Stochiometric quantification of the thiol redox proteome of macrophages reveals subcellular compartmentalization and susceptibility to oxidative perturbations
Abstract
Posttranslational modifications of protein cysteine thiols play a significant role in redox regulation and the pathogenesis of human diseases. However, the cellular redox landscape in terms of quantitative, site-specific occupancies of thiol modifications at the proteome level, especially under physiological conditions, is still largely uncharacterized. Herein, we report the site occupancies of both S-glutathionylation (SSG) and total reversible thiol oxidation (total oxidation) in RAW 264.7 macrophage cells under basal conditions. The occupancies of thiol modifications for ~4,000 cysteine sites were quantified, which revealed a mean site occupancy of 4.0% for SSG and 11.9% for total oxidation, respectively. Proteome-wide site occupancy analysis revealed a strong subcellular compartmentalization in thiol redox status, where the average occupancies of SSG and total oxidation in distinct compartments correlate well with the redox potentials of respective organelles. The lowest site occupancies were observed in more reducing compartments such as mitochondria and nucleus, while the highest site occupancies were found in more oxidizing organelles such as endoplasmic reticulum (ER) and lysosome. Correlations between site occupancies and structural features such as pKa, relative residue surface accessibility, and hydrophobicity were also observed. Furthermore, under oxidative stress induced by exposure to engineered metal oxide nanoparticles, we observed that mitochondria andmore »
- Publication Date:
- Research Org.:
- Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
- Sponsoring Org.:
- USDOE; National Institutes of Health (NIH)
- OSTI Identifier:
- 1644337
- Alternate Identifier(s):
- OSTI ID: 1657206
- Report Number(s):
- PNNL-SA-153520
Journal ID: ISSN 2213-2317; S2213231720308545; 101649; PII: S2213231720308545
- Grant/Contract Number:
- AC05-76RL0 1830; AC05-76RL01830; R01 GM125968; R01 DK122160; U01ES027292
- Resource Type:
- Published Article
- Journal Name:
- Redox Biology
- Additional Journal Information:
- Journal Name: Redox Biology Journal Volume: 36 Journal Issue: C; Journal ID: ISSN 2213-2317
- Publisher:
- Elsevier
- Country of Publication:
- Netherlands
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Protein thiols, redox modification, redox proteomics, S-glutathionylation, siteoccupancy, stoichiometry, macrophage, resin-assisted enrichment
Citation Formats
Duan, Jicheng, Zhang, Tong, Gaffrey, Matthew J., Weitz, Karl K., Moore, Ronald J., Li, Xiaolu, Xian, Ming, Thrall, Brian D., and Qian, Wei-Jun. Stochiometric quantification of the thiol redox proteome of macrophages reveals subcellular compartmentalization and susceptibility to oxidative perturbations. Netherlands: N. p., 2020.
Web. doi:10.1016/j.redox.2020.101649.
Duan, Jicheng, Zhang, Tong, Gaffrey, Matthew J., Weitz, Karl K., Moore, Ronald J., Li, Xiaolu, Xian, Ming, Thrall, Brian D., & Qian, Wei-Jun. Stochiometric quantification of the thiol redox proteome of macrophages reveals subcellular compartmentalization and susceptibility to oxidative perturbations. Netherlands. https://doi.org/10.1016/j.redox.2020.101649
Duan, Jicheng, Zhang, Tong, Gaffrey, Matthew J., Weitz, Karl K., Moore, Ronald J., Li, Xiaolu, Xian, Ming, Thrall, Brian D., and Qian, Wei-Jun. Tue .
"Stochiometric quantification of the thiol redox proteome of macrophages reveals subcellular compartmentalization and susceptibility to oxidative perturbations". Netherlands. https://doi.org/10.1016/j.redox.2020.101649.
@article{osti_1644337,
title = {Stochiometric quantification of the thiol redox proteome of macrophages reveals subcellular compartmentalization and susceptibility to oxidative perturbations},
author = {Duan, Jicheng and Zhang, Tong and Gaffrey, Matthew J. and Weitz, Karl K. and Moore, Ronald J. and Li, Xiaolu and Xian, Ming and Thrall, Brian D. and Qian, Wei-Jun},
abstractNote = {Posttranslational modifications of protein cysteine thiols play a significant role in redox regulation and the pathogenesis of human diseases. However, the cellular redox landscape in terms of quantitative, site-specific occupancies of thiol modifications at the proteome level, especially under physiological conditions, is still largely uncharacterized. Herein, we report the site occupancies of both S-glutathionylation (SSG) and total reversible thiol oxidation (total oxidation) in RAW 264.7 macrophage cells under basal conditions. The occupancies of thiol modifications for ~4,000 cysteine sites were quantified, which revealed a mean site occupancy of 4.0% for SSG and 11.9% for total oxidation, respectively. Proteome-wide site occupancy analysis revealed a strong subcellular compartmentalization in thiol redox status, where the average occupancies of SSG and total oxidation in distinct compartments correlate well with the redox potentials of respective organelles. The lowest site occupancies were observed in more reducing compartments such as mitochondria and nucleus, while the highest site occupancies were found in more oxidizing organelles such as endoplasmic reticulum (ER) and lysosome. Correlations between site occupancies and structural features such as pKa, relative residue surface accessibility, and hydrophobicity were also observed. Furthermore, under oxidative stress induced by exposure to engineered metal oxide nanoparticles, we observed that mitochondria and ER are less susceptible to low oxidative stress perturbations than nucleus and cytoplasm, presumably due to the differences in basal redox states and antioxidant capacity in different compartments.},
doi = {10.1016/j.redox.2020.101649},
journal = {Redox Biology},
number = C,
volume = 36,
place = {Netherlands},
year = {Tue Sep 01 00:00:00 EDT 2020},
month = {Tue Sep 01 00:00:00 EDT 2020}
}
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