SkQ1 improves immune status and normalises the activity of antioxidant and nadph-generating enzymes in adjuvant-induced rheumatoid arthritis in rats
- Authors: Kryl'skii E.D1, Popova T.N1, Zhaglin D.A1, Razuvaev G.A1, Oleynik S.A1
-
Affiliations:
- Voronezh State University
- Issue: Vol 88, No 8 (2023)
- Pages: 1337-1351
- Section: Articles
- URL: https://journals.rcsi.science/0320-9725/article/view/141473
- DOI: https://doi.org/10.31857/S0320972523080043
- EDN: https://elibrary.ru/IIJABG
- ID: 141473
Cite item
Abstract
About the authors
E. D Kryl'skii
Voronezh State University
Email: evgenij.krylsky@yandex.ru
394018 Voronezh, Russia
T. N Popova
Voronezh State University394018 Voronezh, Russia
D. A Zhaglin
Voronezh State University394018 Voronezh, Russia
G. A Razuvaev
Voronezh State University394018 Voronezh, Russia
S. A Oleynik
Voronezh State University394018 Voronezh, Russia
References
- Radu, A. F., and Bungau, S. G. (2021) Management of rheumatoid arthritis: an overview, Cells, 10, 2857, doi: 10.3390/cells10112857.
- Da Fonseca, L. J. S., Nunes-Souza, V., Goulart, M. O. F., and Rabelo, L. A. (2019) Oxidative stress in rheumatoid arthritis: what the future might hold regarding novel biomarkers and add-on therapies, Oxid. Med. Cell. Longev., 2019, 7536805, doi: 10.1155/2019/7536805.
- Phull, A. R., Nasir, B., Ul Haq, I., and Kim, S. J. (2018) Oxidative stress, consequences and ROS mediated cellular signaling in rheumatoid arthritis, Chem. Biol. Interact., 281, 121-136, doi: 10.1016/j.cbi.2017.12.024.
- Ferreira, H. B., Melo, T., Paiva, A., and Domingues, M. R. (2021) Insights in the role of lipids, oxidative stress and inflammation in rheumatoid arthritis unveiled by new trends in lipidomic investigations, Antioxidants, 10, 45, doi: 10.3390/antiox10010045.
- Mititelu, R. R., Pădureanu, R., Băcănoiu, M., Pădureanu, V., Docea, A. O., Calina, D., Barbulescu, A. L., and Buga, A. M. (2020) Inflammatory and oxidative stress markers - mirror tools in rheumatoid arthritis, Biomedicines, 8, 125, doi: 10.3390/biomedicines8050125.
- Del Buono, M., Abbate, A., and Toldo, S. (2018) Interplay of inflammation, oxidative stress and cardiovascular disease in rheumatoid arthritis, Heart, 104, 1991-1992, doi: 10.1136/heartjnl-2018-313313.
- Radovanović-Dinić, B., Tešić-Rajković, S., Zivkovic, V., and Grgov, S. (2018) Clinical connection between rheumatoid arthritis and liver damage, Rheumatol. Int., 38, 715-724, doi: 10.1007/s00296-018-4021-5.
- Steinz, M. M., Santos-Alves, E., and Lanner, J. T. (2020) Skeletal muscle redox signaling in rheumatoid arthritis, Clin. Sci., 134, 2835-2850, doi: 10.1042/CS20190728.
- Lee, S. H., Chang, D. K., Goel, A., Boland, C. R., Bugbee, W., Boyle, D. L., Firestein, G. S. (2003) Microsatellite instability and suppressed DNA repair enzyme expression in rheumatoid arthritis, J. Immunol., 170, 2214-2220, doi: 10.4049/jimmunol.170.4.2214.
- Biniecka, M., Fox, E., Gao, W., Ng, C. T., Veale, D. J., Fearon, U., and O'Sullivan, J. (2011) Hypoxia induces mitochondrial mutagenesis and dysfunction in inflammatory arthritis, Arthritis Rheum., 63, 2172-2182, doi: 10.1002/art.30395.
- Harty, L. C., Biniecka, M., O'Sullivan, J., Fox, E., Mulhall, K., Veale, D. J., and Fearon, U. (2012) Mitochondrial mutagenesis correlates with the local inflammatory environment in arthritis, Ann. Rheum. Dis., 71, 582-588, doi: 10.1136/annrheumdis-2011-200245.
- Kan, S., Duan, M., Liu, Y., Wang, C., and Xie, J. (2014) Role of mitochondria in physiology of chondrocytes and diseases of osteoarthritis and rheumatoid arthritis, Cartilage, 13, 1102S-1121S, doi: 10.1177/19476035211063858.
- Oğul, Y., Gür, F., Cengiz, M., Gür, B., Sarı, R. A., and Kızıltunç, A. (2021) Evaluation of oxidant and intracellular anti-oxidant activity in rheumatoid arthritis patients: in vivo and in silico studies, Int. Immunopharmacol., 97, 107654, doi: 10.1016/j.intimp.2021.107654.
- Mateen, S., Moin, S., Khan, A. Q., Zafar, A., Fatima, N., and Shahzad, S. (2017) Role of hydrotherapy in the amelioration of oxidant-antioxidant status in rheumatoid arthritis patients, Int. J. Rheum. Dis., 21, 1822-1830, doi: 10.1111/1756-185X.13118.
- Behl, T., Upadhyay, T., Singh, S., Chigurupati, S., Alsubayiel, A. M., Mani, V., Vargas-De-La-Cruz, C., Uivarosan, D., Bustea, C., Sava, C., Stoicescu, M., Radu, A. F., Bungau, S. G. (2021) Polyphenols targeting MAPK mediated oxidative stress and inflammation in rheumatoid arthritis, Molecules, 26, 6570, doi: 10.3390/molecules26216570.
- Fan, X. X., Xu, M. Z., Leung, E. L. H., Jun, C., Yuan, Z., and Liu, L. (2020) ROS-responsive berberine polymeric micelles effectively suppressed the inflammation of rheumatoid arthritis by targeting mitochondria, Nano Micro Lett., 12, 76, doi: 10.1007/s40820-020-0410-x.
- D'Amico, D., Olmer, M., Fouassier, A. M., Valdés, P., Andreux, P. A., Rinsch, C., and Lotz, M. (2022) Urolithin A improves mitochondrial health, reduces cartilage degeneration, and alleviates pain in osteoarthritis, Aging Cell, 21, e13662, doi: 10.1111/acel.13662.
- Сенокосова Е. А., Крутицкий С. С., Груздева О. В., Антонова Л. В., Скулачев М. В., Григорьев Е. В. (2022) Исследование антиоксидантного эффекта митохондриально-направленного антиоксиданта SkQ1 на модели изолированного сердца крысы, Общая реаниматология, 18, 36-44, doi: 10.15360/1813-9779-2022-4-36-44.
- Skulachev, V. P., Anisimov, V. N., Antonenko, Y. N., Bakeeva, L. E., Chernyak, B. V., Erichev, V. P., Filenko, O. F., Kalinina, N. I., Kapelko, V. I., Kolosova, N. G., Kopnin, B. P., Korshunova, G. A., Lichinitser, M. R., Obukhova, L. A., Pasyukova, E. G., Pisarenko, O. I., Roginsky, V. A., Ruuge, E. K., Senin, I. I., Severina, I. I., Skulachev, M. V., Spivak, I. M., Tashlitsky, V. N., Tkachuk, V. A., Vyssokikh, M. Y., Yaguzhinsky, L. S., and Zorov, D. B. (2009) An attempt to prevent senescence: a mitochondrial approach, Biochim. Biophys. Acta, 1787, 437-461, doi: 10.1016/j.bbabio.2008.12.008.
- Wei, Y., Troger, A., Spahiu, V., Perekhvatova, N., Skulachev, M., Petrov, A., Chernyak, B., and Asbell, P. (2019) The role of SKQ1 (visomitin) in inflammation and wound healing of the ocular surface, Ophthalmol. Ther., 8, 63-73, doi: 10.1007/s40123-018-0158-2.
- Andreev-Andrievskiy, A. A., Kolosova, N. G., Stefanova, N. A., Lovat, M. V., Egorov, M. V., Manskikh, V. N., Zinovkin, R. A., Galkin, I. I., Prikhodko, A. S., Skulachev, M. V., and Lukashev, A. N. (2016) Efficacy of mitochondrial antioxidant plastoquinonyl-decyl-triphenylphosphonium bromide (SkQ1) in the rat model of autoimmune arthritis, Oxid. Med. Cell. Longev., 2016, 8703645, doi: 10.1155/2016/8703645.
- Taurog, J. D., Argentieri, D. C., McReynolds, R. A. (1988) Adjuvant arthritis, Methods Enzymol., 162, 339-355, doi: 10.1016/0076-6879(88)62089-1.
- Луговская С. А., Морозова В. Т., Почтарь М. Е., Долгов В. В. (2014) Лабораторная гематология, Триада, Тверь.
- Piskarev, I. M., Trofimova, S. V., Ivanova, I. P., and Burkhina, O. E. (2015) Investigation of the level of free-radical processes in substrates and biological samples using induced chemiluminescence, Biophysics, 60, 400-408, doi: 10.1134/S0006350915030148.
- Recknagel, R. O., and Ghoshal, A. K. (1966) Lipoperoxidation of rat liver microsomal lipids induced by carbon tetrachloride, Nature, 210, 1162-1163, doi: 10.1038/2101162a0.
- Nishikimi, M., Rao, N. A., and Yagi, K. (1972) The occurrence of superoxide anion in the reaction of reduced phenazine methosulphate and molecular oxygen, Biochem. Biophys. Res. Commun., 46, 849-864, doi: 10.1016/s0006-291x(72)80218-3.
- Góth, L. (1991) A simple method for determination of serum catalase activity and revision of reference range, Clin. Chim. Acta, 196, 143-151, doi: 10.1016/0009-8981(91)90067-m.
- Paglia, D. E., and Valentine, W. N. (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase, Lab. Clin. Med., 70, 158-169.
- Zanetti, G. (1979) Rabbit liver glutathione reductase. Purification and properties, Arch. Biochem. Biophys., 198, 241-246, doi: 10.1016/0003-9861(79)90415-6.
- Warholm, M., Guthenberg, C., Von Bahr, C., and Mannervik, B. (1985) Glutathione transferases from human liver, Method Enzymol., 113, 499-504, doi: 10.1016/s0076-6879(85)13065-x.
- Ellman, G. L. (1959) Tissue sulfhydryl groups, Arch Biochem Biophys., 82, 70-77, doi: 10.1016/0003-9861(59)90090-6.
- Афанасьев В. Г., Зайцев В. С., Вольфсон Т. И. (1973) К микрометоду определения лимонной кислоты в сыворотке крови с помощью фотоэлектроколориметра, Лаб. дело, 4, 115-116.
- López-Armada, M. J., Fernández-Rodríguez, J. A., and Blanco, F. J. (2022) Mitochondrial dysfunction and oxidative stress in rheumatoid arthritis, Antioxidants, 11, 1151, doi: 10.3390/antiox11061151.
- Liu, R. Z., Zhang, S., Zhang, W., Zhao, X. Y., and Du, G. H. (2023) Baicalein attenuates brain iron accumulation through protecting aconitase 1 from oxidative stress in rotenone-induced Parkinson's disease in rats, Antioxidants, 12, 12, doi: 10.3390/antiox12010012.
- Bashir, N., Ahmad, S. B., Rehman, M. U., Muzamil, S., Bhat, R. R., Mir, M. U. R., Shazly, G. A., Ibrahim, M. A., Elossaily, G. M., Sherif, A. Y., and Kazi, M. (2021) Zingerone (4-(four-hydroxy-3-methylphenyl) butane-two-1) modulates adjuvant-induced rheumatoid arthritis by regulating inflammatory cytokines and antioxidants, Redox Rep., 26, 62-70, doi: 10.1080/13510002.2021.1907518.
- Lu, S., Liu, T., Li, H., and Fan, H. (2019) Fangchinoline supplementation attenuates inflammatory markers in experimental rheumatoid arthritis-induced rats, Biomed. Pharmacother., 111, 142-150, doi: 10.1016/j.biopha.2018.12.043.
- Dai, W., Qi, C., and Wang, S. (2018) Synergistic effect of glucosamine and vitamin E against experimental rheumatoid arthritis in neonatal rats, Biomed. Pharmacother., 105, 835-840, doi: 10.1016/j.biopha.2018.05.136.
- Arablou, T., Aryaeian, N., Djalali, M., Shahram, F., and Rasouli, L. (2019) Association between dietary intake of some antioxidant micronutrients with some inflammatory and antioxidant markers in active rheumatoid arthritis patients, Int. J. Vitamin Nutr. Res., 89, 238-245, doi: 10.1024/0300-9831/a000255.
- Demyanenko, I. A., Popova, E. N., Zakharova, V. V., Ilyinskaya, O. P., Vasilieva, T. V., Romashchenko, V. P., Fedorov, A. V., Manskikh, V. N., Skulachev, M. V., Zinovkin, R. A., Pletjushkina, O. Y., Skulachev, V. P., and Chernyak, B. V. (2015) Mitochondria-targeted antioxidant SkQ1 improves impaired dermal wound healing in old mice, Aging (Albany NY), 7, 475-485, doi: 10.18632/aging.100772.
- Demyanenko, I. A., Zakharova, V. V., Ilyinskaya, O. P., Vasilieva, T. V., Fedorov, A. V., Manskikh, V. N., Zinovkin, R. A., Pletjushkina, O. Y., Chernyak, B. V., Skulachev, V. P., and Popova, E. N. (2017) Mitochondria-targeted antioxidant SkQ1 improves dermal wound healing in genetically diabetic mice, Oxid. Med. Cell. Longev., 2017, 6408278, doi: 10.1155/2017/6408278.
- Riveiro-Naveira, R. R., Valcárcel-Ares, M. N., Almonte-Becerril, M., Vaamonde-García, C., Loureiro, J., Hermida-Carballo, L., López-Peláez, E., Blanco, F. J., López-Armada, M. J. (2016) Resveratrol lowers synovial hyperplasia, inflammatory markers and oxidative damage in an acute antigen-induced arthritis model, Rheumatology, 55, 1889-1900, doi: 10.1093/rheumatology/kew255.
- Kryl'skii, E. D., Popova, T. N., and Kirilova, E. M. (2015) Activity of glutathione antioxidant system and NADPH-generating enzymes in rats with experimental rheumatoid arthritis, Bull. Exp. Biol. Med., 160, 24-27, doi: 10.1007/s10517-015-3089-0.
- Крыльский Е. Д., Попова Т. Н., Кирилова Е. М., Сафонова О. А. (2016) Воздействие липоевой кислоты на активность каспаз, показатели иммунного и антиоксидантного статуса при ревматоидном артрите у крыс, Биоорг. химия, 42, 431-439, doi: 10.7868/S0132342316040138.
- Ponist, S., Zloh, M., and Bauerova, K. (2019) in Animal Models in Medicine and Biology (Tvrdá, E., and Yenisetti, S. C., eds), IntechOpen, London, pp. 195-216.
- Cai, W. W., Yu, Y., Zong, S. Y., and Wei, F. (2020) Metabolic reprogramming as a key regulator in the pathogenesis of rheumatoid arthritis, Inflamm. Res., 69, 1087-1101, doi: 10.1007/s00011-020-01391-5.
- Benna, J. E., Hayem, G., Dang, P. M. C., Fay, M., Chollet-Martin, S., Elbim, C., Meyer, O., and Gougerot-Pocidalo, M. A. (2002) NADPH oxidase priming and p47phox phosphorylation in neutrophils from synovial fluid of patients with rheumatoid arthritis and spondylarthropathy, Inflammation, 26, 273-278, doi: 10.1023/a:1021460517468.
- Shi, Q., Abusarah, J., Baroudi, G., Fernandes, J. C., Fahmi, H., and Benderdour, M. (2012) Ramipril attenuates lipid peroxidation and cardiac fibrosis in an experimental model of rheumatoid arthritis, Arthritis Res. Ther., 14, R223, doi: 10.1186/ar4062.
- Nadeem, A., Al-Harbi, N. O., Ahmad, S. F., Ibrahim, K. E., Siddiqui, N., and Al-Harbi, M. M. (2018) Glucose-6-phosphate dehydrogenase inhibition attenuates acute lung injury through reduction in NADPH oxidase-derived reactive oxygen species, Clin. Exp. Immunol., 191, 279-287, doi: 10.1111/cei.13097.
- Martínez-Navarro, F. J., Martínez-Morcillo, F. J., López-Muñoz, A., Pardo-Sánchez, I., Martínez-Menchón, T., Corbalán-Vélez, R., Cayuela, M. L., Pérez-Oliva, A. B., García-Moreno, D., and Mulero, V. (2020) The vitamin B6-regulated enzymes PYGL and G6PD fuel NADPH oxidases to promote skin inflammation, Dev. Comp. Immunol., 108, 103666, doi: 10.1016/j.dci.2020.103666.