Resveratrol attenuates behavioral impairments and reduces cortical and hippocampal loss in a rat controlled cortical impact model of traumatic brain injury

Journal of Neurotrauma

Volumn 27, Issue 6, 2010, Pages 1091-1099

  Singleton, Richard H ^a   Yan, Hong Q ^a   Fellows Mayle, Wendy ^a   Dixon, C Edward ^a  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

controlled cortical impact; contusion; neuroprotection; resveratrol (3,5,40 trihydroxystilbene); traumatic brain injury

Indexed keywords

RESVERATROL; NEUROPROTECTIVE AGENT; STILBENE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; BRAIN CONTUSION; BRAIN NERVE CELL; CELL COUNT; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DISEASE MODEL; DISEASE SEVERITY; DOSE RESPONSE; DRUG EFFECT; DRUG EFFICACY; HIPPOCAMPUS; MALE; MAZE TEST; MEMORY DISORDER; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; NEUROPROTECTION; NONHUMAN; RAT; SPATIAL MEMORY; TRAUMATIC BRAIN INJURY; WALKING; ANALYSIS OF VARIANCE; ANIMAL; BRAIN CORTEX; BRAIN INJURIES; CELL DEATH; DRUG EFFECTS; MOTOR ACTIVITY; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; RANDOMIZATION; SPRAGUE DAWLEY RAT;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN INJURIES; CELL COUNT; CELL DEATH; CEREBRAL CORTEX; DOSE-RESPONSE RELATIONSHIP, DRUG; HIPPOCAMPUS; MALE; MAZE LEARNING; MOTOR ACTIVITY; NEURONS; NEUROPROTECTIVE AGENTS; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; STILBENES;

EID: 77953956124     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2010.1291     Document Type: Article

References (59)

1. Ates, O. Cayli, S., Altinoz, E., Gurses, I., Yucel, N., Kocak, A., Yologlu, S., and Turkoz, Y. (2006). Effects of resveratrol and methylprednisolone on biochemical, neurobehavioral and histopathological recovery after experimental spinal cord injury. Acta Pharmacol. Sin. 27, 1317-1325.
2. Ates, O., Cayli, S., Altinoz, E., Gurses, I., Yucel, N., Sener, M., Kocak, A., and Yologlu, S. (2007). Neuroprotection by resveratrol against traumatic brain injury in rats. Mol. Cell Biochem. 294, 137-144.
3. Baur, J.A., Pearson, K.J., Price, N.L., Jamieson, H.A., Lerin, C., Kalra, A., Prabhu, V.V., Allard, J.S., Lopez-Lluch, G., Lewis, K., Pistell, P.J., Poosala, S., Becker, K.G., Boss, O., Gwinn, D., Wang, M., Ramaswamy, S., Fishbein, K.W., Spencer, R.G., Lakatta, E.G., Le Couteur, D., Shaw, R.J., Navas, P., Puigserver, P., Ingram, D.K., de Cabo, R., and Sinclair, D.A. (2006). Resveratrol improves health and survival of mice on a highcalorie diet. Nature 444, 337-342.
4. Baur, J.A., and Sinclair, D.A. (2006). Therapeutic potential of resveratrol: the in vivo evidence. Nat. Rev. Drug Discov. 5, 493-506.
5. Bramlett, H.M., and Dietrich, W.D. (2001). Neuropathological protection after traumatic brain injury in intact female rats versus males or ovariectomized females. J. Neurotrauma 18, 891-900.
6. Buryanovskyy, L., Fu, Y., Boyd, M., Ma, Y., Hsieh, T.C., Wu, J.M., and Zhang, Z. (2004). Crystal structure of quinone reductase 2 in complex with resveratrol. Biochemistry 43, 11417-11426. (Pubitemid 39186963)
7. Chun, Y.J., Kim, M.Y., and Guengerich, F.P. (1999). Resveratrol is a selective human cytochrome P450 1A1 inhibitor. Biochem. Biophys. Res. Commun. 262, 20-24.
8. Ciolino, H.P., Daschner, P.J., and Yeh, G.C. (1998). Resveratrol inhibits transcription of CYP1A1 in vitro by preventing activation of the aryl hydrocarbon receptor. Cancer Res. 58, 5707-5712.
9. Crowell, J.A., Korytko, P.J., Morrissey, R.L., Booth, T.D., and Levine, B.S. (2004). Resveratrol-associated renal toxicity. Toxicol. Sci. 82, 614-619.
10. Della-Morte, D., Dave, K.R., DeFazio, R.A., Bao, Y.C., Raval, A.P., and Perez-Pinzon, M.A. (2009). Resveratrol pretreatment protects rat brain from cerebral ischemic damage via a sirtuin 1-uncoupling protein 2 pathway. Neuroscience 159, 993-1002.
11. Dixon, C.E., Clifton, G.L., Lighthall, J.W., Yaghmai, A.A., and Hayes, R.L. (1991). A controlled cortical impact model of traumatic brain injury in the rat. J. Neurosci. Methods 39, 253-262.
12. Dixon, C.E., Hamm, R.J., Taft, W.C., and Hayes, R.L. (1994). Increased anticholinergic sensitivity following closed skull impact and controlled cortical impact traumatic brain injury in the rat. J. Neurotrauma 11, 275-287.
13. Dixon, C.E., Kochanek, P.M., Yan, H.Q., Schiding, J.K., Griffith, R.G., Baum, E., Marion, D.W., and DeKosky, S.T. (1999a). One-year study of spatial memory performance, brain morphology, and cholinergic markers after moderate controlled cortical impact in rats. J. Neurotrauma 16, 109-122.
14. Dixon, C.E., Kraus, M.F., Kline, A.E., Ma, X., Yan, H.Q., Griffith, R.G., Wolfson, B.M., and Marion, D.W. (1999b). Amantadine improves water maze performance without affecting motor behavior following traumatic brain injury in rats. Restor. Neurol. Neurosci. 14, 285-294.
15. Dixon, C.E., Ma, X., Kline, A.E., Yan, H.Q., Ferimer, H., Kochanek, P.M., Wisniewski, S.R., Jenkins, L.W., and Marion, D.W. (2003). Acute etomidate treatment reduces cognitive deficits and histopathology in rats with traumatic brain injury. Crit. Care Med. 31, 2222-2227.
16. Dong, W., Li, N., Gao, D., Zhen, H., Zhang, X., and 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.
17. Dubal, D.B., Zhu, H., Yu, J., Rau, S.W., Shughrue, P.J., Merchenthaler, I., Kindy, M.S., and Wise, P.M. (2001). Estrogen receptor alpha, not beta, is a critical link in estradiol-mediated protection against brain injury. Proc. Natl. Acad. Sci. U.S.A. 98, 1952-1957.
18. Emerson, C.S., Headrick, J.P., and Vink, R. (1993). Estrogen improves biochemical and neurologic outcome following traumatic brain injury in male rats, but not in females. Brain Res. 608, 95-100.
19. Feeney, D.M., Gonzalez, A., and Law, W.A. (1982). Amphetamine, haloperidol, and experience interact to affect rate of recovery after motor cortex injury. Science 217, 855-857.
20. Floreani, M., Napoli, E., Quintieri, L., and Palatini, P. (2003). Oral administration of trans-resveratrol to guinea pigs increases cardiac DT-diaphorase and catalase activities, and protects isolated atria from menadione toxicity. Life Sci. 72, 2741-2750.
21. Frankel, E.N., Waterhouse, A.L., and Kinsella, J.E. (1993). Inhibition of human LDL oxidation by resveratrol. Lancet 341, 1103-1104.
22. Freyberger, A., and Schmuck, G. (2005). Screening for estrogenicity and anti-estrogenicity: a critical evaluation of an MVLN cell-based transactivation assay. Toxicol. Lett. 155, 1-13.
23. Gehm, B.D., McAndrews, J.M., Chien, P.Y., and Jameson, J.L. (1997). Resveratrol, a polyphenolic compound found in grapes and wine, is an agonist for the estrogen receptor. Proc. Natl. Acad. Sci. U.S.A. 94, 14138-14143.
24. Gupta, Y.K., Briyal, S., and Chaudhary, G. (2002a). Protective effect of trans-resveratrol against kainic acid-induced seizures and oxidative stress in rats. Pharmacol. Biochem. Behav. 71, 245-249.
25. Gupta, Y.K., Chaudhary, G., Sinha, K., and Srivastava, A.K. (2001). Protective effect of resveratrol against intracortical FeCl3-induced model of posttraumatic seizures in rats. Methods Find. Exp. Clin. Pharmacol. 23, 241-244.
26. Gupta, Y.K., Chaudhary, G., and Srivastava, A.K. (2002b). Protective effect of resveratrol against pentylenetetrazole-induced seizures and its modulation by an adenosinergic system. Pharmacology 65, 170-174.
27. Hamm, R.J., Dixon, C.E., Gbadebo, D.M., Singha, A.K., Jenkins, L.W., Lyeth, B.G., and Hayes, R.L. (1992). Cognitive deficits following traumatic brain injury produced by controlled cortical impact. J. Neurotrauma 9, 11-20.
28. Howitz, K.T., Bitterman, K.J., Cohen, H.Y., Lamming, D.W., Lavu, S., Wood, J.G., Zipkin, R.E., Chung, P., Kisielewski, A., Zhang, L.L., Scherer, B., and Sinclair, D.A. (2003). Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 425, 191-196.
29. Jang, M., Cai, L., Udeani, G.O., Slowing, K.V., Thomas, C.F., Beecher, C.W., Fong, H.H., Farnsworth, N.R., Kinghorn, A.D., Mehta, R.G., Moon, R.C., and Pezzuto, J.M. (1997). Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 275, 218-220.
30. Kaeberlein, M., McDonagh, T., Heltweg, B., Hixon, J., Westman, E.A., Caldwell, S.D., Napper, A., Curtis, R., DiStefano, P.S., Fields, S., Bedalov, A., and Kennedy, B.K. (2005). Substratespecific activation of sirtuins by resveratrol. J. Biol. Chem. 280, 17038-17045.
31. Kaga, S., Zhan, L., Matsumoto, M., and Maulik, N. (2005). Resveratrol enhances neovascularization in the infarcted rat myocardium through the induction of thioredoxin-1, heme oxygenase-1 and vascular endothelial growth factor. J. Mol. Cell Cardiol. 39, 813-822.
32. Kaplan, S., Bisleri, G., Morgan, J.A., Cheema, F.H., and Oz, M.C. (2005). Resveratrol, a natural red wine polyphenol, reduces ischemia-reperfusion- induced spinal cord injury. Ann. Thorac. Surg. 80, 2242-2249.
33. Karlsson, J., Emgard, M., Brundin, P., and Burkitt, M.J. (2000). Trans-resveratrol protects embryonic mesencephalic cells from tert-butyl hydroperoxide: electron paramagnetic resonance spin trapping evidence for a radical scavenging mechanism. J. Neurochem. 75, 141-150.
34. Kiziltepe, U., Turan, N.N., Han, U., Ulus, A.T., and Akar, F. (2004). Resveratrol, a red wine polyphenol, protects spinal cord from ischemia-reperfusion injury. J. Vasc. Surg. 40, 138-145.
35. Kline, A.E., and Dixon, C.E. (2001). Contemporery in vivo models of brain trauma and a comparison of injury responses. In: Head trauma: Basic, preclinical, and Clinical Directions. Miller, L.P., Hayes, R.L. (eds). John Wiley and Sons: New York. PPs. 65-84.
36. Lagouge, M., Argmann, C., Gerhart-Hines, Z., Meziane, H., Lerin, C., Daussin, F., Messadeq, N., Milne, J., Lambert, P., Elliott, P., Geny, B., Laakso, M., Puigserver, P., and Auwerx, J. (2006). Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 127, 1109-1122.
37. Li, C., Yan, Z., Yang, J., Chen, H., Li, H., Jiang, Y., and Zhang, Z. (2010). Neuroprotective effects of resveratrol on ischemic injury mediated by modulating the release of neurotransmitter and neuromodulator in rats. Neurochem. Int. 56, 495-500.
38. Liu, B.Q., Gao, Y.Y., Niu, X.F., Xie, J.S., Meng, X., Guan, Y., and Wang, H.Q. (2009). Implication of unfolded protein response in resveratrol-induced inhibition of K562 cell proliferation. Biochem. Biophys. Res. Commun. 391, 778-782.
39. Manna, S.K., Mukhopadhyay, A., and Aggarwal, B.B. (2000). Resveratrol suppresses TNF-induced activation of nuclear transcription factors NF-kappa B, activator protein-1, and apoptosis: potential role of reactive oxygen intermediates and lipid peroxidation. J. Immunol. 164, 6509-6519.
40. Morris, R. (1984). Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11, 47-60.
41. Mouton, P.R. (2002). Principles and Practices of Unbiased Stereology. Johns Hopkins University Press: Baltimore.
42. National Academy Press. (1996). Guide for the Care and Use of Laboratory Animals. National Academy Press: Washington, DC.
43. Parker, J.A., Arango, M., Abderrahmane, S., Lambert, E., Tourette, C., Catoire, H., and Neri, C. (2005). Resveratrol rescues mutant polyglutamine cytotoxicity in nematode and mammalian neurons. Nat. Genet. 37, 349-350.
44. Piver, B., Berthou, F., Dreano, Y., and Lucas, D. (2001). Inhibition of CYP3A, CYP1A and CYP2E1 activities by resveratrol and other non volatile red wine components. Toxicol. Lett. 125, 83-91.
45. Raval, A.P., Dave, K.R., and Perez-Pinzon, M.A. (2006). Resveratrol mimics ischemic preconditioning in the brain. J. Cereb. Blood Flow Metab. 26, 1141-1147.
46. Roof, R.L., and Hall, E.D. (2000). Estrogen-related gender difference in survival rate and cortical blood flow after impactacceleration head injury in rats. J. Neurotrauma 17, 1155-1169.
47. Saatman, K.E., Duhaime, A.C., Bullock, R., Maas, A.I., Valadka, A., and Manley, G.T. (2008). Classification of traumatic brain injury for targeted therapies. J. Neurotrauma 25, 719-738.
48. Scheff, S.W., Baldwin, S.A., Brown, R.W., and Kraemer, P.J. (1997). Morris water maze deficits in rats following traumatic brain injury: lateral controlled cortical impact. J. Neurotrauma 14, 615-627.
49. Sinha, K., Chaudhary, G., and 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.
50. Sonmez, U., Sonmez, A., Erbil, G., Tekmen, I., and Baykara, B. (2007). Neuroprotective effects of resveratrol against traumatic brain injury in immature rats. Neurosci. Lett. 420, 133-137.
51. Tsai, S.H., Lin-Shiau, S.Y., and Lin, J.K. (1999). Suppression of nitric oxide synthase and the down-regulation of the activation of NFkappaB in macrophages by resveratrol. Br. J. Pharmacol. 126, 673-680.
52. Viswanathan, M., Kim, S.K., Berdichevsky, A., and Guarente, L. (2005). A role for SIR-2.1 regulation of ER stress response genes in determining C. elegans life span. Dev. Cell. 9, 605-615.
53. Vorhees, C.V., and Williams, M.T. (2006). Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat. Protoc. 1, 848-858.
54. Wagner, A.K., Willard, L.A., Kline, A.E., Wenger, M.K., Bolinger, B.D., Ren, D., Zafonte, R.D., and Dixon, C.E. (2004). Evaluation of estrous cycle stage and gender on behavioral outcome after experimental traumatic brain injury. Brain Res. 998, 113-121.
55. Wang, Q., Xu, J., Rottinghaus, G.E., Simonyi, A., Lubahn, D., Sun, G.Y., and Sun, A.Y. (2002). Resveratrol protects against global cerebral ischemic injury in gerbils. Brain Res. 958, 439-447.
56. West, T., Atzeva, M., and Holtzman, D.M. (2007). Pomegranate polyphenols and resveratrol protect the neonatal brain against hypoxic-ischemic injury. Dev. Neurosci. 29, 363-372.
57. Wu, Z., Xu, Q., Zhang, L., Kong, D., Ma, R., and Wang, L. (2009). Protective effect of resveratrol against kainate-induced temporal lobe epilepsy in rats. Neurochem. Res. 34, 1393-1400.
58. Yang, Y.B., and Piao, Y.J. (2003). Effects of resveratrol on secondary damages after acute spinal cord injury in rats. Acta Pharmacol. Sin. 24, 703-710.
59. Yu, C., Shin, Y.G., Kosmeder, J.W., Pezzuto, J.M., and van Breemen, R.B. (2003). Liquid chromatography/tandem mass spectrometric determination of inhibition of human cytochrome P450 isozymes by resveratrol and resveratrol-3-sulfate. Rapid Commun. Mass Spectrom. 17, 307-313.