Resveratrol prevents CA1 neurons against ischemic injury by parallel modulation of both GSK-3β and CREB through PI3-K/Akt pathways

European Journal of Neuroscience

Volumn 36, Issue 7, 2012, Pages 2899-2905

  Simão, Fabrício ^a   Matté, Aline ^a   Pagnussat, Aline S ^a   Netto, Carlos A ^a   Salbego, Christianne G ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

Cerebral ischemia; CREB; GSK 3 ; Neuroprotection; PI3 K Akt; Resveratrol

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RESVERATROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN ISCHEMIA; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; DRUG TARGETING; EXPERIMENTAL RAT; HIPPOCAMPAL CA1 REGION; MALE; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; REPERFUSION INJURY; SIGNAL TRANSDUCTION; SURVIVAL RATE;

ANIMALS; APOPTOSIS; BRAIN ISCHEMIA; CA1 REGION, HIPPOCAMPAL; CHROMONES; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; GLYCOGEN SYNTHASE KINASE 3; MALE; MORPHOLINES; NEURONS; NEUROPROTECTIVE AGENTS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; REPERFUSION INJURY; SIGNAL TRANSDUCTION; STILBENES;

EID: 84867029736     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2012.08229.x     Document Type: Article

References (44)

1. Birrell, M.A., McCluskie, K., Wong, S.S., Donnelly, L.E., Barnes, P.J. & Belvisi, M.G. (2005) Resveratrol, an extract of red wine, inhibits lipopolysaccharide induced airway neutrophilia and inflammatory mediators through an NF-kappa B-independent mechanism. FASEB J., 19, 840-841.
2. Chen, C.Y., Jang, J.H., Li, M.H. & Surh, Y.J. (2005) Resveratrol upregulates heme oxygenase-1 expression via activation of NF-E2-related factor 2 in PC12 cells. Biochem. Biophys. Res. Commun., 331, 993-1000.
3. Das, S., Cordis, G.A., Maulik, N. & Das, D.K. (2005a) Pharmacological preconditioning with resveratrol: role of CREB-dependent Bcl-2 signaling via adenosine A3 receptor activation. Am. J. Physiol., 288, H328-H335.
4. Das, S., Tosaki, A., Bagchi, D., Maulik, N. & Das, D.K. (2005b) Resveratrol-mediated activation of cAMP response element-binding protein through adenosine A3 receptor by Akt- dependent and -independent pathways. J. Pharmacol. Exp. Ther., 314, 762-769.
5. Das, S., Fraga, C.G. & Das, D.K. (2006a) Cardioprotective effect of resveratrol via HO-1 expression involves p38 map kinase and PI-3-kinase signaling, but does not involve NFkappaB. Free Radic. Res., 40, 1066-1075.
6. Das, S., Tosaki, A., Bagchi, D., Maulik, N. & Das, D.K. (2006b) Potentiation of a survival signal in the ischemic heart by resveratrol through p38 mitogen-activated protein kinase/mitogen- and stress-activated protein kinase 1/cAMP response element-binding protein signaling. J. Pharmacol. Exp. Ther., 317, 980-988.
7. Della-Morte, D., Dave, K.R., Defazio, R.A., Bao, Y.C., Raval, A.P. & Perez-Pinzon, M.A. (2009) Resveratrol pretreatment protects rat brain from cerebral ischemic damage via a sirtuin 1-uncoupling protein 2 pathway. Neuroscience, 159, 993-02.
8. Delmas, D., Jannin, B. & Latruffe, N. (2005) Resveratrol: preventing properties against vascular alterations and ageing. Mol. Nutr. Food Res., 49, 377-395.
9. Dong, W., Li, N., Gao, D., Zhen, H., Zhang, X. & Li, F. (2008) Resveratrol attenuates ischemic brain damage in the delayed phase after stroke and induces messenger RNA and protein express for angiogenic factors. J. Vasc. Surg., 48, 709-714.
10. Du, K. & Montminy, M. (1998) CREB is a regulatory target for the protein kinase Akt/PKB. J. Biol. Chem., 273, 32377-32379.
11. Fukui, M., Choi, H.J. & Zhu, B.T. (2010) Mechanism for the protective effect of resveratrol against oxidative stress-induced neuronal death. Free Radic. Biol. Med., 49, 800-813.
12. Gao, D., Zhang, X. & Jiang, X. (2006a) Resveratrol reduces the elevated level of MMP-9 induced by cerebral ischemia-reperfusion in mice. Life Sci., 78, 2564-2570.
13. Gao, Z.B., Chen, X.Q. & Hu, G.Y. (2006b) Inhibition of excitatory synaptic transmission by trans-resveratrol in rat hippocampus. Brain Res., 1111, 41-47.
14. Grimes, C.A. & Jope, R.S. (2001) The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Prog. Neurobiol., 65, 391-426.
15. Han, Y.S., Bastianetto, S., Dumont, Y. & Quirion, R. (2006) Specific plasma membrane binding sites for polyphenols, including resveratrol, in the rat brain. J. Pharmacol. Exp. Ther., 318, 238-245.
16. Hattori, R., Otani, H., Maulik, N. & Das, D.K. (2002) Pharmacological preconditioning with resveratrol: role of nitric oxide. Am. J. Physiol., 282, H1988-H1995.
17. Huang, S.S., Tsai, M.C., Chih, C.L., Hung, L.M. & Tsai, S.K. (2001) Resveratrol reduction of infarct size in Long-Evans rats subjected to focal cerebral ischemia. Life Sci., 69, 1057-1065.
18. Hung, L.M., Su, M.J. & Chen, J.K. (2004) Resveratrol protects myocardial ischemia- reperfusion injury through both NO-dependent and NO-independent mechanisms. Free Radic. Biol. Med., 36, 774-781.
19. Imamura, G., Bertelli, A.A., Bertelli, A., Otani, H., Maulik, N. & Das, D.K. (2002) Pharmacological preconditioning with resveratrol: an insight with iNOS knockout mice. Am. J. Physiol., 282, H1996-H2003.
20. Jin, K., Mao, X.O., Batteur, S.P., Mceachron, E., Leahy, A. & Greenberg, D.A. (2001) Caspase-3 and the regulation of hypoxic neuronal death by vascular endothelial growth factor. Neuroscience, 108, 351-358.
21. Jope, R.S. & Johnson, G.V. (2004) The glamour and gloom of glycogen synthase kinase-3. Trends Biochem. Sci., 29, 95-102.
22. Kelly, S., Zhao, H., Hua Sun, G., Cheng, D., Qiao, Y., Luo, J., Martin, K., Steinberg, G.K., Harrison, S.D. & Yenari, M.A. (2004) Glycogen synthase kinase 3beta inhibitor Chir025 reduces neuronal death resulting from oxygen-glucose deprivation, glutamate excitotoxicity, and cerebral ischemia. Exp. Neurol., 188, 378-386.
23. Kiziltepe, U., Turan, N.N., Han, U., Ulus, A.T. & Akar, F. (2004) Resveratrol, a red wine polyphenol, protects spinal cord from ischemia-reperfusion injury. J. Vasc. Surg., 40, 138-145.
24. Lastra, C.A. & Villegas, I. (2005) Resveratrol as an anti-inflammatory and anti-aging agent: mechanisms and clinical implications. Mol. Nutr. Food Res., 49, 405-430.
25. Lu, K.T., Chiou, R.Y.Y., Chen, L.G., Chen, M.H., Tseng, W.T., Hsieh, H.T. & Yang, Y.L. (2006) Neuroprotective effects of resveratrol on cerebral ischemia-induced neuron loss mediated by free radical scavenging and cerebral blood flow elevation. J. Agric. Food Chem., 54, 3126-3131.
26. Noshita, N., Lewen, A., Sugawara, T. & Chan, P.H. (2001) Evidence of phosphorylaiton of Akt and neuronal survival after transient focal cerebral ischemia in mice. J. Cereb. Blood Flow Metab., 21, 1442-1450.
27. Pallàs, M., Casadesús, G., Smith, M.A., Coto-Montes, A., Pelegri, C., Vilaplana, J. & Camins, A. (2009) Resveratrol and neurodegenerative diseases: activation of SIRT1 as the potential pathway towards neuroprotection. Curr. Neurovasc. Res., 6, 70-81.
28. Raval, A.P., Dave, K.R. & Pérez-Pinzón, M.A. (2006) Resveratrol mimics ischemic preconditioning in the brain. J. Cereb. Blood Flow Metab., 26, 1141-1147.
29. Shaywitz, A.J. & Greenberg, M.E. (1999) CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu. Rev. Biochem., 68, 821-861.
30. Shibata, M., Yamawaki, T., Sasaki, T., Hattori, H., Hamada, J., Fukuuchi, Y., Okano, H. & Miura, M. (2002) Upregulation of Akt phosphoryaltion at the early stage of middle cerebral artery occlusion in mice. Brain Res., 942, 1-10.
31. Shigematsu, S., Ishida, S., Hara, M., Takahashi, N., Yoshimatsu, H. & Sakata, T. (2003) Resveratrol, a red wine constituent polyphenol, prevents superoxide-dependent inflammatory responses induced by ischemia/reperfusion, platelet-activating factor, or oxidants. Free Radic. Biol. Med., 34, 810-817.
32. Shin, J.A., Lee, H., Lim, Y.K., Koh, Y., Choi, J.H. & Park, E.M. (2010) Therapeutic effects of resveratrol during acute periods following experimental ischemic stroke. J. Neuroimmunol., 227, 93-100.
33. +, -ATPase activity induced by transient global cerebral ischemia in rats. J. Nutr. Biochem., 22, 921-928.
34. Simão, F., Pagnussat, A.S., Seo, J.H., Navaratna, D., Leung, W., Lok, J., Guo, S., Waeber, C., Salbego, C.G. & Lo, E.H. (2012) Pro-angiogenic effects of resveratrol in brain endothelial cells: nitric oxide-mediated regulation of vascular endothelial growth factor and metalloproteinases. J. Cereb. Blood Flow Metab., 32, 884-895.
35. Sinha, K., Chaudhary, G. & Gupta, Y.K. (2002) Protective effect of resveratrol against oxidative stress in middle cerebral artery occlusion model of stroke in rats. Life Sci., 71, 655-665.
36. Walton, M.R. & Dragunow, I. (2000) Is CREB a key to neuronal survival?Trends Neurosci., 23, 48-53.
37. Wang, Q., Xu, J.F., Rottinghaus, G.E., Simonyi, A., Lubahn, D., Sun, G.Y. & Sun, A.Y. (2002) Resveratrol protects against global cerebral ischemic injury in gerbils. Brain Res., 958, 439-447.
38. Wood, J.G., Rogina, B., Lavu, S., Howitz, K., Helfand, S.L., Tatar, M. & Sinclair, D. (2004) Sirtuin activators mimic caloric restriction and delay ageing in metazoans. Nature, 430, 686-689.
39. Yang, J., Marden, J.J., Fan, C., Sanlioglu, S., Weiss, R.M., Ritchie, T.C., Davisson, R.L. & Engelhardt, J.F. (2003) Genetic redox preconditioning differentially modulates AP-1 and NF kappa B responses following cardiac ischemia/reperfusion injury and protects against necrosis and apoptosis. Mol. Ther., 7, 341-353.
40. Yang, L.C., Zhang, Q.G., Zhou, C.F., Yang, F., Zhang, Y.D., Wang, R.M. & Brann, D.W. (2010) Extranuclear estrogen receptors mediate the neuroprotective effects of estrogen in the rat hippocampus. PLoS One, 5, 9851.
41. Yano, S., Morioka, M., Fukunaga, K., Kawano, T., Hara, T., Kai, Y., Hamada, J., Miyamoto, E. & Ushio, Y. (2001) Activation of Akt/protein kinase B contributes to induction of ischemic tolerance in the CA1 subfield of gerbil hippocampus. J. Cereb. Blood Flow Metab., 21, 351-360.
42. Zamin, L.L., Dillenburg-Pilla, P., Argenta-Comiran, R., Horn, A.P., Simão, F., Nassif, M., Gerhardt, D., Frozza, R.L. & Salbego, C. (2006) Protective effect of resveratrol against oxygen-glucose deprivation in organotypic hippocampal slice cultures: involvement of PI3-K pathway. Neurobiol. Dis., 24, 170-182.
43. Zhang, F., Yin, W. & Chen, J. (2004) Apoptosis in cerebral ischemia: executional and regulatory signaling mechanisms. Neurol. Res., 26, 835-845.
44. Zhang, F., Signore, A.P., Zhou, Z., Wang, S., Cao, G. & Chen, J. (2006) Erythropoietin protects CA1 neurons against global cerebral ischemia in rat. J. Neurosci. Res., 83, 1241-1251.