https://doi.org/10.3390/ijms25168710 ·
Journal: International Journal of Molecular Sciences, 2024, №16, p.8710
Publisher: MDPI AG
Authors:
- Katarína Pružinská
- Martin Chrastina
- Sasan Khademnematolahi
- Veronika Vyletelová
- Lívia Gajdošová
- Lucia Pastvová
- František Dráfi
- Silvester Poništ
- Ľudmila Pašková
- Jarmila Kucharská
- Zuzana Sumbalová
- Jana Muchová
- Silvia Martiniaková
- Katarína Bauerová
Abstract
This in vivo study performed in rat adjuvant arthritis aims to advance the understanding of astaxanthin’s therapeutic properties for the possible treatment of rheumatoid arthritis (RA) in monotherapy and along with the standard RA treatment, methotrexate (MTX), in combination therapy. The main goal was to elucidate astaxanthin’s full therapeutic potential, evaluate its dose dependency, and compare its effects in monotherapy with other carotenoids such as β-carotene and β-cryptoxanthin (KXAN). Moreover, potential differences in therapeutic activity caused by using different sources of astaxanthin, synthetic (ASYN) versus isolated from Blakeslea trispora (ASTAP), were evaluated using one-way ANOVA (Tukey-Kramer post hoc test). KXAN was the most effective in reducing plasma MMP-9 levels in monotherapy, significantly better than MTX, and in reducing hind paw swelling. The differences in the action of ASTAP and ASYN have been observed across various biometric, anti-inflammatory, and antioxidative parameters. In combined therapy with MTX, the ASYN + MTX combination proved to be better. These findings, especially the significant anti-arthritic effect of KXAN and ASYN + MTX, could be the basis for further preclinical studies.
List of references
- Yaqoob, Mechanistic role of astaxanthin derived from shrimp against certain metabolic disorders, Food Sci. Nutr., № 10, с. 12
https://doi.org/10.1002/fsn3.2623 - Landry, Quantitation of carotenoids and fatty acids from Atlantic salmon using a portable Raman device, Analyst, № 147, с. 4379
https://doi.org/10.1039/D2AN01140A - Ambati, Astaxanthin: Sources, extraction, stability, biological activities and its commercial applications—A review, Mar. Drugs, № 12, с. 128
https://doi.org/10.3390/md12010128 - Goycoolea, Astaxanthin: A review of its chemistry and applications, Crit. Rev. Food Sci. Nutr., № 46, с. 185
https://doi.org/10.1080/10408690590957188 - Gupta, Biosynthesis and extraction of high-value carotenoid from algae, Front. Biosci., № 26, с. 171
https://doi.org/10.52586/4932 - Pereira, Antioxidant and anti-inflammatory mechanisms of action of astaxanthin in cardiovascular diseases (Review), Int. J. Mol. Med., № 47, с. 37
https://doi.org/10.3892/ijmm.2020.4783 - Kanwugu, O.N., and Glukhareva, T.V. (2023). Activation of Nrf2 pathway as a protective mechanism against oxidative stress-induced diseases: Potential of astaxanthin. Arch. Biochem. Biophys., 741.
https://doi.org/10.1016/j.abb.2023.109601 - Kohandel, Z., Farkhondeh, T., Aschner, M., Pourbagher-Shahri, A.M., and Samarghandian, S. (2022). Anti-inflammatory action of astaxanthin and its use in the treatment of various diseases. Biomed. Pharmacother., 145.
https://doi.org/10.1016/j.biopha.2021.112179 - Nishida, Y., Berg, P.C., Shakersain, B., Hecht, K., Takikawa, A., Tao, R., Kakuta, Y., Uragami, C., Hashimoto, H., and Misawa, N. (2023). Astaxanthin: Past, Present, and Future. Mar. Drugs, 21.
https://doi.org/10.3390/md21100514 - Devasagayam, Carotenoids, tocopherols and thiols as biological singlet molecular oxygen quenchers, Biochem. Soc. Trans., № 18, с. 1054
https://doi.org/10.1042/bst0181054 - Visioli, Astaxanthin in cardiovascular health and disease: Mechanisms of action, therapeutic merits, and knowledge gaps, Food Funct., № 8, с. 39
https://doi.org/10.1039/C6FO01721E - Lakey-Beitia, J., Kumar, D.J., Hegde, M.L., and Rao, K.S. (2019). Carotenoids as Novel Therapeutic Molecules Against Neurodegenerative Disorders: Chemistry and Molecular Docking Analysis. Int. J. Mol. Sci., 20.
https://doi.org/10.3390/ijms20225553 - Medoro, A., Davinelli, S., Milella, L., Willcox, B.J., Allsopp, R.C., Scapagnini, G., and Willcox, D.C. (2023). Dietary Astaxanthin: A Promising Antioxidant and Anti-Inflammatory Agent for Brain Aging and Adult Neurogenesis. Mar. Drugs, 21.
https://doi.org/10.3390/md21120643 - Masoudi, Anti-inflammatory and antioxidant effects of astaxanthin following spinal cord injury in a rat animal model, Brain Res. Bull., № 177, с. 324
https://doi.org/10.1016/j.brainresbull.2021.10.014 - Bjørklund, G., Gasmi, A., Lenchyk, L., Shanaida, M., Zafar, S., Mujawdiya, P.K., Lysiuk, R., Antonyak, H., Noor, S., and Akram, M. (2022). The Role of Astaxanthin as a Nutraceutical in Health and Age-Related Conditions. Molecules, 27.
https://doi.org/10.3390/molecules27217167 - Giannaccare, G., Pellegrini, M., Senni, C., Bernabei, F., Scorcia, V., and Cicero, A.F.G. (2020). Clinical Applications of Astaxanthin in the Treatment of Ocular Diseases: Emerging Insights. Mar. Drugs, 18.
https://doi.org/10.3390/md18050239 - Fu, Astaxanthin inhibiting oxidative stress damage of placental trophoblast cells in vitro, Syst. Biol. Reprod. Med., № 67, с. 79
https://doi.org/10.1080/19396368.2020.1824031 - Ohgami, Effects of astaxanthin on lipopolysaccharide-induced inflammation in vitro and in vivo, Investig. Ophthalmol. Vis. Sci., № 44, с. 2694
https://doi.org/10.1167/iovs.02-0822 - Gaki, Oxidative stress-induced signaling pathways implicated in the pathogenesis of Parkinson’s disease, Neuromolecular Med., № 16, с. 217
https://doi.org/10.1007/s12017-014-8294-x - Kurashige, Inhibition of oxidative injury of biological membranes by astaxanthin, Physiol. Chem. Phys. Med. NMR, № 22, с. 27
- Toronyi Ácsová, A., Hojerová, J., Hergesell, K., Hideg, E., Csepregi, K., Bauerová, K., Pružinská, K., and Martiniaková, S. (2022). Antioxidant and Anti-Pollution Effect of Naturally Occurring Carotenoids Astaxanthin and Crocin for Human Skin Protection. ChemistrySelect, 7.
https://doi.org/10.1002/slct.202201595 - Guerin, Haematococcus astaxanthin: Applications for human health and nutrition, Trends Biotechnol., № 21, с. 210
https://doi.org/10.1016/S0167-7799(03)00078-7 - Speranza, Astaxanthin treatment reduced oxidative induced pro-inflammatory cytokines secretion in U937: SHP-1 as a novel biological target, Mar. Drugs, № 10, с. 890
https://doi.org/10.3390/md10040890 - Rao, Evaluation of hepatoprotective and antioxidant activity of astaxanthin and astaxanthin esters from microalga-Haematococcus pluvialis, J. Food Biosci. Technol., № 52, с. 6703
https://doi.org/10.1007/s13197-015-1775-6 - Augusti, Astaxanthin prevents changes in the activities of thioredoxin reductase and paraoxonase in hypercholesterolemic rabbits, J. Clin. Biochem. Nutr., № 51, с. 42
https://doi.org/10.3164/jcbn.11-74 - Kamath, Ulcer preventive and antioxidative properties of astaxanthin from Haematococcus pluvialis, Eur. J. Pharmacol., № 590, с. 387
https://doi.org/10.1016/j.ejphar.2008.06.042 - Kochi, T., Shimizu, M., Sumi, T., Kubota, M., Shirakami, Y., Tanaka, T., and Moriwaki, H. (2014). Inhibitory effects of astaxanthin on azoxymethane-induced colonic preneoplastic lesions in C57/BL/KsJ-db/db mice. BMC Gastroenterol., 14.
https://doi.org/10.1186/s12876-014-0212-z - Ni, Y., Nagashimada, M., Zhuge, F., Zhan, L., Nagata, N., Tsutsui, A., Nakanuma, Y., Kaneko, S., and Ota, T. (2015). Astaxanthin prevents and reverses diet-induced insulin resistance and steatohepatitis in mice: A comparison with vitamin E. Sci. Rep., 5.
https://doi.org/10.1038/srep17192 - Bai, beta-Carotene inhibits inflammatory gene expression in lipopolysaccharide-stimulated macrophages by suppressing redox-based NF-kappaB activation, Exp. Mol. Med., № 37, с. 323
https://doi.org/10.1038/emm.2005.42 - Park, Amelioration of the Development of Osteoarthritis by Daily Intake of β-Cryptoxanthin, Biol. Pharm. Bull., № 40, с. 1116
https://doi.org/10.1248/bpb.b17-00161 - Webb, Animal models of human disease: Inflammation, Biochem. Pharmacol., № 87, с. 121
https://doi.org/10.1016/j.bcp.2013.06.014 - Kong, The use of animal models in rheumatoid arthritis research, J. Yeungnam Med. Sci., № 40, с. 23
https://doi.org/10.12701/jyms.2022.00773 - Kaklamanis, Experimental animal models resembling rheumatoid arthritis, Clin. Rheumatol., № 11, с. 41
https://doi.org/10.1007/BF02207082 - Drafi, F., Bauerova, K., Chrastina, M., Taghdisiesfejír, M., Rocha, J., Direito, R., Figueira, M.E., Sepodes, B., and Ponist, S. (2023). Rhodiola rosea L. Extract, a Known Adaptogen, Evaluated in Experimental Arthritis. Molecules, 28.
https://doi.org/10.3390/molecules28135053 - Chrastina, M., Dráfi, F., Pružinská, K., Poništ, S., Kamga, K.S., Khademnematolahi, S., Bilka, F., Novák, P., Pašková, Ľ., and Bauerová, K. (2023). Crocus sativus L. Extract (Saffron) Effectively Reduces Arthritic and Inflammatory Parameters in Monotherapy and in Combination with Methotrexate in Adjuvant Arthritis. Nutrients, 15.
https://doi.org/10.3390/nu15194108 - The effects of β-glucan isolated from Pleurotus ostreatus on methotrexate treatment in rats with adjuvant arthritis, Rheumatol. Int., № 31, с. 507
https://doi.org/10.1007/s00296-009-1258-z - Bauerova, Markers of inflammation and oxidative stress studied in adjuvant-induced arthritis in the rat on systemic and local level affected by pinosylvin and methotrexate and their combination, Autoimmunity, № 48, с. 46
https://doi.org/10.3109/08916934.2014.939268 - Choudhary, Experimental animal models for rheumatoid arthritis, Immunopharmacol. Immunotoxicol., № 40, с. 193
https://doi.org/10.1080/08923973.2018.1434793 - Meehan, Preclinical models of arthritis for studying immunotherapy and immune tolerance, Ann. Rheum. Dis., № 80, с. 1268
https://doi.org/10.1136/annrheumdis-2021-220043 - Hussein, Astaxanthin, a carotenoid with potential in human health and nutrition, J. Nat. Prod., № 69, с. 443
https://doi.org/10.1021/np050354+ - Farruggia, Astaxanthin exerts anti-inflammatory and antioxidant effects in macrophages in NRF2-dependent and independent manners, J. Nutr. Biochem., № 62, с. 202
https://doi.org/10.1016/j.jnutbio.2018.09.005 - Zarneshan, S.N., Fakhri, S., Farzaei, M.H., Khan, H., and Saso, L. (2020). Astaxanthin targets PI3K/Akt signaling pathway toward potential therapeutic applications. Food Chem. Toxicol., 145.
https://doi.org/10.1016/j.fct.2020.111714 - Brotosudarmo, T.H.P., Limantara, L., Setiyono, E. (2020). Structures of Astaxanthin and Their Consequences for Therapeutic Application. Int. J. Food Sci., 2020.
https://doi.org/10.1155/2020/2156582 - Guedes, Microalgae as sources of carotenoids, Mar. Drugs, № 9, с. 625
https://doi.org/10.3390/md9040625 - Shinde, Methotrexate: A gold standard for treatment of rheumatoid arthritis, J. Pain. Palliat. Care Pharmacother., № 28, с. 351
https://doi.org/10.3109/15360288.2014.959238 - García-González, C.M., and Baker, J. (2022). Treatment of early rheumatoid arthritis: Methotrexate and beyond. Curr. Opin. Pharmacol., 64.
https://doi.org/10.1016/j.coph.2022.102227 - Ponist, Reduction of oxidative stress in adjuvant arthritis. Comparison of efficacy of two pyridoindoles: Stobadine dipalmitate and SMe1.2HCl, Acta Biochim. Pol., № 57, с. 223
https://doi.org/10.18388/abp.2010_2398 - Zhu, Anti-arthritic activity of ferulic acid in complete Freund’s adjuvant (CFA)-induced arthritis in rats: JAK2 inhibition, Inflammopharmacology, № 28, с. 463
https://doi.org/10.1007/s10787-019-00642-0 - Hassan, Amelioration of adjuvant induced arthritis in Sprague Dawley rats through modulation of inflammatory mediators by Ribes alpestre Decne, J. Ethnopharmacol., № 235, с. 460
https://doi.org/10.1016/j.jep.2019.02.025 - Cui, Evaluation of antiarthritic activity of nimbolide against Freund’s adjuvant induced arthritis in rats, Artif. Cells Nanomed. Biotechnol., № 47, с. 3391
https://doi.org/10.1080/21691401.2019.1649269 - Res, Astaxanthin supplementation does not augment fat use or improve endurance performance, Med. Sci. Sports Exerc., № 45, с. 1158
https://doi.org/10.1249/MSS.0b013e31827fddc4 - Aoi, Astaxanthin improves muscle lipid metabolism in exercise via inhibitory effect of oxidative CPT I modification, Biochem. Biophys. Res. Commun., № 366, с. 892
https://doi.org/10.1016/j.bbrc.2007.12.019 - Radice, Effects of astaxanthin in animal models of obesity-associated diseases: A systematic review and meta-analysis, Free Radic. Biol. Med., № 171, с. 156
https://doi.org/10.1016/j.freeradbiomed.2021.05.008 - Jurcovicova, Methotrexate treatment ameliorated testicular suppression and anorexia related leptin reduction in rats with adjuvant arthritis, Rheumatol. Int., № 29, с. 1187
https://doi.org/10.1007/s00296-009-0838-2 - Zhang, L., Chen, H., Ding, K., He, S., Li, G., Qu, J., Qiao, Y., Zhang, L., Sui, X., and Fan, C. (2021). Astaxanthin intake alleviates gouty arthritis in patients and rats by modulating the levels of various inflammatory markers. J. Funct. Foods, 87.
https://doi.org/10.1016/j.jff.2021.104823 - Zhao, L., Tao, X., and Song, T. (2021). Astaxanthin alleviates neuropathic pain by inhibiting the MAPKs and NF-κB pathways. Eur. J. Pharmacol., 912.
https://doi.org/10.1016/j.ejphar.2021.174575 - Capelli, Synthetic astaxanthin is significantly inferior to algal-based astaxanthin as an antioxidant and may not be suitable as a human nutraceutical supplement, Nutrafoods, № 12, с. 145
https://doi.org/10.1007/s13749-013-0051-5 - Villaró, S., Ciardi, M., Morillas-España, A., Sanchez Zurano, A., Acién-Fernández, G., and Lafarga, T. (2021). Microalgae Derived Astaxanthin: Research and Consumer Trends and Industrial Use as Food. Foods, 10.
https://doi.org/10.3390/foods10102303 - Janega, Effect of methotrexate on inflammatory cells redistribution in experimental adjuvant arthritis, Rheumatol. Int., № 32, с. 3517
https://doi.org/10.1007/s00296-011-2177-3 - Ishizuka, Treatment with Anti-γ-Glutamyl Transpeptidase Antibody Attenuates Osteolysis in Collagen-Induced Arthritis Mice, J. Bone Miner. Res., № 22, с. 1933
https://doi.org/10.1359/jbmr.070726 - Ponist, Association between tissue gamma-glutamyl-transferase and clinical markers of adjuvant arthritis in Lewis rats, Neuro Endocrinol. Lett., № 27, с. 172
- Drafi, Pharmacological influence on processes of adjuvant arthritis: Effect of the combination of an antioxidant active substance with methotrexate, Interdiscip. Toxicol., № 5, с. 84
https://doi.org/10.2478/v10102-012-0015-4 - Ghlissi, Evaluation of efficacy of natural astaxanthin and vitamin E in prevention of colistin-induced nephrotoxicity in the rat model, Environ. Toxicol. Pharmacol., № 37, с. 960
https://doi.org/10.1016/j.etap.2014.03.004 - Gaffen, Recent advances in the IL-17 cytokine family, Curr. Opin. Immunol., № 23, с. 613
https://doi.org/10.1016/j.coi.2011.07.006 - Katz, Interleukin-17 enhances tumor necrosis factor alpha-induced synthesis of interleukins 1,6, and 8 in skin and synovial fibroblasts: A possible role as a “fine-tuning cytokine” in inflammation processes, Arthritis Rheumatol., № 44, с. 2176
https://doi.org/10.1002/1529-0131(200109)44:9<2176::AID-ART371>3.0.CO;2-4 - Vincenti, Using inhibitors of metalloproteinases to treat arthritis. Easier said than done?, Arthritis Rheumatol., № 37, с. 1115
https://doi.org/10.1002/art.1780370802 - Cunnane, Early joint erosions and serum levels of matrix metalloproteinase 1, matrix metalloproteinase 3, and tissue inhibitor of metalloproteinases 1 in rheumatoid arthritis, Arthritis Rheumatol., № 44, с. 2263
https://doi.org/10.1002/1529-0131(200110)44:10<2263::AID-ART389>3.0.CO;2-1 - Taghdisiesfejir, Treatment with coenzyme Q10, omega-3-polyunsaturated fatty acids and their combination improved bioenergetics and levels of coenzyme Q9 and Q10 in skeletal muscle mitochondria in experimental model of arthritis, Physiol. Res., № 70, с. 723
- Bauerova, Combined methotrexate and coenzyme Q₁₀ therapy in adjuvant-induced arthritis evaluated using parameters of inflammation and oxidative stress, Acta Biochim. Pol., № 57, с. 347
https://doi.org/10.18388/abp.2010_2415 - Gvozdjáková, A., Sumbalová, Z., Kucharská, J., Szamosová, M., Čápová, L., Rausová, Z., Vančová, O., Mojto, V., Langsjoen, P., and Palacka, P. (2021). Platelet mitochondrial respiration and coenzyme Q10 could be used as new diagnostic strategy for mitochondrial dysfunction in rheumatoid diseases. PLoS ONE, 16.
https://doi.org/10.1371/journal.pone.0256135 - Bozek, Regeneration of coenzyme Q9 redox state and inhibition of oxidative stress by Rooibos tea (Aspalathus linearis) administration in carbon tetrachloride liver damage, Physiol. Res., № 53, с. 515
- Chrastina, M., Poništ, S., Tóth, J., Czigle, S., Pašková, Ľ., Vyletelová, V., Švík, K., and Bauerová, K. (2022). Combination Therapy of Carnosic Acid and Methotrexate Effectively Suppressed the Inflammatory Markers and Oxidative Stress in Experimental Arthritis. Molecules, 27.
https://doi.org/10.3390/molecules27207115 - Niu, Astaxanthin Induces the Nrf2/HO-1 Antioxidant Pathway in Human Umbilical Vein Endothelial Cells by Generating Trace Amounts of ROS, J. Agric. Food Chem., № 66, с. 1551
https://doi.org/10.1021/acs.jafc.7b05493 - Saw, Astaxanthin and omega-3 fatty acids individually and in combination protect against oxidative stress via the Nrf2-ARE pathway, Food Chem. Toxicol., № 62, с. 869
https://doi.org/10.1016/j.fct.2013.10.023 - Pašková, Ľ., Kuncírová, V., Poništ, S., Mihálová, D., Nosáľ, R., Harmatha, J., Hrádková, I., Čavojský, T., Bilka, F., and Šišková, K. (2016). Effect of N-Feruloylserotonin and Methotrexate on Severity of Experimental Arthritis and on Messenger RNA Expression of Key Proinflammatory Markers in Liver. J. Immunol. Res., 2016.
https://doi.org/10.1155/2016/7509653 - Zhao, Z., Hua, Z., Luo, X., Li, Y., Yu, L., Li, M., Lu, C., Zhao, T., and Liu, Y. (2022). Application and pharmacological mechanism of methotrexate in rheumatoid arthritis. Biomed. Pharmacother., 150.
https://doi.org/10.1016/j.biopha.2022.113074 - Brody, Mechanism of action of methotrexate: Experimental evidence that methotrexate blocks the binding of interleukin 1 beta to the interleukin 1 receptor on target cells, Eur. J. Clin. Chem. Clin. Biochem., № 31, с. 667
- Howard, The expression and localization of plasma platelet-activating factor acetylhydrolase in endotoxemic rats, J. Biol. Chem., № 275, с. 19891
https://doi.org/10.1074/jbc.M001462200 - Memon, In vivo regulation of plasma platelet-activating factor acetylhydrolase during the acute phase response, Am. J. Physiol., № 277, с. R94
- Tselepis, Association of the inflammatory state in active juvenile rheumatoid arthritis with hypo-high-density lipoproteinemia and reduced lipoprotein-associated platelet-activating factor acetylhydrolase activity, Arthritis Rheum., № 42, с. 373
https://doi.org/10.1002/1529-0131(199902)42:2<373::AID-ANR21>3.0.CO;2-3 - Luczaj, W., Jarocka-Karpinska, I., Sierakowski, S., Andrisic, L., Zarkovic, N., and Skrzydlewska, E. (2014). Lipid peroxidation in Rheumatoid arthritis; consequences and monitoring. Free Radic. Biol. Med., 75.
https://doi.org/10.1016/j.freeradbiomed.2014.10.816 - Stafforini, Biology of platelet-activating factor acetylhydrolase (PAF-AH, lipoprotein associated phospholipase A2), Cardiovasc. Drugs Ther., № 23, с. 73
https://doi.org/10.1007/s10557-008-6133-8 - Södergren, A., Karp, K., Bengtsson, C., Möller, B., Rantapää-Dahlqvist, S., and Wållberg-Jonsson, S. (2015). Is Lipoprotein-Associated Phospholipase A2 a Link between Inflammation and Subclinical Atherosclerosis in Rheumatoid Arthritis?. Biomed. Res. Int., 2015.
https://doi.org/10.1155/2015/673018 - Raza, Beneficial effects and health benefits of Astaxanthin molecules on animal production: A review, Res. Vet. Sci., № 138, с. 69
https://doi.org/10.1016/j.rvsc.2021.05.023 - Kumar, Astaxanthin attenuates oxidative stress and inflammatory responses in complete Freund-adjuvant-induced arthritis in rats, Pharmacol. Rep., № 72, с. 104
https://doi.org/10.1007/s43440-019-00022-z - Mattei, Astaxanthin limits fish oil-related oxidative insult in the anterior forebrain of Wistar rats: Putative anxiolytic effects?, Pharmacol. Biochem. Behav., № 99, с. 349
https://doi.org/10.1016/j.pbb.2011.05.009 - Sangeetha, Retinol-deficient rats can convert a pharmacological dose of astaxanthin to retinol: Antioxidant potential of astaxanthin, lutein, and β-carotene, Can. J. Physiol. Pharmacol., № 88, с. 977
https://doi.org/10.1139/Y10-074 - Pashkow, Astaxanthin: A novel potential treatment for oxidative stress and inflammation in cardiovascular disease, Altern. Med. Rev., № 13, с. 247
- Fassett, Astaxanthin: A potential therapeutic agent in cardiovascular disease, Mar. Drugs, № 9, с. 447
https://doi.org/10.3390/md9030447 - Antioxidant activities of astaxanthin and related carotenoids, J. Agric. Food Chem., № 48, с. 1150
https://doi.org/10.1021/jf991106k - Sandhiya, Conformation-dependent antioxidant properties of β-carotene, Org. Biomol. Chem., № 20, с. 152
https://doi.org/10.1039/D1OB01723C - Gao, M., Dang, F., and Deng, C. (2019). β-Cryptoxanthin induced anti-proliferation and apoptosis by G0/G1 arrest and AMPK signal inactivation in gastric cancer. Eur. J. Pharmacol., 859.
https://doi.org/10.1016/j.ejphar.2019.172528 - Pružinská, K., Slovák, L., Dráfi, F., Poništ, S., Juránek, I., Chrastina, M., Švík, K., Strojný, L., Ambro, Ľ., and Bauerová, K. (2022). Enhanced Anti-Inflammatory Effect of the Combination of Lactiplantibacillus plantarum LS/07 with Methotrexate Compared to Their Monotherapies Studied in Experimental Arthritis. Molecules, 28.
https://doi.org/10.3390/molecules28010297 - Kuncirova, N-feruloylserotonin in preventive combination therapy with methotrexate reduced inflammation in adjuvant arthritis, Fundam. Clin. Pharmacol., № 28, с. 616
https://doi.org/10.1111/fcp.12085 - Imada, Anti-arthritic actions of β-cryptoxanthin against the degradation of articular cartilage in vivo and in vitro, Biochem. Biophys. Res. Commun., № 476, с. 352
https://doi.org/10.1016/j.bbrc.2016.05.126 - Pattison, Dietary beta-cryptoxanthin and inflammatory polyarthritis: Results from a population-based prospective study, Am. J. Clin. Nutr., № 82, с. 451
https://doi.org/10.1093/ajcn/82.2.451 - Cerhan, Antioxidant micronutrients and risk of rheumatoid arthritis in a cohort of older women, Am. J. Epidemiol., № 157, с. 345
https://doi.org/10.1093/aje/kwf205 - Tsiklauri, L., Švík, K., Chrastina, M., Poništ, S., Dráfi, F., Slovák, L., Alania, M., Kemertelidze, E., and Bauerova, K. (2021). Bioflavonoid robinin from Astragalus falcatus Lam. mildly improves the effect of methotrexate in rats with adjuvant arthritis. Nutrients, 13.
https://doi.org/10.3390/nu13041268 - Venkidasamy, B., Thiruvengadam, M., Thirupathi, P., and Subramanian, U. (2020). Inhibition of histone deacetylases is the major pathway mediated by astaxanthin to antagonize LPS-induced inflammatory responses in mammary epithelial cells. J. Biochem. Mol. Toxicol., 34.
https://doi.org/10.1002/jbt.22507 - Mohamed, N.M., Abdelhamid, A.M., Aref, M., Abdelhafeez, M., Faris Alotabi, H., Mohammed Abdelrahman, D.S., and Elwany, N.E. (2024). Role of cytokines and Th17/Tregs imbalance in the pathogenesis of otitis media with effusion. Modulation of Notch1/Hes1/mTORC1/S6k1 signalling pathway underlies the protective effect of astaxanthin. Int. Immunopharmacol., 128.
https://doi.org/10.1016/j.intimp.2024.111521 - Kishimoto, Astaxanthin suppresses scavenger receptor expression and matrix metalloproteinase activity in macrophages, Eur. J. Nutr., № 49, с. 119
https://doi.org/10.1007/s00394-009-0056-4 - Nagendraprabhu, Astaxanthin inhibits tumor invasion by decreasing extracellular matrix production and induces apoptosis in experimental rat colon carcinogenesis by modulating the expressions of ERK-2, NFkB and COX-2, Investig. New Drugs, № 29, с. 207
https://doi.org/10.1007/s10637-009-9342-5 - Uekawa, Rosuvastatin ameliorates early brain injury after subarachnoid hemorrhage via suppression of superoxide formation and nuclear factor-kappa B activation in rats, J. Stroke Cerebrovasc. Dis., № 23, с. 1429
https://doi.org/10.1016/j.jstrokecerebrovasdis.2013.12.004 - Zhang, Astaxanthin reduces matrix metalloproteinase-9 expression and activity in the brain after experimental subarachnoid hemorrhage in rats, Brain Res., № 22, с. 113
https://doi.org/10.1016/j.brainres.2015.07.020 - (2010, September 22). Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the Protection of Animals Used for Scientific Purposes (Official Journal L 276/33). Available online: https://eur-lex.europa.eu/eli/dir/2010/63/oj.
- European Medicines Agency (2017, February 24). Regulatory Acceptance of 3R (Replacement, Reduction, Refinement) Testing Approaches—Scientific Guideline, Available online: https://www.ema.europa.eu/en/regulatory-acceptance-3r-replacement-reduction-refinement-testing-approaches-scientific-guideline.
- Bevaart, Evaluation of therapeutic targets in animal models of arthritis: How does it relate to rheumatoid arthritis?, Arthritis Rheum., № 62, с. 2192
https://doi.org/10.1002/art.27503 - Thole, Cloning of the Mycobacterial Epitope Recognized by T Lymphocytes in Adjuvant Arthritis, Nature, № 331, с. 171
https://doi.org/10.1038/331171a0 - Bauerova, Utilization of adjuvant arthritis model for evaluation of new approaches in rheumatoid arthritis therapy focused on regulation of immune processes and oxidative stress, Interdiscip. Toxicol., № 4, с. 33
https://doi.org/10.2478/v10102-011-0007-9 - Ponist, S., Gardi, C., Paskova, L., Svik, K., Slovak, L., Bilka, F., Tedesco, I., Bauerova, K., and Russo, L.G. (2020). Modulation of methotrexate efficacy by green tea polyphenols in rat adjuvant arthritis. PharmaNutrition, 14.
https://doi.org/10.1016/j.phanu.2020.100228 - Bauerova, Chondroitin sulfate effect on induced arthritis in rats, Osteoarthr. Cartil., № 19, с. 1373
https://doi.org/10.1016/j.joca.2011.08.006 - Bauerova, Effect of nonanimal high- and low-molecular-mass chondroitin sulfates produced by a biotechnological process in an animal model of polyarthritis, Pharmacology, № 94, с. 109
https://doi.org/10.1159/000366285 - Orlowski, The gamma-glutamyl cycle: A possible transport system for amino acids, Proc. Natl. Acad. Sci. USA, № 67, с. 1248
https://doi.org/10.1073/pnas.67.3.1248 - Ondrejickova, Evaluation of ischemia-reperfusion injury by malondialdehyde, glutathione and gamma-glutamyl transpeptidase: Lack of specific local effects in diverse parts of the dog heart following acute coronary occlusion, Cardioscience, № 4, с. 225
- Mosca, Assay of coenzyme Q(10) in plasma by a single dilution step, Anal. Biochem., № 305, с. 49
https://doi.org/10.1006/abio.2002.5653 - Lang, Simultaneous determination of tocopherols, ubiquinols, and ubiquinones in blood, plasma, tissue homogenates, and subcellular fractions, Anal. Biochem., № 157, с. 106
https://doi.org/10.1016/0003-2697(86)90203-4 - Drabkin, Spectrophotometric studies I. Spectrophotometric constants for common hemoglobin derivatives in human, dog and rabbit blood, J. Biol. Chem., № 98, с. 719
https://doi.org/10.1016/S0021-9258(18)76122-X - Bergmeyer, H.U. (1983). Enzymes 1: Oxidoreductases, Transferases. Methods of Enzymatic Analysis, Chemie.
- Esterbauer, A spectrophotometric assay for lipid peroxides in serum lipoproteins using a commercially available reagent, J. Lipid Res., № 30, с. 627
https://doi.org/10.1016/S0022-2275(20)38354-1 - Re, Antioxidant activity applying an improved ABTS radical cation decolorization assay, Free Radic. Biol. Med., № 9–10, с. 1231
https://doi.org/10.1016/S0891-5849(98)00315-3 - Wooley, The usefulness and the limitations of animal models in identifying targets for therapy in arthritis, Best Pr. Res. Clin. Rheumatol., № 18, с. 47
https://doi.org/10.1016/j.berh.2003.09.007 - Asquith, Animal models of rheumatoid arthritis, Eur. J. Immunol., № 39, с. 2040
https://doi.org/10.1002/eji.200939578
About this publication
Publication type | Журнальна стаття |
Number of citations | 0 |
Number of works in the list of references | 122 |
Journal indexed in Scopus | Yes |
Journal indexed in Web of Science | Yes |