Resveratrol inhibits the IL-1β-induced expression ofMMP-13 and IL-6 in human articular chondrocytes viaTLR4/MyD88-dependent and-independent signaling cascades

International Journal of Molecular Medicine

Volumn 39, Issue 3, 2017, Pages 734-740

  Gu, Hailun ^a   Jiao, Yongliang ^a,b   Yu, Xiaolu ^a   Li, Xingyao ^a   Wang, Wei ^a   Ding, Lifeng ^a   Liu, Li ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

^b Jilin Institute of Physical Education   (China)

Author keywords

Chondrocytes; Interleukin 6; Matrix metalloproteinase 13; Myeloid differentiation factor 88; Resveratrol; Toll like receptor 4

Indexed keywords

COLLAGENASE 3; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; MYELOID DIFFERENTIATION FACTOR 88; RESVERATROL; TOLL LIKE RECEPTOR 4; BIOLOGICAL MARKER; STILBENE DERIVATIVE;

ADULT; AGED; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BIOLOGICAL ACTIVITY; CATABOLISM; CELL STIMULATION; CELL VIABILITY; CHONDROCYTE; CLINICAL ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; HUMAN CELL; INFLAMMATION; MALE; MTS ASSAY; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; CELL SURVIVAL; DRUG EFFECTS; GENE EXPRESSION; GENETICS; METABOLISM; MIDDLE AGED; OSTEOARTHRITIS; PATHOLOGY; PHENOTYPE;

AGED; BIOMARKERS; CELL SURVIVAL; CHONDROCYTES; GENE EXPRESSION; HUMANS; INTERLEUKIN-1BETA; INTERLEUKIN-6; MATRIX METALLOPROTEINASE 13; MIDDLE AGED; MYELOID DIFFERENTIATION FACTOR 88; OSTEOARTHRITIS; PHENOTYPE; SIGNAL TRANSDUCTION; STILBENES; TOLL-LIKE RECEPTOR 4;

EID: 85013106591     PISSN: 11073756     EISSN: 1791244X     Source Type: Journal    
DOI: 10.3892/ijmm.2017.2885     Document Type: Article

References (41)

1. Goldring SR: The role of bone in osteoarthritis pathogenesis. Rheum Dis Clin North Am 34: 561-571, 2008.
2. Sofat N, Ejindu V and Kiely P: What makes osteoarthritis painful? The evidence for local and central pain processing. Rheumatology (Oxford) 50: 2157-2165, 2011.
3. Man GS and Mologhianu G: Osteoarthritis pathogenesis-A complex process that involves the entire joint. J Med Life 7: 37-41, 2014.
4. Scanzello CR, Plaas A and Crow MK: Innate immune system activation in osteoarthritis: is osteoarthritis a chronic wound? Curr Opin Rheumatol 20: 565-572, 2008.
5. Ting JP, Duncan JA and Lei Y: How the noninflammasome NLRs function in the innate immune system. Science 327: 286-290, 2010.
6. McCormack WJ, Parker AE and O'Neill LA: Toll-like receptors and NOD-like receptors in rheumatic diseases. Arthritis Res Ther 11: 243, 2009.
7. Haglund L, Bernier SM, Onnerfjord P and Recklies AD: Proteomic analysis of the LPS-induced stress response in rat chondrocytes reveals induction of innate immune response components in articular cartilage. Matrix Biol 27: 107-118, 2008.
8. Schelbergen RF, Blom AB, van den Bosch MH, Slöetjes A, Abdollahi-Roodsaz S, Schreurs BW, Mort JS, Vogl T, Roth J, van den Berg WB and van Lent PL: Alarmins S100A8 and S100A9 elicit a catabolic effect in human osteoarthritic chondrocytes that is dependent on Toll-like receptor 4. Arthritis Rheum 64: 1477-1487, 2012.
9. Abdollahi-Roodsaz S, Joosten LA, Roelofs MF, Radstake TR, Matera G, Popa C, van der Meer JW, Netea MG and van den Berg WB: Inhibition of Toll-like receptor 4 breaks the inflammatory loop in autoimmune destructive arthritis. Arthritis Rheum 56: 2957-2967, 2007.
10. Shotorbani SS, Su ZL and Xu HX: Toll-like receptors are potential therapeutic targets in rheumatoid arthritis. World J Biol Chem 2: 167-172, 2011.
11. Bobacz K, Sunk IG, Hofstaetter JG, Amoyo L, Toma CD, Akira S, Weichhart T, Saemann M and Smolen JS: Toll-like receptors and chondrocytes: The lipopolysaccharide-induced decrease in cartilage matrix synthesis is dependent on the presence of toll-like receptor 4 and antagonized by bone morphogenetic protein 7. Arthritis Rheum 56: 1880-1893, 2007.
12. Sgaglione NA: Biologic approaches to articular cartilage surgery: future trends. Orthop Clin North Am 36: 485-495, 2005.
13. Im HJ, Li X, Chen D, Yan D, Kim J, Ellman MB, Stein GS, Cole B, Kc R, Cs-Szabo G and van Wijnen AJ: Biological effects of the plant-derived polyphenol resveratrol in human articular cartilage and chondrosarcoma cells. J Cell Physiol 227: 3488-3497, 2012.
14. Yadav M, Jain S, Bhardwaj A, Nagpal R, Puniya M, Tomar R, Singh V, Parkash O, Prasad GB, Marotta F and Yadav H: Biological and medicinal properties of grapes and their bioactive constituents: An update. J Med Food 12: 473-484, 2009.
15. Eo SH, Cho H and Kim SJ: Resveratrol inhibits nitric oxide-induced apoptosis via the NF-kappa B pathway in rabbit articular chondrocytes. Biomol Ther (Seoul) 21: 364-370, 2013.
16. Csaki C, Keshishzadeh N, Fischer K and Shakibaei M: Regulation of inflammation signalling by resveratrol in human chondrocytes in vitro. Biochem Pharmacol 75: 677-687, 2008.
17. Shakibaei M, John T, Seifarth C and Mobasheri A: Resveratrol inhibits IL-1 beta-induced stimulation of caspase-3 and cleavage of PARP in human articular chondrocytes in vitro. Ann N Y Acad Sci 1095: 554-563, 2007.
18. Elmali N, Esenkaya I, Harma A, Ertem K, Turkoz Y and Mizrak B: Effect of resveratrol in experimental osteoarthritis in rabbits. Inflamm Res 54: 158-162, 2005.
19. Elmali N, Baysal O, Harma A, Esenkaya I and Mizrak B: Effects of resveratrol in inflammatory arthritis. Inflammation 30: 1-6, 2007.
20. Lei M, Wang JG, Xiao DM, Fan M, Wang DP, Xiong JY, Chen Y, Ding Y and Liu SL: Resveratrol inhibits interleukin 1β-mediated inducible nitric oxide synthase expression in articular chondrocytes by activating SIRT1 and thereby suppressing nuclear factor-κB activity. Eur J Pharmacol 674: 73-79, 2012.
21. Shakibaei M, Mobasheri A and Buhrmann C: Curcumin synergizes with resveratrol to stimulate the MAPK signaling pathway in human articular chondrocytes in vitro. Genes Nutr 6: 171-179, 2011.
22. Eo SH, Cho HS and Kim SJ: Resveratrol regulates type II collagen and COX-2 expression via the ERK, p38 and Akt signaling pathways in rabbit articular chondrocytes. Exp Ther Med 7: 640-648, 2014.
23. Han KJ, Su X, Xu LG, Bin LH, Zhang J and Shu HB: Mechanisms of the TRIF-induced interferon-stimulated response element and NF-kappaB activation and apoptosis pathways. J Biol Chem 279: 15652-15661, 2004.
24. Baumgarten G, Knuefermann P, Nozaki N, Sivasubramanian N, Mann DL and Vallejo JG: In vivo expression of proinflammatory mediators in the adult heart after endotoxin administration: The role of toll-like receptor-4. J Infect Dis 183: 1617-1624, 2001.
25. Jakus PB, Kalman N, Antus C, Radnai B, Tucsek Z, Gallyas F Jr, Sumegi B and Veres B: TRAF6 is functional in inhibition of TLR4-mediated NF-κB activation by resveratrol. J Nutr Biochem 24: 819-823, 2013.
26. Liu L, Gu H, Liu H, Jiao Y, Li K, Zhao Y, An L and Yang J: Protective effect of resveratrol against IL-1β-induced inflammatory response on human osteoarthritic chondrocytes partly via the TLR4/MyD88/NF-κB signaling pathway: An in vitro study. Int J Mol Sci 15: 6925-6940, 2014.
27. Sebai H, Ristorcelli E, Sbarra V, Hovsepian S, Fayet G, Aouani E and Lombardo D: Protective effect of resveratrol against LPS-induced extracellular lipoperoxidation in AR42J cells partly via a Myd88-dependent signaling pathway. Arch Biochem Biophys 495: 56-61, 2010.
28. Jung DY, Lee H, Jung BY, Ock J, Lee MS, Lee WH and Suk K: TLR4, but not TLR2, signals autoregulatory apoptosis of cultured microglia: A critical role of IFN-beta as a decision maker. J Immunol 174: 6467-6476, 2005.
29. Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-Time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408, 2001.
30. Vincenti MP and Brinckerhoff CE: Transcriptional regulation of collagenase (MMP-1, MMP-13) genes in arthritis: integration of complex signaling pathways for the recruitment of gene-specific transcription factors. Arthritis Res 4: 157-164, 2002.
31. Yammani RR, Carlson CS, Bresnick AR and Loeser RF: Increase in production of matrix metalloproteinase 13 by human articular chondrocytes due to stimulation with S100A4: role of the receptor for advanced glycation end products. Arthritis Rheum 54: 2901-2911, 2006.
32. Im HJ, Pacione C, Chubinskaya S, Van Wijnen AJ, Sun Y and Loeser RF: Inhibitory effects of insulin-like growth factor-1 and osteogenic protein-1 on fibronectin fragment-And interleukin-1beta-stimulated matrix metalloproteinase-13 expression in human chondrocytes. J Biol Chem 278: 25386-25394, 2003.
33. Muddasani P, Norman JC, Ellman M, van Wijnen AJ and Im HJ: Basic fibroblast growth factor activates the MAPK and NFkappaB pathways that converge on Elk-1 to control production of matrix metalloproteinase-13 by human adult articular chondrocytes. J Biol Chem 282: 31409-31421, 2007.
34. Legendre F, Bogdanowicz P, Boumediene K and Pujol JP: Role of interleukin 6 (IL-6)/IL-6R-induced signal tranducers and activators of transcription and mitogen-Activated protein kinase/extracellular. J Rheumatol 32: 1307-1316, 2005.
35. Estrov Z, Shishodia S, Faderl S, Harris D, Van Q, Kantarjian HM, Talpaz M and Aggarwal BB: 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 102: 987-995, 2003.
36. Kundu JK, Shin YK and Surh YJ: Resveratrol modulates phorbol ester-induced pro-inflammatory signal transduction pathways in mouse skin in vivo: NF-kappaB and AP-1 as prime targets. Biochem Pharmacol 72: 1506-1515, 2006.
37. Liu-Bryan R and Terkeltaub R: Chondrocyte innate immune myeloid differentiation factor 88-dependent signaling drives procatabolic effects of the endogenous Toll-like receptor 2/Toll-like receptor 4 ligands low molecular weight hyaluronan and high mobility group box chromosomal protein 1 in mice. Arthritis Rheum 62: 2004-2012, 2010.
38. Weighardt H, Jusek G, Mages J, Lang R, Hoebe K, Beutler B and Holzmann B: Identification of a TLR4-And TRIF-dependent activation program of dendritic cells. Eur J Immunol 34: 558-564, 2004.
39. Björkbacka H, Fitzgerald KA, Huet F, Li X, Gregory JA, Lee MA, Ordija CM, Dowley NE, Golenbock DT and Freeman MW: The induction of macrophage gene expression by LPS predominantly utilizes Myd88-independent signaling cascades. Physiol Genomics 19: 319-330, 2004.
40. Jiang Z, Mak TW, Sen G and Li X: Toll-like receptor 3-mediated activation of NF-kappaB and IRF3 diverges at Toll-IL-1 receptor domain-containing adapter inducing IFN-beta. Proc Natl Acad Sci USA 101: 3533-3538, 2004.
41. Sato S, Sugiyama M, Yamamoto M, Watanabe Y, Kawai T, Takeda K and Akira S: Toll/IL-1 receptor domain-containing adaptor inducing IFN-beta (TRIF) associates with TNF receptor-Associated factor 6 and TANK-binding kinase 1, and activates two distinct transcription factors, NF-kappa B and IFN-regulatory factor-3, in the Toll-like receptor signaling. J Immunol 171: 4304-4310, 2003.