A novel translational control mechanism involving RNA structures within coding sequences

  1. Juana Díez1
  1. 1Molecular Virology Group, Department of Experimental and Health Sciences, Universitat Pompeu Fabra, 08003 Barcelona, Spain;
  2. 2Max Planck Research Group for RNA Biology, Max Planck Institute for Molecular Biomedicine, 48149 Münster, Germany;
  3. 3Cells-in-Motion Cluster of Excellence, University of Münster, 48149 Münster, Germany;
  4. 4Research Programme on Biomedical Informatics (GRIB), Department of Experimental and Health Sciences, Universitat Pompeu Fabra, Hospital del Mar Medical Research Institute (IMIM), 08003 Barcelona, Spain;
  5. 5Institute for Molecular Biology, Göttingen University Medical Department, 37073 Göttingen, Germany;
  6. 6Program of Cancer Research, Hospital del Mar Medical Research Institute (IMIM), 08003 Barcelona, Spain;
  7. 7Statistical Genomics, Centro Nacional de Analisis Genomica, 08028 Barcelona, Spain;
  8. 8Göttingen Center for Molecular Biosciences, Georg-August University, 37073 Göttingen, Germany;
  9. 9Faculty of Medicine, University of Münster, 48149 Münster, Germany
  1. Corresponding author: juana.diez{at}upf.edu
  1. 10 These authors contributed equally to this work.

Abstract

The impact of RNA structures in coding sequences (CDS) within mRNAs is poorly understood. Here, we identify a novel and highly conserved mechanism of translational control involving RNA structures within coding sequences and the DEAD-box helicase Dhh1. Using yeast genetics and genome-wide ribosome profiling analyses, we show that this mechanism, initially derived from studies of the Brome Mosaic virus RNA genome, extends to yeast and human mRNAs highly enriched in membrane and secreted proteins. All Dhh1-dependent mRNAs, viral and cellular, share key common features. First, they contain long and highly structured CDSs, including a region located around nucleotide 70 after the translation initiation site; second, they are directly bound by Dhh1 with a specific binding distribution; and third, complementary experimental approaches suggest that they are activated by Dhh1 at the translation initiation step. Our results show that ribosome translocation is not the only unwinding force of CDS and uncover a novel layer of translational control that involves RNA helicases and RNA folding within CDS providing novel opportunities for regulation of membrane and secretome proteins.

Footnotes

  • Received April 26, 2016.
  • Accepted November 3, 2016.

This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.

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