Resveratrol attenuated TNF-α–induced MMP-3 expression in human nucleus pulposus cells by activating autophagy via AMPK/SIRT1 signaling pathway

Experimental Biology and Medicine

Volumn 241, Issue 8, 2016, Pages 848-853

  Wang, Xiao Hu ^a   Zhu, Lei ^a   Hong, Xin ^a   Wang, Yun Tao ^a   Wang, Feng ^a   Bao, Jun Ping ^a   Xie, Xin Hui ^a   Liu, Lei ^a   Wu, Xiao Tao ^a  

^a MEDICAL SCHOOL OF SOUTHEAST UNIVERSITY   (China)

Author keywords

AMPK; autophagy; MMP 3; nucleus pulposus cell; Resveratrol; SIRT1; TNF

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; RESVERATROL; SIRTUIN 1; STROMELYSIN; TUMOR NECROSIS FACTOR ALPHA; SIRT1 PROTEIN, HUMAN; STILBENE DERIVATIVE; TUMOR NECROSIS FACTOR;

ANALYSIS OF VARIANCE; ARTICLE; AUTOPHAGY; CHEMOLUMINESCENCE; CONTROLLED STUDY; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INTERVERTEBRAL DISK DEGENERATION; INTERVERTEBRAL DISK HERNIA; PROTEIN EXPRESSION; RADIOIMMUNOPRECIPITATION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; CELL CULTURE; DRUG EFFECTS; METABOLISM; NUCLEUS PULPOSUS; PHYSIOLOGY;

AMP-ACTIVATED PROTEIN KINASES; AUTOPHAGY; BLOTTING, WESTERN; CELLS, CULTURED; HUMANS; MATRIX METALLOPROTEINASE 3; NUCLEUS PULPOSUS; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SIRTUIN 1; STILBENES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84971671593     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.1177/1535370216637940     Document Type: Article

References (43)

1. E.H.CassinelliR.A.HallJ.D.Kang. Biochemistry of intervertebral disc degeneration and the potential for gene therapy applications. Spine J2001; 1: 205–14.
2. M.KrismerM.van Tulder. Low Back Pain Group of the B, Joint Health Strategies for Europe P. Strategies for prevention and management of musculoskeletal conditions. Low back pain (non-specific). Best Pract Res Clin Rheumatol2007; 21: 77–91.
3. G.Waddell. Low back pain: a twentieth century health care enigma. Spine (Phila Pa 1976)1996; 21: 2820–5.
4. A.JoudI.F.PeterssonM.Englund. Low back pain: epidemiology of consultations. Arthritis Care Res (Hoboken)2012; 64: 1084–8.
5. S.LeeC.S.MoonD.SulJ.LeeM.BaeY.HongM.LeeS.ChoiR.DerbyB.J.KimJ.KimJ.S.YoonL.WolferJ.KimJ.WangS.W.HwangS.H.Lee. Comparison of growth factor and cytokine expression in patients with degenerated disc disease and herniated nucleus pulposus. Clin Biochem2009; 42: 1504–11.
6. C.WeilerA.G.NerlichB.E.BachmeierN.Boos. Expression and distribution of tumor necrosis factor alpha in human lumbar intervertebral discs: a study in surgical specimen and autopsy controls. Spine (Phila Pa 1976)2005; 30: 44–53. discussion 4.
7. D.PurmessurB.A.WalterP.J.RoughleyD.M.LaudierA.C.HechtJ.Iatridis. A role for TNFalpha in intervertebral disc degeneration: a non-recoverable catabolic shift. Biochem Biophys Res Commun2013; 433: 151–6.
8. C.A.SeguinR.M.PilliarP.J.RoughleyR.A.Kandel. Tumor necrosis factor-alpha modulates matrix production and catabolism in nucleus pulposus tissue. Spine (Phila Pa 1976)2005; 30: 1940–8.
9. Y.TianW.YuanN.FujitaJ.WangH.WangI.M.ShapiroM.V.Risbud. Inflammatory cytokines associated with degenerative disc disease control aggrecanase-1 (ADAMTS-4) expression in nucleus pulposus cells through MAPK and NF-kappaB. Am J Pathol2013; 182: 2310–21.
10. C.A.SeguinR.M.PilliarJ.A.MadriR.A.Kandel. TNF-alpha induces MMP2 gelatinase activity and MT1-MMP expression in an in vitro model of nucleus pulposus tissue degeneration. Spine (Phila Pa 1976)2008; 33: 356–65.
11. C.A.de la LastraI.Villegas. Resveratrol as an anti-inflammatory and anti-aging agent: mechanisms and clinical implications. Mol Nutr Food Res2005; 49: 405–30.
12. L.E.DonnellyR.NewtonG.E.KennedyP.S.FenwickR.H.LeungK.ItoR.E.RussellP.J.Barnes. Anti-inflammatory effects of resveratrol in lung epithelial cells: molecular mechanisms. Am J Physiol Lung Cell Mol Physiol2004; 287: L774–83.
13. C.C.UdenigweV.R.RamprasathR.E.AlukoP.J.Jones. Potential of resveratrol in anticancer and anti-inflammatory therapy. Nutr Rev2008; 66: 445–54.
14. L.M.HungJ.K.ChenS.S.HuangR.S.LeeM.J.Su. Cardioprotective effect of resveratrol, a natural antioxidant derived from grapes. Cardiovasc Res2000; 47: 549–55.
15. N.ElmaliI.EsenkayaA.HarmaK.ErtemY.TurkozB.Mizrak. Effect of resveratrol in experimental osteoarthritis in rabbits. Inflamm Res2005; 54: 158–62.
16. N.ElmaliO.BaysalA.HarmaI.EsenkayaB.Mizrak. Effects of resveratrol in inflammatory arthritis. Inflammation2007; 30: 1–6.
17. L.ZhangY.LiZ.GuY.WangM.ShiY.JiJ.SunX.XuL.ZhangJ.JiangW.Shi. Resveratrol inhibits enterovirus 71 replication and pro-inflammatory cytokine secretion in rhabdosarcoma cells through blocking IKKs/NF-kappaB signaling pathway. PLoS One2015; 10: e0116879–e0116879.
18. S.BastianettoC.MenardR.Quirion. Neuroprotective action of resveratrol. Biochim Biophys Acta2015; 1852: 1195–201.
19. B.BellaverD.G.SouzaD.O.SouzaA.Quincozes-Santos. Resveratrol increases antioxidant defenses and decreases proinflammatory cytokines in hippocampal astrocyte cultures from newborn, adult and aged Wistar rats. Toxicol in Vitro2014; 28: 479–84.
20. D.WangZ.HuJ.HaoB.HeQ.GanX.ZhongX.ZhangJ.ShenJ.FangW.Jiang. SIRT1 inhibits apoptosis of degenerative human disc nucleus pulposus cells through activation of Akt pathway. Age (Dordr)2013; 35: 1741–53.
21. W.JiangX.ZhangJ.HaoJ.ShenJ.FangW.DongD.WangX.ZhangW.ShuiY.LuoL.LinQ.QiuB.LiuZ.Hu. SIRT1 protects against apoptosis by promoting autophagy in degenerative human disc nucleus pulposus cells. Sci Rep2014; 4: 7456–7456.
22. X.H.WangX.HongL.ZhuY.T.WangJ.P.BaoL.LiuF.WangX.T.Wu. Tumor necrosis factor alpha promotes the proliferation of human nucleus pulposus cells via nuclear factor-kappaB, c-Jun N-terminal kinase, and p38 mitogen-activated protein kinase. Exp Biol Med (Maywood)2015; 240: 411–7.
23. D.J.KlionskyF.C.AbdallaH.AbeliovichR.T.AbrahamA.Acevedo-ArozenaK.AdeliL.AgholmeM.AgnelloP.AgostinisJ.A.Aguirre-Ghiso. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy2012; 8: 445–544.
24. S.A.JonesK.H.MillsJ.Harris. Autophagy and inflammatory diseases. Immunol Cell Biol2013; 91: 250–8.
25. G.QiuX.LiX.CheC.WeiS.HeJ.LuZ.JiaK.PangL.Fan. SIRT1 is a regulator of autophagy: Implications in gastric cancer progression and treatment. FEBS Lett2015; 589: 2034–42.
26. Y.WuX.LiJ.X.ZhuW.XieW.LeZ.FanJ.JankovicT.Pan. Resveratrol-activated AMPK/SIRT1/autophagy in cellular models of Parkinson’s disease. Neurosignals2011; 19: 163–74.
27. J.R.ChinG.MurphyZ.Werb. Stromelysin, a connective tissue-degrading metalloendopeptidase secreted by stimulated rabbit synovial fibroblasts in parallel with collagenase. Biosynthesis, isolation, characterization, and substrates. J Biol Chem1985; 260: 12367–76.
28. J.J.WuM.W.LarkL.E.ChunD.R.Eyre. Sites of stromelysin cleavage in collagen types II, IX, X, and XI of cartilage. J Biol Chem1991; 266: 5625–8.
29. R.K.StuderL.G.GilbertsonH.GeorgescuG.SowaN.VoJ.D.Kang. p38 MAPK inhibition modulates rabbit nucleus pulposus cell response to IL-1. J Orthop Res2008; 26: 991–8.
30. Y.OgataJ.J.EnghildH.Nagase. Matrix metalloproteinase 3 (stromelysin) activates the precursor for the human matrix metalloproteinase 9. J Biol Chem1992; 267: 3581–4.
31. G.MurphyM.I.CockettP.E.StephensB.J.SmithA.J.Docherty. Stromelysin is an activator of procollagenase. A study with natural and recombinant enzymes. Biochem J1987; 248: 265–8.
32. M.TakahashiH.HaroY.WakabayashiT.Kawa-uchiH.KomoriK.Shinomiya. The association of degeneration of the intervertebral disc with 5a/6a polymorphism in the promoter of the human matrix metalloproteinase-3 gene. J Bone Joint Surg Br2001; 83: 491–5.
33. M.KanemotoS.HukudaY.KomiyaA.KatsuuraJ.Nishioka. Immunohistochemical study of matrix metalloproteinase-3 and tissue inhibitor of metalloproteinase-1 human intervertebral discs. Spine (Phila Pa 1976)1996; 21: 1–8.
34. S.J.Millward-SadlerP.W.CostelloA.J.FreemontJ.A.Hoyland. Regulation of catabolic gene expression in normal and degenerate human intervertebral disc cells: implications for the pathogenesis of intervertebral disc degeneration. Arthritis Res Ther2009; 11: R65–R65.
35. D.J.KlionskyS.D.Emr. Autophagy as a regulated pathway of cellular degradation. Science2000; 290: 1717–21.
36. J.TianJ.W.ChenJ.S.GaoL.LiX.Xie. Resveratrol inhibits TNF-alpha-induced IL-1beta, MMP-3 production in human rheumatoid arthritis fibroblast-like synoviocytes via modulation of PI3kinase/Akt pathway. Rheumatol Int2013; 33: 1829–35.
37. X.ZhuQ.LiuM.WangM.LiangX.YangX.XuH.ZouJ.Qiu. Activation of SIRT1 by resveratrol inhibits TNF-alpha induced inflammation in fibroblasts. PLoS One2011; 6: e27081–e27081.
38. J.ZhuW.YongX.WuY.YuJ.LvC.LiuX.MaoY.ZhuK.XuX.HanC.Liu. Anti-inflammatory effect of resveratrol on TNF-alpha-induced MCP-1 expression in adipocytes. Biochem Biophys Res Commun2008; 369: 471–7.
39. O.H.KangH.J.JangH.S.ChaeY.C.OhJ.G.ChoiY.S.LeeJ.H.KimY.C.KimD.H.SohnH.ParkD.Y.Kwon. Anti-inflammatory mechanisms of resveratrol in activated HMC-1 cells: pivotal roles of NF-kappaB and MAPK. Pharmacol Res2009; 59: 330–7.
40. Y.C.OhO.H.KangJ.G.ChoiH.S.ChaeY.S.LeeO.O.BriceH.J.JungS.H.HongY.M.LeeD.Y.Kwon. Anti-inflammatory effect of resveratrol by inhibition of IL-8 production in LPS-induced THP-1 cells. Am J Chin Med2009; 37: 1203–14.
41. B.BellaverD.G.SouzaL.D.BoberminD.O.SouzaC.A.GoncalvesA.Quincozes-Santos. Resveratrol protects hippocampal astrocytes against LPS-induced neurotoxicity through HO-1, p38 and ERK Pathways. Neurochem Res2015; 40: 1600–8.
42. C.CantoZ.Gerhart-HinesJ.N.FeigeM.LagougeL.NoriegaJ.C.MilneP.J.ElliottP.PuigserverJ.Auwerx. AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature2009; 458: 1056–60.
43. H.GuoY.ChenL.LiaoW.Wu. Resveratrol protects HUVECs from oxidized-LDL induced oxidative damage by autophagy upregulation via the AMPK/SIRT1 pathway. Cardiovasc Drugs Ther2013; 27: 189–98.