays 27 2005 408 415
10. C. Dai, L. Whitesell, A.B. Rogers, and S. Lindquist Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis Cell 130 2007 1005 1018
11. J. Durieux, S. Wolff, and A. Dillin The cell-non-autonomous nature of electron transport chain-mediated longevity Cell 144 2011 79 91
12. A. Finka, A.F.H. Cuendet, F.J.M. Maathuis, Y. Saidi, and P. Goloubinoff Plasma membrane cyclic nucleotide gated calcium channels control land plant thermal sensing and acquired thermotolerance Plant Cell 24 2012 3333 3348
13. J. Frydman Folding of newly translated proteins in vivo: the role of molecular chaperones Annu. Rev. Biochem. 70 2001 603 647
14. H. Geng, Q. Liu, C. Xue, L.L. David, T.M. Beer, G.V. Thomas, M.S. Dai, and D.Z. Qian HIF1α protein stability is increased by acetylation at lysine 709 J. Biol. Chem. 287 2012 35496 35505
15. T. Gidalevitz, V. Prahlad, and R.I. Morimoto The stress of protein misfolding: from single cells to multicellular organisms Cold Spring Harb. Perspect. Biol. 3 2011 a009704
16. T. Guettouche, F. Boellmann, W.S. Lane, and R. Voellmy Analysis of phosphorylation of human heat shock factor 1 in cells experiencing a stress BMC Biochem. 6 2005 4
17. E. Guisbert, D.M. Czyz, K. Richter, P.D. McMullen, and R.I. Morimoto Identification of a tissue-selective heat shock response regulatory network PLoS Genet. 9 2013 e1003466
18. R. Gupta, P. Kasturi, A. Bracher, C. Loew, M. Zheng, A. Villella, D. Garza, F.U. Hartl, and S. Raychaudhuri Firefly luciferase mutants as sensors of proteome stress Nat. Methods 8 2011 879 884
19. F.U. Hartl, A. Bracher, and M. Hayer-Hartl Molecular chaperones in protein folding and proteostasis Nature 475 2011 324 332
20. V. Hietakangas, J.K. Ahlskog, A.M. Jakobsson, M. Hellesuo, N.M. Sahlberg, C.I. Holmberg, A. Mikhailov, J.J. Palvimo, L. Pirkkala, and L. Sistonen Phosphorylation of serine 303 is a prerequisite for the stress-inducible SUMO modification of heat shock factor 1 Mol. Cell. Biol. 23 2003 2953 2968
21. C.I. Holmberg, V. Hietakangas, A. Mikhailov, J.O. Rantanen, M. Kallio, A. Meinander, J. Hellman, N. Morrice, C. MacKintosh, and R.I. Morimoto et al. Phosphorylation of serine 230 promotes inducible transcriptional activity of heat shock factor 1 EMBO J. 20 2001 3800 3810
22. R. Kittler, A.K. Heninger, K. Franke, B. Habermann, and F. Buchholz Production of endoribonuclease-prepared short interfering RNAs for gene silencing in mammalian cells Nat. Methods 2 2005 779 784
23. R. Kittler, L. Pelletier, A.K. Heninger, M. Slabicki, M. Theis, L. Miroslaw, I. Poser, S. Lawo, H. Grabner, and K. Kozak et al. Genome-scale RNAi profiling of cell division in human tissue culture cells Nat. Cell Biol. 9 2007 1401 1412
24. A. Laemmle, A. Lechleiter, V. Roh, C. Schwarz, S. Portmann, C. Furer, A. Keogh, M.P. Tschan, D. Candinas, S.A. Vorburger, and D. Stroka Inhibition of SIRT1 impairs the accumulation and transcriptional activity of HIF-1α protein under hypoxic conditions PLoS ONE 7 2012 e33433
25. M.L. Mendillo, S. Santagata, M. Koeva, G.W. Bell, R. Hu, R.M. Tamimi, E. Fraenkel, T.A. Ince, L. Whitesell, and S. Lindquist HSF1 drives a transcriptional program distinct from heat shock to support highly malignant human cancers Cell 150 2012 549 562
26. P.A. Mercier, N.A. Winegarden, and J.T. Westwood Human heat shock factor 1 is predominantly a nuclear protein before and after heat stress J. Cell Sci. 112 1999 2765 2774
27. R.I. Morimoto Dynamic remodeling of transcription complexes by molecular chaperones Cell 110 2002 281 284
28. D.W. Neef, A.M. Jaeger, and D.J. Thiele Heat shock transcription factor 1 as a therapeutic target in neurodegenerative diseases Nat. Rev. Drug Discov. 10 2011 930 944
29. S.E. Ong, B. Blagoev, I. Kratchmarova, D.B. Kristensen, H. Steen, A. Pandey, and M. Mann Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics Mol. Cell. Proteomics 1 2002 376 386
30. S.H. Park, Y. Kukushkin, R. Gupta, T. Chen, A. Konagai, M.S. Hipp, M. Hayer-Hartl, and F.U. Hartl PolyQ proteins interfere with nuclear degradation of cytosolic proteins by sequestering the Sis1p chaperone Cell 154 2013 134 145
31. H.R. Pelham A regulatory upstream promoter element in the Drosophila hsp 70 heat-shock gene Cell 30 1982 517 528
32. H.R. Pelham Hsp70 accelerates the recovery of nucleolar morphology after heat shock EMBO J. 3 1984 3095 3100
33. S.J. Petesch, and J.T. Lis Rapid, transcription-independent loss of nucleosomes over a large chromatin domain at Hsp70 loci Cell 134 2008 74 84
34. E.T. Powers, R.I. Morimoto, A. Dillin, J.W. Kelly, and W.E. Balch Biological and chemical approaches to diseases of proteostasis deficiency Annu. Rev. Biochem. 78 2009 959 991
35. V. Prahlad, T. Cornelius, and R.I. Morimoto Regulation of the cellular heat shock response in Caenorhabditis elegans by thermosensory neurons Science 320 2008 811 814
36. R. Raynes, K.M. Pombier, K. Nguyen, J. Brunquell, J.E. Mendez, and S.D. Westerheide The SIRT1 modulators AROS and DBC1 regulate HSF1 activity and the heat shock response PLoS ONE 8 2013 e54364
37. K. Richter, M. Haslbeck, and J. Buchner The heat shock response: life on the verge of death Mol. Cell 40 2010 253 266
38. S.J. Russell, K.A. Steger, and S.A. Johnston Subcellular localization, stoichiometry, and protein levels of 26 S proteasome subunits in yeast J. Biol. Chem. 274 1999 21943 21952
39. A.H. Saad, and G.M. Hahn Activation of potassium channels: relationship to the heat shock response Proc. Natl. Acad. Sci. USA 89 1992 9396 9399
40. S. Santagata, M.L. Mendillo, Y.C. Tang, A. Subramanian, C.C. Perley, S.P. Roche, B. Wong, R. Narayan, H. Kwon, and M. Koeva et al. Tight coordination of protein translation and HSF1 activation supports the anabolic malignant state Science 341 2013 1238303
41. K.D. Sarge, S.P. Murphy, and R.I. Morimoto Activation of heat shock gene transcription by heat shock factor 1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress Mol. Cell. Biol. 13 1993 1392 1407
42. Y. Shi, D.D. Mosser, and R.I. Morimoto Molecular chaperones as HSF1-specific transcriptional repressors Genes Dev. 12 1998 654 666
43. P. van Oosten-Hawle, R.S. Porter, and R.I. Morimoto Regulation of organismal proteostasis by transcellular chaperone signaling Cell 153 2013 1366 1378
44. S.D. Westerheide, J. Anckar, S.M. Stevens Jr.; L. Sistonen, and R.I. Morimoto Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1 Science 323 2009 1063 1066
45. J. Zou, Y. Guo, T. Guettouche, D.F. Smith, and R. Voellmy Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1 Cell 94 1998 471 480
46. N.F. Bence, R.M. Sampat, and R.R. Kopito Impairment of the ubiquitin-proteasome system by protein aggregation Science 292 2001 1552 1555
47. F.M. Boisvert, Y.W. Lam, D. Lamont, and A.I. Lamond A quantitative proteomics analysis of subcellular proteome localization and changes induced by DNA damage Mol. Cell. Proteomics 9 2010 457 470
48. M. Boutros, A.A. Kiger, S. Armknecht, K. Kerr, M. Hild, B. Koch, S.A. Haas, R. Paro, N. Perrimon Heidelberg Fly Array Consortium Genome-wide RNAi analysis of growth and viability in Drosophila cells Science 303 2004 832 835
49. A. Brunet, L.B. Sweeney, J.F. Sturgill, K.F. Chua, P.L. Greer, Y. Lin, H. Tran, S.E. Ross, R. Mostoslavsky, and H.Y. Cohen et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase Science 303 2004 2011 2015
50. A. Chatr-Aryamontri, B.J. Breitkreutz, S. Heinicke, L. Boucher, A. Winter, C. Stark, J. Nixon, L. Ramage, N. Kolas, and L. O'Donnell et al. The BioGRID interaction database: 2013 update Nucleic Acids Res. 41 Database issue 2013 D816 D823
51. U. Knauf, E.M. Newton, J. Kyriakis, and R.E. Kingston Repression of human heat shock factor 1 activity at control temperature by phosphorylation Genes Dev. 10 1996 2782 2793
52. H.T. Ma, and R.Y. Poon Synchronization of HeLa cells Methods Mol. Biol. 761 2011 151 161
53. E. Makareeva, N.A. Aviles, and S. Leikin Chaperoning osteogenesis: new protein-folding disease paradigms Trends Cell Biol. 21 2011 168 176
54. N. Malo, J.A. Hanley, S. Cerquozzi, J. Pelletier, and R. Nadon Statistical practice in high-throughput screening data analysis Nat. Biotechnol. 24 2006 167 175
55. T. Mosmann Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays J. Immunol. Methods 65 1983 55 63
56. S.E. Ong, and M. Mann A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC) Nat. Protoc. 1 2006 2650 2660
57. J. Rappsilber, Y. Ishihama, and M. Mann Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics Anal. Chem. 75 2003 663 670
58. A. Shevchenko, M. Wilm, O. Vorm, and M. Mann Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels Anal. Chem. 68 1996 850 858
59. J.R. Wiśniewski, A. Zougman, N. Nagaraj, and M. Mann Universal sample preparation method for proteome analysis Nat. Methods 6 2009 359 362
60. J.A. Young, D. Sermwittayawong, H.J. Kim, S. Nandu, N. An, H. Erdjument-Bromage, P. Tempst, L. Coscoy, and A. Winoto Fas-associated death domain (FADD) and the E3 ubiquitin-protein ligase TRIM21 interact to negatively regulate virus-induced interferon production J. Biol. Chem. 286 2011 6521 6531