Cyclophosphamide-Induced Lipid Peroxidation and Changes in Cholesterol Content: Protective Role of Reduced Glutathione Cyclophosphamide induced lipid peroxidation
Iranian Journal of Pharmaceutical Sciences,
Vol. 7 No. 4 (2011),
1 October 2011
,
Page 255-267
https://doi.org/10.22037/ijps.v7.41308
Abstract
The study was designed with an aim to evaluate the protective effects of reduced glutathione on cyclophosphamide induced lipid peroxidation and also changes in cholesterol content. Goat liver and white New Zealand rabbit were used as lipid source for the models. Lipid peroxidation study was performed by measuring the malondialdehyde, 4-hydroxy-2-nonenal, reduced glutathione and nitric oxide content of tissue homogenates or rabbit blood.In the cholesterol profile total cholesterol and high density lipoprotein cholesterol content of rabbit
blood was determined. The data presented in this work demonstrate the lipid peroxidation induction potential of cyclophosphamide and the antiperoxidative potential of reduced glutathione on cyclophosphamide-induced lipid peroxidation. It was also observed that reduced glutathione has protective effect on cyclophosphamide-induced changes in cholesterol
content. A significant correlation was also found between malondialdehyde, 4hydroxy-2-nonenal with total cholesterol as well as between reduced glutathione and nitric oxide with HDL cholesterol. These findings from both in vitro as well as in vivo models indicate the lipid peroxidation induction potential of cyclophosphamide which may be related to its toxic potential. The results also suggest the antiperoxidative effects of reduced glutathione and demonstrate its potential to reduce cyclophosphamide-induced lipid peroxidation and thus to increase therapeutic index of the drug by way of reducing toxicity that may be mediated through free radical mechanisms.
Keywords:
- Cholesterol
- Cyclophosphamide
- 4-Hydroxy-2-nonenal
- Malondialdehyde
- Nitric oxide
- Reduced glutathione
How to Cite
Supratim Ray, Subrata Chakraborty, Bibhas Pandit, & Sumit Das. (2011). Cyclophosphamide-Induced Lipid Peroxidation and Changes in Cholesterol Content: Protective Role of Reduced Glutathione: Cyclophosphamide induced lipid peroxidation. Iranian Journal of Pharmaceutical Sciences, 7(4), 255–267. https://doi.org/10.22037/ijps.v7.41308
References
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1997; 1360: 45-52.
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[15] Bhatia K, Ahmad F, Rashid H, Raisuddin S. Protective effect of S-allylcysteine against cyclophosphamide-induced bladder hemorrhagic cystitis in mice. Food Chem Toxicol 2008; 46: 3368-74.
[16] Tripathi DN, Jena GB. Astaxanthin inhibits cytotoxic and genotoxic effects of cyclophosphamide in mice germ cells. Toxicology 2008; 248: 96-103.
[17] Eliot RS. Stress and the heart. New York: Futura Publishing Company, 1974; pp. 41-63.
[18] Lata H, Ahuja GK, Narang APS. Effect of starvation stress on lipid peroxidation and lipid profile in rabbits. Indian J Physiol Pharmacol 2002; 46: 371-4.
[19] Ray S, Roy K, Sengupta C. Cisplatin-induced lipid peroxidation and its inhibition with ascorbic acid. Indian J Pharm Sci 2006; 68: 199-204.
[20] Ray S, Roy K, Sengupta C. Evaluation of protective effects of water extract of Spirulina platensis (blue green algae) on cisplatin-induced lipid peroxidation. Indian J Pharm Sci 2007; 69:378-83.
[21] Ray S, Sengupta C, Roy K. in vitro evaluation of protective effects of ascorbic acid and water extract of Spirulina platensis (blue green algae) on 5-fluorouracil-induced lipid peroxidation. Acta Pol Pharm-Drug Res 2007; 64: 335-44.
[22] Ray S, Roy K, Sengupta C. Exploring the protective effect of ascorbic acid and water extract of Spirulina platensis (blue green algae) on methotrexate-induced lipid peroxidation. Iranian J Pharm Sci 2007; 3: 217-28.
[23] Hilditch TP, Williams PN. The chemical constituents of fats. London: Chapman & Hall, 1964; pp. 100-33.
[24] Ohkawa H, Ohishi N, Yagi K. Assay of lipid peroxidation in animal tissue by thiobarbituric acid reaction. Anal Biochem 1979; 95: 351-8.
[25] Ellman GL. Tissue sulfhydryl groups. Arch Biochem Biophys 1959; 82: 70-7.
[26] Kinter M. Quantitative analysis of 4-hydroxy-2nonenal. In: Punchard NA, Kelly GJ, (editors). Free radicals- a practical approach. Oxford: Oxford University Press, 1996; pp. 130-6.
[27] Sastry KVH, Moudgal RP, Mohan J, Tyagi JS, Rao GS. Spectrophotometric determination of serum nitrite and nitrate by copper-cadmium alloy. Anal Biochem 2002; 306: 79-82.
[28] Wybenga DR, Pileqqi VJ, Dirstine PH, Di Giorquio J. Direct manual determination of serum total cholesterol with a single stable reagent. Clin Chem 1970; 16: 980-4.
[29] Snedecor GW, Cochran WG. Statistical methods. New Delhi: Oxford & IBH Publishing Co Pvt Ltd, 1967; pp. 375-85.
[30] Bolton S. Statistics. In: Gennaro AR, (editor). Remington: The science and practice of pharmacy. Philadelphia: Lippincott Williams & Wilkins, 2001; pp. 124-58.
[31] Naito Y, Yoshikawa T, Yoshida N, Kondo M. Role of oxygen radical and lipid peroxidation in indomethacin-induced gastric mucosal injury. Dig Dis Sci 1998; 43: 30-4S.
[32] Yahya MD, Pinnsa JL, Meinke GC, Lung CC. Antibodies against malondialdehyde (MDA) in MLR/lpr/lpr mice: evidence for an autoimmune mechanism involving lipid peroxidation. J Autoimmunity 1996; 9: 3-9.
[33] Winrow VR, Winyard PG, Morris CJ, Black DR. Free radicals in inflammation: second messengers and mediators of tissue destruction. Br Med Bull 1993; 49: 506-22.
[34] Esterbauer H, Benedetti A, Lang J, Fulceri R, Fauler G, Comporti M. Studies on the mechanism of formation of 4-hydroxynonenal during microsomal lipid peroxidation. Biochim Biophys Acta 1986; 876: 154-66.
[35] Esterbauer H, Schaur RJ, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 1991; 11: 81-128.
[36] Uchida K, Szweda LI, Chae HZ, Stadtman ER. Immunochemical detection of 4-hydroxynonenal protein adducts in oxidized hepatocytes. Proc Natl Acad Sci USA 1993; 90: 8742-6.
[37] Ethen CM, Reilly C, Fenq X, Olsen TW, Ferrington DA. Age-related macular degeneration and retinal protein modification by 4-hydroxy-2nonenal. Invest Ophthamol Vis Sci 2007; 48: 3469-79.
[38] Sen CK. Nutritional biochemistry of cellular glutathione. J Nutr Biochem 1997; 8: 660-72.
[39] Kosower EM, Kosower NS. Glutathione metabolism and function. New York: Raven Press, 1976; pp. 133-9.
[40] Nathan C. Nitric oxide as a secretory product of mammalian cells. Faseb J 1992; 6: 3051-64.
[41] Waldman SA, Murad F. Biochemical mechanisms underlying vascular smooth muscle relaxation: the guanylate cyclase-cyclic GMP system. J Cardiovasc Pharmacol 1988; 12: S115-8.
[42] Ignarro LJ, Byrans RE, Buga GM, Wood KS. Endothelium-derived relaxing factor from pulmonary artery and vein possesses pharmacologic and chemical properties identical to those of nitric oxide radical. Circ Res 1987; 61: 866-79.
[43] Cohen GA, Hobbs AJ, Flich RM, Zinner MJ, Chaudhuri G, Ignarro LJ. Nitric oxide regulates endothelium-dependent vasodilator responses in rabbit hindquarters vascular bed in vivo. Am J Physiol Heart Circ Physiol 1996; 271: H133-9.
[44] Moncada S, Higgs A. The L-arginine-nitric oxide pathway. N Engl J Med 1993; 329: 2002-12.
[45] Beckman JS, Beckman TW, Chen J, Marshal PA, Freeman BA. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 1990; 87: 1620-4.
[46] Hogg N, kalyanaraman B, Joseph J, Struck A, Parthasarathy S. Inhibition of low density lipoprotein oxidation by nitric oxide: potential role in atherogenesis. FEBS Lett 1993; 334: 170-4.
[47] Rubho H, Parthasarathy S, Barnes S, Kirk M, kalyanaraman B, Freeman BA. Nitric oxide inhibition of lipoxygenase dependent liposomes and low-density lipoprotein oxidation: Termination of radical chain propagation reactions and formation of nitrogen containing oxidized lipid derivatives. Arch Biochem Biophys 1995; 324: 15-25.
[48] Yamanaka N, Oda O, Nagao S. Nitric oxide released from zwitterionic polyamine/NO adducts inhibit Cu2+ -induced low-density lipoprotein oxidation. FEBS Lett 1996; 398: 53-60.
[49] Odonnel VB, Chumley PH, Hogg N, Bloodsworth A, Freeman BA. Nitric oxide inhibition of lipid peroxidation: kinetics of reaction with lipid peroxyl radicals and comparison with alphatocopherol.
Biochemistry 1997; 36: 15216-23.
[50] Kelly EE, Wagner BA, Buettner GR, Patrick Burns C. Nitric oxide inhibits iron-induced lipid peroxidation in HL-60 cells. Arch Biochem Biophys 1999; 370: 97-104.
[51] Yalcin AS, Sabuncu N, Kilinc A. Increased plasma and erythrocyte lipid peroxidation in hyperlipidemic individuals. Atherosclerosis 1989; 80: 169-70.
[52] Mehmetcik G, Toker G, Uysal M. Endogenous and copper-induced lipid peroxidation and antioxidant activity of serum in hypercholesterolemic subjects. Horm Metab Res 1997; 29: 63-5.
[53] Anderson JW, Gowri MS, Turner J. Antioxidant supplementation effects on low-density lipoprotein oxidation for individuals with type 2 diabetes mellitus. J Am Coll Nutr 1999; 18: 451-61.
[54] Kurowska EM, Spence JD, Jordan J, Wetmore S, Freeman DJ, Piche LA, Serratore P. HDLcholesterol-raising effect of orange juice in subjects with hypercholesterolemia. Am J Clin Nutr 2000; 72: 1095-1100.
[55] Owu DU, Antai AB, Udofia KH, Obembe AO, Obasi KO, Eteng MU. Vitamin C improves basal metabolic rate and lipid profile in alloxan-induced diabetes mellitus in rats. J Biosci 2006; 31: 5759.
[56]Das S, Snehlata, Srivastava LM. Effect of ascorbic acid on lipid profile and lipid peroxidation in hypercholesterolemic rabbits. Nutr Res 1997; 17:231-41.
[57] Prasad K, Karla J. Oxygen free radicals and hypercholesterolemic atherosclerosis: effect of vitamin E. Am Heart J 1993; 125: 958-73.
[2] Cerruti PA. In: Colburn NH, Moses HL, Stanbridge EJ, (editors.). Growth Factors, Tumor Promoters and Cancer Genes. New York: Alan R Liss Inc, 1998; pp: 239-47.
[3] Goidstein BD, Witz G, Amomso M, Troll W. Protease inhibitors antagonize the activation of polymorphonuclear leukocyte oxygen consumption. Biochem Biophys Res Commun 1979; 88: 854-60.
[4] Parola M., Belloma G, Robino G, Barrera G, Dianzani, MU. 4-Hydroxynonenal as a biological signal: molecular basis and pathophysiological implications. Antioxid Redox Signal 1999; 1:255-84.
[5] Halliwell B, Gutteridge JMC. Free radicals in biology and medicine. Oxford: Oxford University Press, 1989; pp. 195-205.
[6] Wagner BA, Buerrner GR, Burns CP. Increased generation of lipid-derived and ascorbate free radicals by L1210 cells exposed to the ether lipid edelfosine. Cancer Res 1993; 53: 711-3.
[7] Kampkotter A, Nkwonkam CG, Zurawski RF, Timpel C, Chovolou Y, Watjen W, Kahl R. Investigations of protective effects of the flavonoids quercetin and rutin on stress resistance in the model organism Caenorhabditis elegans. Toxicology 2007; 234: 113-23.
[8] Ratty AK, Sunamoto J, Das NP. Interaction of flavonoids with 1, 1-diphenyl-2-picrylhydrazyl free radical, liposomal membranes and soybean lipoxygenase-1. Biochem Pharmacol 1988; 37: 989-95.
[9] Halliwell B. Drug antioxidant effects-A basis for drug selection. Drugs 1991; 42: 569-605.
[10] Luo X, Evrovsky Y, Cole D, Trines J, Benson LN, Lehotay DC. Doxorubicin- induced acute changes in cytotoxic aldehydes, antioxidant status and cardiac function in the rat. Biochim Biophys Acta
1997; 1360: 45-52.
[11] Stankiewicz A, Skrzydlewska E, Makiela M. Effects of amifostine on liver oxidative stress caused by cyclophosphamide administration to rats. Drug Metabol Drug Interact 2002; 19: 67-82.
[12] Premkumar K, Pachiappan A, Abraham SK, Santhiya ST, Gopinath PM, Ramesh A. Effect of Spirulina fusiformis on cyclophosphamide and mitomycin-C induced genotoxicity and oxidative stress in mice. Fitoterapia 2001; 72: 906-11.
[13] Venkatesan N, Chandrakasan G. in vivo administration of taurine and niacin modulate cyclophosphamide-induced lung injury. Eur J Pharmacol 1994; 292: 75-80.
[14] Sudharsan PT, Mythili Y, Selvakumar E, Varalakshmi P. Cardioprotective effect of pentacyclic triterpene, lupeol and its ester on cyclophosphamide- induced oxidative stress. Hum Exp Toxicol 2005; 24: 313-8.
[15] Bhatia K, Ahmad F, Rashid H, Raisuddin S. Protective effect of S-allylcysteine against cyclophosphamide-induced bladder hemorrhagic cystitis in mice. Food Chem Toxicol 2008; 46: 3368-74.
[16] Tripathi DN, Jena GB. Astaxanthin inhibits cytotoxic and genotoxic effects of cyclophosphamide in mice germ cells. Toxicology 2008; 248: 96-103.
[17] Eliot RS. Stress and the heart. New York: Futura Publishing Company, 1974; pp. 41-63.
[18] Lata H, Ahuja GK, Narang APS. Effect of starvation stress on lipid peroxidation and lipid profile in rabbits. Indian J Physiol Pharmacol 2002; 46: 371-4.
[19] Ray S, Roy K, Sengupta C. Cisplatin-induced lipid peroxidation and its inhibition with ascorbic acid. Indian J Pharm Sci 2006; 68: 199-204.
[20] Ray S, Roy K, Sengupta C. Evaluation of protective effects of water extract of Spirulina platensis (blue green algae) on cisplatin-induced lipid peroxidation. Indian J Pharm Sci 2007; 69:378-83.
[21] Ray S, Sengupta C, Roy K. in vitro evaluation of protective effects of ascorbic acid and water extract of Spirulina platensis (blue green algae) on 5-fluorouracil-induced lipid peroxidation. Acta Pol Pharm-Drug Res 2007; 64: 335-44.
[22] Ray S, Roy K, Sengupta C. Exploring the protective effect of ascorbic acid and water extract of Spirulina platensis (blue green algae) on methotrexate-induced lipid peroxidation. Iranian J Pharm Sci 2007; 3: 217-28.
[23] Hilditch TP, Williams PN. The chemical constituents of fats. London: Chapman & Hall, 1964; pp. 100-33.
[24] Ohkawa H, Ohishi N, Yagi K. Assay of lipid peroxidation in animal tissue by thiobarbituric acid reaction. Anal Biochem 1979; 95: 351-8.
[25] Ellman GL. Tissue sulfhydryl groups. Arch Biochem Biophys 1959; 82: 70-7.
[26] Kinter M. Quantitative analysis of 4-hydroxy-2nonenal. In: Punchard NA, Kelly GJ, (editors). Free radicals- a practical approach. Oxford: Oxford University Press, 1996; pp. 130-6.
[27] Sastry KVH, Moudgal RP, Mohan J, Tyagi JS, Rao GS. Spectrophotometric determination of serum nitrite and nitrate by copper-cadmium alloy. Anal Biochem 2002; 306: 79-82.
[28] Wybenga DR, Pileqqi VJ, Dirstine PH, Di Giorquio J. Direct manual determination of serum total cholesterol with a single stable reagent. Clin Chem 1970; 16: 980-4.
[29] Snedecor GW, Cochran WG. Statistical methods. New Delhi: Oxford & IBH Publishing Co Pvt Ltd, 1967; pp. 375-85.
[30] Bolton S. Statistics. In: Gennaro AR, (editor). Remington: The science and practice of pharmacy. Philadelphia: Lippincott Williams & Wilkins, 2001; pp. 124-58.
[31] Naito Y, Yoshikawa T, Yoshida N, Kondo M. Role of oxygen radical and lipid peroxidation in indomethacin-induced gastric mucosal injury. Dig Dis Sci 1998; 43: 30-4S.
[32] Yahya MD, Pinnsa JL, Meinke GC, Lung CC. Antibodies against malondialdehyde (MDA) in MLR/lpr/lpr mice: evidence for an autoimmune mechanism involving lipid peroxidation. J Autoimmunity 1996; 9: 3-9.
[33] Winrow VR, Winyard PG, Morris CJ, Black DR. Free radicals in inflammation: second messengers and mediators of tissue destruction. Br Med Bull 1993; 49: 506-22.
[34] Esterbauer H, Benedetti A, Lang J, Fulceri R, Fauler G, Comporti M. Studies on the mechanism of formation of 4-hydroxynonenal during microsomal lipid peroxidation. Biochim Biophys Acta 1986; 876: 154-66.
[35] Esterbauer H, Schaur RJ, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 1991; 11: 81-128.
[36] Uchida K, Szweda LI, Chae HZ, Stadtman ER. Immunochemical detection of 4-hydroxynonenal protein adducts in oxidized hepatocytes. Proc Natl Acad Sci USA 1993; 90: 8742-6.
[37] Ethen CM, Reilly C, Fenq X, Olsen TW, Ferrington DA. Age-related macular degeneration and retinal protein modification by 4-hydroxy-2nonenal. Invest Ophthamol Vis Sci 2007; 48: 3469-79.
[38] Sen CK. Nutritional biochemistry of cellular glutathione. J Nutr Biochem 1997; 8: 660-72.
[39] Kosower EM, Kosower NS. Glutathione metabolism and function. New York: Raven Press, 1976; pp. 133-9.
[40] Nathan C. Nitric oxide as a secretory product of mammalian cells. Faseb J 1992; 6: 3051-64.
[41] Waldman SA, Murad F. Biochemical mechanisms underlying vascular smooth muscle relaxation: the guanylate cyclase-cyclic GMP system. J Cardiovasc Pharmacol 1988; 12: S115-8.
[42] Ignarro LJ, Byrans RE, Buga GM, Wood KS. Endothelium-derived relaxing factor from pulmonary artery and vein possesses pharmacologic and chemical properties identical to those of nitric oxide radical. Circ Res 1987; 61: 866-79.
[43] Cohen GA, Hobbs AJ, Flich RM, Zinner MJ, Chaudhuri G, Ignarro LJ. Nitric oxide regulates endothelium-dependent vasodilator responses in rabbit hindquarters vascular bed in vivo. Am J Physiol Heart Circ Physiol 1996; 271: H133-9.
[44] Moncada S, Higgs A. The L-arginine-nitric oxide pathway. N Engl J Med 1993; 329: 2002-12.
[45] Beckman JS, Beckman TW, Chen J, Marshal PA, Freeman BA. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 1990; 87: 1620-4.
[46] Hogg N, kalyanaraman B, Joseph J, Struck A, Parthasarathy S. Inhibition of low density lipoprotein oxidation by nitric oxide: potential role in atherogenesis. FEBS Lett 1993; 334: 170-4.
[47] Rubho H, Parthasarathy S, Barnes S, Kirk M, kalyanaraman B, Freeman BA. Nitric oxide inhibition of lipoxygenase dependent liposomes and low-density lipoprotein oxidation: Termination of radical chain propagation reactions and formation of nitrogen containing oxidized lipid derivatives. Arch Biochem Biophys 1995; 324: 15-25.
[48] Yamanaka N, Oda O, Nagao S. Nitric oxide released from zwitterionic polyamine/NO adducts inhibit Cu2+ -induced low-density lipoprotein oxidation. FEBS Lett 1996; 398: 53-60.
[49] Odonnel VB, Chumley PH, Hogg N, Bloodsworth A, Freeman BA. Nitric oxide inhibition of lipid peroxidation: kinetics of reaction with lipid peroxyl radicals and comparison with alphatocopherol.
Biochemistry 1997; 36: 15216-23.
[50] Kelly EE, Wagner BA, Buettner GR, Patrick Burns C. Nitric oxide inhibits iron-induced lipid peroxidation in HL-60 cells. Arch Biochem Biophys 1999; 370: 97-104.
[51] Yalcin AS, Sabuncu N, Kilinc A. Increased plasma and erythrocyte lipid peroxidation in hyperlipidemic individuals. Atherosclerosis 1989; 80: 169-70.
[52] Mehmetcik G, Toker G, Uysal M. Endogenous and copper-induced lipid peroxidation and antioxidant activity of serum in hypercholesterolemic subjects. Horm Metab Res 1997; 29: 63-5.
[53] Anderson JW, Gowri MS, Turner J. Antioxidant supplementation effects on low-density lipoprotein oxidation for individuals with type 2 diabetes mellitus. J Am Coll Nutr 1999; 18: 451-61.
[54] Kurowska EM, Spence JD, Jordan J, Wetmore S, Freeman DJ, Piche LA, Serratore P. HDLcholesterol-raising effect of orange juice in subjects with hypercholesterolemia. Am J Clin Nutr 2000; 72: 1095-1100.
[55] Owu DU, Antai AB, Udofia KH, Obembe AO, Obasi KO, Eteng MU. Vitamin C improves basal metabolic rate and lipid profile in alloxan-induced diabetes mellitus in rats. J Biosci 2006; 31: 5759.
[56]Das S, Snehlata, Srivastava LM. Effect of ascorbic acid on lipid profile and lipid peroxidation in hypercholesterolemic rabbits. Nutr Res 1997; 17:231-41.
[57] Prasad K, Karla J. Oxygen free radicals and hypercholesterolemic atherosclerosis: effect of vitamin E. Am Heart J 1993; 125: 958-73.
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