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Coding RNAs with a non-coding function: Maintenance of open chromatin structure

Caudron-Herger, Maïwen and Müller-Ott, Katharina and Mallm, Jan-Philipp and Marth, Caroline and Schmidt, Ute and Fejes-Tóth, Katalin and Rippe, Karsten (2011) Coding RNAs with a non-coding function: Maintenance of open chromatin structure. Nucleus, 2 (5). pp. 410-424. ISSN 1949-1034. https://resolver.caltech.edu/CaltechAUTHORS:20200416-152054085

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Abstract

The multi-layered organization of the genome in a large nucleoprotein complex termed chromatin regulates nuclear functions by establishing subcompartments with distinct DNA-associated activities. Here, we demonstrate that RNA plays an important role in maintaining a decondensed and biologically active interphase chromatin conformation in human and mouse cell lines. As shown by RNase A microinjection and fluorescence microscopy imaging, digestion of single-stranded RNAs induced a distinct micrometer scale chromatin aggregation of these decondensed regions. In contrast, pericentric heterochromatin was more resistant to RNase A treatment. We identified a class of coding RNA transcripts that are responsible for this activity, and thus termed these ‘chromatin-interlinking’ RNAs or ciRNAs. The initial chromatin distribution could be restored after RNase A treatment with a purified nuclear RNA fraction that was analyzed by high-throughput sequencing. It comprised long >500 nucleotides (nt) RNA polymerase II (RNAP II) transcripts that were spliced, depleted of polyadenylation and was enriched with long 3'-untranslated regions (3’-UTRs) above ~800 nt in length. Furthermore, similar reversible changes of the chromatin conformation and the RNAP II distribution were induced by either RNA depletion or RNAP II inhibition. Based on these results we propose that ciRNAs could act as genome organizing architectural factors of actively transcribed chromatin compartments.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.4161/nucl.2.5.17736DOIArticle
ORCID:
AuthorORCID
Fejes-Tóth, Katalin0000-0001-6558-2636
Additional Information:© 2011 Landes Bioscience. Received 20 Jun 2011, Accepted 12 Aug 2011, Published online: 25 Oct 2011. We are grateful to Gernot Längst, Karsten Richter, Anne Seefeld, Joel Beaudouin, Nathan Brady, Undine Mechold, Thomas Sandmann, Dirk-Peter Herten and Ingrid Grummt for help and discussions, and to Greg Hannon, Peter Lichter and Roland Eils for their support of the project, and like to thank the two reviewers of the paper for their detailed and insightful comments. Parts of the fluorescence microscopy work were conducted at the DKFZ Microscopy Core Facility and the Advanced Light Microscopy Facility at the European Molecular Biology Laboratory (Heidelberg, Germany). The project was supported by a fellowship of the Christiane Nüsslein-Volhard foundation and the “For Women in Science” program of L’Oréal-UNESCO to M.C., the SBCancer program within the Helmholtz Alliance on Systems Biology and by the BMBF funded EpiGenSys project within the EraSysBio+ program. No potential conflicts of interest were disclosed.
Funders:
Funding AgencyGrant Number
Christiane Nüsslein-Volhard FoundationUNSPECIFIED
L’Oréal-UNESCO For Women in Science ProgramUNSPECIFIED
Helmholtz Alliance on Systems BiologyUNSPECIFIED
Bundesministerium für Bildung und Forschung (BMBF)UNSPECIFIED
Subject Keywords:chromatin organization, heterochromatin, fluorescence microscopy, transcriptome sequencing, nuclear architecture, untranslated RNA regions, microinjection
Issue or Number:5
Record Number:CaltechAUTHORS:20200416-152054085
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200416-152054085
Official Citation:Maïwen Caudron-Herger, Katharina Müller-Ott, Jan-Philipp Mallm, Caroline Marth, Ute Schmidt, Katalin Fejes-Tóth & Karsten Rippe (2011) Coding RNAs with a non-coding function: Maintenance of open chromatin structure, Nucleus, 2:5, 410-424, DOI: 10.4161/nucl.2.5.17736
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:102590
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:16 Apr 2020 22:34
Last Modified:16 Apr 2020 22:34

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