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Acute ethanol stress induces sumoylation of conserved chromatin structural proteins in Saccharomyces cerevisiae

Stress is ubiquitous to life and can irreparably damage essential biomolecules and organelles in cells. To survive, organisms must sense and adapt to stressful conditions. One highly conserved adaptive stress response is through the posttranslational modification of proteins by the small ubiquitin-l...

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Autores principales: Bradley, Amanda I., Marsh, Nicole M., Borror, Heather R., Mostoller, Kaitlyn E., Gama, Amber I., Gardner, Richard G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8351541/
https://www.ncbi.nlm.nih.gov/pubmed/33788582
http://dx.doi.org/10.1091/mbc.E20-11-0715
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author Bradley, Amanda I.
Marsh, Nicole M.
Borror, Heather R.
Mostoller, Kaitlyn E.
Gama, Amber I.
Gardner, Richard G.
author_facet Bradley, Amanda I.
Marsh, Nicole M.
Borror, Heather R.
Mostoller, Kaitlyn E.
Gama, Amber I.
Gardner, Richard G.
author_sort Bradley, Amanda I.
collection PubMed
description Stress is ubiquitous to life and can irreparably damage essential biomolecules and organelles in cells. To survive, organisms must sense and adapt to stressful conditions. One highly conserved adaptive stress response is through the posttranslational modification of proteins by the small ubiquitin-like modifier (SUMO). Here, we examine the effects of acute ethanol stress on protein sumoylation in the budding yeast Saccharomyces cerevisiae. We found that cells exhibit a transient sumoylation response after acute exposure to ≤7.5% vol/vol ethanol. By contrast, the sumoylation response becomes chronic at 10% ethanol exposure. Mass spectrometry analyses identified 18 proteins that are sumoylated after acute ethanol exposure, with 15 known to associate with chromatin. Upon further analysis, we found that the chromatin structural proteins Smc5 and Smc6 undergo ethanol-induced sumoylation that depends on the activity of the E3 SUMO ligase Mms21. Using cell-cycle arrest assays, we observed that Smc5 and Smc6 ethanol-induced sumoylation occurs during G1 and G2/M phases but not S phase. Acute ethanol exposure also resulted in the formation of Rad52 foci at levels comparable to Rad52 foci formation after exposure to the DNA alkylating agent methyl methanesulfonate (MMS). MMS exposure is known to induce the intra-S-phase DNA damage checkpoint via Rad53 phosphorylation, but ethanol exposure did not induce Rad53 phosphorylation. Ethanol abrogated the effect of MMS on Rad53 phosphorylation when added simultaneously. From these studies, we propose that acute ethanol exposure induces a change in chromatin leading to sumoylation of specific chromatin structural proteins.
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spelling pubmed-83515412021-08-10 Acute ethanol stress induces sumoylation of conserved chromatin structural proteins in Saccharomyces cerevisiae Bradley, Amanda I. Marsh, Nicole M. Borror, Heather R. Mostoller, Kaitlyn E. Gama, Amber I. Gardner, Richard G. Mol Biol Cell Articles Stress is ubiquitous to life and can irreparably damage essential biomolecules and organelles in cells. To survive, organisms must sense and adapt to stressful conditions. One highly conserved adaptive stress response is through the posttranslational modification of proteins by the small ubiquitin-like modifier (SUMO). Here, we examine the effects of acute ethanol stress on protein sumoylation in the budding yeast Saccharomyces cerevisiae. We found that cells exhibit a transient sumoylation response after acute exposure to ≤7.5% vol/vol ethanol. By contrast, the sumoylation response becomes chronic at 10% ethanol exposure. Mass spectrometry analyses identified 18 proteins that are sumoylated after acute ethanol exposure, with 15 known to associate with chromatin. Upon further analysis, we found that the chromatin structural proteins Smc5 and Smc6 undergo ethanol-induced sumoylation that depends on the activity of the E3 SUMO ligase Mms21. Using cell-cycle arrest assays, we observed that Smc5 and Smc6 ethanol-induced sumoylation occurs during G1 and G2/M phases but not S phase. Acute ethanol exposure also resulted in the formation of Rad52 foci at levels comparable to Rad52 foci formation after exposure to the DNA alkylating agent methyl methanesulfonate (MMS). MMS exposure is known to induce the intra-S-phase DNA damage checkpoint via Rad53 phosphorylation, but ethanol exposure did not induce Rad53 phosphorylation. Ethanol abrogated the effect of MMS on Rad53 phosphorylation when added simultaneously. From these studies, we propose that acute ethanol exposure induces a change in chromatin leading to sumoylation of specific chromatin structural proteins. The American Society for Cell Biology 2021-05-15 /pmc/articles/PMC8351541/ /pubmed/33788582 http://dx.doi.org/10.1091/mbc.E20-11-0715 Text en © 2021 Bradley et al. “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology. https://creativecommons.org/licenses/by-nc-sa/3.0/This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License.
spellingShingle Articles
Bradley, Amanda I.
Marsh, Nicole M.
Borror, Heather R.
Mostoller, Kaitlyn E.
Gama, Amber I.
Gardner, Richard G.
Acute ethanol stress induces sumoylation of conserved chromatin structural proteins in Saccharomyces cerevisiae
title Acute ethanol stress induces sumoylation of conserved chromatin structural proteins in Saccharomyces cerevisiae
title_full Acute ethanol stress induces sumoylation of conserved chromatin structural proteins in Saccharomyces cerevisiae
title_fullStr Acute ethanol stress induces sumoylation of conserved chromatin structural proteins in Saccharomyces cerevisiae
title_full_unstemmed Acute ethanol stress induces sumoylation of conserved chromatin structural proteins in Saccharomyces cerevisiae
title_short Acute ethanol stress induces sumoylation of conserved chromatin structural proteins in Saccharomyces cerevisiae
title_sort acute ethanol stress induces sumoylation of conserved chromatin structural proteins in saccharomyces cerevisiae
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8351541/
https://www.ncbi.nlm.nih.gov/pubmed/33788582
http://dx.doi.org/10.1091/mbc.E20-11-0715
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