ROS signaling in innate immunity via oxidative protein modifications
Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články, přehledy, práce podpořená grantem
PubMed
38515749
PubMed Central
PMC10954773
DOI
10.3389/fimmu.2024.1359600
Knihovny.cz E-zdroje
- Klíčová slova
- inflammation, innate immune response, macrophage, neutrophils, oxidative stress, protein oxidation, reactive oxygen species,
- MeSH
- kyselina chlorná MeSH
- oxidace-redukce MeSH
- oxidační stres MeSH
- peroxid vodíku * MeSH
- přirozená imunita MeSH
- superoxidy * MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
- Názvy látek
- kyselina chlorná MeSH
- peroxid vodíku * MeSH
- superoxidy * MeSH
The innate immune response represents the first-line of defense against invading pathogens. Reactive oxygen species (ROS) and reactive nitrogen species (RNS) have been implicated in various aspects of innate immune function, which involves respiratory bursts and inflammasome activation. These reactive species widely distributed within the cellular environment are short-lived intermediates that play a vital role in cellular signaling and proliferation and are likely to depend on their subcellular site of formation. NADPH oxidase complex of phagocytes is known to generate superoxide anion radical (O2 •-) that functions as a precursor for antimicrobial hydrogen peroxide (H2O2) production, and H2O2 is utilized by myeloperoxidase (MPO) to generate hypochlorous acid (HOCl) that mediates pathogen killing. H2O2 modulates the expression of redox-responsive transcriptional factors, namely NF-kB, NRF2, and HIF-1, thereby mediating redox-based epigenetic modification. Survival and function of immune cells are under redox control and depend on intracellular and extracellular levels of ROS/RNS. The current review focuses on redox factors involved in the activation of immune response and the role of ROS in oxidative modification of proteins in macrophage polarization and neutrophil function.
Department of Biophysics Faculty of Science Palacký University Olomouc Czechia
German Red Cross Blood Service Baden Württemberg Hessen Mannheim Germany
Laboratory of Genetic Technologies Siberian State Medical University Tomsk Russia
Zobrazit více v PubMed
Checa J, Aran JM. Reactive oxygen species: drivers of physiological and pathological processes. JIR. (2020) 13:1057–73. doi: 10.2147/JIR.S275595 PubMed DOI PMC
Phaniendra A, Jestadi DB, Periyasamy L. Free radicals: properties, sources, targets, and their implication in various diseases. Ind J Clin Biochem. (2015) 30:11–26. doi: 10.1007/s12291-014-0446-0 PubMed DOI PMC
Prasad A, Manoharan RR, Sedlářová M, Pospíšil P. Free radical-mediated protein radical formation in differentiating monocytes. IJMS. (2021) 22:9963. doi: 10.3390/ijms22189963 PubMed DOI PMC
Manoharan RR, Sedlářová M, Pospíšil P, Prasad A. Detection and characterization of free oxygen radicals induced protein adduct formation in differentiating macrophages. Biochim Biophys Acta (BBA) Gen Subj. (2023) 1867:130324. doi: 10.1016/j.bbagen.2023.130324 PubMed DOI
Sharifi-Rad M, Anil Kumar NV, Zucca P, Varoni EM, Dini L, Panzarini E, et al. . Lifestyle, oxidative stress, and antioxidants: back and forth in the pathophysiology of chronic diseases. Front Physiol. (2020) 11:694. doi: 10.3389/fphys.2020.00694 PubMed DOI PMC
Sies H, Jones DP. Reactive oxygen species (ROS) as pleiotropic physiological signaling agents. Nat Rev Mol Cell Biol. (2020) 21:363–83. doi: 10.1038/s41580-020-0230-3 PubMed DOI
Lambeth JD. Nox enzymes, ROS, and chronic disease: An example of antagonistic pleiotropy. Free Radical Biol Med. (2007) 43:332–47. doi: 10.1016/j.freeradbiomed.2007.03.027 PubMed DOI PMC
Zorov DB, Juhaszova M, Sollott SJ. Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol Rev. (2014) 94:909–50. doi: 10.1152/physrev.00026.2013 PubMed DOI PMC
Fransen M, Nordgren M, Wang B, Apanasets O. Role of peroxisomes in ROS/RNS-metabolism: Implications for human disease. Biochim Biophys Acta (BBA) Mol Basis Dis. (2012) 1822:1363–73. doi: 10.1016/j.bbadis.2011.12.001 PubMed DOI
Nguyen GT, Green ER, Mecsas J. Neutrophils to the ROScue: mechanisms of NADPH oxidase activation and bacterial resistance. Front Cell Infect Microbiol. (2017) 7:373. doi: 10.3389/fcimb.2017.00373 PubMed DOI PMC
Morris G, Gevezova M, Sarafian V, Maes M. Redox regulation of the immune response. Cell Mol Immunol. (2022) 19:1079–101. doi: 10.1038/s41423-022-00902-0 PubMed DOI PMC
Muri J, Thut H, Feng Q, Kopf M. Thioredoxin-1 distinctly promotes NF-κB target DNA binding and NLRP3 inflammasome activation independently of Txnip. eLife. (2020) 9:e53627. doi: 10.7554/eLife.53627 PubMed DOI PMC
Holmström KM, Finkel T. Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat Rev Mol Cell Biol. (2014) 6:411–21. doi: 10.1038/nrm3801 PubMed DOI
Van der Vliet A, Janssen-Heininger YM. Hydrogen peroxide as a damage signal in tissue injury and inflammation: murderer, mediator, or messenger? J Cell Biochem. (2014) 3:427–35. doi: 10.1002/jcb.24683 PubMed DOI PMC
Hattori H, Subramanian KK, Sakai J, Jia Y, Li Y, Porter TF, et al. . Small-molecule screen identifies reactive oxygen species as key regulators of neutrophil chemotaxis. Proc Natl Acad Sci USA. (2010) 107:3546–51. doi: 10.1073/pnas.0914351107 PubMed DOI PMC
Gostner JM, Becker K, Fuchs D, Sucher R. Redox regulation of the immune response. Redox Rep. (2013) 18:88–94. doi: 10.1179/1351000213Y.0000000044 PubMed DOI PMC
Rendra E, Riabov V, Mossel DM, Sevastyanova T, Harmsen MC, Kzhyshkowska J. Reactive oxygen species (ROS) in macrophage activation and function in diabetes. Immunobiology. (2019) 224:242–53. doi: 10.1016/j.imbio.2018.11.010 PubMed DOI
Ikeda S, Yamaoka-Tojo M, Hilenski L, Patrushev NA, Anwar GM, Quinn MT, et al. . IQGAP1 regulates reactive oxygen species-dependent endothelial cell migration through interacting with Nox2. Arteriosc Thromb Vasc Biol. (2005) 11:2295–300. doi: 10.1161/01.ATV.0000187472.55437.af PubMed DOI
Roh JS, Sohn DH. Damage-associated molecular patterns in inflammatory diseases. Immune Netw. (2018) 18:e27. doi: 10.4110/in.2018.18.e27 PubMed DOI PMC
Pitocco D, Tesauro M, Alessandro R, Ghirlanda G, Cardillo C. Oxidative stress in diabetes: implications for vascular and other complications. Int J Mol Sci. (2013) 14:21525–50. doi: 10.3390/ijms141121525 PubMed DOI PMC
Freemerman AJ, Johnson AR, Sacks GN, Milner JJ, Kirk EL, Troester MA, et al. . Metabolic reprogramming of macrophages: glucose transporter 1 (GLUT1)-mediated glucose metabolism drives a Pro-inflammatory phenotype. J Biol Chem. (2014) 289:7884–96. doi: 10.1074/jbc.M113.522037 PubMed DOI PMC
Yao J, Wu D, Qiu Y. Adipose tissue macrophage in obesity-associated metabolic diseases. Front Immunol. (2022) 13:977485. doi: 10.3389/fimmu.2022.977485 PubMed DOI PMC
Wu J, Yan Z, Schwartz DE, Yu J, Malik AB, Hu G. Activation of NLRP3 inflammasome in alveolar macrophages contributes to mechanical stretch-induced lung inflammation and injury. J Immunol. (2013) 190:3590–9. doi: 10.4049/jimmunol.1200860 PubMed DOI PMC
Reczek CR, Chandel NS. ROS-dependent signal transduction. Curr Opin Cell Biol. (2015) 33:8–13. doi: 10.1016/j.ceb.2014.09.010 PubMed DOI PMC
Hasheminasabgorji E, Jha JC. Dyslipidemia, diabetes and atherosclerosis: role of inflammation and ROS-redox-sensitive factors. Biomedicines. (2021) 11:1602. doi: 10.3390/biomedicines9111602 PubMed DOI PMC
Panday A, Sahoo MK, Osorio D, Batra S. NADPH oxidases: an overview from structure to innate immunity-associated pathologies. Cell Mol Immunol. (2015) 1:5–23. doi: 10.1038/cmi.2014.89 PubMed DOI PMC
Shen N, Wang Y, Sun X, Bai X, He J, Cui Q, et al. . Expression of hypoxia-inducible factor 1α, glucose transporter 1, and hexokinase 2 in primary central nervous system lymphoma and the correlation with the biological behaviors. Brain Behav. (2020) 10:e01718. doi: 10.1002/brb3.1718 PubMed DOI PMC
Baillet A, Hograindleur M, El Benna J, Grichine A, Berthier S, Morel F, et al. . Unexpected function of the phagocyte NADPH oxidase in supporting hyperglycolysis in stimulated neutrophils: key role of 6-phosphofructo-2-kinase. FASEB J. (2017) 31:663–73. doi: 10.1096/fj.201600720R PubMed DOI
Tirichen H, Yaigoub H, Xu W, Wu C, Li R, Li Y. Mitochondrial reactive oxygen species and their contribution in chronic kidney disease progression through oxidative stress. Front Physiol. (2021) 12:627837. doi: 10.3389/fphys.2021.627837 PubMed DOI PMC
Forrester SJ, Kikuchi DS, Hernandes MS, Xu Q, Griendling KK. Reactive oxygen species in metabolic and inflammatory signaling. Circ Res. (2018) 6:877–902. doi: 10.1161/CIRCRESAHA.117.311401 PubMed DOI PMC
Cao SS, Kaufman RJ. Endoplasmic reticulum stress and oxidative stress in cell fate decision and human disease. Antioxid Redox Signal. (2014) 3:396–413. doi: 10.1089/ars.2014.5851 PubMed DOI PMC
Espinosa-Diez C, Miguel V, Mennerich D, Kietzmann T, Sánchez-Pérez P, Cadenas S, et al. . Antioxidant responses and cellular adjustments to oxidative stress. Redox Biol. (2015) 6:183–97. doi: 10.1016/j.redox.2015.07.008 PubMed DOI PMC
Zeeshan HM, Lee GH, Kim HR, Chae HJ. Endoplasmic reticulum stress and associated ROS. Int J Mol Sci. (2016) 3:327. doi: 10.3390/ijms17030327 PubMed DOI PMC
Prior KK, Wittig I, Leisegang MS, Groenendyk J, Weissmann N, Michalak M, et al. . The endoplasmic reticulum chaperone calnexin is a NADPH oxidase NOX4 interacting protein. J Biol Chem. (2016) 13:7045–59. doi: 10.1074/jbc.M115.710772 PubMed DOI PMC
Fransen M, Lismont C, Walton P. The peroxisome-mitochondria connection: how and why? Int J Mol Sci. (2017) 6:1126. doi: 10.3390/ijms18061126 PubMed DOI PMC
Wanders RJ, Waterham HR, Ferdinandusse S. Metabolic interplay between peroxisomes and other subcellular organelles including mitochondria and the endoplasmic reticulum. Front Cell Dev Biol. (2016) 3:83. doi: 10.3389/fcell.2015.00083 PubMed DOI PMC
Vermot A, Petit-Härtlein I, Smith SME, Fieschi F. NADPH oxidases (NOX): an overview from discovery, molecular mechanisms to physiology and pathology. Antioxid (Basel). (2021) 6:890. doi: 10.3390/antiox10060890 PubMed DOI PMC
Zamora R, Vodovotz Y, Billiar TR. Inducible nitric oxide synthase and inflammatory diseases. Mol Med. (2000) 6:347–73. doi: 10.1007/BF03401781 PubMed DOI PMC
Santos CXC, Stolf BS, Takemoto PVA, Amanso AM, Lopes LR, Souza EB, et al. . Protein disulfide isomerase (PDI) associates with NADPH oxidase and is required for phagocytosis of Leishmania chagasi promastigotes by macrophages. J Leuk Biol. (2009) 86:989–98. doi: 10.1189/jlb.0608354 PubMed DOI
Reddie KG, Carroll KS. Expanding the functional diversity of proteins through cysteine oxidation. Curr Opin Chem Biol. (2008) 12:746–54. doi: 10.1016/j.cbpa.2008.07.028 PubMed DOI
Trujillo M, Alvarez B, Radi R. One- and two-electron oxidation of thiols: mechanisms, kinetics and biological fates. Free Radical Res. (2016) 50:150–71. doi: 10.3109/10715762.2015.1089988 PubMed DOI
Nagy P, Ashby MT. Reactive sulfur species: kinetics and mechanisms of the oxidation of cysteine by hypohalous acid to give cysteine sulfenic acid. J Am Chem Soc. (2007) 129:14082–91. doi: 10.1021/ja0737218 PubMed DOI
Vivancos AP, Castillo EA, Biteau B, Nicot C, Ayté J, Toledano MB, et al. . A cysteine-sulfinic acid in peroxiredoxin regulates H 2 O 2 -sensing by the antioxidant Pap1 pathway. Proc Natl Acad Sci USA. (2005) 102:8875–80. doi: 10.1073/pnas.0503251102 PubMed DOI PMC
Zabel R, Weber G. Comparative study of the oxidation behavior of sulfur-containing amino acids and glutathione by electrochemistry-mass spectrometry in the presence and absence of cisplatin. Anal Bioanal Chem. (2016) 408:1237–47. doi: 10.1007/s00216-015-9233-x PubMed DOI
Xiong Y, Uys JD, Tew KD, Townsend DM. S-glutathionylation: from molecular mechanisms to health outcomes. Antioxid Redox Signaling. (2011) 15:233–70. doi: 10.1089/ars.2010.3540 PubMed DOI PMC
Rodríguez-García A, García-Vicente R, Morales ML, Ortiz-Ruiz A, Martínez-López J, Linares M. Protein carbonylation and lipid peroxidation in hematological Malignancies. Antioxidants. (2020) 9:1212. doi: 10.3390/antiox9121212 PubMed DOI PMC
Kehm R, Baldensperger T, Raupbach J, Höhn A. Protein oxidation - Formation mechanisms, detection and relevance as biomarkers in human diseases. Redox Biol. (2021) 42:2213–317. doi: 10.1016/j.redox.2021.101901 PubMed DOI PMC
Kim C-S, Park S, Kim J. The role of glycation in the pathogenesis of aging and its prevention through herbal products and physical exercise. JENB. (2017) 21:55–61. doi: 10.20463/jenb.2017.0027 PubMed DOI PMC
Baldensperger T, Sanzo SD, Ori A, Glomb MA. Quantitation of reactive acyl-CoA species mediated protein acylation by HPLC–MS/MS. Anal Chem. (2019) 91:12336–43. doi: 10.1021/acs.analchem.9b02656 PubMed DOI
McCaskill ML, Kharbanda KK, Tuma DJ, Reynolds JD, DeVasure JM, Sisson JH, et al. . Hybrid malondialdehyde and acetaldehyde protein adducts form in the lungs of mice exposed to alcohol and cigarette smoke: MAA ADDUCTS IN LUNG. Alcoholism: Clin Exp Res. (2011) 35:1106–13. doi: 10.1111/j.1530-0277.2011.01443.x PubMed DOI PMC
Gonos ES, Kapetanou M, Sereikaite J, Bartosz G, Naparło K, Grzesik M, et al. . Origin and pathophysiology of protein carbonylation, nitration and chlorination in age-related brain diseases and aging. Aging. (2018) 10:868–901. doi: 10.18632/aging.101450 PubMed DOI PMC
Ayala A, Muñoz MF, Argüelles S. Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid Med Cell Longevity. (2014) 2014:1–31. doi: 10.1155/2014/360438 PubMed DOI PMC
Monroy CA, Doorn JA, Roman DL. Modification and functional inhibition of regulator of G-protein signaling 4 (RGS4) by 4-hydroxy-2-nonenal. Chem Res Toxicol. (2013) 26:1832–9. doi: 10.1021/tx400212q PubMed DOI PMC
Aiken CT, Kaake RM, Wang X, Huang L. Oxidative stress-mediated regulation of proteasome complexes. Mol Cell Proteomics. (2011) 10:5. doi: 10.1074/mcp.M110.006924 PubMed DOI PMC
Curtis JM, Hahn WS, Long EK, Burrill JS, Arriaga EA, Bernlohr DA. Protein carbonylation and metabolic control systems. Trends Endocrinol Metab. (2012) 23:399–406. doi: 10.1016/j.tem.2012.05.008 PubMed DOI PMC
Stringfellow HM, Jones MR, Green MC, Wilson AK, Francisco JS. Selectivity in ROS-induced peptide backbone bond cleavage. J Phys Chem A. (2014) 118:11399–404. doi: 10.1021/jp508877m PubMed DOI
Bollineni RC, Fedorova M, Blüher M, Hoffmann R. Carbonylated plasma proteins as potential biomarkers of obesity induced type 2 diabetes mellitus. J Proteome Res. (2014) 13:5081–93. doi: 10.1021/pr500324y PubMed DOI
Cassinadio JS, Jones BR, Chamberlain GR, Baxter GF. Nitric oxide treatments as adjuncts to reperfusion in acute myocardial infarction: a systematic review of experimental and clinical studies. Basic Res Cardiol. (2016) 111:23. doi: 10.1007/s00395-016-0540-y PubMed DOI PMC
Radi R. Oxygen radicals, nitric oxide, and peroxynitrite: Redox pathways in molecular medicine. Proc Natl Acad Sci USA. (2018) 115:5839–48. doi: 10.1073/pnas.1804932115 PubMed DOI PMC
Cassina P, Cassina A, Pehar M, Castellanos R, Gandelman M, de Leon A, et al. . Mitochondrial dysfunction in SOD1G93A-bearing astrocytes promotes motor neuron degeneration: prevention by mitochondrial-targeted antioxidants. J Neurosci. (2008) 28:4115–22. doi: 10.1523/JNEUROSCI.5308-07.2008 PubMed DOI PMC
Wang Z, Wang Y, Liu H, Che Y, Xu Y, E L. Age-related variations of protein carbonyls in human saliva and plasma: is saliva protein carbonyls an alternative biomarker of aging? AGE. (2015) 37:48. doi: 10.1007/s11357-015-9781-1 PubMed DOI PMC
Sharma A, Weber D, Raupbach J, Dakal TC, Fließbach K, Ramirez A, et al. . Advanced glycation end products and protein carbonyl levels in plasma reveal sex-specific differences in Parkinson’s and Alzheimer’s disease. Redox Biol. (2020) 34:101546. doi: 10.1016/j.redox.2020.101546 PubMed DOI PMC
Almogbel E, Rasheed N. Elevated levels of protein carbonylation in patients with diabetic nephropathy: therapeutic and diagnostic prospects. Am J Med Sci. (2019) 358:26–32. doi: 10.1016/j.amjms.2019.03.01 PubMed DOI
Lou B, Boger M, Bennewitz K, Sticht C, Kopf S, Morgenstern J, et al. . Elevated 4-hydroxynonenal induces hyperglycaemia via Aldh3a1 loss in zebrafish and associates with diabetes progression in humans. Redox Biol. (2020) 37:101723. doi: 10.1016/j.redox.2020.101723 PubMed DOI PMC
Neelofar K, Arif Z, Arafat MY, Alam K, Ahmad J. A study on correlation between oxidative stress parameters and inflammatory markers in type 2 diabetic patients with kidney dysfunction in north Indian population. J Cell Biochem. (2019) 120:4892–902. doi: 10.1002/jcb.27763 PubMed DOI
Yavuzer H, Yavuzer S, Cengiz M, Erman H, Doventas A, Balci H, et al. . Biomarkers of lipid peroxidation related to hypertension in aging. Hypertens Res. (2016) 39:342–8. doi: 10.1038/hr.2015.156 PubMed DOI
Stankova TR, Delcheva GT, Maneva AI, Vladeva SV. Serum levels of carbamylated LDL, nitrotyrosine and soluble lectin-like oxidized low-density lipoprotein receptor-1 in poorly controlled type 2 diabetes mellitus. Folia Med. (2019) 61:419–25. doi: 10.3897/folmed.61.e39343 PubMed DOI
Silva Servato JP, Ueira Vieira C, De Faria PR, Cardoso SV, Loyola AM. The importance of inducible nitric oxide synthase and nitrotyrosine as prognostic markers for oral squamous cell carcinoma. J Oral Pathol Med. (2019) 48:967–75. doi: 10.1111/jop.12942 PubMed DOI
Hawkins CL, Davies MJ. Detection, identification, and quantification of oxidative protein modifications. J Biol Chem. (2019) 294:19683–708. doi: 10.1074/jbc.REV119.006217 PubMed DOI PMC
Viola A, Munari F, Sánchez-Rodríguez R, Scolaro T, Castegna A. The metabolic signature of macrophage responses. Front Immunol. (2019) 10:1462. doi: 10.3389/fimmu.2019.01462 PubMed DOI PMC
Canton M, Sánchez-Rodríguez R, Spera I, Venegas FC, Favia M, Viola A, et al. . Reactive oxygen species in macrophages: sources and targets. Front Immunol. (2021) 12:734229. doi: 10.3389/fimmu.2021.734229 PubMed DOI PMC
Palsson-McDermott EM, Curtis AM, Goel G, Lauterbach MA, Sheedy FJ, Gleeson LE, et al. . Pyruvate kinase M2 regulates Hif-1α activity and IL-1β induction and is a critical determinant of the warburg effect in LPS-activated macrophages. Cell Metab. (2015) 21:65–80. doi: 10.1016/j.cmet.2014.12.005 PubMed DOI PMC
Gordon S, Mantovani A. Diversity and plasticity of mononuclear phagocytes. Eur J Immunol. (2011) 41:2470–2. doi: 10.1002/eji.201141988 PubMed DOI
Strizova Z, Benesova I, Bartolini R, Novysedlak R, Cecrdlova E, Foley LK, et al. . M1/M2 macrophages and their overlaps - myth or reality? Clin Sci (Lond). (2023) 15:1067–93. doi: 10.1042/CS20220531 PubMed DOI PMC
Murray PJ, Allen JE, Biswas SK, Fisher EA, Gilroy DW, Goerdt S, et al. . Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity. (2014) 41:14–20. doi: 10.1016/j.immuni.2014.06.008 PubMed DOI PMC
Geeraerts X, Bolli E, Fendt SM, Van Ginderachter JA. Macrophage metabolism as therapeutic target for cancer, atherosclerosis, and obesity. Front Immunol. (2017) 8:289. doi: 10.3389/fimmu.2017.00289 PubMed DOI PMC
Xue J, Schmidt SV, Sander J, Draffehn A, Krebs W, Quester I, et al. . Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity. (2014) 40:274–88. doi: 10.1016/j.immuni.2014.01.006 PubMed DOI PMC
Nelson VL, Nguyen HCB, Garcìa-Cañaveras JC, Briggs ER, Ho WY, DiSpirito JR, et al. . PPARγ is a nexus controlling alternative activation of macrophages via glutamine metabolism. Genes Dev. (2018) 32:1035–44. doi: 10.1101/gad.312355.118 PubMed DOI PMC
Wang T, Liu H, Lian G, Zhang S-Y, Wang X, Jiang C. HIF1 α -induced glycolysis metabolism is essential to the activation of inflammatory macrophages. Mediators Inflammation. (2017) 17:1–10. doi: 10.1155/2017/9029327 PubMed DOI PMC
Nizet V, Johnson RS. Interdependence of hypoxic and innate immune responses. Nat Rev Immunol. (2009) 9:609–17. doi: 10.1038/nri2607 PubMed DOI PMC
Wang F, Zhang S, Vuckovic I, Jeon R, Lerman A, Folmes CD, et al. . Glycolytic stimulation is not a requirement for M2 macrophage differentiation. Cell Metab. (2018) 28:463–475.e4. doi: 10.1016/j.cmet.2018.08.012 PubMed DOI PMC
Wang S, Liu G, Li Y, Pan Y. Metabolic reprogramming induces macrophage polarization in the tumor microenvironment. Front Immunol. (2022) 13:840029. doi: 10.3389/fimmu.2022.840029 PubMed DOI PMC
Jeon J-H, Hong C-W, Kim EY, Lee JM. Current understanding on the metabolism of neutrophils. Immune Netw. (2020) 20:e46. doi: 10.4110/in.2020.20.e46 PubMed DOI PMC
Papayannopoulos V, Metzler KD, Hakkim A, Zychlinsky A. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J Cell Biol. (2010) 191:677–91. doi: 10.1083/jcb.201006052 PubMed DOI PMC
Douda DN, Khan MA, Grasemann H, Palaniyar N. SK3 channel and mitochondrial ROS mediate NADPH oxidase-independent NETosis induced by calcium influx. Proc Natl Acad Sci USA. (2015) 112:2817–22. doi: 10.1073/pnas.1414055112 PubMed DOI PMC
Mullen L, Mengozzi M, Hanschmann E-M, Alberts B, Ghezzi P. How the redox state regulates immunity. Free Radical Biol Med. (2020) 157:3–14. doi: 10.1016/j.freeradbiomed.2019.12.022 PubMed DOI
Sônego F, Castanheira FVES, Ferreira RG, Kanashiro A, Leite CAVG, Nascimento DC, et al. . Paradoxical roles of the neutrophil in sepsis: protective and deleterious. Front Immunol. (2016) 7:155. doi: 10.3389/fimmu.2016.00155 PubMed DOI PMC
Carrera-Quintanar L, Funes L, Herranz-López M, Martínez-Peinado P, Pascual-García S, Sempere JM, et al. . Antioxidant supplementation modulates neutrophil inflammatory response to exercise-induced stress. Antioxidants. (2020) 9:1242. doi: 10.3390/antiox9121242 PubMed DOI PMC
Akong-Moore K, Chow OA, Von Köckritz-Blickwede M, Nizet V. Influences of chloride and hypochlorite on neutrophil extracellular trap formation. PloS One. (2012) 7:e42984. doi: 10.1371/journal.pone.0042984 PubMed DOI PMC
Clemen R, Arlt K, Miebach L, von Woedtke T, Bekeschus S. Oxidized proteins differentially affect maturation and activation of human monocyte-derived cells. Cells. (2022) 11:3659. doi: 10.3390/cells11223659 PubMed DOI PMC
Diotallevi M, Checconi P, Palamara AT, Celestino I, Coppo L, Holmgren A, et al. . Glutathione fine-tunes the innate immune response toward antiviral pathways in a macrophage cell line independently of its antioxidant properties. Front Immunol. (2017) 8:1239. doi: 10.3389/fimmu.2017.01239 PubMed DOI PMC
Helou DG, Noël B, Gaudin F, Groux H, El Ali Z, Pallardy M, et al. . Cutting edge: Nrf2 regulates neutrophil recruitment and accumulation in skin during contact hypersensitivity. J Immunol. (2019) 202:2189–94. doi: 10.4049/jimmunol.180106 PubMed DOI
Luo J-F, Shen X-Y, Lio CK, Dai Y, Cheng C-S, Liu J-X, et al. . Activation of Nrf2/HO-1 pathway by nardochinoid C inhibits inflammation and oxidative stress in lipopolysaccharide-stimulated macrophages. Front Pharmacol. (2018) 9:911. doi: 10.3389/fphar.2018.00911 PubMed DOI PMC
Rugemalira E, Roine I, Kuligowski J, Sánchez-Illana Á, Piñeiro-Ramos JD, Andersson S, et al. . Protein oxidation biomarkers and myeloperoxidase activation in cerebrospinal fluid in childhood bacterial meningitis. Antioxidants. (2019) 8:441. doi: 10.3390/antiox8100441 PubMed DOI PMC
García-Giménez JL, Òlaso G, Hake SB, Bönisch C, Wiedemann SM, Markovic J, et al. . Histone h3 glutathionylation in proliferating mammalian cells destabilizes nucleosomal structure. Antioxid Redox Signaling. (2013) 19:1305–20. doi: 10.1089/ars.2012.5021 PubMed DOI PMC
Tyurin VA, Balasubramanian K, Winnica D, Tyurina YY, Vikulina AS, He RR, et al. . Oxidatively modified phosphatidylserines on the surface of apoptotic cells are essential phagocytic ‘eat-me’ signals: cleavage and inhibition of phagocytosis by Lp-PLA2. Cell Death Differ. (2014) 21:825–35. doi: 10.1038/cdd.2014.1 PubMed DOI PMC
Wu C, Li A, Hu J, Kang J. Histone deacetylase 2 is essential for LPS-induced inflammatory responses in macrophages. Immunol Cell Biol. (2019) 97:72–84. doi: 10.1111/imcb.12203 PubMed DOI PMC
Chen S, Yang J, Wei Y, Wei X. Epigenetic regulation of macrophages: from homeostasis maintenance to host defense. Cell Mol Immunol. (2020) 17:36–49. doi: 10.1038/s41423-019-0315-0 PubMed DOI PMC
Clements MK, Siemsen DW, Swain SD, Hanson AJ, Nelson-Overton LK, Rohn TT, et al. . Inhibition of actin polymerization by peroxynitrite modulates neutrophil functional responses. J Leuk Biol. (2003) 73:344–55. doi: 10.1189/jlb.080240 PubMed DOI
Łuczaj W, Gindzienska-Sieskiewicz E, Jarocka-Karpowicz I, Andrisic L, Sierakowski S, Zarkovic N, et al. . The onset of lipid peroxidation in rheumatoid arthritis: consequences and monitoring. Free Radical Res. (2016) 50:304–13. doi: 10.3109/10715762.2015.1112901 PubMed DOI
Hecker M, Wagner AH. Role of protein carbonylation in diabetes. J Inherit Metab Dis. (2018) 41:29–38. doi: 10.1007/s10545-017-0104-9 PubMed DOI
Kondo A, Morita H, Nakamura H, Kotani K, Kobori K, Ito S, et al. . Influence of fibrate treatment on malondialdehyde-modified LDL concentration. Clinica Chimica Acta. (2004) 339:97–103. doi: 10.1016/j.cccn.2003.09.005 PubMed DOI
Kietzmann T, Petry A, Shvetsova A, Gerhold JM, Görlach A. The epigenetic landscape related to reactive oxygen species formation in the cardiovascular system: ROS and epigenetic modifications. Br J Pharmacol. (2017) 174:1533–54. doi: 10.1111/bph.13792 PubMed DOI PMC
O’Connor KM, Das AB, Winterbourn CC, Hampton MB. Inhibition of DNA methylation in proliferating human lymphoma cells by immune cell oxidants. J Biol Chem. (2020) 295:7839–48. doi: 10.1074/jbc.RA120.013092 PubMed DOI PMC
Binder CJ, Papac-Milicevic N, Witztum JL. Innate sensing of oxidation-specific epitopes in health and disease. Nat Rev Immunol. (2016) 8:485–97. doi: 10.1038/nri.2016.63 PubMed DOI PMC
Liguori I, Russo G, Curcio F, Bulli G, Aran L, Della-Morte D, et al. . Oxidative stress, aging, and diseases. Clin Interventions Aging. (2018) 13:757–72. doi: 10.2147/CIA.S158513 PubMed DOI PMC
Kurutas EB. The importance of antioxidants which play the role in cellular response against oxidative/nitrosative stress: current state. Nutr J. (2016) 1:71. doi: 10.1186/s12937-016-0186-5 PubMed DOI PMC
Yuan T, Yang T, Chen H, Fu D, Hu Y, Wang J, et al. . New insights into oxidative stress and inflammation during diabetes mellitus-accelerated atherosclerosis. Redox Biol. (2019) 20:247–60. doi: 10.1016/j.redox.2018.09.025 PubMed DOI PMC
Mulder WJM, Ochando J, Joosten LAB, Fayad ZA, Netea MG. Therapeutic targeting of trained immunity. Nat Rev Drug Discovery. (2019) 18:553–66. doi: 10.1038/s41423-022-00902-0 PubMed DOI PMC
Jiang J, Wang K, Chen Y, Chen H, Nice EC, Huang C. Redox regulation in tumor cell epithelial–mesenchymal transition: Molecular basis and therapeutic strategy. Signal Transduct Target Ther. (2017) 1:1–12. doi: 10.1038/sigtrans.2017.36 PubMed DOI PMC
Jiang J, Wang K, Nice EC, Zhang T, Huang C. High-throughput screening of cellular redox sensors using modern redox proteomics approaches. Expert Rev Proteomics. (2015) 12:543–55. doi: 10.1586/14789450.2015.1069189 PubMed DOI
Weigert A, von Knethen A, Fuhrmann D, Dehne N, Brüne B. Redox-signals and macrophage biology. Mol Aspects Med. (2018) 63:70–87. doi: 10.1016/j.mam.2018.01.003 PubMed DOI