Protective effect of resveratrol against chronic intermittent hypoxia-induced spatial memory deficits, hippocampal oxidative DNA damage and increased p47Phox NADPH oxidase expression in young rats

Behavioural Brain Research

Volumn 305, Issue , 2016, Pages 65-75

  Abdel Wahab, Basel A ^a   Abdel Wahab, Mahmoud M ^b  

^a Assiut University Faculty of Medicine   (Egypt)

^b FAYOUM UNIVERSITY   (Egypt)

Author keywords

DNA damage; Intermittent hypoxia; NADPH oxidase; Resveratrol; Sleep apnea

Indexed keywords

GLUTAMIC ACID; GLUTATHIONE; HEMOGLOBIN; PROTEIN P47; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RESVERATROL; THIOBARBITURIC ACID REACTIVE SUBSTANCE; 8-OXO-7-HYDRODEOXYGUANOSINE; DEOXYGUANOSINE; GLUTATHIONE REDUCTASE; NEUROPROTECTIVE AGENT; NEUTROPHIL CYTOSOLIC FACTOR 1; STILBENE DERIVATIVE;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; BIOCHEMISTRY; COGNITIVE DEFECT; CONTROLLED STUDY; DNA DAMAGE; DRUG MECHANISM; ELEVATED PLUS MAZE TEST; HIPPOCAMPUS; LEARNING DISORDER; MALE; MORRIS WATER MAZE TEST; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SLEEP DISORDERED BREATHING; SPATIAL MEMORY; ANALOGS AND DERIVATIVES; ANIMAL; COMPLICATION; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; GENETICS; HYPOXIA; MAZE TEST; MEMORY DISORDERS; METABOLISM; PATHOLOGY; REACTION TIME; WISTAR RAT;

ANIMALS; DEOXYGUANOSINE; DISEASE MODELS, ANIMAL; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUTAMIC ACID; GLUTATHIONE; GLUTATHIONE REDUCTASE; HEMOGLOBINS; HIPPOCAMPUS; HYPOXIA; MALE; MAZE LEARNING; MEMORY DISORDERS; NADPH OXIDASE; NEUROPROTECTIVE AGENTS; RATS; RATS, WISTAR; REACTION TIME; STILBENES; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

EID: 84960849836     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2016.02.030     Document Type: Article

References (65)

1. Morrell M., Twigg G. Neural consequences of sleep disordered breathing: the role of intermittent hypoxia. Adv. Exp. Med. Biol. 2006, 588:75-88.
2. Chang S., Chae K. Obstructive sleep apnea syndrome in children: epidemiology pathophysiology, diagnosis and sequelae. Korean J. Pediatr. 2010, 53:863-871.
3. Gozal D., Daniel J.M., Dohanich G.P. Behavioral and anatomical correlates of chronic episodic hypoxia during sleep in the rat. J. Neurosci. 2001, 21:2442-2450.
4. Arnaud C., Dematteis M., Pepin J., Baguet J., Lévy P. Obstructive sleep apnea, immuno-inflammation, and atherosclerosis. Semin. Immunol. Pathol. 2009, 31:113-125.
5. Nair D., Dayyat E.A., Zhang S.X., Wang Y., Gozal D. Intermittent hypoxia-induced cognitive deficits are mediated by NADPH oxidase activity in a murine model of sleep apnea. PLoS One 2011, 6:e19847.
6. Godoy J., Mellado P., Tapia J., Santin J. Obstructive sleep apnea as an independent stroke risk factor: possible mechanisms. Curr. Mol. Med. 2009, 9(2):203-209.
7. Shan X., Chi L., Ke Y., Luo C., Qian S.Y., Gozal D., et al. Manganese superoxide dismutase protects mouse cortical neurons from chronic intermittent hypoxia mediated oxidative damage. Neurobiol. Dis. 2007, 28:206-215.
8. Li R.C., Row B.W., Gozal E., Kheirandish L., Fan Q., Brittian K.R., Guo S.Z., Sachleben L.R., Gozal D. Cyclooxygenase 2 and intermittent hypoxia-induced spatial deficits in the rat. Am. J. Respir. Crit. Care Med. 2003, 168:469-475.
9. Li R.C., Row B.W., Kheirandish L., Brittian K.R., Gozal E., Guo S.Z., Sachleben L.R., Gozal D. Nitric oxide synthase and intermittent hypoxia-induced spatial learning deficits in the rat. Neurobiol. Dis. 2004, 17:44-53.
10. Nair D., Dayyat E.A., Zhang S.X., Wang Y., Gozal D. Intermittent hypoxia-induced cognitive deficits are mediated by NADPH oxidase activity in a murine model of sleep apnea. PLoS One 2011, 6:e19847. (Epub 12011 May 19823).
11. Veasey S.C., Davis C.W., Fenik P., Zhan G., Hsu Y.J., Pratico D., Gow A. Long-term intermittent hypoxia in mice: protracted hypersomnolence with oxidative injury to sleep-wake brain regions. Sleep 2004, 27:194-201.
12. Abdel-Wahab B.A., Abd El-Aziz S.M. Ginkgo biloba protects against intermittent hypoxia-induced memory deficits and hippocampal DNA damage in rats. Phytomedicine 2012, 19:444-450.
13. Zhao Y., Guo X., Wang H. The neuroprotective effects of grape seed proanthocyanidin on rat brain injury caused by chronic intermittent hypoxia. Neurol. Asia 2014, 19:399-403.
14. Lam C.S., Tipoe G.L., So K.F., Fung M.L. Neuroprotective mechanism of lycium barbarum polysaccharides against hippocampal-Dependent spatial memory deficits in a rat model of obstructive sleep apnea. PLoS One 2015, 10:e0117990.
15. Sun A.Y., Wang Q., Simonyi A., Sun G.Y. Botanical phenolics and brain health. Neuromol. Med. 2008, 10:259-274.
16. Orallo F. Comparative studies of the antioxidant effects of cis-and trans-resveratrol. Curr. Med. Chem. 2006, 13:87-98.
17. Baur J.A., Sinclair D.A. Therapeutic potential of resveratrol: the in vivo evidence. Nat. Rev. Drug Discov. 2006, 5:493-506.
18. Vingtdeux V., Dreses-Werringloer U., Zhao H., Davies P., Marambaud P. Therapeutic potential of resveratrol in Alzheimer's disease. BMC. Neurosci. 2008, 9(Suppl. 2):S6.
19. Das S., Das D.K. Anti-inflammatory responses of resveratrol. Inflamm. Allergy Drug Targets 2007, 6:168-173.
20. Liu G.S., Zhang Z.S., Yang B., He W. Resveratrol attenuates oxidative damage and ameliorates cognitive impairment in the brain of senescence-accelerated mice. Life Sci. 2012, 91:872-877.
21. Huang T.C., Lu K.T., Wo Y.Y., Wu Y.J., Yang Y.L. Resveratrol protects rats from Aβ-induced neurotoxicity by the reduction of iNOS expression and lipid peroxidation. PLoS One 2011, 6(12):e29102.
22. Ren J., Fan C., Chen N., Huang J., Yang Q. Resveratrol pretreatment attenuates cerebral ischemic injury by upregulating expression of transcription factor Nrf2 and HO-1 in rats. Neurochem. Res. 2011, 36:2352-2362.
23. Palacios J.A., Herranz D., De Bonis M.L., Velasco S., Serrano M., Blasco M.A. SIRT1 contributes to telomere maintenance and augments global homologous recombination. J. Cell Biol. 2010, 191:1299-1313.
24. Rajamohan S.B., Pillai V.B., Gupta M., Sundaresan N.R., Birukov K.G., Samant S., et al. SIRT1 promotes cell survival under stress by deacetylation-dependent deactivation of poly(ADP-ribose) polymerase 1. Mol. Cell. Biol. 2009, 29:4116-4129.
25. Cohen H.Y., Miller C., Bitterman K.J., Wall N.R., Hekking B., Kessler B., et al. Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase. Science 2004, 305(5682):390-392.
26. Lim J.H., Lee Y.M., Chun Y.S., Chen J., Kim J.E., Park J.W. Sirtuin 1 modulates cellular responses to hypoxia by deacetylating hypoxia-inducible factor 1alpha. Mol. Cell 2010, 38:864-878.
27. Rodgers J.T., Puigserver P. Fasting-dependent glucose and lipid metabolic response through hepatic sirtuin 1. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:12861-12866.
28. Purushotham A., Schug T.T., Xu Q., Surapureddi S., Guo X., Li X. Hepatocyte-specific deletion of SIRT1 alters fatty acid metabolism and results in hepatic steatosis and inflammation. Cell Metab. 2009, 9:327-338.
29. Hasegawa K., Yoshikawa K. Necdin regulates p53 acetylation via Sirtuin1 to modulate DNA damage response in cortical neurons. J. Neurosci. 2008, 28(35):8772-8784.
30. Yeung F., Hoberg J.E., Ramsey C.S., Keller M.D., Jones D.R., Frye R.A., Mayo M.W. Modulation of NF-kappa B-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J. 2004, 23:2369-2380.
31. Chakraborty S., Levenson A.S., Biswas P.K. Structural insights into Resveratrol's antagonist and partial agonist actions on estrogen receptor alpha. BMC Struct. Biol. 2013, 25(13):27.
32. Yao Y., Li J., Niu Y., Yu J.Q., Yan L., Miao Z.H., et al. Resveratrol inhibits oligomeric Aβ-induced microglial activation via NADPH oxidase. Mol. Med. Rep. 2015, 12:6133-6139.
33. Gozal D., Daniel J.M., Dohanich G.P. Behavioral and anatomical correlates of chronic episodic hypoxia during sleep in the rat. J. Neurosci. 2001, 21:2442-2450.
34. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Meth. 1984, 11:47-60.
35. File S.E. Behavioural detection of anxiolytic action. In Experimental Approaches to Anxiety and Depression 1992, 25-44. John Wiley & Sons, Marsden, CA. New York. J.M. Elliot, D.J. Heal (Eds.).
36. Ohkawa H., Ohishi N., Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 1979, 95:351-358.
37. Griffith O.W. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal. Biochem. 1980, 106:207-212.
38. Lund P. l-glutamine and l-glutamate: UV-method with glutaminase and glutamate dehydrogenase. Methods Enzyme Analys 1986, 357-363. VCH Verlagesllschaft, Weinheim. H.U. Bergmeyer (Ed.).
39. Paglia D.E., Valentine W.N. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J. Lab. Clin. Med. 1967, 70:158-169.
40. Lowry O., Rosenbrough N., Farr A., Randall R. Protein measurement with the Folinphenol reagent. J. Biol. Chem. 1951, 193:265-275.
41. Parle M., Singh N. Animal models of testing memory. Asia Pac. J. Pharmacol. 2004, 16:101-120.
42. Cai X.H., Zhou Y.H., Zhang C.X., Hu L.G., Fan X.F., Li C.C., et al. Chronic intermittent hypoxia exposure induces memory impairment in growing rats. Acta. Neurobiol. Exp. 2010, 70:279-287.
43. Al-Qahtani J.M., Abdel-Wahab B.A., Abd El-Aziz S.M. Long-term moderate dose exogenous erythropoietin treatment protects from intermittent hypoxia-induced spatial learning deficits and hippocampal oxidative stress in young rats. Neurochem. Res. 2014, 39:161-171.
44. Kheirandish L., Row B.W., Li R.C., Brittian K.R., Gozal D. Apolipoprotein E-deficient mice exhibit increased vulnerability to intermittent hypoxia-induced spatial learning deficits. Sleep 2005, 28:1412-1417.
45. Damián J.P., Acosta V., Da Cuña M., Ramírez I., Oddone N., Zambrana A., et al. Effect of resveratrol on behavioral performance of streptozotocin induced diabetic mice in anxiety tests. Exp. Anim. 2014, 63(3):277-287.
46. Campbell E.L., Johnston G.A.R. Resveratrol is a GABAC receptor antagonist. Proc. Aust. Neurosci. Soc. 2003, 14:P156.
47. Cho K.S., Lee E.J., Kwon K.J., Gonzales E.L., Kim Y.B., Cheong J.H., Bahn G.H., Lee J., Han S.H., Kim Y.T., Shin C.Y. Resveratrol down-regulates a glutamate-induced tissue plasminogen activator via Erk and AMPK/mTOR pathways in rat primary cortical neurons. Food Funct. 2014, 5:951-960.
48. Wang G., Amato S., Gilbert J., Man H.Y. Resveratrol up-regulates AMPA receptor expression via AMP-activated protein kinase-mediated protein translation. Neuropharmacology 2015, 95:144-153.
49. Rauchová H., Vokurková M., Koudelová J. Hypoxia-induced lipid peroxidation in the brain during postnatal ontogenesis. Physiol. Res. 2012, 61(Suppl. 1):S89-101.
50. Hensley K., Harris-White M.E. Redox regulation of autophagy in healthy brain and neurodegeneration. Neurobiol. Dis. 2015, 11(March). (Epub ahead of print).
51. Singh N., Agrawal M., Doré S., Singh N. Neuroprotective properties and mechanisms of resveratrol in in vitro and in vivo experimental cerebral strock models. ACS Chem. Neurosci. 2013, 4:1151-1162.
52. Khanduja K.L., Bhardwaj A. Stable free radical scavenging and antiperoxidative properties of resveratrol compared in vitro with some other bioflavonoids. Indian J. Biochem. Biophys. 2003, 40(December (6)):416-422.
53. Qureshi A.A., Guan X.Q., Reis J.C., Papasian C.J., Jabre S., Morrison D.C., Qureshi N. Inhibition of nitric oxide and inflammatory cytokines in LPS-stimulated murine macrophages by resveratrol, a potent proteasome inhibitor. Lipids Health Dis. 2012, 10(11):76.
54. Centeno-Baez C., Dallaire P., Marette A. Resveratrol inhibition of inducible nitric oxide synthase in skeletal muscle involves AMPK but not SIRT1. Am. J. Physiol. Endocrinol. Metab. 2011, 301:E922-30.
55. Cheng Y., Xue J., Jiang H., Wang M., Gao L., Ma D., Zhang Z. Neuroprotective effect of resveratrol on arsenic trioxide-induced oxidative stress in feline brain. Hum. Exp. Toxicol. 2014, 33:737-747.
56. Fukui M., Choi H.J., Zhu B.T. Mechanism for the protective effect of resveratrol against oxidative stress-induced neuronal death. Free Radic. Biol. Med. 2010, 49:800-813.
57. Ungvari Z., Bagi Z., Feher A., Recchia F.A., Sonntag W.E., Pearson K., de Cabo R., Csiszar A. Resveratrol confers endothelial protection via activation of the antioxidant transcription factor Nrf2. Am. J. Physiol. Heart Circ. Physiol. 2010, 299:H18-24.
58. Rakkar K., Srivastava K., Bayraktutan U. Attenuation of urokinase activity during experimental ischaemia protects the cerebral barrier from damage through regulation of matrix metalloproteinase-2 and NAD(P)H oxidase. Eur. J. Neurosci. 2014, 39:2119-2128.
59. Nisbet R.E., Graves A.S., Kleinhenz D.J., Rupnow H.L., Reed A.L., Fan T.H., et al. The role of NADPH oxidase in chronic intermittent hypoxia-induced pulmonary hypertension in mice. Am. J. Respir. Cell Mol. Biol. 2009, 40:601-609.
60. Nair D., Ramesh V., Gozal D. Adverse cognitive effects of high-fat diet in a murine model of sleep apnea are mediated by NADPH oxidase activity. Neuroscience 2012, 227:361-369.
61. Chen F., Qian L.H., Deng B., Liu Z.M., Zhao Y., Le Y.Y. Resveratrol protects vascular endothelial cells from high glucoseinduced apoptosis through inhibition of NADPH oxidase activation-driven oxidative stress. CNS Neurosci. Ther. 2013, 19:675-681.
62. He T., Guan X., Wang S., Xiao T., Yang K., Xu X., Wang J., Zhao J. Resveratrol prevents high glucose-induced epithelial-mesenchymal transition in renal tubular epithelial cells by inhibiting NADPH oxidase/ROS/ERK pathway. Mol. Cell. Endocrinol. 2015, 15(402):13-20.
63. Valavanidis A., Vlachogianni T., Fiotakis C. 8-hydroxy-2-deoxyguanosine (8-OHdG): a critical biomarker of oxidative stress and carcinogenesis. J. Environ. Sci. Health C: Environ. Carcinog. Ecotoxicol. Rev. 2009, 27:120-139.
64. Alturfan A.A., Tozan-Beceren A., Sehirli A.O., Demiralp E., Sener G., Omurtag G.Z. Resveratrol ameliorates oxidative DNA damage and protects against acrylamide-induced oxidative stress in rats. Mol. Biol. Rep. 2012, 39:4589-4596.
65. Zaky A., Mohammad B., Moftah M., Kandeel K.M., Bassiouny A.R. Apurinic/apyrimidinic endonuclease 1 is a key modulator of aluminum-induced neuroinflammation. BMC. Neurosci. 2013, 11(14):26.