Effects of resveratrol on hydrogen peroxide-induced oxidative stress in embryonic neural stem cells

doi:10.3969/j.issn.1673-5374.2013.06.001

Abstract

Abstract:

Resveratrol, a natural phenolic compound, has been shown to prevent cardiovascular diseases and cancer and exhibit neuroprotective effects. In this study, we examined the neuroprotective and antioxidant effects of resveratrol against hydrogen peroxide in embryonic neural stem cells. Hydrogen peroxide treatment alone increased catalase and glutathione peroxidase activities but did not change superoxide dismutase levels compared with hydrogen peroxide + resveratrol treatment. Nitric oxide synthase activity and concomitant nitric oxide levels increased in response to hydrogen peroxide treatment. Conversely, resveratrol treatment decreased nitric oxide synthase activity and nitric oxide levels. Resveratrol also attenuated hydrogen peroxide-induced nuclear or mitochondrial DNA damage. We propose that resveratrol may be a promising agent for protecting embryonic neural stem cells because of its potential to decrease oxidative stress by inducing higher activity of antioxidant enzymes, decreasing nitric oxide production and nitric oxide synthase activity, and alleviating both nuclear and mitochondrial DNA damage.

Key words: neural regeneration, traditional Chinese medicine, stem cells, resveratrol, embryonic neural stem cells, hydrogen peroxide, catalase, glutathione peroxidase, nitric oxide synthase, nitric oxide, DNA damage, neuroprotection, grants-supported paper, neuroregeneration

Sibel Konyalioglu, Guliz Armagan, Ayfer Yalcin, Cigdem Atalayin, Taner Dagci. Effects of resveratrol on hydrogen peroxide-induced oxidative stress in embryonic neural stem cells[J]. Neural Regeneration Research, 2013, 8(6): 485-495.

References

[1] Coyle JT, Puttfarcken P. Oxidative stress, glutamate, and neurodegenerative disorders. Science. 1993;262(5134): 689-695.

[2] Dringen R. Metabolism and functions of glutathione in brain. Prog Neurobiol. 2000;62:649-471.

[3] Lafon-Cazal M, Culcasi M, Gaven F, et al. Nitric oxide, superoxide and peroxynitrite: putative mediators of NMDA-induced cell death in cerebellar granule cells. Neuropharmacology. 1993;32(11):1259-1266.

[4] Dickens MG, Franz KJ. A prochelator activated by hydrogen peroxide prevents metal-induced amyloid-aggregation. Chem Biochem. 2010;11(1):59-62.

[5] Yamato M, Kudo W, Shiba T, et al. Determination of ROS associated with the degeneration of dopaminergic neurons during dopamine metabolism. Free Radic Res. 2010;44(3):249-257.

[6] Fernández-Ferreiro A, Gil-Longo J.Vascular pro-oxidant effects related to the autoxidation of dopamine. Free Radic Res. 2009;43(3):295-303.

[7] Arthur PG, Lim SC, Meloni BP, et al. The protective effect of hypoxic preconditioning on cortical neuronal cultures is associated with increases in the activity of several antioxidant enzymes. Brain Res. 2004;1017(1-2):146-154.

[8] Floyd RA, Carney JM. Free radical damage to protein and DNA: mechanisms involved and relevant observations on brain undergoing oxidative stress. Ann Neurol. 1992; Suppl:S22-27.

[9] Gutteridge JM. Hydroxyl radicals, iron, oxidative stress, and neurodegeneration. Ann N Y Acad Sci. 1994;738: 201-213.

[10] Malins DC, Polissar NL, Gunselman SJ. Progression of human breast cancers to the metastatic state is linked to hydroxyl radical-induced DNA damage. Proc Natl Acad Sci U S A. 1996;93(6):2557-2563.

[11] Chen X, Zhang Q, Cheng Q, et al. Protective effect of salidroside against H2O2-induced cell apoptosis in primary culture of rat hippocampal neurons. Mol Cell Biochem. 2009;332(1-2):85-93.

[12] Silani V, Corbo M. Cell-replacement therapy with stem cells in neurodegenerative diseases. Curr Neurovasc Res. 2004;1(3):283-289.

[13] Kimura H, Yoshikawa M, Matsuda R, et al. Transplantation of embryonic stem cell-derived neural stem cells for spinal cord injury in adult mice. Neurol Res. 2005;27(8):812-829.

[14] Kerr DA, Lladó J, Shamblott MJ, et al. Human embryonic germ cell derivatives facilitate motor recovery of rats with diffuse motor neuron injury. J Neurosci. 2003;23 (12): 5131-5140.

[15] Klein SM, Behrstock S, McHugh J, et al. GDNF delivery using human neural progenitor cells in a rat model of ALS. Hum Gene Ther. 2005;16(4):509-521.

[16] Lee J, Ryu H, Kowall NW. Differential regulation of neuronal and inducible nitric oxide synthase (NOS) in the spinal cord of mutant SOD1 (G93A) ALS mice. Biochem Biophys Res Commun. 2009;387(1):202-206.

[17] Bacigaluppi M, Pluchino S, Peruzzotti-Jametti L, et al. Delayed post-ischaemic neuroprotection following systemic neural stem cell transplantation involves multiple mechanisms. Brain. 2009;132(Pt 8):2239-2251.

[18] Gescher AJ, Steward WP. Relationship between mechanisms, bioavailibility, and preclinical chemopreventive efficacy of resveratrol: A conundrum. Cancer Epidemiol Biomarkers Prev. 2003;12(10):953-957.

[19] Wenzel E, Somaza V. Metabolism and bioavailability of trans-resveratrol. Mol Nutr Food Res. 2004;49(5):472-481.

[20] Delmas D, Lançon A, Colin D, et al. Resveratrol as a chemopreventive agent: a promising molecule for fighting cancer. Curr Drug Targets. 2006;7(4):423-442.

[21] Das S, Fraga CG, Das DK. 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. 2006;40(10):1066-1075.

[22] Chanvitayapongs S, Draczynska-Lusiak B, Sun AY. Amelioration of oxidative stress by antioxidants and resveratrol in PC12 cells. Neuroreport. 1997;8(6): 1499-1502.

[23] Tredici G, Miloso M, Nicolini G, et al. Resveratrol, map kinases and neuronal cells: might wine be a neuroprotectant? Drugs Exp Clin Res. 1999;25(2-3): 99-103.

[24] Marambaud P, Zhao H, Davies P. Resveratrol promotes clearance of Alzheimer's disease amyloid-beta peptides. J Biol Chem. 2005;280(45):37377-37382.

[25] Quincozes-Santos A, Andreazza AC, Nardin P, et al. Resveratrol attenuates oxidative-induced DNA damage in C6 Glioma cells. Neurotoxicology. 2007;28(4):886-891.

[26] Mancuso C, Bates TE, Butterfield DA, et al. Natural antioxidants in Alzheimer's disease. Expert Opin Investig Drugs. 2007;16(12):1921-1931.

[27] Donfack HJ, Kengap RT, Ngameni B, et al. Ficus cordata thunb (moraceae) is a potential source of some hepatoprotective and antioxidant compounds. Pharmacologia. 2011;2 (5):137-145.

[28] Ozyurt D, Demirata B, Apak R. Determination of total antioxidant capacity by a new spectrophotometric method based on Ce(IV) reducing capacity measurement. Talanta.     2007;71(3):1155-1165.

[29] López M, Mart??nez F, Del Valle C, et al. Study of phenolic compounds as natural antioxidants by a fluorescence method. Talanta. 2003;60(2-3):609-616.

[30] Chen AS, Taguchi T, Sakai K, et al. Antioxidant activities of chitobiose and chitotriose. Biol Pharm Bull. 2003;26(9): 1326-1330.

[31] Han SS, Kang DY, Mujtaba T, et al. Grafted lineage- restricted precursors differentiate exclusively into neurons in the adult spinal cord. Exp Neurol. 2003;177(2):360-375.

[32] Lepore AC, Fischer I. Lineage-restricted neural precursors survive, migrate, and differentiate following transplantation into the injured adult spinal cord. Exp Neurol. 2005;194(1): 230-242.

[33] Lepore AC, Han SS, Tyler-Polsz CJ, et al. Differential fate of multipotent and lineage-restricted neural precursors following transplantation into the adult CNS. Neuron Glia Biol. 2004;1(2):113-126.

[34] Bastianetto S, Zheng WH, Quirion R. Neuroprotective abilities of resveratrol and other red wine constituents against nitric oxide-related toxicity in cultured hippocampal neurons. Br J Pharmacol. 2000;131(4): 711-720.

[35] Koh JY, Choi DW. Quantitative determination of glutamate mediated cortical neuronal injury in cell culture by lactate dehydrogenase efflux assay. J Neurosci Methods. 1987; 20(1):83-90.

[36] Kendig DM, Tarloff JB. Inactivation of lactate dehydrogenase by several chemicals: implications for in vitro toxicology studies. Toxicol In Vitro. 2007;21(1): 125-132.

[37] Aebi H. Catalase in vitro. Methods Enzymol. 1984;105: 121-126.

[38] Rikans LE, Hornbrook KR. Lipid peroxidation, antioxidant protection and aging. Biochim Biophys Acta. 1997;1362: 116-127.

[39] El-Far MA, Bakr MA, Farahat SE, et al. Glutathione peroxidase activity in patients with renal disorders. Clin Exp Nephrol. 2005;9(2):127-131.

[40] Hamada Y, Ikata T, Katoh S, et al. Roles of nitric oxide in compression injury of rat spinal cord. Free Rad Biol Med. 1996;20:1-9.

[41] Tice RR, Agurell E, Anderson D, et al. Single cell gel/ comet assay: guide for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen. 2000;35: 206-221.

[42] Nadin SB, Vargas-Roig M, Ciocca R. A silver staining method for single-cell gel assay. J Histochem Cytochem. 2001;49:1183-1186.

[43] Spanier G, Xu H, Xia N, et al. Resveratrol reduces of superoxide dismutase 1, glutathione peroxidase 1 and NADPH oxidase subunit (Nox4). J Physiol Pharmacol. 2009;60(4):111-116.

[44] Théry C, Chamak B, Mallat M. Cytotoxic effect of brain macrophages on developing. Eur J Neurosci. 1991;3(11): 1155-1164.

[45] Desagher S, Glowinski J, Premont J. Astrocytes protect neurons from hydrogen peroxide toxicity. J Neurosci. 1996; 16(8):2553-2562.

[46] De Ruvo C, Amodio R, Algeri S, et al. Nutritional antioxidants as antidegenerative agents. Int J Dev Neurosci. 2000;18(4-5):359-366.

[47] Rubiolo JA, Vega FV. Resveratrol protects primary rat hepatocytes against necrosis induced by reactive oxygen species. Biomed Pharmacother. 2008;62(9):606-612.

[48] Miura T, Muraoka S, Ikeda N, et al. Antioxidative and prooxidative action of stilbene derivatives. Pharmacol Toxicol. 2000;86(5):203-208.

[49] Jang JH, Surh YJ. Protective effects of resveratrol on hydrogen peroxide-induced apoptosis in rat pheochromocytoma (PC12) cells. Mutat Res. 2001; 496(1-2):181-190.

[50] Pervaiz S. Resveratrol: from grapevines to mammalian biology. FASEB J. 2003;17(14):1975-1985.

[51] King RE, Kent KD, Bomser JA. Resveratrol reduces oxidation and proliferation of human retinal pigment epithelial cells via extracellular signal-regulated kinase         inhibition. Chem Biol Interact. 2005;151(2):143-149.

[52] Hirrlinger J, Resch A, Gutterer JM, et al. Oligodendroglial cells in culture effectively dispose of exogenous hydrogen peroxide: comparison with cultured neurones, astroglial and microglial cells. J Neurochem. 2002;82(3):635-644.

[53] Buckman TD, Sutphin MS, Mitrovic B. Oxidative stress in a clonal cell line of neuronal origin: effects of antioxidant enzyme modulation. J Neurochem. 1993;60(6):2046-2058.

[54] Behl C, Davis JB, Lesley R, et al. Hydrogen peroxide mediates amyloid beta protein toxicity. Cell. 1994;77(6): 817-827.

[55] Whittemore ER, Loo DT, Cotman CW. Exposure to hydrogen peroxide induces cell death via apoptosis in cultured rat cortical neurons. Neuroreport. 1994;5(12): 1485-1488.

[56] Okawara M, Katsuki H, Kurimoto E, et al. Resveratrol protects dopaminergic neurons in midbrain slice culture from multiple insults. Biochem Pharmacol. 2007;73(4): 550-560.

[57] Zini R, Morin C, Bertelli A, et al. Effects of resveratrol on the rat brain respiratory chain. Drugs Exp Clin Res. 1999;25:87-97.

[58] Li Y, Cao Z, Zhu H. Upregulation of endogenous antioxidants and phase 2 enzymes by the red wine polyphenol, resveratrol in cultured aortic smooth muscle cells leads to cytoprotection against oxidative and electrophilic stress. Pharmacol Res. 2006;53(1):6-15.

[59] Good PF, Werner P, Hsu A, et al. Evidence of neuronal oxidative damage in Alzheimer's disease. Am J Pathol. 1996;149(1):21-28.

[60] Good PF, Hsu A, Werner P, et al. Protein nitration in Parkinson's disease. J Neuropathol Exp Neurol. 1998; 57(4):338-342.

[61] Beal MF, Ferrante RJ, Browne SE, et al. Increased 3-nitrotyrosine in both sporadic and familial amyotrophic lateral sclerosis. Ann Neurol. 1997;42(4):644-654.

[62] Lee ST, Chu K, Jung KH, et al. Anti-inflammatory mechanism of intravascular neural stem cell transplantation in haemorrhagic stroke. Brain. 2008; 131(Pt 3):616-629.

[63] Meneghini R. Genotoxicity of active oxygen species in mammalian cells. Mutat Res. 1988;195(3):215-230.

[64] Villani P, Altavista PL, Castaldi L, et al. Analysis of DNA damage related to cell proliferation. Mutat Res. 2000;464: 229-237.

[65] Kowaltowski AJ, Vercesi AE. Mitochondrial damage induced by conditions of oxidative stress. Free Radic Biol Med. 1999;26(3-4):463-471.

[66] Birch-Machin MA. The role of mitochondria in ageing and carcinogenesis. Clin Exp Dermatol. 2006;31(4):548-552.

[67] Zini R, Morin C, Bertelli A, et al. Resveratrol-induced limitation of dysfunction of mitochondria isolated from rat brain in an anoxia-reoxygenation model. Life Sci. 2002;71: 3091-3108.

[68] Morin C, Zini R, Albengres E, et al. Evidence for resveratrol-induced preservation of brain mitochondria functions after hypoxia-reoxygenation. Drugs Exp Clin Res. 2003;29:227-233.

[69] Parker JA, Arango M, Abderrahmane S, et al. Resveratrol rescues mutant polyglutamine cytotoxicity in nematode and mammalian neurons. Nat Genet. 2005;37:349-350.

[70] Valenzano DR, Terzibasi E, Genade T, et al. Resveratrol prolongs lifespan and retards the onset of age-related markers in a short-lived vertebrate. Curr Biol. 2006;16(3): 296-300.