Stochiometric quantification of the thiol redox proteome of macrophages reveals subcellular compartmentalization and susceptibility to oxidative perturbations

Duan, Jicheng; Zhang, Tong; Gaffrey, Matthew J.; Weitz, Karl K.; Moore, Ronald J.; Li, Xiaolu; Xian, Ming; Thrall, Brian D.; Qian, Wei-Jun

doi:10.1016/j.redox.2020.101649

Title: Stochiometric quantification of the thiol redox proteome of macrophages reveals subcellular compartmentalization and susceptibility to oxidative perturbations

Journal Article · Tue Sep 01 00:00:00 EDT 2020 · Redox Biology

DOI:https://doi.org/10.1016/j.redox.2020.101649· OSTI ID:1644337

; Zhang, Tong; Gaffrey, Matthew J.; Weitz, Karl K.; Moore, Ronald J.; Li, Xiaolu; Xian, Ming; Thrall, Brian D.; Qian, Wei-Jun

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.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE; National Institutes of Health (NIH)

Grant/Contract Number:: AC05-76RL0 1830; AC05-76RL01830; R01 GM125968; R01 DK122160; U01ES027292

OSTI ID:: 1644337

Alternate ID(s):: OSTI ID: 1657206

Report Number(s):: PNNL-SA-153520; S2213231720308545; 101649; PII: S2213231720308545

Journal Information:: Redox Biology, Journal Name: Redox Biology Vol. 36 Journal Issue: C; ISSN 2213-2317

Publisher:: ElsevierCopyright Statement

Country of Publication:: Netherlands

Language:: English

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Title: Stochiometric quantification of the thiol redox proteome of macrophages reveals subcellular compartmentalization and susceptibility to oxidative perturbations

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