H3K4 monomethylation dictates nucleosome dynamics and chromatin remodeling at stress-responsive genes

Chromatin remodeling is essential for proper adaptation to extracellular stimuli. The p38-related Hog1 SAPK is an important regulator of transcription that mediates chromatin remodeling upon stress. Hog1 targets the RSC chromatin remodeling complex to stress-responsive genes and rsc deficient cells...

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Authors: Nadal Ribelles, Mariona, 1984-, Mas Martín, Glòria, Millán Zambrano, Gonzalo, Solé, Carme, Ammerer, Gustav, Chávez, Sebastián, Posas Garriga, Francesc, Nadal Clanchet, Eulàlia de
Format: article
Status:Published version
Publication Date:2015
Country:España
Institution:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
Repository:Recercat. Dipósit de la Recerca de Catalunya
OAI Identifier:oai:recercat.cat:10230/25728
Online Access:http://hdl.handle.net/10230/25728
http://dx.doi.org/10.1093/nar/gkv220
Access Level:Open access
Keyword:Saccharomyces cerevisiae -- Metabolisme
Histones
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spelling H3K4 monomethylation dictates nucleosome dynamics and chromatin remodeling at stress-responsive genesNadal Ribelles, Mariona, 1984-Mas Martín, GlòriaMillán Zambrano, GonzaloSolé, CarmeAmmerer, GustavChávez, SebastiánPosas Garriga, FrancescNadal Clanchet, Eulàlia deSaccharomyces cerevisiae -- MetabolismeHistonesChromatin remodeling is essential for proper adaptation to extracellular stimuli. The p38-related Hog1 SAPK is an important regulator of transcription that mediates chromatin remodeling upon stress. Hog1 targets the RSC chromatin remodeling complex to stress-responsive genes and rsc deficient cells display reduced induction of gene expression. Here we show that the absence of H3K4 methylation, either achieved by deletion of the SET1 methyltransferase or by amino acid substitution of H3K4, bypasses the requirement of RSC for stress-responsive gene expression. Monomethylation of H3K4 is specifically inhibiting RSC-independent chromatin remodeling and thus, it prevents osmostress-induced gene expression. The absence of H3K4 monomethylation permits that the association of alternative remodelers with stress-responsive genes and the Swr1 complex (SWR-C) is instrumental in the induction of gene expression upon stress. Accordingly, the absence of SWR-C or histone H2A.Z results in compromised chromatin remodeling and impaired gene expression in the absence of RSC and H3K4 methylation. These results indicate that expression of stress-responsive genes is controlled by two remodeling mechanisms: RSC in the presence of monomethylated H3K4, and SWR-C in the absence of H3K4 monomethylation. Our findings point to a novel role for H3K4 monomethylation in dictating the specificity of chromatin remodeling, adding an extra layer of regulation to the transcriptional stress response.M.N. was a recipient of an FIS fellowship. G.M.Z. was a recipient of an FPU fellowship from the Spanish Government. Spanish Ministry of Economy and Competitiveness [BFU2012–33503 and FEDER to F.P., BFU2011–26722 to E.N., BFU2013–48643-C3–1-P and FEDER to S.C.]; Catalan Government (2014 SGR 599) and the Andalusian Government [BIO-271; P12-BIO-1938 and FEDER to S.C.]. Fundación Botín, by Banco Santander through its Santander Universities Global Division to F.P. F.P. and E.N. are recipients of an ICREA Acadèmia (Generalitat de Catalunya). The authors declare no competing financial interest. Funding for open access charge: Spanish Ministry of Economy and Competitiveness [BFU2012-33503 and FEDER to F.P.].Oxford University Press201620162015info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/25728http://dx.doi.org/10.1093/nar/gkv220reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésNucleic Acids Research. 2015;43(10):4937-49info:eu-repo/grantAgreement/ES/3PN/BFU2012–33503info:eu-repo/grantAgreement/ES/3PN/BFU2011–26722info:eu-repo/grantAgreement/ES/1PE/BFU2013–48643© The Author(s) 2015. Published by Oxford University Press on behalf of Nucleic Acids Research./nThis is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly citedhttp://creativecommons.org/licenses/by-nc/4.0/info:eu-repo/semantics/openAccessoai:recercat.cat:10230/257282026-05-29T05:05:01Z
dc.title.none.fl_str_mv H3K4 monomethylation dictates nucleosome dynamics and chromatin remodeling at stress-responsive genes
title H3K4 monomethylation dictates nucleosome dynamics and chromatin remodeling at stress-responsive genes
spellingShingle H3K4 monomethylation dictates nucleosome dynamics and chromatin remodeling at stress-responsive genes
Nadal Ribelles, Mariona, 1984-
Saccharomyces cerevisiae -- Metabolisme
Histones
title_short H3K4 monomethylation dictates nucleosome dynamics and chromatin remodeling at stress-responsive genes
title_full H3K4 monomethylation dictates nucleosome dynamics and chromatin remodeling at stress-responsive genes
title_fullStr H3K4 monomethylation dictates nucleosome dynamics and chromatin remodeling at stress-responsive genes
title_full_unstemmed H3K4 monomethylation dictates nucleosome dynamics and chromatin remodeling at stress-responsive genes
title_sort H3K4 monomethylation dictates nucleosome dynamics and chromatin remodeling at stress-responsive genes
dc.creator.none.fl_str_mv Nadal Ribelles, Mariona, 1984-
Mas Martín, Glòria
Millán Zambrano, Gonzalo
Solé, Carme
Ammerer, Gustav
Chávez, Sebastián
Posas Garriga, Francesc
Nadal Clanchet, Eulàlia de
author Nadal Ribelles, Mariona, 1984-
author_facet Nadal Ribelles, Mariona, 1984-
Mas Martín, Glòria
Millán Zambrano, Gonzalo
Solé, Carme
Ammerer, Gustav
Chávez, Sebastián
Posas Garriga, Francesc
Nadal Clanchet, Eulàlia de
author_role author
author2 Mas Martín, Glòria
Millán Zambrano, Gonzalo
Solé, Carme
Ammerer, Gustav
Chávez, Sebastián
Posas Garriga, Francesc
Nadal Clanchet, Eulàlia de
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Saccharomyces cerevisiae -- Metabolisme
Histones
topic Saccharomyces cerevisiae -- Metabolisme
Histones
description Chromatin remodeling is essential for proper adaptation to extracellular stimuli. The p38-related Hog1 SAPK is an important regulator of transcription that mediates chromatin remodeling upon stress. Hog1 targets the RSC chromatin remodeling complex to stress-responsive genes and rsc deficient cells display reduced induction of gene expression. Here we show that the absence of H3K4 methylation, either achieved by deletion of the SET1 methyltransferase or by amino acid substitution of H3K4, bypasses the requirement of RSC for stress-responsive gene expression. Monomethylation of H3K4 is specifically inhibiting RSC-independent chromatin remodeling and thus, it prevents osmostress-induced gene expression. The absence of H3K4 monomethylation permits that the association of alternative remodelers with stress-responsive genes and the Swr1 complex (SWR-C) is instrumental in the induction of gene expression upon stress. Accordingly, the absence of SWR-C or histone H2A.Z results in compromised chromatin remodeling and impaired gene expression in the absence of RSC and H3K4 methylation. These results indicate that expression of stress-responsive genes is controlled by two remodeling mechanisms: RSC in the presence of monomethylated H3K4, and SWR-C in the absence of H3K4 monomethylation. Our findings point to a novel role for H3K4 monomethylation in dictating the specificity of chromatin remodeling, adding an extra layer of regulation to the transcriptional stress response.
publishDate 2015
dc.date.none.fl_str_mv 2015
2016
2016
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10230/25728
http://dx.doi.org/10.1093/nar/gkv220
url http://hdl.handle.net/10230/25728
http://dx.doi.org/10.1093/nar/gkv220
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Nucleic Acids Research. 2015;43(10):4937-49
info:eu-repo/grantAgreement/ES/3PN/BFU2012–33503
info:eu-repo/grantAgreement/ES/3PN/BFU2011–26722
info:eu-repo/grantAgreement/ES/1PE/BFU2013–48643
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by-nc/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by-nc/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:Recercat. Dipósit de la Recerca de Catalunya
instname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
instname_str Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
reponame_str Recercat. Dipósit de la Recerca de Catalunya
collection Recercat. Dipósit de la Recerca de Catalunya
repository.name.fl_str_mv
repository.mail.fl_str_mv
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