Abstract
Oxidative stress has long been implicated in the neurotoxic effects of glutamate acting through N-methyl-D-aspartate (NMDA) receptors. Therefore, present study has been designed to explore the effect of rofecoxib and caffeic acid on the involvement of oxidative stress, mitochondrial dysfunction and neuronal linked with NMDA receptor-mediated excitotoxicity. Caffeic acid, is a well-known antioxidant flavanoid, implicate anti-inflammatory and immunomodulatory like actions. The present study is an attempt to investigate the antioxidant-like effect of caffeic acid and rofecoxib and their combination against QA-induced oxidative damage, mitochondrial dysfunction and histological alterations. Intrastriatal injection of quinolinic acid (300 nmol) significantly increased oxidative stress (raised lipid peroxidation, nitrite concentration, depleted SOD and catalase), altered mitochondrial complex enzyme activities and histological alteration in the ex vivo striatum. Caffeic acid (5 and 10 mg/kg, p.o.) and rofecoxib (10 and 20 mg/kg, p.o.) treatment for 21 days significantly attenuated oxidative damage and impairment in mitochondrial activities of complex enzymes in the ex vivo striatum. Further, combination of sub effective doses of rofecoxib (10 mg/kg, p.o.) and caffeic acid (5 mg/kg, p.o.) potentiated their protective effect which was significant as compared to their effect per se. The present study suggests the therapeutic effect of caffeic acid and rofecoxib combination against QA-induced ex vivo oxidative damage, mitochondrial and histological alterations in rats.
Similar content being viewed by others
References
Amodio R, De Ruvo C, Sacchetti A, Di Santo A, Martelli N, Di Matteo V, Lorenzet R, Poggi A, Rotilio D, Cacchio M, Esposito E (2003) Caffeic acid phenethyl ester blocks apoptosis induced by low potassium in cerebellar granule cells. Int J Dev Neurosci 21(7):379–389
Andreyev AY, Fahy B, Fiskum G (1998) Cytochrome c release from brain mitochondria is independent of the mitochondrial permeability transition. FEBS Lett 439(3):373–376
Araujo DM, Cherry SR, Tatsukawa KJ, Toyokuni T, Kornblum HI (2000) Deficits in striatal dopamine D(2) receptors and energy metabolism detected by in vivo micro PET imaging in a rat model of Huntington’s disease. Exp Neurol 166(2):287–297
Arenas J, Campos Y, Ribacoba R, Martín MA, Rubio JC, Ablanedo P, Cabello A (1998) Complex I defect in muscle from patients with Huntington’s disease. Ann Neurol 43(3):397–400
Beal MF, Ferrante RJ, Swartz KJ, Kowall NW (1991) Chronic quinolinic acid lesions in rats closely resemble Huntington’s disease. J Neurosci 11(6):1649–1659
Behan WM, McDonald M, Darlington LG, Stone TW (1999) Oxidative stress as a mechanism for quinolinic acid-induced hippocampal damage: protection by melatonin and deprenyl. Br J Pharmacol 128(8):1754–1760
Berman SB, Hastings TG (1999) Dopamine oxidation alters mitochondrial respiration and induces permeability transition in brain mitochondria: implications for Parkinson’s disease. J Neurochem 73:1127–1137
Budd SL, Nicholls DG (1996) Mitochondria, calcium regulation, and acute glutamate excitotoxicity in cultured cerebellar granule cells. J Neurochem 67(6):2282–2291
Cabrera J, Reiter RJ, Tan DX, Qi W, Sainz RM, Mayo JC, Garcia JJ, Kim SJ, El-Sokkary G (2000) Melatonin reduces oxidative neurotoxicity due to quinolinic acid: in vitro and in vivo findings. Neuropharmacology 39(3):507–514
Choi DW (1994) Calcium and excitotoxic neuronal injury. Ann NY Acad Sci 747:162–171
Chung MJ, Walker PA, Hogstrand C (2006) Dietary phenolic antioxidants, caffeic acid and Trolox, protect rainbow trout gill cells from nitric oxide-induced apoptosis. Aquat Toxicol 80(4):321–328
Devipriya N, Sudheer AR, Menon VP (2008) Caffeic acid protects human peripheral blood lymphocytes against gamma radiation-induced cellular damage. J Biochem Mol Toxicol 22(3):175–186
Dykens JA (1994) Isolated cerebral and cerebellar mitochondria produce free radicals when exposed to elevated CA2+ and Na+: implications for neurodegeneration. J Neurochem 63(2):584–591
Ganzella M, Jardim FM, Boeck CR, Vendite D (2006) Time course of oxidative events in the hippocampus following intracerebroventricular infusion of quinolinic acid in mice. Neurosci Res 55(4):397–402
Gornall AG, Bardawill CJ, David MM (1949) Determination of serum proteins by means of the biuret reaction. J Biol Chem 177(2):751–766
Green LC, Wagner DA, Glgowski J, Skipper PL, Wishnok JS, Tannebaum SR (1982) Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Ann Biochem 126:131
Guidetti P, Schwarcz R (2003) 3-Hydroxykynurenine and quinolinate: pathogenic synergism in early grade Huntington’s disease? Adv Exp Med Biol 527:137
Halliwell B (2001) Role of free radicals in the neurodegenerative diseases: therapeutic implications for antioxidant treatment. Drugs Aging 18(9):685–716
Hurley SD, Olschowka JA, O’Banion MK (2002) Cyclooxygenase inhibition as a strategy to ameliorate brain injury. J Neurotrauma 19(1):1–15
Kang NJ, Lee KW, Shin BJ, Jung SK, Hwang MK, Bode AM, Heo YS, Lee HJ, Dong Z (2009) Caffeic acid, a phenolic phytochemical in coffee, directly inhibits Fyn kinase activity and UVB-induced COX-2 expression. Carcinogenesis 30(2):321–330
Kart A, Cigremis Y, Ozen H, Dogan O (2009) Caffeic acid phenethyl ester prevents ovary ischemia/reperfusion injury in rabbits. Food Chem Toxicol 47(8):1980–1984
Kiechle T, Dedeoglu A, Kubilus J, Kowall NW, Beal MF, Friedlander RM, Hersch SM, Ferrante RJ (2002) Cytochrome C and caspase-9 expression in Huntington’s disease. Neuromolecular Med 1(3):183–195
King TE (1967) Preparation of succinate dehydrogenase and reconstitution of succinate oxidase. Methods Enzymol 10:322
King TE, Howard RL (1967) Preparations and properties of soluble NADH dehydrogenases from cardiac muscle. Methods Enzymol 10:275
Kono Y (1978) Generation of superoxide radical during auto-oxidation of hydroxylamine and an assay of superoxide dismutase. Arch Biochem biophysics 186:189
Kumar A, Seghal N, Padi SV, Naidu PS (2006) Differential effects of cyclooxygenase inhibitors on intracerebroventricular colchicine induced dysfunction and oxidative stress in rats. Eur J Pharmacol 551(1–3):58–66
Kumar P, Padi SS, Naidu PS, Kumar A (2007) Cyclooxygenase inhibition attenuates 3-nitropropionic acid-induced neurotoxicity in rats: possible antioxidant mechanisms. Fundam Clin Pharmacol 21(3):297–306
Leipnitz G, Schumacher C, Scussiato K, Dalcin KB, Wannmacher CM, Wyse AT, Dutra-Filho CS, Wajner M, Latini A (2005) Quinolinic acid reduces the antioxidant defenses in cerebral cortex of young rats. Int J Dev Neurosci 23(8):695–701
Liu H, Bowes RC, Van de Water B, Sillence C, Nagelkerke JF, Stevens JL (1997) Endoplasmic reticulum chaperones GRP78 and calreticulin prevent oxidative stress, Ca2+ disturbances, and cell death in renal epithelial cells. J Biol Chem 272(35):21751–21759
Lodovici M, Guglielmi F, Meoni M, Dolara P (2001) Effect of natural phenolic acids on DNA oxidation in vitro. Food Chem Toxicol 39(12):1205–1210
Luck H (1971) Catalase. In: Bergmeyer HU (ed) Methods of enzyme analysis. Academic Press, New York, p 885
Maharaj H, Maharaj DS, Daya S (2006) Acetylsalicylic acid and acetaminophen protect against oxidative neurotoxicity. Metab Brain Dis 21:189–199
McEleny K, Coffey R, Morrissey C, Fitzpatrick JM, Watson RW (2004) Caffeic acid phenethyl ester-induced PC-3 cell apoptosis is caspase-dependent and mediated through the loss of inhibitors of apoptosis proteins. BJU Int 94(3):402–406
Mosmann T (1983) Rapid colorimetric assay for cellular growth survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55
Nakai M, Qin ZH, Wang Y, Chase TN (1999) Free radical scavenger OPC-14117 attenuates quinolinic acid-induced NF-κB activation and apoptosis in rat striatum. Brain Res Mol Brain Res 64(1):59–68
Noelker C, Bacher M, Gocke P, Wei X, Klockgether T, Du Y, Dodel R (2005) The flavanoide caffeic acid phenethyl ester blocks 6-hydroxydopamine-induced neurotoxicity. Neurosci Lett 383(1–2):39–43
Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates, 6th edn. Academic Press, San Diego
Peng TI, Greenamyre JT (1998) Privileged access to mitochondria of calcium influx through N-methyl-D-aspartate receptors. Mol Pharmacol 53(6):974–980
Prasad NR, Jeyanthimala K, Ramachandran S (2009) Caffeic acid modulates ultraviolet radiation-B induced oxidative damage in human blood lymphocytes. J Photochem Photobiol B 95(3):196–203
Radi R, Cassina A, Hodara R, Quijano C, Castro L (2002) Peroxynitrite reactions and formation in mitochondria. Free Radic Biol Med 33(11):1451–1464
Rodríguez-Martínez E, Camacho A, Maldonado PD, Pedraza-Chaverrí J, Santamaría D, Galván-Arzate S, Santamaría A (2000) Effect of quinolinic acid on endogenous antioxidants in rat corpus striatum. Brain Res 858(2):436–439
Rossato JI, Zeni G, Mello CF, Rubin MA, Rocha JB (2002) Ebselen blocks the quinolinic acid-induced production of thiobarbituric acid reactive species but does not prevent the behavioral alterations produced by intra-striatal quinolinic acid administration in the rat. Neurosci Lett 318(3):137–140
Rothman SM (1985) The neurotoxicity of excitatory amino acids is produced by passive chloride influx. J Neurosci 5:1483–1489
Rustin P, Rötig A (2002) Inborn errors of complex-II unusual human mitochondrial diseases. Biochim Biophys Acta 1553(1–2):117–122
Santamaría A, Ríos C (1993) MK-801, an N-methyl-D-aspartate receptor antagonist, blocks quinolinic acid-induced lipid peroxidation in rat corpus striatum. Neurosci Lett 159:51–54
Schanne FA, Kane AB, Young EE, Farber JL (1979) Calcium dependence of toxic cell death: a final common pathway. Science 206:700–702
Schuck PF, Tonin A, da Costa Ferreira G, Rosa RB, Latini A, Balestro F, Perry ML, Wannmacher CM, de Souza Wyse AT, Wajner M (2007) In vitro effect of quinolinic acid on energy metabolism in brain of young rats. Neurosci Res 57(2):277–288
Schwarcz R, Foster AC, French ED, Whetsell WO Jr, Kohler C (1984) Excitotoxic models for neurodegenerative disorders. Life Sci 35:19–32
Sottocasa GL, Kuylenstierna B, Ernster L, Bergstrand A (1967) An electron-transport system associated with the outer membrane of liver mitochondria, a biochemical and morphological study. J Cell Biol 32:415
Sousa SC, Maciel EN, Vercesi AE, Castilho RF (2003) Ca2+-induced oxidative stress in brain mitochondria treated with the respiratory chain inhibitor rotenone. FEBS Lett 543(1–3):179–183
Stone TW (1993) Neuropharmacology of quinolinic and kynurenic acids. Pharmacol Rev 45(3):309–379
Sul D, Kim HS, Lee D, Joo SS, Hwang KW, Park SY (2009) Protective effect of caffeic acid against beta-amyloid-induced neurotoxicity by the inhibition of calcium influx and tau phosphorylation. Life Sci 84(9–10):257–262
Tymianski M, Wallace MC, Spigelman I, Uno M, Carlen PL, Tator CH, Charlton MP (1993) Cell-permeant Ca2+ chelators reduce early excitotoxic and ischemic neuronal injury in vitro and in vivo. Neuron 11(2):221–235
Wei X, Ma Z, Fontanilla CV, Zhao L, Xu ZC, Taggliabraci V, Johnstone BH, Dodel RC, Farlow MR, Du Y (2008) Caffeic acid phenethyl ester prevents cerebellar granule neurons (CGNs) against glutamate-induced neurotoxicity. Neuroscience 155(4):1098–1105
Wills ED (1966) Mechanism of lipid peroxide formation in animal tissue. Biochem J 99:667
Yildiz OG, Soyuer S, Saraymen R, Eroglu C (2008) Protective effects of caffeic acid phenethyl ester on radiation induced lung injury in rats. Clin Invest Med 31(5):E242–E247
Yilmaz HR, Uz E, Gökalp O, Ozçelik N, Ciçek E, Ozer MK (2008) Protective role of caffeic acid phenethyl ester and erdosteine on activities of purine catabolizing enzymes and level of nitric oxide in red blood cells of isoniazid administered rats. Toxicol Ind Health 24(8):519–524
Zheng ZS, Xue GZ, Grunberger D, Prystowsky JH (1995) Caffeic acid phenethyl ester inhibits proliferation of human keratinocytes and interferes with the EGF regulation of ornithine decarboxylase. Oncol Res 7(9):445–452
Acknowledgment
The major research project grant sanctioned to Dr. Anil Kumar by University Grant Commission is greatly acknowledged.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kalonia, H., Kumar, P., Kumar, A. et al. Effect of caffeic acid and rofecoxib and their combination against intrastriatal quinolinic acid induced oxidative damage, mitochondrial and histological alterations in rats. Inflammopharmacol 17, 211–219 (2009). https://doi.org/10.1007/s10787-009-0012-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10787-009-0012-1