The heat shock response: A case study of chromatin dynamics in gene regulation

Biochemistry and Cell Biology

Volumn 91, Issue 1, 2013, Pages 42-48

  Teves, Sheila S ^a,b   Henikoff, Steven ^a,c  

^a Fred Hutchinson Cancer Research Center   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Epigenome; Heat shock; Nucleosome turnover; RNA polymerase II

Indexed keywords

CONTROL OF GENE EXPRESSION; EPIGENOMES; HEAT-SHOCK; NUCLEOSOMES; RNA POLYMERASE II; TRANSCRIPTION FACTOR BINDING; TRANSCRIPTIONAL ACTIVATIONS; TRANSCRIPTIONAL REGULATION;

DYNAMICS; GENES; RNA; TRANSCRIPTION FACTORS;

TRANSCRIPTION;

DEOXYRIBONUCLEASE I; HEAT SHOCK PROTEIN 70; RNA POLYMERASE;

CELL ELONGATION; CELL STRUCTURE; CHROMATIN; GENE ACTIVATION; GENE EXPRESSION; GENE REPRESSION; HEAT SHOCK RESPONSE; HUMAN; NONHUMAN; NUCLEOSOME; REVIEW; THERMODYNAMICS; TRANSCRIPTION REGULATION;

ANIMALS; CHROMATIN; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; HEAT-SHOCK RESPONSE; HSP70 HEAT-SHOCK PROTEINS; HUMANS; NUCLEOSOMES; PROMOTER REGIONS, GENETIC; RNA POLYMERASE II; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84874917748     PISSN: 08298211     EISSN: 12086002     Source Type: Journal    
DOI: 10.1139/bcb-2012-0075     Document Type: Review

References (78)

1. Akerfelt M. Morimoto R.I. Sistonen L. 2010. Heat shock factors: integrators of cell stress, development and lifespan. Nat. Rev. Mol. Cell Biol. 11: 545-555. 10.1038/nrm2938. 20628411.
2. Bai L. Charvin G. Siggia E.D. Cross F.R. 2010. Nucleosome-Depleted Regions in Cell-Cycle-Regulated Promoters Ensure Reliable Gene Expression in Every Cell Cycle. Dev. Cell, 18: 544-555. 10.1016/j.devcel.2010.02.007. 20412770.
3. Baranello L. Bertozzi D. Fogli M.V. Pommier Y. Capranico G. 2010. DNA topoisomerase I inhibition by camptothecin induces escape of RNA polymerase II from promoter-proximal pause site, antisense transcription and histone acetylation at the human HIF-1 gene locus. Nucleic Acids Res. 38: 159-171. 10.1093/nar/gkp817. 19854946.
4. Baumann M. Pontiller J. Ernst W. 2010. Structure and Basal Transcription Complex of RNA Polymerase II Core Promoters in the Mammalian Genome: An Overview. Mol. Biotechnol. 45: 241-247. 10.1007/s12033-010-9265-6. 20300884.
5. Becavin C. Barbi M. Victor J.-M. Lesne A. 2010. Transcription within Condensed Chromatin: Steric Hindrance Facilitates Elongation. Biophys. J. 98: 824-833. 10.1016/j.bpj.2009.10.054. 20197036.
6. Bintu L. Kopaczynska M. Hodges C. Lubkowska L. Kashlev M. Bustamante C. 2011. The elongation rate of RNA polymerase determines the fate of transcribed nucleosomes. Nat. Struct. Mol. Biol. 18: 1394-1399. 10.1038/nsmb.2164. 22081017.
7. Cernilogar F.M. Onorati M.C. Kothe G.O. Burroughs A.M. Parsi K.M. Breiling A. et al. 2011. Chromatin-associated RNA interference components contribute to transcriptional regulation in Drosophila. Nature, 480: 391-395. 10.1038/nature10492. 22056986.
8. Chen W. Luo L. Zhang L. 2010. The organization of nucleosomes around splice sites. Nucleic Acids Res. 38: 2788-2798. 10.1093/nar/gkq007. 20097656.
9. Costlow N. Lis J.T. 1984. High-resolution mapping of DNase I-hypersensitive sites of Drosophila heat shock genes in Drosophila melanogaster and Saccharomyces cerevisiae. Mol. Cell. Biol. 4: 1853-1863. 6436689.
10. Czarnota G.J. Bazett-Jones D.P. Mendez E. Allfrey V.G. Ottensmeyer F.P. 1997. High Resolution Microanalysis and Three-Dimensional Nucleosome Structure Associated with Transcribing Chromatin. Micron, 28: 419-431. 10.1016/S0968-4328(97)00050-4. 9519470.
11. Deal R.B. Henikoff J.G. Henikoff S. 2010. Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science, 328: 1161-1164. 10.1126/science.1186777. 20508129.
12. Desai N.A. Shankar V. 2003. Single-strand-specific nucleases. FEMS Microbiol. Rev. 26: 457-491. 10.1016/S0168-6445(02)00129-8. 12586391.
13. Erkina T.Y. Zou Y. Freeling S. Vorobyev V.I. Erkine A.M. 2010. Functional interplay between chromatin remodeling complexes RSC, SWI/SNF and ISWI in regulation of yeast heat shock genes. Nucleic Acids Res. 38: 1441-1449. 10.1093/nar/gkp1130. 20015969.
14. Fish R.N. Kane C.M. 2002. Promoting elongation with transcript cleavage stimulatory factors. Biochim. Biophys. Acta, 1577: 287-307. 10.1016/S0167- 4781(02)00459-1. 12213659.
15. Gartenberg M.R. Wang J.C. 1992. Positive supercoiling of DNA greatly diminishes mRNA synthesis in yeast. Proc. Natl. Acad. Sci. U.S.A. 89: 11461-11465. 10.1073/pnas.89.23.11461. 1333610.
16. Gilchrist D.A. Nechaev S. Lee C. Ghosh S.K.B. Collins J.B. Li L. et al. 2008. NELF-mediated stalling of Pol II can enhance gene expression by blocking promoter-proximal nucleosome assembly. Genes Dev. 22: 1921-1933. 10.1101/gad.1643208. 18628398.
17. Gilchrist D.A. Dos Santos G. Fargo D.C. Xie B. Gao Y. Li L. Adelman K. 2010. Pausing of RNA polymerase II disrupts DNA-specified nucleosome organization to enable precise gene regulation. Cell, 143: 540-551. 10.1016/j.cell.2010.10.004. 21074046.
18. Gilmour D.S. Lis J.T. 1986. RNA Polymerase II interacts with the promoter region of the noninduced hsp70 gene in Drosophila melanogaster cells. Mol. Cell Biol. 6: 3984-3989. 3099167.
19. Guertin M.J. Lis J.T. 2010. Chromatin Landscape Dictates HSF Binding to Target DNA Elements. PLoS Genet. 6: e1001114. 10.1371/journal.pgen.1001114. 20844575.
20. Guertin M.J. Martins A.L. Siepel A. Lis J.T. 2012. Accurate Prediction of Inducible Transcription Factor Binding Intensities In Vivo. PLoS Genet. 8: e1002610. 10.1371/journal.pgen.1002610. 22479205.
21. Gupta P. Zlatanova J. Tomschik M. 2009. Nucleosome Assembly Depends on the Torsion in the DNA Molecule: A Magnetic Tweezers Study. Biophys. J. 97: 3150-3157. 10.1016/j.bpj.2009.09.032. 20006952.
22. Henikoff S. 2008. Nucleosome destabilization in the epigenetic regulation of gene expression. Nat. Rev. Genet. 9: 15-26. 10.1038/nrg2206. 18059368.
23. Henikoff J.G. Belsky J.A. Krassovsky K. MacAlpine D.M. Henikoff S. 2011. Epigenome characterization at single base-pair resolution. Proc. Natl. Acad. Sci. U.S.A. 108: 18318-18323. 10.1073/pnas.1110731108. 22025700.
24. Hizume K. Yoshimura S.H. Takeyasu K. 2004. Atomic force microscopy demonstrates a critical role of DNA superhelicity in nucleosome dynamics. Cell Biochem. Biophys. 40: 249-261. 10.1385/CBB:40:3:249. 15211026.
25. Iyer, V., and Struhl, K. 1995. Poly(dA:dT), a ubiquitous promoter element that stimulates transcription via its intrinsic DNA structure. EMBO J. 14: 2570-2579. PMID:7781610.
26. Jamrich M. Greenleaf A.L. Bautz E.K. 1977. Localization of RNA polymerase in polytene chromosomes of Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 74: 2079-2083. 10.1073/pnas.74.5.2079. 405671.
27. Jenuwein T. Allis C.D. 2001. Translating the histone code. Science, 293: 1074-1080. 10.1126/science.1063127. 11498575.
28. Jin C. Felsenfeld G. 2007. Nucleosome stability mediated by histone variants H3.3 and H2A.Z. Genes Dev. 21: 1519-1529. 10.1101/gad.1547707. 17575053.
29. Jin J. Bai L. Johnson D.S. Fulbright R.M. Kireeva M.L. Kashlev M. Wang M.D. 2010. Synergistic action of RNA polymerases in overcoming the nucleosomal barrier. Nat. Struct. Mol. Biol. 17: 745-752. 10.1038/nsmb.1798. 20453861.
30. Joshi R.S. Pina B. Roca J. 2010. Positional dependence of transcriptional inhibition by DNA torsional stress in yeast chromosomes. EMBO J. 29: 740-748. 10.1038/emboj.2009.391. 20057354.
31. Kent N.A. Adams S. Moorhouse A. Paszkiewicz K. 2011. Chromatin particle spectrum analysis: a method for comparative chromatin structure analysis using paired-end mode next-generation DNA sequencing. Nucleic Acids Res. 39: e26. 10.1093/nar/gkq1183. 21131275.
32. Kim H. Erickson B. Luo W. Seward D. Graber J.H. Pollock D.D. et al. 2010. Gene-specific RNA polymerase II phosphorylation and the CTD code. Nat. Struct. Mol. Biol. 17: 1279-1286. 10.1038/nsmb.1913. 20835241.
33. Kireeva M.L. Walter W. Tchernajenko V. Bondarenko V. Kashlev M. Studitsky V.M. 2002. Nucleosome remodeling induced by RNA polymerase II: loss of the H2A/H2B dimer during transcription. Mol. Cell, 9: 541-552. 10.1016/S1097- 2765(02)00472-0. 11931762.
34. Knezetic J.A. Luse D.S. 1986. The presence of nucleosomes on a DNA template prevents initiation by RNA polymerase II in vitro. Cell, 45: 95-104. 10.1016/0092-8674(86)90541-6. 3955658.
35. Kulaeva O.I. Hsieh F.-K. Studitsky V.M. 2010. RNA polymerase complexes cooperate to relieve the nucleosomal barrier and evict histones. Proc. Natl. Acad. Sci. U.S.A. 107: 11325-11330. 10.1073/pnas.1001148107. 20534568.
36. Kuryan B.G. Kim J. Tran N.N.H. Lombardo S.R. Venkatesh S. Workman J.L. Carey M. 2012. Histone density is maintained during transcription mediated by the chromatin remodeler RSC and histone chaperone NAP1 in vitro. Proc. Natl. Acad. Sci. U.S.A. 109: 1931-1936. 10.1073/pnas.1109994109. 22308335.
37. Levine M. 2011. Paused RNA polymerase II as a developmental checkpoint. Cell, 145: 502-511. 10.1016/j.cell.2011.04.021. 21565610.
38. Levy A. Noll M. 1981. Chromatin fine structure of active and repressed genes. Nature, 289: 198-203. 10.1038/289198a0. 6779207.
39. Li J. Gilmour D.S. 2011. Promoter proximal pausing and the control of gene expression. Curr. Opin. Genet. Dev. 21: 231-235. 10.1016/j.gde.2011.01.010. 21324670.
40. Lindquist S. 1981. Regulation of protein synthesis during heat shock. Nature, 293: 311-314. 10.1038/293311a0.
41. Lindquist S. 1986. The heat-shock response. Annu. Rev. Biochem. 55: 1151-1191. 10.1146/annurev.biochem.55.1.1151. 2427013.
42. Lis J.T. 1998. Promoter-associated Pausing in Promoter Architecture and Postinitiation Transcriptional Regulation. Cold Spring Harb. Symp. Quant. Biol. 63: 347-356. 10.1101/sqb.1998.63.347. 10384299.
43. Liu L.F. Wang J.C. 1987. Supercoiling of the DNA template during transcription. Proc. Natl. Acad. Sci. U.S.A. 84: 7024-7027. 10.1073/pnas.84.20. 7024.
44. Lu Q. Wallrath L.L. Granok H. Elgin S.C. 1993. (CT)n (GA)n repeats and heat shock elements have distinct roles in chromatin structure and transcriptional activation of the Drosophila hsp26 gene. Mol. Cell Biol. 13: 2802-2814.
45. Luger K. Mäder A.W. Richmond R.K. Sargent D.F. Richmond T.J. 1997. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389: 251-260. 9305837.
46. Luse D.S. Studitsky V.M. 2011. The mechanism of nucleosome traversal by RNA polymerase II: roles for template uncoiling and transcript elongation factors. RNA Biol. 8: 581-585. 10.4161/rna.8.4.15389. 21519186.
47. Marshall N.F. Price D.H. 1995. Purification of P-TEFb, a transcription factor required for the transition into productive elongation. J. Biol. Chem. 270: 12335-12338. 10.1074/jbc.270.21.12335. 7759473.
48. Marshall N.F. Peng J. Xie Z. Price D.H. 1996. Control of RNA Polymerase II Elongation Potential by a Novel Carboxyl-terminal Domain Kinase. J. Biol. Chem. 271: 27176-27183. 10.1074/jbc.271.43.27176. 8900211.
49. Mavrich T.N. Jiang C. Ioshikhes I.P. Li X. Venters B.J. Zanton S.J. et al. 2008. Nucleosome organization in the Drosophila genome. Nature, 453: 358-362. 10.1038/nature06929. 18408708.
50. McKenzie S.L. Henikoff S. Meselson M. 1975. Localization of RNA from heat-induced polysomes at puff sites in Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 72: 1117-1121. 10.1073/pnas.72.3.1117. 805422.
51. Missra A. Gilmour D.S. 2010. Interactions between DSIF (DRB sensitivity inducing factor), NELF (negative elongation factor), and the Drosophila RNA polymerase II transcription elongation complex. Proc. Natl. Acad. Sci. U.S.A. 107: 11301-11306. 10.1073/pnas.1000681107. 20534440.
52. Mito Y. Henikoff J.G. Henikoff S. 2005. Genome-scale profiling of histone H3.3 replacement patterns. Nat. Genet. 37: 1090-1097. 10.1038/ng1637. 16155569.
53. Peterlin B.M. Price D.H., 2006. Controlling the elongation phase of transcription with P-TEFb. Mol. Cell, 23: 297-305. 10.1016/j.molcel.2006.06.014. 16885020.
54. Petesch S.J. Lis J.T. 2008. Rapid, Transcription-Independent Loss of Nucleosomes over a Large Chromatin Domain at Hsp70 Loci. Cell, 134: 74-84. 10.1016/j.cell.2008.05.029. 18614012.
55. Petesch, S.J., and Lis, J.T. 2012. Overcoming the nucleosome barrier during transcript elongation. Trends Genet. 28: 285-294. doi:10.1016/j.tig.2012. 02.005. PMID:22465610.
56. Rando O.J. 2012. Combinatorial complexity in chromatin structure and function: revisiting the histone code. Curr. Opin. Genet. Dev. 22: 148-155. 10.1016/j.gde.2012.02.013. 22440480.
57. Rhee H.S. Pugh B.F. 2011. Comprehensive genome-wide protein-DNA interactions detected at single-nucleotide resolution. Cell, 147: 1408-1419. 10.1016/j.cell.2011.11.013. 22153082.
58. Rougvie A.E. Lis J.T. 1988. The RNA polymerase II molecule at the 5′ end of the uninduced hsp7-gene of D. melanogaster is transcriptionally engaged. Cell, 54: 795-804. 10.1016/S0092-8674(88)91087-2. 3136931.
59. Schwartz B.E. Ahmad K. 2005. Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev. 19: 804-814. 10.1101/gad.1259805. 15774717.
60. Shandilya J. Roberts S.G.E. 2012. The transcription cycle in eukaryotes: From productive initiation to RNA polymerase II recycling. Biochim. Biophys. Acta, 1819: 391-400. 10.1016/j.bbagrm.2012.01.010. 22306664.
61. Shivaswamy S. Iyer V.R. 2008. Stress-dependent dynamics of global chromatin remodeling in yeast: dual role for SWI/SNF in the heat shock stress response. Mol. Cell. Biol. 28: 2221-2234. 10.1128/MCB.01659-07. 18212068.
62. Shivaswamy S. Bhinge A. Zhao Y. Jones S. Hirst M. Iyer V.R. 2008. Dynamic Remodeling of Individual Nucleosomes Across a Eukaryotic Genome in Response to Transcriptional Perturbation. PLoS Biol. 6: e65. 10.1371/journal.pbio.0060065. 18351804.
63. Shopland L.S. Hirayoshi K. Fernandes M. Lis J.T. 1995. HSF access to heat shock elements in vivo depends critically on promoter architecture defined by GAGA factor, TFIID, and RNA polymerase II binding sites. Genes Dev. 9: 2756-2769. 10.1101/gad.9.22.2756. 7590251.
64. Simon, J., Sutton, C., Lobell, R., Glaser, R., and Lis, J.T. 1985. Determinants of heat shock-induced chromosome puffing. Cell. 40: 805-817. doi:10.1016/0092-8674(85)90340-X. PMID:3986904.
65. Teves S.S. Henikoff S. 2011. Heat shock reduces stalled RNA polymerase II and nucleosome turnover genome-wide. Genes Dev. 25: 2387-2397. 10.1101/gad.177675.111. 22085965.
66. Tissieres A. Mitchell H.K. Tracy U.M. 1974. Protein synthesis in salivary glands of Drosophila melanogaster: relation to chromosome puffs. J. Mol. Biol. 84: 389-398. 10.1016/0022-2836(74)90447-1. 4219221.
67. Tsukiyama T. Becker P.B. Wu C. 1994. ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor. Nature, 367: 525-532. 10.1038/367525a0. 8107823.
68. Villeponteau, B., and Martinson, H. 1987. Gamma rays and bleomycin nick DNA and reverse the DNase I sensitivity of beta-globin gene chromatin in vivo. Mol. Cell. Biol. 7: 1917-1924. PMID:2439900.
69. Villeponteau B. Lundell M. Martinson H. 1984. Torsional stress promotes the DNAase I sensitivity of active genes. Cell. 39: 469-478. 10.1016/0092-8674(84)90454-9. 6096006.
70. Weber C.M. Henikoff J.G. Henikoff S. 2010. H2A.Z nucleosomes enriched over active genes are homotypic. Nat. Struct. Mol. Biol. 17: 1500-1507. 10.1038/nsmb.1926. 21057526.
71. Wu C. 1980. The 5′ ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I. Nature, 286: 854-860. 10.1038/286854a0. 6774262.
72. Wu, C., Wong, Y., and Elgin, S. 1979. The chromatin structure of specific genes: II. Disruption of chromatin structure during gene activity. Cell. 16: 807-814. doi:10.1016/0092-8674(79)90096-5. PMID:455450.
73. Wu C.-H. Yamaguchi Y. Benjamin L.R. Horvat-Gordon M. Washinsky J. Enerly E. et al. 2003. NELF and DSIF cause promoter proximal pausing on the hsp70 promoter in Drosophila. Genes Dev. 17: 1402-1414. 10.1101/gad.1091403. 12782658.
74. Wutz A. 2011. Gene silencing in X-chromosome inactivation: advances in understanding facultative heterochromatin formation. Nat. Rev. Genet. 12: 542-553. 10.1038/nrg3035. 21765457.
75. Yakovchuk P. Goodrich J.A. Kugel J.F. 2009. B2 RNA and Alu RNA repress transcription by disrupting contacts between RNA polymerase II and promoter DNA within assembled complexes. Proc. Natl. Acad. Sci. U.S.A. 106: 5569-5574. 10.1073/pnas.0810738106. 19307572.
76. Yamada T. Yamaguchi Y. Inukai N. Okamoto S. Mura T. Handa H. 2006. P-TEFb-mediated phosphorylation of hSpt5 C-terminal repeats is critical for processive transcription elongation. Mol. Cell, 21: 227-237. 10.1016/j.molcel.2005.11.024. 16427012.
77. Zanton S.J. Pugh B.F. 2006. Full and partial genome-wide assembly and disassembly of the yeast transcription machinery in response to heat shock. Genes Dev. 20: 2250-2265. 10.1101/gad.1437506. 16912275.
78. Zlatanova J. Victor J.-M. 2009. How are nucleosomes disrupted during transcription elongation? HFSP J. 3: 373-378. 10.2976/1.3249971. 20514129.