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Authors: Maïwen Caudron-Herger, Katharina Müller-Ott, Jan-Philipp Mallm, Caroline Marth, Ute Schmidt, Katalin Fejes-Tóth and Karsten Rippe

Maïwen Caudron-Herger

Research Group Genome Organization & Function, Deutsches Krebsforschungszentrum (DKFZ) and BioQuant, Im Neuenheimer Feld 280, 69120 Heidelberg, Germany

Katharina Müller-Ott

Research Group Genome Organization & Function, Deutsches Krebsforschungszentrum (DKFZ) and BioQuant, Im Neuenheimer Feld 280, 69120 Heidelberg, Germany

Jan-Philipp Mallm

Research Group Genome Organization & Function, Deutsches Krebsforschungszentrum (DKFZ) and BioQuant, Im Neuenheimer Feld 280, 69120 Heidelberg, Germany

Caroline Marth

Research Group Genome Organization & Function, Deutsches Krebsforschungszentrum (DKFZ) and BioQuant, Im Neuenheimer Feld 280, 69120 Heidelberg, Germany

Ute Schmidt

Research Group Intracellular RNA Trafficking, Institut de Génétique Moléculaire de Montpellier CNRS-UMR 5535, 1919 Route de Mende, 34293 Montpellier-Cedex 5, France

Katalin Fejes-Tóth

California Institute of Technology, 1200 E California Blvd, MC 156-29, 91125 Pasadena, CA, USA

Karsten Rippe

Corresponding author: Karsten.Rippe@dkfz.de
Research Group Genome Organization & Function, Deutsches Krebsforschungszentrum (DKFZ) and BioQuant, Im Neuenheimer Feld 280, 69120 Heidelberg, Germany

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.

Received: June 20, 2011; Accepted: August 12, 2011

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