Skip to main content

Advertisement

SpringerLink
Log in

Brain oxidative damage restored by Sesbania grandiflora in cigarette smoke-exposed rats

  • Research Article
  • Published:
Metabolic Brain Disease Aims and scope Submit manuscript

Abstract

Cigarette smoking has been associated with high risk of neurological diseases such as stroke, Alzheimer’s disease, multiple sclerosis, etc., The present study was designed to evaluate the restorative effects of Sesbania grandiflora (S. grandiflora) on oxidative damage induced by cigarette smoke exposure in the brain of rats. 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, 1000 mg/kg body weight per day by oral gavage) for a period of 3 weeks. The levels of protein carbonyl, nitric oxide, and activities of cytochrome P450, NADPH oxidase and xanthine oxidase were significantly increased, whereas the levels of total thiol, protein thiol, non-protein thiol, nucleic acids, tissue protein and the activities of Na+/K+-ATPase, Ca2+-ATPase and Mg2+-ATPase were significantly diminished in the brain of rats exposed to cigarette smoke as compared with control rats. Also cigarette smoke exposure resulted in a significant alteration in brain total lipid, total cholesterol, triglycerides and phospholipids content. Treatment of SGAS is regressed these alterations induced by cigarette smoke. The results of our study suggest that S. grandiflora restores the brain from cigarette smoke induced oxidative damage. S. grandiflora could have rendered protection to the brain by stabilizing their cell membranes and prevented the protein oxidation, probably through its free radical scavenging and anti-peroxidative effect.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Anbarasi K, Vani G, Balakrishna K, Devi CS (2005a) Effect of bacoside A on membrane-bound ATPases in the brain of rats exposed to cigarette smoke. J Biochem Mol Toxicol 19:59–65

    Article  CAS  PubMed  Google Scholar 

  • Anbarasi K, Vani G, Devi CS (2005b) Protective effect of bacoside A on cigarette smoking-induced brain mitochondrial dysfunction in rats. J Environ Pathol Toxicol Oncol 24:225–234

    Article  CAS  PubMed  Google Scholar 

  • Ballentine R, Burford DD (1957) Determination of metals. In: Colowick SP, Kaplan NO (eds) Methods in enzymology, vol 3. Academic, New York, pp 1002–1035

    Google Scholar 

  • Bonting SL (1970) Sodium-potassium activated adenosine triphosphatase and cation transport. In: Bittar EE (ed) Membrane and ion transport, vol I. Wiley-Interscience, London, pp 257–363

    Google Scholar 

  • Burton K (1956) A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochem J 62:315–323

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chelland Campbell S, Moffatt RJ, Stamford BA (2008) Smoking and smoking cessation: the relationship between cardiovascular disease and lipoprotein metabolism. Atherosclerosis 201:225–235

    Article  PubMed  Google Scholar 

  • Ching LS, Mohamed S (2001) Alpha-tocopherol content in 62 edible tropical plants. J Agric Food Chem 49:3101–3105

    Article  CAS  PubMed  Google Scholar 

  • Czekaj P, Wiaderkiewicz A, Florek E, Wiaderkiewicz R (2005) Tobacco smoke-dependent changes in cytochrome P450 1A1, 1A2, and 2E1 protein expressions in fetuses, newborns, pregnant rats, and human placenta. Arch Toxicol 79:13–24

    Article  CAS  PubMed  Google Scholar 

  • Dajas-Bailador FA, Soliakov L, Wonnacott S (2002) Nicotine activates the extracellular signal-regulated kinase 1/2 via the (α) 7 nicotinic acetylcholine receptor and protein kinase A, in SH-SY5Y cells and hippocampal neurons. J Neurochem 80:520–534

    Article  CAS  PubMed  Google Scholar 

  • Das P, Raghuramulu N, Rao KC (2005) Determination of in vitro availability of iron from common foods. J Hum Ecol 18:13–20

    Google Scholar 

  • Das S, Gautam N, Dey SK, Maiti T, Roy S (2009) Oxidative stress in the brain of nicotine-induced toxicity: protective role of Andrographis paniculata Nees and vitamin E. Appl Physiol Nutr Metab 34:124–135

    Article  CAS  PubMed  Google Scholar 

  • Deliconstantinos G, Villiotou V (2000) Gas phase oxidants of cigarette smoke increase nitric oxide synthase and xanthine oxidase activities of rabbit brain synaptosomes. Neurochem Res 25:769–774

    Article  CAS  PubMed  Google Scholar 

  • Dhanya CR, Indu AR, Deepadevi KV, Kurup PA (2003) Inhibition of membraneNa+-K+ ATPase of brain, liver and RBC in rats administered di(2-ethyl hexyl) phthalate (DEHP), a plasticizer used in polyvinyl chloride (PVC) blood storage bags. Indian J Exp Biol 41:814–820

    CAS  PubMed  Google Scholar 

  • Dilsiz N, Olcucu A, Cay M, Naziroglu M, Cabanoglu D (1999) Protective effects of selenium, vitamin C and vitamin E against oxidative stress of cigarette smoke in rats. Cell Biochem Funct 17:1–7

    Article  CAS  PubMed  Google Scholar 

  • Doddola S, Pasupulati H, Koganti B, Prasad KV (2008) Evaluation of Sesbania grandiflora for antiurolithiatic and antioxidant properties. J Nat Med 62:300–307

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Fadillioglu E, Yilmaz HR, Erdogan H, Sogut S (2003) The activities of tissue xanthine oxidase and adenosine deaminase and the levels of hydroxyproline and nitric oxide in rat hearts subjected to doxorubicin: protective effect of erdosteine. Toxicology 191:153–158

    Article  CAS  PubMed  Google Scholar 

  • Fiske CV, Subbarow Y (1925) Calorimetric determination of phosphorus. J Biol Chem 66:75–400

    Google Scholar 

  • Folch J, Lee M, Sloanes SH (1957) A simple method for the unknown and purification of total lipids from unknown tissues. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  • Foster LB, Dunn RT (1973) Stable reagents for the determination of serum triglycerides by a colorimetric hanzsob condensation method. J Clin Chem 82:473–482

    Google Scholar 

  • Fraga DB, Deroza PF, Ghedim FV et al (2011) Prenatal exposure to cigarette smoke causes persistent changes in the oxidative balance and in DNA structural integrity in rats submitted to the animal model of schizophrenia. J Psychiatr Res 45:1497–1503

    Article  PubMed  Google Scholar 

  • Haga H (1992) Effects of dietary magnesium supplementation on diurnal variations of blood pressure and plasma Na+-K+ ATPase activity in essential hypertension. Jpn Heart J 33:785–800

    Article  CAS  PubMed  Google Scholar 

  • Hjerten S, Pan H (1983) Purification and characterization of two forms of a low affinity Ca2 + −ATPase from erythrocyte membranes. Biochim Biophys Acta 728:281–288

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Joshi SG (2000) Leguminoceae. Textbook of medicinal plants. Oxford and TBH Publishing Co Pvt Ltd, New Delhi, p 130

    Google Scholar 

  • Kasture VS, Deshmukh VK, Chopde CT (2002) Anxiolytic and anticonvulsive activity of Sesbania grandiflora leaves in experimental animals. Phytother Res 16:455–460

    Article  PubMed  Google Scholar 

  • Khanna A, Guo M, Mehra M, Royal W III (2013) Inflammation and oxidative stress induced by cigarette smoke in Lewis rat brains. J Neuroimmunol 254:69–75

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Levine RL, Garland D, Oliver CN, Amici A, Lenz AZ, Ahn B, Shaltiel S, Stadtman ER (1990) Assay of carbonyl in protein. Methods Enzymol 186:464–478

    Article  CAS  PubMed  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–276

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5:62–71

    Article  CAS  PubMed  Google Scholar 

  • Mustafa RA, Hamid AA, Mohamed S, Bakar FA (2010) Total phenolic compounds, flavonoids, and radical scavenging activity of 21 selected tropical plants. J Food Sci 75:C28–C35

    Article  CAS  PubMed  Google Scholar 

  • Ohnishi T, Suzuki T, Suzuki Y, Ozawa K (1982) A comparative study of plasma membrane Mg2+-ATPase activities in normal, regenerating and malignant cells. Biochim Biophys Acta 684:67–74

    Article  CAS  PubMed  Google Scholar 

  • Omura T, Sato R (1964) The carbon monoxide-binding pigment of liver microsomes: I. Evidence for its hemoprotein nature. J Biol Chem 239:2370–2378

    CAS  PubMed  Google Scholar 

  • Ozkol H, Tülüce 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

    Article  PubMed  Google Scholar 

  • Pacher P, Beckman JS, Liaudet L (2007) Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87:315–424

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Panayiotidis MI, Stabler SP, Allen RH, Ahmed A, White CW (2004) Cigarette smoke extract inceases S-adenosyl methionine and cystathionine in human lung epithelial-like (A549) cells. Chem Biol Interact 147:87–97

    Article  CAS  PubMed  Google Scholar 

  • Parekh AC, Jung DH (1970) Determination of cholesterol with ferric acetate, uranyl acetate, sulfuric acid, and ferrous sulfate reagents. Anal Chem 42:1523–1529

    Article  Google Scholar 

  • Pari L, Uma A (2003) Protective effect of Sesbania grandiflora against erythromycin estolate-induced hepatotoxicity. Therapie 58:439–443

    Article  PubMed  Google Scholar 

  • Pelletier MR, Wadia JS, Mills LR, Carlen PL (1999) Seizureinduced cell death produced by repeated tetanic stimulation in vitro: possible role of endoplasmic reticulum calcium stores. J Neurophysiol 81:3054–3064

    CAS  PubMed  Google Scholar 

  • Pryor WA, Stone K (1993) Oxidants in cigarette smoke. Radicals, hydrogen peroxide, peroxynitrate, and peroxynitrite. Ann N Y Acad Sci 686:12–27

    Article  CAS  PubMed  Google Scholar 

  • Ramesh T, Begum VH (2008) Protective effect of Sesbania grandiflora against cigarette smoke induced oxidative damage in rats. J Med Food 11:369–375

    Article  CAS  PubMed  Google Scholar 

  • Ramesh T, Mahesh R, Begum VH (2007) Effect of Sesbania grandiflora on membrane- bound ATP-ases in cigarette smoke-exposed rats. J Physiol Toxicol 2:559–566

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Ramesh T, Sureka C, Bhuvana S, Begum VH (2014) Oxidative stress in the brain of cigarette smoke-induced noxiousness: neuroprotective role of Sesbania grandiflora. Metab Brain Dis. doi:10.1007/s11011-014-9614-4

    PubMed  Google Scholar 

  • Rani PJA, Panneerselvam C (2001) The role of L-carnitine in the activities of membrane-bound enzymes in the brains of aged rats. J Anti-aging Med 4:147–155

    Article  Google Scholar 

  • Rawal UM, Patel US, Rao GN, Desai RR (1977) Clinical and biochemical studies on cateractous human lens. III. Quantitative study of protein, RNA and DNA. Arogya J Health Sci 3:69–72

    Google Scholar 

  • Rivlin RS (2001) Riboflavin. In: Bowman BA, Rusell RM (eds) Present knowledge in nutrition. ILSI Press, Washington DC, pp 191–198

    Google Scholar 

  • Sakuma S, Fujimoto Y, Sakamoto Y, Uchiyama T, Yoshioka K, Nishida H, Fujita T (1997) Peroxynitrite induces the conversion of xanthine dehydrogenase to oxidase in rabbit liver. Biochem Biophys Res Commun 230:476–479

    Article  CAS  PubMed  Google Scholar 

  • Sawa T, Tatemichi M, Akaike T, Barbin A, Ohshima H (2006) Analysis of urinary 8-nitroguanine, a marker of nitrative nucleic acid damage, by high-performance liquid chromatography–electrochemical detection coupled with immunoaffinity purification: association with cigarette smoking. Free Radic Biol Med 40:711–720

    Article  CAS  PubMed  Google Scholar 

  • Sedlak J, Lindsay RH (1968) Estimation of total, protein bound, and non-protein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25:192–205

    Article  CAS  PubMed  Google Scholar 

  • Shrivastav N, Janin SK (1993) Plants bearing antifertility properties. Hamdard Med 36:91–98

    Google Scholar 

  • Sinko I, Morocz M, Zadori J, Kokavszky K, Rasko I (2005) Effect of cigarette smoking on DNA damage of human cumulus cells analysed by comet assay. Reprod Toxicol 20:65–71

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Steyn-Parve EP, Benert H (1958) On the mechanism of dehydrogenation of fatty acyl derivatives of coenzyme A. J Biol Chem 233:843–852

    CAS  PubMed  Google Scholar 

  • Stripe F, Della Corte E (1969) The regulation of rat liver xanthine oxidase. J Biol Chem 244:3855–3863

    Google Scholar 

  • Swan GE, Lessov-Schlaggar CN (2007) The effects of tobacco smoke and nicotine on cognition and the brain. Neuropsychol Rev 17:259–273

    Article  PubMed  Google Scholar 

  • Tamboli SA (1996) Anti-inflammatory activity of Sesbania grandiflora. Ind Drug 33:504–506

    Google Scholar 

  • Tamboli SA (2000) Analgesic and antipyretic activity of Sesbania grandiflora. Ind Drug 37:95–98

    Google Scholar 

  • The Wealth of India (1972) Raw materials, vol 9. Council of Scientific Industrial Research (CSIR), New Delhi, pp 295–298

    Google Scholar 

  • Tselepis AD, Panagiotakos DB, Pitsavos C, Tellis CC, Chrysohoou C, Stefanadis C (2009) Smoking induces lipoprotein-associated phospholipase A2 in cardiovascular disease free adults: the ATTICA Study. Atherosclerosis 206:303–308

    Article  CAS  PubMed  Google Scholar 

  • Tulenko TN, Rabinowitz JL, Cox RH, Santamore WP (1988) Altered Na+-K+-ATPase, cell Na+ and lipid profiles in canine arterial wall with chronic cigarette smoking. Int J Biochem 20:285–289

  • Tuon T, Valvassori SS, Lopes-Borges J, Fries GR, Silva LA, Kapczinski F, Quevedo J, Pinho RA (2010) Effects of moderate exercise on cigarette smoke exposure-induced hippocampal oxidative stress values and neurological behaviors in mice. Neurosci Lett 475:16–19

    Article  CAS  PubMed  Google Scholar 

  • Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84

    Article  CAS  PubMed  Google Scholar 

  • Vink R, McIntosh TK, Faden AI (1989) Magnesium in central nervous system. In: Adelman G (ed) Neuroscience year. Supplement 1 to the encyclopedia of neuroscience. Birkhauser, Boston, pp 93–94

    Google Scholar 

  • Xiao AY, Wei L, Xia S, Rothman S, Yu SP (2002) Ionic mechanism of ouabain-induced concurrent apoptosis and necrosis in individual cultured cortical neurons. J Neurosci 22:1350–1362

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Conflict of interest

We declare that we have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Biochemistry, College of Medicine, Salman Bin Abdulaziz University, Al-Kharj, 11942, Kingdom of Saudi Arabia

    Thiyagarajan Ramesh

  2. Department of Siddha Medicine, Faculty of Science, Tamil University, Vakaiyur, Thanjavur, 613 010, Tamil Nadu, India

    Chandrabose Sureka & Vavamohaideen Hazeena Begum

  3. Department of Food Safety and Quality Testing, Indian Institute of Crop Processing Technology, Pudukkottai Road, Thanjavur, 613 005, Tamil Nadu, India

    Shanmugham Bhuvana

Authors
  1. Thiyagarajan Ramesh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chandrabose Sureka
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shanmugham Bhuvana
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vavamohaideen Hazeena Begum
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thiyagarajan Ramesh.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ramesh, T., Sureka, C., Bhuvana, S. et al. Brain oxidative damage restored by Sesbania grandiflora in cigarette smoke-exposed rats. Metab Brain Dis 30, 959–968 (2015). https://doi.org/10.1007/s11011-015-9654-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11011-015-9654-4

Keywords

Search

Navigation