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Original Research

Resveratrol Exerts Anti-Osteoarthritic Effect by Inhibiting TLR4/NF-κB Signaling Pathway via the TLR4/Akt/FoxO1 Axis in IL-1β-Stimulated SW1353 Cells

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Pages 2079-2090 | Published online: 26 May 2020

References

  • WoolfAD, PflegerB. Burden of major musculoskeletal conditions. Bull World Health Organ. 2003;81(9):646–656.14710506
  • GoldringMB, OteroM. Inflammation in osteoarthritis. Curr Opin Rheumatol. 2011;23(5):471–478. doi:10.1097/BOR.0b013e328349c2b121788902
  • AbramsonSB, AtturM. Developments in the scientific understanding of osteoarthritis. Arthritis Res Ther. 2009;11(3):227. doi:10.1186/ar265519519925
  • RobinsonWH, LepusCM, WangQ, et al. Low-grade inflammation as a key mediator of the pathogenesis of osteoarthritis. Nat Rev Rheumatol. 2016;12(10):580–592. doi:10.1038/nrrheum.2016.13627539668
  • SohnDH, SokoloveJ, SharpeO, et al. Plasma proteins present in osteoarthritic synovial fluid can stimulate cytokine production via toll-like receptor 4. Arthritis Res Ther. 2012;14(1):R7.22225630
  • MassicotteF, LajeunesseD, BenderdourM, et al. Can altered production of interleukin-1beta, interleukin-6, transforming growth factor-beta and prostaglandin E(2) by isolated human subchondral osteoblasts identify two subgroups of osteoarthritic patients. Osteoarthritis Cartilage. 2002;10(6):491–500.12056853
  • WuTJ, LinCY, TsaiCH, HuangYL, TangCH. Glucose suppresses IL-1beta-induced MMP-1 expression through the FAK, MEK, ERK, and AP-1 signaling pathways. Environ Toxicol. 2018;33(10):1061–1068.30098273
  • WangQ, XuX, KangZ, ZhangZ, LiY. Paeonol prevents IL-1beta-induced inflammatory response and degradation of type II collagen in human primary chondrocytes. Artif Cells Nanomed Biotechnol. 2019;47(1):2139–2145.31146598
  • ScanzelloCR, PlaasA, CrowMK. Innate immune system activation in osteoarthritis: is osteoarthritis a chronic wound? Curr Opin Rheumatol. 2008;20(5):565–572.18698179
  • KimHA, ChoML, ChoiHY, et al. The catabolic pathway mediated by toll-like receptors in human osteoarthritic chondrocytes. Arthritis Rheum. 2006;54(7):2152–2163. doi:10.1002/art.2195116802353
  • LiuL, GuH, LiuH, et al. Protective effect of resveratrol against IL-1beta-induced inflammatory response on human osteoarthritic chondrocytes partly via the TLR4/MyD88/NF-kappaB signaling pathway: an “in vitro study”. Int J Mol Sci. 2014;15(4):6925–6940. doi:10.3390/ijms1504692524758933
  • JiangM, LiX, YuX, et al. Oral administration of resveratrol alleviates osteoarthritis pathology in C57BL/6J mice model induced by a high-fat diet. Mediators Inflamm. 2017;2017:7659023. doi:10.1155/2017/765902328250578
  • GaliliN, DavisRJ, FredericksWJ, et al. Fusion of a fork head domain gene to PAX3 in the solid tumour alveolar rhabdomyosarcoma. Nat Genet. 1993;5(3):230–235. doi:10.1038/ng1193-2308275086
  • FanW, MorinagaH, KimJJ, et al. FoxO1 regulates Tlr4 inflammatory pathway signalling in macrophages. EMBO J. 2010;29(24):4223–4236. doi:10.1038/emboj.2010.26821045807
  • GunterBR, ButlerKA, WallaceRL, SmithSM, HarirforooshS. Non-steroidal anti-inflammatory drug-induced cardiovascular adverse events: a meta-analysis. J Clin Pharm Ther. 2017;42(1):27–38. doi:10.1111/jcpt.1248428019014
  • AbrahamNS, El-SeragHB, HartmanC, RichardsonP, DeswalA. Cyclooxygenase-2 selectivity of non-steroidal anti-inflammatory drugs and the risk of myocardial infarction and cerebrovascular accident. Aliment Pharmacol Ther. 2007;25(8):913–924. doi:10.1111/j.1365-2036.2007.03292.x17402995
  • SoleasGJ, DiamandisEP, GoldbergDM. Resveratrol: a molecule whose time has come? And gone? Clin Biochem. 1997;30(2):91–113. doi:10.1016/S0009-9120(96)00155-59127691
  • SatoM, MaulikG, BagchiD, DasDK. Myocardial protection by protykin, a novel extract of trans-resveratrol and emodin. Free Radic Res. 2000;32(2):135–144. doi:10.1080/1071576000030014110653484
  • GambiniJ, InglesM, OlasoG, et al. Properties of resveratrol: in vitro and in vivo studies about metabolism, bioavailability, and biological effects in animal models and humans. Oxid Med Cell Longev. 2015;2015:837042. doi:10.1155/2015/83704226221416
  • EoSH, ChoH, KimSJ. Resveratrol inhibits nitric oxide-induced apoptosis via the NF-Kappa B pathway in rabbit articular chondrocytes. Biomol Ther. 2013;21(5):364–370. doi:10.4062/biomolther.2013.029
  • JinH, LiangQ, ChenT, WangX. Resveratrol protects chondrocytes from apoptosis via altering the ultrastructural and biomechanical properties: an AFM study. PLoS One. 2014;9(3):e91611. doi:10.1371/journal.pone.009161124632762
  • BuhrmannC, PopperB, AggarwalBB, ShakibaeiM. Resveratrol downregulates inflammatory pathway activated by lymphotoxin alpha (TNF-beta) in articular chondrocytes: comparison with TNF-alpha. PLoS One. 2017;12(11):e0186993. doi:10.1371/journal.pone.018699329095837
  • ImHJ, LiX, ChenD, et al. Biological effects of the plant-derived polyphenol resveratrol in human articular cartilage and chondrosarcoma cells. J Cell Physiol. 2012;227(10):3488–3497. doi:10.1002/jcp.2404922252971
  • CsakiC, MobasheriA, ShakibaeiM. Synergistic chondroprotective effects of curcumin and resveratrol in human articular chondrocytes: inhibition of IL-1beta-induced NF-kappaB-mediated inflammation and apoptosis. Arthritis Res Ther. 2009;11(6):R165. doi:10.1186/ar285019889203
  • OlivieroF, ScanuA, Zamudio-CuevasY, PunziL, SpinellaP. Anti-inflammatory effects of polyphenols in arthritis. J Sci Food Agric. 2018;98(5):1653–1659. doi:10.1002/jsfa.866428886220
  • GuH, LiK, LiX, et al. Oral resveratrol prevents osteoarthritis progression in C57BL/6J mice fed a high-fat diet. Nutrients. 2016;8(4):233. doi:10.3390/nu804023327104565
  • GuH, JiaoY, YuX, et al. Resveratrol inhibits the IL-1beta-induced expression of MMP-13 and IL-6 in human articular chondrocytes via TLR4/MyD88-dependent and -independent signaling cascades. Int J Mol Med. 2017;39(3):734–740. doi:10.3892/ijmm.2017.288528204817
  • XuX, LiuX, YangY, et al. Resveratrol inhibits the development of obesity-related osteoarthritis via the TLR4 and PI3K/Akt signaling pathways. Connect Tissue Res. 2019;60(6):571–582. doi:10.1080/03008207.2019.160118730922122
  • HongGU, LeeJY, KangH, et al. Inhibition of osteoarthritis-related molecules by isomucronulatol 7-O-beta-d-glucoside and ecliptasaponin A in IL-1beta-stimulated chondrosarcoma cell model. Molecules. 2018;23:11. doi:10.3390/molecules23112807
  • EstrovZ, ShishodiaS, FaderlS, et al. Resveratrol blocks interleukin-1beta-induced activation of the nuclear transcription factor NF-kappaB, inhibits proliferation, causes S-phase arrest, and induces apoptosis of acute myeloid leukemia cells. Blood. 2003;102(3):987–995. doi:10.1182/blood-2002-11-355012689943
  • BorrielloA, CucciollaV, Della RagioneF, GallettiP. Dietary polyphenols: focus on resveratrol, a promising agent in the prevention of cardiovascular diseases and control of glucose homeostasis. NMCD. 2010;20(8):618–625. doi:10.1016/j.numecd.2010.07.00420850033
  • WalleT, HsiehF, DeLeggeMH, OatisJE Jr., WalleUK. High absorption but very low bioavailability of oral resveratrol in humans. Drug Metab Dispos. 2004;32(12):1377–1382. doi:10.1124/dmd.104.00088515333514
  • YuC, ShinYG, ChowA, et al. Human, rat, and mouse metabolism of resveratrol. Pharm Res. 2002;19(12):1907–1914. doi:10.1023/A:102141412928012523673
  • DaveM, AtturM, PalmerG, et al. The antioxidant resveratrol protects against chondrocyte apoptosis via effects on mitochondrial polarization and ATP production. Arthritis Rheum. 2008;58(9):2786–2797. doi:10.1002/art.2379918759268
  • ShakibaeiM, CsakiC, NebrichS, MobasheriA. Resveratrol suppresses interleukin-1beta-induced inflammatory signaling and apoptosis in human articular chondrocytes: potential for use as a novel nutraceutical for the treatment of osteoarthritis. Biochem Pharmacol. 2008;76(11):1426–1439. doi:10.1016/j.bcp.2008.05.02918606398
  • WeiY, JiaJ, JinX, TongW, TianH. Resveratrol ameliorates inflammatory damage and protects against osteoarthritis in a rat model of osteoarthritis. Mol Med Rep. 2018;17(1):1493–1498. doi:10.3892/mmr.2017.803629138829
  • HanadaM, FengJ, HemmingsBA. Structure, regulation and function of PKB/AKT–a major therapeutic target. Biochim Biophys Acta. 2004;1697(1–2):3–16. doi:10.1016/j.bbapap.2003.11.00915023346
  • TarassishinL, SuhHS, LeeSC. Interferon regulatory factor 3 plays an anti-inflammatory role in microglia by activating the PI3K/Akt pathway. J Neuroinflammation. 2011;8:187. doi:10.1186/1742-2094-8-18722208359
  • ZhouLT, WangKJ, LiL, LiH, GengM. Pinocembrin inhibits lipopolysaccharide-induced inflammatory mediators production in BV2 microglial cells through suppression of PI3K/Akt/NF-kappaB pathway. Eur J Pharmacol. 2015;761:211–216. doi:10.1016/j.ejphar.2015.06.00326049009
  • AhmadSF, AnsariMA, NadeemA, et al. Resveratrol attenuates pro-inflammatory cytokines and activation of JAK1-STAT3 in BTBR T + Itpr3 tf /J autistic mice. Eur J Pharmacol. 2018;829:70–78. doi:10.1016/j.ejphar.2018.04.00829654783
  • ChenJ, CaoX, CuiY, ZengG, ChenJ, ZhangG. Resveratrol alleviates lysophosphatidylcholine-induced damage and inflammation in vascular endothelial cells. Mol Med Rep. 2018;17(3):4011–4018.29257345
  • XuM, ChenX, ChenD, YuB, HuangZ. FoxO1: a novel insight into its molecular mechanisms in the regulation of skeletal muscle differentiation and fiber type specification. Oncotarget. 2017;8(6):10662–10674.27793012
  • UrbanekP, KlotzLO. Posttranscriptional regulation of FOXO expression: microRNAs and beyond. Br J Pharmacol. 2017;174(12):1514–1532.26920226
  • AcciliD, ArdenKC. FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell. 2004;117(4):421–426.15137936
  • WebbAE, BrunetA. FOXO transcription factors: key regulators of cellular quality control. Trends Biochem Sci. 2014;39(4):159–169.24630600
  • KortylewskiM, FeldF, KrugerKD, et al. Akt modulates STAT3-mediated gene expression through a FKHR (FOXO1a)-dependent mechanism. J Biol Chem. 2003;278(7):5242–5249.12456685
  • HuangX, SunJ, ChenG, et al. Resveratrol promotes diabetic wound healing via SIRT1-FOXO1-c-Myc signaling pathway-mediated angiogenesis. Front Pharmacol. 2019;10:421.31068817
  • SinTK, YungBY, SiuPM. Modulation of SIRT1-Foxo1 signaling axis by resveratrol: implications in skeletal muscle aging and insulin resistance. Cell Physiol Biochem. 2015;35(2):541–552.25612477
  • FengYL, JiangXT, MaFF, HanJ, TangXL. Resveratrol prevents osteoporosis by upregulating FoxO1 transcriptional activity. Int J Mol Med. 2018;41(1):202–212.29115382
  • HongYA, BaeSY, AhnSY, et al. Resveratrol ameliorates contrast induced nephropathy through the activation of SIRT1-PGC-1alpha-foxo1 signaling in mice. Kidney Blood Press Res. 2017;42(4):641–653.29035878
  • LeeJY, YeJ, GaoZ, et al. Reciprocal modulation of toll-like receptor-4 signaling pathways involving MyD88 and phosphatidylinositol 3-kinase/AKT by saturated and polyunsaturated fatty acids. J Biol Chem. 2003;278(39):37041–37051.12865424
  • SaponaroC, CianciulliA, CalvelloR, DragoneT, IacobazziF, PanaroMA. The PI3K/Akt pathway is required for LPS activation of microglial cells. Immunopharmacol Immunotoxicol. 2012;34(5):858–865.22397361
  • BrunetA, BonniA, ZigmondMJ, et al. Akt promotes cell survival by phosphorylating and inhibiting a forkhead transcription factor. Cell. 1999;96(6):857–868.10102273