Protective effect of quercetin on lead-induced oxidative stress and endoplasmic reticulum stress in rat liver via the IRE1/JNK and PI3K/Akt pathway

References

• Berridge MJ. The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 2002;32:235–249.
   Google Scholar
• Natsume Y, Ito S, Satsu H, Shimizu M. Protective effect of quercetin on ER stress caused by calcium dynamics dysregulation in intestinal epithelial cells. Toxicology 2009; 258:164–175.
   Google Scholar
• Oyadomari S, Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 2004;11: 381–389.
   Google Scholar
• Mori K, Ogawa N, Kawahara T, Yanagi H, Yura T. mRNA splicing-mediated C-terminal replacement of transcription factor Hac1p is required for efficient activation of the unfolded protein response. Proc Natl Acad Sci USA 2000;97: 4660–4665.
   Google Scholar
• Shen X, Zhang K, Kaufman RJ. The unfolded protein response–a stress signaling pathway of the endoplasmic reticulum. J Chem Neuroanat 2004;28:79–92.
   Google Scholar
• Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007; 8:519–529.
   Google Scholar
• Ni M, Lee AS. ER chaperones in mammalian development and human diseases. FEBS Lett 2007;581:3641–3651.
   Google Scholar
• Shinkai Y, Yamamoto C, Kaji T. Lead induces the expression of endoplasmic reticulum chaperones GRP78 and GRP94 in vascular endothelial cells via the JNK-AP-1 pathway. Toxicol Sci 2010;114:378–386.
   Google Scholar
• Tully DB, Collins BJ, Overstreet JD, Smith CS, Dinse GE, Mumtaz MM, Chapin RE. Effects of arsenic, cadmium, chromium, and lead on gene expression regulated by a battery of 13 different promoters in recombinant HepG2 cells. Toxicol Appl Pharmacol 2000;168:79–90.
   Google Scholar
• El-Ghor AA, Noshy MM, Eid JI. Lead acetate and arsenic trioxide induce instability of microsatellites at three different fragile sites (6q21, 9q32–9q33 and 15p14) within the genome of the rat. Mutat Res 2011;726:195–199.
   Google Scholar
• Shaban El-Neweshy M, Said El-Sayed Y. Influence of vitamin C supplementation on lead-induced histopathological alterations in male rats. Exp Toxicol Pathol 2011;63:221–227.
   Google Scholar
• Qian Y, Falahatpisheh MH, Zheng Y, Ramos KS, Tiffany-Castiglioni E. Induction of 78 kD glucose-regulated protein (GRP78) expression and redox-regulated transcription factor activity by lead and mercury in C6 rat glioma cells. Neurotox Res 2001;3:581–589.
   Google Scholar
• Qian Y, Harris ED, Zheng Y, Tiffany-Castiglioni E. Lead targets GRP78, a molecular chaperone, in C6 rat glioma cells. Toxicol Appl Pharmacol 2000;163:260–266.
   Google Scholar
• White LD, Cory-Slechta DA, Gilbert ME, Tiffany-Castiglioni E, Zawia NH, Virgolini M, . New and evolving concepts in the neurotoxicology of lead. Toxicol Appl Pharmacol 2007; 225:1–27.
   Google Scholar
• Mudipalli A. Lead hepatotoxicity & potential health effects. Indian J Med Res 2007;126:518–527.
   Google Scholar
• Liu CM, Zheng YL, Lu J, Zhang ZF, Fan SH, Wu DM, Ma JQ. Quercetin protects rat liver against lead-induced oxidative stress and apoptosis. Environ Toxicol Pharmacol 2010;29: 158–166.
   Google Scholar
• Liu CM, Ma JQ, Sun YZ. Protective role of puerarin on lead-induced alterations of the hepatic glutathione antioxidant system and hyperlipidemia in rats. Food Chem Toxicol 2011;49:3119–3127.
   Google Scholar
• Liu CM, Ma JQ, Sun YZ. Puerarin protects rat kidney from lead-induced apoptosis by modulating the PI3K/Akt/eNOS pathway. Toxicol Appl Pharmacol 2012;258:330–342.
   Google Scholar
• Liu CM, Sun JM, Sun YZ, Ma JQ, Chao C. Protective role of quercetin against lead-induced in flammatory response in rat kidney through the ROS-mediated MAPKs and NF-κB pathway. Biochimic a et Biophysica Acta 2012;1820: 1693–1703.
   Google Scholar
• Porta C, Figlin RA. Phosphatidylinositol-3-kinase/Akt signaling pathway and kidney cancer, and the therapeutic potential of phosphatidylinositol-3-kinase/Akt inhibitors. J Urology 2009;182:2569–2577.
   Google Scholar
• Han PZ, Couvillon AD, Exton JH. Critical role of endogenous Akt/IAPs and MEK1/ERK pathways in counteracting endoplasmic reticulum stress-induced cell death. J Biol Chem 2004;279:49420–49429.
   Google Scholar
• Dai R, Chen R, Li H. Cross-talk between PI3K/Akt and MEK/ERK pathways mediates endoplasmic reticulum stress-induced cell cycle progression and cell death in human hepatocellular carcinoma cells. Int J Oncol 2009;34:1749–1757.
   Google Scholar
• Wang Z, Zhang H, Xu X, Shi H, Yu X, Wang X, . bFGF inhibits ER stress induced by ischemic oxidative injury via activation of the PI3K/Akt and ERK1/2 pathways. Toxicol Lett 2012;212:137–146.
   Google Scholar
• Franke TF, Hornik CP, Segev L, Shostak GA, Sugimoto C. PI3K/Akt and apoptosis: size matters. Oncogene 2003;22: 8983–8998.
   Google Scholar
• Boots AW, Haenen GR, Bast A. Health effects of quercetin: from antioxidant to nutraceutical. Eur J Pharmacol 2008; 585:325–337.
   Google Scholar
• Ghosh A, Mandal AK, Sarkar S, Panda S, Das N. Nanoencapsulation of quercetin enhances its dietary efficacy in combating arsenic-induced oxidative damage in liver and brain of rats. Life Sci 2009;16:75–80.
   Google Scholar
• Morales AI, Vicente-Sánchez C, Jerkic M, Santiago JM, Sánchez-González PD, Pérez-Barriocanal F, López-Novoa JM. Effect of quercetin on metallothionein, nitric oxide synthases and cyclooxygenase-2 expression on experimental chronic cadmium nephrotoxicity in rats. Toxicol Appl Pharmacol 2006;210:128–135.
   Google Scholar
• Galicia-Moreno M, Favari L, Muriel P. Antifibrotic and antioxidant effects of N-acetylcysteine in an experimental cholestatic model. Eur J Gastroen Hepat 2012;24:179–185.
   Google Scholar
• Haleagrahara N, Jackie T, Chakravarthi S, Rao M, Kulur A. Protective effect of Etlingera elatior (torch ginger) extract on lead acetate-induced hepatotoxicity in rats. J Toxicol Sci 2008; 60:289–294.
   Google Scholar
• Driver AS, Kodavanti PS, Mundy WR. Age related changes in reactive oxygen species production in rat brain homogenates.Neurotox Teratol 2000;22:175–181.
   Google Scholar
• Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979;95:351–358.
   Google Scholar
• Zhang Q, Li N, Zhou G, Lu X, Xu Z, Li Z. In vivo antioxidant activity of polysaccharide fraction from Porphyra haitanesis (Rhodephyta) in aging mice. Pharmacol Res 2003;48: 151–155.
   Google Scholar
• Malhotra JD, Kaufman RJ. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword?Antioxid Redox Sign 2007;9:2277–22793.
   Google Scholar
• Bernales S, McDonald KL, Walter P. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol 2006;4:e423.
   Google Scholar
• Steensma A, Beamand JA, Walters DG, Price RJ, Lake BG. Metabolism of coumarin and 7-ethoxycoumarin by rat, mouse, guinea pig, cynomolgus monkey and man precision-cut liver slices. Xenobiotica 1994;24:893–907.
   Google Scholar
• Zhang Y, Li H, Zhao Y, Gao Z. Dietary supplementation of baicalin and quercetin attenuates iron overload induced mouse liver injury. Eur J Pharmacol 2006;535:263–269.
   Google Scholar
• Xu J, Ji LD, Xu LH. Endoplasmic reticulum may not be involved in the lead-induced apoptosis in PC 12 cells in vitro. Environ Toxicol 2010;25:55–60.
   Google Scholar
• Tchounwou PB, Yedjou CG, Foxx DN, Ishaque AB, Shen E. Lead-induced cytotoxicity and transcriptional activation of stress genes in man liver carcinoma (HepG 2) cells. Mol Cell Biochem 2004;255:161–170.
   Google Scholar
• Sandhir R, Gill KD. Alterations in calcium homeostasis on lead vexposure in rat synaptosomes. Mol Cell Biochem 1994; 131:25–33.
   Google Scholar
• Sharma SK, Goloubinoff P, Christen P. Heavy metal ions are potent inhibitors of protein folding. Biochem Biophys Res Commun 2008;372:341–345.
   Google Scholar
• Arumugam S, Thandavarayan RA, Arozal W, Sari FR, Giridharan VV, Soetikno V, . Quercetin offers cardioprotection against progression of experimental autoimmune myocarditis by suppression of oxidative and endoplasmic reticulum stress via endothelin-1/MAPK signalling. Free Radical Res 2012;46:154–163.
   Google Scholar
• Ohta K, Mizuno A, Li S, Itoh M, Ueda M, Ohta E, . Endoplasmic reticulum stress enhances γ-secretase activity. Biochem Biophys Res Commun 2011;416:362–366.
   Google Scholar
• Jiang Y, Zhang Y, Wark L, Ortiz E, Lim S, He H, . Wolfberry water soluble phytochemicals down-regulate ER stress biomarkers and modulate multiple signaling pathways leading to inhibition of proliferation and induction of apoptosis in jurkat cells. J Nutr Food Sci 2011;S2:1–6.
   Google Scholar
• Jurczuk M, Moniuszko-Jakoniuk J, Brzóska MM. Hepatic and renal concentrations of vitamins E and C in Lead- and ethanol-exposed rats. An assessment of their involvement in the mechanisms of peroxidative damage. Food Chem Toxicol 2007;45:1478–1486.
   Google Scholar
• Villarreal-Trevino CM, Villegas-Navarro A. Differential Accumulation of lead by soft tissues of rabbit. Bull Environ Contam Toxicol 1987;39:334–342.
   Google Scholar
• Malešev D, Kuntić V. Investigation of metal–flavonoid chelates and the determination of flavonoids via metal–flavonoid complexing reactions. J Serb Chem Soc 2007;72:921–939.
   Google Scholar
• Amudha K, Pari L. Beneficial role of naringin, a flavanoid on nickel induced nephrotoxicity in rats. Chem Biol Interact 2011;193:57–64.
   Google Scholar
• Pari L, Amudha K. Hepatoprotective role of naringin on nickel-induced toxicity in male Wistar rats. Eur J Pharmacol 2011;650:364–370.
   Google Scholar
• Hu P, Wang M, Chen WH, Liu J, Chen L, Yin ST, . Quercetin relieves chronic lead exposure-induced impairment of synaptic plasticity in rat dentate gyrus in vivo. Naunyn-Schmiedeberg's Arch Pharmacol 2008;378:43–51.
   Google Scholar
• Franco R, Sánchez-Olea R, Reyes-Reyes EM, Panayiotidis MI. Environmental toxicity, oxidative stress and apoptosis:Ménage à Trois Mutat Res 2009;674:3–22.
   Google Scholar
• Kitamura M, Hiramatsu N. The oxidative stress: endoplasmic reticulum stress axis in cadmium toxicity. Biometals 2010; 23:941–950.
   Google Scholar
• Fraga CG, Galleano M, Verstraeten S, Oteiza PI. Basic biochemical mechanisms behind the health benefits of polyphenols. Mol. Aspects Med 2010;31:435–445.
   Google Scholar
• Wiseman RL, Zhang Y, Lee KPK, Harding HP, Haynes CM, Price J, . Flavonol activation defines an unanticipated ligand binding site in the kinase-RNase domain of IRE1. Mol Cell 2010;38:291–304.
   Google Scholar
• Matsukawa J, Matsuzawa A, Takeda K, Ichijo H. The ASK1-MAP kinase cascades in mammalian stress response. J Biochem 2004;136:261–265.
   Google Scholar
• Haas MJ, Raheja P, Jaimungal S, Sheikh-Ali M, Mooradian AD. Estrogen-dependent inhibition of dextrose-induced endoplasmic reticulum stress and superoxide generation in endothelial cells. Free Radical Biol Med 2012;52:2161–2167.
   Google Scholar
• Xu M, Zhang F, Da L, Li T, Zhao M. Microspherule protein 2 associates with ASK1 and acts as a negative regulator of stress-induced ASK1 activation. FEBS Lett 2012;586: 1678–1686.
   Google Scholar
• Hosoi T, Hyoda K, Okuma Y, Nomura Y, Ozawa K. Akt up- and down-regulation in response to endoplasmic reticulum stress. Brain Res 2007;1152:27–31.
   Google Scholar
• McGuckin MA, Eri RD, Das I, Lourie R, Florin TH. ER stress and the unfolded protein response in intestinal inflammation. Am J Physiol Gastrointest Liver Physiol 2010;298: 820–832.
   Google Scholar
• Bobrovnikova-Marjon E, Pytel D, Riese MJ, Vaites LP, Singh N, Koretzky GA, . PERK utilizes intrinsic lipid kinase activity to generate phosphatidic acid, mediate Akt activation, and promote adipocyte differentiation. Mol Cell Biol 2012;32:2268–2278.
   Google Scholar
• Li C, Xing T, Tang M, Yong W, Yan D, Deng H, . Involvement of cyclin D1/CDK4 and pRb mediated by PI3K/AKT pathway activation in Pb2+-induced neuronal death in cultured hippocampal neurons. Toxicol Appl Pharmacol 2008;229:351–361.
   Google Scholar