Quantitative Profiling of Protein S-Glutathionylation Reveals Redox-Dependent Regulation of Macrophage Function During Nanoparticle-Induced Oxidative Stress

Duan, Jicheng; Kodali, Vamsi K.; Gaffrey, Matthew J.; Guo, Jia; Chu, Rosalie K.; Camp, David G.; Smith, Richard D.; Thrall, Brian D.; Qian, Wei-Jun

doi:10.1021/acsnano.5b05524

Title: Quantitative Profiling of Protein S-Glutathionylation Reveals Redox-Dependent Regulation of Macrophage Function During Nanoparticle-Induced Oxidative Stress

Journal Article · Wed Dec 23 00:00:00 EST 2015 · ACS Nano

DOI:https://doi.org/10.1021/acsnano.5b05524· OSTI ID:1236919

Duan, Jicheng ^[1]; Kodali, Vamsi K. ^[1]; Gaffrey, Matthew J. ^[1]; Guo, Jia ^[1]; Chu, Rosalie K. ^[2]; Camp, David G. ^[1]; Smith, Richard D. ^[3]; Thrall, Brian D. ^[1]; Qian, Wei-Jun ^[1]

Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Sciences Division
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Sciences Division; Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)

Engineered nanoparticles (ENPs) are emerging functional materials increasingly utilized for commercial and medical applications. Due to the potential hazard effects of ENPs to human health, it is significant to assess and understand the underlying mechanisms of nanotoxicity. Here, we investigate protein S-glutathionylation (SSG) as an underlying regulatory mechanism for ENP-induced oxidative stress in macrophages by applying a recently developed quantitative redox proteomics approach for site-specific measurements of SSG. Three high-volume production ENPs (SiO₂, Fe₃O₄ and CoO) were selected as representative ENPs with low, moderate, and high reactive oxygen species (ROS) activity, respectively. Among these nanoparticles, we observe that CoO led to the most significant dose-dependent oxidative stress and increase of protein SSG modifications in macrophages. Our site-specific SSG changes highlighted a broad set of redox sensitive proteins and their specific Cys residues potentially implicated in stress response. Functional analysis revealed that the most significantly enriched functional categories for SSG-modified proteins were stress response, cellular structure change, and cell death or survival. Moreover, ENPs-induce oxidative stress levels (CoO > Fe₃O₄ > SiO₂) were found to correlate well with the levels of impairment of macrophage phagocytic activity and the overall degrees of increases in SSG. RNA silencing knockdown experiment of glutaredoxin 1 (Grx1) also led to a decreased phagocytic activity in macrophages, which suggested a regulatory role of SSG in phagocytosis. Together, the results provided valuable insights of protein SSG as a potential regulatory mechanism in response to nanomaterial-induced oxidative stress and immunity dysfunction.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-76RL01830; DP2OD006668; UC4 DK104167; ES019544; P41 GM103493; U24-CA-160019

OSTI ID:: 1236919

Report Number(s):: PNNL-SA-112721; 48135; 400412000

Journal Information:: ACS Nano, Vol. 10, Issue 1; ISSN 1936-0851

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 67 works

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Dual Maleimide Tagging for Relative and Absolute Quantitation of Cysteine-Containing Peptides by MALDI-TOF MS Ouyang, Fuzhong; Zhao, Zhihao; Gao, Ruifang ChemBioChem, Vol. 19, Issue 11 https://doi.org/10.1002/cbic.201800031	journal	May 2018
Acute in vitro and in vivo toxicity of a commercial grade boron nitride nanotube mixture Kodali, Vamsi K.; Roberts, Jenny R.; Shoeb, Mohammad Nanotoxicology, Vol. 11, Issue 8 https://doi.org/10.1080/17435390.2017.1390177	journal	September 2017
Detecting post-translational modification signatures as potential biomarkers in clinical mass spectrometry Mnatsakanyan, Ruzanna; Shema, Gerta; Basik, Mark Taylor & Francis https://doi.org/10.6084/m9.figshare.6736181	text	January 2018
Mass spectrometry-based proteomics for system-level characterization of biological responses to engineered nanomaterials Zhang, Tong; Gaffrey, Matthew J.; Thrall, Brian D. Analytical and Bioanalytical Chemistry, Vol. 410, Issue 24 https://doi.org/10.1007/s00216-018-1168-6	journal	June 2018
Isotopically Labeled Clickable Glutathione to Quantify Protein S‐Glutathionylation VanHecke, Garrett C.; Yapa Abeywardana, Maheeshi; Huang, Bo ChemBioChem, Vol. 21, Issue 6 https://doi.org/10.1002/cbic.201900528	journal	October 2019
Characterization of LXR-activating nanoparticle formulations in primary mouse macrophages Smith, Tyler K. T.; Kahiel, Zaina; LeBlond, Nicholas D. Molecules https://doi.org/10.1101/746784	posted_content	August 2019
Differential proteomics highlights macrophage-specific responses to amorphous silica nanoparticles Dalzon, Bastien; Aude-Garcia, Catherine; Collin-Faure, Véronique Nanoscale, Vol. 9, Issue 27 https://doi.org/10.1039/c7nr02140b	journal	January 2017
Detecting post-translational modification signatures as potential biomarkers in clinical mass spectrometry Mnatsakanyan, Ruzanna; Shema, Gerta; Basik, Mark Expert Review of Proteomics, Vol. 15, Issue 6 https://doi.org/10.1080/14789450.2018.1483340	journal	June 2018
Glutathione Metabolism in Renal Cell Carcinoma Progression and Implications for Therapies Xiao, Yi; Meierhofer, David Freie Universität Berlin https://doi.org/10.17169/refubium-25310	text	January 2019
Targeting of miR-96-5p by catalpol ameliorates oxidative stress and hepatic steatosis in LDLr-/- mice via p66shc/cytochrome C cascade Zhang, Yukun; Wang, Changyuan; Lu, Jiawei Aging, Vol. 12, Issue 3 https://doi.org/10.18632/aging.102721	journal	February 2020

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