Login Register Cart 0
Generic placeholder image

Current Protein & Peptide Science

Editor-in-Chief

ISSN (Print): 1389-2037
ISSN (Online): 1875-5550

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Oxidative Stress in Autoimmune Diseases: An Under Dealt Malice

Author(s): Sheetal Ramani, Ayush Pathak, Vikram Dalal, Anamika Paul and Sagarika Biswas*

Volume 21, Issue 6, 2020

Page: [611 - 621] Pages: 11

DOI: 10.2174/1389203721666200214111816

Price: $65

Abstract

Oxidative stress is the off-balance of antioxidants and free radicals. All kinds of diseases and disorders give rise to oxidative damage including autoimmune diseases. An autoimmune disorder is a pathological condition characterized by the breakdown of self-tolerance of the immune system in the body. Immunological processes against tissues and organs lead to enhanced oxidative stress and, in turn, misbalance of oxidative stress aggravates the pathobiology of the disease. Highly reactive nature of free radicals, for example hydroxyl and superoxide ions, alters DNA, protein, and lipids in the body which augment the pathologic processes of diseases. The damaged biomolecules are responsible for systemic complications and secondary disease co-morbidities. In this review, we discuss the role of oxidative stress in some incapacitating autoimmune diseases like Rheumatoid arthritis, Systemic Lupus Erythematosus, Type 1 Diabetes, and Multiple Sclerosis. Oxidative stress plays a central and course defining role in these diseases and it has become a necessity to study the pathological mechanism involved in oxidative stress to better understand and offer treatment holistically. Presently there are no clinically available parameters for measurement and treatment of pathological oxidative stress, therefore it requires intensive research. Probably, in the future, the discovery of easily detectable markers of oxidative stress can aid in the diagnosis, prognosis, and treatment of progressively destructive autoimmune diseases.

Keywords: Autoimmune diseases, oxidative stress, reactive oxygen species, rheumatoid arthritis, systemic lupus erythematosus, type 1 diabetes, multiple sclerosis.

« Previous Next »
Graphical Abstract

[1]
Saegusa, J. Seiji Kawano; and Shunichi Kumagai, Oxidative Stress and Autoimmune Diseases; Oxidative Stress, Disease, and Cancer, 2006, pp. 461-475.
[2]
Isoherranen, K.; Westermarck, J.; Kähäri, V-M.; Jansén, C.; Punnonen, K. Differential regulation of the AP-1 family members by UV irradiation in vitro and in vivo. Cell. Signal., 1998, 10(3), 191-195.
[http://dx.doi.org/10.1016/S0898-6568(97)00100-9] [PMID: 9607142]
[3]
Saliou, C.; Kitazawa, M.; McLaughlin, L.; Yang, J-P.; Lodge, J.K.; Tetsuka, T.; Iwasaki, K.; Cillard, J.; Okamoto, T.; Packer, L. Antioxidants modulate acute solar ultraviolet radiation-induced NFkappa-B activation in a human keratinocyte cell line. Free Radic.Biol. Med., 1999, 26(1-2), 174-183..
[http://dx.doi.org/10.1016/S0891-5849(98)00212-3] [PMID: 9890652]
[4]
Dalal, V.; Sharma, N.K.; Biswas, S. Oxidative Stress: Diagnostic Methods and Application in Medical Science.Oxidative Stress: Diagnostic Methods and Applications in Medical Science; Springer, 2017, pp. 23-45.
[http://dx.doi.org/10.1007/978-981-10-4711-4_2]
[5]
Kumagai, S.; Jikimoto, T.; Saegusa, J. Pathological roles of oxidative stress in autoimmune diseases. Jpn. J. Clin. Pathol., 2003, 51, 126-132.
[http://dx.doi.org/10.12659/MSM.914898]
[6]
Lennon, S.V.; Martin, S.J.; Cotter, T.G. Dose-dependent induction of apoptosis in human tumour cell lines by widely diverging stimuli. Cell Prolif., 1991, 24(2), 203-214.
[http://dx.doi.org/10.1111/j.1365-2184.1991.tb01150.x] [PMID: 2009322]
[7]
Mittal, M.; Siddiqui, M.R.; Tran, K.; Reddy, S.P.; Malik, A.B. Reactive oxygen species in inflammation and tissue injury. Antioxid. Redox Signal., 2014, 20(7), 1126-1167..
[http://dx.doi.org/10.1089/ars.2012.5149] [PMID: 23991888]
[8]
Owen, R.W.; Giacosa, A.; Hull, W.E.; Haubner, R.; Spiegelhalder, B.; Bartsch, H. The antioxidant/anticancer potential of phenolic compounds isolated from olive oil. Eur. J. Cancer,, 2000, 36(10), 1235-1247.
[http://dx.doi.org/10.1016/S0959-8049(00)00103-9] [PMID: 10882862]
[9]
Gilgun-Sherki, Y.; Melamed, E.; Offen, D. Oxidative stress induced-neurodegenerative diseases: the need for antioxidants that penetrate the blood brain barrier. Neuropharmacology, 2001, 40(8), 959-975..
[http://dx.doi.org/10.1016/S0028-3908(01)00019-3] [PMID: 11406187]
[10]
Utz, P.J.; Anderson, P. Posttranslational protein modifications, apoptosis, and the bypass of tolerance to autoantigens. Arthritis Rheum., 1998, 41(7), 1152-1160.
[http://dx.doi.org/10.1002/1529-0131 (199807)41:7<1152::AIDART3> 3.0.CO;2-L] [PMID: 9663470]
[11]
Henrotin, Y.; Kurz, B.; Aigner, T. Oxygen and reactive oxygen species in cartilage degradation: friends or foes? Osteoarthritis Cartilage, 2005, 13(8), 643-654.
[http://dx.doi.org/10.1016/j.joca.2005.04.002] [PMID: 15936958]
[12]
Bashir, S.; Harris, G.; Denman, M.A.; Blake, D.R.; Winyard, P.G. Oxidative DNA damage and cellular sensitivity to oxidative stress in human autoimmune diseases. Ann. Rheum. Dis., 1993, 52(9), 659-666.
[http://dx.doi.org/10.1136/ard.52.9.659] [PMID: 8239761]
[13]
Bhusate, L.L.; Herbert, K.E.; Scott, D.L.; Perrett, D. Increased DNA strand breaks in mononuclear cells from patients with rheumatoid arthritis. Ann. Rheum. Dis., 1992, 51(1), 8-12.
[http://dx.doi.org/10.1136/ard.51.1.8] [PMID: 1540043]
[14]
Ryan, B.J.; Nissim, A.; Winyard, P.G. Oxidative post-translational modifications and their involvement in the pathogenesis of autoimmune diseases. Redox Biol., 2014, 2, 715-724.
[http://dx.doi.org/10.1016/j.redox.2014.05.004] [PMID: 24955328]
[15]
Liu, W.; Shi, L.J.; Li, S.G. The Immunomodulatory Effect of Alpha-Lipoic Acid in Autoimmune Diseases. BioMed Res. Int., 2019, 2019 8086257
[http://dx.doi.org/10.1155/2019/8086257] [PMID: 31016198]
[16]
Kasiri, N.; Rahmati, M.; Ahmadi, L.; Eskandari, N. The significant impact of apigenin on different aspects of autoimmune disease. Inflammopharmacology, 2018, 26(6), 1359-1373.
[http://dx.doi.org/10.1007/s10787-018-0531-8] [PMID: 30229507]
[17]
Dai, Q.; Zhou, D.; Xu, L.; Song, X. Curcumin alleviates rheumatoid arthritis-induced inflammation and synovial hyperplasia by targeting mTOR pathway in rats. Drug Des. Devel. Ther., 2018, 12, 4095-4105.
[http://dx.doi.org/10.2147/DDDT.S175763] [PMID: 30584274]
[18]
Picerno, V.; Ferro, F.; Adinolfi, A.; Valentini, E.; Tani, C.; Alunno, A. One year in review: the pathogenesis of rheumatoid arthritis. Clin. Exp. Rheumatol., 2015, 33(4), 551-558.
[PMID: 26203933]
[19]
Smolen, J.S.; Aletaha, D.; Barton, A.; Burmester, G.R.; Emery, P.; Firestein, G.S.; Kavanaugh, A.; McInnes, I.B.; Solomon, D.H.; Strand, V.; Yamamoto, K. Rheumatoid arthritis. Nat. Rev. Dis. Primers, 2018, 4, 18001.
[http://dx.doi.org/10.1038/nrdp.2018.1] [PMID: 29417936]
[20]
Handa, R.; Rao, U.R.K.; Lewis, J.F.; Rambhad, G.; Shiff, S.; Ghia, C.J. Literature review of rheumatoid arthritis in India. Int. J. Rheum. Dis., 2016, 19(5), 440-451.
[http://dx.doi.org/10.1111/1756-185X.12621] [PMID: 26171649]
[21]
van der Helm-van Mil, A.H.; Wesoly, J.Z.; Huizinga, T.W. Understanding the genetic contribution to rheumatoid arthritis. Curr. Opin. Rheumatol., 2005, 17(3), 299-304.
[http://dx.doi.org/10.1097/01.bor.0000160780.13012.be] [PMID: 15838240]
[22]
Jimenez-Boj, E.; Redlich, K.; Türk, B.; Hanslik-Schnabel, B.; Wanivenhaus, A.; Chott, A.; Smolen, J.S.; Schett, G. Interaction between synovial inflammatory tissue and bone marrow in rheumatoid arthritis. J. Immunol., 2005, 175(4), 2579-2588.
[http://dx.doi.org/10.4049/jimmunol.175.4.2579] [PMID: 16081832]
[23]
Mapp, P.I.; Grootveld, M.C.; Blake, D.R. Hypoxia, oxidative stress and rheumatoid arthritis. Br. Med. Bull., 1995, 51(2), 419-436.
[http://dx.doi.org/10.1093/oxfordjournals.bmb.a072970] [PMID: 7552073]
[24]
Ozkan, Y.; Yardým-Akaydýn, S.; Sepici, A.; Keskin, E.; Sepici, V.; Simsek, B. Oxidative status in rheumatoid arthritis. Clin. Rheumatol., 2007, 26(1), 64-68.
[http://dx.doi.org/10.1007/s10067-006-0244-z] [PMID: 16565896]
[25]
Iskander, K.; Li, J.; Han, S.; Zheng, B.; Jaiswal, A.K. NQO1 and NQO2 regulation of humoral immunity and autoimmunity. J. Biol. Chem., 2006, 281(41), 30917-30924.
[http://dx.doi.org/10.1074/jbc.M605809200] [PMID: 16905546]
[26]
Wruck, C.J.; Fragoulis, A.; Gurzynski, A.; Brandenburg, L-O.; Kan, Y.W.; Chan, K.; Hassenpflug, J.; Freitag-Wolf, S.; Varoga, D.; Lippross, S.; Pufe, T. Role of oxidative stress in rheumatoid arthritis: insights from the Nrf2-knockout mice. Ann. Rheum. Dis., 2011, 70(5), 844-850.
[http://dx.doi.org/10.1136/ard.2010.132720] [PMID: 21173018]
[27]
Kundu, S.; Ghosh, P.; Datta, S.; Ghosh, A.; Chattopadhyay, S.; Chatterjee, M. Oxidative stress as a potential biomarker for determining disease activity in patients with rheumatoid arthritis. Free Radic. Res., 2012, 46(12), 1482-1489.
[http://dx.doi.org/10.3109/10715762.2012.727991] [PMID: 22998065]
[28]
Newkirk, M.M.; Goldbach-Mansky, R.; Lee, J.; Hoxworth, J.; McCoy, A.; Yarboro, C.; Klippel, J.; El-Gabalawy, H.S. Advanced glycation end-product (AGE)-damaged IgG and IgM autoantibodies to IgG-AGE in patients with early synovitis. Arthritis Res. Ther., 2003, 5(2), R82-R90.
[http://dx.doi.org/10.1186/ar622] [PMID: 12718751]
[29]
Kurien, B.T.; Scofield, R.H. Autoimmunity and oxidatively modified autoantigens. Autoimmun. Rev., 2008, 7(7), 567-573.
[http://dx.doi.org/10.1016/j.autrev.2008.04.019] [PMID: 18625446]
[30]
Lapolla, A.; Fedele, D.; Garbeglio, M.; Martano, L.; Tonani, R.; Seraglia, R.; Favretto, D.; Fedrigo, M.A.; Traldi, P. Matrix-assisted laser desorption/ionization mass spectrometry, enzymatic digestion, and molecular modeling in the study of nonenzymatic glycation of IgG. J. Am. Soc. Mass Spectrom., 2000, 11(2), 153-159.
[http://dx.doi.org/10.1016/S1044-0305(99)00134-8] [PMID: 10689668]
[31]
Migita, K.; Yamasaki, S.; Kita, M.; Ida, H.; Shibatomi, K.; Kawakami, A.; Aoyagi, T.; Eguchi, K. Nitric oxide protects cultured rheumatoid synovial cells from Fas-induced apoptosis by inhibiting caspase-3. Immunology, 2001, 103(3), 362-367.
[http://dx.doi.org/10.1046/j.1365-2567.2001.01252.x] [PMID: 11454065]
[32]
Xu, K.; Xu, P.; Yao, J-F.; Zhang, Y-G.; Hou, W.K.; Lu, S-M. Reduced apoptosis correlates with enhanced autophagy in synovial tissues of rheumatoid arthritis. Inflamm. Res., 2013, 62(2), 229-237.
[http://dx.doi.org/10.1007/s00011-012-0572-1] [PMID: 23178792]
[33]
Veselinovic, M.; Barudzic, N.; Vuletic, M.; Zivkovic, V.; Tomic-Lucic, A.; Djuric, D.; Jakovljevic, V. Oxidative stress in rheumatoid arthritis patients: relationship to diseases activity. Mol. Cell. Biochem., 2014, 391(1-2), 225-232.
[http://dx.doi.org/10.1007/s11010-014-2006-6] [PMID: 24610042]
[34]
Filippin, L.I.; Vercelino, R.; Marroni, N.P.; Xavier, R.M. Redox signalling and the inflammatory response in rheumatoid arthritis. Clin. Exp. Immunol., 2008, 152(3), 415-422.
[http://dx.doi.org/10.1111/j.1365-2249.2008.03634.x] [PMID: 18422737]
[35]
Jikimoto, T.; Nishikubo, Y.; Koshiba, M.; Kanagawa, S.; Morinobu, S.; Morinobu, A.; Saura, R.; Mizuno, K.; Kondo, S.; Toyokuni, S.; Nakamura, H.; Yodoi, J.; Kumagai, S. Thioredoxin as a biomarker for oxidative stress in patients with rheumatoid arthritis. Mol. Immunol., 2002, 38(10), 765-772.
[http://dx.doi.org/10.1016/S0161-5890(01)00113-4] [PMID: 11841836]
[36]
Sklodowska, M.; Gromadzińska, J.; Biernacka, M.; Wasowicz, W.; Wolkanin, P.; Marszalek, A.; Brózik, H.; Pokuszyńska, K.; Vitamin, E. Vitamin E, thiobarbituric acid reactive substance concentrations and superoxide dismutase activity in the blood of children with juvenile rheumatoid arthritis. Clin. Exp. Rheumatol., 1996, 14(4), 433-439.
[PMID: 8871845]
[37]
Oztürk, H.S.; Çimen, M.Y.; Çimen, Ö.B.; Kaçmaz, M.; Durak, I. Oxidant/antioxidant status of plasma samples from patients with rheumatoid arthritis. Rheumatol. Int., 1999, 19(1-2), 35-37.
[http://dx.doi.org/10.1007/s002960050097] [PMID: 10651080]
[38]
Walwadkar, S.D.; Suryakar, A.N.; Katkam, R.V.; Kumbar, K.M.; Ankush, R.D. Oxidative stress and calcium-phosphorus levels in Rheumatoid arthritis. Indian J. Clin. Biochem., 2006, 21(2), 134-137.
[http://dx.doi.org/10.1007/BF02912928] [PMID: 23105630]
[39]
García-González, A.; Gaxiola-Robles, R.; Zenteno-Savín, T. Oxidative stress in patients with rheumatoid arthritis. Rev. Invest. Clin., 2015, 67(1), 46-53.
[http://dx.doi.org/10.1155/2016/6097417] [PMID: 25857584]
[40]
Hassan, S.Z.; Gheita, T.A.; Kenawy, S.A.; Fahim, A.T.; El-Sorougy, I.M.; Abdou, M.S. Oxidative stress in systemic lupus erythematosus and rheumatoid arthritis patients: relationship to disease manifestations and activity. Int. J. Rheum. Dis., 2011, 14(4), 325-331.
[http://dx.doi.org/10.1111/j.1756-185X.2011.01630.x] [PMID: 22004228]
[41]
Hadjigogos, K. The role of free radicals in the pathogenesis of rheumatoid arthritis. Panminerva Med., 2003, 45(1), 7-13.
[PMID: 12682616]
[42]
Heliövaara, M.; Knekt, P.; Aho, K.; Aaran, R.K.; Alfthan, G.; Aromaa, A. Serum antioxidants and risk of rheumatoid arthritis. Ann. Rheum. Dis., 1994, 53(1), 51-53.https://dx.doi.org/10.1136%2Fard.53.1.51
[http://dx.doi.org/10.1136/ard.53.1.51] [PMID: 8311556]
[43]
Corsiero, E.; Pratesi, F.; Prediletto, E.; Bombardieri, M.; Migliorini, P. NETosis as source of autoantigens in rheumatoid arthritis. Front. Immunol., 2016, 7, 485.
[PMID: 27895639]
[44]
Kuhn, A.; Bonsmann, G.; Anders, H.J.; Herzer, P.; Tenbrock, K.; Schneider, M. The diagnosis and treatment of systemic lupus erythematosus. Dtsch. Arztebl. Int., 2015, 112(25), 423-432.
[http://dx.doi.org/10.3238/arztebl.2015.0423]
[45]
Baechler, E.C.; Batliwalla, F.M.; Karypis, G. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc. Natl. Acad. Sci. U.S.A., 2003, 100(5) 2610e5.2003,
[http://dx.doi.org/10.1073/pnas.0337679100]
[46]
Perl, A.; Hanczko, R.; Doherty, E. Assessment of mitochondrial dysfunction in lymphocytes of patients with systemic lupus erythematosus. Methods Mol. Biol., 2012, 900, 61-89.
[http://dx.doi.org/10.1007/978-1-60761-720-4_4] [PMID: 22933065]
[47]
Shah, D.; Kiran, R.; Wanchu, A.; Bhatnagar, A. Soluble granzyme B and cytotoxic T lymphocyte activity in the pathogenesis of systemic lupus erythematosus. Cell. Immunol., 2011, 269(1), 16-21.
[http://dx.doi.org/10.1016/j.cellimm.2011.03.004] [PMID: 21458778]
[48]
Casciola-Rosen, L.A.; Anhalt, G.; Rosen, A. Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J. Exp. Med., 1994, 179(4), 1317-1330.
[http://dx.doi.org/10.1084/jem.179.4.1317] [PMID: 7511686]
[49]
Knight, J.S.; Carmona-Rivera, C.; Kaplan, M.J. Proteins derived from neutrophil extracellular traps may serve as self-antigens and mediate organ damage in autoimmune diseases. Front. Immunol., 2012, 3, 380.
[http://dx.doi.org/10.3389/fimmu.2012.00380] [PMID: 23248629]
[50]
Durcan, L.; Petri, M. Immunomodulators in SLE: Clinical evidence and immunologic actions. J. Autoimmun., 2016, 74, 73-84.
[http://dx.doi.org/10.1016/j.jaut.2016.06.010] [PMID: 27371107]
[51]
Munoz, L.E.; van Bavel, C.; Franz, S.; Berden, J.; Herrmann, M.; van der Vlag, J. Apoptosis in the pathogenesis of systemic lupus erythematosus. Lupus, 2008, 17(5), 371-375.
[http://dx.doi.org/10.1177/0961203308089990] [PMID: 18490410]
[52]
Alam, K. Moinuddin; Jabeen, S. Immunogenicity of mitochondrial DNA modified by hydroxyl radical. Cell. Immunol., 2007, 247(1), 12-17.
[http://dx.doi.org/10.1016/j.cellimm.2007.06.007] [PMID: 17716639]
[53]
Perl, A.; Gergely, P., Jr; Banki, K. Mitochondrial dysfunction in T cells of patients with systemic lupus erythematosus. Int. Rev. Immunol., 2004, 23(3-4), 293-313.
[http://dx.doi.org/10.1080/08830180490452576] [PMID: 15204090]
[54]
Ahsan, H.; Ali, A.; Ali, R. Oxygen free radicals and systemic autoimmunity. Clin. Exp. Immunol., 2003, 131(3), 398-404.
[http://dx.doi.org/10.1046/j.1365-2249.2003.02104.x] [PMID: 12605691]
[55]
Perl, A. Oxidative stress in the pathology and treatment of systemic lupus erythematosus. Nat. Rev. Rheumatol., 2013, 9(11), 674-686.
[http://dx.doi.org/10.1038/nrrheum.2013.147] [PMID: 24100461]
[56]
Shah, D.; Sah, S.; Wanchu, A.; Wu, M.X.; Bhatnagar, A. Altered redox state and apoptosis in the pathogenesis of systemic lupus erythematosus. Immunobiology, 2013, 218(4), 620-627.
[http://dx.doi.org/10.1016/j.imbio.2012.07.030] [PMID: 22940256]
[57]
Vignais, P.V. The superoxide-generating NADPH oxidase: structural aspects and activation mechanism. Cell. Mol. Life Sci., 2002, 59(9), 1428-1459.
[http://dx.doi.org/10.1007/s00018-002-8520-9] [PMID: 12440767]
[58]
Rimbach, G.; Höhler, D.; Fischer, A.; Roy, S.; Virgili, F.; Pallauf, J.; Packer, L. Methods to assess free radicals and oxidative stress in biological systems. Arch. Tierernahr., 1999, 52(3), 203-222.https://doi.org/10.1106%2F108201302026770
[http://dx.doi.org/10.1080/17450399909386163] [PMID: 10553486]
[59]
Calingasan, N.Y.; Uchida, K.; Gibson, G.E. Protein-bound acrolein: a novel marker of oxidative stress in Alzheimer’s disease. J. Neurochem., 1999, 72(2), 751-756.
[http://dx.doi.org/10.1046/j.1471-4159.1999.0720751.x] [PMID: 9930749]
[60]
Hartley, D.P.; Kroll, D.J.; Petersen, D.R. Prooxidant-initiated lipid peroxidation in isolated rat hepatocytes: detection of 4-hydroxynonenal- and malondialdehyde-protein adducts. Chem. Res. Toxicol., 1997, 10(8), 895-905.
[http://dx.doi.org/10.1021/tx960181b] [PMID: 9282839]
[61]
Levine, R.L.; Garland, D.; Oliver, C.N.; Amici, A.; Climent, I.; Lenz, A-G.; Ahn, B-W.; Shaltiel, S.; Stadtman, E.R. Determination of carbonyl content in oxidatively modified proteins.Methods in Enzymology; Elsevier, 1990, pp. 464-478.
[62]
Shah, D.; Sah, S.; Nath, S.K. Interaction between glutathione and apoptosis in systemic lupus erythematosus. Autoimmun. Rev., 2013, 12(7), 741-751.
[http://dx.doi.org/10.1016/j.autrev.2012.12.007] [PMID: 23279845]
[63]
Al-Shobaili, H.A.; Al Robaee, A.A.; Alzolibani, A.A.; Rasheed, Z. Antibodies against 4-hydroxy-2-nonenal modified epitopes recognized chromatin and its oxidized forms: role of chromatin, oxidized forms of chromatin and 4-hydroxy-2-nonenal modified epitopes in the etiopathogenesis of SLE. Dis. Markers, 2012, 33(1), 19-34.
[http://dx.doi.org/10.1155/2012/532497] [PMID: 22710866]
[64]
Jovanović, V.; Abdul Aziz, N.; Lim, Y.T.; Ng Ai Poh, A.; Jin, Hui.Chan. S.; Ho Xin Pei, E.; Lew, F.C.; Shui, G.; Jenner, A.M.; Bowen, L.; McKinney, E.F.; Lyons, P.A.; Kemeny, M.D.; Smith, K.G.; Wenk, M.R.; Macary, P.A. Lipid anti-lipid antibody responses correlate with disease activity in systemic lupus erythematosus. PLoS One, 2013, 8(2) e55639
[http://dx.doi.org/10.1371/journal.pone.0055639] [PMID: 23409013]
[65]
Messina, J.P.; Lawrence, D.A. Cell cycle progression of glutathione-depleted human peripheral blood mononuclear cells is inhibited at S phase. J. Immunol., 1989, 143(6), 1974-1981.
[PMID: 2789253]
[66]
Peterson, J.D.; Herzenberg, L.A.; Vasquez, K.; Waltenbaugh, C. Glutathione levels in antigen-presenting cells modulate Th1 versus Th2 response patterns. Proc. Natl. Acad. Sci. USA, 1998, 95(6), 3071-3076.
[http://dx.doi.org/10.1073/pnas.95.6.3071] [PMID: 9501217]
[67]
Shah, D.; Kiran, R.; Wanchu, A.; Bhatnagar, A. Relationship between T lymphocyte subsets and cortisol in systemic lupus erythematosus. Kathmandu Univ. Med. J.[KUMJ], 2009, 7(27), 213-219.
[http://dx.doi.org/10.3126/kumj.v7i3.2726] [PMID: 20071865]
[68]
Shah, D.; Aggarwal, A.; Bhatnagar, A.; Kiran, R.; Wanchu, A. Association between T lymphocyte sub-sets apoptosis and peripheral blood mononuclear cells oxidative stress in systemic lupus erythematosus. Free Radic. Res., 2011, 45(5), 559-567.
[http://dx.doi.org/10.3109/10715762.2011.555765] [PMID: 21284579]
[69]
Shah, D.; Kiran, R.; Wanchu, A.; Bhatnagar, A. Oxidative stress in systemic lupus erythematosus: relationship to Th1 cytokine and disease activity. Immunol. Lett., 2010, 129(1), 7-12.
[http://dx.doi.org/10.1016/j.imlet.2010.01.005] [PMID: 20105444]
[70]
Turgay, M.; Durak, I.; Erten, S.; Ertugrul, E.; Devrim, E.; Avci, A.; Turgay, F. Oxidative stress and antioxidant parameters in a Turkish group of patients with active and inactive systemic lupus erythematosus. Int. J. Rheum. Dis., 2007, 10, 101-106.
[http://dx.doi.org/10.1111/j.1479-8077.2007.00268.x]
[71]
Dwivedi, N.; Radic, M. Citrullination of autoantigens implicates NETosis in the induction of autoimmunity. Ann. Rheum. Dis., 2014, 73(3), 483-491.
[http://dx.doi.org/10.1136/annrheumdis-2013-203844] [PMID: 24291655]
[72]
Barrajón-Catalán, E.; Herranz-López, M.; Joven, J.; Segura-Carretero, A.; Alonso-Villaverde, C.; Menéndez, J.A.; Micol, V. Molecular promiscuity of plant polyphenols in the management of age-related diseases: far beyond their antioxidant properties. Adv. Exp. Med. Biol., 2014, 824, 141-159.
[http://dx.doi.org/10.1007/978-3-319-07320-0_11] [PMID: 25038998]
[73]
Guo, Y.; Yu, S.; Zhang, C.; Kong, A.N. Epigenetic regulation of Keap1-Nrf2 signaling. Free Radic. Biol. Med., 2015, 88(Pt B), 337-349..
[http://dx.doi.org/10.1016/j.freeradbiomed.2015.06.013] [PMID: 26117320]
[74]
Atkinson, M.A.; Eisenbarth, G.S.; Michels, A.W. Type 1 diabetes. Lancet, 2014, 383(9911), 69-82.
[http://dx.doi.org/10.1016/S0140-6736(13)60591-7] [PMID: 23890997]
[75]
Alkholy, U.M.; Abdalmonem, N.; Zaki, A.; Elkoumi, M.A.; Hashim, M.I.A.; Basset, M.A.; Salah, H.E. The antioxidant status of coenzyme Q10 and vitamin E in children with type 1 diabetes. J. Pediatr. (Rio J.), 2018.
[http://dx.doi.org/10.1016/j.jped.2017.12.005] [PMID: 29425798]
[76]
Francescato, M.P.; Stel, G.; Geat, M.; Cauci, S. Oxidative stress in patients with type 1 diabetes mellitus: is it affected by a single bout of prolonged exercise? PLoS One, 2014, 9(6) e99062
[http://dx.doi.org/10.1371/journal.pone.0099062] [PMID: 24905823]
[77]
Vistoli, G.; De Maddis, D.; Cipak, A.; Zarkovic, N.; Carini, M.; Aldini, G. Aldini. Advanced glycoxidation and lipoxidation end products (AGEs and ALEs): an overview of their mechanisms of formation. Free Radical Res., 2013, 47(Supl. 1), 3-27.
[http://dx.doi.org/10.3109/10715762.2013.815348]
[78]
Rubin, M.R.; Paschalis, E.P.; Poundarik, A.; Sroga, G.E.; McMahon, D.J.; Gamsjaeger, S.; Klaushofer, K.; Vashishth, D. Advanced glycation endproducts and bone material properties in type 1 diabetic mice. PLoS One, 2016, 11(5) e0154700
[http://dx.doi.org/10.1371/journal.pone.0154700] [PMID: 27140650]
[79]
Loghmani, E. Diabetes mellitus: type 1 and type 2. Guidelines for adolescent nutrition services 2005, 167-182..
[http://dx.doi.org/10.1371/journal.pone.0154700]
[80]
Kangralkar, V.; Patil, S.D.; Bandivadekar, R. Oxidative stress and diabetes: a review. Int. J. Pharm. Appl., 2010, 1, 38-45.
[http://dx.doi.org/10.1016/j.jsps.2015.03.013]
[81]
Ozougwu, J.; Obimba, K.; Belonwu, C.; Unakalamba, C. The pathogenesis and pathophysiology of type 1 and type 2 diabetes mellitus. J. Physiol. Pathophysiol., 2013, 4, 46-57.
[http://dx.doi.org/10.5897/JPAP2013.0001]
[82]
Kawasaki, E. Type 1 diabetes and autoimmunity. Clin. Pediatr. Endocrinol., 2014, 23(4), 99-105.
[http://dx.doi.org/10.1297/cpe.23.99] [PMID: 25374439]
[83]
Kordonouri, O.; Klinghammer, A.; Lang, E.B.; Grüters-Kieslich, A.; Grabert, M.; Holl, R.W. Thyroid autoimmunity in children and adolescents with type 1 diabetes: a multicenter survey. Diabetes Care, 2002, 25(8), 1346-1350.
[http://dx.doi.org/10.2337/diacare.25.8.1346] [PMID: 12145233]
[84]
Steck, A.K.; Vehik, K.; Bonifacio, E.; Lernmark, A.; Ziegler, A.G.; Hagopian, W.A.; She, J.; Simell, O.; Akolkar, B.; Krischer, J.; Schatz, D.; Rewers, M.J. TEDDY Study Group. Predictors of progression from the appearance of islet autoantibodies to early childhood diabetes: The Environmental Determinants of Diabetes in the Young (TEDDY). Diabetes Care, 2015, 38(5), 808-813.
[http://dx.doi.org/10.2337/dc14-2426] [PMID: 25665818]
[85]
Towns, R.; Pietropaolo, M. GAD65 autoantibodies and its role as biomarker of Type 1 diabetes and Latent Autoimmune Diabetes in Adults (LADA). Drugs Future, 2011, 36(11), 847.
[http://dx.doi.org/10.1358/dof.2011.036.11.1710754] [PMID: 22869930]
[86]
Maritim, A.C.; Sanders, R.A.; Watkins, J.B. III Diabetes, oxidative stress, and antioxidants: a review. J. Biochem. Mol. Toxicol., 2003, 17(1), 24-38.
[http://dx.doi.org/10.1002/jbt.10058] [PMID: 12616644]
[87]
Moussa, S. Oxidative stress in diabetes mellitus. Rom. J. Biophys., 2008, 18, 225-236.
[http://dx.doi.org/10.15761/IOD.1000116]
[88]
Ayepola, O.R.; Brooks, N.L.; Oguntibeju, O.O. Oxidative stress and diabetic complications: The role of antioxidant vitamins and flavonoids. In: Antioxidant-Antidiabetic Agents and Human Health, In Tech; , 2014.
[http://dx.doi.org/10.5772/572822]
[89]
Ceriello, A. Oxidative stress and diabetes-associated complications. Endocr. Pract., 2006, 12(Suppl. 1), 60-62.
[http://dx.doi.org/10.4158/EP.12.S1.60] [PMID: 16627383]
[90]
Wang, Y.; Xiao, Y.; Zhong, L.; Ye, D.; Zhang, J.; Tu, Y.; Bornstein, S.R.; Zhou, Z.; Lam, K.S.; Xu, A. Increased neutrophil elastase and proteinase 3 and augmented NETosis are closely associated with β-cell autoimmunity in patients with type 1 diabetes. Diabetes, 2014, 63(12), 4239-4248.
[http://dx.doi.org/10.2337/db14-0480] [PMID: 25092677]
[91]
Liu, C.W.; Bramer, L.; Webb-Robertson, B.J.; Waugh, K.; Rewers, M.J.; Zhang, Q. Temporal expression profiling of plasma proteins reveals oxidative stress in early stages of Type 1 Diabetes progression. J. Proteomics, 2018, 172, 100-110.
[http://dx.doi.org/10.1016/j.jprot.2017.10.004] [PMID: 28993202]
[92]
Adamczyk, B.; Adamczyk-Sowa, M. New insights into the role of oxidative stress mechanisms in the pathophysiology and treatment of multiple sclerosis. Oxid. Med. Cell. Longev., 2016, 2016 1973834
[http://dx.doi.org/10.1155/2016/1973834] [PMID: 27829982]
[93]
Gilgun-Sherki, Y.; Melamed, E.; Offen, D. The role of oxidative stress in the pathogenesis of multiple sclerosis: the need for effective antioxidant therapy. J. Neurol., 2004, 251(3), 261-268.
[http://dx.doi.org/10.1007/s00415-004-0348-9] [PMID: 15015004]
[94]
Wingerchuk, D.M.; Lucchinetti, C.F.; Noseworthy, J.H. Multiple sclerosis: current pathophysiological concepts. Lab. Invest., 2001, 81(3), 263-281.
[http://dx.doi.org/10.1038/labinvest.3780235] [PMID: 11310820]
[95]
Musse, A.A.; Boggs, J.M.; Harauz, G. Deimination of membrane-bound myelin basic protein in multiple sclerosis exposes an immunodominant epitope. Proc. Natl. Acad. Sci. USA, 2006, 103(12), 4422-4427.
[http://dx.doi.org/10.1073/pnas.0509158103] [PMID: 16537438]
[96]
Ponomarenko, N.A.; Durova, O.M.; Vorobiev, I.I.; Belogurov, A.A., Jr; Kurkova, I.N.; Petrenko, A.G.; Telegin, G.B.; Suchkov, S.V.; Kiselev, S.L.; Lagarkova, M.A.; Govorun, V.M.; Serebryakova, M.V.; Avalle, B.; Tornatore, P.; Karavanov, A.; Morse, H.C., III; Thomas, D.; Friboulet, A.; Gabibov, A.G. Autoantibodies to myelin basic protein catalyze site-specific degradation of their antigen. Proc. Natl. Acad. Sci. USA, 2006, 103(2), 281-286.
[http://dx.doi.org/10.1073/pnas.0509849103] [PMID: 16387849]
[97]
Ortiz, G.G.; Pacheco-Moisés, F.P.; Bitzer-Quintero, O.K.; Ramírez-Anguiano, A.C.; Flores-Alvarado, L.J.; Ramírez-Ramírez, V.; Macias-Islas, M.A.; Torres-Sánchez, E.D. Immunology and oxidative stress in multiple sclerosis: clinical and basic approach. Clin. Dev. Immunol., 2013, 2013 708659
[http://dx.doi.org/10.1155/2013/708659] [PMID: 24174971]
[98]
Polman, C.H.; O’Connor, P.W.; Havrdova, E.; Hutchinson, M.; Kappos, L.; Miller, D.H.; Phillips, J.T.; Lublin, F.D.; Giovannoni, G.; Wajgt, A.; Toal, M.; Lynn, F.; Panzara, M.A.; Sandrock, A.W. AFFIRM Investigators. A randomized, placebo-controlled trial of natalizumab for relapsing multiple sclerosis. N. Engl. J. Med., 2006, 354(9), 899-910.
[http://dx.doi.org/10.1056/NEJMoa044397] [PMID: 16510744]
[99]
Hug, A.; Korporal, M.; Schröder, I.; Haas, J.; Glatz, K.; Storch-Hagenlocher, B.; Wildemann, B. Thymic export function and T cell homeostasis in patients with relapsing remitting multiple sclerosis. J. Immunol., 2003, 171(1), 432-437.
[http://dx.doi.org/10.4049/jimmunol.171.1.432] [PMID: 12817027]
[100]
Matute, C.; Sánchez-Gómez, M.V.; Martínez-Millán, L.; Miledi, R. Glutamate receptor-mediated toxicity in optic nerve oligodendrocytes. Proc. Natl. Acad. Sci. USA, 1997, 94(16), 8830-8835.
[http://dx.doi.org/10.1073/pnas.94.16.8830] [PMID: 9238063]
[101]
McDonald, J.W.; Althomsons, S.P.; Hyrc, K.L.; Choi, D.W.; Goldberg, M.P. Oligodendrocytes from forebrain are highly vulnerable to AMPA/kainate receptor-mediated excitotoxicity. Nat. Med., 1998, 4(3), 291-297.
[http://dx.doi.org/10.1038/nm0398-291] [PMID: 9500601]
[102]
Werner, P.; Pitt, D.; Raine, C.S. Multiple sclerosis: altered glutamate homeostasis in lesions correlates with oligodendrocyte and axonal damage. Ann. Neurol., 2001, 50(2), 169-180.
[http://dx.doi.org/10.1002/ana.1077] [PMID: 11506399]
[103]
Dringen, R.; Pawlowski, P.G.; Hirrlinger, J. Peroxide detoxification by brain cells. J. Neurosci. Res., 2005, 79(1-2), 157-165.
[http://dx.doi.org/10.1002/jnr.20280] [PMID: 15573410]
[104]
Van der Goes, A.; Wouters, D.; Van Der Pol, S.M.; Huizinga, R.; Ronken, E.; Adamson, P.; Greenwood, J.; Dijkstra, C.D.; De Vries, H.E. Reactive oxygen species enhance the migration of monocytes across the blood-brain barrier in vitro. FASEB J., 2001, 15(10), 1852-1854.
[http://dx.doi.org/10.1096/fj.00-0881fje] [PMID: 11481252]
[105]
Schreibelt, G.; Musters, R.J.; Reijerkerk, A.; de Groot, L.R.; van der Pol, S.M.; Hendrikx, E.M.; Döpp, E.D.; Dijkstra, C.D.; Drukarch, B.; de Vries, H.E. Lipoic acid affects cellular migration into the central nervous system and stabilizes blood-brain barrier integrity. J. Immunol., 2006, 177(4), 2630-2637.
[http://dx.doi.org/10.4049/jimmunol.177.4.2630] [PMID: 16888025]
[106]
Woodberry, T.; Bouffler, S.E.; Wilson, A.S.; Buckland, R.L.; Brüstle, A. The emerging role of neutrophil granulocytes in multiple sclerosis. J. Clin. Med., 2018, 7(12), 511.
[http://dx.doi.org/10.3390/jcm7120511] [PMID: 30513926]

Rights & Permissions Print Cite
Article Metrics
76
1
World Immunization Week
© 2024 Bentham Science Publishers | Privacy Policy