Correlation between Oxidative Stress with Cartilage Thickness and Catalase Activity in Osteoarthritis Model Rat after MSC-WJ Treatment
Abstract
Objective: This study was conducted to investigate the involvement of oxidative damage in rat model of osteoarthritis treated with Mesenchymal Stem Cell Wharton Jelly and to elucidate whether oxidative stress indicators correlate with cartilage damage and catalase activity.
Methods: This research is an experimental research with Posttest-Only Control Group Design. The sample consisted of 30 OA rat divided into 5 groups. Group I was the OA rat control group, group II was the OA rat group after 4 weeks, group III was the OA rat group after 8 weeks, group IV was the OA rat group after 4 weeks of treatment with MSC-WJ and group V is the OA rat group after 8 weeks treated with MSC-WJ. Malondialdehyde were measured by Ohkawa method, Cartilage Thickness were measured by using the Betaview program and catalase activity were measured by modification of Shinha.
Results: The results showed that the analysis of the Correlation between MDA with Cartilage Thickness (r= – 0.665) and CAT activity (r= – 0.666) in osteoarthritis Model Rat after Mesenchymal Stem Cell Wharton’s Jelly Treatment.
Conclusion: This study demonstrated a strong negative correlation between oxidative stress and knee cartilage thickness and catalase activity of MSC-WJ treated OA rats.
Keywords
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Xia B, Di C, Zhang J, Hu S, Jin H, Tong P, Osteoarthritis pathogenesis: a review of molecular mechanisms, Calcif. Tissue Int. 95 (2014) 495–505. DOI: 10.1007/s00223-014-9917-9
Sellam J, Berenbaum F. Clinical features of osteoarthritis. In:Firestein GS, Budd RC, Harris Jr ED, McInnes IB, Ruddy S,Sergent JS, Eds. Kelley’s Textbook of Rheumatology. Philadelphia: Elsevier Inc; 2008:1547-61
Licastro F, Candore G, Lio D, Porcellini E, Colonna-Romano G, Franceschi C, et al. Innate immunity and inflammation in ageing: a key for understanding age-related diseases. ImmunAgeing 2005 May 18;2(1):8. DOI: 10.1186/1742-4933-2-8
Loeser RF. Aging and osteoarthritis. Curr Opin Rheumatol 2011Sep;23(5):492-6. DOI: 10.1097/BOR.0b013e3283494005
Mobasheri A, Matta C, Zakany R, Musumeci G. Chondrosenescence: definition, hallmarks and potential role in the pathogenesis of osteoarthritis, Maturitas 80(2015) 237–244. DOI: 10.1016/j.maturitas.2014.12.003
Bates EJ, Lowther DA, Handley CJ. Oxygen free-radicals mediate an inhibition of proteoglycan synthesis in cultured articular cartilage. Ann Rheum Dis. 43 (1984)462–469. DOI: 10.1136/ard.43.3.462
Wu GJ, Chen TG, Chang HC, Chiu WT, Chang CC, Chen RM. Nitric oxide fromboth exogenous and endogenous sources activates mitochondria-dependentevents and induces insults to human chondrocytes. J Cell Biochem. 101 (2007)1520–1531. DOI: 10.1002/jcb.21268
Dawson J, Walters M. Uric acid and xanthine oxidase: future therapeutic targetsin the prevention of cardiovascular disease? Br J Clin Pharmacol. 62 (2006)633–644. DOI: 10.1111/j.1365-2125.2006.02785.x
Li D, Xie G, Wang W. Reactive oxygen species: the 2-edged sword of osteoarthritis. Am. J. Med. Sci. 344 (2012) 486–490. DOI: 10.1097/MAJ.0b013e3182579dc6
Henrotin Y, Kurz B, Aigner T. Oxygen and reactive oxygen species in cartilage degradation: friends or foes? Osteoarthr. Cartil. 13 (2005) 643–654. DOI: 10.1016/j.joca.2005.04.002
Henrotin Y, Deby-Dupont G, Deby C, De Bruyn M, Lamy M, Franchimont P. Production of active oxygen species by isolated human chondrocytes. Br. J. Rheumatol.32(1993) 562–567. DOI: 10.1093/rheumatology/32.7.562
Rathakrishnan C, Tiku K, Raghavan A, Tiku ML. Release of oxygen radicals byarticular chondrocytes: a study of luminol-dependent chemiluminescence and hydrogen peroxide secretion. J. Bone Miner. Res. 7 (1992) 1139–1148. DOI: 10.1002/jbmr.5650071005
Tiku ML, Liesch J.B, Robertson FM. Production of hydrogen peroxide by rabbit articular chondrocytes. Enhancement by cytokines. J. Immunol. 145 (1990)690–696.
Henrotin YE, Bruckner P, Pujol JP. The role of reactive oxygen species in homeostasis and degradation of cartilage, Osteoarthr. Cartil. 11 (2003) 747–755. DOI: 10.1016/s1063-4584(03)00150-x
Altay MA, Erturk C, Bilge A, Yapti M, Levent A, Aksoy N. Evaluation of prolidase activity and oxidative status in patients with knee osteoarthritis: relationships with radiographic severity and clinical parameters. Rheumatol. Int. (2015). DOI: 10.1007/s00296-015-3290-5
Erturk C, Altay MA, Selek S, Kocyigit A. Paraoxonase-1 activity and oxidativestatus in patients with knee osteoarthritis and their relationship with radiological and clinical parameters, Scand. J. Clin. Lab. Invest. 72 (2012) 433–439. DOI: 10.3109/00365513.2012.687116
Altindag O, Erel O, Aksoy N, Selek S, Celik H, Karaoglanoglu M. Increased oxidative stress and its relation with collagen metabolism in knee osteoarthritis. Rheumatol. Int. 27 (2007) 339–344. DOI: 10.1007/s00296-006-0247-8
Davies CM, Guilak F, Weinberg JB, Fermor B, Reactive nitrogen and oxygen species in interleukin-1-mediated DNA damage associated with osteoarthritis,Osteoarthr. Cartil. 16 (2008) 624–630. DOI: 10.1016/j.joca.2007.09.012
Karan A, Karan M.A, Vural P, Erten N, Tascioglu C, Aksoy C, Canbaz M, Oncel A. Synovial fluid nitric oxide levels in patients with knee osteoarthritis. Clin.Rheumatol. 22 (2003) 397–399. DOI: 10.1007/s10067-003-0761-y
Sakurai H, Kohsaka H, Liu MF, Higashiyama H, Hirata Y, Kanno K, Saito I, Miyasaka N. Nitric oxide production and inducible nitric oxide synthase expressionin inflammatory arthritides. J. Clin. Invest. 96 (1995) 2357–2363. DOI: 10.1172/jci118292
Ersoy Y, Ozerol E, Baysal O, Temel I, MacWalter RS, Meral U, Altay ZE. Serum nitrate and nitrite levels in patients with rheumatoid arthritis. ankylosing spondylitis, and osteoarthritis. Ann. Rheum. Dis. 61 (2002) 76–78. DOI: 10.1136/ard.61.1.76
Nemirovskiy OV, Radabaugh MR, Aggarwal P, Funckes-Shippy CL, Mnich SJ, Meyer DM, Sunyer T, Rodney Mathews W, Misko TP. Plasma 3-nitrotyrosine is a biomarker in animal models of arthritis: pharmacological dissection of iNOS'role in disease. Nitric Oxide 20 (2009) 150–156. DOI: 10.1016/j.niox.2008.12.005
Ostalowska A, Birkner E, Wiecha M, Kasperczyk S, Kasperczyk A, Kapolka D, Zon-Giebel A. Lipid peroxidation and antioxidant enzymes in synovialfluid ofpatients with primary and secondary osteoarthritis of the knee joint. Osteoarthr.Cartil. 14 (2006) 139–145. DOI: 10.1016/j.joca.2005.08.009
Carlo MD, Loeser RF. Increased oxidative stress with aging reduces chondrocyte survival: correlation with intracellular glutathione levels. Arthritis Rheum.48 (2003) 3419–3430. DOI: 10.1002/art.11338
Regan EA, Bowler RP, Crapo JD. Jointfluid antioxidants are decreased inosteoarthritic joints compared to joints with macroscopically intact cartilage andsubacute injury. Osteoarthr. Cartil. 16 (2008) 515–521. DOI: 10.1016/j.joca.2007.09.001
Fernandez-Moreno M, Soto-Hermida A, Pertega S, Oreiro N, Fernandez-Lopez C, Rego-Perez I, Blanco FJ. Mitochondrial DNA (mtDNA) haplogroups and serumlevels of anti-oxidant enzymes in patients with osteoarthritis. BMC Musculoskelet.Disord. 12 (2011) 264.
Soran N, Altindag O, Cakir H, Celik H, Demirkol A, Aksoy N. Assessment of paraoxonase activities in patients with knee osteoarthritis. Redox Rep. 13 (2008)194–19. DOI: 10.1179/135100008X308911
Tiku ML, Shah R, Allison GT. Evidence linking chondrocyte lipid peroxidation to cartilage matrix protein degradation. Possible role in cartilage aging and the pathogenesis of osteoarthritis. J. Biolumin. Chemilumin. 275 (2000) 20069–20076. DOI: 10.1074/jbc.M907604199
Surapaneni KM and Venkataramana G. Status of lipid peroxidation, glutathione, ascorbic acid, vitamin E and antioxidant enzymes in patients with osteoarthritis. Indian J. Med. Sci. 61 (2007) 9–14. DOI: 10.4103/0019-5359.29592
Shah R, Raska Jr K, Tiku ML. The presence of molecular markers of in vivo lipidperoxidation in osteoarthritic cartilage: a pathogenic role in osteoarthritis. ArthritisRheum. 52 (2005) 2799–2807. DOI: 10.1002/art.21239
Sen CK. Oxygen toxicity and antioxidants: state of the art. Indian J. Physiol.Pharmacol. 39 (1995) 177–196.
Sarban S, Kocyigit A, Yazar M, Isikan UE. Plasma total antioxidant capacity, lipidperoxidation, and erythrocyte antioxidant enzyme activities in patients with rheumatoid arthritis and osteoarthritis. Clin. Biochem. 38 (2005) 981–986. DOI: 10.1016/j.clinbiochem.2005.08.003
Suantawee T, Tantavisut S, Adisakwattana S, Tanavalee A, Yuktanandana P, Anomasiri W, Deepaisarnsakul B, Honsawek S. Oxidative stress, vitamin e, and anti-oxidant capacity in knee osteoarthritis. J. Clin. Diagn. Res. 7 (2013) 1855–1859. DOI: 10.7860/JCDR/2013/5802.3333
Morquette B, Shi Q, Lavigne P, Ranger P, Fernandes JC, Benderdour M. Production of lipid peroxidation products in osteoarthritic tissues: new evidence linking4-hydroxynonenal to cartilage degradation. Arthritis Rheum. 54 (2006) 271–281. DOI: 10.1002/art.21559
Stowe DF, Camara AK. Mitochondrial reactive oxygen species production in excitable cells: modulators of mitochondrial and cell function. Antioxid. Redox Signal.11 (2009) 1373–1414. DOI: 10.1089/ars.2008.2331
Khan IM, Gilbert SJ, Caterson B, Sandell LJ, Archer CW. Oxidative stress induces expression of osteoarthritis markers procollagen IIA and 3B3(−) in adult bovine articular cartilage. Osteoarthr. Cartil. 16 (2008) 698–707. DOI: 10.1016/j.joca.2007.10.004
Vincent F, Brun H, Clain E, Ronot X, Adolphe M. Effects of oxygen-free radicals on proliferation kinetics of cultured rabbit articular chondrocytes. J. Cell. Physiol. 141(1989) 262–266. DOI: 10.1002/jcp.1041410205
Dozin B, Malpeli M, Camardella L, Cancedda R, Pietranqelo A. Response of young, aged and osteoarthritic human articular chondrocytes to inflammatory cytokines: molecular and cellular aspects.Matrix Biol 2002;21:449-59. DOI: 10.1016/s0945-053x(02)00028-8
Janusz MJ, Hookfin EB, Heitmeyer SA, Woessner JF, Freemont AJ, Hoyland JA, Brown K. K, Hsieh LC, Almstead NG, De B, Natchus MG, Pikul S and Taiwo YO. Moderation of iodoacetate-induced experimental osteoarthritis in rats by matrix metalloproteinase inhibitors. J. OsteoArthritis Research Society Int. 2001;9 (8): 751–760. DOI: 10.1053/joca.2001.0472
Schuelert N, McDougall JJ. Grading of monosodium iodoacetate-induced osteoarthritis reveals a concentration-dependent sensitization of nociceptors in the knee joint of the rat. Neuroscience Letters. 2009;465: 184–188. DOI: 10.1016/j.neulet.2009.08.063
Javanmard MZ, Asgari D, Karimipour M, Atabaki F, Farjah G, and Niakani A. Mesenchymal Stem Cells Inhibit Proteoglycan Degeneration in a Rat Model of Osteoarthritis. Gene Cell Tisue. 2015; 2(4): e31011: 1-5. DOI : 10.17795/gct-31011.
Guzman RE, Evan MG, Bove S, Morenko B, and Kilgore K. Mono-Iodoacetate-Induced Histologic Changes in Subchondral Boneand Articular Cartilage of Rat Femorotibial Joints:An Animal Model of Osteoarthritis. Toxicologic Pathology. 2003; 31(6):619–624, 2003. DOI: 10.1080/01926230390241800
Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxidesin animal tissues by thiobarbituric acid reaction. Anal. Biochem 1979;95:351-8. DOI: 10.1016/0003-2697(79)90738-3
Sinha, A. K. (1972). Colorimetric assay of catalase. Analytical Biochemistry, 47(2), 389–394. doi:10.1016/0003-2697(72)90132-7.
Nemirovskiy OV, Radabaugh MR, Aggarwal P, Funckes-Shippy CL, Mnich SJ,. Meyer DM, Sunyer T, Mathews WR, Misko TP. Plasma 3-nitrotyrosine is a biomarker in animal models of arthritis: pharmacological dissection of iNOS'role in disease. Nitric Oxide 20 (2009) 150–156. DOI: 10.1016/j.niox.2008.12.005
Ostalowska A, Birkner E, Wiecha M, Kasperczyk S, Kasperczyk A, Kapolka D, and Zon-Giebel A. Lipid peroxidation and antioxidant enzymes in synovial fluid of patients with primary and secondary osteoarthritis of the knee joint. OsteoArthritis and Cartilage (2006) 14,139-145. DOI: 10.1016/j.joca.2005.08.009
Suantawee T, Tantavisut S, Adisakwattana S, Tanavalee A, Yuktanandana P, Anomasiri W, et al. Oxidative Stress, Vitamin E, and Antioxidant Capacity in Knee Osteoarthritis. Journl of Clinical and Diagnostic Research. 2013;7(9):1855-9. DOI: 10.7860/JCDR/2013/5802.3333
Grigolo B, Roseti L, Fiorini M, Facchini A. Enhanced lipid peroxidation in synoviocytes from patients with osteoarthritis. J Rheumatol 2003;30:345-7.
Hiran T.S, Moulton P.J, Hancock J.T. Detection of superoxide and NADPH oxidase in porcine articular chondrocytes. Free Radic. Biol. Med. 23 (1997) 736–743. DOI: 10.1016/s0891-5849(97)00054-3
Moulton PJ, Goldring MB, Hancock JT. NADPH oxidase of chondrocytes contains an isoform of the gp91phox subunit, Biochem. J. 329 (Pt 3) (1998) 449–451. DOI: 10.1042/bj3290449
van Lent PL, Nabbe KC, Blom AB, Sloetjes A, Holthuysen AE, Kolls J, Van DeLoo FA, Holland SM, Van Den Berg WB. NADPH-oxidase-driven oxygen radical production determines chondrocyte death and partly regulates metalloproteinase-mediated cartilage matrix degradation during interferon-gamma-stimulated immune complex arthritis. Arthritis Res. Ther. 7 (2005) R885–R895. DOI: 10.1186/ar1760
Baker MS, Feigan J, Lowther DA. The mechanism of chondrocyte hydrogen peroxide damage. Depletion of intracellular ATP due to suppression of glycolysis caused by oxidation of glyceraldehyde-3-phosphatedehydrogenase. J Rheumatol 1989;16:7–14.
Bates EJ, Johnson CC, Lowther DA. Inhibition of proteoglycan synthesis by hydrogen peroxide in cultured bovine articular cartilage. BiochimBiophys Acta 1985;838:221-8. DOI: 10.1016/0304-4165(85)90082-0
Asada S, Fukuda K, Nishisaka F, Matsukawa M, Hamanisi C. Hydrogen peroxide induces apoptosis of chondrocytes: involvement of calciumion and extracellular signal-regulated protein kinase. Inflamm Res2001;50:19-23. DOI: 10.1007/s000110050719
Tiku ML, Gupta S, Deshmukh DR. Aggrecan degradation in chondrocytes is mediated by reactive oxygen species and protected by antioxidants. Free Radic Res 1999;30:395-405. DOI: 10.1080/10715769900300431
Greenwald RA, Moy WW. Inhibition of collagen gelation by action of the super-oxide radical, Arthritis Rheum. 22 (1979) 251–259. DOI: 10.1002/art.1780220307
Stowe DF, Camara AK, Mitochondrial reactive oxygen species production in excitable cells: modulators of mitochondrial and cell function, Antioxid. Redox Signal.11 (2009) 1373–1414. DOI: 10.1089/ars.2008.2331
Monboisse JC, Braquet P, Randoux A, Borel JP, Non-enzymatic degradation of acid-soluble calf skin collagen by superoxide ion: protective effect of flavonoids,Biochem. Pharmacol. 32 (1983) 53–58.
Endrinaldi E, Darwin E, Zubir N, Revilla G. The Effect of Mesenchymal Stem Cell Wharton's Jelly on Matrix Metalloproteinase-1 and Interleukin-4 Levels in Osteoarthritis Rat Model. Open Access Macedonian Journal of Medical Sciences. 2019;7(4):529-535. DOI: 10.3889/oamjms.2019.152
Koga H, Muneta T, Nagase T et al. Comparison of mesenchymal tissues-derived stem cells for in vivo chondrogenesis: Suitable conditionsfor cell therapy of cartilage defects in rabbit. Cell Tissue Res 2008;333:207–215. DOI: 10.1007/s00441-008-0633-5
Redman S N, Oldfield S F, Archer C W. Current strategies for articular repair. Eur Cell Mater.2005 Apr 14;9:23-32. DOI: 10.22203/ecm.v009a04
Tanabe T, Otani H, Mishima K, Ogawa R, Inagaki C. Phorbol 12-myristate 13-acetate (PMA)-induced oxy-radical production in rheumatoid synovial cells. Jpn JPharmacol 1997;73:347-51.
Gutteridge JMC. Iron promoters of the Fenton reaction and lipid peroxidation can be released from haemoglobin by peroxides. FEBS Lett 1986;201:291-5. https://doi.org/10.1016/0014-5793(86)80626-3
Alpaslan C, Bilgihan A, Alpaslan GH, Guner B, Ozgur YM, Erbas D. Effect of arthrocentesis and sodium hyaluronate injection on nitrite, nitrate, and thiobarbituricacid-reactive substance levels in the synovial fluid.Oral Surg 2000;89:686-90. https://doi.org/10.1067/moe.2000.105518
Ivanova E, Ivanova B. Mechanisms of extracellular antioxidant defend. Exp Pathol 2000;4:49-59.
Valle-Prieto A, Conget PA. Human mesenchymal stem cells efficiently manage oxidative stress.Stem Cells Dev. 2010;19(12):1885-1893. DOI: 10.1089/scd.2010.0093
Gorbunov NV, Garrison BR, McDaniel DP, et al. Adaptive redox response of mesenchymal stromal cells to stimulation with lipopolysaccharide inflammagen: mechanisms of remodeling of tissue barriers in sepsis.Oxid Med Cell Longev. 2013;2013:1-16. DOI: 10.1155/2013/186795
Liu B, Ding F-X, Liu Y, et al. Human umbilical cord-derived mesenchymal stem cells conditioned medium attenuate interstitial fibrosis and stimulate the repair of tubular epithelial cells in an irreversible model of unilateral ureteral obstruction.Nephrol Ther. 2018;23(8):728-736. DOI: 10.1111/nep.13099
Ma Z, Song G, Zhao D, et al. Bone marrow-derived mesenchymal stromal cells ameliorate severe acute pancreatitis in rats viahemeoxygenase-1-mediated anti-oxidant and anti-inflammatoryeffects.Cytotherapy. 2019;21(2):162-174. DOI: 10.1016/j.jcyt.2018.11.013
Xie C, Jin J, Lv X, Tao J, Wang R, Miao D. Anti-aging effect of transplanted amniotic membrane mesenchymal stem cells in a pre-mature aging model of Bmi-1 deficiency.Sci Rep. 2015;5(1):13975. DOI: 10.1038/srep13975
Jung K-J, Lee KW, Park CH, et al. Mesenchymal stem cells decrease oxidative stress in the bowels of Interleukin-10 knockout mice.GutLiver. 2020;14(1):100-107. DOI: 10.5009/gnl18438
Calió ML, Marinho DS, Ko GM, et al. Transplantation of bone mar-row mesenchymal stem cells decreases oxidative stress, apoptosis,and hippocampal damage in brain of a spontaneous stroke model.Free Radic Biol Med. 2014;70:141-154. DOI: 10.1016/j.freeradbiomed.2014.01.024
Stavely R and Nurgali K. The emerging antioxidant paradigm of mesenchymal stem cell therapy. Stem Cells Transl Med.2020;9:985–1006.
