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REVIEW

Oxidative Stress Contributes to Inflammatory and Cellular Damage in Systemic Lupus Erythematosus: Cellular Markers and Molecular Mechanism

, & ORCID Icon
Pages 453-465 | Received 27 Nov 2022, Accepted 18 Jan 2023, Published online: 04 Feb 2023

References

  • Pannu N, Bhatnagar A. Oxidative stress and immune complexes: pathogenic mechanisms in pristane induced murine model of lupus. Immunobiology. 2020;225(1):151871. doi:10.1016/j.imbio.2019.11.006
  • Smallwood MJ, Nissim A, Knight AR, Whiteman M, Haigh R, Winyard PG. Oxidative stress in autoimmune rheumatic diseases. Free Radic Biol Med. 2018;125:3–14. doi:10.1016/j.freeradbiomed.2018.05.086
  • Fujii J, Kurahashi T, Konno T, Homma T, Iuchi Y. Oxidative stress as a potential causal factor for autoimmune hemolytic anemia and systemic lupus erythematosus. World J Nephrol. 2015;4(2):213–222. doi:10.5527/wjn.v4.i2.213
  • Duarte-Delgado NP, Cala MP, Barreto A, Rodriguez CL. Metabolites and metabolic pathways associated with rheumatoid arthritis and systemic lupus erythematosus. J Transl Autoimmun. 2022;5:100150. doi:10.1016/j.jtauto.2022.100150
  • Ahsan H, Ali A, Ali R. Oxygen free radicals and systemic autoimmunity. Clin Exp Immunol. 2003;131(3):398–404. doi:10.1046/j.1365-2249.2003.02104.x
  • Wojcik P, Gegotek A, Zarkovic N, Skrzydlewska E. Oxidative stress and lipid mediators modulate immune cell functions in autoimmune diseases. Int J Mol Sci. 2021;22(2):723. doi:10.3390/ijms22020723
  • Ahmad R, Ahsan H. Singlet oxygen species and systemic lupus erythematosus: a brief review. J Immunoassay Immunochem. 2019;40(4):343–349. doi:10.1080/15321819.2019.1616555
  • Shruthi S, Thabah MM, Zachariah B, Negi VS. Association of oxidative stress with disease activity and damage in systemic lupus erythematosus: a cross sectional study from a tertiary care centre in Southern India. Indian J Clin Biochem. 2021;36(2):185–193. doi:10.1007/s12291-020-00879-5
  • Wang S, Liu Y, Liu J, et al. Mitochondria-derived methylmalonic acid, a surrogate biomarker of mitochondrial dysfunction and oxidative stress, predicts all-cause and cardiovascular mortality in the general population. Redox Biol. 2020;37:101741. doi:10.1016/j.redox.2020.101741
  • Costa JH, Mohanapriya G, Bharadwaj R, et al. ROS/RNS balancing, aerobic fermentation regulation and cell cycle control - a complex early trait (‘CoV-MAC-TED’) for combating SARS-CoV-2-induced cell reprogramming. Front Immunol. 2021;12:673692. doi:10.3389/fimmu.2021.673692
  • Zhang VX, Sze KM, Chan LK, et al. Antioxidant supplements promote tumor formation and growth and confer drug resistance in hepatocellular carcinoma by reducing intracellular ROS and induction of TMBIM1. Cell Biosci. 2021;11(1):217. doi:10.1186/s13578-021-00731-0
  • Hu C, Zhang J, Hong S, et al. Oxidative stress-induced aberrant lipid metabolism is an important causal factor for dysfunction of immunocytes from patients with systemic lupus erythematosus. Free Radic Biol Med. 2021;163:210–219. doi:10.1016/j.freeradbiomed.2020.12.006
  • Wang L, Law HKW. Immune complexes impaired glomerular endothelial cell functions in lupus nephritis. Int J Mol Sci. 2019;20(21):5281. doi:10.3390/ijms20215281
  • Nabatian-Asl M, Ghorbanihaghjo A, Malek Mahdavi A, Khabbazi A, Hajialilo M, Ghojazadeh M. Effects of melatonin supplementation on serum oxidative stress markers and disease activity in systemic lupus erythematosus patients: a randomised, double-blind, placebo-controlled trial. Int J Clin Pract. 2021;75(7):e14246. doi:10.1111/ijcp.14246
  • Ene CD, Georgescu SR, Tampa M, et al. Cellular response against oxidative stress, a novel insight into lupus nephritis pathogenesis. J Pers Med. 2021;11(8):693. doi:10.3390/jpm11080693
  • Fortner KA, Blanco LP, Buskiewicz I, et al. Targeting mitochondrial oxidative stress with MitoQ reduces NET formation and kidney disease in lupus-prone MRL-lpr mice. Lupus Sci Med. 2020;7(1):e000387. doi:10.1136/lupus-2020-000387
  • Ramalingam A, Budin SB, Mohd Fauzi N, Ritchie RH, Zainalabidin S. Targeting mitochondrial reactive oxygen species-mediated oxidative stress attenuates nicotine-induced cardiac remodeling and dysfunction. Sci Rep. 2021;11(1):13845. doi:10.1038/s41598-021-93234-4
  • Nazim UM, Yin H, Park SY. Autophagy flux inhibition mediated by celastrol sensitized lung cancer cells to TRAILinduced apoptosis via regulation of mitochondrial transmembrane potential and reactive oxygen species. Mol Med Rep. 2019;19(2):984–993. doi:10.3892/mmr.2018.9757
  • Lee HT, Wu TH, Lin CS, et al. The pathogenesis of systemic lupus erythematosus - From the viewpoint of oxidative stress and mitochondrial dysfunction. Mitochondrion. 2016;30:1–7. doi:10.1016/j.mito.2016.05.007
  • Perl A. Activation of mTOR (mechanistic target of rapamycin) in rheumatic diseases. Nat Rev Rheumatol. 2016;12(3):169–182. doi:10.1038/nrrheum.2015.172
  • Liu J, Ming S, Song W, et al. B and T lymphocyte attenuator regulates autophagy in mycobacterial infection via the AKT/mTOR signal pathway. Int Immunopharmacol. 2021;91:107215. doi:10.1016/j.intimp.2020.107215
  • Zhang JC, Chen G, Chen L, et al. TGF-beta/BAMBI pathway dysfunction contributes to peripheral Th17/Treg imbalance in chronic obstructive pulmonary disease. Sci Rep. 2016;6:31911. doi:10.1038/srep31911
  • Szwed A, Kim E, Jacinto E. Regulation and metabolic functions of mTORC1 and mTORC2. Physiol Rev. 2021;101(3):1371–1426. doi:10.1152/physrev.00026.2020
  • Shi H, Chapman NM, Wen J, et al. Amino acids license kinase mTORC1 activity and Treg cell function via small G proteins Rag and Rheb. Immunity. 2019;51(6):1012–27e7. doi:10.1016/j.immuni.2019.10.001
  • Oaks Z, Winans T, Huang N, Banki K, Perl A. Activation of the mechanistic target of rapamycin in SLE: explosion of evidence in the last five years. Curr Rheumatol Rep. 2016;18(12):73. doi:10.1007/s11926-016-0622-8
  • Peixoto TV, Carrasco S, Botte DAC, et al. CD4(+)CD69(+) T cells and CD4(+)CD25(+)FoxP3(+) Treg cells imbalance in peripheral blood, spleen and peritoneal lavage from pristane-induced systemic lupus erythematosus (SLE) mice. Adv Rheumatol. 2019;59(1):30. doi:10.1186/s42358-019-0072-x
  • Sahni A, Narra HP, Sahni SK. Activation of mechanistic target of rapamycin (mTOR) in human endothelial cells infected with pathogenic spotted fever group rickettsiae. Int J Mol Sci. 2020;21(19):7179. doi:10.3390/ijms21197179
  • Braga A, Neves E, Guimaraes J, Braga J, Vasconcelos C. The dynamics of Th17 / Treg ratio in SLE patients during pregnancy. J Reprod Immunol. 2022;151:103622. doi:10.1016/j.jri.2022.103622
  • He J, Ma J, Ren B, Liu A. Advances in systemic lupus erythematosus pathogenesis via mTOR signaling pathway. Semin Arthritis Rheum. 2020;50(2):314–320. doi:10.1016/j.semarthrit.2019.09.022
  • He S, Xue M, Cai G. IL-6 alters migration capacity of CD4(+)Foxp3(+) regulatory T cells in systemic lupus erythematosus. Scand J Immunol. 2021;94(5):e13099. doi:10.1111/sji.13099
  • Zhang X, Lindwall E, Gauthier C, et al. Circulating CXCR5+CD4+helper T cells in systemic lupus erythematosus patients share phenotypic properties with germinal center follicular helper T cells and promote antibody production. Lupus. 2015;24(9):909–917. doi:10.1177/0961203314567750
  • Gigante A, Iannazzo F, Navarini L, et al. Metabolic syndrome and adipokine levels in systemic lupus erythematosus and systemic sclerosis. Clin Rheumatol. 2021;40(10):4253–4258. doi:10.1007/s10067-021-05731-6
  • Yang J, Yang X, Zou H, Li M. Oxidative stress and Treg and Th17 dysfunction in systemic lupus erythematosus. Oxid Med Cell Longev. 2016;2016:2526174. doi:10.1155/2016/2526174
  • Shan J, Jin H, Xu Y. T Cell Metabolism: a new perspective on Th17/Treg cell imbalance in systemic lupus erythematosus. Front Immunol. 2020;11:1027. doi:10.3389/fimmu.2020.01027
  • Yu H, Jiang L, Liu R, et al. Association between the ratio of aryl hydrocarbon receptor (AhR) in Th17 cells to AhR in Treg cells and SLE skin lesions. Int Immunopharmacol. 2019;69:257–262. doi:10.1016/j.intimp.2019.01.039
  • de Araujo EF, Feriotti C, Galdino NAL, Preite NW, Calich VLG, Loures FV. The IDO-AhR axis controls Th17/Treg immunity in a pulmonary model of fungal infection. Front Immunol. 2017;8:880. doi:10.3389/fimmu.2017.00880
  • Mockel T, Basta F, Weinmann-Menke J, Schwarting A. B cell activating factor (BAFF): structure, functions, autoimmunity and clinical implications in systemic lupus erythematosus (SLE). Autoimmun Rev. 2021;20(2):102736. doi:10.1016/j.autrev.2020.102736
  • Stohl W, Yu N, Chalmers S, Putterman C, Jacob CO. Development of murine systemic lupus erythematosus in the absence of BAFF. Arthritis Rheumatol. 2020;72(2):292–302. doi:10.1002/art.41097
  • Wilson CS, Stocks BT, Hoopes EM, et al. Metabolic preconditioning in CD4+ T cells restores inducible immune tolerance in lupus-prone mice. JCI Insight. 2021;6(19):e143245. doi:10.1172/jci.insight.143245
  • Pathak S, Kumar KR, Kanta H, et al. Fatty acid amide hydrolase regulates peripheral B cell receptor revision, polyreactivity, and B1 cells in lupus. J Immunol. 2016;196(4):1507–1516. doi:10.4049/jimmunol.1500291
  • Dong GF, Zhang X, He DN, Li L, Zhang GF. Effect of leflunomide on the abnormal expression of lipid rafts and F-actin in B lymphocytes from patients with systemic lupus erythematosus. J Immunol Res. 2015;2015:832916. doi:10.1155/2015/832916
  • Azzouz D, Khan MA, Palaniyar N. ROS induces NETosis by oxidizing DNA and initiating DNA repair. Cell Death Discov. 2021;7(1):113. doi:10.1038/s41420-021-00491-3
  • Breitenstein MK, Hu VJ, Bhatnagar R, Ratnagiri M. Approaching neural net feature interpretation using stacked autoencoders: gene expression profiling of systemic lupus erythematosus patients. AMIA Jt Summits Transl Sci Proc. 2019;2019:435–442.
  • Campbell AM, Kashgarian M, Shlomchik MJ. NADPH oxidase inhibits the pathogenesis of systemic lupus erythematosus. Sci Transl Med. 2012;4(157):157ra41. doi:10.1126/scitranslmed.3004801
  • El-Ghoneimy DH, Hesham M, Hasan R, Tarif M, Gouda S. The behavior of neutrophil extracellular traps and NADPH oxidative activity in pediatric systemic lupus erythematosus: relation to disease activity and lupus nephritis. Clin Rheumatol. 2019;38(9):2585–2593. doi:10.1007/s10067-019-04547-9
  • Bao Y, Ledderose C, Graf AF, et al. mTOR and differential activation of mitochondria orchestrate neutrophil chemotaxis. J Cell Biol. 2015;210(7):1153–1164. doi:10.1083/jcb.201503066
  • Lightfoot YL, Blanco LP, Kaplan MJ. Metabolic abnormalities and oxidative stress in lupus. Curr Opin Rheumatol. 2017;29(5):442–449. doi:10.1097/BOR.0000000000000413
  • Bona N, Pezzarini E, Balbi B, et al. Oxidative stress, inflammation and disease activity biomarkers in lupus nephropathy. Lupus. 2020;29(3):311–323. doi:10.1177/0961203320904784
  • Granick M, Leuin AS, Trepanier LA. Plasma and urinary F2-isoprostane markers of oxidative stress are increased in cats with early (stage 1) chronic kidney disease. J Feline Med Surg. 2021;23(8):692–699. doi:10.1177/1098612X20969358
  • Krata N, Foroncewicz B, Zagozdzon R, et al. Peroxiredoxins as markers of oxidative stress in IgA nephropathy, membranous nephropathy and lupus nephritis. Arch Immunol Ther Exp (Warsz). 2021;70(1):3. doi:10.1007/s00005-021-00638-1
  • Zavadskiy S, Sologova S, Moldogazieva N. Oxidative distress in aging and age-related diseases: spatiotemporal dysregulation of protein oxidation and degradation. Biochimie. 2022;195:114–134. doi:10.1016/j.biochi.2021.12.002
  • Song YR, Kim JK, Lee HS, Kim SG, Choi EK. Serum levels of protein carbonyl, a marker of oxidative stress, are associated with overhydration, sarcopenia and mortality in hemodialysis patients. BMC Nephrol. 2020;21(1):281. doi:10.1186/s12882-020-01937-z
  • Ahsan H. 3-Nitrotyrosine: a biomarker of nitrogen free radical species modified proteins in systemic autoimmunogenic conditions. Hum Immunol. 2013;74(10):1392–1399. doi:10.1016/j.humimm.2013.06.009
  • Ren W, Liu G, Yin J, et al. Amino-acid transporters in T-cell activation and differentiation. Cell Death Dis. 2017;8(3):e2655. doi:10.1038/cddis.2016.222
  • Liu T, Han J, Zhang R, et al. Characteristics of purified anti-beta2GPI IgG N-glycosylation associate with thrombotic, obstetric and catastrophic antiphospholipid syndrome. Rheumatology (Oxford). 2022;61(3):1243–1254. doi:10.1093/rheumatology/keab416
  • Peluso M, Russo V, Mello T, Galli A. Oxidative stress and DNA damage in chronic disease and environmental studies. Int J Mol Sci. 2020;21(18):6936. doi:10.3390/ijms21186936
  • Ntouros PA, Vlachogiannis NI, Pappa M, et al. Effective DNA damage response after acute but not chronic immune challenge: SARS-CoV-2 vaccine versus systemic lupus erythematosus. Clin Immunol. 2021;229:108765. doi:10.1016/j.clim.2021.108765
  • Tumurkhuu G, Chen S, Montano EN, et al. Oxidative DNA damage accelerates skin inflammation in pristane-induced lupus model. Front Immunol. 2020;11:554725. doi:10.3389/fimmu.2020.554725
  • Ene CD, Penescu MN, Georgescu SR, Tampa M, Nicolae I. Posttranslational modifications pattern in clear cell renal cell carcinoma. Metabolites. 2020;11(1):10. doi:10.3390/metabo11010010
  • Ray D, Strickland FM, Richardson BC. Oxidative stress and dietary micronutrient deficiencies contribute to overexpression of epigenetically regulated genes by lupus T cells. Clin Immunol. 2018;196:97–102. doi:10.1016/j.clim.2018.04.003
  • Gorelik GJ, Yarlagadda S, Patel DR, Richardson BC. Protein kinase Cdelta oxidation contributes to ERK inactivation in lupus T cells. Arthritis Rheum. 2012;64(9):2964–2974. doi:10.1002/art.34503
  • Richardson B, Strickland FM, Sawalha AH, Gorelik G. Protein kinase Cdelta mutations may contribute to lupus through effects on T cells: comment on the article by Belot et al. Arthritis Rheumatol. 2014;66(1):228–229. doi:10.1002/art.38235
  • He XJ, Ding Y, Xiang W, Dang XQ. Roles of 1,25(OH)2D3 and vitamin D receptor in the pathogenesis of rheumatoid arthritis and systemic lupus erythematosus by regulating the activation of CD4+ T cells and the PKCdelta/ERK signaling pathway. Cell Physiol Biochem. 2016;40(3–4):743–756. doi:10.1159/000453135
  • Zhang CX, Wang HY, Yin L, Mao YY, Zhou W. Immunometabolism in the pathogenesis of systemic lupus erythematosus. J Transl Autoimmun. 2020;3:100046. doi:10.1016/j.jtauto.2020.100046
  • Bethunaickan R, Sahu R, Liu Z, et al. Anti-tumor necrosis factor alpha treatment of interferon-alpha-induced murine lupus nephritis reduces the renal macrophage response but does not alter glomerular immune complex formation. Arthritis Rheum. 2012;64(10):3399–3408. doi:10.1002/art.34553
  • Tian Y, Guo H, Miao X, et al. Nestin protects podocyte from injury in lupus nephritis by mitophagy and oxidative stress. Cell Death Dis. 2020;11(5):319. doi:10.1038/s41419-020-2547-4
  • Perl A. Oxidative stress in the pathology and treatment of systemic lupus erythematosus. Nat Rev Rheumatol. 2013;9(11):674–686. doi:10.1038/nrrheum.2013.147
  • Akiyama M, Kaneko Y, Takeuchi T. Lupus aortitis: a fatal, inflammatory cardiovascular complication in systemic lupus erythematosus. Lupus. 2020;29(12):1652–1654. doi:10.1177/0961203320950017
  • Martin N, Tu X, Egan AJ, Stover C. Complement activation on endothelial cell-derived microparticles-A key determinant for cardiovascular risk in patients with systemic lupus erythematosus? Medicina. 2020;56(10):533. doi:10.3390/medicina56100533
  • Giannelou M, Mavragani CP. Cardiovascular disease in systemic lupus erythematosus: a comprehensive update. J Autoimmun. 2017;82:1–12. doi:10.1016/j.jaut.2017.05.008
  • Lopez-Pedrera C, Barbarroja N, Jimenez-Gomez Y, Collantes-Estevez E, Aguirre MA, Cuadrado MJ. Oxidative stress in the pathogenesis of atherothrombosis associated with anti-phospholipid syndrome and systemic lupus erythematosus: new therapeutic approaches. Rheumatology. 2016;55(12):2096–2108. doi:10.1093/rheumatology/kew054
  • Lozovoy MA, Simao AN, Morimoto HK, et al. Hypertension is associated with serologically active disease in patients with systemic lupus erythematosus: role of increased Th1/Th2 ratio and oxidative stress. Scand J Rheumatol. 2014;43(1):59–62. doi:10.3109/03009742.2013.834963
  • Russell-Goldman E, Nazarian RM. Subacute cutaneous lupus erythematosus with positive anti-Ro antibodies following palbociclib and letrozole treatment: a case report and literature review. J Cutan Pathol. 2020;47(7):654–658. doi:10.1111/cup.13673
  • Lozovoy MA, Simao AN, Panis C, et al. Oxidative stress is associated with liver damage, inflammatory status, and corticosteroid therapy in patients with systemic lupus erythematosus. Lupus. 2011;20(12):1250–1259. doi:10.1177/0961203311411350
  • Wu T, Ye Y, Min SY, et al. Prevention of murine lupus nephritis by targeting multiple signaling axes and oxidative stress using a synthetic triterpenoid. Arthritis Rheumatol. 2014;66(11):3129–3139. doi:10.1002/art.38782
  • Lai ZW, Hanczko R, Bonilla E, et al. N-acetylcysteine reduces disease activity by blocking mammalian target of rapamycin in T cells from systemic lupus erythematosus patients: a randomized, double-blind, placebo-controlled trial. Arthritis Rheum. 2012;64(9):2937–2946. doi:10.1002/art.34502
  • Tan MKX, Heng TYJ, Mak A. The potential use of metformin, dipyridamole, N-Acetylcysteine and statins as adjunctive therapy for systemic lupus erythematosus. Cells. 2019;8(4):323. doi:10.3390/cells8040323
  • Monaco A, Ferrandino I, Boscaino F, et al. Conjugated linoleic acid prevents age-dependent neurodegeneration in a mouse model of neuropsychiatric lupus via the activation of an adaptive response. J Lipid Res. 2018;59(1):48–57. doi:10.1194/jlr.M079400
  • Bergamo P, Maurano F, Rossi M. Phase 2 enzyme induction by conjugated linoleic acid improves lupus-associated oxidative stress. Free Radic Biol Med. 2007;43(1):71–79. doi:10.1016/j.freeradbiomed.2007.03.023
  • Oaks Z, Winans T, Caza T, et al. Mitochondrial dysfunction in the liver and antiphospholipid antibody production precede disease onset and respond to rapamycin in lupus-prone mice. Arthritis Rheumatol. 2016;68(11):2728–2739. doi:10.1002/art.39791
  • Lai ZW, Borsuk R, Shadakshari A, et al. Mechanistic target of rapamycin activation triggers IL-4 production and necrotic death of double-negative T cells in patients with systemic lupus erythematosus. J Immunol. 2013;191(5):2236–2246. doi:10.4049/jimmunol.1301005
  • Buskiewicz IA, Montgomery T, Yasewicz EC, et al. Reactive oxygen species induce virus-independent MAVS oligomerization in systemic lupus erythematosus. Sci Signal. 2016;9(456):ra115. doi:10.1126/scisignal.aaf1933
  • Lopez-Pedrera C, Villalba JM, Patino-Trives AM, et al. Therapeutic potential and immunomodulatory role of coenzyme Q(10) and its analogues in systemic autoimmune diseases. Antioxidants. 2021;10(4):600. doi:10.3390/antiox10040600
  • Blanco LP, Pedersen HL, Wang X, et al. Improved mitochondrial metabolism and reduced inflammation following attenuation of murine lupus with coenzyme Q10 analog idebenone. Arthritis Rheumatol. 2020;72(3):454–464. doi:10.1002/art.41128
  • Lin M, Li L, Zhang Y, et al. Baicalin ameliorates H2O2 induced cytotoxicity in HK-2 cells through the inhibition of ER stress and the activation of Nrf2 signaling. Int J Mol Sci. 2014;15(7):12507–12522. doi:10.3390/ijms150712507
  • Ding H, Wang H, Zhao Y, Sun D, Zhai X. Protective effects of baicalin on Abeta(1)(-)(4)(2)-induced learning and memory deficit, oxidative stress, and apoptosis in rat. Cell Mol Neurobiol. 2015;35(5):623–632. doi:10.1007/s10571-015-0156-z
  • Park D, Jeong H, Lee MN, et al. Resveratrol induces autophagy by directly inhibiting mTOR through ATP competition. Sci Rep. 2016;6:21772. doi:10.1038/srep21772
  • Tsai PY, Ka SM, Chang JM, et al. Antroquinonol differentially modulates T cell activity and reduces interleukin-18 production, but enhances Nrf2 activation, in murine accelerated severe lupus nephritis. Arthritis Rheum. 2012;64(1):232–242. doi:10.1002/art.33328
  • Tsai PY, Ka SM, Chang JM, et al. Epigallocatechin-3-gallate prevents lupus nephritis development in mice via enhancing the Nrf2 antioxidant pathway and inhibiting NLRP3 inflammasome activation. Free Radic Biol Med. 2011;51(3):744–754. doi:10.1016/j.freeradbiomed.2011.05.016
  • Fouad H, Yahia S, Elsaid A, et al. Oxidative stress and vitamin D receptor BsmI gene polymorphism in Egyptian children with systemic lupus erythematosus: a single center study. Lupus. 2019;28(6):771–777. doi:10.1177/0961203319846380
  • Costenbader KH, Kang JH, Karlson EW. Antioxidant intake and risks of rheumatoid arthritis and systemic lupus erythematosus in women. Am J Epidemiol. 2010;172(2):205–216. doi:10.1093/aje/kwq089
  • Sporn MB, Liby KT, Yore MM, Fu L, Lopchuk JM, Gribble GW. New synthetic triterpenoids: potent agents for prevention and treatment of tissue injury caused by inflammatory and oxidative stress. J Nat Prod. 2011;74(3):537–545. doi:10.1021/np100826q
  • Pagano G, Castello G, Pallardo FV. Sjogren’s syndrome-associated oxidative stress and mitochondrial dysfunction: prospects for chemoprevention trials. Free Radic Res. 2013;47(2):71–73. doi:10.3109/10715762.2012.748904
  • Tobore TO. Oxidative/nitroxidative stress and multiple sclerosis. J Mol Neurosci. 2021;71(3):506–514. doi:10.1007/s12031-020-01672-y
  • Yevgi R, Demir R. Oxidative stress activity of fingolimod in multiple sclerosis. Clin Neurol Neurosurg. 2021;202:106500. doi:10.1016/j.clineuro.2021.106500