Quercetin ameliorates the hepatic apoptosis of foetal rats induced by in utero exposure to fenitrothion via the transcriptional regulation of paraoxonase-1 and apoptosis-related genes

References

• Abraham, A.G., and O’Neill, E., 2014. PI3K/Akt-mediated regulation of p53 in cancer. Biochemical society transactions, 42 (4), 798–803.
   PubMed Web of Science ®Google Scholar
• Adresi, Y., 2003. Butyrylcholinesterase: structure and physiological importance. Turkish journal of biochemistry, 28 (2), 54–61.
   Google Scholar
• Aebi, H., 1984. [13] Catalase in vitro. Methods in enzymology, 105 (C), 121–126.
   PubMed Web of Science ®Google Scholar
• Al-Attar, A.M., 2011. Vitamin E attenuates liver injury induced by exposure to lead, mercury, cadmium and copper in albino mice. Saudi journal of biological sciences, 18 (4), 395–401.
   PubMed Web of Science ®Google Scholar
• Aldonza, M.B.D., et al., 2017. Paraoxonase-1 (PON1) induces metastatic potential and apoptosis escape via its antioxidative function in lung cancer cells. Oncotarget, 8 (26), 42817–42835.
   PubMedGoogle Scholar
• Ambali, S.F., and Ayo, J.O., 2011. Sensorimotor performance deficits induced by chronic chlorpyrifos exposure in wistar rats: mitigative effect of vitamin C. Toxicological & environmental chemistry, 93 (6), 1212–1226.
   Web of Science ®Google Scholar
• Asrani, S.K., et al., 2019. Burden of liver diseases in the world. Journal of hepatology, 70 (1), 151–171.
   PubMed Web of Science ®Google Scholar
• Banni, M., et al., 2010. Metallothionein gene expression in liver of rats exposed to cadmium and supplemented with zinc and selenium. Archives of environmental contamination and toxicology, 59 (3), 513–519.
   PubMed Web of Science ®Google Scholar
• Bartling, A., et al., 2007. Enzyme-kinetic investigation of different sarin analogues reacting with human acetylcholinesterase and butyrylcholinesterase. Toxicology, 233 (1–3), 166–172.
   PubMed Web of Science ®Google Scholar
• Boots, A.W., Haenen, G.R.M.M., and Bast, A., 2008. Health effects of quercetin: from antioxidant to nutraceutical. European journal of pharmacology, 585 (2–3), 325–337.
   PubMed Web of Science ®Google Scholar
• Bradford, M.M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical biochemistry, 72 (1-2), 248–254.
   PubMed Web of Science ®Google Scholar
• Bradman, A., et al., 2003. Measurement of pesticides and other toxicants in amniotic fluid as a potential biomarker of prenatal exposure: a validation study. Environmental health perspectives, 111 (14), 1779–1782.
   PubMed Web of Science ®Google Scholar
• Braun, J.B.S., et al., 2017. Neuroprotective effects of pretreatment with quercetin as assessed by acetylcholinesterase assay and behavioral testing in poloxamer-407 induced hyperlipidemic rats. Biomedicine & pharmacotherapy, 88, 1054–1063.
   PubMed Web of Science ®Google Scholar
• Bu, T., et al., 2012. Alleviative effect of quercetin on germ cells intoxicated by 3-methyl-4-nitrophenol from diesel exhaust particles. Journal of Zhejiang university. Science. B, 13 (4), 318–326.
   PubMed Web of Science ®Google Scholar
• Cao, D., et al., 2019. Presence and human exposure assessment of organophosphate flame retardants (OPEs) in indoor dust and air in Beijing, China. Ecotoxicology and environmental safety, 169, 383–391.
   PubMed Web of Science ®Google Scholar
• Cao, G., Sofic, E., and Prior, R.L., 1997. Antioxidant and prooxidant behavior of flavonoids: Structure-activity relationships. Free radical biology & medicine, 22 (5), 749–760.
   PubMed Web of Science ®Google Scholar
• Chipuk, J.E., and Green, D.R., 2008. How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? Trends in cell biology, 18 (4), 157–164.
   PubMed Web of Science ®Google Scholar
• Costa, L.G., 2006. Current issues in organophosphate toxicology. Clinica chimica acta, 366 (1–2), 1–13.
   PubMed Web of Science ®Google Scholar
• Cui, Y., Zhao, M., and Han, L., 2020. Differences in biological activities between recombinant human paraoxonase 1 (rhPON1) subtype isozemys R/Q as antidotes against organophosphorus poisonings. Toxicology letters, 325, 51–61.
   PubMed Web of Science ®Google Scholar
• Day, A.J., et al., 2000. Dietary flavonoid and isoflavone glycosides are hydrolysed by the lactase site of lactase phlorizin hydrolase. FEBS letters, 468 (2–3), 166–170.
   PubMed Web of Science ®Google Scholar
• Downie, T., 1990. Theory and practice of histological techniques edited by J.D. Bancroft & A. Stevens, Churchill Livingstone, Edinburgh, 740 pages, £55.00. Histopathology, 17 (4), 386–386.
   Google Scholar
• Draganov, D.I., and La Du, B.N., 2004. Pharmacogenetics of paraoxonases: a brief review. Naunyn-Schmiedeberg’s archives of pharmacology, 369 (1), 78–88.
   PubMed Web of Science ®Google Scholar
• Ellman, G.L., et al., 1961. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical pharmacology, 7 (2), 88–95.
   PubMed Web of Science ®Google Scholar
• Elmore, S., 2007. Apoptosis: a review of programmed cell death. Toxicologic pathology, 35 (4), 495–516.
   PubMed Web of Science ®Google Scholar
• Eraslan, G., et al., 2007. Evaluation of aspect of some oxidative stress parameters using vitamin E, proanthocyanidin and N-acetylcysteine against exposure to cyfluthrin in mice. Pesticide biochemistry and physiology, 88 (1), 43–49.
   Web of Science ®Google Scholar
• Fahmi, A.A., et al., 2018. Flaxseed alleviates toxic effects of some environmental pollutants on pregnant rats and their foetuses. Bioscience research, 15 (3), 1832–1844.
   Web of Science ®Google Scholar
• Fang, P., et al., 2020. Quercetin attenuates d-GaLN-induced L02 cell damage by suppressing oxidative stress and mitochondrial apoptosis via inhibition of HMGB1. Frontiers in pharmacology, 11, 608.
   PubMed Web of Science ®Google Scholar
• Farkhondeh, T., et al., 2020. Oxidative stress and mitochondrial dysfunction in organophosphate pesticide-induced neurotoxicity and its amelioration: a review. Environmental science and pollution research international, 27 (20), 24799–24814.,
   PubMed Web of Science ®Google Scholar
• Ferenczyova, K., Kalocayova, B., and Bartekova, M., 2020. Potential implications of quercetin and its derivatives in cardioprotection. International journal of molecular sciences, 21 (5), 1585.
   Web of Science ®Google Scholar
• Franco, J.L., et al., 2009. Zinc reverses malathion-induced impairment in antioxidant defenses. Toxicology letters, 187 (3), 137–143.
   PubMed Web of Science ®Google Scholar
• Gan, L., and Johnson, J.A., 2014. Oxidative damage and the Nrf2-ARE pathway in neurodegenerative diseases. Biochimica et biophysica acta - molecular basis of disease, 1842 (8), 1208–1218.
   Web of Science ®Google Scholar
• Gao, F.J., et al., 2017. Quercetin declines apoptosis, ameliorates mitochondrial function and improves retinal ganglion cell survival and function in in vivo model of glaucoma in rat and retinal ganglion cell culture in vitro. Frontiers in molecular neuroscience, 10, 285.
   PubMed Web of Science ®Google Scholar
• Garige, M., et al., 2010. Quercetin up-regulates paraoxonase 1 gene expression via sterol regulatory element binding protein 2 that translocates from the endoplasmic reticulum to the nucleus where it specifically interacts with sterol responsive element-like sequence in paraoxonas. Metabolism, 59 (9), 1372–1378.
   PubMed Web of Science ®Google Scholar
• Giordano, G., et al., 2007. Organophosphorus insecticides chlorpyrifos and diazinon and oxidative stress in neuronal cells in a genetic model of glutathione deficiency. Toxicology and applied pharmacology, 219 (2–3), 181–189.
   PubMed Web of Science ®Google Scholar
• Goel, A., Dani, V., and Dhawan, D.K., 2005. Protective effects of zinc on lipid peroxidation, antioxidant enzymes and hepatic histoarchitecture in chlorpyrifos-induced toxicity. Chemico-biological interactions, 156 (2–3), 131–140.
   PubMed Web of Science ®Google Scholar
• Gosselin, E.J., et al., 1986. Immunocytochemistry: its evolution and criteria for its application in the study of epon-embedded cells and tissue. The American journal of anatomy, 175 (2–3), 135–160.
   PubMedGoogle Scholar
• Gouédard, C., Barouki, R., and Morel, Y., 2004. Dietary polyphenols increase paraoxonase 1 gene expression by an aryl hydrocarbon receptor-dependent mechanism. Molecular and cellular biology, 24 (12), 5209–5222.
   PubMed Web of Science ®Google Scholar
• Gultekin, F., Ozturk, M., and Akdogan, M., 2000. The effect of organophosphate insecticide chlorpyrifos-ethyl on lipid peroxidation and antioxidant enzymes (in vitro). Archives of toxicology, 74 (9), 533–538.
   PubMed Web of Science ®Google Scholar
• Guo, Y., and Bruno, R.S., 2015. Endogenous and exogenous mediators of quercetin bioavailability. The journal of nutritional biochemistry, 26 (3), 201–210.
   PubMed Web of Science ®Google Scholar
• Habig, W.H., Pabst, M.J., and Jakoby, W.B., 1974. Glutathione S transferases. The first enzymatic step in mercapturic acid formation. Journal of biological chemistry, 249 (22), 7130–7139.
   PubMed Web of Science ®Google Scholar
• Hafez, M.M., et al., 2014. Association between paraoxonases gene expression and oxidative stress in hepatotoxicity induced by CCl4. Oxidative medicine and cellular longevity, 2014, 893212–893212.
   PubMed Web of Science ®Google Scholar
• Hassani, S., et al., 2018. Alteration of hepatocellular antioxidant gene expression pattern and biomarkers of Oxidative damage in Diazinon-induced acute toxicity in wistar rat: A time-course mechanistic study. EXCLI journal, 17, 57–71.
   PubMed Web of Science ®Google Scholar
• Huxley, R.R., and Neil, H.A.W., 2003. The relation between dietary flavonol intake and coronary heart disease mortality: A meta-analysis of prospective cohort studies. European journal of clinical nutrition, 57 (8), 904–908.
   PubMed Web of Science ®Google Scholar
• Hwang, M.K., et al., 2009. Activation of phosphatidylinositol 3-kinase is required for tumor necrosis factor-alpha-induced upregulation of matrix metalloproteinase-9: its direct inhibition by quercetin. The international journal of biochemistry & cell biology, 41 (7), 1592–1600.
   PubMed Web of Science ®Google Scholar
• Ibrahim, K.A., et al., 2020a. Modulation of paraoxonase-1 and apoptotic gene expression involves in the cardioprotective role of flaxseed following gestational exposure to diesel exhaust particles and/or fenitrothion insecticide. Cardiovascular toxicology, 20 (6), 604–617.
   PubMed Web of Science ®Google Scholar
• Ibrahim, K.A., et al., 2020b. Quercetin attenuates the oxidative injury–mediated upregulation of apoptotic gene expression and catecholaminergic neurotransmitters of the fetal rats’ brain following prenatal exposure to fenitrothion insecticide. Neurotoxicity research, 37 (4), 871–882.
   PubMed Web of Science ®Google Scholar
• Ibrahim, K.A., et al., 2019. Propolis relieves the cardiotoxicity of chlorpyrifos in diabetic rats via alleviations of paraoxonase-1 and xanthine oxidase genes expression. Pesticide biochemistry and physiology, 159, 127–135.
   PubMed Web of Science ®Google Scholar
• John, P.J., and Prakash, A., 2003. Bioaccumulation of pesticides on some organs of freshwater catfish Mystus vittatus. Bulletin of environmental contamination and toxicology, 70 (5), 1013–1016.
   PubMed Web of Science ®Google Scholar
• Julvez, J., and Grandjean, P., 2009. Neurodevelopmental toxicity risks due to occupational exposure to industrial chemicals during pregnancy. Industrial health, 47 (5), 459–468.
   PubMed Web of Science ®Google Scholar
• Karampour, N.S., et al., 2014. Quercetin preventive effects on theophylline-induced anomalies in rat embryo. Jundishapur journal of natural pharmaceutical products, 9 (3), e17834.
   PubMedGoogle Scholar
• Kawai, Y., et al., 2008. Macrophage as a target of quercetin glucuronides in human atherosclerotic arteries: Implication in the anti-atherosclerotic mechanism of dietary flavonoids. The journal of biological chemistry, 283 (14), 9424–9434.
   PubMed Web of Science ®Google Scholar
• Klotz, L.O., and Sies, H., 2003. Defenses against peroxynitrite: selenocompounds and flavonoids. Toxicology letters, 140–141, 125–132.
   PubMed Web of Science ®Google Scholar
• Kono, Y., and Fridovich, I., 1982. Superoxide radical inhibits catalase. Journal of biological chemistry, 257 (10), 5751–5754.
   PubMed Web of Science ®Google Scholar
• Koren-Gluzer, M., Aviram, M., and Hayek, T., 2013. Paraoxonase1 (PON1) reduces insulin resistance in mice fed a high-fat diet, and promotes GLUT4 overexpression in myocytes, via the IRS-1/Akt pathway. Atherosclerosis, 229 (1), 71–78.
   PubMed Web of Science ®Google Scholar
• Krynetskiy, E., 2006. Role of HMGB1 nuclear protein in enhancement of apoptosis by chemotherapeutic agents. Cancer research, 66 (8 Supplement), 1163.
   Web of Science ®Google Scholar
• Lavoie, J.C., and Chessex, P., 1997. Gender and maturation affect glutathione status in human neonatal tissues. Free radical biology & medicine, 23 (4), 648–657.
   PubMed Web of Science ®Google Scholar
• Lee, J.Y., Hwang, W.I., and Lim, S.T., 2004. Antioxidant and anticancer activities of organic extracts from Platycodon grandiflorum A. de Candolle roots. Journal of ethnopharmacology, 93 (2-3), 409–415.
   PubMed Web of Science ®Google Scholar
• Lozano-Paniagua, D., et al., 2016. Activity and determinants of cholinesterases and paraoxonase-1 in blood of workers exposed to non-cholinesterase inhibiting pesticides. Chemico-biological interactions, 259, 160–167.
   PubMed Web of Science ®Google Scholar
• Lu, X.L., et al., 2017. Quercetin attenuates high fructose feeding-induced atherosclerosis by suppressing inflammation and apoptosis via ROS-regulated PI3K/AKT signaling pathway. Biomedicine & pharmacotherapy = biomedecine & pharmacotherapie, 85, 658–671.
   PubMed Web of Science ®Google Scholar
• Lukaszewicz-Hussain, A., 2010. Role of oxidative stress in organophosphate insecticide toxicity - Short review. Pesticide biochemistry and physiology, 98 (2), 145–150.
   Web of Science ®Google Scholar
• Marklund, S., and Marklund, G., 1974. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. European journal of biochemistry, 47 (3), 469–474.
   PubMedGoogle Scholar
• Medina-Díaz, I.M., et al., 2017. Downregulation of human paraoxonase 1 (PON1) by organophosphate pesticides in HepG2 cells. Environmental toxicology, 32 (2), 490–500.
   PubMed Web of Science ®Google Scholar
• Mehta, A., Verma, R.S., and Srivastava, N., 2009. Chlorpyrifos induced alterations in the levels of hydrogen peroxide, nitrate and nitrite in rat brain and liver. Pesticide biochemistry and physiology, 94 (2-3), 55–59.
   Web of Science ®Google Scholar
• Meng, Y., et al., 2017. Role of the PI3K/AKT signalling pathway in apoptotic cell death in the cerebral cortex of streptozotocin-induced diabetic rats. Experimental and therapeutic medicine, 13 (5), 2417–2422.
   PubMed Web of Science ®Google Scholar
• Milošević, M.D., et al., 2018. Role of selenium and vitamin C in mitigating oxidative stress induced by fenitrothion in rat liver. Biomedicine & pharmacotherapy = biomedecine & pharmacotherapie, 106, 232–238.
   PubMed Web of Science ®Google Scholar
• Mosialou, E., et al., 1993. Evidence that rat liver microsomal glutathione transferase is responsible for glutathione-dependent protection against lipid peroxidation. Biochemical pharmacology, 45 (8), 1645–1651.
   PubMed Web of Science ®Google Scholar
• Mossa, A.T.H., Refaie, A.A., and Ramadan, A., 2011. Effect of exposure to mixture of four organophosphate insecticides at no observed adverse effect level dose on rat liver: the protective role of vitamin C. Research journal of environmental toxicology, 5 (6), 323–335.
   Google Scholar
• Myhrstad, M.C.W., et al., 2002. Flavonoids increase the intracellular glutathione level by transactivation of the γ-glutamylcysteine synthetase catalytical subunit promoter. Free radical biology & medicine, 32 (5), 386–393.
   PubMed Web of Science ®Google Scholar
• Noori, S., et al., 2009. Reduction of carbon tetrachloride-induced rat liver injury by coffee and green tea. Pakistan journal of nutrition, 8 (4), 452–458.
   Google Scholar
• Nordberg, J., and Arnér, E.S.J., 2001. Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free radical biology and medicine, 31 (11), 1287–1312.
   Google Scholar
• Nowotny, K., et al., 2015. Advanced glycation end products and oxidative stress in type 2 diabetes mellitus. Biomolecules, 5 (1), 194–222.
   PubMed Web of Science ®Google Scholar
• Oršolić, N., et al., 2004. Immunomodulatory and antimetastatic action of propolis and related polyphenolic compounds. Journal of ethnopharmacology, 94 (2–3), 307–315.
   PubMed Web of Science ®Google Scholar
• Poet, T.S., et al., 2003. In vitro rat hepatic and intestinal metabolism of the organophosphate pesticides chlorpyrifos and diazinon. Toxicological sciences: an official journal of the society of toxicology, 72 (2), 193–200.
   PubMed Web of Science ®Google Scholar
• Reznick, A.Z., and Packer, L., 1994. Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods in enzymology, 233 (C), 357–363.
   PubMed Web of Science ®Google Scholar
• Ridnour, L.A., et al., 2000. A spectrophotometric method for the direct detection and quantitation of nitric oxide, nitrite, and nitrate in cell culture media. Analytical biochemistry, 281 (2), 223–229.
   PubMed Web of Science ®Google Scholar
• Saquib, Q., et al., 2012. Phorate-induced oxidative stress, DNA damage and transcriptional activation of p53 and caspase genes in male Wistar rats. Toxicology and applied pharmacology, 259 (1), 54–65.
   PubMed Web of Science ®Google Scholar
• Saraei, F., et al., 2016. Study of the effects of Diazinon on fetal liver in BALB/c mice. Iranian red crescent medical journal, 18 (4), 28076.
   PubMed Web of Science ®Google Scholar
• Sedlak, J., and Lindsay, R.H., 1968. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Analytical biochemistry, 25 (1), 192–205.
   PubMed Web of Science ®Google Scholar
• Selmi, S., et al., 2018. Malathion, an organophosphate insecticide, provokes metabolic, histopathologic and molecular disorders in liver and kidney in prepubertal male mice. Toxicology reports, 5, 189–195.
   PubMed Web of Science ®Google Scholar
• Sharmila, G., et al., 2014. Chemopreventive effect of quercetin, a natural dietary flavonoid on prostate cancer in in vivo model. Clinical nutrition (Edinburgh, Scotland), 33 (4), 718–726.
   PubMed Web of Science ®Google Scholar
• Struve, M.F., Turner, K.J., and Dorman, D.C., 2007. Preliminary investigation of changes in the sexually dimorphic nucleus of the rat medial preoptic area following prenatal exposure to fenitrothion. Journal of applied toxicology: JAT, 27 (6), 631–636.
   PubMed Web of Science ®Google Scholar
• Verma, R.S., Mehta, A., and Srivastava, N., 2007. In vivo chlorpyrifos induced oxidative stress: Attenuation by antioxidant vitamins. Pesticide biochemistry and physiology, 88 (2), 191–196.
   Web of Science ®Google Scholar
• Wang, B., et al., 2017. Involvement of xanthine oxidase and paraoxonase 1 in the process of oxidative stress in nonalcoholic fatty liver disease. Molecular medicine reports, 15 (1), 387–395.
   PubMed Web of Science ®Google Scholar
• Wills, E.D., 1966. Mechanisms of lipid peroxide formation in animal tissues. The biochemical journal, 99 (3), 667–676.
   PubMed Web of Science ®Google Scholar
• Xu, D., et al., 2019. Antioxidant activities of quercetin and its complexes for medicinal application. Molecules, 24 (6), 1123.
   PubMed Web of Science ®Google Scholar
• Yin, H., Xu, L., and Porter, N.A., 2011. Free radical lipid peroxidation: mechanisms and analysis. Chemical reviews, 111 (10), 5944–5972.
   PubMed Web of Science ®Google Scholar
• Yuan, J.S., et al., 2006. Statistical analysis of real-time PCR data. BMC bioinformatics, 7 (1), 85.
   PubMed Web of Science ®Google Scholar