Protective effect of naringin against BPA-induced cardiotoxicity through prevention of oxidative stress in male Wistar rats

References

• Ahangarpour, A., 2018. Chronic exposure to arsenic and high fat diet additively induced cardiotoxicity in male mice. Research in Pharmaceutical Sciences, 13 (1), 47–56.
   PubMed Web of Science ®Google Scholar
• Alam, M.A., et al., 2013. Naringin improves diet-induced cardiovascular dysfunction and obesity in high carbohydrate, high fat diet-fed rats. Nutrients, 5 (3), 637–650.
   PubMed Web of Science ®Google Scholar
• Anderson, E.J., et al., 2012. Mitochondria as a source and target of lipid peroxidation products in healthy and diseased heart. Clinical and Experimental Pharmacology and Physiology, 39 (2), 179–193.,
   PubMed Web of Science ®Google Scholar
• Arafa, H.M., et al., 2005. Abatement by naringenin of doxorubicin-induced cardiac toxicity in rats. JNCI: Journal of the National Cancer Institute, 17, 291–300.
   Google Scholar
• Arslan, F., et al., 2013. Mesenchymal stem cell-derived exosomes increase ATP levels, decrease oxidative stress and activate PI3K/Akt pathway to enhance myocardial viability and prevent adverse remodeling after myocardial ischemia/reperfusion injury. Stem Cell Research, 10 (3), 301–312.
   PubMed Web of Science ®Google Scholar
• Asano, S., et al., 2010. Bisphenol A activates Maxi-K (K(Ca)1.1) channels in coronary smooth muscle. British Journal of Pharmacology, 160 (1), 160–170.
   PubMed Web of Science ®Google Scholar
• Aydoğan, M., et al., 2008. The effect of vitamin C on bisphenol A, nonylphenol and octylphenol induced brain damages of male rats. Toxicology, 249 (1), 35–39.
   PubMed Web of Science ®Google Scholar
• Aydoğan, M., et al., 2010. Pro-oxidant effect of vitamin C coadministration with bisphenol A, nonylphenol, and octylphenol on the reproductive tract of male rats. Drug Chemical Toxicology, 33 (2), 193–203.
   PubMed Web of Science ®Google Scholar
• Bae, S., et al., 2012. Associations of bisphenol A exposure with heart rate variability and blood pressure. Hypertension, 112, 1–9.
   Google Scholar
• Baradaran, A., Nasri, H., and Rafieian-Kopaei, M., 2014. Oxidative stress and hypertension: Possibility of hypertension therapy with antioxidants. Journal of Research in Medical Sciences, 19, 358–367.
   PubMed Web of Science ®Google Scholar
• Bindhumol, V., Chitra, K.C., and Mathur, P.P., 2003. Bisphenol A induces reactive oxygen species generation in the liver of male rats. Toxicology, 188 (2–3), 117–124.
   PubMed Web of Science ®Google Scholar
• Briones, A.M., and Touyz, R.M., 2010. Oxidative stress and hypertension: current concepts. Current Hypertension Reports, 12 (2), 135–142.
   PubMed Web of Science ®Google Scholar
• Calafat, A.M., et al., 2004. Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population. Environmental Health Perspectives, 113 (4), 391–395.
   Web of Science ®Google Scholar
• Calafat, A.M., et al., 2007. Exposure of the US population to bisphenol A and 4-tertiary-octylphenol: 2003–2004. Environmental Health Perspectives, 116 (1), 39–44.
   Web of Science ®Google Scholar
• Celiz, G., Daz, M., and Audisio, M.C., 2011. Antibacterial activity of naringin derivatives against pathogenic strains. Journal of Applied Microbiology, 111 (3), 731–738.
   PubMed Web of Science ®Google Scholar
• Chen, J., et al., 2014a. Naringin Inhibits ROS-activated MAPK pathway in high glucose-induced injuries in H9c2 cardiac cells. Basic and Clinical Pharmacology and Toxicology, 114 (4), 293–304.
   PubMed Web of Science ®Google Scholar
• Chen, J., et al., 2014b. Inhibition of the leptin-induced activation of the p38 MAPK pathway contributes to the protective effects of naringin against high glucose-induced injury in H9c2 cardiac cells. International Journal of Molecular Medicine, 33 (3), 605–612.
   PubMed Web of Science ®Google Scholar
• Chitra, K., Latchoumycandane, C., and Mathur, P., 2003. Induction of oxidative stress by bisphenol A in the epididymal sperm of rats. Toxicology, 185 (1–2), 119–127.
   PubMed Web of Science ®Google Scholar
• Diamanti-Kandarakis, E., et al., 2009. Endocrine-disrupting chemicals: an endocrine society scientific statement. Endocrine Reviews, 30 (4), 293–342.
   PubMed Web of Science ®Google Scholar
• Ellman, G.L., 1959. Tissue sulfhydryl groups. Archives of Biochemistry and Biophysics, 82 (1), 70–77.
   PubMed Web of Science ®Google Scholar
• Ezz, H.S.A., Khadrawy, Y.A., and Mourad, I.M., 2015. The effect of bisphenol A on some oxidative stress parameters and acetylcholinesterase activity in the heart of male albino rats. Cytotechnology, 67 (1), 145–155.
   PubMed Web of Science ®Google Scholar
• Fang, F., et al., 2015. Effects of Bisphenol A on glucose homeostasis and brain insulin signaling pathways in male mice. General and Comparative Endocrinology, 212, 44–50.
   PubMed Web of Science ®Google Scholar
• Förstermann, U., 2010. Nitric oxide and oxidative stress in vascular disease. Pflügers Archiv-European Journal of Physiology, 4, 923–939.
   Web of Science ®Google Scholar
• Gong, Y., and Han, X.D., 2006. Nonylphenol-induced oxidative stress and cytotoxicity in testicular sertoli cells. Reproductive Toxicology, 22 (4), 623–630.
   PubMed Web of Science ®Google Scholar
• Grohe, C., et al., 1998. Expression of oestrogen receptor alpha and beta in rat heart: role of local oestrogen synthesis. Journal of Endocrinology, 156 (2), R1–R7.
   PubMed Web of Science ®Google Scholar
• Hassani, F.V., et al., 2017. Protective effect of crocin on BPA-induced liver toxicity in rats through inhibition of oxidative stress and downregulation of MAPK and MAPKAP signaling pathway and miRNA-122 expression. Food and Chemical Toxicology, 107, 395–405.
   PubMed Web of Science ®Google Scholar
• Ho, E., et al., 2013. Biological markers of oxidative stress: applications to cardiovascular research and practice. Redox Biology, 1 (1), 483–491.
   PubMed Web of Science ®Google Scholar
• Jagetia, A., Jagetia, Gc., and Jha, S., 2007. Naringin, a grapefruit flavanone, protects V79 cells against the bleomycin‐induced genotoxicity and decline in survival. Journal of Applied Toxicology, 27 (2), 122–132.
   PubMed Web of Science ®Google Scholar
• Jeon, S.M., et al., 2001. Antioxidative activity of naringin and lovastatin in high cholesterol-fed rabbits. Life Sciences, 69 (24), 2855.
   PubMed Web of Science ®Google Scholar
• Jeon, S.M., et al., 2002. Comparison of antioxidant effects of naringin and probucol in cholesterol-fed rabbits. Clinica Chimica Acta; International Journal of Clinical Chemistry, 317 (1–2), 181–190.
   PubMed Web of Science ®Google Scholar
• Kabuto, H., Amakawa, M., and Shishibori, T., 2004. Exposure to bisphenol A during embryonic/fetal life and infancy increases oxidative injury and causes underdevelopment of the brain and testis in mice. Life Sciences, 74 (24), 2931–2940.
   PubMed Web of Science ®Google Scholar
• Kang, J.H., Kondo, F., and Katayama, Y., 2006. Human exposure to bisphenol A. Toxicology, 226 (2–3), 79–89.
   PubMed Web of Science ®Google Scholar
• Kazemi, S., et al., 2017. Low dose administration of Bisphenol A induces liver toxicity in adult rats. Biochemical and Biophysical Research Communications, 494 (1–2), 107–112.
   PubMed Web of Science ®Google Scholar
• Kim, J.H., and Hong, Y.C., 2017. Increase of urinary malondialdehyde level by bisphenol A exposure: a longitudinal panel study. Environmental Health, 16, 1–9.
   PubMed Web of Science ®Google Scholar
• Kovacic, P., 2010. How safe is bisphenol A? Fundamentals of toxicity: Metabolism, electron transfer and oxidative stress. Medical Hypotheses, 75 (1), 1–4.
   PubMed Web of Science ®Google Scholar
• Kwatra, M., et al., 2016. Ameliorative effect of naringin against doxorubicin-induced acute cardiac toxicity in rats. Pharmaceutical Biology, 54 (4), 637–647.
   PubMed Web of Science ®Google Scholar
• Lee, S., et al., 2011. Effects of interventions on oxidative stress and inflammation of cardiovascular diseases. World Journal of Cardiology, 3, 18.
   PubMedGoogle Scholar
• Li, H., et al., 2013. Naringin inhibits growth potential of human triple-negative breast cancer cells by targeting β-catenin signaling pathway. Toxicology Letters, 220 (3), 219–228.
   PubMed Web of Science ®Google Scholar
• Li, H., Horke, S., and Förstermann, U., 2014. Vascular oxidative stress, nitric oxide and atherosclerosis. Atherosclerosis, 237 (1), 208–219.
   PubMed Web of Science ®Google Scholar
• Lind, P.M., and Lind, L., 2011. Circulating levels of bisphenol A and phthalates are related to carotid atherosclerosis in the elderly. Atherosclerosis, 218 (1), 207–213.
   PubMed Web of Science ®Google Scholar
• Marmugi, A., et al., 2012. Low doses of bisphenol A induce gene expression related to lipid synthesis and trigger triglyceride accumulation in adult mouse liver. Hepatology (Baltimore, Md.), 55 (2), 395–407.
   PubMed Web of Science ®Google Scholar
• Martin, K.R., and Appel, C.L., 2010. Polyphenols as dietary supplements: a double-edged sword. Nutrition and Dietary Supplements, 2, 1–12.
   Google Scholar
• Maulik, S.K., and Kumar, S., 2012. Oxidative stress and cardiac hypertrophy: a review. Toxicology Mechanisms and Methods, 22 (5), 359–366.
   PubMed Web of Science ®Google Scholar
• Mei, Y., et al., 2015. Autophagy and oxidative stress in cardiovascular diseases. Biochimica Et Biophysica Acta, 1852 (2), 243–251.
   PubMed Web of Science ®Google Scholar
• Melzer, D., et al., 2010. Association of urinary bisphenol a concentration with heart disease: evidence from NHANES 2003/06. PLoS One, 5 (1), e8673.
   PubMed Web of Science ®Google Scholar
• Melzer, D., et al., 2012. Urinary Bisphenol A concentration and risk of future coronary artery disease in apparently healthy men and women clinical perspective. Circulation, 125 (12), 1482–1490.
   PubMed Web of Science ®Google Scholar
• Mo, L., and Wu, K., 2015. GW26-e4796 Effect of Naringin on myocardial remodeling by regulating the expression of FABP4, FFA in rats with diabetes cardiomyopathy. Journal of the American College of Cardiology, 66 (16), C130.
   Web of Science ®Google Scholar
• Moghaddam, H.S., Samarghandian, S., and Farkhondeh, T., 2015. Effect of bisphenol A on blood glucose, lipid profile and oxidative stress indices in adult male mice. Toxicology Mechanisms and Methods, 25 (7), 507–513.
   PubMed Web of Science ®Google Scholar
• Moriyama, K., et al., 2002. Thyroid hormone action is disrupted by bisphenol A as an antagonist. The Journal of Clinical Endocrinology and Metabolism, 87 (11), 5185–5190.
   PubMed Web of Science ®Google Scholar
• Münzel, T., et al., 2015. Pathophysiological role of oxidative stress in systolic and diastolic heart failure and its therapeutic implications. European Heart Journal, 36 (38), 2555–2564.
   PubMed Web of Science ®Google Scholar
• Niwa, T., et al., 2001. Metabolism and interaction of bisphenol A in human hepatic cytochrome P450 and steroidogenic CYP17. Biological & Pharmaceutical Bulletin, 24 (9), 1064–1067.
   PubMed Web of Science ®Google Scholar
• O’Brien, E., Dolinoy, D.C., and Mancuso, P., 2014. Perinatal bisphenol A exposures increase production of pro-inflammatory mediators in bone marrow-derived mast cells of adult mice. Journal of Immunotoxicology, 11 (3), 205–212.
   PubMed Web of Science ®Google Scholar
• O’Reilly, A.O., et al., 2012. Bisphenol A binds to the local anesthetic receptor site to block the human cardiac sodium channel. PLoS One, 7 (7), e41667.
   PubMed Web of Science ®Google Scholar
• Paglia, D.E., Valentine, W.N., and Dahlgren, J.G., 1975. Effects of low-level lead exposure on pyrimidine 5'-nucleotidase and other erythrocyte enzymes: Possible role of pyrimidine 5'-nucleotidase in the pathogenesis of lead-induced anemia. Journal of Clinical Investigation, 56 (5), 1164–1169.
   PubMed Web of Science ®Google Scholar
• Pant, J., Ranjan, P., and Deshpande, S.B., 2011. Bisphenol A decreases atrial contractility involving NO‐dependent G‐cyclase signaling pathway. Journal of Applied Toxicology, 31 (7), 698–702.
   PubMed Web of Science ®Google Scholar
• Papasani, V.M.R., Hanumantharayappa, B., and Annapurna, A., 2014. Cardioprotective effect of naringin against doxorubicin induced cardiomyopathy in rats. Indo American Journal of Pharmaceutical Research, 4, 2593–2598.
   Google Scholar
• Pari, L., and Amudha, K., 2011. Hepatoprotective role of naringin on nickel-induced toxicity in male Wistar rats. European Journal of Pharmacology, 650 (1), 364–370.
   PubMed Web of Science ®Google Scholar
• Patel, B.B., et al., 2015. Chronic exposure to bisphenol A reduces successful cardiac remodeling after an experimental myocardial infarction in male C57bl/6n mice. Toxicological Sciences, 146 (1), 101–115.
   PubMed Web of Science ®Google Scholar
• Popa, D.S., et al., 2011. Study of oxidative stress induction after exposure to bisphenol A and methylparaben in rats. Farmacia, 59, 539–549.
   Web of Science ®Google Scholar
• Popolo, A., et al., 2013. Oxidative stress in patients with cardiovascular disease and chronic renal failure. Free Radical Research, 47 (5), 346–356.
   PubMed Web of Science ®Google Scholar
• Posnack, N.G., et al., 2015. Physiological response of cardiac tissue to Bisphenol A: Alterations in ventricular pressure and contractility. American Journal of Physiology-Heart and Circulatory Physiology, 309 (2), H267–H275.
   PubMed Web of Science ®Google Scholar
• Ptak, A., and Gregoraszczuk, E.L., 2012. Bisphenol A induces leptin receptor expression, creating more binding sites for leptin, and activates the JAK/Stat, MAPK/ERK and PI3K/Akt signaling pathways in human ovarian cancer cell. Toxicology Letters, 210 (3), 332–337.
   PubMed Web of Science ®Google Scholar
• Ptak, A., et al., 2014. Bisphenol A induce ovarian cancer cell migration via the MAPK and PI3K/Akt signalling pathways. Toxicology Letters, 229 (2), 357–365.
   PubMed Web of Science ®Google Scholar
• Rajadurai, M., and Mainzen Prince, P.S., 2006. Preventive effect of naringin on lipid peroxides and antioxidants in isoproterenol-induced cardiotoxicity in Wistar rats: biochemical and histopathological evidences. Toxicology, 228 (2–3), 259–268.
   PubMed Web of Science ®Google Scholar
• Rajadurai, M., and Mainzen Prince, P.S., 2007. Preventive effect of naringin on cardiac markers, electrocardiographic patterns and lysosomal hydrolases in normal and isoproterenol-induced myocardial infarction in Wistar rats. Toxicology, 230 (2–3), 178–188.
   PubMed Web of Science ®Google Scholar
• Rani, N., et al., 2013. Regulation of heat shock proteins 27 and 70, p-Akt/p-eNOS and MAPKs by Naringin Dampens myocardial injury and dysfunction in vivo after ischemia/reperfusion. PLoS One, 8 (12), e82577.
   PubMed Web of Science ®Google Scholar
• Rodrigo, R., et al., 2013. Oxidative stress-related biomarkers in essential hypertension and ischemia-reperfusion myocardial damage. Disease Markers, 35, 773–790.
   PubMed Web of Science ®Google Scholar
• Savastano, S., et al., 2015. Bisphenol-A plasma levels are related to inflammatory markers, visceral obesity and insulin-resistance: A cross-sectional study on adult male population. Journal of Translational Medicine, 13, 169.
   PubMed Web of Science ®Google Scholar
• Sinha, M., Manna, P., and Sil, P.C., 2008. Arjunolic acid attenuates arsenic-induced nephrotoxicity. Pathophysiology, 15 (3), 147–156.
   PubMedGoogle Scholar
• Sokolovic, D., et al., 2008. Melatonin reduces oxidative stress induced by chronic exposure of microwave radiation from mobile phones in rat brain. Journal of Radiation Research, 49 (6), 579–586.
   PubMed Web of Science ®Google Scholar
• Tarafder, P., et al., 2013. Inhibition of heart ventricular function of rat by bisphenol A through oxidative stress induced injury of ventricular tissue. International Journal of Pharm and Bio Sciences, 4, 811–820.
   Google Scholar
• Thorpe, C., et al., 2002. Sulfhydryl oxidases: Emerging catalysts of protein disulfide bond formation in eukaryotes. Archives Biochemistry Biophysics, 405 (1), 1–12.
   PubMed Web of Science ®Google Scholar
• Tsutsui, H., Kinugawa, S., and Matsushima, S., 2008. Mitochondrial oxidative stress and dysfunction in myocardial remodeling. Cardiovascular Research, 81 (3), 449–456.
   PubMed Web of Science ®Google Scholar
• Valentino, R., et al., 2013. Bisphenol-A impairs insulin action and up-regulates inflammatory pathways in human subcutaneous adipocytes and 3T3-L1 cells. PLoS One, 8 (12), e82099.
   PubMed Web of Science ®Google Scholar
• Vandenberg, L.N., et al., 2007. Human exposure to bisphenol A (BPA). Reproductive Toxicology (Elmsford, N.Y.), 24 (2), 139–177.
   PubMed Web of Science ®Google Scholar
• Vandenberg, L.N., et al., 2010. Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Environmental Health Perspectives, 118 (8), 1055–1070.
   PubMed Web of Science ®Google Scholar
• Wetherill, Y.B., et al., 2007. In vitro molecular mechanisms of bisphenol A action. Reproductive Toxicology, 24 (2), 178–198.
   PubMed Web of Science ®Google Scholar
• Woolliams, J.A., et al., 1983. Variation in the activities of glutathione peroxidase and superoxide dismutase and in the concentration of copper in the blood in various breed crosses of sheep. Research in Veterinary Science, 34, 253–256.
   PubMed Web of Science ®Google Scholar
• Xianchu, L., et al., 2016. Naringin protects against lipopolysaccharide-induced cardiac injuryin mice. Environmental Toxicology and Pharmacology, 48, 1–6.
   PubMed Web of Science ®Google Scholar
• Xu, L.C., et al., 2005. Evaluation of androgen receptor transcriptional activities of bisphenol A, octylphenol and nonylphenol in vitro. Toxicology, 216 (2–3), 197–203.
   PubMed Web of Science ®Google Scholar
• Xulu, S., and Oroma Owira, P.M., 2012. Naringin ameliorates atherogenic dyslipidemia but not hyperglycemia in rats with type 1 diabetes. Journal of Cardiovascular Pharmacology, 59 (2), 133–141.
   PubMed Web of Science ®Google Scholar
• Yan, S., et al., 2011. Bisphenol A and 17β-estradiol promote arrhythmia in the female heart via alteration of calcium handling. PloS One, 6 (9), e25455.
   PubMed Web of Science ®Google Scholar
• Yang, M., et al., 2016. Bisphenol A promotes adiposity and inflammation in a nonmonotonic dose-response way in 5-week-old male and female C57BL/6J mice fed a low-calorie diet. Endocrinology, 157 (6), 2333–2345.
   PubMed Web of Science ®Google Scholar
• Yang, Y.J., et al., 2009. Bisphenol A exposure is associated with oxidative stress and inflammation in postmenopausal women. Environmental Research, 109 (6), 797–801.
   PubMed Web of Science ®Google Scholar
• Yu, Y.S., and Zheng, H., 2012. Chronic hydrogen-rich saline treatment reduces oxidative stress and attenuates left ventricular hypertrophy in spontaneous hypertensive rats. Molecular and Cellular Biochemistry, 365 (1–2), 233–242.
   PubMed Web of Science ®Google Scholar
• Zhu, J., et al., 2015. MAPK and NF-κB pathways are involved in bisphenol A-induced TNF-α and IL-6 production in BV2 microglial cells. Inflammation, 38 (2), 637–648.
   PubMed Web of Science ®Google Scholar
• Zoeller, R.T., et al., 2012. Endocrine-disrupting chemicals and public health protection: A statement of principles from the endocrine society. Endocrinology, 153 (9), 4097–4110.
   PubMed Web of Science ®Google Scholar