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1Academic Journal
Authors: E. K. Fetisova, N. V. Vorobjeva, M. S. Muntyan, Е. К. Фетисова, Н. В. Воробьева, М. С. Мунтян
Contributors: This research was performed under the state assignment of Moscow State University, project numbers 119121690043-3, 1243020800089-2, 121042600047-9., Работа выполнена в рамках госзадания МГУ на госбюджетной основе (научные проекты №/№ 119121690043-3, 1243020800089-2,121042600047-9).
Source: Vestnik Moskovskogo universiteta. Seriya 16. Biologiya; Том 79, № 4 (2024); 269-279 ; Вестник Московского университета. Серия 16. Биология; Том 79, № 4 (2024); 269-279 ; 0137-0952
Subject Terms: старение, oxidative stress, reactive oxygen species, neutrophils, mitochondria–targeted antioxidants, stem cells, helminth therapy, aging, окислительный стресс, активные формы кислорода, нейтрофилы, митохондриально-направленные антиоксиданты, стволовые клетки, гельминтотерапия
File Description: application/pdf
Relation: https://vestnik-bio-msu.elpub.ru/jour/article/view/1434/699; Huang W.J., Chen W.W., Zhang X. Multiple sclerosis: Pathology, diagnosis and treatments. Exp. Ther. Med. 2017;13(6):3163–3166.; Hauser S.L., Cree B.A.C. Treatment of multiple sclerosis: A review. Am. J. Med. 2020;133(12):1380-1390.e2.; Macaron G., Larochelle C., Arbour N., Galmard M., Girard J.M., Prat A., Duquette P. Impact of aging on treatment considerations for multiple sclerosis patients. Front. Neurol. 2023;14:1197212.; Ostolaza A., Corroza J., Ayuso T. Multiple sclerosis and aging: comorbidity and treatment challenges. Mult. Scler. Relat. Disord. 2021;50:102815.; Zhang Y., Atkinson J., Burd C.E., Graves J., Segal B.M. Biological aging in multiple sclerosis. Mult. Scler. 2023;29(14):1701–1708.; Zeydan B., Kantarci O.H. Impact of age on multiple sclerosis disease activity and progression. Curr. Neurol. Neurosci. Rep. 2020;20(7):24.; Fetisova E., Vorobjeva N., Muntyan M. Multiple sclerosis. Some features of pathology and prospects for therapy. Part 1. Adv. Gerontol. 2024;14(2):35–48.; Vorobjeva N.V., Chernyak B.V. NETosis: molecular mechanisms, role in physiology and pathology. Biochemistry (Mosc.). 2020;85(10):1178–1190.; De Bondt M., Hellings N., Opdenakker G., Struyf S. Neutrophils: underestimated players in the pathogenesis of multiple sclerosis (MS). Int. J. Mol. Sci. 2020;21(12):4558.; Dhaiban S., Al-Ani M., Elemam N.M., AlAawad M.H., Al-Rawi Z., Maghazachi A.A. Role of peripheral immune cells in multiple sclerosis and experimental autoimmune encephalomyelitis. Science. 2021;3(1):12.; Grebenciucova E., Pruitt A. Infections in patients receiving multiple sclerosis disease-modifying therapies. Curr. Neurol. Neurosci. Rep. 2017;17(11):88.; Fetisova E., Chernyak B., Korshunova G., Muntyan M., Skulachev V. Mitochondria-targeted antioxidants as a prospective therapeutic strategy for multiple sclerosis. Curr. Med. Chem. 2017;24(19):2086–2114.; Fetisova E.K., Muntyan M.S., Lyamzaev K.G., Chernyak B.V. Therapeutic effect of the mitochondriatargeted antioxidant SkQ1 on the culture model of multiple sclerosis. Oxid. Med. Cell. Longev. 2019;2019:2082561.; Fock E.M., Parnova R.G. Protective effect of mitochondria-targeted antioxidants against inflammatory response to lipopolysaccharide challenge: a review. Pharmaceutics. 2021;13(2):144.; Jiang Q., Yin J., Chen J., Ma X., Wu M., Liu G., Yao K., Tan B., Yin Y. Mitochondria-targeted antioxidants: a step towards disease treatment. Oxid. Med. Cell. Longev. 2020;2020:8837893.; Liberman E.A., Topaly V.P., Tsofina L.M., Jasaitis A.A., Skulachev V.P. Mechanism of coupling of oxidative phosphorylation and the membrane potential of mitochondria. Nature. 1969;222(5198):1076–1078.; Korshunova G.A., Shishkina A.V., Skulachev M.V. Design, synthesis, and some aspects of the biological activity of mitochondria-targeted antioxidants. Biochemistry (Mosc.). 2017;82(7):760–777.; Fields M., Marcuzzi A., Gonelli A., Celeghini C., Maximova N., Rimondi E. Mitochondria-targeted antioxidants, an innovative class of antioxidant compounds for neurodegenerative diseases: perspectives and limitations. Int. J. Mol. Sci. 2023;24(4):3739.; Skulachev V.P., Antonenko Y.N., Cherepanov D.A., et al. Prevention of cardiolipin oxidation and fatty acid cycling as two antioxidant mechanisms of cationic derivatives of plastoquinone (SkQs). Biochim. Biophys. Acta BBA-Bioenergetics. 2010;1797(6–7):878–89.; Antonenko Y.N., Avetisyan A.V., Bakeeva L.E., et al. Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 1. Cationic plastoquinone derivatives: synthesis and in vitro studies. Biochemistry (Mosc.). 2008;73(12):1273–1287.; Murphy M.P., Smith R.A.J. Targeting antioxidants to mitochondria by conjugation to lipophilic cations. Annu. Rev. Pharmacol. Toxicol. 2007;47(1):629–656.; Открытое исследование I фазы по изучению фармакокинетики, безопасности и переносимости препарата Пластомитин® при однократном приеме возрастающих доз у здоровых добровольцев. (Ответственный исследователь Щукин И.А.) [Электронный ресурс]. Государственный реестр лекарственных средств. 2016. Дата обновления: 15.12.2024. URL: https://grlsbase.ru/clinicaltrails/clintrail/3570 (дата обращения: 15.12.2024).; Fassas A., Anagnostopoulos A., Kazis A., Kapinas K., Sakellari I., Kimiskidis V., Tsompanakou A. Peripheral blood stem cell transplantation in the treatment of progressive multiple sclerosis: first results of a pilot study. Bone Marrow Transpl. 1997;20(8):631–638.; Iacobaeus E., Kadri N., Lefsihane K., Boberg E., Gavin C., Törnqvist Andrén A., Lilja A., Brundin L., Blanc K.L. Short and long term clinical and immunologic follow up after bone marrow mesenchymal stromal cell therapy in progressive multiple sclerosis – a phase I study. J. Clin. Med. 2019;8(12):2102.; Федулов А.С., Борисов А.В., Зафранская М.М., Кривенко С.И., Марченко Л.Н., Качан Т.В., Московских Ю.В., Нижегородова Д.Б. Сравнительная оценка эффективности однократного и курсового применения аутологичной трансплантации мезенхимальных стволовых клеток в терапии рассеянного склероза. РМЖ. Медицинское обозрение. 2019;3(4-2):54–58.; Bisaga G.N., Topuzova M.P., Malko V.A., Motorin D.V., Alekseeva Yu.A., Badaev R.S., Krinitsina T.V., Alekseeva T.M. High-dose chemotherapy with autologous hematopoietic stem cell transplantation in multiple sclerosis: intermediate results of 3 years research. Russ. Neurol. J. 2022;27(6):22–31.; Pluchino S., Quattrini A., Brambilla E., Gritti A., Salani G., Dina G., Galli R., Del Carro U., Amadio S., Bergami A., Furlan R., Comi G., Vescovi A.L., Martino G. Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature. 2003;422(6933):688–694.; Genchi A., Brambilla E., Sangalli F., et al. Neural stem cell transplantation in patients with progressive multiple sclerosis: an open-label, phase 1 study. Nat. Med. 2023;29(1):75–85.; Uccelli A., Laroni A., Ali R., et al. Safety, tolerability, and activity of mesenchymal stem cells versus placebo in multiple sclerosis (MESEMS): a phase 2, randomised, double-blind crossover trial. Lancet Neurol. 2021;20(11):917–929.; Сороковикова Т.В., Морозов А.М., Крюкова А.Н., Наумова С.А., Беляк М.А. Перспективы лечения прогрессирующих форм рассеяного склероза трасплантацией стволовых клеток (обзор литературы). Вестник медицинского института «Реавиз». Реабилитация, врач и здоровье. 2023;13(4):154–161.; Cecerska-Heryć E., Pękała M., Serwin N., Gliźniewicz M., Grygorcewicz B., Michalczyk A., Heryć R., Budkowska M., Dołęgowska B. The use of stem cells as a potential treatment method for selected neurodegenerative diseases: review. Cell Mol. Neurobiol. 2023;43(6):2643–2673.; Xie C., Liu Y.Q., Guan Y.T., Zhang G.X. Induced stem cells as a novel multiple sclerosis therapy. Curr. Stem Cell Res. Ther. 2016;11(4):313–320.; Yun W., Choi K.A., Hwang I., et al. OCT4-induced oligodendrocyte progenitor cells promote remyelination and ameliorate disease. NPJ Regen. Med. 2022;7(1):4.; Wang Y., Chang K., Liu C., Na W., Jiang Z., Xiong J. Clemastine promotes oligodendrocyte precursor cell differentiation and myelination after acute radiation injury. J. Radiat. Res. Radiat. Proces. 2023;39(5):48–55.; Caverzasi E., Papinutto N., Cordano C., Kirkish G., Gundel T.J., Zhu A., Akula A.V., Boscardin W.J., Neeb H., Henry R.G., Chan J.R., Green A.J. MWF of the corpus callosum is a robust measure of remyelination: Results from the ReBUILD trial. Proc. Nat. Acad. Sci. U.S.A. 2023;120(20):e2217635120.; Hansen C.S., Hasseldam H., Bacher I.H., Thamsborg S.M., Johansen F.F., Kringel H. Trichuris suis secrete products that reduce disease severity in a multiple sclerosis model. Acta Parasitol. 2017;62(1):22–28.; Fleming J., Hernandez G., Hartman L., Maksimovic J., Nace S., Lawler B., Risa T., Cook T., Agni R., Reichelderfer M., Luzzio C., Rolak L., Field A., Fabry Z. Safety and efficacy of helminth treatment in relapsing-remitting multiple sclerosis: results of the HINT 2 clinical trial. Mult. Scler. J. 2019;25(1):81–91.; Yordanova I.A., Ebner F., Schulz A.R., Steinfelder S., Rosche B., Bolze A., Paul F., Mei H.E., Hartmann S. The worm-specific immune response in multiple sclerosis patients receiving controlled Trichuris suis ova immunotherapy. Life (Basel). 2021;11(2):101.; Libbey J.E., Cusick M.F., Fujinami R.S. Role of pathogens in multiple sclerosis. Int. Rev. Immunol. 2014;33(4):266–283.; Tanasescu R., Tench C.R., Constantinescu C.S., Telford G., Singh S., Frakich N., Onion D., Auer D.P., Gran B., Evangelou N., Falah Y., Ranshaw C., Cantacessi C., Jenkins T.P., Pritchard D.I. Hookworm treatment for relapsing multiple sclerosis: a randomized double-blinded placebo-controlled trial. JAMA Neurol. 2020;77(9):1089–1098.; Jenkins T.P., Pritchard D.I., Tanasescu R., Telford G., Papaiakovou M., Scotti R., Cortés A., Constantinescu C.S., Cantacessi C. Experimental infection with the hookworm, Necator americanus, is associated with stable gut microbial diversity in human volunteers with relapsing multiple sclerosis. BMC Biol. 2021;19(1):74.; Wegener Parfrey L., Jirků M., Šíma R., Jalovecka M., Sak B., Grigore K., Jirků Pomajbíková K. A benign helminth alters the host immune system and the gut microbiota in a rat model system. PLoS One. 2017;12(8):e0182205.; Calvani N.E.D., De Marco Verissimo C., Jewhurst H.L., Cwiklinski K., Flaus A., Dalton J.P. Two distinct superoxidase dismutases (SOD) secreted by the helminth parasite Fasciola hepatica play roles in defence against metabolic and host immune cell-derived reactive oxygen species (ROS) during growth and development. Antioxidants. 2022;11(10):1968.; Otero L., Bonilla M., Protasio A.V., Fernández C., Gladyshev V.N., Salinas G. Thioredoxin and glutathione systems differ in parasitic and free-living platyhelminths. BMC Genomics. 2010;11:237.; Xiang C., Zhong G., Wang H. IL-9 plays a critical role in helminth-induced protection against COVID-19- related cytokine storms. mBio. 2024;15(7):e0122924.; Cao Z., Wang J., Liu X., Liu Y., Li F., Liu M., Chiu S., Jin X. Helminth alleviates COVID-19-related cytokine storm in an IL-9-dependent way. mBio. 2024;15(6):e00905-24.; Solaro C., Ponzio M., Moran E., Tanganelli P., Pizio R., Ribizzi G., Venturi S., Mancardi G.L., Battaglia M.A. The changing face of multiple sclerosis: Prevalence and incidence in an aging population. Mult. Scler. 2015;21(10):1244–1250.; Marrie R.A., Cohen J., Stuve O., Trojano M., Sørensen P.S., Reingold S., Cutter G., Reider N. A systematic review of the incidence and prevalence of comorbidity in multiple sclerosis: overview. Mult. Scler. 2015;21(3):263–281.; Noseworthy J., Paty D., Wonnacott T., Feasby T., Ebers G. Multiple sclerosis after age 50. Neurology 1983;33(12):1537–1537.; Minden S.L., Frankel D., Hadden L.S., Srinath K.P., Perloff J.N. Disability in elderly people with multiple sclerosis: An analysis of baseline data from the Sonya Slifka Longitudinal Multiple Sclerosis Study. NeuroRehabilitation. 2004;19(1):55–67.; Zinganell A., Göbel G., Berek K., Hofer B., Asenbaum-Nan S., Barang M., Böck K., Bsteh C., Bsteh G., Eger S., Eggers C., Fertl E., Joldic D., Khalil M., Langenscheidt D. et al. Multiple sclerosis in the elderly: a retrospective cohort study. J. Neurol. 2024;271(2):674–687.; Weideman A.M., Tapia-Maltos M.A., Johnson K., Greenwood M., Bielekova B. Meta-analysis of the age-dependent efficacy of multiple sclerosis treatments. Front. Neurol. 2017;8:577.; Bjornevik K., Cortese M., Healy, B.C., Kuhle J., Mina M.J., Leng Y., Elledge S.J., Niebuhr D.W., Scher A.I., Munger K.L., Ascherio A. Longitudinal analysis reveals high prevalence of Epstein-Barr virus associated with multiple sclerosis. Science. 2022;375(6578):296–301.; Matell H., Lycke J., Svenningsson A., Holmén C., Khademi M., Hillert J., Olsson T., Piehl F. Age-dependent effects on the treatment response of natalizumab in MS patients. Mult. Scler. 2015;21(1):48–56.; Gelibter S., Saraceno L., Pirro F., Susani E.L., Protti A. As time goes by: Treatment challenges in elderly people with multiple sclerosis. J. Neuroimmunol. 2024;391:578368.; Muñoz J.S., Santiago A.D., Escudero J.C., Merino J.A.G. Case report: Primary cytomegalovirus infection in a patient with late onset multiple sclerosis treated with dimethyl fumarate. Front. Neurol. 2024;15:1363876.; Oudrer N. Multiple sclerosis in elderly patients: When we can stopped treatment? Mult. Scler. Relat. Disord. 2023;80:105181.; Skulachev V.P., Anisimov V.N., Antonenko Y.N., et al. An attempt to prevent senescence: a mitochondrial approach. Biochim. Biophys. Acta (BBA)-Bioenergetics. 2009;1787(5):437–461.; Zielonka J., Joseph J., Sikora A., Hardy M., Ouari O., Vasquez-Vivar J., Cheng G., Lopez M., Kalyanaraman B. Mitochondria-targeted triphenylphosphonium-based compounds: syntheses, mechanisms of action, and therapeutic and diagnostic applications. Chem. Rev. 2017;117(15):10043–10120.; Lin M.M., Liu N., Qin Z.H., Wang Y. Mitochondrial-derived damage-associated molecular patterns amplify neuroinflammation in neurodegenerative diseases. Acta Pharmacol. Sin. 2022;43(10):2439–2447.; Sanabria-Castro A., Alape-Girón A., FloresDíaz M., Echeverri-McCandless A., Parajeles-Vindas A. Oxidative stress involvement in the molecular pathogenesis and progression of multiple sclerosis: a literature review. Rev. Neurosci. 2024;35(3):355–371.; Sutter P.A., McKenna M.G., Imitola J., Pijewski R.S., Crocker S.J. Therapeutic opportunities for targeting cellular senescence in progressive multiple sclerosis. Curr. Opin. Pharmacol. 2022;63:102184.; Ghosh A., Chandran K., Kalivendi S.V., Joseph J., Antholine W.E., Hillard C.J., Kanthasamy A.,Kanthasamy A., Kalyanaraman B. Neuroprotection by a mitochondria-targeted drug in a Parkinson’s Disease model. Free Radical Biol. Med. 2010;49:1674−1684.
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2Academic Journal
Authors: E. K. Fetisova, N. V. Vorobjeva, M. S. Muntyan, Е. К. Фетисова, Н. В. Воробьева, М. С. Мунтян
Contributors: This research was performed under the state assignment of Moscow State University, project number АААА-А19-119031390114-5.
Source: Vestnik Moskovskogo universiteta. Seriya 16. Biologiya; Том 79, № 2 (2024); 87-101 ; Вестник Московского университета. Серия 16. Биология; Том 79, № 2 (2024); 87-101 ; 0137-0952
Subject Terms: старение, oxidative stress, reactive oxygen species, mitochondria-targeted antioxidants, demyelination, oligodendrocytes, microglia, aging, окислительный стресс, активные формы кислорода, митохондриально-направленные антиоксиданты, демиелинизация, олигодендроциты, микроглия
File Description: application/pdf
Relation: https://vestnik-bio-msu.elpub.ru/jour/article/view/1367/668; Walton C., King R., Rechtman L., Kaye W., Leray E., Marrie R. A., Robertson N, La Rocca N., Uitdehaag B., van der Mei I., Wallin M., Helme A., Angood Napier C., Rijke N., Baneke P. Rising prevalence of multiple sclerosis worldwide: insights from the atlas of MS. Mult. Scler. J. 2020;26(14):1816–1821.; Dobson R., Giovannoni G. Multiple sclerosis – a review. Eur. J. Neurol. 2019;26(1):27–40.; Axthelm M.K., Bourdette D.N., Marracci G.H., Su W., Mullaney E.T., Manoharan M., Kohama S.G., Pollaro J., Witkowski E., Wang P., Rooney W.D., Sherman L.S., Wong S.W. Japanese macaque encephalomyelitis: a spontaneous multiple sclerosis-like disease in a nonhuman primate. Ann. Neurol. 2011;70(3):362–373.; Hedström A.K., Hössjer O., Katsoulis M., Kockum I., Olsson T., Alfredsson L. Organic solvents and MS susceptibility. Interaction with MS risk HLA genes. Neurology. 2018;91(5):e455–e462.; Баринский И.Ф., Гребенникова Т.В., Альховский С.В., Кочергин-Никитский К.С., Сергеев О.В., Грибенча С.В., Раев С.А. Молекулярно-генетическая характеристика вируса, выделенного от больных острым энцефаломиелитом человека и множественным склерозом. Вопросы вирусологии. 2015;60(4):14–18.; Buljevac D., Flach H.Z., Hop W.C., Hijdra D., Laman J.D., Savelkoul H.F., van Der Meche F.G., van Doorn P.A., Hintzen R.Q. Prospective study on the relationship between infections and multiple sclerosis exacerbations. Brain. 2002;125(Pt. 5):952–960.; Kriesel J.D., White A., Hayden F.G., Spruance S.L., Petajan J. Multiple sclerosis attacks are associated with picornavirus infections. Mult. Scler. 2004;10(2):145–148.; Cossu D., Yokoyama K., Hattori N. Bacteria-host interactions in multiple sclerosis. Front. Microbiol. 2018;9:2966.; Bjornevik K., Cortese M., Healy, B.C., Kuhle J., Mina M.J., Leng Y., Elledge S.J., Niebuhr D.W., Scher A.I., Munger K.L., Ascherio A. Longitudinal analysis reveals high prevalence of Epstein-Barr virus associated with multiple sclerosis. Science. 2022;375(6578):296–301.; Handel A.E., Handunnetthi L., Ebers G.C. Ramagopalan S.V. Type 1 diabetes mellitus and multiple sclerosis: common etiological features. Nat. Rev. Endocrinol. 2009;5(12):655–664.; Nielsen N.M., Westergaard T., Frisch M., Rostgaard K., Wohlfahrt J., Koch-Henriksen N., Melbye M., Hjalgrim H. Type 1 diabetes and multiple sclerosis: A Danish population-based cohort study. Arch. Neurol. 2006;63(7):1001–1004.; Bechtold S., Blaschek A., Raile K., Dost A., Freiberg C., Askenas M., Fröhlich-Reiterer E., Molz E., Holl R.W. Higher relative risk for multiple sclerosis in a pediatric and adolescent diabetic population: analysis from DPV database. Diabetes Care. 2014;37(1):96–101.; Magyari M., Sorensen P.S. Comorbidity in multiple sclerosis. Front. Neurol. 2020;11:851.; Лапштаева А.В., Абросимова Ю.Г., Еремкина Т.Я., Костина Ю.A. Микробные агенты как триггеры развития рассеянного склероза. Инфекция и иммунитет. 2021;11(6):1050–1056.; Conway S.E., Healy B.C., Zurawski J., Severson C., Kaplan T., Stazzone L., Galetta K., Chitnis T., Houtchens M.K. COVID-19 severity is associated with worsened neurological outcomes in multiple sclerosis and related disorders. Mult. Scler. Relat. Dis. 2022;63:103946.; Najjar S., Najjar A., Chong D.J., Pramanik B.K., Kirsch C., Kuzniecky R.I., Pacia S.V., Azhar S. Central nervous system complications associated with SARS-CoV-2 infection: integrative concepts of pathophysiology and case reports. J. Neuroinflamm. 2020;17(1):231.; Sormani M.P., Schiavetti I., Carmisciano L. et al. COVID-19 severity in multiple sclerosis: putting data into context. Neurol. Neuroimmunol. Neuroinflamm. 2021;9(1):e1105.; Michelena G., Casas M., Eizaguirre M.B., Pita M.C., Cohen L., Alonso R., Garcea O., Silva B.A. ¿ Can COVID-19 exacerbate multiple sclerosis symptoms? A case series analysis. Mult. Scler. Relat. Dis. 2022;57:103368.; Lima M., Aloizou A.M., Siokas V., Bakirtzis C., Liampas I., Tsouris Z., Bogdanos D.P., Baloyannis S.J. Dardiotis E. Coronaviruses and their relationship with multiple sclerosis: is the prevalence of multiple sclerosis going to increase after the Covid-19 pandemia? Rev. Neurosci. 2022;33(7):703–720.; Ximeno-Rodríguez I., Blanco-delRío I., Astigarraga E., Barreda-Gómez G. Acquired immune deficiency syndrome correlation with SARS-CoV-2 N genotypes. Biomed. J. 2023;100650. https://doi.org/10.1016/j.bj.2023.100650.; Bauer L., Laksono B.M., de Vrij F.M.S., Kushner S.A., Harschnitz O., van Riel D. The neuroinvasiveness, neurotropism, and neurovirulence of SARS-CoV-2. Trends Neurosci. 2022;45(5):358–368.; Stoiloudis P., Kesidou E., Bakirtzis C., Sintila S-A., Konstantinidou N., Boziki M., Grigoriadis N. The role of diet and interventions on multiple sclerosis: a review. Nutrients. 2022; 14(6):1150.; Tarlinton R.E., Khaibullin T., Granatov E., Martynova E., Rizvanov A., Khaiboullina S. The interaction between viral and environmental risk factors in the pathogenesis of multiple sclerosis. Int. J. Mol. Sci. 2019;20(2):303.; Fazia T., Baldrighi G.N., Nova A., Bernardinelli L. A systematic review of Mendelian randomization studies on multiple sclerosis. Eur. J. Neurosci., 2023;58(4):3172–3194.; Dhaiban S., Al-Ani M., Elemam N.M., AlAawad M.H., Al-Rawi Z., Maghazachi A.A. Role of peripheral immune cells in multiple sclerosis and experimental autoimmune encephalomyelitis. Science. 2021;3(1):12.; Theodosis-Nobelos P., Rekka E.A. Efforts towards repurposing of antioxidant drugs and active compounds for multiple sclerosis control. Neurochem. Res. 2023;48(3):725–744.; Nozari E., Ghavamzadeh S., Razazian N. The effect of vitamin B12 and folic acid supplementation on serum homocysteine, anemia status and quality of life of patients with multiple sclerosis. Clin. Nutr. Res. 2019;8(1):36–45.; Magyari M., Koch-Henriksen N. Quantitative effect of sex on disease activity and disability accumulation in multiple sclerosis. J. Neurol. Neurosurg. Psychiatry. 2022;93(7):716–722.; Salpietro V., Polizzi A., Recca G., Ruggieri M. The role of puberty and adolescence in the pathobiology of pediatric multiple sclerosis. Mult. Scler. Demyelinating Disord. 2018;3:2.; Ostolaza A., Corroza J., Ayuso T. Multiple sclerosis and aging): comorbidity and treatment challenges. Mult. Scler. Relat. Disord. 2021;50:102815.; Zhang Y., Atkinson J., Burd C.E., Graves J., Segal B.M. Biological aging in multiple sclerosis. Mult. Scler. 2023;29(14):1701–1708.; Lotti C.B.D.C., Oliveira A.S.B., Bichuetti D.B., Castro I.D., Oliveira E.M.L. Late onset multiple sclerosis: concerns in aging patients. Arq. Neuropsiquiatr. 2017;75(7):451–456.; Noseworthy J., Paty D., Wonnacott T., Feasby T., Ebers G. Multiple sclerosis after age 50. Neurology. 1983;33(12):1537–1537.; Zeydan B., Kantarci O.H. Impact of age on multiple sclerosis disease activity and progression. Curr. Neurol. Neurosci. Rep. 2020;20(7):24.; Marrie R.A., Cohen J., Stuve O., Trojano M., Sørensen P.S., Reingold S., Cutter G., Reider N. A systematic review of the incidence and prevalence of comorbidity in multiple sclerosis: overview. Mult. Scler. 2015;21(3):263–281.; Branco M., Ruano L., Portaccio E., Goretti B., Niccolai C., Patti F., Chisari C., Gallo P., Grossi P., Ghezzi A., Roscio M., Mattioli F., Bellomi F., Simone M., Gemma R., Amato M.P. Aging with multiple sclerosis: prevalence and profile of cognitive impairment. Neurol. Sci. 2019;40(8):1651–1657.; Jakimovski D., Weinstock-Guttman B., Roy S., Jaworski III M., Hancock L., Nizinski A., Srinivasan P., Fuchs T.A., Szigeti K., Zivadinov R., Benedict R.H. Cognitive profiles of aging in multiple sclerosis. Front. Aging Neurosci. 2019;11:105.; Boyko A., Melnikov M. Prevalence and incidence of multiple sclerosis in Russian Federation: 30 years of studies. Brain Sci. 2020;10(5):305.; Fetisova E., Chernyak B., Korshunova G., Muntyan M., Skulachev V. Mitochondria-targeted antioxidants as a prospective therapeutic strategy for multiple sclerosis. Curr. Med. Chem. 2017;24(19):2086–2114.; Морозов С.П., Владзимирский А.В., Черняева Г.Н., Бажин А.В., Пимкин А.А., Беляев М.Г., Кляшторный В.Г., Горшкова Т.Н., Курочкина Н.С., Якушева С.Ф. Валидация диагностической точности алгоритма «искусственного интеллекта» для выявления рассеянного склероза в условиях городской поликлиники. Лучевая диагностика и терапия. 2020;11(2):58–65.; Kiselev I., Bashinskaya V., Baulina N., Kozin M., Popova E., Boyko A., Favorova O., Kulakova O. Genetic differences between primary progressive and relapsingremitting multiple sclerosis: the impact of immune-related genes variability. Mult. Scler. Relat. Dis. 2019;29:130–136.; Kiselev I.S., Kulakova O.G., Baulina N.M., Bashinskaya V.V., Popova E.V., Boyko A.N., Favorova O.O. Variability of the MIR196A2 gene as a risk factor in primary-progressive multiple sclerosis development. Mol. Biol. 2019;53(2):249–255.; International Multiple Sclerosis Genetics Consortium. A systems biology approach uncovers cell-specific gene regulatory effects of genetic associations in multiple sclerosis. Nat. Commun. 2019;10:2236.; Patsopoulos N.A. Genetics of multiple sclerosis: an overview and new directions. Cold Spring Harb. Perspect. Med. 2018;8(7):a028951.; Ransohoff R.M., Hafler D.A., Lucchinetti C.F. Multiple sclerosis – a quiet revolution. Nat. Rev. Neurol. 2015;11(3):134–142.; Pytel V., Matías-Guiu J.A., Torre-Fuentes L., Montero P., Gómez-Graña Á., García-Ramos R., Moreno-Ramos T., Oreja-Guevara C., Fernández-Arquero M., Gómez-Pinedo U., Matías-Guiu J. Familial multiple sclerosis and association with other autoimmune diseases. Brain Behav. 2017;8(1):e00899.; Lublin F.D., Reingold S.C., Cohen J.A., Cutter G.R., Sørensen P.S., Thompson A.J., Wolinsky J.S., Balcer L.J., Banwell B., Barkhof F., Bebo B. Defining the clinical course of multiple sclerosis: the 2013 revisions. Neurology. 2014;83(3):278–286.; Govindhan E., Pavithra J., Yuvaraj K., Muralidharan P. A comprehensive review on multiple sclerosis: it’s etiology, symptoms, epidemiology and current therapeutic approaches. Int. J. Sci. Res. Arch. 2023;8(2):462–474.; Hendriks J.J., Teunissen C.E., de Vries H.E., Dijkstra C.D. Macrophages and neurodegeneration. Brain Res. Rev. 2005;48(2):185–195.; Zheng C., Chen J., Chu F., Zhu J., Jin T. Inflammatory role of TLR-MyD88 signaling in multiple sclerosis. Front. Mol. Neurosci. 2020;12:314.; Van Horssen J., Witte M.E., Schreibelt G., de Vries H.E. Radical changes in multiple sclerosis pathogenesis. BBA-Mol. Basis Dis. 2011;1812(2):141–150.; Friese M.A., Schattling B., Fugger L. Mechanisms of neurodegeneration and axonal dysfunction in multiple sclerosis. Nat. Rev. Neurol. 2014;10(4):225–238.; Scalfari A., Neuhaus A., Daumer M., Muraro P.A., Ebers G.C. Onset of secondary progressive phase and longterm evolution of multiple sclerosis. J. Neurol. Neurosurg. Psychiatry. 2014;85(1):67–75.; Goodin D.S. The epidemiology of multiple sclerosis: insights to a causal cascade. Handbook of clinical neurology. Eds. M.J. Aminoff, F. Boller, and D.F. Swaab. Elsevier; 2016;138:173–206.; Dong Y., Yong V.W. When encephalitogenic T cells collaborate with microglia in multiple sclerosis. Nat. Rev. Neurol. 2019;15(12):704–717.; Guerrero B.L., Sicotte N.L. Microglia in multiple sclerosis: friend or foe? Front. Immunol. 2020;11:374.; Inoue M., Shinohara M.L. NLRP3 Inflammasome and MS/EAE. Autoimmune Dis. 2013;2013:859145.; Shao S., Chen C., Shi G., Zhou Y., Wei Y., Fan N., Yang Y., Wu L., Zhang T. Therapeutic potential of the target on NLRP3 inflammasome in multiple sclerosis. Pharmacol. Therapeut. 2021;227:107880.; Bulua A.C., Simon A., Maddipati R., Pelletier M., Park H., Kim K.Y., Sack M.N., Kastner D.L., Siegel R.M. Mitochondrial reactive oxygen species promote production of proinflammatory cytokines and are elevated in TNFR1- associated periodic syndrome (TRAPS). J. Exp. Med. 2011;208(3):519–533.; Gris D., Ye Z., Iocca H.A., Wen H., Craven R.R., Gris P., Huang M., Schneider M., Miller S.D., Ting J.P. NLRP3 plays a critical role in the development of experimental autoimmune encephalomyelitis by mediating Th1 and Th17 responses. J. Immunol. 2010;185(2):974–981.; Abais J.M., Xia M., Zhang Y., Boini K.M., Li P.L. Redox regulation of NLRP3 inflammasomes: ROS as trigger or effector? Antioxid. Redox Sign. 2015;22(13):1111–1129.; Chen Y., Ye X., Escames G., Lei W., Zhang X., Li M., Jing T., Yao Y., Qiu Z., Wang Z., Acuña-Castroviejo D., Yang Y. The NLRP3 inflammasome: contributions to inflammation-related diseases. Cell Mol. Biol. Lett. 2023;28(1):51.; Wolburg H., Neuhaus J., Kniesel U., Krauß B., Schmid E.M., Ocalan M., Farrell C., Risau W. Modulation of tight junction structure in blood-brain barrier endothelial cells. Effects of tissue culture, second messengers and cocultured astrocytes. J. Cell Sci. 1994;107(5):1347–1357.; Owens T., Bechmann I., Engelhardt B. Perivascular spaces and the two steps to neuroinflammation. J. Neuropath. Exp. Neur. 2008;67(12):1113–1121.; Ortiz G.G., Pacheco-Moisés F.P., Macías-Islas M.Á., Flores-Alvarado L.J., Mireles-Ramírez M.A., González-Renovato E.D., Hernández-Navarro V.E., Sánchez-López A.L., Alatorre-Jiménez M.A. Role of the blood-brain barrier in multiple sclerosis. Arch. Med. Res. 2014;45(8):687–697.; Zinovkin R.A., Romaschenko V.P., Galkin I.I., Zakharova V.V., Pletjushkina O.Y., Chernyak B.V., Popova E.N. Role of mitochondrial reactive oxygen species in age-related inflammatory activation of endothelium. Aging (Albany N.Y.). 2014;6(8):661.; Zakharova V.V., Pletjushkina O.Y., Galkin I.I., Zinovkin R.A., Chernyak B.V., Krysko D.V., Skulachev V.P., Popova E.N. Low concentration of uncouplers of oxidative phosphorylation decreases the TNF-induced endothelial permeability and lethality in mice. BBA-Mol. Basis Dis. 2017;1863(4):968–977.; Sanabria-Castro A., Alape-Girón A., FloresDíaz M., Echeverri-McCandless A., Parajeles-Vindas A. Oxidative stress involvement in the molecular pathogenesis and progression of multiple sclerosis: a literature review. Rev. Neurosci. 2024;35(3):355–371.; Calkins M.J., Johnson D.A., Townsend J.A., Vargas M.R., Dowell J.A., Williamson T.P., Kraft A.D., Lee J.M., Li J., Johnson J.A. The Nrf2/ARE pathway as a potential therapeutic target in neurodegenerative disease. Antioxid. Redox Sign. 2009;11(3):497–508.; Kharel P., McDonough J., Basu S. Evidence of extensive RNA oxidation in normal appearing cortex of multiple sclerosis brain. Neurochem. Int. 2016;92:43–48.; Tully M., Shi R. New insights in the pathogenesis of multiple sclerosis – role of acrolein in neuronal and myelin damage. Int. J. Mol. Sci. 2013;14(10):20037–20047.; Zhang J., Sturla S., Lacroix C., Schwab C. Gut microbial glycerol metabolism as an endogenous acrolein source. mBio. 2018;9(1):e01947-17.; Nonneman A., Robberecht W., Van Den Bosch L.V. The role of oligodendroglial dysfunction in amyotrophic lateral sclerosis. Neurodegen. Dis. Manag. 2014;4(3):223–239.; van Horssen J., Schreibelt G., Drexhage J., Hazes T., Dijkstra C.D., van der Valk P., de Vries H.E. Severe oxidative damage in multiple sclerosis lesions coincides with enhanced antioxidant enzyme expression. Free Radical. Biol. Med. 2008;45(12):1729–1737.; Spaas J., van Veggel L., Schepers M., Tiane A., van Horssen J., Wilson D.M. 3rd, Moya P.R., Piccart E., Hellings N., Eijnde B.O., Derave W., Schreiber R., Vanmierlo T. Oxidative stress and impaired oligodendrocyte precursor cell differentiation in neurological disorders. Cell Mol. Life Sci. 2021;78(10):4615–4637.; Witte M.E., Geurts J.J., de Vries H.E., van der Valk P., van Horssen J. Mitochondrial dysfunction: a potential link between neuroinflammation and neurodegeneration? Mitochondrion. 2010;10(5):411–418.; Padureanu R., Albu C.V., Mititelu R.R., Bacanoiu M.V., Docea A.O., Calina D., Padureanu V., Olaru G., Sandu R.E., Malin R.D., Buga A.M. Oxidative stress and inflammation interdependence in multiple sclerosis. J. Clin. Med. 2019;8(11):1815.; Michaličková D., Šíma M., Slanař O. New insights in the mechanisms of impaired redox signaling and its interplay with inflammation and immunity in multiple sclerosis. Physiol. Res. 2020;69(1):1–19.; Ragupathy H., Vukku M., Barodia S.K. Cell-typespecific mitochondrial quality control in the brain: a plausible mechanism of neurodegeneration. Int. J. Mol. Sci. 2023;24(19):14421.; Petersen R.C., Thomas R.G., Grundman M., Bennett D., Doody R., Ferris S., Galasko D., Jin S., Kaye J., Levey A., Pfeiffer E., Sano M., van Dyck C.H., Thal L.J., Alzheimer’s Disease Cooperative Study Group. Vitamin E and donepezil for the treatment of mild cognitive impairment. N. Engl. J. Med. 2005;352(23):2379–2388.; Kamat C.D., Gadal S., Mhatre M., Williamson K.S., Pye Q.N., Hensley K. Antioxidants in central nervous system diseases: preclinical promise and translational challenges. J. Alzheimers Dis. 2008;15(3):473–493.; Bjelakovic G., Nikolova D., Gluud L.L., Simonetti R.G., Gluud C. Antioxidant supplements for prevention of mortality in healthy participants and patients with various diseases. Cochrane Database Syst. Rev. 2012;2012(3):CD007176.; Antonenko Y.N., Avetisyan A.V., Bakeeva L.E., et al. Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 1. Cationic plastoquinone derivatives: synthesis and in vitro studies. Biochemistry (Mosc.). 2008;73(12):1273–1287.; Fetisova E.K., Muntyan M.S., Lyamzaev K.G., Chernyak B.V. Therapeutic effect of the mitochondriatargeted antioxidant SkQ1 on the culture model of multiple sclerosis. Oxid. Med. Cell. Longev. 2019;2019:2082561.; Fock E.M., Parnova R.G. Protective effect of mitochondria-targeted antioxidants against inflammatory response to lipopolysaccharide challenge: a review. Pharmaceutics. 2021;13(2):144.; Vorobjeva N.V., Chernyak B.V. NETosis: molecular mechanisms, role in physiology and pathology. Biochemistry (Mosc.). 2020;85(10):1178–1190.