Rvb1/Rvb2 proteins couple transcription and translation during glucose starvation

During times of unpredictable stress, organisms must adapt their gene expression to maximize survival. Along with changes in transcription, one conserved means of gene regulation during conditions that quickly repress translation is the formation of cytoplasmic phase-separated mRNP granules such as...

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Published in:eLife
Main Authors: Yang S Chen, Wanfu Hou, Sharon Tracy, Alex T Harvey, Vince Harjono, Fan Xu, James J Moresco, John R Yates III, Brian M Zid
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-09-01
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Online Access:https://elifesciences.org/articles/76965
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author Yang S Chen
Wanfu Hou
Sharon Tracy
Alex T Harvey
Vince Harjono
Fan Xu
James J Moresco
John R Yates III
Brian M Zid
author_facet Yang S Chen
Wanfu Hou
Sharon Tracy
Alex T Harvey
Vince Harjono
Fan Xu
James J Moresco
John R Yates III
Brian M Zid
author_sort Yang S Chen
collection DOAJ
container_title eLife
description During times of unpredictable stress, organisms must adapt their gene expression to maximize survival. Along with changes in transcription, one conserved means of gene regulation during conditions that quickly repress translation is the formation of cytoplasmic phase-separated mRNP granules such as P-bodies and stress granules. Previously, we identified that distinct steps in gene expression can be coupled during glucose starvation as promoter sequences in the nucleus are able to direct the subcellular localization and translatability of mRNAs in the cytosol. Here, we report that Rvb1 and Rvb2, conserved ATPase proteins implicated as protein assembly chaperones and chromatin remodelers, were enriched at the promoters and mRNAs of genes involved in alternative glucose metabolism pathways that we previously found to be transcriptionally upregulated but translationally downregulated during glucose starvation in yeast. Engineered Rvb1/Rvb2-binding on mRNAs was sufficient to sequester mRNAs into mRNP granules and repress their translation. Additionally, this Rvb tethering to the mRNA drove further transcriptional upregulation of the target genes. Further, we found that depletion of Rvb2 caused decreased alternative glucose metabolism gene mRNA induction, but upregulation of protein synthesis during glucose starvation. Overall, our results point to Rvb1/Rvb2 coupling transcription, mRNA granular localization, and translatability of mRNAs during glucose starvation. This Rvb-mediated rapid gene regulation could potentially serve as an efficient recovery plan for cells after stress removal.
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spelling doaj-art-9a40172625d64ca686f4f4c4e251ccc32025-08-19T21:23:40ZengeLife Sciences Publications LtdeLife2050-084X2022-09-011110.7554/eLife.76965Rvb1/Rvb2 proteins couple transcription and translation during glucose starvationYang S Chen0https://orcid.org/0000-0003-3174-091XWanfu Hou1Sharon Tracy2Alex T Harvey3Vince Harjono4Fan Xu5https://orcid.org/0000-0002-0041-4276James J Moresco6John R Yates III7https://orcid.org/0000-0001-5267-1672Brian M Zid8https://orcid.org/0000-0003-1876-2479Division of Biological Sciences, University of California, San Diego, San Diego, United States; Department of Chemistry and Biochemistry, University of California San Diego, San Diego, United StatesDepartment of Chemistry and Biochemistry, University of California San Diego, San Diego, United StatesDepartment of Chemistry and Biochemistry, University of California San Diego, San Diego, United StatesDepartment of Chemistry and Biochemistry, University of California San Diego, San Diego, United StatesDepartment of Chemistry and Biochemistry, University of California San Diego, San Diego, United StatesDivision of Biological Sciences, University of California, San Diego, San Diego, United StatesDepartment of Chemical Physiology, The Scripps Research Institute, La Jolla, United StatesDepartment of Chemical Physiology, The Scripps Research Institute, La Jolla, United StatesDepartment of Chemistry and Biochemistry, University of California San Diego, San Diego, United StatesDuring times of unpredictable stress, organisms must adapt their gene expression to maximize survival. Along with changes in transcription, one conserved means of gene regulation during conditions that quickly repress translation is the formation of cytoplasmic phase-separated mRNP granules such as P-bodies and stress granules. Previously, we identified that distinct steps in gene expression can be coupled during glucose starvation as promoter sequences in the nucleus are able to direct the subcellular localization and translatability of mRNAs in the cytosol. Here, we report that Rvb1 and Rvb2, conserved ATPase proteins implicated as protein assembly chaperones and chromatin remodelers, were enriched at the promoters and mRNAs of genes involved in alternative glucose metabolism pathways that we previously found to be transcriptionally upregulated but translationally downregulated during glucose starvation in yeast. Engineered Rvb1/Rvb2-binding on mRNAs was sufficient to sequester mRNAs into mRNP granules and repress their translation. Additionally, this Rvb tethering to the mRNA drove further transcriptional upregulation of the target genes. Further, we found that depletion of Rvb2 caused decreased alternative glucose metabolism gene mRNA induction, but upregulation of protein synthesis during glucose starvation. Overall, our results point to Rvb1/Rvb2 coupling transcription, mRNA granular localization, and translatability of mRNAs during glucose starvation. This Rvb-mediated rapid gene regulation could potentially serve as an efficient recovery plan for cells after stress removal.https://elifesciences.org/articles/76965stress granulestranslationyeastgene expressionstresscotranscriptional loading
spellingShingle Yang S Chen
Wanfu Hou
Sharon Tracy
Alex T Harvey
Vince Harjono
Fan Xu
James J Moresco
John R Yates III
Brian M Zid
Rvb1/Rvb2 proteins couple transcription and translation during glucose starvation
stress granules
translation
yeast
gene expression
stress
cotranscriptional loading
title Rvb1/Rvb2 proteins couple transcription and translation during glucose starvation
title_full Rvb1/Rvb2 proteins couple transcription and translation during glucose starvation
title_fullStr Rvb1/Rvb2 proteins couple transcription and translation during glucose starvation
title_full_unstemmed Rvb1/Rvb2 proteins couple transcription and translation during glucose starvation
title_short Rvb1/Rvb2 proteins couple transcription and translation during glucose starvation
title_sort rvb1 rvb2 proteins couple transcription and translation during glucose starvation
topic stress granules
translation
yeast
gene expression
stress
cotranscriptional loading
url https://elifesciences.org/articles/76965
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