Proteome solubility is differentially reshaped by thermal stress and regulators of ubiquitination

The ubiquitin-proteasome system maintains proteostasis by degrading proteins that unfold and become insoluble upon stress. Some proteins have high insolubility in normal conditions because of their structure, subcellular localization, and interactions but it remains incompletely understood how the u...

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Published inThe Journal of biological chemistry Vol. 301; no. 9; p. 110517
Main Authors Hunt, Liam C., Stephan, Anna, Poudel, Suresh, Yu, Kaiwen, Kavdia, Kanisha, Pagala, Vishwajeeth R., Wang, Wei, Fu, Yingxue, Wang, Yong-Dong, Wang, Xusheng, Graca, Flavia A., Alford, Daniel, Grime, John, High, Anthony A., Peng, Junmin, Demontis, Fabio
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 01.09.2025
American Society for Biochemistry and Molecular Biology
Subjects
E2 ubiquitin-conjugating enzymes
HUWE1
insolubilome
insoluble proteins
Methods and Resources
protein-quality control
proteome solubility
thermal stress
insolubilome
insoluble proteins
E2 ubiquitin-conjugating enzymes
NT
HUWE1
PTM
TMT
thermal stress
protein-quality control
proteome solubility
Online AccessGet full text
ISSN0021-9258
1083-351X
1083-351X
DOI10.1016/j.jbc.2025.110517

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Abstract The ubiquitin-proteasome system maintains proteostasis by degrading proteins that unfold and become insoluble upon stress. Some proteins have high insolubility in normal conditions because of their structure, subcellular localization, and interactions but it remains incompletely understood how the ubiquitin-proteasome system regulates them. Here, we utilized mass spectrometry to profile heat-induced solubility changes (insolubilome) and associated post-translational modifications in human cells (http://thermal-stress-insolubilome.stjude.org). We find that the solubility of several protein categories is oppositely modulated by thermal stress. Some proteins become more soluble upon heat shock, whereas others, including several ubiquitin-conjugating enzymes, become more insoluble. By analyzing the changes in protein abundance induced by RNAi for E2 ubiquitin-conjugating enzymes, we identify E2-specific biases in targeting proteins with higher-than-average insolubility. Analysis of the E3 ubiquitin ligase HUWE1, which was previously found to detect proteins with exposed hydrophobic residues, indicates that siHUWE1-downregulated proteins have higher-than-average insolubility, suggesting that HUWE1 stabilizes subsets of insoluble proteins. Altogether, this study identifies components of the ubiquitination cascade that control and remodel the solubility of the human proteome.
AbstractList The ubiquitin-proteasome system maintains proteostasis by degrading proteins that unfold and become insoluble upon stress. Some proteins have high insolubility in normal conditions because of their structure, subcellular localization, and interactions but it remains incompletely understood how the ubiquitin-proteasome system regulates them. Here, we utilized mass spectrometry to profile heat-induced solubility changes (insolubilome) and associated post-translational modifications in human cells ( http://thermal-stress-insolubilome.stjude.org ). We find that the solubility of several protein categories is oppositely modulated by thermal stress. Some proteins become more soluble upon heat shock, whereas others, including several ubiquitin-conjugating enzymes, become more insoluble. By analyzing the changes in protein abundance induced by RNAi for E2 ubiquitin-conjugating enzymes, we identify E2-specific biases in targeting proteins with higher-than-average insolubility. Analysis of the E3 ubiquitin ligase HUWE1, which was previously found to detect proteins with exposed hydrophobic residues, indicates that siHUWE1-downregulated proteins have higher-than-average insolubility, suggesting that HUWE1 stabilizes subsets of insoluble proteins. Altogether, this study identifies components of the ubiquitination cascade that control and remodel the solubility of the human proteome.
The ubiquitin-proteasome system maintains proteostasis by degrading proteins that unfold and become insoluble upon stress. Some proteins have high insolubility in normal conditions because of their structure, subcellular localization, and interactions but it remains incompletely understood how the ubiquitin-proteasome system regulates them. Here, we utilized mass spectrometry to profile heat-induced solubility changes (insolubilome) and associated post-translational modifications in human cells (http://thermal-stress-insolubilome.stjude.org). We find that the solubility of several protein categories is oppositely modulated by thermal stress. Some proteins become more soluble upon heat shock, whereas others, including several ubiquitin-conjugating enzymes, become more insoluble. By analyzing the changes in protein abundance induced by RNAi for E2 ubiquitin-conjugating enzymes, we identify E2-specific biases in targeting proteins with higher-than-average insolubility. Analysis of the E3 ubiquitin ligase HUWE1, which was previously found to detect proteins with exposed hydrophobic residues, indicates that siHUWE1-downregulated proteins have higher-than-average insolubility, suggesting that HUWE1 stabilizes subsets of insoluble proteins. Altogether, this study identifies components of the ubiquitination cascade that control and remodel the solubility of the human proteome.
The ubiquitin-proteasome system maintains proteostasis by degrading proteins that unfold and become insoluble upon stress. Some proteins have high insolubility in normal conditions because of their structure, subcellular localization, and interactions but it remains incompletely understood how the ubiquitin-proteasome system regulates them. Here, we utilized mass spectrometry to profile heat-induced solubility changes (insolubilome) and associated post-translational modifications in human cells (http://thermal-stress-insolubilome.stjude.org). We find that the solubility of several protein categories is oppositely modulated by thermal stress. Some proteins become more soluble upon heat shock, whereas others, including several ubiquitin-conjugating enzymes, become more insoluble. By analyzing the changes in protein abundance induced by RNAi for E2 ubiquitin-conjugating enzymes, we identify E2-specific biases in targeting proteins with higher-than-average insolubility. Analysis of the E3 ubiquitin ligase HUWE1, which was previously found to detect proteins with exposed hydrophobic residues, indicates that siHUWE1-downregulated proteins have higher-than-average insolubility, suggesting that HUWE1 stabilizes subsets of insoluble proteins. Altogether, this study identifies components of the ubiquitination cascade that control and remodel the solubility of the human proteome.The ubiquitin-proteasome system maintains proteostasis by degrading proteins that unfold and become insoluble upon stress. Some proteins have high insolubility in normal conditions because of their structure, subcellular localization, and interactions but it remains incompletely understood how the ubiquitin-proteasome system regulates them. Here, we utilized mass spectrometry to profile heat-induced solubility changes (insolubilome) and associated post-translational modifications in human cells (http://thermal-stress-insolubilome.stjude.org). We find that the solubility of several protein categories is oppositely modulated by thermal stress. Some proteins become more soluble upon heat shock, whereas others, including several ubiquitin-conjugating enzymes, become more insoluble. By analyzing the changes in protein abundance induced by RNAi for E2 ubiquitin-conjugating enzymes, we identify E2-specific biases in targeting proteins with higher-than-average insolubility. Analysis of the E3 ubiquitin ligase HUWE1, which was previously found to detect proteins with exposed hydrophobic residues, indicates that siHUWE1-downregulated proteins have higher-than-average insolubility, suggesting that HUWE1 stabilizes subsets of insoluble proteins. Altogether, this study identifies components of the ubiquitination cascade that control and remodel the solubility of the human proteome.
ArticleNumber 110517
Author Stephan, Anna
Wang, Wei
Fu, Yingxue
Peng, Junmin
High, Anthony A.
Grime, John
Poudel, Suresh
Yu, Kaiwen
Wang, Xusheng
Hunt, Liam C.
Demontis, Fabio
Kavdia, Kanisha
Pagala, Vishwajeeth R.
Wang, Yong-Dong
Alford, Daniel
Graca, Flavia A.
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Keywords insolubilome
insoluble proteins
E2 ubiquitin-conjugating enzymes
NT
HUWE1
PTM
TMT
thermal stress
protein-quality control
proteome solubility
Language English
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Snippet The ubiquitin-proteasome system maintains proteostasis by degrading proteins that unfold and become insoluble upon stress. Some proteins have high insolubility...
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SubjectTerms E2 ubiquitin-conjugating enzymes
HUWE1
insolubilome
insoluble proteins
Methods and Resources
protein-quality control
proteome solubility
thermal stress
Title Proteome solubility is differentially reshaped by thermal stress and regulators of ubiquitination
URI https://dx.doi.org/10.1016/j.jbc.2025.110517
https://www.ncbi.nlm.nih.gov/pubmed/40713964
https://www.proquest.com/docview/3233998751
https://pubmed.ncbi.nlm.nih.gov/PMC12391699
Volume 301
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