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Dynamic sumoylation of a conserved transcription corepressor prevents persistent inclusion formation during hyperosmotic stress

Dynamic sumoylation of a conserved transcription corepressor prevents persistent inclusion formation during hyperosmotic stress
Dynamic sumoylation of a conserved transcription corepressor prevents persistent inclusion formation during hyperosmotic stress
Cells are often exposed to physical or chemical stresses that can damage the structures of essential biomolecules. Stress-induced cellular damage can become deleterious if not managed appropriately. Rapid and adaptive responses to stresses are therefore crucial for cell survival. In eukaryotic cells, different stresses trigger post-translational modification of proteins with the small ubiquitin-like modifier SUMO. However, the specific regulatory roles of sumoylation in each stress response are not well understood. Here, we examined the sumoylation events that occur in budding yeast after exposure to hyperosmotic stress. We discovered by proteomic and biochemical analyses that hyperosmotic stress incurs the rapid and transient sumoylation of Cyc8 and Tup1, which together form a conserved transcription corepressor complex that regulates hundreds of genes. Gene expression and cell biological analyses revealed that sumoylation of each protein directs distinct outcomes. In particular, we discovered that Cyc8 sumoylation prevents the persistence of hyperosmotic stress-induced Cyc8-Tup1 inclusions, which involves a glutamine-rich prion domain in Cyc8. We propose that sumoylation protects against persistent inclusion formation during hyperosmotic stress, allowing optimal transcriptional function of the Cyc8-Tup1 complex.
Gene Expression Regulation, Fungal, Osmotic Pressure, Promoter Regions, Genetic, Proteomics, Repressor Proteins/biosynthesis, Saccharomyces cerevisiae, Sumoylation/genetics, Transcription, Genetic
1553-7390
e1005809
Oeser, Michelle L
3fe66ab8-6a12-442b-b21b-82116ca2b456
Amen, Triana
388dc540-e819-4d07-8f1e-ee0f3949a54b
Nadel, Cory M
de529d5d-3960-404b-9c54-5407b8b1e4ff
Bradley, Amanda I
8036416d-9110-4a5b-bdb1-7f38ee89c165
Reed, Benjamin J
7a885c4d-ccf6-49a6-bd12-873ca52dd09e
Jones, Ramon D
333033c9-ad6a-4972-80b6-4a7ee26d5083
Gopalan, Janani
d1ccfec4-9919-4d37-8d53-606d9b477f5f
Kaganovich, Daniel
ebb13f4e-e925-4aef-88e7-ddc25ef52d8f
Gardner, Richard G
0e858b70-0e70-4b2b-9080-0389b6a4f6e4
et al.
Oeser, Michelle L
3fe66ab8-6a12-442b-b21b-82116ca2b456
Amen, Triana
388dc540-e819-4d07-8f1e-ee0f3949a54b
Nadel, Cory M
de529d5d-3960-404b-9c54-5407b8b1e4ff
Bradley, Amanda I
8036416d-9110-4a5b-bdb1-7f38ee89c165
Reed, Benjamin J
7a885c4d-ccf6-49a6-bd12-873ca52dd09e
Jones, Ramon D
333033c9-ad6a-4972-80b6-4a7ee26d5083
Gopalan, Janani
d1ccfec4-9919-4d37-8d53-606d9b477f5f
Kaganovich, Daniel
ebb13f4e-e925-4aef-88e7-ddc25ef52d8f
Gardner, Richard G
0e858b70-0e70-4b2b-9080-0389b6a4f6e4

Oeser, Michelle L, Amen, Triana, Nadel, Cory M and Kaganovich, Daniel , et al. (2016) Dynamic sumoylation of a conserved transcription corepressor prevents persistent inclusion formation during hyperosmotic stress. PLoS Genetics, 12 (1), e1005809. (doi:10.1371/journal.pgen.1005809).

Record type: Article

Abstract

Cells are often exposed to physical or chemical stresses that can damage the structures of essential biomolecules. Stress-induced cellular damage can become deleterious if not managed appropriately. Rapid and adaptive responses to stresses are therefore crucial for cell survival. In eukaryotic cells, different stresses trigger post-translational modification of proteins with the small ubiquitin-like modifier SUMO. However, the specific regulatory roles of sumoylation in each stress response are not well understood. Here, we examined the sumoylation events that occur in budding yeast after exposure to hyperosmotic stress. We discovered by proteomic and biochemical analyses that hyperosmotic stress incurs the rapid and transient sumoylation of Cyc8 and Tup1, which together form a conserved transcription corepressor complex that regulates hundreds of genes. Gene expression and cell biological analyses revealed that sumoylation of each protein directs distinct outcomes. In particular, we discovered that Cyc8 sumoylation prevents the persistence of hyperosmotic stress-induced Cyc8-Tup1 inclusions, which involves a glutamine-rich prion domain in Cyc8. We propose that sumoylation protects against persistent inclusion formation during hyperosmotic stress, allowing optimal transcriptional function of the Cyc8-Tup1 complex.

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More information

Published date: 22 January 2016
Keywords: Gene Expression Regulation, Fungal, Osmotic Pressure, Promoter Regions, Genetic, Proteomics, Repressor Proteins/biosynthesis, Saccharomyces cerevisiae, Sumoylation/genetics, Transcription, Genetic

Identifiers

Local EPrints ID: 475607
URI: http://eprints.soton.ac.uk/id/eprint/475607
ISSN: 1553-7390
PURE UUID: 4025fc87-fbc2-4d1a-800f-efb4de9b7fab
ORCID for Triana Amen: ORCID iD orcid.org/0000-0003-4808-7806
ORCID for Daniel Kaganovich: ORCID iD orcid.org/0000-0003-2398-1596

Catalogue record

Date deposited: 22 Mar 2023 17:40
Last modified: 17 Mar 2024 04:22

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Contributors

Author: Michelle L Oeser
Author: Triana Amen ORCID iD
Author: Cory M Nadel
Author: Amanda I Bradley
Author: Benjamin J Reed
Author: Ramon D Jones
Author: Janani Gopalan
Author: Daniel Kaganovich ORCID iD
Author: Richard G Gardner
Corporate Author: et al.

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