Neuroprotective effects of resveratrol against β-amyloid-induced neurotoxicity in rat hippocampal neurons: Involvement of protein kinase C

British Journal of Pharmacology

Volumn 141, Issue 6, 2004, Pages 997-1005

  Han, Ying Shan ^a   Zheng, Wen Hua ^a   Bastianetto, Stéphane ^a   Chabot, Jean Guy ^a   Quirion, Rémi ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

amyloid; Hippocampus; Neuroprotection; Red wine extracts; Resveratrol; Signal transduction pathway

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4ALPHA PHORBOL; AMYLOID BETA PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; NEUROPROTECTIVE AGENT; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE C; PROTEIN KINASE C ACTIVATOR; PROTEIN KINASE C INHIBITOR; RESVERATROL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; DRUG SCREENING; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FEMALE; FETUS; HIPPOCAMPUS; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION;

AMYLOID BETA-PROTEIN; ANIMALS; BLOTTING, WESTERN; CELL SURVIVAL; CELLS, CULTURED; CYTOTOXINS; ENZYME ACTIVATION; FEMALE; HIPPOCAMPUS; NEURONS; NEUROPROTECTIVE AGENTS; PEPTIDE FRAGMENTS; PREGNANCY; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; STILBENES;

EID: 1942472491     PISSN: 00071188     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjp.0705688     Document Type: Article

References (45)

1. BASTIANETTO, S., RAMASSAMY, C., POIRIER, J. & QUIRION, R. (1999). Dehydroepiandrosterone (DHEA) protects hippocampal cells from oxidative stress-induced damage. Mol. Brain Res., 66, 35-41.
2. BASTIANETTO, S., RAMASSAMY, C., DORE, S., CHRISTEN, Y., POIRIER, J. & QUIRION, R. (2000). The Ginkgo biloba extract (EGb 761) protects hippocampal neurons against cell death induced by beta-amyloid. Eur. J. Neurosci., 12, 1882-1890.
3. BASTIANETTO, S. & QUIRION, R. (2001). Resveratrol and red wine constituents: evaluation of their neuroprotective properties. Pharm. News, 8, 33-38.
4. BASTIANETTO, S., ZHENG, W.H. & QUIRION, R. (2000). Neuroprotective abilities of resveratrol and other red wine constituents against nitric oxide-related toxicity in cultured hippocampal neurons. Br. J. Pharmacol., 131, 711-720.
5. BEHRENS, M.M., STRASSER, U., KOH, J.Y., GWAG, B.J. & CHOI, D.W. (1999). Prevention of neuronal apoptosis by phorbol ester-induced activation of protein kinase C: blockade of p38 mitogen-activated protein kinase. Neuroscience, 94, 917-927.
6. BUTTERFIELD, D.A. (2002). Amyloid beta-peptide (1-42)-induced oxidative stress and neurotoxicity: implications for neurodegeneration in Alzheimer's disease brain. Free Radic. Res., 36, 1307-1313.
7. CHANVITAYAPONGS, S., DRACZYNSKA-LUSIAK, B. & SUN, A.Y. (1997). Amelioration of oxidative stress by antioxidants and resveratrol in PC12 cells. Neuroreport, 8, 1499-1502.
8. CORDEY, M., GUNDIMEDA, U., GOPALAKRISHNA, R. & PIKE, C.J. (2003). Estrogen activates protein kinase C in neurons: role in neuroprotection. J. Neurochem., 84, 1340-1348.
9. DEACON, E.M., PONGRACZ, J., GRIFFITHS, G. & LORD, J.M. (1997). Isoenzymes of protein kinase C: differential involvement in apoptosis and pathogenesis. Mol. Pathol., 50, 124-131.
10. DELLA RAGIONE, F., CUCCIOLLA, V., CRINITI, V., INDACO, S., BORRIELLO, A. & ZAPPIA, V. (2002). Antioxidants induce different phenotypes by a distinct modulation of signal transduction. FEBS Lett., 532, 289-294.
11. DORE, S., TAKAHASHI, M., FERRIS, C.D., ZAKHARY, R., HESTER, L.D., GUASTELLA, D. & SNYDER, S.H. (1999). Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proc. Natl. Acad. Sci U.S.A., 96, 2445-2450.
12. DRACZYNSKA-LUSIAK, B., DOUNG, A. & SUN, A.Y. (1998). Oxidized lipoproteins may play a role in neuronal cell death in Alzheimer disease. Mol. Chem. Neuropathol., 33, 139-148.
13. GELINAS, S. & MARTINOLI, M.G. (2002). Neuroprotective effect of estradiol and phytoestrogens on MPP+-induced cytotoxicity in neuronal PC12 cells. J. Neurosci. Res., 70, 90-96.
14. GHAYUR, T., HUGUNIN, M., TALANIAN, R.V., RATNOFSKY, S., QUINLAN, C., EMOTO, Y., PANDEY, P., DATTA, R., HUANG, Y., KHARBANDA, S., ALLEN, H., KAMEN, R., WONG, W. & KUFE, D. (1996). Proteolytic activation of protein kinase C delta by an ICE/CED 3-like protease induces characteristics of apoptosis. J. Exp. Med., 184, 2399-2404.
15. GUBINA, E., RINAUDO, M.S., SZALLASI, Z., BLUMBERG, P.M. & MUFSON, R.A. (1998). Overexpression of protein kinase C isoform epsilon but not delta in human interleukin-3-dependent cells suppresses apoptosis and induces bcl-2 expression. Blood, 91, 823-829.
16. HARDY, J. & SELKOE, D.J. (2002). The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science, 297, 353-356.
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. ISHIGE, K., SCHUBERT, D. & SAGARA, Y. (2001). Flavonoids protect neuronal cells from oxidative stress by three distinct mechanisms. Free Radic. Biol. Med., 30, 433-446.
19. JANG, J.H. & SURH, Y.J. (2001). Protective effects of resveratrol on hydrogen peroxide-induced apoptosis in rat pheochromocytoma (PC12) cells. Mutat. Res., 496, 181-190.
20. JANG, J.H. & SURH, Y.J. (2003). Protective effects of resveratrol on β-amyloid-induced oxidative PC12 cell death. Free Radic. Biol. Med., 34, 1100-1110.
21. KARLSSON, J., EMGARD, M., BRUNDIN, P. & BURKITT, M.J. (2000). Trans-resveratrol protects embryonic mesencephalic cells from tertbutyl hydroperoxide: electron paramagnetic resonance spin trapping evidence for a radical scavenging mechanism. J. Neurochem., 75, 141-150.
22. KONISHI, H., MATSUZAKI, H., TAKAISHI, H., YAMAMOTO, T., FUKUNAGA, M., ONO, Y. & KIKKAWA, U. (1999). Opposing effects of protein kinase C delta and protein kinase B alpha on H(2)O(2)-induced apoptosis in CHO cells. Biochem. Biophys. Res. Commun., 264, 840-846.
23. LEIBOVICI, D., RITCHIE, K., LEDESERT, B. & TOUCHON, J. (1999). The effects of wine and tobacco consumption on cognitive performance in the elderly: a longitudinal study of relative risk. Int. J. Epidemiol., 28, 77-81.
24. LEVITES, Y., AMIT, T., YOUDIM, M.B. & MANDEL, S. (2002). Involvement of protein kinase C activation and cell survival/cell cycle genes in green tea polyphenol (-)-epigallocatechin 3-gallate neuroprotective action. J. Biol. Chem., 277, 30574-30580.
25. MAHER, P. (2001). How protein kinase C activation protects nerve cells from oxidative stress-induced cell death. J. Neurosci., 21, 2929-2938.
26. MARCOTTE, E.R., SRIVASTAVA, L.K. & QUIRION, R. (2003). cDNA microarray and proteomic approaches in the study of brain diseases: focus on schizophrenia and Alzheimer's disease. Pharmacol. Therapeut., 100, 63-74.
27. MATTSON, M.P. (1997). Cellular actions of beta-amyloid precursor protein and its soluble and fibrillogenic derivatives. Physiol. Rev., 77, 1081-1132.
28. MILLER, N.J. & RICE-EVANS, C.A. (1995). Antioxidant activity of resveratrol in red wine. Clin. Chem., 41, 1789.
29. MILOSO, M., BERTELLI, A.A., NICOLINI, G. & TREDICI, G. (1999). Resveratrol-induced activation of the mitogen-activated protein kinases, ERK1 and ERK2, in human neuroblastoma SH-SY5Y cells. Neurosci. Lett., 264, 141-144.
30. MURRAY, N.R. & FIELDS, A.P. (1997). Atypical protein kinase C iota protects human leukemia cells against drug-induced apoptosis. J. Biol. Chem., 272, 27521-27524.
31. NEWTON, A.C. (1997). Regulation of protein kinase C. Curr. Opin. Cell Biol., 9, 161-167.
32. NICOLINI, G., RIGOLIO, R., MILOSO, M., BERTELLI, A.A. & TREDICI, G. (2001). Anti-apoptotic effect of trans-resveratrol on paclitaxel-induced apoptosis in the human neuroblastoma SH-SY5Y cell line. Neurosci. Lett., 302, 41-44.
33. NICOLINI, G., RIGOLIO, R., SCUTERI, A., MILOSO, M., SACCOMANNO, D., CAVALETTI, G. & TREDICI, G. (2003). Effect of trans-resveratrol on signal transduction pathways involved in paclitaxel-induced apoptosis in human neuroblastoma SH-SY5Y cells. Neurochem. Int., 42, 419-429.
34. NISHIZUKA, Y. (1992). Intracellular signaling by hydrolysis of phosopholipids and activation of protein kinase C. Science, 258, 607-614.
35. ORGOGOZO, J.M., DARTIGUES, J.F., LAFONT, S., LETENNEUR, L., COMMENGES, D., SALAMON, R., RENAUD, S. & BRETELER, M.B. (1997). Wine consumption and dementia in the elderly: a prospective community study in the Bordeaux area. Rev. Neurol. (Paris), 153, 185-192.
36. RUSSO, A., PALUMBO, M., ALIANO, C., LEMPEREUR, L., SCOTO, G. & RENIS, M. (2003). Red wine micronutrients as protective agents in Alzheimer-like induced insult. Life Sci., 72, 2369-2379.
37. SHARMA, M. & GUPTA, Y.K. (2002). Chronic treatment with trans resveratrol prevents intracerebroventricular streptozotocin induced cognitive impairment and oxidative stress in rats. Life Sci., 71, 2489-2498.
38. 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.
39. SUBBARAMAIAH, K., CHUNG, W.J., MICHALUART, P., TELANG, N., TANABE, T., INOUE, H., JANG, M., PEZZUTO, J.M. & DANNENBERG, A.J. (1998). Resveratrol inhibits cyclooxygenase-2 transcription and activity in phorbol ester-treated human mammary epithelial cells. J. Biol. Chem., 273, 21875-21882.
40. VIRGILI, M. & CONTESTABILE, A. (2000). Partial neuroprotection of in vivo excitotoxic brain damage by chronic administration of the red wine antioxidant agent, trans-resveratrol in rats. Neurosci. Lett., 281, 123-126.
41. WANG, Q., XU, J., 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.
42. WHELAN, R.D. & PARKER, P.J. (1998). Loss of protein kinase C function induces an apoptotic response. Oncogene, 16, 1939-1944.
43. XIE, J., GUO, Q., ZHU, H., WOOTEN, M.W. & MATTSON, M.P. (2000). Protein kinase C protects neural cells against apoptosis induced by amyloid β-peptide. Mol. Brain Res., 82, 107-113.
44. ZHENG, W.H., KAR, S. & QUIRION, R. (2002). Insulin-like growth factor-1-induced phosphorylation of transcription factor FKHRL1 is mediated by phosphatidylinositol 3-kinase/Akt kinase and role of this pathway in insulin-like growth factor-1-induced survival of cultured hippocampal neurons. Mol. Pharmacol., 62, 225-233.
45. ZHUANG, H., KIM, Y.S., KOEHLER, R.C. & DORE, S. (2003). Potential mechanism by which resveratrol, a red wine constituent, protects neurons. Ann. N. Y. Acad. Sci., 993, 276-286.