Abstract
Cigarette smoking is concerned as a major risk factor in the development of various neurological disorders. Oxidative stress is suggested as a possible contributing factor in the pathogenesis of cigarette smoking-induced toxicity. Therefore, the present study was intended to evaluate the neuroprotective role of Sesbania grandiflora (S. grandiflora) against chronic cigarette smoke induced oxidative damage in rat brain. Adult male Wistar-Kyoto rats were exposed to cigarette smoke for a period of 90 days and consecutively treated with S. grandiflora aqueous suspension (SGAS, 1,000 mg/kg body weight per day by oral gavage) for a period of 3 weeks. Lipid peroxidation and antioxidants status were analyzed in the brain. Rats exposed to cigarette smoke showed significant increase in conjugated diens (CD), hydroperoxides (HP) and malendialdehyde (MDA) levels with concomitant decrease in superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPx), glutathione reductase (GR), glutathione-S-transferase (GST) and glucose-6-phosphate dehydrogenase (G6PDH) activities and the levels of reduced glutathione (GSH), vitamin C and vitamin E. Also cigarette smoke-exposure resulted in a marked increase in copper and decrease in zinc, manganese and selenium levels in brain. Administration of SGAS attenuates lipid peroxidation, enhanced the antioxidant status, restored the levels of micronutrients and retained the brain histology. The results of our study indicate that chronic cigarette smoke-exposure accelerates oxidative stress, thereby disquieting the brain defensive mechanism and S. grandiflora protects the brain from the oxidative damage through its biopotency.
References
Adikesavan G, Vinayagam MM, Abdulrahman LA, Chinnasamy T (2013) (−) Epigallocatechin-gallate (EGCG) stabilize the mitochondrial enzymes and inhibits the apoptosis in cigarette smoke-induced myocardial dysfunction in rats. Mol Biol Rep 40:6533–6545
Anbarasi K, Vani G, Balakrishna K, Devi CS (2006) Effect of bacoside A on brain antioxidant status in cigarette smoke exposed rats. Life Sci 78:1378–1384
Anbarasi K, Vani G, Balakrishna K, Devi CS (2005) Effect of bacoside A on membrane-bound ATPases in the brain of rats exposed to cigarette smoke. J Biochem Mol Toxicol 19:59–65
Barrett JR (2007) Dementia and second hand smoke. Environ Health Perspect 115:A401
Beuge JA, Aust SD (1978) The thiobarbituric acid assay. Methods Enzymol 52:306–307
Bou-Resli MN, Mathew TC, Dashti HM, Al-Zaid NS (2002) Brain selenium accumulation in rat pups of selenium supplemented mothers. Anat Histol Embryol 31:228–231
Brown KM, Morrice PC, Duthie GG (1997) Erythrocyte vitamin E and plasma ascorbate concentrations in relation to erythrocyte peroxidation in smokers and non-smokers: dose response to vitamin E supplementation. Am J Clin Nutr 65:496–502
Cataldo JK, Prochaska JJ, Glantz SA (2010) Cigarette smoking is a risk factor for Alzheimer's disease: an analysis controlling for tobacco industry affiliation. J Alzheimers Dis 19:465–480
Ching LS, Mohamed S (2001) Alpha-tocopherol content in 62 edible tropical plants. J Agric Food Chem 49:3101–3105
Coyle JT, Puttfarken P (1993) Oxidative stress, glutamate and neurodegenerative disorders. Science 262:689–695
Czubak A, Nowakowska E, Kus K, Sadowski C, Matschay A (2008) Effect of gabapentin on cognitive processes in rats not exposed and exposed to tobacco smoke during fetal life. Hum Exp Toxicol 27:883–894
Das P, Raghuramulu N, Rao KC (2005) Determination of in vitro availability of iron from common foods. J Hum Ecol 18:13–20
Desai ID (1984) Vitamin E analysis methods for animal tissues. Method Enzymol 105:138–147
Doddola S, Pasupulati H, Koganti B, Prasad KV (2008) Evaluation of Sesbania grandiflora for antiurolithiatic and antioxidant properties. J Nat Med 62:300–307
Dubick MA, Keen CL (1991) Influence of nicotine on tissue trace element concentrations and tissue antioxidant defense. Biol Trace Elem Res 31:97–109
Ellis HA, Kirkman HN (1961) A colorimetric method for assay of erythrocyte glucose-6-phosphatase dehydrogenase. Proc Soc Exp Biol Med 106:607–609
Eun-Mi P, Young-Mee P, Young-Seob G (1998) Oxidative damage in tissues of rats exposed to cigarette smoke. Free Radic Biol Med 25:79–86
Groten JP, Sinkeldam EJ, Muys T, Luten JB, Van Bladeren PJ (1991) Interaction of dietary Ca, P, Mg, Mn, Cu, Fe, Zn and Se with the accumulation and oral toxicity of cadmium in rats. Food Chem Toxicol 29:249–258
Habig WH, Pabst MJ, Jakpoby WB (1974) Glutathione transferase: a first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139
Jaques JA, Doleski PH, Castilhos LG et al (2013) Free and nanoencapsulated curcumin prevents cigarette smoke-induced cognitive impairment and redox imbalance. Neurobiol Learn Mem 100:98–107
Jiang ZY, Hunt JV, Wolff SP (1992) Ferrous ion oxidation in the presence of xylenol orange for detection of lipid hydroperoxide in low density lipoprotein. Annu Rev Plant Physiol Plant Mol Biol 202:384–387
Joshi SG (2000) Leguminoceae. Textbook of Medicinal Plants. Oxford and TBH Publishing Co Pvt Ltd, New Delhi, p 130
Kakkar B, Das PN, Viswanathan A (1984) Modified spectrophotometric assay of SOD. Ind J Biochem Biophys 21:130–132
Kasture VS, Deshmukh VK, Chopde CT (2002) Anxiolytic and anticonvulsive activity of Sesbania grandiflora leaves in experimental animals. Phytother Res 16:455–460
Koike K, Ishigami A, Sato Y et al (2014) Vitamin C prevents cigarette smoke-induced pulmonary emphysema in mice and provides pulmonary restoration. Am J Respir Cell Mol Biol 50:347–357
Kumaravel M, Karthiga K, Raviteja V, Rukkumani R (2011) Protective effects of Sesbania grandiflora on kidney during alcohol and polyunsaturated fatty acid-induced oxidative stress. Toxicol Mech Methods 21:418–425
Lapenna D, Mezzetti A, de Gioia S et al (1995a) Plasma copper and lipid peroxidation in cigarette smokers. Free Radic Biol Med 19:849–852
Lapenna D, de Gioia S, Mezzetti A et al (1995b) Cigarette smoke, ferritin, and lipid peroxidation. Am J Res Crit Car Med 151:431–435
Llewellyn DJ, Lang IA, Langa KM, Naughton F, Matthews FE (2009) Exposure to second hand smoke and cognitive impairment in nonsmokers: national cross sectional study with cotinine measurement. BMJ 338:b462
Lowry OH, Roseberg NJ, Farr AL, Randall RJ (1951) Protein measurements with folin phenol reagent. J Biol Chem 193:265–275
Luchese C, Pinton S, Nogueira CW (2009) Brain and lungs of rats are differently affected by cigarette smoke exposure: antioxidant effect of an organo selenium compound. Pharmacol Res 59:194–201
Mansvelder HD, Mertz M, Role LW (2009) Nicotinic modulation of synaptic transmission and plasticity in cortico-limbic circuits. Semin Cell Dev Biol 20:432–440
Mellick GD (2006) CYP450, genetics and Parkinson’s disease: gene x environment interactions hold the key. J Neural Transm Suppl 70:159–165
Moron MS, de Pierre JW, Mannervik B (1979) Levels of glutathione, glutathione reductase and glutathione-S-transferase in rat lung and liver. Biochim Biophys Acta 82:67–70
Mustafa RA, Hamid AA, Mohamed S, Bakar FA (2010) Total phenolic compounds, flavonoids, and radical scavenging activity of 21 selected tropical plants. J Food Science 75:C28–C35
Nowakowska E, Kus K, Florek E, Czubak A, Jodynis-Liebert J (2006) The influence of tobacco smoke and nicotine on antidepressant and memory-improving effects of venlafaxine. Hum Exp Toxicol 25:199–209
Omaye ST, Turnbull JD, Sauberlich HE (1979) Selected methods for the determinations of ascorbic acid in animal cell, tissues and fluids. Method Enzymol 67:1–11
Ozkan A, Fiskin K, Ayhan AG (2007) Effect of vitamin E and selenium on antioxidant enzymes in brain, kidney and liver of cigarette smoke-exposed mice. Biologia 62:360–364
Ozkol H, Tuluce Y, Koyuncu I (2012) Subacute effect of cigarette smoke exposure in rats: protection by pot marigold (Calendula officinalis L.) extract. Toxicol Ind Health 28:3–9
Pari L, Uma A (2003) Protective effect of Sesbania grandiflora against erythromycin estolate-induced hepatotoxicity. Therapie 58:439–443
Pryor WA, Stone K (1993) Oxidants in cigarette smoke: radicals, hydrogen peroxide, peroxynitrate, and peroxynitrite. Ann New York Acad Sci 686:12–27
Pryor WA (1997) Cigarette smoke radicals and the role of free radicals in chemical carcinogenicity. Environ Health Perspect 105:875–882
Ramesh T, Mahesh R, Hazeena Begum V (2007) Effect of Sesbania grandiflora on lung antioxidant defense system in cigarette smoke exposed rats. Int J Biol Chem 1:141–148
Ramesh T, Begum VH (2008) Protective effect of Sesbania grandiflora against cigarette smoke induced oxidative damage in rats. J Med Food 11:369–375
Ramesh T, Mahesh R, Sureka C, Begum VH (2008) Cardioprotective effects of Sesbania grandiflora in cigarette smoke-exposed rats. J Cardiovasc Pharmacol 52:338–343
Ramesh T, Sureka C, Bhuvana S, Hazeena Begum V (2010) Sesbania grandiflora diminishes oxidative stress and ameliorates antioxidant capacity in liver and kidney of rats exposed to cigarette smoke. J Physiol Pharmacol 61:467–476
Rotruck JT, Pope AL, Ganther HE et al (1973) Selenium: biochemical role as a component of glutathione peroxidase. Science 179:588–590
Shah RS, Cole JW (2010) Smoking and stroke: the more you smoke the more you stroke. Expert Rev Cardiovasc Ther 8:917–932
Shrivastav N, Janin SK (1993) Plants bearing antifertility properties. Hamdard Med 36:91–98
Sinha AK (1972) Colorimetric assay of catalase. Anal Biochem 47:389–394
Slater TI (1984) Overview of methods used for detecting lipid peroxidation. Method Enzymol 105:283–293
Smith CJ, Livingston SD, Doolittle DJ (1997) An international literature survey of IARC Group I carcinogens. Reported in main stream cigarette smoke. Food Chem Toxicol 35:1107–1130
Sreelatha S, Padma PR, Umasankari E (2011) Evaluation of anticancer activity of ethanol extract of Sesbania grandiflora (Agati Sesban) against Ehrlich ascites carcinoma in Swiss albino mice. J Ethnopharmacol 134:984–987
Staal GE, Visser J, Veeger C (1969) Purification and properties of glutathione reductase of human erythrocytes. Biochim Biophys Acta 185:39–48
Stangherlin EC, Luchese C, Ardais AP, Nogueira CW (2009) Passive smoke exposure induces oxidative damage in brains of rat pups: Protective role of diphenyl diselenide. Inhal Toxicol 21:868–874
Sulochana KN, Ramakrishnan S, Punitham R, Biju J (1998) Cadmium and superoxide dismutase in tobacco chewers with cataract. Ind J Pharmacol 30:413
Sundstrom P, Nystrom L, Hallmans G (2008) Smoke exposure increases the risk for multiple sclerosis. Eur J Neurol 15:579–583
Tamboli SA (2000) Analgesic and antipyretic activity of Sesbania grandiflora. Ind Drug 37:95–98
Tamboli SA (1996) Anti-inflammatory activity of Sesbania grandiflora. Ind Drug 33:504–506
The Wealth of India (1972) Raw materials, Vol. 9. Council of Scientific Industrial Research (CSIR); New Delhi, India pp 295–298
Thome GR, Spanevello RM, Mazzanti A et al (2011) Vitamin E decreased the activity of acetylcholinesterase and level of lipid peroxidation in brain of rats exposed to aged and diluted sidestream smoke. Nicotine Tob Res 13:1210–1219
Wu YL, Lin AH, Chen CH et al (2014) Glucosamine attenuates cigarette smoke-induced lung inflammation by inhibiting ROS-sensitive inflammatory signaling. Free Radic Biol Med 69:208–218
Zarena AS, Gopal S, Vineeth R (2014) Antioxidant, antibacterial, and cytoprotective activity of agathi leaf protein. J Anal Methods Chem 2014:989543. doi:10.1155/ 2014/ 989543
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Ramesh, T., Sureka, C., Bhuvana, S. et al. Oxidative stress in the brain of cigarette smoke-induced noxiousness: neuroprotective role of Sesbania grandiflora . Metab Brain Dis 30, 573–582 (2015). https://doi.org/10.1007/s11011-014-9614-4
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DOI: https://doi.org/10.1007/s11011-014-9614-4