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SWI/SNF regulates half of its targets without the need of ATP-driven nucleosome remodeling by Brahma

BACKGROUND: Brahma (BRM) is the only catalytic subunit of the SWI/SNF chromatin-remodeling complex of Drosophila melanogaster. The function of SWI/SNF in transcription has long been attributed to its ability to remodel nucleosomes, which requires the ATPase activity of BRM. However, recent studies h...

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Autores principales: Jordán-Pla, Antonio, Yu, Simei, Waldholm, Johan, Källman, Thomas, Östlund Farrants, Ann-Kristin, Visa, Neus
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5960078/
https://www.ncbi.nlm.nih.gov/pubmed/29776334
http://dx.doi.org/10.1186/s12864-018-4746-2
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author Jordán-Pla, Antonio
Yu, Simei
Waldholm, Johan
Källman, Thomas
Östlund Farrants, Ann-Kristin
Visa, Neus
author_facet Jordán-Pla, Antonio
Yu, Simei
Waldholm, Johan
Källman, Thomas
Östlund Farrants, Ann-Kristin
Visa, Neus
author_sort Jordán-Pla, Antonio
collection PubMed
description BACKGROUND: Brahma (BRM) is the only catalytic subunit of the SWI/SNF chromatin-remodeling complex of Drosophila melanogaster. The function of SWI/SNF in transcription has long been attributed to its ability to remodel nucleosomes, which requires the ATPase activity of BRM. However, recent studies have provided evidence for a non-catalytic function of BRM in the transcriptional regulation of a few specific genes. RESULTS: Here we have used RNA-seq and ChIP-seq to identify the BRM target genes in S2 cells, and we have used a catalytically inactive BRM mutant (K804R) that is unable to hydrolyze ATP to investigate the magnitude of the non-catalytic function of BRM in transcription regulation. We show that 49% of the BRM target genes in S2 cells are regulated through mechanisms that do not require BRM to have an ATPase activity. We also show that the catalytic and non-catalytic mechanisms of SWI/SNF regulation operate on two subsets of genes that differ in promoter architecture and are linked to different biological processes. CONCLUSIONS: This study shows that the non-catalytic role of SWI/SNF in transcription regulation is far more prevalent than previously anticipated and that the genes that are regulated by SWI/SNF through ATPase-dependent and ATPase-independent mechanisms have specialized roles in different cellular and developmental processes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4746-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-59600782018-05-24 SWI/SNF regulates half of its targets without the need of ATP-driven nucleosome remodeling by Brahma Jordán-Pla, Antonio Yu, Simei Waldholm, Johan Källman, Thomas Östlund Farrants, Ann-Kristin Visa, Neus BMC Genomics Research Article BACKGROUND: Brahma (BRM) is the only catalytic subunit of the SWI/SNF chromatin-remodeling complex of Drosophila melanogaster. The function of SWI/SNF in transcription has long been attributed to its ability to remodel nucleosomes, which requires the ATPase activity of BRM. However, recent studies have provided evidence for a non-catalytic function of BRM in the transcriptional regulation of a few specific genes. RESULTS: Here we have used RNA-seq and ChIP-seq to identify the BRM target genes in S2 cells, and we have used a catalytically inactive BRM mutant (K804R) that is unable to hydrolyze ATP to investigate the magnitude of the non-catalytic function of BRM in transcription regulation. We show that 49% of the BRM target genes in S2 cells are regulated through mechanisms that do not require BRM to have an ATPase activity. We also show that the catalytic and non-catalytic mechanisms of SWI/SNF regulation operate on two subsets of genes that differ in promoter architecture and are linked to different biological processes. CONCLUSIONS: This study shows that the non-catalytic role of SWI/SNF in transcription regulation is far more prevalent than previously anticipated and that the genes that are regulated by SWI/SNF through ATPase-dependent and ATPase-independent mechanisms have specialized roles in different cellular and developmental processes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4746-2) contains supplementary material, which is available to authorized users. BioMed Central 2018-05-18 /pmc/articles/PMC5960078/ /pubmed/29776334 http://dx.doi.org/10.1186/s12864-018-4746-2 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Jordán-Pla, Antonio
Yu, Simei
Waldholm, Johan
Källman, Thomas
Östlund Farrants, Ann-Kristin
Visa, Neus
SWI/SNF regulates half of its targets without the need of ATP-driven nucleosome remodeling by Brahma
title SWI/SNF regulates half of its targets without the need of ATP-driven nucleosome remodeling by Brahma
title_full SWI/SNF regulates half of its targets without the need of ATP-driven nucleosome remodeling by Brahma
title_fullStr SWI/SNF regulates half of its targets without the need of ATP-driven nucleosome remodeling by Brahma
title_full_unstemmed SWI/SNF regulates half of its targets without the need of ATP-driven nucleosome remodeling by Brahma
title_short SWI/SNF regulates half of its targets without the need of ATP-driven nucleosome remodeling by Brahma
title_sort swi/snf regulates half of its targets without the need of atp-driven nucleosome remodeling by brahma
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5960078/
https://www.ncbi.nlm.nih.gov/pubmed/29776334
http://dx.doi.org/10.1186/s12864-018-4746-2
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