Resveratrol neuroprotection in stroke and traumatic CNS injury

Neurochemistry International

Volumn 89, Issue , 2015, Pages 75-82

  Lopez, Mary S ^a   Dempsey, Robert J ^a   Vemuganti, Raghu ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

CNS injury; Inflammation; Ischemia; Neuroprotection; Oxidative stress; Polyphenols

Indexed keywords

ESTROGEN RECEPTOR; MATRIX METALLOPROTEINASE; NITRIC OXIDE; RESVERATROL; ANTIOXIDANT; NEUROPROTECTIVE AGENT; STILBENE DERIVATIVE;

ANTIEXCITOTOXIC ACTIVITY; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; APOPTOSIS; CENTRAL NERVOUS SYSTEM; CEREBROVASCULAR ACCIDENT; DRUG ACTIVITY; DRUG EFFICACY; EXTRACELLULAR MATRIX; HUMAN; ISCHEMIC PRECONDITIONING; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; TRAUMATIC BRAIN INJURY; ANIMAL; BRAIN INJURIES; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; STROKE;

ANIMALS; ANTIOXIDANTS; BRAIN INJURIES; HUMANS; NEUROPROTECTION; NEUROPROTECTIVE AGENTS; STILBENES; STROKE;

EID: 84942293290     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2015.08.009     Document Type: Review

References (146)

1. M. Agrawal, V. Kumar, M.P. Kashyap, V.K. Khanna, G.S. Randhawa, and A.B. Pant Ischemic insult induced apoptotic changes in PC12 cells: protection by trans resveratrol Eur. J. Pharmacol. 666 2011 5 11
2. N.J. Alkayed, I. Harukuni, A.S. Kimes, E.D. London, R.J. Traystman, and P.D. Hurn Gender-linked brain injury in experimental stroke Stroke J. Cereb. Circ. 29 1998 159 166
3. S.A. Andrabi, M.G. Spina, P. Lorenz, U. Ebmeyer, G. Wolf, and T.F. Horn Oxyresveratrol (trans-2,3′,4,5′-tetrahydroxystilbene) is neuroprotective and inhibits the apoptotic cell death in transient cerebral ischemia Brain Res. 1017 2004 98 107
4. M. Asahi, X. Wang, T. Mori, T. Sumii, J.-C. Jung, M.A. Moskowitz, M.E. Fini, and E.H. Lo Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia J. Neurosci. 21 2001 7724 7732
5. O. Ates, S. Cayli, E. Altinoz, I. Gurses, N. Yucel, A. Kocak, S. Yologlu, and Y. Turkoz Effects of resveratrol and methylprednisolone on biochemical, neurobehavioral and histopathological recovery after experimental spinal cord injury Acta Pharmacol. Sin. 27 2006 1317 1325
6. O. Ates, S. Cayli, E. Altinoz, I. Gurses, N. Yucel, M. Sener, A. Kocak, and S. Yologlu Neuroprotection by resveratrol against traumatic brain injury in rats Mol. Cell. Biochem. 294 2007 137 144
7. M. Bains, and E.D. Hall Antioxidant therapies in traumatic brain and spinal cord injury Biochim. Biophys. Acta 1822 2012 675 684
8. J.A. Baur, K.J. Pearson, N.L. Price, H.A. Jamieson, C. Lerin, A. Kalra, V.V. Prabhu, J.S. Allard, G. Lopez-Lluch, and K. Lewis Resveratrol improves health and survival of mice on a high-calorie diet Nature 444 2006 337 342
9. X.L. Bi, J.Y. Yang, Y.X. Dong, J.M. Wang, Y.H. Cui, T. Ikeshima, Y.Q. Zhao, and C.F. Wu Resveratrol inhibits nitric oxide and TNF-α production by lipopolysaccharide-activated microglia Int. Immunopharmacol. 5 2005 185 193
10. M.T. Borra, B.C. Smith, and J.M. Denu Mechanism of human SIRT1 activation by resveratrol J. Biol. Chem. 280 2005 17187 17195
11. J.L. Bowers, V.V. Tyulmenkov, S.C. Jernigan, and C.M. Klinge Resveratrol acts as a mixed agonist/antagonist for estrogen receptors α and β 1 Endocrinology 141 2000 3657 3667
12. G. Bureau, F. Longpré, and M.G. Martinoli Resveratrol and quercetin, two natural polyphenols, reduce apoptotic neuronal cell death induced by neuroinflammation J. Neurosci. Res. 86 2008 403 410
13. M. Cai, Y.-L. Ma, P. Qin, Y. Li, L.-X. Zhang, H. Nie, Z. Peng, H. Dong, H.-L. Dong, and W.-G. Hou The loss of estrogen efficacy against cerebral ischemia in aged postmenopausal female mice Neurosci. Lett. 558 2014 115 119
14. E. Calleri, G. Pochetti, K.S.S. Dossou, A. Laghezza, R. Montanari, D. Capelli, E. Prada, F. Loiodice, G. Massolini, M. Bernier, and R. Moaddel Resveratrol and its metabolites bind to PPARs ChemBioChem. 15 2014 1154 1160
15. E. Candelario-Jalil, A.C. de Oliveira, S. Graf, H.S. Bhatia, M. Hull, E. Munoz, and B.L. Fiebich Resveratrol potently reduces prostaglandin E2 production and free radical formation in lipopolysaccharide-activated primary rat microglia J. Neuroinflammation 4 2007 25
16. C.-Y. Chen, J.-H. Jang, M.-H. Li, and Y.-J. Surh Resveratrol upregulates heme oxygenase-1 expression via activation of NF-E2-related factor 2 in PC12 cells Biochem. Biophys. Res. Commun. 331 2005 993 1000
17. G. Cheng, X. Zhang, D. Gao, X. Jiang, and W. Dong Resveratrol inhibits MMP-9 expression by up-regulating PPAR alpha expression in an oxygen glucose deprivation-exposed neuron model Neurosci. Lett. 451 2009 105 108
18. D.W. Choi Excitotoxic cell death J. Neurobiol. 23 1992 1261 1276
19. B. Dasgupta, and J. Milbrandt Resveratrol stimulates AMP kinase activity in neurons Proc. Natl. Acad. Sci. U. S. A. 104 2007 7217 7222
20. F. De Bilbao, D. Arsenijevic, P. Vallet, O.P. Hjelle, O.P. Ottersen, C. Bouras, Y. Raffin, K. Abou, W. Langhans, and S. Collins Resistance to cerebral ischemic injury in UCP2 knockout mice: evidence for a role of UCP2 as a regulator of mitochondrial glutathione levels J. Neurochem. 89 2004 1283 1292
21. P. Delerive, P. Gervois, J.-C. Fruchart, and B. Staels Induction of IκBα expression as a mechanism contributing to the anti-inflammatory activities of peroxisome proliferator-activated receptor-α activators J. Biol. Chem. 275 2000 36703 36707
22. 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
23. V.K. Dhodda, K.A. Sailor, K.K. Bowen, and R. Vemuganti Putative endogenous mediators of preconditioning-induced ischemic tolerance in rat brain identified by genomic and proteomic analysis J. Neurochem. 89 2004 73 89
24. V. Di Liberto, J. Mäkelä, L. Korhonen, M. Olivieri, T. Tselykh, A. Mälkiä, H. Do Thi, N. Belluardo, D. Lindholm, and G. Mudò Involvement of estrogen receptors in the resveratrol-mediated increase in dopamine transporter in human dopaminergic neurons and in striatum of female mice Neuropharmacology 62 2012 1011 1018
25. U. Dirnagl, C. Iadecola, and M.A. Moskowitz Pathobiology of ischaemic stroke: an integrated view Trends Neurosci. 22 1999 391 397
26. U. Dirnagl, R.P. Simon, and J.M. Hallenbeck Ischemic tolerance and endogenous neuroprotection Trends Neurosci. 26 2003 248 254
27. C. Domínguez, P. Delgado, A. Vilches, P. Martín-Gallán, M. Ribó, E. Santamarina, C. Molina, N. Corbeto, V. Rodríguez-Sureda, and A. Rosell Oxidative stress after thrombolysis-induced reperfusion in human stroke Stroke J. Cereb. Circ. 41 2010 653 660
28. D.B. Dubal, S.W. Rau, P.J. Shughrue, H. Zhu, J. Yu, A.B. Cashion, S. Suzuki, L.M. Gerhold, M.B. Bottner, and S.B. Dubal Differential modulation of estrogen receptors (ERs) in ischemic brain injury: a role for ERα in estradiol-mediated protection against delayed cell death Endocrinology 147 2006 3076 3084
29. 2+ levels and nitric oxide release in human endothelial cells Mol. Nutr. Food Res. 55 2011 1237 1248
30. J.G. Elzer, S. Muhammad, T.M. Wintermantel, A. Regnier-Vigouroux, J. Ludwig, G. Schütz, and M. Schwaninger Neuronal estrogen receptor-α mediates neuroprotection by 17β-estradiol J. Cereb. Blood Flow Metab. 30 2010 935 942
31. U. Forstermann, and T. Munzel Endothelial nitric oxide synthase in vascular disease: from marvel to menace Circulation 113 2006 1708 1714
32. D. Gao, T. Huang, X. Jiang, S. Hu, L. Zhang, and Z. Fei Resveratrol protects primary cortical neuron cultures from transient oxygen-glucose deprivation by inhibiting MMP-9 Mol. Med. Rep. 9 2014 2197 2204
33. D. Gao, X. Zhang, X. Jiang, Y. Peng, W. Huang, G. Cheng, and L. Song Resveratrol reduces the elevated level of MMP-9 induced by cerebral ischemia-reperfusion in mice Life Sci. 78 2006 2564 2570
34. Z.B. Gao, X.Q. Chen, and G.Y. Hu Inhibition of excitatory synaptic transmission by trans-resveratrol in rat hippocampus Brain Res. 1111 2006 41 47
35. J.W. Gatson, M.M. Liu, K. Abdelfattah, J.G. Wigginton, S. Smith, S. Wolf, and J.P. Minei Resveratrol decreases inflammation in the brain of mice with mild traumatic brain injury J. Trauma Acute Care Surg. 74 2013 470 474 discussion 474-475
36. B.D. Gehm, J.M. McAndrews, P.-Y. Chien, and J.L. Jameson Resveratrol, a polyphenolic compound found in grapes and wine, is an agonist for the estrogen receptor Proc. Natl. Acad. Sci. 94 1997 14138 14143
37. J.M. Gidday Cerebral preconditioning and ischaemic tolerance Nat. Rev. Neurosci. 7 2006 437 448
38. C. Girbovan, L. Morin, and H. Plamondon Repeated resveratrol administration confers lasting protection against neuronal damage but induces dose-related alterations of behavioral impairments after global ischemia Behav. Pharmacol. 23 2012 1 13
39. C. Girbovan, and H. Plamondon Resveratrol downregulates type-1 glutamate transporter expression and microglia activation in the hippocampus following cerebral ischemia reperfusion in rats Brain Res. 1608 2015 203 214
40. 2+ concentrations are involved in resveratrol protection against apoptosis in rat primary neuron cultures Acta Pharmacol. Sin. 28 2007 1724 1730
41. B.A. Haines, S.L. Mehta, S.M. Pratt, C.H. Warden, and P.A. Li Deletion of mitochondrial uncoupling protein-2 increases ischemic brain damage after transient focal ischemia by altering gene expression patterns and enhancing inflammatory cytokines J. Cereb. Blood Flow Metab.: Off. J. Int. Soc. Cereb. Blood Flow Metab. 30 2010 1825 1833
42. E.D. Hall, R.A. Vaishnav, and A.G. Mustafa Antioxidant therapies for traumatic brain injury Neurother.: J. Am. Soc. Exp. Neurother. 7 2010 51 61
43. A.S. Hazell Excitotoxic mechanisms in stroke: an update of concepts and treatment strategies Neurochem. Int. 50 2007 941 953
44. J.J. Heynekamp, W.M. Weber, L.A. Hunsaker, A.M. Gonzales, R.A. Orlando, L.M. Deck, and D.L. Vander Jagt Substituted trans-stilbenes, including analogues of the natural product resveratrol, inhibit the human tumor necrosis factor alpha-induced activation of transcription factor nuclear factor kappaB J. Med. Chem. 49 2006 7182 7189
45. K. Hochrainer, K. Jackman, J. Anrather, and C. Iadecola Reperfusion rather than ischemia drives the formation of ubiquitin aggregates after middle cerebral artery occlusion Stroke J. Cereb. Circ. 43 2012 2229 2235
46. S.S. Huang, M.C. Tsai, C.L. Chih, L.M. Hung, and S.K. Tsai Resveratrol reduction of infarct size in Long-Evans rats subjected to focal cerebral ischemia Life Sci. 69 2001 1057 1065
47. H. Inoue Brain protection by resveratrol and fenofibrate against stroke requires peroxisome proliferator-activated receptor α in mice Neurosci. Lett. 352 3 11 December 2003 203 206
48. S. Jäger, C. Handschin, J.S. Pierre, and B.M. Spiegelman AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1α Proc. Natl. Acad. Sci. 104 2007 12017 12022
49. M. Jang, L. Cai, G.O. Udeani, K.V. Slowing, C.F. Thomas, C.W. Beecher, H.H. Fong, N.R. Farnsworth, A.D. Kinghorn, and R.G. Mehta Cancer chemopreventive activity of resveratrol, a natural product derived from grapes Science 275 1997 218 220
50. E. Kansanen, S.M. Kuosmanen, H. Leinonen, and A.L. Levonen The Keap1-Nrf2 pathway: mechanisms of activation and dysregulation in cancer Redox Biol. 1 2013 45 49
51. S. Kaplan, G. Bisleri, J.A. Morgan, F.H. Cheema, and M.C. Oz Resveratrol, a natural red wine polyphenol, reduces ischemia-reperfusion-induced spinal cord injury Ann. Thorac. Surg. 80 2005 2242 2249
52. F. Karalis, V. Soubasi, T. Georgiou, C.T. Nakas, C. Simeonidou, O. Guiba-Tziampiri, and E. Spandou Resveratrol ameliorates hypoxia/ischemia-induced behavioral deficits and brain injury in the neonatal rat brain Brain Res. 1425 2011 98 110
53. A. Karaoglan, O. Akdemir, S. Barut, S. Kokturk, H. Uzun, M. Tasyurekli, and A. Colak The effects of resveratrol on vasospasm after experimental subarachnoidal hemorrhage in rats Surg. Neurol. 70 2008 337 343
54. V. Kesherwani, F. Atif, S. Yousuf, and S.K. Agrawal Resveratrol protects spinal cord dorsal column from hypoxic injury by activating Nrf-2 Neuroscience 241 2013 80 88
55. B. Khodr, and Z. Khalil Modulation of inflammation by reactive oxygen species: implications for aging and tissue repair Free Radic. Biol. Med. 30 2001 1 8
56. C.M. Klinge, N.S. Wickramasinghe, M.M. Ivanova, and S.M. Dougherty Resveratrol stimulates nitric oxide production by increasing estrogen receptor alpha-Src-caveolin-1 interaction and phosphorylation in human umbilical vein endothelial cells FASEB J.: Off. Publ. Fed. Am. Soc. Exp. Biol. 22 2008 2185 2197
57. H.S. Ko, H.J. Lee, S.H. Kim, and E.O. Lee Piceatannol suppresses breast cancer cell invasion through the inhibition of MMP-9: involvement of PI3K/AKT and NF-kappaB pathways J. Agric. Food Chem. 60 2012 4083 4089
58. P. Kocina Body composition of spinal cord injured adults Sports Med. 23 1997 48 60
59. M. Lagouge, C. Argmann, Z. Gerhart-Hines, H. Meziane, C. Lerin, F. Daussin, N. Messadeq, J. Milne, P. Lambert, and P. Elliott Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1α Cell 127 2006 1109 1122
60. S.E. Lakhan, A. Kirchgessner, and M. Hofer Inflammatory mechanisms in ischemic stroke: therapeutic approaches J. Transl. Med. 7 2009 97
61. S.E. Lakhan, A. Kirchgessner, D. Tepper, and A. Leonard Matrix metalloproteinases and blood-brain barrier disruption in acute ischemic stroke Front. Neurol. 4 2013
62. A. Lanzillotta, G. Pignataro, C. Branca, O. Cuomo, I. Sarnico, M. Benarese, L. Annunziato, P. Spano, and M. Pizzi Targeted acetylation of NF-kappaB/RelA and histones by epigenetic drugs reduces post-ischemic brain injury in mice with an extended therapeutic window Neurobiol. Dis. 49 2013 177 189
63. Y.-j. Lee, Y. Mou, D. Klimanis, J.D. Bernstock, and J.M. Hallenbeck Global SUMOylation is a molecular mechanism underlying hypothermia-induced ischemic tolerance Front. Cell. Neurosci. 8 2014
64. C. Li, Z. Yan, J. Yang, H. Chen, H. Li, Y. Jiang, and Z. Zhang Neuroprotective effects of resveratrol on ischemic injury mediated by modulating the release of neurotransmitter and neuromodulator in rats Neurochem. Int. 56 2010 495 500
65. H. Li, and U. Förstermann Uncoupling of endothelial NO synthase in atherosclerosis and vascular disease Curr. Opin. Pharmacol. 13 2013 161 167
66. Z. Li, L. Pang, F. Fang, G. Zhang, J. Zhang, M. Xie, and L. 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
67. C.J. Lin, T.H. Chen, L.Y. Yang, and C.M. Shih Resveratrol protects astrocytes against traumatic brain injury through inhibiting apoptotic and autophagic cell death Cell Death Dis. 5 2014 e1147
68. H.Y. Lin, H.Y. Tang, F.B. Davis, and P.J. Davis Resveratrol and apoptosis Ann. N. Y. Acad. Sci. 1215 2011 79 88
69. H. Ling, H. Yang, S.H. Tan, W.K. Chui, and E.H. Chew 6-Shogaol, an active constituent of ginger, inhibits breast cancer cell invasion by reducing matrix metalloproteinase-9 expression via blockade of nuclear factor-κB activation Br. J. Pharmacol. 161 2010 1763 1777
70. A. Liu, H. Fang, W. Wei, O. Dirsch, and U. Dahmen Ischemic preconditioning protects against liver ischemia/reperfusion injury via heme oxygenase-1-mediated autophagy Crit. Care Med. 42 2014 e762 e771
71. C. Liu, Z. Shi, L. Fan, C. Zhang, K. Wang, and B. Wang Resveratrol improves neuron protection and functional recovery in rat model of spinal cord injury Brain Res. 1374 2011 100 109
72. Y. Liu, L. Chen, X. Xu, E. Vicaut, and R. Sercombe Both ischemic preconditioning and ghrelin administration protect hippocampus from ischemia/reperfusion and upregulate uncoupling protein-2 BMC Physiol. 9 2009 17
73. Y. Liu, H. Kato, N. Nakata, and K. Kogure Protection of rat hippocampus against ischemic neuronal damage by pretreatment with sublethal ischemia Brain Res. 586 1992 121 124
74. P. Lorenz, S. Roychowdhury, M. Engelmann, G. Wolf, and T.F. Horn Oxyresveratrol and resveratrol are potent antioxidants and free radical scavengers: effect on nitrosative and oxidative stress derived from microglial cells Nitric Oxide Biol. Chem./Off. J. Nitric Oxide Soc. 9 2003 64 76
75. Z. Lu, X. Xu, X. Hu, J. Fassett, G. Zhu, Y. Tao, J. Li, Y. Huang, P. Zhang, and B. Zhao PGC-1α regulates expression of myocardial mitochondrial antioxidants and myocardial oxidative stress after chronic systolic overload Antioxid. Redox Signal. 13 2010 1011 1022
76. T. Malinski, F. Bailey, Z. Zhang, and M. Chopp Nitric oxide measured by a porphyrinic microsensor in rat brain after transient middle cerebral artery occlusion J. Cereb. Blood Flow Metab. 13 1993 355 358
77. S. Manzanero, T. Santro, and T.V. Arumugam Neuronal oxidative stress in acute ischemic stroke: sources and contribution to cell injury Neurochem. Int. 62 2013 712 718
78. B.E. Masel, and D.S. DeWitt Traumatic brain injury: a disease process, not an event J. Neurotrauma 27 2010 1529 1540
79. G. Mattiasson, M. Shamloo, G. Gido, K. Mathi, G. Tomasevic, S. Yi, C.H. Warden, R.F. Castilho, T. Melcher, and M. Gonzalez-Zulueta Uncoupling protein-2 prevents neuronal death and diminishes brain dysfunction after stroke and brain trauma Nat. Med. 9 2003 1062 1068
80. M.P. Mattson Hormesis defined Ageing Res. Rev. 7 2008 1 7
81. H.E. Mohamed, S.E. El-Swefy, R.A. Hasan, and A.A. Hasan Neuroprotective effect of resveratrol in diabetic cerebral ischemic-reperfused rats through regulation of inflammatory and apoptotic events Diabetol. Metab. Syndr. 6 2014 88 101
82. K.C. Morris-Blanco, C.H. Cohan, J.T. Neumann, T.J. Sick, and M.A. Perez-Pinzon Protein kinase C epsilon regulates mitochondrial pools of Nampt and NAD following resveratrol and ischemic preconditioning in the rat cortex J. Cereb. Blood Flow Metab.: Off. J. Int. Soc. Cereb. Blood Flow Metab. 34 2014 1024 1032
83. K.C. Morris, H.W. Lin, J.W. Thompson, and M.A. Perez-Pinzon Pathways for ischemic cytoprotection: role of sirtuins in caloric restriction, resveratrol, and ischemic preconditioning J. Cereb. Blood Flow Metab.: Off. J. Int. Soc. Cereb. Blood Flow Metab. 31 2011 1003 1019
84. V.P. Nakka, B.T. Lang, D.J. Lenschow, D.E. Zhang, R.J. Dempsey, and R. Vemuganti Increased cerebral protein ISGylation after focal ischemia is neuroprotective J. Cereb. Blood Flow Metab.: Off. J. Int. Soc. Cereb. Blood Flow Metab. 31 2011 2375 2384
85. V.P. Nakka, P. Prakash-babu, and R. Vemuganti Crosstalk between endoplasmic reticulum stress, oxidative stress, and autophagy: potential therapeutic targets for acute CNS injuries Mol. Neurobiol. 2014 1 13
86. S. Nolan Traumatic brain injury: a review Crit. Care Nurs. Q. 28 2005 188 194
87. T.P. Obrenovitch, and J. Urenjak Altered glutamatergic transmission in neurological disorders: from high extracellular glutamate to excessive synaptic efficacy Prog. Neurobiol. 51 1997 39 87
88. J.F. Padín, A.M. de Diego, J.C. Fernández-Morales, C. Merino, M. Maroto, E. Calvo-Gallardo, J.A. Arranz, M. Yáñez, and A.G. García Resveratrol augments nitric oxide generation and causes store calcium release in chromaffin cells Eur. J. Pharmacol. 685 2012 99 107
89. S.J. Park, F. Ahmad, A. Philp, K. Baar, T. Williams, H. Luo, H. Ke, H. Rehmann, R. Taussig, A.L. Brown, M.K. Kim, M.A. Beaven, A.B. Burgin, V. Manganiello, and J.H. Chung Resveratrol ameliorates aging-related metabolic phenotypes by inhibiting cAMP phosphodiesterases Cell 148 2012 421 433
90. A. Quincozes-Santos, L.D. Bobermin, A. Latini, M. Wajner, D.O. Souza, C.A. Goncalves, and C. Gottfried Resveratrol protects C6 astrocyte cell line against hydrogen peroxide-induced oxidative stress through heme oxygenase 1 PloS one 8 2013 e64372
91. J. Rachmat, S. Sastroasmoro, F.D. Suyatna, and G. Soejono Ischemic preconditioning reduces apoptosis in open heart surgery Asian Cardiovasc. Thorac. Ann. 22 2014 276 283
92. M. Ramos-Fernandez, M.F. Bellolio, and L.G. Stead Matrix metalloproteinase-9 as a marker for acute ischemic stroke: a systematic review J. Stroke Cerebrovasc. Dis. 20 2011 47 54
93. A.P. Raval, K.R. Dave, and M.A. Perez-Pinzon Resveratrol mimics ischemic preconditioning in the brain J. Cereb. Blood Flow Metab.: Off. J. Int. Soc. Cereb. Blood Flow Metab. 26 2006 1141 1147
94. S.D. Rege, S. Kumar, D.N. Wilson, L. Tamura, T. Geetha, S.T. Mathews, K.W. Huggins, T.L. Broderick, and J.R. Babu Resveratrol protects the brain of obese mice from oxidative damage Oxid. Med. Cell. Longev. 2013 2013 419092
95. J. Ren, C. Fan, N. Chen, J. Huang, and Q. Yang Resveratrol pretreatment attenuates cerebral ischemic injury by upregulating expression of transcription factor Nrf2 and HO-1 in rats Neurochem. Res. 36 2011 2352 2362
96. J.T. Rodgers, C. Lerin, W. Haas, S.P. Gygi, B.M. Spiegelman, and P. Puigserver Nutrient control of glucose homeostasis through a complex of PGC-1α and SIRT1 Nature 434 2005 113 118
97. Y. Sakata, H. Zhuang, H. Kwansa, R.C. Koehler, and S. Dore Resveratrol protects against experimental stroke: putative neuroprotective role of heme oxygenase 1 Exp. Neurol. 224 2010 325 329
98. 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
99. M.C. Saleh, B.J. Connell, and T.M. Saleh Resveratrol induced neuroprotection is mediated via both estrogen receptor subtypes, ER(alpha) and ER(beta) Neurosci. Lett. 548 2013 217 221
100. Y.-J. Shang, Y.-P. Qian, X.-D. Liu, F. Dai, X.-L. Shang, W.-Q. Jia, Q. Liu, J.-G. Fang, and B. Zhou Radical-scavenging activity and mechanism of resveratrol-oriented analogues: influence of the solvent, radical, and substitution J. Org. Chem. 74 2009 5025 5031
101. A.W. Shao, H.J. Wu, S. Chen, A.B. Ammar, J.M. Zhang, and Y. Hong Resveratrol attenuates early brain injury after subarachnoid hemorrhage through inhibition of NF-kappaB-dependent inflammatory/MMP-9 pathway CNS Neurosci. Ther. 20 2014 182 185
102. Y. Shigemori, Y. Katayama, T. Mori, T. Maeda, and T. Kawamata Matrix metalloproteinase-9 is associated with blood-brain barrier opening and brain edema formation after cortical contusion in rats Brain Edema XIII 2006 Springer 130 133
103. J.A. Shin, H. Lee, Y.K. Lim, Y. Koh, J.H. Choi, and E.M. Park Therapeutic effects of resveratrol during acute periods following experimental ischemic stroke J. Neuroimmunol. 227 2010 93 100
104. J.A. Shin, K.E. Lee, H.S. Kim, and E.M. Park Acute resveratrol treatment modulates multiple signaling pathways in the ischemic brain Neurochem. Res. 37 2012 2686 2696
105. J.A. Shin, S. Oh, J.H. Ahn, and E.M. Park Estrogen receptor-mediated resveratrol actions on blood-brain barrier of ovariectomized mice Neurobiol. Aging 36 2015 993 1006
106. E. Siemann, and L. Creasy Concentration of the phytoalexin resveratrol in wine Am. J. Enol. Vitic. 43 1992 49 52
107. N.A. Silva, N. Sousa, R.L. Reis, and A.J. Salgado From basics to clinical: a comprehensive review on spinal cord injury Prog. Neurobiol. 114 2014 25 57
108. F. Simao, A. Matte, C. Matte, F.M. Soares, A.T. Wyse, C.A. Netto, and C.G. Salbego Resveratrol prevents oxidative stress and inhibition of Na(+)K(+)-ATPase activity induced by transient global cerebral ischemia in rats J. Nutr. Biochem. 22 2011 921 928
109. F. Simao, A. Matte, A.S. Pagnussat, C.A. Netto, and C.G. Salbego Resveratrol preconditioning modulates inflammatory response in the rat hippocampus following global cerebral ischemia Neurochem. Int. 61 2012 659 665
110. F. Simao, A. Matte, A.S. Pagnussat, C.A. Netto, and C.G. Salbego Resveratrol prevents CA1 neurons against ischemic injury by parallel modulation of both GSK-3beta and CREB through PI3-K/Akt pathways Eur. J. Neurosci. 36 2012 2899 2905
111. F. Simao, A.S. Pagnussat, J.H. Seo, D. Navaratna, W. Leung, J. Lok, S. Guo, C. Waeber, C.G. Salbego, and E.H. Lo 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. Off. J. Int. Soc. Cereb. Blood Flow Metab. 32 2012 884 895
112. R.H. Singleton, H.Q. Yan, W. Fellows-Mayle, and C.E. Dixon Resveratrol attenuates behavioral impairments and reduces cortical and hippocampal loss in a rat controlled cortical impact model of traumatic brain injury J. Neurotrauma 27 2010 1091 1099
113. K. Sinha, G. Chaudhary, and Y. Kumar Gupta Protective effect of resveratrol against oxidative stress in middle cerebral artery occlusion model of stroke in rats Life Sci. 71 2002 655 665
114. J. Song, S.Y. Cheon, W. Jung, W.T. Lee, and J.E. Lee Resveratrol induces the expression of interleukin-10 and brain-derived neurotrophic factor in BV2 microglia under hypoxia Int. J. Mol. Sci. 15 2014 15512 15529
115. U. Sonmez, A. Sonmez, G. Erbil, I. Tekmen, and B. Baykara Neuroprotective effects of resveratrol against traumatic brain injury in immature rats Neurosci. Lett. 420 2007 133 137
116. M.R. Spasić, P. Callaerts, and K.K. Norga AMP-activated protein kinase (AMPK) molecular crossroad for metabolic control and survival of neurons Neurosci. 15 2009 309 316
117. J. St-Pierre, S. Drori, M. Uldry, J.M. Silvaggi, J. Rhee, S. Jäger, C. Handschin, K. Zheng, J. Lin, W. Yang, D.K. Simon, R. Bachoo, and B.M. Spiegelman Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators Cell 127 2006 397 408
118. J. St-Pierre, J. Lin, S. Krauss, P.T. Tarr, R. Yang, C.B. Newgard, and B.M. Spiegelman Bioenergetic analysis of peroxisome proliferator-activated receptor γ coactivators 1α and 1β (PGC-1α and PGC-1β) in muscle cells J. Biol. Chem. 278 2003 26597 26603
119. R.A. Stetler, R.K. Leak, Y. Gan, P. Li, F. Zhang, X. Hu, Z. Jing, J. Chen, M.J. Zigmond, and Y. Gao Preconditioning provides neuroprotection in models of CNS disease: paradigms and clinical significance Prog. Neurobiol. 114 2014 58 83
120. M. Takaoka Of the phenolic substances of white hellebore (Veratrum grandiflorum Loes. fil.) J. Fac. Sci. Hokkaido Imp. Univ. 3 1940 1 16
121. B.L. Tang Resveratrol is neuroprotective because it is not a direct activator of Sirt1-A hypothesis Brain Res. Bull. 81 2010 359 361
122. S.K. Tsai, L.M. Hung, Y.T. Fu, H. Cheng, M.W. Nien, H.Y. Liu, F.B. Zhang, and S.S. Huang Resveratrol neuroprotective effects during focal cerebral ischemia injury via nitric oxide mechanism in rats J. Vasc. Surg. 46 2007 346 353
123. Y.F. Tsai, F.C. Liu, Y.T. Lau, and H.P. Yu Role of Akt-dependent pathway in resveratrol-mediated cardioprotection after trauma-hemorrhage J. Surg. Res. 176 2012 171 177
124. H. Tsutsui, R. Tanaka, M. Yamagata, T. Yukimura, M. Ohkita, and Y. Matsumura Protective effect of ischemic preconditioning on ischemia/reperfusion-induced acute kidney injury through sympathetic nervous system in rats Eur. J. Pharmacol. 718 2013 206 212
125. Z. Ungvari, Z. Bagi, A. Feher, F.A. Recchia, W.E. Sonntag, K. Pearson, R. de Cabo, and A. Csiszar Resveratrol Confers Endothelial Protection via Activation of the Antioxidant Transcription Factor Nrf2 2010 H18 H24
126. M. Virgili, and A. Contestabile Partial neuroprotection of in vivo excitotoxic brain damage by chronic administration of the red wine antioxidant agent, trans-resveratrol in rats Neurosci. Lett. 281 2000 123 126
127. T. Wallerath, G. Deckert, T. Ternes, H. Anderson, H. Li, K. Witte, and U. Förstermann Resveratrol, a polyphenolic phytoalexin present in red wine, enhances expression and activity of endothelial nitric oxide synthase Circulation 106 2002 1652 1658
128. H.D. Wang, Y.M. Shi, L. Li, J.D. Guo, Y.P. Zhang, and S.X. Hou Treatment with resveratrol attenuates sublesional bone loss in spinal cord-injured rats Br. J. Pharmacol. 170 2013 796 806
129. L. Wang, Z.G. Zhang, R.L. Zhang, S.R. Gregg, A. Hozeska-Solgot, Y. LeTourneau, Y. Wang, and M. Chopp Matrix metalloproteinase 2 (MMP2) and MMP9 secreted by erythropoietin-activated endothelial cells promote neural progenitor cell migration J. Neurosci.: Off. J. Soc. Neurosci. 26 2006 5996 6003
130. M. Wang, H. Huang, S. Hsieh, K. Jeng, and J. Kuo Resveratrol inhibits interleukin-6 production in cortical mixed glial cells under hypoxia/hypoglycemia followed by reoxygenation J. Neuroimmunol. 112 2001 28 34
131. T. Wang, J. Gu, P.F. Wu, F. Wang, Z. Xiong, Y.J. Yang, W.N. Wu, L.D. Dong, and J.G. Chen Protection by tetrahydroxystilbene glucoside against cerebral ischemia: involvement of JNK, SIRT1, and NF-kappaB pathways and inhibition of intracellular ROS/RNS generation Free Radic. Biol. Med. 47 2009 229 240
132. T. West, M. Atzeva, and D.M. Holtzman Pomegranate polyphenols and resveratrol protect the neonatal brain against hypoxic-ischemic injury Dev. Neurosci. 29 2007 363 372
133. J.M. Westberry, A.K. Prewitt, and M.E. Wilson Epigenetic regulation of the estrogen receptor alpha promoter in the cerebral cortex following ischemia in male and female rats Neuroscience 152 2008 982 989
134. J.G. Wood, B. Rogina, S. Lavu, K. Howitz, S.L. Helfand, M. Tatar, and D. Sinclair Sirtuin activators mimic caloric restriction and delay ageing in metazoans Nature 430 2004 686 689
135. N. Xia, A. Daiber, A. Habermeier, E.I. Closs, T. Thum, G. Spanier, Q. Lu, M. Oelze, M. Torzewski, K.J. Lackner, T. Munzel, U. Forstermann, and H. Li Resveratrol reverses endothelial nitric-oxide synthase uncoupling in apolipoprotein E knockout mice J. Pharmacol. Exp. Ther. 335 2010 149 154
136. Y.-B. Yang, and Y.-J. Piao Effects of resveratrol on secondary damages after acute spinal cord injury in rats Acta Pharmacol. Sin. 24 2003 703 710
137. Y. Yang, W. Duan, Y. Li, J. Yan, W. Yi, Z. Liang, N. Wang, D. Yi, and Z. Jin New role of silent information regulator 1 in cerebral ischemia Neurobiol. aging 34 2013 2879 2888
138. F. Yeung, J.E. Hoberg, C.S. Ramsey, M.D. Keller, D.R. Jones, R.A. Frye, and M.W. Mayo Modulation of NF-κB-dependent transcription and cell survival by the SIRT1 deacetylase EMBO J. 23 2004 2369 2380
139. S. Yousuf, F. Atif, M. Ahmad, N. Hoda, T. Ishrat, B. Khan, and F. Islam Resveratrol exerts its neuroprotective effect by modulating mitochondrial dysfunctions and associated cell death during cerebral ischemia Brain Res. 1250 2009 242 253
140. H.P. Yu, T.L. Hwang, C.H. Yen, and Y.T. Lau Resveratrol prevents endothelial dysfunction and aortic superoxide production after trauma hemorrhage through estrogen receptor-dependent hemeoxygenase-1 pathway Crit. Care Med. 38 2010 1147 1154
141. L.L. Zamin, P. Dillenburg-Pilla, R. Argenta-Comiran, A.P. Horn, F. Simao, M. Nassif, D. Gerhardt, R.L. Frozza, and C. Salbego Protective effect of resveratrol against oxygen-glucose deprivation in organotypic hippocampal slice cultures: involvement of PI3-K pathway Neurobiol. Dis. 24 2006 170 182
142. R. Zamora, Y. Vodovotz, and T.R. Billiar Inducible nitric oxide synthase and inflammatory diseases Mol. Med. 6 2000 347
143. M. Zhang, C. An, Y. Gao, R.K. Leak, J. Chen, and F. Zhang Emerging roles of Nrf2 and phase II antioxidant enzymes in neuroprotection Prog. Neurobiol. 100 2013 30 47
144. X.M. Zhou, M.L. Zhou, X.S. Zhang, Z. Zhuang, T. Li, J.X. Shi, and X. Zhang Resveratrol prevents neuronal apoptosis in an early brain injury model J. Surg. Res. 189 2014 159 165
145. H. Zhuang, Y.-S. Kim, R.C. Koehler, and S. DorÉ Potential mechanism by which resveratrol, a red wine constituent, protects neurons Ann. N. Y. Acad. Sci. 993 2003 276 286
146. J.L. Zweier, and M.H. Talukder The role of oxidants and free radicals in reperfusion injury Cardiovasc. Res. 70 2006 181 190