Resveratrol pretreatment attenuates injury and promotes proliferation of neural stem cells following oxygen-glucose deprivation/reoxygenation by upregulating the expression of Nrf2, HO-1 and NQO1 in vitro

Molecular Medicine Reports

Volumn 14, Issue 4, 2016, Pages 3646-3654

  Shen, Changbo ^a   Cheng, Wei ^a   Yu, Pingping ^a   Wang, Li ^a   Zhou, Lulin ^a   Zeng, Li ^a   Yang, Qin ^a  

^a THE FIRST AFFILIATED HOSPITAL OF CHONGQING MEDICAL UNIVERSITY   (China)

Author keywords

Apoptosis; Neural stem cells; Oxidative stress; Oxygen glucose deprivation reoxygenation; Resveratrol

Indexed keywords

GLUCOSE; GLUTATHIONE; HEME OXYGENASE 1; MALONALDEHYDE; OXYGEN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOPHATE) DEHYDROGENASE (QUINONE) 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); RESVERATROL; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; ANTIOXIDANT; NEUROPROTECTIVE AGENT; NFE2L2 PROTEIN, RAT; NQO1 PROTEIN, RAT; STILBENE DERIVATIVE;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL NUCLEUS; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; FEMALE; FLOW CYTOMETRY; IN VITRO STUDY; MALE; NERVOUS SYSTEM INJURY; NEURAL STEM CELL; NEWBORN; NONHUMAN; PROTEIN CONTENT; PROTEIN DETERMINATION; PROTEIN EXPRESSION; RAT; REOXYGENATION; UPREGULATION; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; METABOLISM; OXIDATIVE STRESS; PATHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; CELL PROLIFERATION; CELLS, CULTURED; FEMALE; GLUCOSE; HEME OXYGENASE-1; MALE; NAD(P)H DEHYDROGENASE (QUINONE); NEURAL STEM CELLS; NEUROPROTECTIVE AGENTS; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; OXYGEN; RATS, SPRAGUE-DAWLEY; STILBENES;

EID: 84988507768     PISSN: 17912997     EISSN: 17913004     Source Type: Journal    
DOI: 10.3892/mmr.2016.5670     Document Type: Article

References (39)

1. Keuters MH, Aswendt M, Tennstaedt A, Wiedermann D, Pikhovych A, Rotthues S, Fink GR, Schroeter M, Hoehn M and Rueger MA: Transcranial direct current stimulation promotes the mobility of engrafted NSCs in the rat brain. NMR Biomed 28: 231-239, 2015.
2. Lu P, Graham L, Wang Y, Wu D and Tuszynski M: Promotion of survival and differentiation of neural stem cells with fibrin and growth factor cocktails after severe spinal cord injury. J Vis Exp: e50641, 2014.
3. Sarnowska A, Jablonska A, Jurga M, Dainiak M, Strojek L, Drela K, Wright K, Tripathi A, Kumar A, Jungvid H, et al: Encapsulation of mesenchymal stem cells by bioscaffolds protects cell survival and attenuates neuroinflammatory reaction in injured brain tissue after transplantation. Cell Transplant 22 (Suppl 1): S67-S82, 2013.
4. Tang S, Liao X, Shi B, Qu Y, Huang Z, Lin Q, Guo X and Pei F: The effects of controlled release of neurotrophin-3 from PCLA scaffolds on the survival and neuronal differentiation of transplanted neural stem cells in a rat spinal cord injury model. PLoS One 9: e107517, 2014.
5. Liang Y, Walczak P and Bulte JW: The survival of engrafted neural stem cells within hyaluronic acid hydrogels. Biomaterials 34: 5521-5529, 2013.
6. Walle T: Bioavailability of resveratrol. Ann N Y Acad Sci 1215: 9-15, 2011.
7. Baur JA and Sinclair DA: Therapeutic potential of resveratrol: The in vivo evidence. Nat Rev Drug Discov 5: 493-506, 2006.
8. Lin HY, Tang HY, Davis FB and Davis PJ: Resveratrol and apoptosis. Ann N Y Acad Sci 1215: 79-88, 2011.
9. Sinha K, Chaudhary G and Gupta YK: Protective effect of resveratrol against oxidative stress in middle cerebral artery occlusion model of stroke in rats. Life Sci 71: 655-665, 2002.
10. Jin F, Wu Q, Lu YF, Gong QH and Shi JS: Neuroprotective effect of resveratrol on 6-OHDA-induced Parkinson's disease in rats. Eur J Pharmacol 600: 78-82, 2008.
11. Li F, Gong Q, Dong H and Shi J: Resveratrol, a neuroprotective supplement for Alzheimer's disease. Curr Pharm Des 18: 27-33, 2012.
12. Li Z, Pang L, Fang F, Zhang G, Zhang J, Xie M and Wang L: Resveratrol attenuates brain damage in a rat model of focal cerebral ischemia via up-regulation of hippocampal Bcl-2. Brain Res 1450: 116-124, 2012.
13. Madhyastha S, Sekhar S and Rao G: Resveratrol improves postnatal hippocampal neurogenesis and brain derived neurotrophic factor in prenatally stressed rats. Int J Dev Neurosci 31: 580-585, 2013.
14. Moriya J, Chen R, Yamakawa J, Sasaki K, Ishigaki Y and Takahashi T: Resveratrol improves hippocampal atrophy in chronic fatigue mice by enhancing neurogenesis and inhibiting apoptosis of granular cells. Biol Pharm Bull 34: 354-359, 2011.
15. Ren JW, Fan C, Chen N, Huang J and Yang Q: Resveratrol pretreatment attenuates cerebral ischemic injury by upregulating expression of transcription factor Nrf2 and HO-1 in rats. Neurochem Res 36: 2352-2362, 2011.
16. Gorbunov N, Petrovski G, Gurusamy N, Ray D, Kim doH and Das DK: Regeneration of infarcted myocardium with resveratrol-modified cardiac stem cells. J Cell Mol Med 16: 174-184, 2012.
17. Mohagheghi F, Khalaj L, Ahmadiani A and Rahmani B: Gemfibrozil pretreatment affecting antioxidant defense system and inflammatory, but not Nrf-2 signaling pathways resulted in female neuroprotection and male neurotoxicity in the rat models of global cerebral ischemia-reperfusion. Neurotox Res 23: 225-237, 2013.
18. Zhang DD: Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug metab Rev 38: 769-789, 2006.
19. Ping Z, Liu W, Kang Z, Cai J, Wang Q, Cheng N, Wang S, Wang S, Zhang JH and Sun X: Sulforaphane protects brains against hypoxic-ischemic injury through induction of Nrf2-dependent phase 2 enzyme. Brain Res 1343: 178-185, 2010.
20. Reynolds BA, Tetzlaff W and Weiss S: A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci 12: 4565-4574, 1992.
21. Andersen RK, Johansen M, Blaabjerg M, Zimmer J and Meyer M: Neural tissue-spheres: A microexplant culture method for propagation of precursor cells from the rat forebrain subventricular zone. J Neurosci Methods 165: 55-63, 2007.
22. Babu H, Claasen JH, Kannan S, Rünker AE, Palmer T and Kempermann G: A protocol for isolation and enriched monolayer cultivation of neural precursor cells from mouse dentate gyrus. Front Neurosci 5: 89, 2011.
23. Chen T, Liu W, Chao X, Qu Y, Zhang L, Luo P, Xie K, Huo J and Fei Z: Neuroprotective effect of osthole against oxygen and glucose deprivation in rat cortical neurons: Involvement of mitogen-activated protein kinase pathway. Neuroscience 183: 203-211, 2011.
24. Wu X, Zhao J, Yu S, Chen Y, Wu J and Zhao Y: Sulforaphane protects primary cultures of cortical neurons against injury induced by oxygen-glucose deprivation/reoxygenation via anti-apoptosis. Neurosci Bull 28: 509-516, 2012.
25. Harada N, Zhao J, Kurihara H, Nakagata N and Okajima K: Resveratrol improves cognitive function in mice by increasing production of insulin-like growth factor-I in the hippocampus. J Nutr Biochem 22: 1150-1159, 2011.
26. Park HR, Kong KH, Yu BP, Mattson MP and Lee J: Resveratrol inhibits the proliferation of neural progenitor cells and hippocampal neurogenesis. J Biol Chem 287: 42588-42600, 2012.
27. Leong CW, Wong CH, Lao SC, Leong EC, Lao IF, Law PT, Fung KP, Tsang KS, Waye MM, Tsui SK, et al: Effect of resveratrol on proliferation and differentiation of embryonic cardiomyoblasts. Biochem Biophys Res Commun 360: 173-180, 2007.
28. Slemmer JE, Shacka JJ, Sweeney MI and Weber JT: Antioxidants and free radical scavengers for the treatment of stroke, traumatic brain injury and aging. Curr Med Chem 15: 404-414, 2008.
29. Nassar NN, Abdelsalam RM, Abdel-Rahman AA and Abdallah DM: Possible involvement of oxidative stress and inflammatory mediators in the protective effects of the early preconditioning window against transient global ischemia in rats. Neurochem Res 37: 614-621, 2012.
30. Oh YI, Kim JH and Kang CW: Protective effect of short-term treatment with parathyroid hormone 1-34 on oxidative stress is involved in insulin-like growth factor-I and nuclear factor erythroid 2-related factor 2 in rat bone marrow derived mesenchymal stem cells. Regul Pept 189: 1-10, 2014.
31. De la Lastra CA and Villegas I: Resveratrol as an antioxidant and pro-oxidant agent: Mechanisms and clinical implications. Biochem Soc Trans 35: 1156-1160, 2007.
32. Konyalioglu S, Armagan G, Yalcin A, Atalayin C and Dagci T: Effects of resveratrol on hydrogen peroxide-induced oxidative stress in embryonic neural stem cells. Neural Regen Res 8: 485-495, 2013.
33. Maher J and Yamamoto M: The rise of antioxidant signaling-the evolution and hormetic actions of Nrf2. Toxicol Appl Pharmacol 244: 4-15, 2010.
34. Quincozes-Santos A, Bobermin LD, Latini A, Wajner M, Souza DO, Gonçalves CA and Gottfried C: Resveratrol protects C6 astrocyte cell line against hydrogen peroxide-induced oxidative stress through heme oxygenase 1. PloS One 8: e64372, 2013.
35. Yang C, Zhang X, Fan H and Liu Y: Curcumin upregulates transcription factor Nrf2, HO-1 expression and protects rat brains against focal ischemia. Brain Res 1282: 133-141, 2009.
36. Sakata Y, Zhuang H, Kwansa H, Koehler RC and Doré S: Resveratrol protects against experimental stroke: Putative neuroprotective role of heme oxygenase 1. Exp Neurol 224: 325-329, 2010.
37. Lin TK, Chen SD, Chuang YC, Lin HY, Huang CR, Chuang JH, Wang PW, Huang ST, Tiao MM, Chen JB and Liou CW: Resveratrol partially prevents rotenone-induced neurotoxicity in dopaminergic SH-SY5Y cells through induction of heme oxygenase-1 dependent autophagy. Int J Mol Sci 15: 1625-1646, 2014.
38. Ghanim H, Sia CL, Korzeniewski K, Lohano T, Abuaysheh S, Marumganti A, Chaudhuri A and Dandona P: A resveratrol and polyphenol preparation suppresses oxidative and inflammatory stress response to a high-fat, high-carbohydrate meal. J Clin Endocrinol Metab 96: 1409-1414, 2011.
39. Gurusamy N, Ray D, Lekli I and Das DK: Red wine antioxidant resveratrol-modified cardiac stem cells regenerate infarcted myocardium. J Cell Mol Med 14: 2235-2239, 2010.