Roquin targets mRNAs in a 3′-UTR-specific manner by different modes of regulation

Katharina Essig, Nina Kronbeck, Joao C. Guimaraes, Claudia Lohs, Andreas Schlundt, Anne Hoffmann, Gesine Behrens, Sven Brenner, Joanna Kowalska, Cristina Lopez-Rodriguez, Jacek Jemielity, Helmut Holtmann, Kristin Reiche, Jörg Hackermüller, Michael Sattler, Mihaela Zavolan () and Vigo Heissmeyer ()
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Katharina Essig: Ludwig-Maximilians-Universität München
Nina Kronbeck: Ludwig-Maximilians-Universität München
Joao C. Guimaraes: Computational and Systems Biology, Biozentrum, University of Basel
Claudia Lohs: Research Unit Molecular Immune Regulation, Helmholtz Zentrum München
Andreas Schlundt: Institute of Structural Biology, Helmholtz Zentrum München
Anne Hoffmann: Helmholtz Centre for Environmental Research—UFZ
Gesine Behrens: Ludwig-Maximilians-Universität München
Sven Brenner: Research Unit Molecular Immune Regulation, Helmholtz Zentrum München
Joanna Kowalska: Division of Biophysics, Institute of Experimental Physics, Faculty of Physics, University of Warsaw
Cristina Lopez-Rodriguez: Pompeu Fabra University
Jacek Jemielity: University of Warsaw
Helmut Holtmann: Institute of Biochemistry, Hannover Medical School
Kristin Reiche: Helmholtz Centre for Environmental Research—UFZ
Jörg Hackermüller: Helmholtz Centre for Environmental Research—UFZ
Michael Sattler: Institute of Structural Biology, Helmholtz Zentrum München
Mihaela Zavolan: Computational and Systems Biology, Biozentrum, University of Basel
Vigo Heissmeyer: Ludwig-Maximilians-Universität München

Nature Communications, 2018, vol. 9, issue 1, 1-17

Abstract: Abstract The RNA-binding proteins Roquin-1 and Roquin-2 redundantly control gene expression and cell-fate decisions. Here, we show that Roquin not only interacts with stem–loop structures, but also with a linear sequence element present in about half of its targets. Comprehensive analysis of a minimal response element of the Nfkbid 3′-UTR shows that six stem–loop structures cooperate to exert robust and profound post-transcriptional regulation. Only binding of multiple Roquin proteins to several stem–loops exerts full repression, which redundantly involved deadenylation and decapping, but also translational inhibition. Globally, most Roquin targets are regulated by mRNA decay, whereas a small subset, including the Nfat5 mRNA, with more binding sites in their 3′-UTRs, are also subject to translational inhibition. These findings provide insights into how the robustness and magnitude of Roquin-mediated regulation is encoded in complex cis-elements.

Date: 2018
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DOI: 10.1038/s41467-018-06184-3

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