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Effect of Camellia sinensis, Hypericum perforatum and Urtica dioica on kidney and liver injury induced by carbon tetrachloride in rats
Corresponding Author(s) : Sahabettin Selek
Cellular and Molecular Biology,
Vol. 65 No. 5: Issue 5
Abstract
This study is aimed to investigate the effects of Camellia sinensis (CS), Hypericum perforatum (HP) and Urtica dioica (UD) in kidney and liver injury induced by carbon tetrachloride (CCl4) in rats. Highly toxic CCl4 which is used as a solvent in industry comprises experimental toxicity in rats and is widely used in hepatotoxicity and other tissue injury models. The purpose of this investigation is to monitor blood and various tissues by biochemical and histopathological analysis for preventive effects of CS, HP and UD on oxidative stress induced by administration of CCl4 and to enlighten the probable mechanism. Fifty eight rats were divided into five groups; sham group (Group 1, untreated animals), control CCl4 treated group (Group 2), HP extract-treated group (Group 3), UD extract-treated group (Group 4), CS extract-treated group (Group 5). All rats were anaesthetized at the end of the experiment and the blood was collected from each rat. Afterwards, tissue specimens were obtained. The tissue specimens were immersed in 10% formaldehyde for 24 hours. After routine tissue processing, the liver, kidney and stomach were sectioned in 5µm thickness, stained in hematoxylin and eosin. The histological study was performed by using light microscope. The serum marker enzymes were found to be significantly increased in CCl4–induced liver and kidney damage when compared with the sham group (p<0.05). However, treatment with CS, HP, and UD extracts resulted in decreased activity of serum enzymes. Malondialdehyde (MDA) levels were decreased by 20.51±0.95, 27.98±1.58, and 32.39±3.1 nmol/g wet weight protein in kidney homogenates and 16.65±1.75, 17.22±0.71 and 18.92±71 nmol/g wet weight protein in liver homogenates in CS, HP and UD treated groups, respectively. Our results have shown that additive antioxidants like CS, HP and UD will aid in diminishing these deviations in cases of liver and kidney dysfunction.
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- Edwards M, Keller B, Kauffman F, Thurman R. The involvement of Kupffer cells in carbon tetrachloride toxicity. Toxicology and applied pharmacology. 1993;119(2):275-9.
- Johnston DE, Kroening C. Mechanism of early carbon tetrachloride toxicity in cultured rat hepatocytes. Pharmacology & toxicology. 1998;83(6):231-9.
- Persson JO, Terelius Y, Ingelman-Sundberg M. Cytochrome P-450-dependent formation of reactive oxygen radicals: isozyme-specific inhibition of P-450-mediated reduction of oxygen and carbon tetrachloride. Xenobiotica; the fate of foreign compounds in biological systems. 1990;20(9):887-900.
- Adewole S, Salako A, Doherty O, Naicker T. Effect of melatonin on carbon tetrachloride- induced kidney injury in wistar rats. African Journal of Biomedical Research. 2010;10(2).
- Esterbauer H, Gebicki J, Puhl H, Jurgens G. The role of lipid peroxidation and antioxidants in oxidative modification of LDL. Free Radic Biol Med. 1992;13(4):341-90.
- Tirkey N, Pilkhwal S, Kuhad A, Chopra K. Hesperidin, a citrus bioflavonoid, decreases the oxidative stress produced by carbon tetrachloride in rat liver and kidney. BMC Pharmacol. 2005;5(1):2.
- Dahanukar S, Kulkarni R, Rege N. Pharmacology of medicinal plants and natural products. Indian journal of pharmacology. 2000;32(4):S81-S118.
- Gomes A, Vedasiromoni JR, Das M, Sharma RM, Ganguly DK. Anti-hyperglycemic effect of black tea (Camellia sinensis) in rat. J Ethnopharmacol. 1995;45(3):223-6.
- Packer JE, Slater TF, Willson RL. Direct observation of a free radical interaction between vitamin E and vitamin C. Nature. 1979;278(5706):737-8.
- Tanaka H, Hirose M, Kawabe M, Sano M, Takesada Y, Hagiwara A, et al. Post-initiation inhibitory effects of green tea catechins on 7,12-dimethylbenz[a]anthracene-induced mammary gland carcinogenesis in female Sprague-Dawley rats. Cancer Lett. 1997;116(1):47-52.
- Akbay P, Basaran AA, Undeger U, Basaran N. In vitro immunomodulatory activity of flavonoid glycosides from Urtica dioica L. Phytother Res. 2003;17(1):34-7.
- Ernst E, Rand JI, Barnes J, Stevinson C. Adverse effects profile of the herbal antidepressant St. John's wort (Hypericum perforatum L.). Eur J Clin Pharmacol. 1998;54(8):589-94.
- Tahri A, Yamani S, Legssyer A, Aziz M, Mekhfi H, Bnouham M, et al. Acute diuretic, natriuretic and hypotensive effects of a continuous perfusion of aqueous extract of Urtica dioica in the rat. J Ethnopharmacol. 2000;73(1-2):95-100.
- Khan AU, Gilani AH. Antidiarrheal, antisecretory, and bronchodilatory activities of Hypericum perforatum. Pharm Biol. 2009;47(10):962-7.
- Capasso R, Borrelli F, Capasso F, Mascolo N, Izzo AA. Inhibitory effect of the antidepressant St. John's Wort (hypericum perforatum) on rat bladder contractility in vitro. Urology. 2004;64(1):168-72.
- Gulcin I, Kufrevioglu OI, Oktay M, Buyukokuroglu ME. Antioxidant, antimicrobial, antiulcer and analgesic activities of nettle (Urtica dioica L.). J Ethnopharmacol. 2004;90(2-3):205-15.
- Lin JK, Liang YC, Lin-Shiau SY. Cancer chemoprevention by tea polyphenols through mitotic signal transduction blockade. Biochem Pharmacol. 1999;58(6):911-5.
- Siddiqui IA, Saleem M, Adhami VM, Asim M, Mukhtar H. Tea beverage in chemoprevention and chemotherapy of prostate cancer. Acta Pharmacol Sin. 2007;28(9):1392-408.
- Olfert ED, Cross BM, McWilliam AA. Guide to the care and use of experimental animals: Canadian Council on Animal Care Ottawa; 1993.
- Goldner J. A modification of the Masson trichrome technique for routine laboratory purposes. The American journal of pathology. 1938;14(2):237.
- Hegde K, Henein M, Varma S. Establishment of the mouse as a model animal for the study of diabetic cataracts. Ophthalmic research. 2003;35(1):12-8.
- Obrosova IG, Fathallah L, Greene DA. Early changes in lipid peroxidation and antioxidative defense in diabetic rat retina: effect of dl-α-lipoic acid. European Journal of Pharmacology. 2000;398(1):139-46.
- Johansson LH, Borg LA. A spectrophotometric method for determination of catalase activity in small tissue samples. Anal Biochem. 1988;174(1):331-6.
- Habig WH, Pabst MJ, Jakoby WB. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem. 1974;249(22):7130-9.
- Kakkar P, Das B, Viswanathan PN. A modified spectrophotometric assay of superoxide dismutase. Indian J Biochem Biophys. 1984;21(2):130-2.
- Tappel AL. Glutathione peroxidase and hydroperoxides. Methods in enzymology. 1978;52:506-13.
- Zar JH. Biostatistical analysis, 663 pp. Prentice Hall, Englewood Cliffs; 1999.
- Lundh HA. Sequence Comparison between Kidney and Liver Lesions in the Rat following Carbon Tetrachloride Poisoning. Journal of Occupational and Environmental Medicine. 1964;6(3):123-8.
- Gentilini P, La Villa G. Liver–kidney pathophysiological interrelationships in liver diseases. Digestive and Liver Disease. 2008;40(12):909-19.
- Salomon MI, Zak FG. The kidney in hepatic disease and in gout: clinical and pathologic aspects. J Am Geriatr Soc. 1966;14(5):475-89.
- Striker GE, Smuckler EA, Kohnen PW, Nagle RB. Structural and functional changes in rat kidney during CCl4 intoxication. Am J Pathol. 1968;53(5):769-89.
- Walker G, Kunz D, Pignat W, Wiesenberg I, Van den Bosch H, Pfeilschifter J. Tetranactin inhibits interleukin 1 beta and cAMP induction of group II phospholipase A2 in rat renal mesangial cells. Eur J Pharmacol. 1996;306(1-3):265-70.
- Zimmerman HJ, Kodera Y, West M. Rate of Increase in Plasma Levels of Cytoplasmic and Mitochondrial Enzymes in Experimental Carbon Tetrachloride Hepatotoxicity. J Lab Clin Med. 1965;66(2):315-23.
- Aleynik SI, Leo MA, Ma XL, Aleynik MK, Lieber CS. Polyenylphosphatidylcholine prevents carbon tetrachloride-induced lipid peroxidation while it attenuates liver fibrosis. J Hepatol. 1997;27(3):554-61.
- Recknagel RO, Glende EA, Jr., Dolak JA, Waller RL. Mechanisms of carbon tetrachloride toxicity. Pharmacol Ther. 1989;43(1):139-54.
- Rincon AR, Covarrubias A, Pedraza-Chaverri J, Poo JL, Armendariz-Borunda J, Panduro A. Differential effect of CCl4 on renal function in cirrhotic and non-cirrhotic rats. Exp Toxicol Pathol. 1999;51(3):199-205.
- Williamson EM, Okpako DT, Evans FJ. Selection, preparation and pharmacological evaluation of plant material: John Wiley & Sons; 1996.
- Imai M, Kokko JP. Sodium chloride, urea, and water transport in the thin ascending limb of Henle. Generation of osmotic gradients by passive diffusion of solutes. J Clin Invest. 1974;53(2):393-402.
- Laks MM, Pincus IJ, Goldberg D. Renal excretion of bilirubin in the common duct ligated dog. Gastroenterology. 1963;44(4):469-74.
- Balch PA. Prescription for nutritional healing: Penguin; 2006.
- Butt AA, Michaels S, Greer D, Clark R, Kissinger P, Martin DH. Serum LDH level as a clue to the diagnosis of histoplasmosis. The AIDS reader. 2002;12(7):317-21.
- Cattell V, Cook T, Moncada S. Glomeruli synthesize nitrite in experimental nephrotoxic nephritis. Kidney Int. 1990;38(6):1056-60.
- Halliwell B, Gutteridge JM. Free radicals in biology and medicine: Oxford University Press, USA; 2015.
- Yamamoto Y, Yamashita S. Plasma ubiquinone to ubiquinol ratio in patients with hepatitis, cirrhosis, and hepatoma, and in patients treated with percutaneous transluminal coronary reperfusion. Biofactors. 1999;9(2-4):241-6.
- Branten AJ, Mulder TP, Peters WH, Assmann KJ, Wetzels JF. Urinary excretion of glutathione S transferases alpha and pi in patients with proteinuria: reflection of the site of tubular injury. Nephron. 2000;85(2):120-6.
- Tsukahara H, Toyo-Oka M, Kanaya Y, Ogura K, Kawatani M, Hata A, et al. Quantitation of glutathione S transferase-pi in the urine of preterm neonates. Pediatr Int. 2005;47(5):528-31.
- Matsushima H, Yonemura K, Ohishi K, Hishida A. The role of oxygen free radicals in cisplatin-induced acute renal failure in rats. J Lab Clin Med. 1998;131(6):518-26.
- Weber LWD, Boll M, Stampfl A. Hepatotoxicity and Mechanism of Action of Haloalkanes: Carbon Tetrachloride as a Toxicological Model. Critical Reviews in Toxicology. 2003;33(2):105-36.
- Mei Y, Wei D, Liu J. Reversal of multidrug resistance in KB cells with tea polyphenol antioxidant capacity. Cancer Biol Ther. 2005;4(4):468-73.
- Shapiro H, Singer P, Halpern Z, Bruck R. Polyphenols in the treatment of inflammatory bowel disease and acute pancreatitis. Gut. 2007;56(3):426-35.
- Mennini T, Gobbi M. The antidepressant mechanism of Hypericum perforatum. Life sciences. 2004;75(9):1021-7.
- Barnes J, Anderson LA, Phillipson JD. St John's wort (Hypericum perforatum L.): a review of its chemistry, pharmacology and clinical properties. J Pharm Pharmacol. 2001;53(5):583-600.
- Obertreis B, Ruttkowski T, Teucher T, Behnke B, Schmitz H. Ex-vivo in-vitro inhibition of lipopolysaccharide stimulated tumor necrosis factor-alpha and interleukin-1 beta secretion in human whole blood by extractum urticae dioicae foliorum. Arzneimittelforschung. 1996;46(4):389-94.
- Riehemann K, Behnke B, Schulze-Osthoff K. Plant extracts from stinging nettle (Urtica dioica), an antirheumatic remedy, inhibit the proinflammatory transcription factor NF-κB. FEBS Letters. 1999;442(1):89-94.
References
Edwards M, Keller B, Kauffman F, Thurman R. The involvement of Kupffer cells in carbon tetrachloride toxicity. Toxicology and applied pharmacology. 1993;119(2):275-9.
Johnston DE, Kroening C. Mechanism of early carbon tetrachloride toxicity in cultured rat hepatocytes. Pharmacology & toxicology. 1998;83(6):231-9.
Persson JO, Terelius Y, Ingelman-Sundberg M. Cytochrome P-450-dependent formation of reactive oxygen radicals: isozyme-specific inhibition of P-450-mediated reduction of oxygen and carbon tetrachloride. Xenobiotica; the fate of foreign compounds in biological systems. 1990;20(9):887-900.
Adewole S, Salako A, Doherty O, Naicker T. Effect of melatonin on carbon tetrachloride- induced kidney injury in wistar rats. African Journal of Biomedical Research. 2010;10(2).
Esterbauer H, Gebicki J, Puhl H, Jurgens G. The role of lipid peroxidation and antioxidants in oxidative modification of LDL. Free Radic Biol Med. 1992;13(4):341-90.
Tirkey N, Pilkhwal S, Kuhad A, Chopra K. Hesperidin, a citrus bioflavonoid, decreases the oxidative stress produced by carbon tetrachloride in rat liver and kidney. BMC Pharmacol. 2005;5(1):2.
Dahanukar S, Kulkarni R, Rege N. Pharmacology of medicinal plants and natural products. Indian journal of pharmacology. 2000;32(4):S81-S118.
Gomes A, Vedasiromoni JR, Das M, Sharma RM, Ganguly DK. Anti-hyperglycemic effect of black tea (Camellia sinensis) in rat. J Ethnopharmacol. 1995;45(3):223-6.
Packer JE, Slater TF, Willson RL. Direct observation of a free radical interaction between vitamin E and vitamin C. Nature. 1979;278(5706):737-8.
Tanaka H, Hirose M, Kawabe M, Sano M, Takesada Y, Hagiwara A, et al. Post-initiation inhibitory effects of green tea catechins on 7,12-dimethylbenz[a]anthracene-induced mammary gland carcinogenesis in female Sprague-Dawley rats. Cancer Lett. 1997;116(1):47-52.
Akbay P, Basaran AA, Undeger U, Basaran N. In vitro immunomodulatory activity of flavonoid glycosides from Urtica dioica L. Phytother Res. 2003;17(1):34-7.
Ernst E, Rand JI, Barnes J, Stevinson C. Adverse effects profile of the herbal antidepressant St. John's wort (Hypericum perforatum L.). Eur J Clin Pharmacol. 1998;54(8):589-94.
Tahri A, Yamani S, Legssyer A, Aziz M, Mekhfi H, Bnouham M, et al. Acute diuretic, natriuretic and hypotensive effects of a continuous perfusion of aqueous extract of Urtica dioica in the rat. J Ethnopharmacol. 2000;73(1-2):95-100.
Khan AU, Gilani AH. Antidiarrheal, antisecretory, and bronchodilatory activities of Hypericum perforatum. Pharm Biol. 2009;47(10):962-7.
Capasso R, Borrelli F, Capasso F, Mascolo N, Izzo AA. Inhibitory effect of the antidepressant St. John's Wort (hypericum perforatum) on rat bladder contractility in vitro. Urology. 2004;64(1):168-72.
Gulcin I, Kufrevioglu OI, Oktay M, Buyukokuroglu ME. Antioxidant, antimicrobial, antiulcer and analgesic activities of nettle (Urtica dioica L.). J Ethnopharmacol. 2004;90(2-3):205-15.
Lin JK, Liang YC, Lin-Shiau SY. Cancer chemoprevention by tea polyphenols through mitotic signal transduction blockade. Biochem Pharmacol. 1999;58(6):911-5.
Siddiqui IA, Saleem M, Adhami VM, Asim M, Mukhtar H. Tea beverage in chemoprevention and chemotherapy of prostate cancer. Acta Pharmacol Sin. 2007;28(9):1392-408.
Olfert ED, Cross BM, McWilliam AA. Guide to the care and use of experimental animals: Canadian Council on Animal Care Ottawa; 1993.
Goldner J. A modification of the Masson trichrome technique for routine laboratory purposes. The American journal of pathology. 1938;14(2):237.
Hegde K, Henein M, Varma S. Establishment of the mouse as a model animal for the study of diabetic cataracts. Ophthalmic research. 2003;35(1):12-8.
Obrosova IG, Fathallah L, Greene DA. Early changes in lipid peroxidation and antioxidative defense in diabetic rat retina: effect of dl-α-lipoic acid. European Journal of Pharmacology. 2000;398(1):139-46.
Johansson LH, Borg LA. A spectrophotometric method for determination of catalase activity in small tissue samples. Anal Biochem. 1988;174(1):331-6.
Habig WH, Pabst MJ, Jakoby WB. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem. 1974;249(22):7130-9.
Kakkar P, Das B, Viswanathan PN. A modified spectrophotometric assay of superoxide dismutase. Indian J Biochem Biophys. 1984;21(2):130-2.
Tappel AL. Glutathione peroxidase and hydroperoxides. Methods in enzymology. 1978;52:506-13.
Zar JH. Biostatistical analysis, 663 pp. Prentice Hall, Englewood Cliffs; 1999.
Lundh HA. Sequence Comparison between Kidney and Liver Lesions in the Rat following Carbon Tetrachloride Poisoning. Journal of Occupational and Environmental Medicine. 1964;6(3):123-8.
Gentilini P, La Villa G. Liver–kidney pathophysiological interrelationships in liver diseases. Digestive and Liver Disease. 2008;40(12):909-19.
Salomon MI, Zak FG. The kidney in hepatic disease and in gout: clinical and pathologic aspects. J Am Geriatr Soc. 1966;14(5):475-89.
Striker GE, Smuckler EA, Kohnen PW, Nagle RB. Structural and functional changes in rat kidney during CCl4 intoxication. Am J Pathol. 1968;53(5):769-89.
Walker G, Kunz D, Pignat W, Wiesenberg I, Van den Bosch H, Pfeilschifter J. Tetranactin inhibits interleukin 1 beta and cAMP induction of group II phospholipase A2 in rat renal mesangial cells. Eur J Pharmacol. 1996;306(1-3):265-70.
Zimmerman HJ, Kodera Y, West M. Rate of Increase in Plasma Levels of Cytoplasmic and Mitochondrial Enzymes in Experimental Carbon Tetrachloride Hepatotoxicity. J Lab Clin Med. 1965;66(2):315-23.
Aleynik SI, Leo MA, Ma XL, Aleynik MK, Lieber CS. Polyenylphosphatidylcholine prevents carbon tetrachloride-induced lipid peroxidation while it attenuates liver fibrosis. J Hepatol. 1997;27(3):554-61.
Recknagel RO, Glende EA, Jr., Dolak JA, Waller RL. Mechanisms of carbon tetrachloride toxicity. Pharmacol Ther. 1989;43(1):139-54.
Rincon AR, Covarrubias A, Pedraza-Chaverri J, Poo JL, Armendariz-Borunda J, Panduro A. Differential effect of CCl4 on renal function in cirrhotic and non-cirrhotic rats. Exp Toxicol Pathol. 1999;51(3):199-205.
Williamson EM, Okpako DT, Evans FJ. Selection, preparation and pharmacological evaluation of plant material: John Wiley & Sons; 1996.
Imai M, Kokko JP. Sodium chloride, urea, and water transport in the thin ascending limb of Henle. Generation of osmotic gradients by passive diffusion of solutes. J Clin Invest. 1974;53(2):393-402.
Laks MM, Pincus IJ, Goldberg D. Renal excretion of bilirubin in the common duct ligated dog. Gastroenterology. 1963;44(4):469-74.
Balch PA. Prescription for nutritional healing: Penguin; 2006.
Butt AA, Michaels S, Greer D, Clark R, Kissinger P, Martin DH. Serum LDH level as a clue to the diagnosis of histoplasmosis. The AIDS reader. 2002;12(7):317-21.
Cattell V, Cook T, Moncada S. Glomeruli synthesize nitrite in experimental nephrotoxic nephritis. Kidney Int. 1990;38(6):1056-60.
Halliwell B, Gutteridge JM. Free radicals in biology and medicine: Oxford University Press, USA; 2015.
Yamamoto Y, Yamashita S. Plasma ubiquinone to ubiquinol ratio in patients with hepatitis, cirrhosis, and hepatoma, and in patients treated with percutaneous transluminal coronary reperfusion. Biofactors. 1999;9(2-4):241-6.
Branten AJ, Mulder TP, Peters WH, Assmann KJ, Wetzels JF. Urinary excretion of glutathione S transferases alpha and pi in patients with proteinuria: reflection of the site of tubular injury. Nephron. 2000;85(2):120-6.
Tsukahara H, Toyo-Oka M, Kanaya Y, Ogura K, Kawatani M, Hata A, et al. Quantitation of glutathione S transferase-pi in the urine of preterm neonates. Pediatr Int. 2005;47(5):528-31.
Matsushima H, Yonemura K, Ohishi K, Hishida A. The role of oxygen free radicals in cisplatin-induced acute renal failure in rats. J Lab Clin Med. 1998;131(6):518-26.
Weber LWD, Boll M, Stampfl A. Hepatotoxicity and Mechanism of Action of Haloalkanes: Carbon Tetrachloride as a Toxicological Model. Critical Reviews in Toxicology. 2003;33(2):105-36.
Mei Y, Wei D, Liu J. Reversal of multidrug resistance in KB cells with tea polyphenol antioxidant capacity. Cancer Biol Ther. 2005;4(4):468-73.
Shapiro H, Singer P, Halpern Z, Bruck R. Polyphenols in the treatment of inflammatory bowel disease and acute pancreatitis. Gut. 2007;56(3):426-35.
Mennini T, Gobbi M. The antidepressant mechanism of Hypericum perforatum. Life sciences. 2004;75(9):1021-7.
Barnes J, Anderson LA, Phillipson JD. St John's wort (Hypericum perforatum L.): a review of its chemistry, pharmacology and clinical properties. J Pharm Pharmacol. 2001;53(5):583-600.
Obertreis B, Ruttkowski T, Teucher T, Behnke B, Schmitz H. Ex-vivo in-vitro inhibition of lipopolysaccharide stimulated tumor necrosis factor-alpha and interleukin-1 beta secretion in human whole blood by extractum urticae dioicae foliorum. Arzneimittelforschung. 1996;46(4):389-94.
Riehemann K, Behnke B, Schulze-Osthoff K. Plant extracts from stinging nettle (Urtica dioica), an antirheumatic remedy, inhibit the proinflammatory transcription factor NF-κB. FEBS Letters. 1999;442(1):89-94.