Resveratrol protects CA1 neurons against focal cerebral ischemic reperfusion-induced damage via the ERK-CREB signaling pathway in rats

Pharmacology Biochemistry and Behavior

Volumn 146-147, Issue , 2016, Pages 21-27

  Li, Zhen ^a   Fang, Fang ^a   Wang, Yuanyin ^a   Wang, Liecheng ^a  

^a ANHUI MEDICAL UNIVERSITY   (China)

Author keywords

Cell signaling; Cerebral ischemia; Hippocampus; Learning and memory; Neuroprotection; Resveratrol

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DIZOCILPINE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NEUROPROTECTIVE AGENT; RESVERATROL; 1,3 BUTADIENE DERIVATIVE; DIZOCILPINE MALEATE; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRILE; STILBENE DERIVATIVE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; BRAIN NERVE CELL; CELL DEATH; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; EXPERIMENTAL COGNITIVE DEFECT; HIPPOCAMPAL CA1 REGION; MALE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; REPERFUSION INJURY; SIGNAL TRANSDUCTION; SINGLE DRUG DOSE; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; CEREBRAL INFARCTION; COGNITION; COGNITIVE DYSFUNCTION; COMPLICATION; DRUG EFFECTS; MEMORY; METABOLISM; NERVE CELL; PATHOLOGY; PHOSPHORYLATION;

ANIMALS; BUTADIENES; CA1 REGION, HIPPOCAMPAL; CELL DEATH; CEREBRAL INFARCTION; COGNITION; COGNITIVE DYSFUNCTION; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DIZOCILPINE MALEATE; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; MALE; MEMORY; NEURONS; NEUROPROTECTIVE AGENTS; NITRILES; PHOSPHORYLATION; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; REPERFUSION INJURY; SIGNAL TRANSDUCTION; STILBENES;

EID: 84966270825     PISSN: 00913057     EISSN: 18735177     Source Type: Journal    
DOI: 10.1016/j.pbb.2016.04.007     Document Type: Article

References (55)

1. S.A. Abd El-Aal, M.M. El-Sawalhi, M. Seif-El-Nasr, and S.A. Kenawy Effect of celecoxib and L-NAME on global ischemia-reperfusion injury in the rat hippocampus Drug Chem. Toxicol. 36 2013 385 395
2. J.Y. Ban, S.O. Cho, S.H. Choi, H.S. Ju, J.Y. Kim, K. Bae, K.S. Song, and Y.H. Seong Neuroprotective effect of Smilacis chinae rhizome on NMDA induced neurotoxicity in vitro and focal cerebral ischemia in vivo J. Pharmacol. Sci. 106 2008 68 77
3. Y. Banno, S. Nemoto, M. Murakami, M. Kimura, Y. Ueno, K. Ohguchi, A. Hara, Y. Okano, Y. Kitade, M. Onozuka, T. Murate, and Y. Nozawa Depolarization-induced differentiation of PC12 cells is mediated by phospholipase D2 through the transcription factor CREB pathway J. Neurochem. 104 2008 1372 1386
4. 2 + signals and neuronal death in brain ischemia Stroke 38 2007 674 676
5. F. Block Global ischemia and behavioural deficits Prog. Neurobiol. 58 1999 279 295
6. M.J. Boucher, J. Morisset, P.H. Vachon, J.C. Reed, J. Lainé, and N. Rivard MEK/ERK signaling pathway regulates the expression of Bcl-2, Bcl-x(L), and Mcl-1 and promotes survival of human pancreatic cells J. Cell. Biochem. 79 2000 355 369
7. W. Cai, Y. Zhu, K. Furuya, Z. Li, M. Sokabe, and L. Chen Two different molecular mechanisms underlying progesterone neuroprotective against ischemic brain damage Neuropharmacology 55 2008 127 138
8. D. Castañeda, H. Zhao, D. Mochly-Rosen, and G.K. Steinberg Activating delta PKC antagonizes the protective effect of ERK1/2 inhibition against stroke in rats Brain Res. 1251 2009 1256 1261
9. Y. Chang, and S.J. Wang Inhibitory effect of glutamate release from rat cerebrocortical nerve terminals by resveratrol Neurochem. Int. 54 2009 135 141
10. L. Chen, Y. Miyamoto, K. Furuya, N. Mori, and M. Sokabe PREGS induces LTP in the hippocampal dentate gyrus of adult rats via the tyrosine phosphorylation international cooperative research CREB signaling J. Neurophysiol. 98 3 2007 1538 1548
11. D.W. Choi Glutamate toxicity and diseases of the nervous system Neuron 1 1988 623 634
12. J.A. Crowell, P.J. Korytko, R.L. Morrissey, T.D. Booth, and B.S. Levine Resveratrol-associated renal toxicity Toxicol. Sci. 82 2004 614 619
13. D. Della-Morte, K.R. Dave, R.A. DeFazio, Y.C. Bao, A.P. Raval, and M.A. Perez-Pinzon Resveratrol pretreatment protects rat brain from cerebral ischemic damage via a sirtuin 1-uncoupling protein 2 pathway Neuroscience 159 2009 993 1002
14. D. Delmas, B. Jannin, and N. Latruffe Resveratrol: preventing properties against vascular alterations and ageing Mol. Nutr. Food Res. 49 2005 377 395
15. G.A. Donnan, M. Fisher, M. Macleod, and S.M. Davis Stroke. Lancet. 371 2008 1612 1623
16. U.B. Eyo, J. Peng, P. Swiatkowski, A. Mukherjee, A. Bispo, and L.J. Wu Neuronal hyperactivity recruits microglial processed via neuronal NMDA receptors and microglial P2Y12 receptors after status epilepticus J. Neurosci. 34 2014 10528 10540
17. Q.H. Guan, D.S. Pei, X.M. Liu, X.T. Wang, T.L. Xu, and G.Y. Zhang Neuroprotection against ischemic brain injury by SP600125 via suppressing the extrinsic and intrinsic pathways of apoptosis Brain Res. 1092 2006 36 46
18. N. Howard-Jones A CIOMS ethical code for animal experimentation WHO Chron. 39 1985 51 56
19. M.B. Jørgensen, and N.H. Diemer Selective neuron loss after cerebral ischemia in the rat: possible role of transmitter glutamate Acta Neurol. Scand. 66 1982 536 546
20. T. Jover-Mengual, R.S. Zukin, and A.M. Etgen MAPK signaling is critical to estradiol protection of CA1 neurons in global ischemia Endocrinology 148 2007 1131 1143
21. K. Kitagawa, M. Matsumoto, T. Mabuchi, Y. Yagita, K. Mandai, K. Matsushita, M. Hori, and T. Yanagihara Ischemic tolerance in hippocampal CA1 neurons studied using contralateral controls Neuroscience 81 1997 989 998
22. Z. Li, S. Cui, Z. Zhang, Q. Xie, W. Cai, M. Sokabe, and L. Chen DHEA-neuroprotection and -neurotoxicity after transient cerebral ischemia in rats J. Cereb. Blood Flow Metab. 29 2009 287 296
23. Z. Li, L. Pang, F. Fang, G. Zhang, J. Zhang, M. Xie, and L.C. Wang Resveratrol attenuates brain damage in a rat model of focal cerebral ischemia via up-regulation of hippocampal Bcl-2 Brain Res. 1450 2012 116 124
24. H. Li, Z. Yan, J. Zhu, J. Yang, and J. He Neuroprotective effects of resveratrol on ischemic injury mediated by improving brain energy metabolism and alleviating oxidative stress in rats Neuropharmacology 60 2011 252 258
25. 2 + influx of NMDA receptors Int. J. Neuropsychopharmacol. 15 2012 497 507
26. C.H. Lin, P.S. Chen, and P.W. Gean Glutamate preconditioning prevents neuronal death induced by combined oxygen-glucose deprivation in cultured cortical neurons Eur. J. Pharmacol. 589 2008 85 93
27. Y. Lin, F. Chen, J. Zhang, T. Wang, X. Wei, J. Wu, Y. Feng, Z. Dai, and Q. Wu Neuroprotective effect of resveratrol on ischemia/reperfusion injury in rats through TRPC6/CREB pathways J. Mol. Neurosci. 50 2013 504 513
28. D. Liu, Q. Zhang, J. Gu, X. Wang, K. Xie, X. Xian, J. Wang, H. Jiang, and Z. Wang Resveratrol prevents impaired cognition induced by chronic unpredictable mild stress in rats Prog. Neuro-Psychopharmacol. Biol. Psychiatry 49 2014 21 29
29. A.M. Marini, X. Jiang, X. Wu, H. Pan, Z. Guo, M.P. Mattson, N. Blondeau, A. Novelli, and R.H. Lipsky Preconditioning and neurotrophins: a model for brain adaptation to seizures, ischemia and other stressful stimuli Amino Acids 32 2007 299 304
30. R. Morris Developments of a water-maze procedure for studying spatial learning in the rat J. Neurosci. Methods 11 1984 47 60
31. N.J. Mulcahy, J. Ross, N.J. Rothwell, and S.A. Loddick Delayed administration of interleukin-1 receptor antagonist protects against transient cerebral ischemia in the rat Br. J. Pharmacol. 140 2003 471 476
32. S.V. Narayanan, K.R. Dave, I. Saul, and M.A. Perez-Pinzon Resveratrol preconditioning protects against cerebral ischemic injury via nuclear erythroid 2-related factor 2 Stroke 46 2015 1626 1632
33. M. Niimura, N. Takagi, K. Takagi, H. Funakoshi, T. Nakamura, and S. Takeo Effects of hepatocyte growth factor on phosphorylation of extracellular signal-regulated kinase and hippocampal cell death in rats with transient forebrain ischemia Eur. J. Pharmacol. 535 2006 114 124
34. M. Ninomiya, T. Numakawa, N. Adachi, M. Furuta, S. Chiba, M. Richards, S. Shibata, and H. Kunugi Cortical neurons from intrauterine growth retardation rats exhibit lower response to neurotrophin BDNF Neurosci. Lett. 476 2010 104 109
35. P. Orsu, B.V. Murthy, and A. Akula Cerebroprotective potential of resveratrol through anti-oxidant and anti-inflammatory mechanisms in rats J. Neural Transm. 120 2013 1217 1223
36. H. Ozawa, S. Shioda, K. Dohi, H. Matsumoto, H. Mizushima, C.J. Zhou, H. Funahashi, Y. Nakai, S. Nakajo, and K. Matsumoto Delayed neuronal cell death in the rat hippocampus is mediated by the mitogen-activated protein kinase signal transduction pathway Neurosci. Lett. 262 1999 57 60
37. S.T. Pendlebury, and P.M. Rothwell Prevalence, incidence, and factors associated with pre-stroke and post-stroke dementia: a systematic review and meta-analysis Lancet Neurol. 8 2009 1006 1018
38. M.A. Pérez-Pinzón Neuroprotective effects of ischemic preconditioning in brain mitochondria following cerebral ischemia J. Bioenerg. Biomembr. 36 2004 323 327
39. A.P. Raval, K.R. Dave, and M.A. Pérez-Pinzón Resveratrol mimics ischemic preconditioning in the brain J. Cereb. Blood Flow Metab. 26 2006 1141 1147
40. A.P. Raval, I. Saul, K.R. Dave, R.A. DeFazio, M.A. Pérez-Pinzón, and H. Bramlett Pretreatment with a single estradiol-17beta bolus activates cyclic-AMP response element binding protein and protects CA1 neurons against global cerebral ischemia Neuroscience 160 2009 307 318
41. M.C. Saleh, B.J. Connell, and T.M. Saleh Resveratrol preconditioning induces cellular stress proteins and is mediated via NMDA and estrogen receptors Neuroscience 166 2010 445 454
42. A.K. Shetty Promise of resveratrol for easing status epilepticus and epilepsy Pharmacol. Ther. 131 2011 269 286
43. A. Shuaib, and M.S. Hussain The past and future of neuroprotection in cerebral ischaemic stroke Eur. Neurol. 59 2008 4 14
44. F. Simão, A. Matté, A.S. Pagnussat, C.A. Netto, and C.G. Salbego Resveratrol prevents CA1 neurons against ischemic injury by parallel modulation of both GSK-3β and CREB through PI3-K/Akt pathways Eur. J. Neurosci. 36 2012 2899 2905
45. 2 +-stimulated adenylyl cyclases regulate ERK-dependent activation of MSK1 during fear conditioning Neuron 53 2007 79 89
46. N. Singh, M. Agrawal, and S. Doré Neuroprotective properties and mechanisms of resveratrol in in vitro and in vivo experimental cerebral stroke models ACS Chem. Neurosci. 4 2013 1151 1162
47. J.M. Smoliga, J.A. Baur, and H.A. Hausenblas Resveratrol and health-a comprehensive review of human clinical trials Mol. Nutr. Food Res. 55 2011 1129 1141
48. K. Tanaka, S. Nogawa, E. Nagata, D. Ito, S. Suzuki, T. Dembo, A. Kosakai, and Y. Fukuuchi Persistent CREB phosphorylation with protection of hippocampal CA1 pyramidal neurons following temporary occlusion of the middle cerebral artery in the rat Exp. Neurol. 161 2000 462 471
49. R.Y. Tsai, K.Y. Chou, C.H. Shen, C.C. Chien, W.Y. Tsai, Y.N. Huang, P.L. Tao, Y.S. Lin, and C.S. Wong Resveratrol regulates N-methyl-d-aspartate receptor expression and suppresses neuroinflammation in morphine-tolerant rats Anesth. Analg. 115 2012 944 952
50. R.M. Wang, F. Yang, and Y.X. Zhang Preconditioning-induced activation of ERK5 is dependent on moderate Ca2 + influx via NMDA receptors and contributes to ischemic tolerance in the hippocampal CA1 region of rats Life Sci. 79 2006 1839 1846
51. E.J. Weeber, and J.D. Sweatt Molecular neurobiology of human cognition Neuron 33 2002 845 848
52. L.J. Wu, G. Wu, M.R. Akhavan Sharif, A. Baker, Y. Jia, F.H. Fahey, H.R. Luo, E.P. Feener, and D.E. Clapham The voltage-gated proton channel Hv1 enhances brain damage from ischemic stroke Nat. Neurosci. 15 2012 565 573
53. L. Zhan, H. Yan, H. Zhou, W. Sun, Q. Hou, and E. Xu Hypoxic preconditioning attenuates neuronal cell death by preventing MEK/ERK signaling pathway activation after transient global cerebral ischemia in adult rats Mol. Neurobiol. 48 2013 109 119
54. H. Zhang, G.P. Schools, T. Lei, W. Wang, H.K. Kimelberg, and M. Zhou Resveratrol attenuates early pyramidal neuron excitability impairment and death in acute rat hippocampal slices caused by oxygen-glucose deprivation Exp. Neurol. 212 2008 44 52
55. Y.M. Zhu, C.C. Wang, L. Chen, L.B. Qian, L.L. Ma, J. Yu, M.H. Zhu, C.Y. Wen, L.N. Yu, and M. Yan Both PI3K/Akt and ERK1/2 pathways participate in the protection by dexmedetomidine against transient focal cerebral ischemia/reperfusion injury in rats Brain Res. 1494 2013 1 8