Ameliorative effect of naringin in acetaminophen-induced hepatic and renal toxicity in laboratory rats: role of FXR and KIM-1

References

• Gum SI, Cho MK. Recent updates on acetaminophen hepatotoxicity: The role of nrf2 in hepatoprotection. Toxicol Res. 2013;29:165–172.
   PubMedGoogle Scholar
• Smilkstein MJ, Douglas DR, Daya MR. Acetaminophen poisoning and liver function. N Engl J Med. 1994;331:1310–1311. author reply 1311-1312.
   PubMed Web of Science ®Google Scholar
• Whitcomb Dc, Block Gd. Association of acetaminophen hepatotoxicity with fasting and ethanol use. JAMA. 1994;272:1845–1850.
   PubMed Web of Science ®Google Scholar
• Jaeschke H, McGill MR, Ramachandran A. Oxidant stress, mitochondria, and cell death mechanisms in drug-induced liver injury: Lessons learned from acetaminophen hepatotoxicity. Drug Metab Rev. 2012;44:88–106.
   PubMed Web of Science ®Google Scholar
• McGill MR, Williams CD, Xie Y, Ramachandran A, Jaeschke H. Acetaminophen-induced liver injury in rats and mice: Comparison of protein adducts, mitochondrial dysfunction, and oxidative stress in the mechanism of toxicity. Toxicol Appl Pharmacol. 2012;264:387–394.
   PubMed Web of Science ®Google Scholar
• Nelson SD. Metabolic activation and drug toxicity. J Med Chem. 1982;25:753–765.
   PubMed Web of Science ®Google Scholar
• Jollow DJ, Mitchell JR, Potter WZ, Davis DC, Gillette JR, Brodie BB. Acetaminophen-induced hepatic necrosis. II. Role of covalent binding in vivo. J Pharmacol Exp Ther. 1973;187:195–202.
   PubMed Web of Science ®Google Scholar
• Shon YH, Nam KS. Protective effect of moutan cortex extract on acetaminophen-induced cytotoxicity in human Chang liver cells. Biol Pharm Bull. 2002;25:1427–1431.
   PubMed Web of Science ®Google Scholar
• Adil M, Visnagri A, Kumar VS, Kandhare AD, Ghosh P, Bodhankar SL. Protective effect of naringin on sodium arsenite induced testicular toxicity via modulation of biochernical perturbations in experimental rats. Pharmacologia. 2014;5:222–234.
   Google Scholar
• Ghule AE, Kandhare AD, Jadhav SS, Zanwar AA, Bodhankar SL. Omega-3-fatty acid adds to the protective effect of flax lignan concentrate in pressure overload-induced myocardial hypertrophy in rats via modulation of oxidative stress and apoptosis. Int Immunopharmacol. 2015;28:751–763.
   PubMed Web of Science ®Google Scholar
• Naguib YM, Azmy RM, Samaka RM, Salem MF. Pleurotus ostreatus opposes mitochondrial dysfunction and oxidative stress in acetaminophen-induced hepato-renal injury. BMC Complement Altern Med. 2014;14:494.
   PubMed Web of Science ®Google Scholar
• Lee FY, de Aguiar Vallim TQ, Chong HK, et al. Activation of the farnesoid X receptor provides protection against acetaminophen-induced hepatic toxicity. Mol Endocrinol. 2010;24:1626–1636.
   PubMed Web of Science ®Google Scholar
• Bassuk JA, Tsichlis PN, Sorof S. Liver fatty acid binding protein is the mitosis-associated polypeptide target of a carcinogen in rat hepatocytes. Proc Natl Acad Sci USA. 1987;84:7547–7551.
   PubMed Web of Science ®Google Scholar
• Kandhare AD, Bodhankar SL, Mohan V, Thakurdesai PA. Prophylactic efficacy and possible mechanisms of oligosaccharides based standardized fenugreek seed extract on high-fat diet-induced insulin resistance in C57BL/6 mice. J Appl Pharm Sci. 2015;5:035–045.
   Google Scholar
• Chen A, Tang Y, Davis V, et al. Liver fatty acid binding protein (L-Fabp) modulates murine stellate cell activation and diet-induced nonalcoholic fatty liver disease. Hepatology. 2013;57:2202–2212.
   PubMed Web of Science ®Google Scholar
• Ichimura T, Asseldonk EJ, Humphreys BD, Gunaratnam L, Duffield JS, Bonventre JV. Kidney injury molecule-1 is a phosphatidylserine receptor that confers a phagocytic phenotype on epithelial cells. J Clin Invest. 2008;118:1657–1668.
   PubMed Web of Science ®Google Scholar
• Visnagri A, Kandhare AD, Bodhankar SL. Renoprotective effect of berberine via intonation on apoptosis and mitochondrial-dependent pathway in renal ischemia reperfusion-induced mutilation. Ren Fail. 2015;37:482–493.
   PubMed Web of Science ®Google Scholar
• Michael SL, Pumford NR, Mayeux PR, Niesman MR, Hinson JA. Pretreatment of mice with macrophage inactivators decreases acetaminophen hepatotoxicity and the formation of reactive oxygen and nitrogen species. Hepatology. 1999;30:186–195.
   PubMed Web of Science ®Google Scholar
• Gardner CR, Heck DE, Yang CS, et al. Role of nitric oxide in acetaminophen-induced hepatotoxicity in the rat. Hepatology. 1998;27:748–754.
   PubMed Web of Science ®Google Scholar
• Armesto J, Frutos N, Gonzalez R, Pascual C. In vitro activation of hepatic glutathione reductase from mice by lobenzarit disodium. Agents Actions. 1993;39:69–71.
   PubMedGoogle Scholar
• Prescott LF. The third Lilly Prize Lecture. University of London, January, 1979. The nephrotoxicity and hepatotoxicity of antipyretic analgesics. Br J Clin Pharmacol. 1979;7:453–462.
   PubMed Web of Science ®Google Scholar
• Subramoniam A, Pushpangadan P. Development of phytomedicines for liver disease. Indian J Pharmacol. 1999;31:166–175.
   Google Scholar
• Ahmed B, Alam T, Khan SA. Hepatoprotective activity of Luffa echinata fruits. J Ethnopharmacol. 2001;76:187–189.
   PubMed Web of Science ®Google Scholar
• Yuan R, Lin Y. Traditional Chinese medicine: An approach to scientific proof and clinical validation. Pharmacol Ther. 2000;86:191–198.
   PubMed Web of Science ®Google Scholar
• Kandhare AD, Raygude KS, Ghosh P, Gosavi TP, Bodhankar SL. Patentability of animal models: India and the Globe. Int J Pharm Biol Arch. 2011;2:1024–1032.
   Google Scholar
• Dole S, Kandhare AD, Ghosh P, Gosavi TP, Bodhankar SL. The health outcome after homeopathic treatment in cases of BPH and LUTS: A prospective clinical study. J Pharm Biomed Sci. 2012;22:1–7.
   Google Scholar
• Kandhare AD, Alam J, Patil MV, Sinha A, Bodhankar SL. Wound healing potential of naringin ointment formulation via regulating the expression of inflammatory, apoptotic and growth mediators in experimental rats. Pharm Biol. 2016;54419–432.
   PubMed Web of Science ®Google Scholar
• Visnagri A, Kandhare AD, Chakravarty S, Ghosh P, Bodhankar SL. Hesperidin, a flavanoglycone attenuates experimental diabetic neuropathy via modulation of cellular and biochemical marker to improve nerve functions. Pharm Biol. 2014;52:814–828.
   PubMed Web of Science ®Google Scholar
• Sarkar A, Sengupta A, Mukhrjee A, et al. Antiulcer potential of morin in acetic acid-induced gastric ulcer via modulation of endogenous biomarkers in laboratory animals. Pharmacologia. 2015;6:273–281.
   Google Scholar
• Kumar VS, Rajmane AR, Adil M, Kandhare AD, Ghosh P, Bodhankar SL. Naringin ameliorates acetic acid induced colitis through modulation of endogenous oxido-nitrosative balance and DNA damage in rats. J Biomed Res. 2014;28:132–145.
   PubMedGoogle Scholar
• Jagetia GC, Reddy TK. The grapefruit flavanone naringin protects against the radiation-induced genomic instability in the mice bone marrow: A micronucleus study. Mutat Res. 2002;519:37–48.
   PubMed Web of Science ®Google Scholar
• Kim DH, Jung EA, Sohng IS, Han JA, Kim TH, Han MJ. Intestinal bacterial metabolism of flavonoids and its relation to some biological activities. Arch Pharm Res. 1998;21:17–23.
   PubMed Web of Science ®Google Scholar
• Jeon SM, Park YB, Choi MS. Antihypercholesterolemic property of naringin alters plasma and tissue lipids, cholesterol-regulating enzymes, fecal sterol and tissue morphology in rabbits. Clin Nutr. 2004;23:1025–1034.
   PubMed Web of Science ®Google Scholar
• Kim HJ, Song JY, Park HJ, Park HK, Yun DH, Chung JH. Naringin protects against rotenone-induced apoptosis in human neuroblastoma SH-SY5Y cells. Korean J Physiol Pharmacol. 2009;13:281–285.
   PubMed Web of Science ®Google Scholar
• Kandhare AD, Ghosh P, Bodhankar SL. Naringin, a flavanone glycoside, promotes angiogenesis and inhibits endothelial apoptosis through modulation of inflammatory and growth factor expression in diabetic foot ulcer in rats. Chem Biol Interact. 2014;219:101–112.
   PubMed Web of Science ®Google Scholar
• Kandhare AD, Raygude KS, Ghosh P, Ghule AE, Bodhankar SL. Neuroprotective effect of naringin by modulation of endogenous biomarkers in streptozotocin induced painful diabetic neuropathy. Fitoterapia. 2012;83:650–659.
   PubMed Web of Science ®Google Scholar
• Adil M, Kandhare AD, Visnagri A, Bodhankar SL. Naringin ameliorates sodium arsenite-induced renal and hepatic toxicity in rats: Decisive role of KIM-1, Caspase-3, TGF-β, and TNF-α. Ren Fail. 2015;37:1396–1407.
   PubMed Web of Science ®Google Scholar
• Ahmad ST, Arjumand W, Nafees S, et al. Hesperidin alleviates acetaminophen induced toxicity in Wistar rats by abrogation of oxidative stress, apoptosis and inflammation. Toxicol Lett. 2012;208:149–161.
   PubMed Web of Science ®Google Scholar
• Hegde K, Joshi AB. Hepatoprotective and antioxidant effect of Carissa spinarum root extract against CCl4 and paracetamol-induced hepatic damage in rats. Bangladesh J Pharmacol. 2010;5:73–76.
   Google Scholar
• Gosavi TP, Kandhare AD, Ghosh P, Bodhankar SL. Anticonvulsant activity of Argentum metallicum, a homeopathic preparation. Der Pharmacia Lettre. 2012;4:626–637.
   Google Scholar
• Kandhare AD, Raygude KS, Ghosh P, Bodhankar SL. The ameliorative effect of fisetin, a bioflavonoid, on ethanol-induced and pylorus ligation-induced gastric ulcer in rats. Int J Green Pharm. 2011;5:236.
   Google Scholar
• Kandhare AD, Bodhankar SL, Singh V, Mohan V, Thakurdesai PA. Anti-asthmatic effects of type-A procyanidine polyphenols from cinnamon bark in ovalbumin-induced airway hyperresponsiveness in laboratory animals. Biomed Aging Pathol. 2013;3:23–30.
   Google Scholar
• Kandhare AD, Ghosh P, Ghule AE, Bodhankar SL. Elucidation of molecular mechanism involved in neuroprotective effect of Coenzyme Q10 in alcohol-induced neuropathic pain. Fundam Clin Pharmacol. 2013;27:603–622.
   PubMed Web of Science ®Google Scholar
• Aswar UM, Kandhare AD, Mohan V, Thakurdesai PA. Anti-allergic effect of intranasal administration of type-A procyanidin polyphenols based standardized extract of cinnamon bark in ovalbumin sensitized BALB/c mice. Phytother Res. 2015;29:423–433.
   PubMed Web of Science ®Google Scholar
• Badole SL, Chaudhari SM, Jangam GB, Kandhare AD, Bodhankar SL. Cardioprotective activity of pongamia pinnata in streptozotocin-nicotinamide induced diabetic rats. Biomed Res Int. 2015;2015:403291.
   PubMed Web of Science ®Google Scholar
• Kandhare AD, Ghosh P, Bodhankar SL. Morin Attenuates Airway Hyperresponsiveness of Allergic Asthma Via Down Regulation of Immune-Inflammatory Biomarkers. Paper presented at: In Proceedings of the 15th International Congress of Immunology (ICI), Milan, Italy, August 22–27, 2013.
   Google Scholar
• Devkar S, Kandhare A, Zanwar A, et al. Hepatoprotective effect of withanolide rich fraction in acetaminophen intoxicated rat: Decisive role of TNF-α, IL-1β, COX-II, and iNOS. Pharm Biol. 2016. [Epub ahead of print]. doi: 10.3109/13880209.2016.1157193.
   PubMedGoogle Scholar
• Kandhare AD, Bodhankar SL, Mohan V, Thakurdesai PA. Acute and repeated doses (28 days) oral toxicity study of glycosides based standardized fenugreek seed extract in laboratory mice. Regul Toxicol Pharmacol. 2015;72:323–334.
   PubMed Web of Science ®Google Scholar
• Ghosh A, Sil PC. Anti-oxidative effect of a protein from Cajanus indicus L against acetaminophen-induced hepato-nephro toxicity. J Biochem Mol Biol. 2007;40:1039–1049.
   PubMedGoogle Scholar
• Nelson SD. Molecular mechanisms of the hepatotoxicity caused by acetaminophen. Paper presented at: Semin Liver Dis, 1990.
   Google Scholar
• Kroyer G. [The antioxidant activity of citrus fruit peels]. Z Ernahrungswiss. 1986;25:63–69.
   PubMedGoogle Scholar
• Anandhi R, Annadurai T, Anitha TS, et al. Antihypercholesterolemic and antioxidative effects of an extract of the oyster mushroom, Pleurotus ostreatus, and its major constituent, chrysin, in Triton WR-1339-induced hypercholesterolemic rats. J Physiol Biochem. 2013;69:313–323.
   PubMed Web of Science ®Google Scholar
• Kamble H, Kandhare AD, Bodhankar SL, Mohan V, Thakurdesai PA. Effect of low molecular weight galactomannans from fenugreek seeds on animal models of diabetes mellitus. Biomed Aging Pathol. 2013;3:145–151.
   Google Scholar
• Goswami S, Kandhare A, Zanwar AA, et al. Oral l-glutamine administration attenuated cutaneous wound healing in Wistar rats. Int Wound J. 2016;13:116–124.
   PubMed Web of Science ®Google Scholar
• Raygude KS, Kandhare AD, Ghosh P, Ghule AE, Bodhankar SL. Evaluation of ameliorative effect of quercetin in experimental model of alcoholic neuropathy in rats. Inflammopharmacology. 2012;20:331–341.
   PubMedGoogle Scholar
• Saraswathi KY, Muthal AP, Kandhare A, Rojatkar S, Bodhankar SL. Study of methanolic extract of artemisia pallens wall on endurance of laboratory animals. Pharmacologia. 2014;5:298–309.
   Google Scholar
• Kandhare AD, Bodhankar SL, Mohan V, Thakurdesai PA. Effect of glycosides based standardized fenugreek seed extract in bleomycin-induced pulmonary fibrosis in rats: Decisive role of Bax, Nrf2, NF-κB, Muc5ac, TNF-α and IL-1β . Chem Biol Interact. 2015;237:151–165.
   PubMed Web of Science ®Google Scholar
• Kandhare AD, Ghosh P, Ghule AE, Zambare GN, Bodhankar SL. Protective effect of Phyllanthus amarus by modulation of endogenous biomarkers and DNA damage in acetic acid induced ulcerative colitis: Role of phyllanthin and hypophyllanthin. Apollo Med. 2013;10:87–97.
   Google Scholar
• Patil A, Guru A, Mukhrjee A, et al. Elucidation of gastro-protective activity of Morin in pylorus ligation induced gastric ulcer via modulation of oxidative stress. Der Pharmacia Lettre. 2015;7:131–139.
   Google Scholar
• Zhou B, Wu LJ, Li LH, et al. Silibinin protects against isoproterenol-induced rat cardiac myocyte injury through mitochondrial pathway after up-regulation of SIRT1. J Pharmacol Sci. 2006;102:387–395.
   PubMed Web of Science ®Google Scholar
• Kandhare AD, Raygude KS, Ghosh P, et al. Effect of hydroalcoholic extract of Hibiscus rosa sinensis Linn. leaves in experimental colitis in rats. Asian Pac J Trop Biomed. 2012;2:337–344.
   PubMedGoogle Scholar
• Visnagri A, Kandhare AD, Shiva Kumar V, et al. Elucidation of ameliorative effect of Co-enzyme Q10 in streptozotocin-induced diabetic neuropathic perturbation by modulation of electrophysiological, biochemical and behavioral markers. Biomed Aging Pathol. 2012;2:157–172.
   Google Scholar
• Olaleye MT, Rocha BT. Acetaminophen-induced liver damage in mice: Effects of some medicinal plants on the oxidative defense system. Exp Toxicol Pathol. 2008;59:319–327.
   PubMed Web of Science ®Google Scholar
• Honmore V, Kandhare A, Zanwar AA, Rojatkar S, Bodhankar S, Natu A. Artemisia pallens alleviates acetaminophen induced toxicity via modulation of endogenous biomarkers. Pharm Biol. 2015;53:571–581.
   PubMed Web of Science ®Google Scholar
• Denicola A, Radi R. Peroxynitrite and drug-dependent toxicity. Toxicology. 2005;208:273–288.
   PubMed Web of Science ®Google Scholar
• Kandhare AD, Shivakumar V, Rajmane A, Ghosh P, Bodhankar SL. Evaluation of the neuroprotective effect of chrysin via modulation of endogenous biomarkers in a rat model of spinal cord injury. J Nat Med. 2014;68:586–603.
   PubMed Web of Science ®Google Scholar
• Ketkar S, Rathore A, Kandhare AD, et al. Alleviating exercise-induced muscular stress using neat and processed bee pollen: Oxidative markers, mitochondrial enzymes, and myostatin expression in rats. Integr Med Res. 2015;4:147–160.
   PubMed Web of Science ®Google Scholar
• Raygude KS, Kandhare AD, Ghosh P, Bodhankar SL. Anticonvulsant effect of fisetin by modulation of endogenous biomarkers. Biomed Prev Nutr. 2012;2:215–222.
   Google Scholar
• Ghosh J, Das J, Manna P, Sil PC. Acetaminophen induced renal injury via oxidative stress and TNF-alpha production: Therapeutic potential of arjunolic acid. Toxicology. 2010;268:8–18.
   PubMed Web of Science ®Google Scholar
• Gardner CR, Laskin JD, Dambach DM, et al. Reduced hepatotoxicity of acetaminophen in mice lacking inducible nitric oxide synthase: Potential role of tumor necrosis factor-alpha and interleukin-10. Toxicol Appl Pharmacol. 2002;184:27–36.
   PubMed Web of Science ®Google Scholar
• Knight TR, Kurtz A, Bajt ML, Hinson JA, Jaeschke H. Vascular and hepatocellular peroxynitrite formation during acetaminophen toxicity: Role of mitochondrial oxidant stress. Toxicol Sci. 2001;62:212–220.
   PubMed Web of Science ®Google Scholar
• Abdel-Zaher AO, Abdel-Rahman MM, Hafez MM, Omran FM. Role of nitric oxide and reduced glutathione in the protective effects of aminoguanidine, gadolinium chloride and oleanolic acid against acetaminophen-induced hepatic and renal damage. Toxicology. 2007;234:124–134.
   PubMed Web of Science ®Google Scholar
• Kandhare AD, Raygude KS, Ghosh P, Ghule AE, Bodhankar SL. Therapeutic role of curcumin in prevention of biochemical and behavioral aberration induced by alcoholic neuropathy in laboratory animals. Neurosci Lett. 2012;511:18–22.
   PubMed Web of Science ®Google Scholar
• Kandhare AD, Raygude KS, Shiva Kumar V, et al. Ameliorative effects quercetin against impaired motor nerve function, inflammatory mediators and apoptosis in neonatal streptozotocin-induced diabetic neuropathy in rats. Biomed Aging Pathol. 2012;2:173–186.
   Google Scholar
• Drotman RB, Lawhorn GT. Serum enzymes as indicators of chemically induced liver damage. Drug Chem Toxicol. 1978;1:163–171.
   PubMed Web of Science ®Google Scholar
• Kandhare AD, Kumar VS, Adil M, Rajmane AR, Ghosh P, Bodhankar SL. Investigation of gastro protective activity of Xanthium strumarium L. by modulation of cellular and biochemical marker. Orient Pharm Exp Med. 2012;12:287–299.
   Google Scholar
• Kim KA, Lee WK, Kim JK, et al. Mechanism of refractory ceramic fiber- and rock wool-induced cytotoxicity in alveolar macrophages. Int Arch Occup Environ Health. 2001;74:9–15.
   PubMed Web of Science ®Google Scholar
• Visnagri A, Kandhare AD, Ghosh P, Bodhankar SL. Endothelin receptor blocker bosentan inhibits hypertensive cardiac fibrosis in pressure overload-induced cardiac hypertrophy in rats. Cardiovasc Endocrinol. 2013;2:85–97.
   Google Scholar
• Kobashigawa JA, Kasiske BL. Hyperlipidemia in solid organ transplantation. Transplantation. 1997;63:331–338.
   PubMed Web of Science ®Google Scholar
• Raghavendran HR, Sathivel A, Devaki T. Effect of Sargassum polycystum (Phaeophyceae)-sulphated polysaccharide extract against acetaminophen-induced hyperlipidemia during toxic hepatitis in experimental rats. Mol Cell Biochem. 2005;276:89–96.
   PubMed Web of Science ®Google Scholar
• Forman BM, Goode E, Chen J, et al. Identification of a nuclear receptor that is activated by farnesol metabolites. Cell. 1995;81:687–693.
   PubMed Web of Science ®Google Scholar
• Fiorucci S, Rizzo G, Donini A, Distrutti E, Santucci L. Targeting farnesoid X receptor for liver and metabolic disorders. Trends Mol Med. 2007;13:298–309.
   PubMed Web of Science ®Google Scholar
• Chen WD, Wang YD, Meng Z, Zhang L, Huang W. Nuclear bile acid receptor FXR in the hepatic regeneration. Biochim Biophys Acta. 2011;1812:888–892.
   PubMed Web of Science ®Google Scholar
• Wagner M, Zollner G, Trauner M. Nuclear receptors in liver disease. Hepatology. 2011;53:1023–1034.
   PubMed Web of Science ®Google Scholar
• Yan J, Gong Y, She YM, Wang G, Roberts MS, Burczynski FJ. Molecular mechanism of recombinant liver fatty acid binding protein’s antioxidant activity. J Lipid Res. 2009;50:2445–2454.
   PubMed Web of Science ®Google Scholar
• Raza H, Pongubala JR, Sorof S. Specific high affinity binding of lipoxygenase metabolites of arachidonic acid by liver fatty acid binding protein. Biochem Biophys Res Commun. 1989;161:448–455.
   PubMed Web of Science ®Google Scholar
• Ek BA, Cistola DP, Hamilton JA, Kaduce TL, Spector AA. Fatty acid binding proteins reduce 15-lipoxygenase-induced oxygenation of linoleic acid and arachidonic acid. Biochim Biophys Acta. 1997;1346:75–85.
   PubMed Web of Science ®Google Scholar
• Wang G, Gong Y, Anderson J, et al. Antioxidative function of L-FABP in L-FABP stably transfected Chang liver cells. Hepatology. 2005;42:871–879.
   PubMed Web of Science ®Google Scholar
• Thadhani R, Pascual M, Bonventre JV. Acute renal failure. N Engl J Med. 1996;334:1448–1460.
   PubMed Web of Science ®Google Scholar
• Bonventre JV. Dedifferentiation and proliferation of surviving epithelial cells in acute renal failure. J Am Soc Nephrol. 2003;14(Suppl 1):S55–S61.
   PubMed Web of Science ®Google Scholar
• Kandhare AD, Patil MV, Bodhankar SL. L-Arginine attenuates the ethylene glycol induced urolithiasis in ininephrectomized hypertensive rats: Role of KIM-1, NGAL, and NOs. Ren Fail. 2015;37:709–721.
   PubMed Web of Science ®Google Scholar