Altered protein S-glutathionylation depicts redox imbalance triggered by transition metal oxide nanoparticles in a breastfeeding system

Abu-Elheiga, 2012, Acetyl-CoA carboxylase 2−/− mutant mice are protected against fatty liver under high-fat, high-carbohydrate dietary and de novo lipogenic conditions, J. Biol. Chem., 287, 12578, 10.1074/jbc.M111.309559 Akram, 2014, Citric acid cycle and role of its intermediates in metabolism, Cell Biochem. Biophys., 68, 475, 10.1007/s12013-013-9750-1 Anelli, 2002, Erp44, a novel endoplasmic reticulum folding assistant of the thioredoxin family, EMBO J., 21, 835, 10.1093/emboj/21.4.835 Ashford, 2011, P300 energy loss in aging and Alzheimer’s disease, J. Alzheimers Dis., 26, 229, 10.3233/JAD-2011-0061 Boronat, 2017, Proteomic characterization of reversible thiol oxidations in proteomes and proteins, Antioxid. Redox Signal., 26, 329, 10.1089/ars.2016.6720 Brand, 2011, Assessing mitochondrial dysfunction in cells, Biochem. J., 435, 297, 10.1042/BJ20110162 Burkart, 2011, Adenylate kinase 2 links mitochondrial energy metabolism to the induction of the unfolded protein response, J. Biol. Chem., 286, 4081, 10.1074/jbc.M110.134106 Cai, 2019, Translocation of transition metal oxide nanoparticles to breast milk and offspring: the necessity of bridging mother-offspring-integration toxicological assessments, Environ. Int., 133, 105153, 10.1016/j.envint.2019.105153 Calvo, 2018, Non-coordinative metal selectivity bias in human metallothioneins metal-thiolate clusters, Metallomics, 10, 1777, 10.1039/C8MT00264A Che, 2020, Cyclooxygenase-2 modulates ER-mitochondria crosstalk to mediate superparamagnetic iron oxide nanoparticles induced hepatotoxicity: an in vitro and in vivo study, Nanotoxicology., 14, 162, 10.1080/17435390.2019.1683245 Chen, 2019, Effects of oral exposure to titanium dioxide nanoparticles on gut microbiota and gut-associated metabolism in vivo, Nanoscale, 11, 22398, 10.1039/C9NR07580A Chen, 2020, Tissue-specific oxidative stress and element distribution after oral exposure to titanium dioxide nanoparticles in rats, Nanoscale, 8, 20033, 10.1039/D0NR05591C Cheng, 2013, Mitochondria and metabolic homeostasis, Antioxid. Redox Signal., 19, 240, 10.1089/ars.2013.5255 Choi, 1996, Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury, Am. J. Respir. Cell Mol. Biol., 15, 9, 10.1165/ajrcmb.15.1.8679227 Chong, 2018, Metaboanalyst 4.0: towards more transparent and integrative metabolomics analysis, Nucleic Acids Res., 46, W486, 10.1093/nar/gky310 Chung, 2019, Activity-based ratiometric fret probe reveals oncogene-driven changes in labile copper pools induced by altered glutathione metabolism, Proc. Natl. Acad. Sci. U. S. A., 116, 18285, 10.1073/pnas.1904610116 Cleaves, 2010, Adsorption of nucleic acid components on rutile (TiO(2)) surfaces, Astrobiology, 10, 311, 10.1089/ast.2009.0397 Cui, 2019, Predictive metabolomic signatures for safety assessment of metal oxide nanoparticles, ACS Nano, 13, 13065, 10.1021/acsnano.9b05793 Dalton, 2018, Hypodermal responses to protein synthesis inhibition induce systemic developmental arrest and ampk-dependent survival in caenorhabditis elegans, PLoS Genet., 14, 10.1371/journal.pgen.1007520 Das, 2016, Potential toxicity of engineered nanoparticles in mammalian germ cells and developing embryos: treatment strategies and anticipated applications of nanoparticles in gene delivery, Hum. Reprod. Update, 22, 588, 10.1093/humupd/dmw020 Dastjerdi, 2010, A review on the application of inorganic nano-structured materials in the modification of textiles: focus on anti-microbial properties, Colloids Surf. B. Biointerfaces, 79, 5, 10.1016/j.colsurfb.2010.03.029 Duan, 2016, Quantitative profiling of protein S-glutathionylation reveals redox-dependent regulation of macrophage function during nanoparticle-induced oxidative stress, ACS Nano, 10, 524, 10.1021/acsnano.5b05524 Dudev, 2002, Factors governing the protonation state of cysteines in proteins: an ab initio/cdm study, J. Am. Chem. Soc., 124, 6759, 10.1021/ja012620l Dwivedi, 2018, Inflammatory effects of acrolein, crotonaldehyde and hexanal vapors on human primary bronchial epithelial cells cultured at air-liquid interface, Toxicol. in Vitro, 46, 219, 10.1016/j.tiv.2017.09.016 Filippi, 2015, Toxicology of ZnO and TiO2 nanoparticles on hepatocytes: impact on metabolism and bioenergetics, Nanotoxicology, 9, 126, 10.3109/17435390.2014.895437 Galaris, 2019, Iron homeostasis and oxidative stress: an intimate relationship, Biochim. Biophys. Acta, 1866, 118535, 10.1016/j.bbamcr.2019.118535 Gartner, 2005, American academy of pediatrics section on breastfeeding- breastfeeding and the use of human milk, Pediatrics, 115, 496, 10.1542/peds.2004-2491 Gay, 2018, In vivo lactoactive study investigators. Worldwide variation in human milk metabolome: indicators of breast physiology and maternal lifestyle?, Nutrients, 10, 9, 10.3390/nu10091151 Han, 2013, ER- stress-induced transcriptional regulation increases protein synthesis leading to cell death, Nat. Cell Biol., 15, 481, 10.1038/ncb2738 Hill, 2012, Protein S-glutathiolation: redox-sensitive regulation of protein function, J. Mol. Cell. Cardiol., 52, 559, 10.1016/j.yjmcc.2011.07.009 Ji, 2018, Multi-cellular human bronchial models exposed to diesel exhaust particles: assessment of inflammation, oxidative stress and macrophage polarization, Part. Fibre. Toxicol., 15, 19, 10.1186/s12989-018-0256-2 Kojer, 2015, Kinetic control by limiting glutaredoxin amounts enables thiol oxidation in the reducing mitochondrial intermembrane space, Mol. Biol. Cell, 26, 195, 10.1091/mbc.E14-10-1422 Krizkova, 2018, An insight into the complex roles of metallothioneins in malignant diseases with emphasis on (sub)isoforms/isoforms and epigenetics phenomena, Pharmacol. Ther., 183, 90, 10.1016/j.pharmthera.2017.10.004 Laurent, 2014, Sources and contents of air pollution affecting term low birth weight in Los Angeles County, California, 2001–2008, Environ. Res., 134, 488, 10.1016/j.envres.2014.05.003 Lian, 2018, Glutathione de novo synthesis but not recycling process coordinates with glutamine catabolism to control redox homeostasis and directs murine T cell differentiation, Elife, 7, 10.7554/eLife.36158 Limo, 2018, Interactions between metal oxides and biomolecules: from fundamental understanding to applications, Chem. Rev., 118, 11118, 10.1021/acs.chemrev.7b00660 Lu, 2008, Albumin as a zinc carrier: properties of its high-affinity zinc-binding site, Biochem. Soc. Trans., 36, 1317, 10.1042/BST0361317 Ma, 2013, Ecotoxicity of manufactured ZnO nanoparticles--a review, Environ. Pollut., 172, 76, 10.1016/j.envpol.2012.08.011 Mailloux, 2020, Protein S-glutathionylation reactions as a global inhibitor of cell metabolism for the desensitization of hydrogen peroxide signals, Redox Biol., 32, 101472, 10.1016/j.redox.2020.101472 Mailloux, 2016, Protein S-glutathionlyation links energy metabolism to redox signaling in mitochondria, Redox Biol., 8, 110, 10.1016/j.redox.2015.12.010 Mailloux, 2013, Unearthing the secrets of mitochondrial ROS and glutathione in bioenergetics, Trends Biochem. Sci., 38, 592, 10.1016/j.tibs.2013.09.001 Mailloux, 2014, Redox regulation of mitochondrial function with emphasis on cysteine oxidation reactions, Redox Biol., 2, 123, 10.1016/j.redox.2013.12.011 Mailloux, 2016, Induction of mitochondrial reactive oxygen species production by GSH mediated S-glutathionylation of 2-oxoglutarate dehydrogenase, Redox Biol., 8, 285, 10.1016/j.redox.2016.02.002 Miles, 2018, The plasminogen receptor, Plg-Rkt, is essential for mammary lobuloalveolar development and lactation, J. Thromb. Haemost., 16, 919, 10.1111/jth.13988 Morishita, 2016, Distribution of silver nanoparticles to breast milk and their biological effects on breast-fed offspring mice, ACS Nano, 10, 8180, 10.1021/acsnano.6b01782 Mura, 1999, Photodegradation of organic waste coupling hydrogenase and titanium dioxide, Ann. N. Y. Acad. Sci., 879, 267, 10.1111/j.1749-6632.1999.tb10430.x Ng, 2011, The role of the tumor suppressor p53 pathway in the cellular DNA damage response to zinc oxide nanoparticles, Biomaterials, 32, 8218, 10.1016/j.biomaterials.2011.07.036 Ojeda, 2018, The role of folic acid and selenium against oxidative damage from ethanol in early life programming: a review, Biochem. Cell Biol., 96, 178, 10.1139/bcb-2017-0069 Oka, 2019, Thioredoxin-1 maintains mitochondrial function via mTOR signaling in the heart, Cardiovasc. Res., 116, 1742, 10.1093/cvr/cvz251 Ostergaard, 2007, Deficiency of the alpha subunit of succinate-coenzyme a ligase causes fatal infantile lactic acidosis with mitochondrial DNA depletion, Am. J. Hum. Genet., 81, 383, 10.1086/519222 Ramírez-Torres, 2012, Proteomics and gene expression analyses of squalene-supplemented mice identify microsomal thioredoxin domain-containing protein 5 changes associated with hepatic steatosis, J. Proteome, 77, 27, 10.1016/j.jprot.2012.07.001 Ramming, 2012, The physiological functions of mammalian endoplasmic oxidoreductin 1: on disulfides and more, Antioxid. Redox Signal., 16, 1109, 10.1089/ars.2011.4475 Reshetnikov, 2018, Chemical tools for targeted amplification of reactive oxygen species in neutrophils, Front. Immunol., 9, 1827, 10.3389/fimmu.2018.01827 Sampson, 1984, Measurement of milk yield in the lactating rat from pup weight and weight gain, J. Pediatr. Gastroenterol. Nutr., 3, 613, 10.1097/00005176-198409000-00023 San-Millán, 2017, Reexamining cancer metabolism: lactate production for carcinogenesis could be the purpose and explanation of the Warburg effect, Carcinogenesis., 38, 119 Sannino, 2014, Progressive quality control of secretory proteins in the early secretory compartment by Erp44, J. Cell Sci., 127, 4260 Schraufnagel, 2020, The health effects of ultrafine particles, Exp. Mol. Med., 52, 311, 10.1038/s12276-020-0403-3 Setyawati, 2013, Effect of zinc oxide nanomaterials-induced oxidative stress on the p53 pathway, Biomaterials., 34, 10133, 10.1016/j.biomaterials.2013.09.024 Setyawati, 2015, Mechanistic investigation of the biological effects of SiO2, TiO2, and ZnO nanoparticles on intestinal cells, Small, 11, 3458, 10.1002/smll.201403232 Sies, 2014, Role of metabolic H2O2 generation: redox signaling and oxidative stress, J. Biol. Chem., 289, 8735, 10.1074/jbc.R113.544635 Silva, 2018, Wound healing and omega-6 fatty acids: from inflammation to repair, Mediat. Inflamm., 2018, 2503950, 10.1155/2018/2503950 Singh, 2019, Evidence of oxygen defects mediated enhanced photocatalytic and antibacterial performance of zno nanorods, Colloids Surf. B. Biointerfaces, 184, 110541, 10.1016/j.colsurfb.2019.110541 Sokolov, 2017, Comparison of interaction between ceruloplasmin and lactoferrin/transferrin: to bind or not to bind, Biochemistry, 82, 1073 Stathopoulou, 2016, S-glutathiolation impairs phosphoregulation and function of cardiac myosin-binding protein C in human heart failure, FASEB J., 30, 1849, 10.1096/fj.201500048 Szymańska, 2012, Double-check: validation of diagnostic statistics for pls-da models in metabolomics studies, Metabolomics, 8, 3, 10.1007/s11306-011-0330-3 Ueli, 2011 Vandekeere, 2018, Serine synthesis via phgdh is essential for heme production in endothelial cells, Cell Metab., 28, 573, 10.1016/j.cmet.2018.06.009 Victora, 2016, Lancet breastfeeding series group. Breastfeeding in the 21st Century: epidemiology, mechanisms, and lifelong effect, Lancet, 387, 475, 10.1016/S0140-6736(15)01024-7 Vionnet, 2019, Assessment of lactase activity in humans by measurement of galactitol and galactonate in serum and urine after milk intake, Am. J. Clin. Nutr., 109, 470, 10.1093/ajcn/nqy296 Volkovova, 2015, Health effects of selected nanoparticles in vivo: liver function and hepatotoxicity following intravenous injection of titanium dioxide and Na-oleate-coated iron oxide nanoparticles in rodents, Nanotoxicology, 9, 95, 10.3109/17435390.2013.815285 Wang, 2012, A systems biology approach to identify the signalling network regulated by Rho-gdi-γ during neural stem cell differentiation, Mol. BioSyst., 8, 2916, 10.1039/c2mb25147g Wang, 2015, The role of Txndc5 in castration-resistant prostate cancer-involvement of androgen receptor signaling pathway, Oncogene, 34, 4735, 10.1038/onc.2014.401 Willingham, 2014, Milk collection methods for mice and reeves' Muntjac Deer, J. Vis. Exp., 89 Wishart, 2019, Metabolomics for investigating physiological and pathophysiological processes, Physiol. Rev., 99, 1819, 10.1152/physrev.00035.2018 Yang, 2018, Quantum dots cause acute systemic toxicity in lactating rats and growth restriction of offspring, Nanoscale, 10, 11564, 10.1039/C8NR01248B Zhang, 2008, Abnormal epithelial homeostasis in the cornea of mice with a destrin deletion, Mol. Vis., 14, 1929 Zhou, 2019, Metascape provides a biologist-oriented resource for the analysis of systems-level datasets, Nat. Commun., 10, 1523, 10.1038/s41467-019-09234-6