Glucose stress causes mRNA retention in nuclear Nab2 condensates

Summary: Nuclear mRNA export via nuclear pore complexes is an essential step in eukaryotic gene expression. Although factors involved in mRNA transport have been characterized, a comprehensive mechanistic understanding of this process and its regulation is lacking. Here, we use single-RNA imaging in...

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Main Authors: Stephanie Heinrich, Maria Hondele, Désirée Marchand, Carina Patrizia Derrer, Mostafa Zedan, Alexandra Oswald, Liliana Malinovska, Federico Uliana, Sarah Khawaja, Roberta Mancini, David Grunwald, Karsten Weis
Format: Article
Language:English
Published: Elsevier 2024-01-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124723016054
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author Stephanie Heinrich
Maria Hondele
Désirée Marchand
Carina Patrizia Derrer
Mostafa Zedan
Alexandra Oswald
Liliana Malinovska
Federico Uliana
Sarah Khawaja
Roberta Mancini
David Grunwald
Karsten Weis
author_facet Stephanie Heinrich
Maria Hondele
Désirée Marchand
Carina Patrizia Derrer
Mostafa Zedan
Alexandra Oswald
Liliana Malinovska
Federico Uliana
Sarah Khawaja
Roberta Mancini
David Grunwald
Karsten Weis
author_sort Stephanie Heinrich
collection DOAJ
description Summary: Nuclear mRNA export via nuclear pore complexes is an essential step in eukaryotic gene expression. Although factors involved in mRNA transport have been characterized, a comprehensive mechanistic understanding of this process and its regulation is lacking. Here, we use single-RNA imaging in yeast to show that cells use mRNA retention to control mRNA export during stress. We demonstrate that, upon glucose withdrawal, the essential RNA-binding factor Nab2 forms RNA-dependent condensate-like structures in the nucleus. This coincides with a reduced abundance of the DEAD-box ATPase Dbp5 at the nuclear pore. Depleting Dbp5, and consequently blocking mRNA export, is necessary and sufficient to trigger Nab2 condensation. The state of Nab2 condensation influences the extent of nuclear mRNA accumulation and can be recapitulated in vitro, where Nab2 forms RNA-dependent liquid droplets. We hypothesize that cells use condensation to regulate mRNA export and control gene expression during stress.
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spelling doaj.art-0f3d664a1d67456e919f84eb1b35c85e2023-12-20T07:34:17ZengElsevierCell Reports2211-12472024-01-01431113593Glucose stress causes mRNA retention in nuclear Nab2 condensatesStephanie Heinrich0Maria Hondele1Désirée Marchand2Carina Patrizia Derrer3Mostafa Zedan4Alexandra Oswald5Liliana Malinovska6Federico Uliana7Sarah Khawaja8Roberta Mancini9David Grunwald10Karsten Weis11Department of Biology, Institute of Biochemistry, Swiss Federal Institute of Technology (ETH), 8093 Zurich, Switzerland; Corresponding authorDepartment of Biology, Institute of Biochemistry, Swiss Federal Institute of Technology (ETH), 8093 Zurich, Switzerland; Biozentrum, Center for Molecular Life Sciences, University of Basel, 4056 Basel, SwitzerlandDepartment of Biology, Institute of Biochemistry, Swiss Federal Institute of Technology (ETH), 8093 Zurich, SwitzerlandDepartment of Biology, Institute of Biochemistry, Swiss Federal Institute of Technology (ETH), 8093 Zurich, SwitzerlandDepartment of Biology, Institute of Biochemistry, Swiss Federal Institute of Technology (ETH), 8093 Zurich, SwitzerlandDepartment of Biology, Institute of Biochemistry, Swiss Federal Institute of Technology (ETH), 8093 Zurich, SwitzerlandDepartment of Biology, Institute of Molecular Systems Biology, Swiss Federal Institute of Technology (ETH), 8093 Zurich, SwitzerlandDepartment of Biology, Institute of Biochemistry, Swiss Federal Institute of Technology (ETH), 8093 Zurich, SwitzerlandDepartment of Biology, Institute of Biochemistry, Swiss Federal Institute of Technology (ETH), 8093 Zurich, SwitzerlandDepartment of Biology, Institute of Biochemistry, Swiss Federal Institute of Technology (ETH), 8093 Zurich, SwitzerlandUniversity of Massachusetts Chan Medical School, RNA Therapeutics Institute, Worcester, MA 01605, USADepartment of Biology, Institute of Biochemistry, Swiss Federal Institute of Technology (ETH), 8093 Zurich, Switzerland; Corresponding authorSummary: Nuclear mRNA export via nuclear pore complexes is an essential step in eukaryotic gene expression. Although factors involved in mRNA transport have been characterized, a comprehensive mechanistic understanding of this process and its regulation is lacking. Here, we use single-RNA imaging in yeast to show that cells use mRNA retention to control mRNA export during stress. We demonstrate that, upon glucose withdrawal, the essential RNA-binding factor Nab2 forms RNA-dependent condensate-like structures in the nucleus. This coincides with a reduced abundance of the DEAD-box ATPase Dbp5 at the nuclear pore. Depleting Dbp5, and consequently blocking mRNA export, is necessary and sufficient to trigger Nab2 condensation. The state of Nab2 condensation influences the extent of nuclear mRNA accumulation and can be recapitulated in vitro, where Nab2 forms RNA-dependent liquid droplets. We hypothesize that cells use condensation to regulate mRNA export and control gene expression during stress.http://www.sciencedirect.com/science/article/pii/S2211124723016054CP: Cell biology
spellingShingle Stephanie Heinrich
Maria Hondele
Désirée Marchand
Carina Patrizia Derrer
Mostafa Zedan
Alexandra Oswald
Liliana Malinovska
Federico Uliana
Sarah Khawaja
Roberta Mancini
David Grunwald
Karsten Weis
Glucose stress causes mRNA retention in nuclear Nab2 condensates
Cell Reports
CP: Cell biology
title Glucose stress causes mRNA retention in nuclear Nab2 condensates
title_full Glucose stress causes mRNA retention in nuclear Nab2 condensates
title_fullStr Glucose stress causes mRNA retention in nuclear Nab2 condensates
title_full_unstemmed Glucose stress causes mRNA retention in nuclear Nab2 condensates
title_short Glucose stress causes mRNA retention in nuclear Nab2 condensates
title_sort glucose stress causes mrna retention in nuclear nab2 condensates
topic CP: Cell biology
url http://www.sciencedirect.com/science/article/pii/S2211124723016054
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