Abstract
Background: Prenatal-stress-induced neuronal damage in offspring is multifactorial, including oxidative damage in the developing brain. Resveratrol is known to exert its neuroprotective potentials by upregulating several antioxidant systems. Hence, the study was undertaken to evaluate the neuroprotective effect of resveratrol against prenatal-stress-induced hippocampal damage and oxidative damage in neonate rat brains.
Methods: Pregnant rats were subjected to restraint stress during early or late gestational period. Another set of rats received resveratrol during the entire gestational period along with early or late gestational stress. The study parameters included several antioxidant studies directly from rat brain homogenate on the 40th postnatal day and hippocampal neuronal assay on the 21st postnatal day.
Results: Early as well as late gestational stress resulted in a significant increase in lipid peroxidation and advanced oxidation protein products and decrease in total antioxidant activity and nitric oxide levels in rat brain homogenate. The neurons of the dentate gyrus were severely affected in early and late gestational stress, and only the neurons of the CA3 region were adversely affected in late gestational stress. Administration of resveratrol reversed the prenatal-stress-induced oxidative damage and neurons of dentate gyrus but not the CA3 hippocampal neurons.
Conclusions: These results show the neuroprotective abilities of resveratrol against prenatal-stress-induced oxidative damage in neonatal rat brain.
The authors would like to thank the Indian Council of Medical Research (ICMR), New Delhi, for funding the present work (IRIS ID No. 2008-00150).
Conflict of interest statement
Authors’ conflict of interest disclosure: The authors stated that there are no conflicts of interest regarding the publication of this article. Research funding played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.
Research funding: None declared.
Employment or leadership: None declared.
Honorarium: None declared.
References
1. Lemaire V, Koehl M, Le-Moal M, Abrous DN. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 2000;97:11032–7.10.1073/pnas.97.20.11032Search in Google Scholar
2. Reznikov AG, Nosenko ND, Tarasenko LV, Sinitsyn PV, Polyakova LI. Early and long-term neuroendocrine effects of prenatal stress in male and female rats. Neurosci Behav Physiol 2011;31:1–5.10.1023/A:1026623427246Search in Google Scholar
3. Fameli M, Kitraki E, Stylianopoulou F. Effects of hyperactivity of the maternal hypothalamic-pituitary-adrenal (HPA) axis during pregnancy on the development of the HPA axis and brain monoamines of the offspring. Int J Dev Neurosci 1994;12:651–9.10.1016/0736-5748(94)90017-5Search in Google Scholar
4. Zhu Z, Li X, Chen W, Zhao Y, Li H, Qing C, et al. Prenatal stress causes gender dependent neuronal loss and oxidative stress in rat hippocampus. J Neurosci Res 2004;78:837–44.10.1002/jnr.20338Search in Google Scholar
5. Soleas GJ, Diamandis EP, Goldberg DM. Wine as a biological fluid: history, production, and role in disease prevention. J Clin Lab Anal 199;11:287–313.10.1002/(SICI)1098-2825(1997)11:5<287::AID-JCLA6>3.0.CO;2-4Search in Google Scholar
6. Sinha K, Chaudhary G, Gupta YK. Protective effect of resveratrol against oxidative stress in middle cerebral artery occlusion model of stroke in rats. Life Sci 2002;6:655–65.10.1016/S0024-3205(02)01691-0Search in Google Scholar
7. Yang YB, Piao YJ. Effects of resveratrol on secondary damages after acute spinal cord injury in rats. Acta Pharmacol Sin 2003;24:703–10.Search in Google Scholar
8. Mokni M, Elkahoui S, Limam F, Amri M, Aouani E. Effect of resveratrol on antioxidant enzyme activities in the brain of healthy rat. Neurochem Res 2007;32:981–7.10.1007/s11064-006-9255-zSearch in Google Scholar
9. Sonmez U, Sonmez A, Ebril G, Tekmen I, Baykara B. Neuroprotective effect of resveratrol against traumatic brain injury in immature rats. Neurosci Lett 2007;420:133–7.10.1016/j.neulet.2007.04.070Search in Google Scholar
10. Ates O, Cayli SR, Yucel N, Altinoz E, Kocak A, Durak MA, et al. Central nervous system protection by resveratrol in streptozotocin-induced diabetic rats. J Clin Neurosci 2007;14:256–60.10.1016/j.jocn.2005.12.010Search in Google Scholar
11. Choi SY, Kim S, Son SD, Lee P, Lee J, Lee S, et al. Protective effect of (4-methoxybenzylidene)-(3-methoxynophenyl) amine against neuronal cell death induced by oxygen and glucose deprivation in rat organotypic hippocampal slice culture. Biol Pharm Bull 2007;30:189–92.10.1248/bpb.30.189Search in Google Scholar
12. Okawara M, Katsuki H, Kurimoto E, Shibata H, Kume T, Akaike A. Resveratrol protects dopaminergic neurons in midbrain slice culture from multiple insults. Biochem Pharmacol 2007;73: 550–60.10.1016/j.bcp.2006.11.003Search in Google Scholar
13. Aziz MH, Nihal M, Fu VX, Jarrard DF, Ahmad N. Resveratrol-caused apoptosis of human prostate carcinoma LNCaP cells is mediated via modulation of phosphatidylinositol 3′-kinase/Akt pathway and Bcl-2 family proteins. Mol Cancer Ther 2006;5:1335–41.10.1158/1535-7163.MCT-05-0526Search in Google Scholar
14. Williams LD, Burdock GA, Edwards J, Beck M, Bausch J. Safety studies conducted on high-purity trans-resveratrol in experimental animals. Food Chem Toxicol 2009;47: 2170–82.10.1016/j.fct.2009.06.002Search in Google Scholar
15. Holson RR, Pearce B. Principles and pitfalls in the analysis of prenatal treatment effects in multiparous species. Neurotoxicol Teratol 1992;14:221–8.10.1016/0892-0362(92)90020-BSearch in Google Scholar
16. Madhyastha S, Prabhu LV, Nayak SR, Pai M, Rajalakshmi, Madhyastha P. Effect of Prenatal stress and serotonin depletion on postnatal serotonin metabolism in Wistar rats. Iran J Pharmacol Ther 2008;7:71–7.Search in Google Scholar
17. Madhyastha S, Bairy KL, Nalini K, Somayaji SN. Role of hippocampus in methotrexate induced learning and memory deficit. Can J Physiol Pharmacol 2002;80:1076–84.10.1139/y02-135Search in Google Scholar
18. Buege JA, Aust SD. Microsomal lipid peroxidation. Methods Enzymol 1978;52:302–10.10.1016/S0076-6879(78)52032-6Search in Google Scholar
19. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265–75.10.1016/S0021-9258(19)52451-6Search in Google Scholar
20. Witko-Sarsat VM, Friedlander C, Capeillere-Blandin T, Nguyen-Khoa AT, Nguyen J, Zingraff P, et al. Advanced oxidation protein products as a novel marker of oxidative stress in uremia. Kidney Int 1996;49:1304–13.10.1038/ki.1996.186Search in Google Scholar
21. Koracevic D, Koracevic G, Djordjevic V, Andeejevic S, Cosic V. Method for the measurement of antioxidant activity in human fluids. J Clin Pathol 2001;54:356–61.10.1136/jcp.54.5.356Search in Google Scholar
22. Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem 1982;126:131–8.10.1016/0003-2697(82)90118-XSearch in Google Scholar
23. Fujioka A, Fujioka T, Ishida Y, Maekawa T, Nakamura S. Differential effects of prenatal stress on the morphological maturation of hippocampal neurons. Neurosci 2006;141:907–15.10.1016/j.neuroscience.2006.04.046Search in Google Scholar
24. Reul JM, de Kloet ER. Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 1985;117:2505–11.10.1210/endo-117-6-2505Search in Google Scholar
25. Ylinen A, Bragin A, Nadasdy Z, Jando G, Szabo I, Sik A, et al. Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 1995;15:30–46.10.1523/JNEUROSCI.15-01-00030.1995Search in Google Scholar
26. Rao MK, Rao MS, Rao GS. Centella asiatica (Linn) induced behavioural changes during growth spurt period in neonatal rats. Neuroanatomy 2005;4:18–23.Search in Google Scholar
27. 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 2006;131:711–20.10.1038/sj.bjp.0703626Search in Google Scholar
28. Liu J, Mori A. Stress, aging, and brain oxidative damage. Neurochem Res 1999;24:1479–97.10.1023/A:1022597010078Search in Google Scholar
29. Inoue H, Jiang XF, Katayama T, Osada S, Umesono K, Namura S. Brain protection by resveratrol and fenofibrate against stroke requires peroxisome proliferator-activated receptor a in mice. Neurosci Lett 2003;352:203–6.10.1016/j.neulet.2003.09.001Search in Google Scholar
30. Tadolini B, Juliano C, Piu L, Franconi F, Cabrini L. Resveratrol inhibition of lipid peroxidation. Free Radic Res 2000;33:104–14.10.1080/10715760000300661Search in Google Scholar
31. Chanvitayapongs S, Draczynska-Lusiak B, Sun AY. Amelioration of oxidative stress by antioxidants and resveratrol in PC12 cells. Neuroreport 1997;8:1499–502.10.1097/00001756-199704140-00035Search in Google Scholar
32. Zini R, Morin C, Berteli A, Berteli AA, Tillement JP. Effects of resveratrol on the rat brain respiratory chain. Drugs Exp Clin Res 1999;25:87–97.Search in Google Scholar
33. Mizutani K, Ikeda K, Kawai Y, Yamori Y. Protective effective of resveratrol on oxidative damage in male and female stroke-prone spontaneously hypertensive rats. Clin Exp Pharmacol Physiol 2001;28:55–9.10.1046/j.1440-1681.2001.03415.xSearch in Google Scholar
34. Wang Q, Xu J, Rottinghaus GE, Simonyi A, Lubahn D, Sun GY, et al. Resveratrol protects against global cerebral ischemic injury in gerbils. Brain Res 2002;958:439–47.10.1016/S0006-8993(02)03543-6Search in Google Scholar
35. Zhang F, Shi JS, Zhou H, Wilson B, Hong JS, Gao HM. Resveratrol protects dopamine neurons against lipopolysaccharide induced neurotoxicity through its anti-inflammatory actions. Mol Pharmacol 2010;78:466–77.10.1124/mol.110.064535Search in Google Scholar
36. Esterbauer H. Cytotoxicity and genotoxicity of lipid oxidation products. Am J Clin Nutr 1993;57:785–6.10.1093/ajcn/57.5.779SSearch in Google Scholar
37. Liu J, Yeo HC, Doniger SJ, Ames BN. Assay of aldehydes from lipid peroxidation: gas chromatography-mass spectrometry compared to thiobarbituric acid. Anal Biochem 1997;245:161–6.10.1006/abio.1996.9990Search in Google Scholar
38. Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat Cell Biol 2001;3:193–7.10.1038/35055104Search in Google Scholar
39. Choi YB, Tenneti L, Le DA, Ortiz J, Bai G, Chen HS, et al. Molecular basis of NMDA receptor coupled ion channel modulation by S-nitrosylation. Nat Neurosci 2000;3:15–21.10.1038/71090Search in Google Scholar
40. Lipton SA, Singel DJ, Stamler JS. Nitric oxide in the central nervous system. Brain Res 1994;103:359–64.10.1016/S0079-6123(08)61149-8Search in Google Scholar
41. Riccio A, Alvania RS, Lonze BE, Ramanan N, Kim T, Huang Y, et al. A nitric oxide signalling pathway controls CREB-mediated gene expression in neurons. Mol Cell 2006;21:283–94.10.1016/j.molcel.2005.12.006Search in Google Scholar PubMed
42. Mancuso C, Scapagini G, Curro D, Giuffrida AM, De Marco C, Butterfield DA, et al. Mitochondrial dysfunction, free radical generation and cellular stress response in neurodegenerative disorders. Front Biosci 2007;2:1107–23.10.2741/2130Search in Google Scholar PubMed
43. Kiziltepe U, Turan NN, Han U, Ulus AT, Akar F. Resveratrol a red wine polyphenol, protects spinal cord from ischemia reperfusion injury. J Vasc Surg 2004;40:138–45.10.1016/j.jvs.2004.03.032Search in Google Scholar PubMed
44. Han YS, Bastianetto S, Dumont Y, Quirion R. Specific plasma membrane binding sites for polyphenols, including resveratrol in the rat brain. J Pharmacol Exp Ther 2006;318:238–45.10.1124/jpet.106.102319Search in Google Scholar PubMed
©2014 by Walter de Gruyter Berlin Boston
Articles in the same Issue
- Masthead
- Masthead
- Review
- The relationship between oxidative stress and exercise
- Original articles
- Testosterone promotes glucose intolerance, lipid disorder and oxidative stress in type 1 diabetic rats
- Inhibition of key enzymes linked to type 2 diabetes and sodium nitroprusside-induced lipid peroxidation in rat pancreas by water-extractable phytochemicals from unripe pawpaw fruit (Carica papaya)
- Influence of gallic acid on oxidative stress-linked streptozotocin-induced pancreatic dysfunction in diabetic rats
- The evaluation of the hypoglycemic effect of soft drink leaf extract of Phyllanthus amarus (Euphorbiaceae) in rats
- Antioxidant activities for superoxide dismutase in patients with Crohn’s disease
- Resveratrol for prenatal-stress-induced oxidative damage in growing brain and its consequences on survival of neurons
- Hepatoprotective role of kaempferol during alcohol- and ΔPUFA-induced oxidative stress
- Evaluation of antiulcerogenic potential of antioxidant α-tocopherol in pylorus-ligated albino rats
- Comparison of the penetration and passage of Streptococcus mutans and Aggregatibacter actinomycetemcomitans through membranes loaded with tetracycline, amoxicillin, and chlorhexidine: an in vitro study
- Sodium-hydrogen exchanger inhibitory potential of Malus domestica, Musa × paradisiaca, Daucus carota, and Symphytum officinale
- Methylglyoxal causes endothelial dysfunction: the role of endothelial nitric oxide synthase and AMP-activated protein kinase α
- Reversal of alcohol induced testicular hyperlipidemia by supplementation of ascorbic acid and its comparison with abstention in male guinea pigs
- A cross-sectional study of surveillance of adverse drug reactions in inpatient departments of a tertiary care hospital
Articles in the same Issue
- Masthead
- Masthead
- Review
- The relationship between oxidative stress and exercise
- Original articles
- Testosterone promotes glucose intolerance, lipid disorder and oxidative stress in type 1 diabetic rats
- Inhibition of key enzymes linked to type 2 diabetes and sodium nitroprusside-induced lipid peroxidation in rat pancreas by water-extractable phytochemicals from unripe pawpaw fruit (Carica papaya)
- Influence of gallic acid on oxidative stress-linked streptozotocin-induced pancreatic dysfunction in diabetic rats
- The evaluation of the hypoglycemic effect of soft drink leaf extract of Phyllanthus amarus (Euphorbiaceae) in rats
- Antioxidant activities for superoxide dismutase in patients with Crohn’s disease
- Resveratrol for prenatal-stress-induced oxidative damage in growing brain and its consequences on survival of neurons
- Hepatoprotective role of kaempferol during alcohol- and ΔPUFA-induced oxidative stress
- Evaluation of antiulcerogenic potential of antioxidant α-tocopherol in pylorus-ligated albino rats
- Comparison of the penetration and passage of Streptococcus mutans and Aggregatibacter actinomycetemcomitans through membranes loaded with tetracycline, amoxicillin, and chlorhexidine: an in vitro study
- Sodium-hydrogen exchanger inhibitory potential of Malus domestica, Musa × paradisiaca, Daucus carota, and Symphytum officinale
- Methylglyoxal causes endothelial dysfunction: the role of endothelial nitric oxide synthase and AMP-activated protein kinase α
- Reversal of alcohol induced testicular hyperlipidemia by supplementation of ascorbic acid and its comparison with abstention in male guinea pigs
- A cross-sectional study of surveillance of adverse drug reactions in inpatient departments of a tertiary care hospital