Abstract
Histone chaperones are an integral part of the transcription regulatory machinery. We investigated the involvement of histone chaperones and their functional interactions with ATP-dependent chromatin remodeling complexes in the regulation of yeast heat shock genes. Strong functional interaction between the histone chaperone ASF1 and the ATP-dependent chromatin remodeling complex SWI/SNF is exhibited in synergistic diminishment of nucleosome displacement during heat shock in the ΔASF1/ΔSNF2 strain in comparison to individual ASF1 or SNF2 inactivation. A similar but less pronounced effect was observed for ISW1/ASF1 inactivation but not for ASF1/STH1 (RSC complex) combinatorial inactivation. The depletion of Spt16, which is a major subunit of the FACT histone chaperone complex, leads to a severe growth defect phenotype associated with unusual thermotolerance. The acquired thermotolerance in the Spt16-depleted strain is associated with a defect in the reassembly of nucleosomes at the promoters of heat shock genes during sustained heat stress, leading to increased recruitment of the transcriptional activator HSF and RNA polymerase II. The defect in nucleosome assembly associated with Spt16 depletion also leads to an increased tolerance to stress due to an increased concentration of NaCl.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adkins MW, Tyler JK (2006) Transcriptional activators are dispensable for transcription in the absence of Spt6-mediated chromatin reassembly of promoter regions. Mol Cell 21:405–416
Amoros M, Estruch F (2001) Hsf1p and Msn2/4p cooperate in the expression of Saccharomyces cerevisiae genes HSP26 and HSP104 in a gene- and stress type-dependent manner. Mol Microbiol 39:1523–1532
Belotserkovskaya R, Oh S, Bondarenko VA, Orphanides G, Studitsky VM, Reinberg D (2003) FACT facilitates transcription-dependent nucleosome alteration. Science 301:1090–1093. doi:10.1126/science.1085703
Boeger H, Griesenbeck J, Strattan JS, Kornberg RD (2004) Removal of promoter nucleosomes by disassembly rather than sliding in vivo. Mol Cell 14:667–673
Boy-Marcotte E, Lagniel G, Perrot M, Bussereau F, Boudsocq A, Jacquet M, Labarre J (1999) The heat shock response in yeast: differential regulations and contributions of the Msn2p/Msn4p and Hsf1p regulons. Mol Microbiol 33:274–283
Dai C, Whitesell L, Rogers AB, Lindquist S (2007) Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell 130:1005–1018. doi:10.1016/j.cell.2007.07.020
Das C, Tyler JK, Churchill ME (2010) The histone shuffle: histone chaperones in an energetic dance. Trends Biochem Sci 35:476–489. doi:10.1016/j.tibs.2010.04.001
Duina AA (2011) Histone chaperones Spt6 and FACT: similarities and differences in modes of action at transcribed. Genes Genet Res Int 2011, 625210. doi:10.4061/2011/625210
Elsasser SJ, D'Arcy S (2012) Towards a mechanism for histone chaperones. Biochim Biophys Acta 1819:211–221. doi:10.1016/j.bbagrm.2011.07.007
English CM, Maluf NK, Tripet B, Churchill ME, Tyler JK (2005) ASF1 binds to a heterodimer of histones H3 and H4: a two-step mechanism for the assembly of the H3-H4 heterotetramer on DNA. Biochemistry 44:13673–13682. doi:10.1021/bi051333h
English CM, Adkins MW, Carson JJ, Churchill ME, Tyler JK (2006) Structural basis for the histone chaperone activity of Asf1. Cell 127:495–508. doi:10.1016/j.cell.2006.08.047
Erkina TY, Erkine AM (2006) Displacement of histones at promoters of Saccharomyces cerevisiae heat shock genes is differentially associated with histone H3 acetylation. Mol Cell Biol 26:7587–7600
Erkina TY, Tschetter PA, Erkine AM (2008) Different requirements of the SWI/SNF complex for robust nucleosome displacement at promoters of heat shock factor and Msn2- and Msn4-regulated heat shock genes. Mol Cell Biol 28:1207–1217. doi:10.1128/MCB. 01069-07
Erkina TY, Zou Y, Freeling S, Vorobyev VI, Erkine AM (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. doi:10.1093/nar/gkp1130
Erkine AM, Gross DS (2003) Dynamic chromatin alterations triggered by natural and synthetic activation domains. J Biol Chem 278:7755–7764
Erkine AM, Adams CC, Diken T, Gross DS (1996) Heat shock factor gains access to the yeast HSC82 promoter independently of other sequence-specific factors and antagonizes nucleosomal repression of basal and induced transcription. Mol Cell Biol 16:7004–7017
Erkine AM, Magrogan SF, Sekinger EA, Gross DS (1999) Cooperative binding of heat shock factor to the yeast HSP82 promoter in vivo and in vitro. Mol Cell Biol 19:1627–1639
Estruch F (2000) Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiol Rev 24:469–486
Formosa T (2008) FACT and the reorganized nucleosome. Mol Biosyst 4:1085–1093. doi:10.1039/b812136b
Gangaraju VK, Bartholomew B (2007) Dependency of ISW1a chromatin remodeling on extranucleosomal DNA. Mol Cell Biol 27:3217–3225. doi:10.1128/MCB. 01731-06
Gkikopoulos T, Havas KM, Dewar H, Owen-Hughes T (2009) SWI/SNF and Asf1p cooperate to displace histones during induction of the Saccharomyces cerevisiae HO promoter. Mol Cell Biol 29:4057–4066. doi:10.1128/MCB. 00400-09
Guldener U, Heck S, Fielder T, Beinhauer J, Hegemann JH (1996) A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res 24:2519–2524
Hahn JS, Hu Z, Thiele DJ, Iyer VR (2004) Genome-wide analysis of the biology of stress responses through heat shock transcription factor. Mol Cell Biol 24:5249–5256
Hainer SJ, Charsar BA, Cohen SB, Martens JA (2012) Identification of mutant versions of the Spt16 histone chaperone that are defective for transcription-coupled nucleosome occupancy in Saccharomyces cerevisiae. G3 (Bethesda) 2:555–567. doi:10.1534/g3.112.002451
Han J, Zhou H, Li Z, Xu RM, Zhang Z (2007) Acetylation of lysine 56 of histone H3 catalyzed by RTT109 and regulated by ASF1 is required for replisome integrity. J Biol Chem 282:28587–28596. doi:10.1074/jbc.M702496200
Ivanovska I, Jacques PE, Rando OJ, Robert F, Winston F (2011) Control of chromatin structure by spt6: different consequences in coding and regulatory regions. Mol Cell Biol 31:531–541. doi:10.1128/MCB. 01068-10
Jensen MM, Christensen MS, Bonven B, Jensen TH (2008) Requirements for chromatin reassembly during transcriptional downregulation of a heat shock gene in Saccharomyces cerevisiae. FEBS J 275:2956–2964. doi:10.1111/j.1742-4658.2008.06451.x
Kadosh D, Struhl K (1997) Repression by Ume6 involves recruitment of a complex containing Sin3 corepressor and Rpd3 histone deacetylase to target promoters. Cell 89:365–371
Korber P, Luckenbach T, Blaschke D, Horz W (2004) Evidence for histone eviction in trans upon induction of the yeast PHO5 promoter. Mol Cell Biol 24:10965–10974
Li B, Carey M, Workman JL (2007) The role of chromatin during transcription. Cell 128:707–719. doi:10.1016/j.cell.2007.01.015
Lin LJ, Schultz MC (2011) Promoter regulation by distinct mechanisms of functional interplay between lysine acetylase Rtt109 and histone chaperone Asf1. Proc Natl Acad Sci U S A 108:19599–19604. doi:10.1073/pnas.1111501108
Lorch Y, Maier-Davis B, Kornberg RD (2006) Chromatin remodeling by nucleosome disassembly in vitro. Proc Natl Acad Sci U S A 103:3090–3093. doi:10.1073/pnas.0511050103
Mason PB, Struhl K (2003) The FACT complex travels with elongating RNA polymerase II and is important for the fidelity of transcriptional initiation in vivo. Mol Cell Biol 23:8323–8333
Morimoto RI (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev 12:3788–3796
Schermer UJ, Korber P, Horz W (2005) Histones are incorporated in trans during reassembly of the yeast PHO5 promoter. Mol Cell 19:279–285
Schwabish MA, Struhl K (2006) Asf1 mediates histone eviction and deposition during elongation by RNA polymerase II. Mol Cell 22:415–422
Takahata S, Yu Y, Stillman DJ (2009) FACT and Asf1 regulate nucleosome dynamics and coactivator binding at the HO promoter. Mol Cell 34:405–415. doi:10.1016/j.molcel.2009.04.010
Voellmy R (2004) On mechanisms that control heat shock transcription factor activity in metazoan cells. Cell Stress Chaperones 9:122–133
Voellmy R, Boellmann F (2007) Chaperone regulation of the heat shock protein response. Adv Exp Med Biol 594:89–99
Whitehouse I, Tsukiyama T (2006) Antagonistic forces that position nucleosomes in vivo. Nat Struct Mol Biol 13:633–640. doi:10.1038/nsmb1111
Whitesell L, Lindquist S (2009) Inhibiting the transcription factor HSF1 as an anticancer strategy. Expert Opin Ther Targets 13:469–478. doi:10.1517/14728220902832697
Xin H, Takahata S, Blanksma M, McCullough L, Stillman DJ, Formosa T (2009) yFACT induces global accessibility of nucleosomal DNA without H2A-H2B displacement. Mol Cell 35:365–376. doi:10.1016/j.molcel.2009.06.024
Zhao J, Herrera-Diaz J, Gross DS (2005) Domain-wide displacement of histones by activated heat shock factor occurs independently of Swi/Snf and is not correlated with RNA polymerase II density. Mol Cell Biol 25:8985–8999
Acknowledgments
We thank Pam Crowell for the critical reading of the manuscript and helpful suggestions and Tim Formosa for the anti-Spt16 antibody. This work was supported by the National Science Foundation [MCB-1029254] and the National Institutes of Health [R03 MH097538].
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Erkina, T.Y., Erkine, A. ASF1 and the SWI/SNF complex interact functionally during nucleosome displacement, while FACT is required for nucleosome reassembly at yeast heat shock gene promoters during sustained stress. Cell Stress and Chaperones 20, 355–369 (2015). https://doi.org/10.1007/s12192-014-0556-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12192-014-0556-x