Mammalian Heat Shock Response and Mechanisms Underlying Its Genome-wide Transcriptional Regulation

Molecular Cell

Volumn 62, Issue 1, 2016, Pages 63-78

  Mahat, Dig B ^a   Salamanca, H Hans ^a,b   Duarte, Fabiana M ^a   Danko, Charles G ^a   Lis, John T ^a  

^a Department of Molecular Biology and Genetics   (United States)

^b State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CYTOSKELETON PROTEIN; HEAT SHOCK TRANSCRIPTION FACTOR 1; HEAT SHOCK TRANSCRIPTION FACTOR 2; PROTEIN KINASE; SERUM RESPONSE FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; HEAT SHOCK PROTEIN; HSF1 PROTEIN, MOUSE; HSF2 PROTEIN, MOUSE; RNA POLYMERASE II;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CHROMATIN; CYTOSKELETON; DOWN REGULATION; GENE EXPRESSION; GENETIC ASSOCIATION; HEAT SHOCK RESPONSE; IN VITRO STUDY; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PROMOTER REGION; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; CELL LINE; CYTOLOGY; FIBROBLAST; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; MAMMAL; METABOLISM;

ANIMALS; CELL LINE; DNA-BINDING PROTEINS; FIBROBLASTS; GENE EXPRESSION REGULATION; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; MAMMALS; MICE; PROMOTER REGIONS, GENETIC; RNA POLYMERASE II; SERUM RESPONSE FACTOR; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84962393627     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.02.025     Document Type: Article

References (54)

1. Adelman K., Lis J.T. Promoter-proximal pausing of RNA polymerase II: emerging roles in metazoans. Nat. Rev. Genet. 2012, 13:720-731.
2. Akerfelt M., Morimoto R.I., Sistonen L. Heat shock factors: integrators of cell stress, development and lifespan. Nat. Rev. Mol. Cell Biol. 2010, 11:545-555.
3. Ardehali M.B., Lis J.T. Tracking rates of transcription and splicing in vivo. Nat. Struct. Mol. Biol. 2009, 16:1123-1124.
4. Baird N.A., Douglas P.M., Simic M.S., Grant A.R., Moresco J.J., Wolff S.C., Yates J.R., Manning G., Dillin A. HSF-1-mediated cytoskeletal integrity determines thermotolerance and life span. Science 2014, 346:360-363.
5. Bienz M., Pelham H.R. Heat shock regulatory elements function as an inducible enhancer in the Xenopus hsp70 gene and when linked to a heterologous promoter. Cell 1986, 45:753-760.
6. Brown J.B., Boley N., Eisman R., May G.E., Stoiber M.H., Duff M.O., Booth B.W., Wen J., Park S., Suzuki A.M., et al. Diversity and dynamics of the Drosophila transcriptome. Nature 2014, 512:393-399.
7. Buckley M.S., Kwak H., Zipfel W.R., Lis J.T. Kinetics of promoter Pol II on Hsp70 reveal stable pausing and key insights into its regulation. Genes Dev. 2014, 28:14-19.
8. Chen Y., Negre N., Li Q., Mieczkowska J.O., Slattery M., Liu T., Zhang Y., Kim T.-K., He H.H., Zieba J., et al. Systematic evaluation of factors influencing ChIP-seq fidelity. Nat. Methods 2012, 9:609-614.
9. Core L.J., Waterfall J.J., Lis J.T. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 2008, 322:1845-1848.
10. Core L.J., Martins A.L., Danko C.G., Waters C.T., Siepel A., Lis J.T. Analysis of nascent RNA identifies a unified architecture of initiation regions at mammalian promoters and enhancers. Nat. Genet. 2014, 46:1311-1320.
11. Dai C., Whitesell L., Rogers A.B., Lindquist S. Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell 2007, 130:1005-1018.
12. Danko C.G., Hah N., Luo X., Martins A.L., Core L., Lis J.T., Siepel A., Kraus W.L. Signaling pathways differentially affect RNA polymerase II initiation, pausing, and elongation rate in cells. Mol. Cell 2013, 50:212-222.
13. Danko C.G., Hyland S.L., Core L.J., Martins A.L., Waters C.T., Lee H.W., Cheung V.G., Kraus W.L., Lis J.T., Siepel A. Identification of active transcriptional regulatory elements from GRO-seq data. Nat. Methods 2015, 12:433-438.
14. de la Grange P., Dutertre M., Martin N., Auboeuf D. FAST DB: a website resource for the study of the expression regulation of human gene products. Nucleic Acids Res. 2005, 33:4276-4284.
15. Elsing A.N., Aspelin C., Björk J.K., Bergman H.A., Himanen S.V., Kallio M.J., Roos-Mattjus P., Sistonen L. Expression of HSF2 decreases in mitosis to enable stress-inducible transcription and cell survival. J. Cell Biol. 2014, 206:735-749.
16. Fuda N.J., Ardehali M.B., Lis J.T. Defining mechanisms that regulate RNA polymerase II transcription in vivo. Nature 2009, 461:186-192.
17. Guertin M.J., Lis J.T. Chromatin landscape dictates HSF binding to target DNA elements. PLoS Genet. 2010, 6:e1001114.
18. Heidenreich O., Neininger A., Schratt G., Zinck R., Cahill M.A., Engel K., Kotlyarov A., Kraft R., Kostka S., Gaestel M., Nordheim A. MAPKAP kinase 2 phosphorylates serum response factor in vitro and in vivo. J. Biol. Chem. 1999, 274:14434-14443.
19. Huang W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
20. Jonkers I., Kwak H., Lis J.T. Genome-wide dynamics of Pol II elongation and its interplay with promoter proximal pausing, chromatin, and exons. eLife 2014, 3:e02407.
21. Kampinga H.H., Hageman J., Vos M.J., Kubota H., Tanguay R.M., Bruford E.A., Cheetham M.E., Chen B., Hightower L.E. Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperones 2009, 14:105-111.
22. Kim T.-K., Hemberg M., Gray J.M., Costa A.M., Bear D.M., Wu J., Harmin D.A., Laptewicz M., Barbara-Haley K., Kuersten S., et al. Widespread transcription at neuronal activity-regulated enhancers. Nature 2010, 465:182-187.
23. Kwak H., Fuda N.J., Core L.J., Lis J.T. Precise maps of RNA polymerase reveal how promoters direct initiation and pausing. Science 2013, 339:950-953.
24. Laszlo A. The effects of hyperthermia on mammalian cell structure and function. Cell Prolif. 1992, 25:59-87.
25. Lecomte S., Desmots F., Le Masson F., Le Goff P., Michel D., Christians E.S., Le Dréan Y. Roles of heat shock factor 1 and 2 in response to proteasome inhibition: consequence on p53 stability. Oncogene 2010, 29:4216-4224.
26. Li W., Kong A.-N. Molecular mechanisms of Nrf2-mediated antioxidant response. Mol. Carcinog. 2009, 48:91-104.
27. Lindquist S. The heat-shock response. Annu. Rev. Biochem. 1986, 55:1151-1191.
28. Lindquist S., Craig E.A. The heat-shock proteins. Annu. Rev. Genet. 1988, 22:631-677.
29. Lis J.T., Mason P., Peng J., Price D.H., Werner J. P-TEFb kinase recruitment and function at heat shock loci. Genes Dev. 2000, 14:792-803.
30. Locke M., Tanguay R.M. Diminished heat shock response in the aged myocardium. Cell Stress Chaperones 1996, 1:251-260.
31. Ma X., Xu L., Alberobello A.T., Gavrilova O., Bagattin A., Skarulis M., Liu J., Finkel T., Mueller E. Celastrol Protects against Obesity and Metabolic Dysfunction through Activation of a HSF1-PGC1α Transcriptional Axis. Cell Metab. 2015, 22:695-708.
32. McMillan D.R., Xiao X., Shao L., Graves K., Benjamin I.J. Targeted disruption of heat shock transcription factor 1 abolishes thermotolerance and protection against heat-inducible apoptosis. J. Biol. Chem. 1998, 273:7523-7528.
33. McMillan D.R., Christians E., Forster M., Xiao X., Connell P., Plumier J.C., Zuo X., Richardson J., Morgan S., Benjamin I.J. Heat shock transcription factor 2 is not essential for embryonic development, fertility, or adult cognitive and psychomotor function in mice. Mol. Cell. Biol. 2002, 22:8005-8014.
34. Mendillo M.L., Santagata S., Koeva M., Bell G.W., Hu R., Tamimi R.M., Fraenkel E., Ince T.A., Whitesell L., Lindquist S. HSF1 drives a transcriptional program distinct from heat shock to support highly malignant human cancers. Cell 2012, 150:549-562.
35. Morley J.F., Morimoto R.I. Regulation of longevity in Caenorhabditis elegans by heat shock factor and molecular chaperones. Mol. Biol. Cell 2004, 15:657-664.
36. Neef D.W., Jaeger A.M., Thiele D.J. Heat shock transcription factor 1 as a therapeutic target in neurodegenerative diseases. Nat. Rev. Drug Discov. 2011, 10:930-944.
37. O'Brien T., Lis J.T. RNA polymerase II pauses at the 5' end of the transcriptionally induced Drosophila hsp70 gene. Mol. Cell. Biol. 1991, 11:5285-5290.
38. Parker C.S., Topol J. A Drosophila RNA polymerase II transcription factor binds to the regulatory site of an hsp 70 gene. Cell 1984, 37:273-283.
39. Perisic O., Xiao H., Lis J.T. Stable binding of Drosophila heat shock factor to head-to-head and tail-to-tail repeats of a conserved 5 bp recognition unit. Cell 1989, 59:797-806.
40. Price D.H. P-TEFb, a cyclin-dependent kinase controlling elongation by RNA polymerase II. Mol. Cell. Biol. 2000, 20:2629-2634.
41. Raychaudhuri S., Loew C., Körner R., Pinkert S., Theis M., Hayer-Hartl M., Buchholz F., Hartl F.U. Interplay of acetyltransferase EP300 and the proteasome system in regulating heat shock transcription factor 1. Cell 2014, 156:975-985.
42. Renner D.B., Yamaguchi Y., Wada T., Handa H., Price D.H. A highly purified RNA polymerase II elongation control system. J. Biol. Chem. 2001, 276:42601-42609.
43. Sandqvist A., Björk J.K., Akerfelt M., Chitikova Z., Grichine A., Vourc'h C., Jolly C., Salminen T.A., Nymalm Y., Sistonen L. Heterotrimerization of heat-shock factors 1 and 2 provides a transcriptional switch in response to distinct stimuli. Mol. Biol. Cell 2009, 20:1340-1347.
44. Sarge K.D., Zimarino V., Holm K., Wu C., Morimoto R.I. Cloning and characterization of two mouse heat shock factors with distinct inducible and constitutive DNA-binding ability. Genes Dev. 1991, 5:1902-1911.
45. Schratt G., Weinhold B., Lundberg A.S., Schuck S., Berger J., Schwarz H., Weinberg R.A., Rüther U., Nordheim A. Serum response factor is required for immediate-early gene activation yet is dispensable for proliferation of embryonic stem cells. Mol. Cell. Biol. 2001, 21:2933-2943.
46. Shalgi R., Hurt J.A., Lindquist S., Burge C.B. Widespread inhibition of posttranscriptional splicing shapes the cellular transcriptome following heat shock. Cell Rep. 2014, 7:1362-1370.
47. Sotiropoulos A., Gineitis D., Copeland J., Treisman R. Signal-regulated activation of serum response factor is mediated by changes in actin dynamics. Cell 1999, 98:159-169.
48. Takahashi H., Parmely T.J., Sato S., Tomomori-Sato C., Banks C.A.S., Kong S.E., Szutorisz H., Swanson S.K., Martin-Brown S., Washburn M.P., et al. Human mediator subunit MED26 functions as a docking site for transcription elongation factors. Cell 2011, 146:92-104.
49. Teves S.S., Henikoff S. Heat shock reduces stalled RNA polymerase II and nucleosome turnover genome-wide. Genes Dev. 2011, 25:2387-2397.
50. Theodorakis N.G., Morimoto R.I. Posttranscriptional regulation of hsp70 expression in human cells: effects of heat shock, inhibition of protein synthesis, and adenovirus infection on translation and mRNA stability. Mol. Cell. Biol. 1987, 7:4357-4368.
51. Trinklein N.D., Murray J.I., Hartman S.J., Botstein D., Myers R.M. The role of heat shock transcription factor 1 in the genome-wide regulation of the mammalian heat shock response. Mol. Biol. Cell 2004, 15:1254-1261.
52. Vartiainen M.K., Guettler S., Larijani B., Treisman R. Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science 2007, 316:1749-1752.
53. Westwood J.T., Clos J., Wu C. Stress-induced oligomerization and chromosomal relocalization of heat-shock factor. Nature 1991, 353:822-827.
54. Zhou J., Wan J., Gao X., Zhang X., Jaffrey S.R., Qian S.-B. Dynamic m(6)A mRNA methylation directs translational control of heat shock response. Nature 2015, 526:591-594.