Resveratrol inhibits oxygen-glucose deprivation-induced MMP-3 expression and cell apoptosis in primary cortical cells via the NF-κB pathway

Molecular Medicine Reports

Volumn 10, Issue 2, 2014, Pages 1065-1071

  Huang, Tao ^a   Gao, Dakuan ^a   Jiang, Xiaofan ^a   Hu, Shijie ^a   Zhang, Lei ^a   Fei, Zhou ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Apoptosis; Cortical cells; Inducible nitric oxide synthase; MMP 3; Nitric oxide; Nuclear factor B; Oxygen glucose deprivation; Resveratrol

Indexed keywords

3,3 BIS(2 AMINOETHYL) 1 HYDROXY 2 OXOTRIAZENE; CASPASE 3; GLUCOSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; OXYGEN; PROTEIN BAX; PROTEIN BCL 2; PYRROLIDINE DITHIOCARBAMATE; RESVERATROL; STROMELYSIN; TETRAZOLIUM; NEUROPROTECTIVE AGENT; NITROSO DERIVATIVE; PROLINE; PROLINEDITHIOCARBAMATE; STILBENE DERIVATIVE; THIOCARBAMIC ACID DERIVATIVE;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN CELL; BRAIN CELL CULTURE; BRAIN ISCHEMIA; CELL VIABILITY; CELL VIABILITY ASSAY; CONTROLLED STUDY; CULTURE MEDIUM; DRUG EFFECT; DRUG INHIBITION; ENZYME ACTIVATION; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; MOUSE; MTT ASSAY; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; REOXYGENATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPECTROPHOTOMETRY; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN CORTEX; CELL CULTURE; CELL HYPOXIA; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CASPASE 3; CELL HYPOXIA; CELLS, CULTURED; CEREBRAL CORTEX; GENE EXPRESSION; GLUCOSE; MATRIX METALLOPROTEINASE 3; MICE; NEUROPROTECTIVE AGENTS; NF-KAPPA B; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; NITROSO COMPOUNDS; PROLINE; PROTO-ONCOGENE PROTEINS C-BCL-2; SIGNAL TRANSDUCTION; STILBENES; THIOCARBAMATES;

EID: 84903270233     PISSN: 17912997     EISSN: 17913004     Source Type: Journal    
DOI: 10.3892/mmr.2014.2239     Document Type: Article

References (42)

1. Hallenbeck JM and Dutka AJ: Background review and current concepts of reperfusion injury. Arch Neurol 47: 1245-1254, 1990. (Pubitemid 20381010)
2. Magnoni S, Baker A, George SJ, Duncan WC, Kerr LE, McCulloch J and Horsburgh K: Differential alterations in the expression and activity of matrix metalloproteinases 2 and 9 after transient cerebral ischemia in mice. Neurobiol Dis 17: 188-197, 2004. (Pubitemid 39345775)
3. Oguro K, Jover T, Tanaka H, Lin Y, Kojima T, Oguro N, Grooms SY, Bennett MV and Zukin RS: Global ischemia-induced increases in the gap junctional proteins connexin 32 (Cx32) and Cx36 in hippocampus and enhanced vulnerability of Cx32 knock-out mice. J Neurosci 21: 7534-7542, 2001. (Pubitemid 32904952)
4. Amantea D, Nappi G, Bernardi G, Bagetta G and Corasaniti MT: Post-ischemic brain damage: pathophysiology and role of inflammatory mediators. FEBS J 276: 13-26, 2009.
5. Choi JS, Kim SJ, Shin JA, Lee KE and Park EM: Effects of estrogen on temporal expressions of IL-1beta and IL-1ra in rat organotypic hippocampal slices exposed to oxygen-glucose deprivation. Neurosci Lett 438: 233-237, 2008.
6. Fekete A, Vizi ES, Kovács KJ, Lendvai B and Zelles T: Layer-specific differences in reactive oxygen species levels after oxygen-glucose deprivation in acute hippocampal slices. Free Radic Biol Med 44: 1010-1022, 2008.
7. Kiewert C, Kumar V, Hildmann O, Hartmann J, Hillert M and Klein J: Role of glycine receptors and glycine release for the neuroprotective activity of bilobalide. Brain Res 1201: 143-150, 2008.
8. Rosenberg GA: Matrix metalloproteinases in neuroinflammation. Glia 39: 279-291, 2002.
9. Gurney KJ, Estrada EY and Rosenberg GA: Blood-brain barrier disruption by stromelysin-1 facilitates neutrophil infiltration in neuroinflammation. Neurobiol Dis 23: 87-96, 2006. (Pubitemid 43903633)
10. Garcia AJ, Tom C, Guemes M, Polanco G, Mayorga ME, Wend K, Miranda-Carboni GA and Krum SA: ERα signaling regulates MMP3 expression to induce FasL cleavage and osteoclast apoptosis. J Bone Miner Res 28: 283-290, 2013.
11. Gu Z, Kaul M, Yan B, Kridel SJ, Cui J, Strongin A, Smith JW, Liddington RC and Lipton SA: S-nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science 297: 1186-1190, 2002. (Pubitemid 36193354)
12. Rosenberg GA, Cunningham LA, Wallace J, Alexander S, Estrada EY, Grossetete M, Razhagi A, Miller K and Gearing A: Immunohistochemistry of matrix metalloproteinases in reperfusion injury to rat brain: activation of MMP-9 linked to stromelysin-1 and microglia in cell cultures. Brain Res 893: 104-112, 2001. (Pubitemid 32171902)
13. Wetzel M, Rosenberg GA and Cunningham LA: Tissue inhibitor of metalloproteinases-3 and matrix metalloproteinase-3 regulate neuronal sensitivity to doxorubicin-induced apoptosis. Eur J Neurosci 18: 1050-1060, 2003. (Pubitemid 37115027)
14. Cheng Z, He W, Zhou X, Lv Q, Xu X, Yang S, Zhao C and Guo L: Cordycepin protects against cerebral ischemia/reperfusion injury in vivo and in vitro. Eur J Pharmacol 664: 20-28, 2011.
15. Walker EJ and Rosenberg GA: TIMP-3 and MMP-3 contribute to delayed inflammation and hippocampal neuronal death following global ischemia. Exp Neurol 216: 122-131, 2009.
16. Kim YS, Kim SS, Cho JJ, Choi DH, Hwang O, Shin DH, Chun HS, Beal MF and Joh TH: Matrix metalloproteinase-3: a novel signaling proteinase from apoptotic neuronal cells that activates microglia. J Neurosci 25: 3701-3711, 2005.
17. Choi DH, Kim EM, Son HJ, Joh TH, Kim YS, Kim D, Flint Beal M and Hwang O: A novel intracellular role of matrix metalloproteinase-3 during apoptosis of dopaminergic cells. J Neurochem 106: 405-415, 2008. (Pubitemid 351840221)
18. Kim EM, Shin EJ, Choi JH, Son HJ, Park IS, Joh TH and Hwang O: Matrix metalloproteinase-3 is increased and participates in neuronal apoptotic signaling downstream of caspase-12 during endoplasmic reticulum stress. J Biol Chem 285: 16444-16452, 2010.
19. Csaki C, Mobasheri A and Shakibaei M: Synergistic chondroprotective effects of curcumin and resveratrol in human articular chondrocytes: inhibition of IL-1β-induced NF-κB-mediated inflammation and apoptosis. Arthritis Res Ther 11: R165, 2009.
20. Celotti E, Ferrarini R, Zironi R and Conte LS: Resveratrol content of some wines obtained from dried Valpolicella grapes: Recioto and Amarone. J Chromatogr A 730: 47-52, 1996. (Pubitemid 26141922)
21. Pany S, Majhi A and Das J: PKC activation by resveratrol derivatives with unsaturated aliphatic chain. PLoS One 7: e52888, 2012.
22. Das J, Pany S and Majhi A: Chemical modifications of resveratrol for improved protein kinase C alpha activity. Bioorg Med Chem 19: 5321-5333, 2011.
23. Carrizzo A, Puca A, Damato A, Marino M, Franco E, Pompeo F, Traficante A, Civitillo F, Santini L, Trimarco V and Vecchione C: Resveratrol improves vascular function in patients with hypertension and dyslipidemia by modulating NO metabolism. Hypertension 62: 359-366, 2013.
24. Kesherwani V, Atif F, Yousuf S and Agrawal SK: Resveratrol protects spinal cord dorsal column from hypoxic injury by activating Nrf-2. Neuroscience 241: 80-88, 2013.
25. Wang Q, Xu J, Rottinghaus GE, Simonyi A, Lubahn D, Sun GY and Sun AY: Resveratrol protects against global cerebral ischemic injury in gerbils. Brain Res 958: 439-447, 2002. (Pubitemid 35441199)
26. Gao D, Zhang X, Jiang X, Peng Y, Huang W, Cheng G and Song L: Resveratrol reduces the elevated level of MMP-9 induced by cerebral ischemia-reperfusion in mice. Life Sci 78: 2564-2570, 2006.
27. Tauskela JS, Comas T, Hewitt K, Monette R, Paris J, Hogan M and Morley P: Cross-tolerance to otherwise lethal N-methyl-D-aspartate and oxygen-glucose deprivation in preconditioned cortical cultures. Neuroscience 107: 571-584, 2001. (Pubitemid 33097495)
28. Dal-Cim T, Ludka FK, Martins WC, Reginato C, Parada E, Egea J, López MG and Tasca CI: Guanosine controls inflammatory pathways to afford neuroprotection of hippocampal slices under oxygen and glucose deprivation conditions. J Neurochem 126: 437-450, 2013.
29. Martín-de-Saavedra MD, del Barrio L, Cañas N, Egea J, Lorrio S, Montell E, Vergés J, García AG and López MG: Chondroitin sulfate reduces cell death of rat hippocampal slices subjected to oxygen and glucose deprivation by inhibiting p38, NFκB and iNOS. Neurochem Int 58: 676-683, 2011.
30. Molz S, Dal-Cim T, Budni J, Martín-de-Saavedra MD, Egea J, Romero A, del Barrio L, Rodrigues AL, López MG and Tasca CI: Neuroprotective effect of guanosine against glutamate-induced cell death in rat hippocampal slices is mediated by the phosphatidylinositol-3 kinase/Akt/ glycogen synthase kinase 3β pathway activation and inducible nitric oxide synthase inhibition. J Neurosci Res 89: 1400-1408, 2011.
31. Schaller B and Graf R: Cerebral ischemia and reperfusion: the pathophysiologic concept as a basis for clinical therapy. J Cereb Blood Flow Metab 24: 351-371, 2004. (Pubitemid 38452228)
32. Moskowitz MA, Lo EH and Iadecola C: The science of stroke: mechanisms in search of treatments. Neuron 67: 181-198, 2010.
33. Aoki T, Sumii T, Mori T, Wang X and Lo EH: Blood-brain barrier disruption and matrix metalloproteinase-9 expression during reperfusion injury: mechanical versus embolic focal ischemia in spontaneously hypertensive rats. Stroke 33: 2711-2717, 2002. (Pubitemid 35266446)
34. Maier CM, Hsieh L, Yu F, Bracci P and Chan PH: Matrix metalloproteinase-9 and myeloperoxidase expression: quantitative analysis by antigen immunohistochemistry in a model of transient focal cerebral ischemia. Stroke 35: 1169-1174, 2004. (Pubitemid 38543538)
35. Pfefferkorn T and Rosenberg GA: Closure of the blood-brain barrier by matrix metalloproteinase inhibition reduces rtPA-mediated mortality in cerebral ischemia with delayed reperfusion. Stroke 34: 2025-2030, 2003. (Pubitemid 36944801)
36. Cunningham LA, Wetzel M and Rosenberg GA: Multiple roles for MMPs and TIMPs in cerebral ischemia. Glia 50: 329-339, 2005. (Pubitemid 40780839)
37. Dzwonek J, Rylski M and Kaczmarek L: Matrix metalloproteinases and their endogenous inhibitors in neuronal physiology of the adult brain. FEBS Lett 567: 129-135, 2004. (Pubitemid 38686435)
38. Fujimura M, Tominaga T and Chan PH: Neuroprotective effect of an antioxidant in ischemic brain injury: involvement of neuronal apoptosis. Neurocrit Care 2: 59-66, 2005. (Pubitemid 40404630)
39. Krause GS, White BC, Aust SD, Nayini NR and Kumar K: Brain cell death following ischemia and reperfusion: a proposed biochemical sequence. Crit Care Med 16: 714-726, 1988.
40. Marcu KB, Otero M, Olivotto E, Borzi RM and Goldring MB: NF-kappaB signaling: multiple angles to target OA. Curr Drug Targets 11: 599-613, 2010.
41. Shakibaei M, Csaki C, Nebrich S and Mobasheri A: Resveratrol suppresses interleukin-1β-induced inflammatory signaling and apoptosis in human articular chondrocytes: potential for use as a novel nutraceutical for the treatment of osteoarthritis. Biochem Pharmacol 76: 1426-1439, 2008.
42. Dolinsky VW, Chakrabarti S, Pereira TJ, et al: Resveratrol prevents hypertension and cardiac hypertrophy in hypertensive rats and mice. Biochim Biophys Acta 1832: 1723-1733, 2013.