Grape seed and skin extract protects against acute chemotherapy toxicity induced by doxorubicin in rat red blood cells and plasma

Authors

  • Sonia Hamlaoui Laboratoire de Neurophysiologie Fonctionnelle et Pathologies, Département des Sciences Biologiques, Faculté des Sciences de Tunis. Campus Universitaire El Manar II-2092
  • Meherzia Mokni Laboratoire de Neurophysiologie Fonctionnelle et Pathologies, Département des Sciences Biologiques, Faculté des Sciences de Tunis. Campus Universitaire El Manar II-2092
  • Nadia Limam Laboratoire de Neurophysiologie Fonctionnelle et Pathologies, Département des Sciences Biologiques, Faculté des Sciences de Tunis. Campus Universitaire El Manar II-2092
  • Alice Carrier INSERM, U624 « Stress cellulaire » Case 915 Parc Scientifique de Luminy, 13288 Marseille Cedex 9
  • Ferid Limam Laboratoire des Substances Bioactives, Centre de Biotechnologie, Technopole Borj-Cedria, BP-901, 2050 Hammam-Lif
  • Mohamed Amri Laboratoire de Neurophysiologie Fonctionnelle et Pathologies, Département des Sciences Biologiques, Faculté des Sciences de Tunis. Campus Universitaire El Manar II-2092
  • Lamjed Marzouki Laboratoire de Neurophysiologie Fonctionnelle et Pathologies, Département des Sciences Biologiques, Faculté des Sciences de Tunis. Campus Universitaire El Manar II-2092
  • Ezzedine Aouani Laboratoire des Substances Bioactives, Centre de Biotechnologie, Technopole Borj-Cedria, BP-901, 2050 Hammam-Lif

DOI:

https://doi.org/10.3329/bjp.v7i1.10356

Keywords:

Doxorubicin, Grape Seed and Skin Extract, Erythrocyte, Plasma, Carbonyl protein, Malondialdehyde, H2O2, free iron, Calcium, Superoxide Dismutase, Catalase, Peroxidase.

Abstract

In this study, the protective role of grape seed and skin extract (GSSE) against doxorubicin-induced blood toxicity has been evaluated in rats. Rats were treated with the extract for 8 days and injected with doxorubicin (20 mg/kg) at the 4th day. At the end of the treatment, blood samples were collected for oxidative stress parameters determination and antioxidant enzymes. Doxorubicin increased erythrocytes and plasma malondialdehyde, free iron, H2O2 and carbonylation, decreased calcium and also decreased erythrocytes catalase, peroxidase and superoxide dismutase (specially the Fe isoform). Doxorubicin also decreased plasma catalase and superoxide dismutase (Cu/Zn and Fe isoforms) but increased peroxidase. Doxorubicin increased plasma alanine aminotransferase and aspartate aminotransferase but decreased them within erythrocytes. GSSE co-treatment counteracted almost all deleterious effects induced by doxorubicin. In conclusion, doxorubicin induced a pro-oxidative stress into rat erythrocytes and plasma and GSSE exerted antioxidant properties which can be attributed to free iron and calcium modulation.

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References

Aebi H. Catalase in vitro. Methods Enzymol. 1984; 105: 121-26.

Barbouti A, Amorgianiotis C, Kolettas E, Kanavaros P, Galaris D. Hydrogen peroxide inhibits caspase-dependent apoptosis by inactivating procaspase-9 in an iron-dependent manner. Free Rad Biol Med. 2007; 43: 1377-87.

Borchi E, Bargelli V, Stillitano F, Giordano C, Sebastiani M, Nassi PA, d'Amati G, Cerbai E, Nediani C. Enhanced ROS production By NADPH oxidase is correlated to changes in antioxidant enzyme activity in human heart failure. Biochim Biophys Acta. 2010; 1802: 331-38.

Bryszewska M, Zavodnik IB, Niekurzak A, Szosland K. Oxidative processes in red blood cells from normal and diabetic individuals. Biochem Mol Biol Int. 1995; 37: 345-54.

Buzdar AU, Marcus C, Smith TL, Blumenschein GR. Early and delayed clinical cardiotoxicity of doxorubicin. Cancer. 1985; 55: 2761-65.

Chance B, Maehly AC. Assay of catalases and peroxidases. Methods Enzymol. 1955; 2: 764-817.

Charradi K, Sebai H, Elkahoui S, Ben Hassine F, Limam F, Aouani E. Grape seed extract alleviates high-fat diet-induced obesity and heart dysfunction by preventing cardiac siderosis. Cardiovasc Toxicol. 2011; 11: 28-37.

Chatelain K, Phippen S, Mc Cabe J, Teeters CA, OMalley S, Kingsley K. Cranberry and Grape Seed Extracts Inhibit the Proliferative Phenotype of Oral Squamous Cell Carcinomas. Evidence-Based Complementary and Alternative Medicine. 2011; ID 467691.

Danz E, Skramsted J, Henry N, Bennett JA, Keller RS. Resveratrol prevents doxorubicin cardiotoxicity through mitochondrial stabilization and the Sirt1 pathway. Free Radic Biol Med. 2009; 46: 1589-97.

Das DK, Maulik N. Resveratrol in cardioprotection: a therapeutic promise of alternative medicine. Mol Interv. 2006; 6: 36-47.

Decordé K, Teissedre PL, Sutra T, Ventura E, Cristol JP, Rouanet JM. Chardonnay grape seed procyanidin extract supplementation prevents high-fat diet-induced obesity in hamsters by improving adipokine imbalance and oxidative stress markers. Mol Nutr Food Res 2009; 53: 659-66.

Dewanto V, Wu X, Adom KK, Liu RH. Thermal processing enhances the nutritional value of tomatoes by increasing total antioxidant activity. J Agric Food Chem. 2002; 50: 3010-14.

Doroshow JH, Locker GY, Myers CE. Enzymatic defenses of the mouse heart against reactive oxygen metabolites: alterations produced by doxorubicin. J Clin Invest. 1980; 65: 128-35.

Draper HH, Hadley M. Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol. 1990; 186: 421-31.

Dulundu E, Ozel Y, Topaloglu U, Toklu H, Ercan F, Gedik N, Sener G. Grape seed extract reduces oxidative stress and fibrosis in experimental biliary obstruction. J Gastroenterol Hepatol. 2007; 22: 885-92.

El-Ashmawy IM, Gad SB, Salama OM. Grape seed extract prevents azathioprine toxicity in rats. Phytother Res. 2010; 24: 1710-15.

Hamlaoui-Gasmi S, Mokni M, Limam N, Limam F, Aouani E, Amri M, Marzouki L. Grape seed extract mitigates garlic-induced oxidative stress in rat spleen and plasma. J Med Plants Res. 2011; 5: 6076-84.

Hamlaoui-Gasmi S, Mokni M, Limam N, Limam F, Aouani E, Amri M, Marzouki L. Grape seed and skin extract mitigates garlic-induced oxidative stress in rat liver. Can J Pharm Pharmacol. 2012; 90: 547-56.

Hebbar V, Shen G, Hu R, Kim BR, Chen C, Korytko PJ, Crowell JA, Levine BS, Kong A-NT. Toxicogenomics of resveratrol in rat liver. Life Sci. 2005; 76: 2299-314.

Ishii K, Tamaoka A, Takeda T, Ishii K, Iwasaki N, Shoji S. Clinical and neurological features of organoarsenic compound (diphenylarsenic acid) intoxication in Kamisu. Japan Rinsho Shinkeigaku. 2006; 46: 768.

Isodaa M, Hanawab H, Watanabeb R, Yoshida T, Toba K, Yoshida K, Kojima M, Otaki K, Hao K, Ding L, Tanaka K, Takayama T, Kato K, Okura Y, Kodama M, Ota Y, Hayashi J, Aizawa Y. Expression of the peptide hormone hepcidin increases in cardiomyocytes under myocarditis and myocardial infarction. J Nutr Biochem. 2010; 21: 749-56.

Jensen RA. Doxorubicin cardiotoxicity: contractile changes after long-term treatment in the rat. J Pharmacol Exper Ther. 1986; 236: 197-203.

Jiménez-Aliaga K, Bermejo-Bescós P, Benedí J, Martín-Aragón S Quercetin and rutin exhibit antiamyloidogenic and fibril-disaggregating effects in vitro and potent antioxidant activity in APPswe cells. Life Sci. 2011; 89: 939-45.

Kakinuma K, Yamaguchi T, Kaneda M, Shimada K, Tomita Y, Chance B. A determination of H2O2 release by the treatment of human blood polymorphonuclear leukocytes with myristate. J Biochem. 1979; 86: 87-95.

Kalivendi SV, Konorev EA, Cunnigham S, Vanamala SK, Kaji EH, Joseph J, Kalyanaraman B. Doxorubicin activates nuclear factor of activated T. lymphocytes and Fas ligand transcription: role of mitochondrial reactive oxygen species and calcium. Biochem J. 2005; 389: 527-39.

Kaur M, Mandair R, Agarwal R, Agarwal C. Grape seed extract induces cell cycle arrest and apoptosis in human colon carcinoma cells. Nutr Cancer. 2008; 60: 2-11.

Kelen M, Tepe B. Screening of antioxidative properties and total phenolic compounds of various extracts of three different seed of grape varieties (Vitis vinifera L.) from Turkish flora. Pak J Biol Sci. 2007; 10: 403-08.

Khanal RC, Howard LR, Prior RL. Procyanidin content of grape seed and pomace, and total anthocyanin content of grape pomace as affected by extrusion processing. J Food Sci. 2009; 74: H174-182.

Kowalczyk MC, Kowalczyk P, Tolstykh O, Hanausek M, Walaszek Z, Slaga TJ. Synergistic effects of combined phytochemicals and skin cancer prevention in SENCAR mice. Cancer Prev Res (Phila). 2010; 3: 170-78.

Leardi A, Caraglia M, Selleri C, Pepe S, Pizzi C, Notaro R, Fabbrocini A, De Lorenzo S, Musicò M, Abbruzzese A, Bianco AR, Tagliaferri P. Desferioxamine increases iron depletion and apoptosis induced by ara-C of human myeloid leukaemic cells. Brit J Haematol. 1998; 102: 746-52.

Lebrecht D, Kirschner J, Geist A, Haberstrah J, Walker UA. Respiratory chain deficiency precedes the disrupted calcium homeostasis in chronic doxorubicin cardio myopathy. Cardiovasc Pathol. 2009; 19: 167-74.

Leonard SS, Xia C, Jiang BH, Stinefelt B, Klandorf H, Harris GK, Shi X. Resveratrol scavenges reactive oxygen species and effects radical-induced cellular responses. Biochem Bioph Res Co. 2003; 309: 1017-26.

Levine LR, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S, Stadtman ER. Determination of carbonyl content in oxidatively modified proteins. Method Enzymol. 1990; 186: 464-78.

Mikstacka R, Rimando AM, Ignatowicz E. Antioxidant effect of transresveratrol, pterostilbene, quercetin and their combinations in human erythrocytes in vitro. Plant Foods Hum Nutr. 2010; 65: 57-63.

Misra HP, Fridovich I. The role of superoxide anion in autoxidation of epinephrine and a simple assay for SOD. J Biol Chem. 1972; 247: 3170-75.

Mokni M, Hamlaoui-Guesmi S, Amri M, Marzouki L, Limam F, Aouani E. Grape seed and skin extract protects against acute chemotherapy toxicity induced by doxorubicin in rat heart. Cardiovasc Toxicol. 2012.

National Research Council. Guide for the care and the use of laboratory animals. National institute of health, Bethesda. 1985; 20: 85-123.

Ngamukote S, Mäkynen K, Thilawech T, Adisakwattana S. Cholesterol-lowering activity of the major polyphenols in grape seed. Molecules 2011; 16: 5054-61.

Ohnishi ST, Barr JK. A simple method of quantitating protein using the biuret and phenol reagent. Anal Biochem. 1978; 86: 193-200.

Park KH, Kim SY, Gul R, Kim BJ, Jang KY, Chung HT, Sohn DH. Fatty acids ameliorate doxorubicin-induced intracellular calcium increase and apoptosis in rat cardiomyocytes. Biol Pharm Bull. 2008; 31: 809-15.

Reitman S, Frankel S. A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. Am J Clin Pathol. 1957; 28: 56-63.

Renaud S, De Lorgeril M. Wine, alcohol, platelets, and the French paradox for coronary heart disease. Lancet. 1992; 339(8808): 1523-26.

Rizvi SI, Maurya PK. Markers of oxidative stress in erythrocytes during aging in humans. Ann NY Acad Sci. 2007; 1100: 373-82.

Rosen GM, Halpern HJ. Spin trapping biologically generated free radicals: correlating formation with cellular injury. Method Enzymol. 1990; 18: 611-21.

Safa J, Argani H, Bastani B, Nezami N, Ardebili BR, Ghorbanihaghjo A. Protective effect of grape seed extract on gentamicin-induced acute kidney injury. Iran J Kid Dis. 2010; 4: 285-91.

Sehirli O, Ozel Y, Dulundu E, Topaloglu U, Ercan F, Sener G. Grape seed extract treatment reduces hepatic ischemia-reperfusion injury in rats. Phytother Res. 2008; 22: 43-48.

Singal PK, Deally CM, Weinberg LE. Subcellular effects of adriamycin in the heart: A concise review. J Mol Cell Cardiol. 1987; 19: 817-28.

Singal PK, Iliskovic N. Doxorubicin-induced cardiomyopathy. New Engl J Med. 1998; 339: 900-05.

Singal PK, Siveski-Iliskovic N, Hill M, Thomas TP, Li T. Combination therapy with probucol prevents Adriamycin-induced cardiomyopathy. J Mol Cell Cardiol. 1995; 27: 1055-63.

Singleton VL, Rossi JA. Colorimetry of total phenolic with phosphomolybdic-phosphotungstic acid reagent. Am J Enol Vitic. 1965; 16: 144-58.

Sinha BK, Katki AG, Batist G, Cowan KH, Myers CE. Adriamycin stimulated hydroxyl radical formation in human breast tumor cells. Biochem Pharmacol 1987a; 36: 793-96.

Sinha BK, Katki AG, Batist G, Cowan KH, Myers CE. Differential formation of hydroxyl radicals by adriamycin in sensitive and resistant MCF-7 human breast tumor cells: Implications for the mechanism of action. Biochem. 1987b; 26: 3776-81.

Stern J, Lewis WH. The colorimetric estimation of calcium in serum with ocresolphthalein complexone. Clin Chim Acta. 1957; 2: 576-80.

Sun BS, Ricardo-Da-Silva JM, Spranger MI. Critical factors of vanillin assay for catechins and proanthocyanidins. J Agric Food Chem. 1998; 46: 4267-74.

Suwannaphet W, Meeprom A, Yibchok-Anun S, Adisakwattana S. Preventive effect of GSE against high fructose diet-induced insulin resistance and oxidative stress in rats. Food Chem Toxicol. 2010; 48: 1853-57.

Wang YJ, Thomas P, Zhong JH, Bi FF, Kosaraju S, Pollard A, Fenech M, Zhou XF. Consumption of grape seed extract prevents amyloïd-â deposition and attenuates inflammation in brain of an Alzheimers disease mouse. Neurotox Res. 2009; 15: 3-14.

Yoshioka T, Homma T, Meyrick B, Takeda M, Moore-Jarett T, Kon V, Ichikawa I. Oxidants induce transcriptional activation of manganese superoxide dismutase in glomerular cells. Kidney Int. 1994; 46: 405-13.

Published

2012-05-17

How to Cite

Hamlaoui, S., M. Mokni, N. Limam, A. Carrier, F. Limam, M. Amri, L. Marzouki, and E. Aouani. “Grape Seed and Skin Extract Protects Against Acute Chemotherapy Toxicity Induced by Doxorubicin in Rat Red Blood Cells and Plasma”. Bangladesh Journal of Pharmacology, vol. 7, no. 1, May 2012, pp. 54-62, doi:10.3329/bjp.v7i1.10356.

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Section

Research Articles