Differential inhibitory effects of resveratrol on excitotoxicity and synaptic plasticity: involvement of NMDA receptor subtypes

References

• Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, et al. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev. 2010 Sep;62(3):405–96.
   PubMed Web of Science ®Google Scholar
• Paoletti P, Bellone C, Zhou Q. NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease. Nat Rev Neurosci. 2013 Jun;14(6):383–400.
   PubMed Web of Science ®Google Scholar
• Cull-Candy SG, Leszkiewicz DN. Role of distinct NMDA receptor subtypes at central synapses. Sci STKE. 2004 Oct 19;2004(255):re16.
   PubMedGoogle Scholar
• Cull-Candy S, Brickley S, Farrant M. NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol. 2001 Jun;11(3):327–35.
   PubMed Web of Science ®Google Scholar
• Sanz-Clemente A, Nicoll RA, Roche KW. Diversity in NMDA receptor composition: many regulators, many consequences. Neuroscientist. 2013 Feb;19(1):62–75.
   PubMed Web of Science ®Google Scholar
• Liu Y, Wong TP, Aarts M, Rooyakkers A, Liu L, Lai TW, et al. NMDA receptor subunits have differential roles in mediating excitotoxic neuronal death both in vitro and in vivo. J Neurosci. 2007 Mar 14;27(11):2846–57.
   PubMed Web of Science ®Google Scholar
• Liu L, Wong TP, Pozza MF, Lingenhoehl K, Wang Y, Sheng M, et al. Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science. 2004 May 14;304(5673):1021–4.
   PubMed Web of Science ®Google Scholar
• von Engelhardt J, Coserea I, Pawlak V, Fuchs EC, Kohr G, Seeburg PH, et al. Excitotoxicity in vitro by NR2A- and NR2B-containing NMDA receptors. Neuropharmacology. 2007 Jul;53(1):10–7.
   PubMed Web of Science ®Google Scholar
• Kohr G, Jensen V, Koester HJ, Mihaljevic AL, Utvik JK, Kvello A, et al. Intracellular domains of NMDA receptor subtypes are determinants for long-term potentiation induction. J Neurosci. 2003 Nov 26;23(34):10791–9.
   PubMed Web of Science ®Google Scholar
• Massey PV, Johnson BE, Moult PR, Auberson YP, Brown MW, Molnar E, et al. Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J Neurosci. 2004 Sep 8;24(36):7821–8.
   PubMed Web of Science ®Google Scholar
• Gladding CM, Raymond LA. Mechanisms underlying NMDA receptor synaptic/extrasynaptic distribution and function. Mol Cell Neurosci. 2011 Dec;48(4):308–20.
   PubMed Web of Science ®Google Scholar
• Hatton CJ, Paoletti P. Modulation of triheteromeric NMDA receptors by N-terminal domain ligands. Neuron. 2005 Apr 21;46(2):261–74.
   PubMed Web of Science ®Google Scholar
• Lai TW, Shyu WC, Wang YT. Stroke intervention pathways: NMDA receptors and beyond. Trends Mol Med. 2011 May;17(5):266–75.
   PubMed Web of Science ®Google Scholar
• Milnerwood AJ, Gladding CM, Pouladi MA, Kaufman AM, Hines RM, Boyd JD, et al. Early increase in extrasynaptic NMDA receptor signaling and expression contributes to phenotype onset in Huntington’s disease mice. Neuron. 2010 Jan 28;65(2):178–90.
   PubMed Web of Science ®Google Scholar
• Ronicke R, Mikhaylova M, Ronicke S, Meinhardt J, Schroder UH, Fandrich M, et al. Early neuronal dysfunction by amyloid beta oligomers depends on activation of NR2B-containing NMDA receptors. Neurobiol Aging. 2011 Dec;32(12):2219–28.
   PubMed Web of Science ®Google Scholar
• Qiu S, Li XY, Zhuo M. Post-translational modification of NMDA receptor GluN2B subunit and its roles in chronic pain and memory. Semin Cell Dev Biol. 2011 Jul;22(5):521–9.
   PubMed Web of Science ®Google Scholar
• Yuan H, Myers SJ, Wells G, Nicholson KL, Swanger SA, Lyuboslavsky P, et al. Context-dependent GluN2B-selective inhibitors of NMDA receptor function are neuroprotective with minimal side effects. Neuron. 2015 Mar 18;85(6):1305–18.
   PubMed Web of Science ®Google Scholar
• Hu NW, Klyubin I, Anwyl R, Rowan MJ. Glun2b subunit-containing NMDA receptor antagonists prevent Abeta-mediated synaptic plasticity disruption in vivo. Proc Natl Acad Sci U S A. 2009 Dec 1;106(48):20504–9.
   PubMed Web of Science ®Google Scholar
• Salter MG, Fern R. NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury. Nature. 2005 Dec 22;438(7071):1167–71.
   PubMed Web of Science ®Google Scholar
• Doyle S, Hansen DB, Vella J, Bond P, Harper G, Zammit C, et al. Vesicular glutamate release from central axons contributes to myelin damage. Nat Commun. 2018 Mar 12;9(1):1032.
   PubMedGoogle Scholar
• Chizh BA, Headley PM, Tzschentke TM. NMDA receptor antagonists as analgesics: focus on the NR2B subtype. Trends Pharmacol Sci. 2001 Dec;22(12):636–42.
   PubMed Web of Science ®Google Scholar
• Albensi BC, Igoechi C, Janigro D, Ilkanich E. Why do many NMDA antagonists fail, while others are safe and effective at blocking excitotoxicity associated with dementia and acute injury? Am J Alzheimers Dis Other Demen. 2004 Sep-Oct;19(5):269–74.
   PubMedGoogle Scholar
• Mullin GE. Red wine, grapes, and better health–resveratrol. Nutr Clin Pract. 2011 Dec;26(6):722–3.
   PubMed Web of Science ®Google Scholar
• Shetty AK. Promise of resveratrol for easing status epilepticus and epilepsy. Pharmacol Ther. 2011 Sep;131(3):269–86.
   PubMed Web of Science ®Google Scholar
• Lopez MS, Dempsey RJ, Vemuganti R. Resveratrol neuroprotection in stroke and traumatic CNS injury. Neurochem Int. 2015 Oct;89:75–82.
   PubMed Web of Science ®Google Scholar
• Pervaiz S, Holme AL. Resveratrol: its biologic targets and functional activity. Antioxid Redox Signal. 2009 Nov;11(11):2851–97.
   PubMed Web of Science ®Google Scholar
• Yanez M, Galan L, Matias-Guiu J, Vela A, Guerrero A, Garcia AG. CSF from amyotrophic lateral sclerosis patients produces glutamate independent death of rat motor brain cortical neurons: protection by resveratrol but not riluzole. Brain Res. 2011 Nov 14;1423:77–86.
   PubMed Web of Science ®Google Scholar
• Chen J, Bai Q, Zhao Z, Sui H, Xie X. Resveratrol improves delayed r-tPA treatment outcome by reducing MMPs. Acta Neurol Scand. 2016 Jul;134(1):54–60.
   PubMed Web of Science ®Google Scholar
• Zhang LN, Hao L, Wang HY, Su HN, Sun YJ, Yang XY, et al. Neuroprotective effect of resveratrol against glutamate-induced excitotoxicity. Adv Clin Exp Med. 2015 Jan-Feb;24(1):161–5.
   PubMed Web of Science ®Google Scholar
• Gao ZB, Chen XQ, Hu GY. Inhibition of excitatory synaptic transmission by trans-resveratrol in rat hippocampus. Brain Res. 2006 Sep 21;1111(1):41–7.
   PubMedGoogle Scholar
• Wang YJ, Hsieh CP, Chan MH, Chan TY, Chen L, Chen HH. Distinct effects of resveratrol on seizures and hyperexcitability induced by NMDA and 4-aminopyridine. Nutr Neurosci. 2018 Apr 12:1–11.
   Web of Science ®Google Scholar
• Takehana S, Kubota Y, Uotsu N, Yui K, Iwata K, Shimazu Y, et al. The dietary constituent resveratrol suppresses nociceptive neurotransmission via the NMDA receptor. Mol Pain. 2017 Jan;13:1744806917697010.
   Web of Science ®Google Scholar
• Yang X, Si P, Qin H, Yin L, Yan LJ, Zhang C. The neuroprotective effects of SIRT1 on NMDA-induced excitotoxicity. Oxid Med Cell Longev. 2017;2017:2823454.
   PubMed Web of Science ®Google Scholar
• Knutson N, Wood CE. Interaction of PGHS-2 and glutamatergic mechanisms controlling the ovine fetal hypothalamus-pituitary-adrenal axis. Am J Physiol Regul Integr Comp Physiol. 2010 Jul;299(1):R365–70.
   PubMed Web of Science ®Google Scholar
• Ichikawa M, Muramoto K, Kobayashi K, Kawahara M, Kuroda Y. Formation and maturation of synapses in primary cultures of rat cerebral cortical cells: an electron microscopic study. Neurosci Res. 1993 Feb;16(2):95–103.
   PubMed Web of Science ®Google Scholar
• Schubert D, Piasecki D. Oxidative glutamate toxicity can be a component of the excitotoxicity cascade. J Neurosci. 2001 Oct 1;21(19):7455–62.
   PubMed Web of Science ®Google Scholar
• France G, Fernandez-Fernandez D, Burnell ES, Irvine MW, Monaghan DT, Jane DE, et al. Multiple roles of GluN2B-containing NMDA receptors in synaptic plasticity in juvenile hippocampus. Neuropharmacology. 2017 Jan;112(Pt A):76–83.
   PubMedGoogle Scholar
• Xiao L, Hu C, Feng C, Chen Y. Switching of N-methyl-D-aspartate (NMDA) receptor-favorite intracellular signal pathways from ERK1/2 protein to p38 mitogen-activated protein kinase leads to developmental changes in NMDA neurotoxicity. J Biol Chem. 2011 Jun 10;286(23):20175–93.
   PubMed Web of Science ®Google Scholar
• Sinor JD, Du S, Venneti S, Blitzblau RC, Leszkiewicz DN, Rosenberg PA, et al. NMDA and glutamate evoke excitotoxicity at distinct cellular locations in rat cortical neurons in vitro. J Neurosci. 2000 Dec 1;20(23):8831–7.
   PubMed Web of Science ®Google Scholar
• Wang YJ, Chan MH, Chen L, Wu SN, Chen HH. Resveratrol attenuates cortical neuron activity: roles of large conductance calcium-activated potassium channels and voltage-gated sodium channels. J Biomed Sci. 2016 May 21;23(1):47.
   PubMedGoogle Scholar
• McCalley AE, Kaja S, Payne AJ, Koulen P. Resveratrol and calcium signaling: molecular mechanisms and clinical relevance. Molecules. 2014 Jun 5;19(6):7327–40.
   PubMed Web of Science ®Google Scholar
• Stanika RI, Villanueva I, Kazanina G, Andrews SB, Pivovarova NB. Comparative impact of voltage-gated calcium channels and NMDA receptors on mitochondria-mediated neuronal injury. J Neurosci. 2012 May 9;32(19):6642–50.
   PubMed Web of Science ®Google Scholar
• Carrasco-Pozo C, Pastene E, Vergara C, Zapata M, Sandoval C, Gotteland M. Stimulation of cytosolic and mitochondrial calcium mobilization by indomethacin in Caco-2 cells: modulation by the polyphenols quercetin, resveratrol and rutin. Biochim Biophys Acta. 2012 Dec;1820(12):2052–61.
   PubMed Web of Science ®Google Scholar
• Adamusova E, Cais O, Vyklicky V, Kudova E, Chodounska H, Horak M, et al. Pregnenolone sulfate activates NMDA receptor channels. Physiol Res. 2013;62(6):731–6.
   PubMed Web of Science ®Google Scholar
• Domingues AM, Neugebauer KM, Fern R. Identification of four functional NR3B isoforms in developing white matter reveals unexpected diversity among glutamate receptors. J Neurochem. 2011 May;117(3):449–60.
   PubMed Web of Science ®Google Scholar
• Li JH, Wang YH, Wolfe BB, Krueger KE, Corsi L, Stocca G, et al. Developmental changes in localization of NMDA receptor subunits in primary cultures of cortical neurons. Eur J Neurosci. 1998 May;10(5):1704–15.
   PubMed Web of Science ®Google Scholar
• Ruiz A, Matute C, Alberdi E. Endoplasmic reticulum Ca(2+) release through ryanodine and IP(3) receptors contributes to neuronal excitotoxicity. Cell Calcium. 2009 Oct;46(4):273–81.
   PubMed Web of Science ®Google Scholar
• Genazzani AA, Carafoli E, Guerini D. Calcineurin controls inositol 1,4,5-trisphosphate type 1 receptor expression in neurons. Proc Natl Acad Sci U S A. 1999 May 11;96(10):5797–801.
   PubMed Web of Science ®Google Scholar
• Wayman GA, Yang D, Bose DD, Lesiak A, Ledoux V, Bruun D, et al. PCB-95 promotes dendritic growth via ryanodine receptor-dependent mechanisms. Environ Health Perspect. 2012 Jul;120(7):997–1002.
   PubMed Web of Science ®Google Scholar
• Chazot PL. The NMDA receptor NR2B subunit: a valid therapeutic target for multiple CNS pathologies. Curr Med Chem. 2004 Feb;11(3):389–96.
   PubMed Web of Science ®Google Scholar
• deBacker J, Hawken ER, Normandeau CP, Jones AA, Di Prospero C, Mechefske E, et al. GluN2B-containing NMDA receptors blockade rescues bidirectional synaptic plasticity in the bed nucleus of the stria terminalis of cocaine self-administering rats. Neuropsychopharmacology. 2015 Jan;40(2):394–405.
   PubMed Web of Science ®Google Scholar
• Wang J, Carnicella S, Phamluong K, Jeanblanc J, Ronesi JA, Chaudhri N, et al. Ethanol induces long-term facilitation of NR2B-NMDA receptor activity in the dorsal striatum: implications for alcohol drinking behavior. J Neurosci. 2007 Mar 28;27(13):3593–602.
   PubMed Web of Science ®Google Scholar
• Robb EL, Stuart JA. trans-Resveratrol as a neuroprotectant. Molecules. 2010 Mar 3;15(3):1196–212.
   PubMed Web of Science ®Google Scholar
• Tao L, Ding Q, Gao C, Sun X. Resveratrol attenuates neuropathic pain through balancing pro-inflammatory and anti-inflammatory cytokines release in mice. Int Immunopharmacol. 2016 May;34:165–72.
   PubMed Web of Science ®Google Scholar
• Ramage L, Martel MA, Hardingham GE, Salter DM. NMDA receptor expression and activity in osteoarthritic human articular chondrocytes. Osteoarthritis Cartilage. 2008 Dec;16(12):1576–84.
   PubMed Web of Science ®Google Scholar
• Marouf BH, Hussain SA, Ali ZS, Ahmmad RS. Resveratrol supplementation reduces pain and inflammation in knee osteoarthritis patients treated with Meloxicam: A randomized placebo-controlled study. J Med Food. 2018 Aug 30;21(12):1253–59.
   Web of Science ®Google Scholar
• Imamura Y, Yoshikawa N, Murkami Y, Mitani S, Matsumoto N, Matsumoto H, et al. Effect of histone acetylation on N-methyl-D-aspartate 2B receptor subunits and interleukin-1 receptors in association with nociception-related somatosensory cortex dysfunction in a mouse model of sepsis. Shock. 2016 Jun;45(6):660–7.
   PubMed Web of Science ®Google Scholar
• Guthmann A, Herbert H. Expression of N-methyl-D-aspartate receptor subunits in the rat parabrachial and Kolliker-Fuse nuclei and in selected pontomedullary brainstem nuclei. J Comp Neurol. 1999 Dec 27;415(4):501–17.
   PubMed Web of Science ®Google Scholar
• Wang R, Zhang Y, Li J, Zhang C. Resveratrol ameliorates spatial learning memory impairment induced by Abeta1-42 in rats. Neuroscience. 2017 Mar 6;344:39–47.
   PubMed Web of Science ®Google Scholar
• Bartlett TE, Bannister NJ, Collett VJ, Dargan SL, Massey PV, Bortolotto ZA, et al. Differential roles of NR2A and NR2B-containing NMDA receptors in LTP and LTD in the CA1 region of two-week old rat hippocampus. Neuropharmacology. 2007 Jan;52(1):60–70.
   PubMed Web of Science ®Google Scholar
• Berberich S, Punnakkal P, Jensen V, Pawlak V, Seeburg PH, Hvalby O, et al. Lack of NMDA receptor subtype selectivity for hippocampal long-term potentiation. J Neurosci. 2005 Jul 20;25(29):6907–10.
   PubMed Web of Science ®Google Scholar
• Shipton OA, Paulsen O. Glun2a and GluN2B subunit-containing NMDA receptors in hippocampal plasticity. Philos Trans R Soc Lond B Biol Sci. 2014 Jan 5;369(1633):20130163.
   PubMed Web of Science ®Google Scholar
• Foster TC. Involvement of hippocampal synaptic plasticity in age-related memory decline. Brain Res Brain Res Rev. 1999 Nov;30(3):236–49.
   PubMedGoogle Scholar
• Malenka RC, Bear MF. LTP and LTD: an embarrassment of riches. Neuron. 2004 Sep 30;44(1):5–21.
   PubMed Web of Science ®Google Scholar
• Zhang F, Liu J, Shi JS. Anti-inflammatory activities of resveratrol in the brain: role of resveratrol in microglial activation. Eur J Pharmacol. 2010 Jun 25;636(1–3):1–7.
   PubMed Web of Science ®Google Scholar
• Wang Q, Xu J, Rottinghaus GE, Simonyi A, Lubahn D, Sun GY, et al. Resveratrol protects against global cerebral ischemic injury in gerbils. Brain Res. 2002 Dec 27;958(2):439–47.
   PubMed Web of Science ®Google Scholar
• Kennedy DO, Wightman EL, Reay JL, Lietz G, Okello EJ, Wilde A, et al. Effects of resveratrol on cerebral blood flow variables and cognitive performance in humans: a double-blind, placebo-controlled, crossover investigation. Am J Clin Nutr. 2010 Jun;91(6):1590–7.
   PubMed Web of Science ®Google Scholar
• Almeida L, Vaz-da-Silva M, Falcao A, Soares E, Costa R, Loureiro AI, et al. Pharmacokinetic and safety profile of trans-resveratrol in a rising multiple-dose study in healthy volunteers. Mol Nutr Food Res. 2009 May;53(Suppl 1):S7–15.
   PubMedGoogle Scholar