Imidacloprid affects rat liver mitochondrial bioenergetics by inhibiting F_oF₁-ATP synthase activity

References

• Abou-Donia, M. B., L. B. Goldstein, S. Bullman, T. Tu, W. A. Khan, A. M. Dechkovskaia, and A. A. Abdel-Rahman. 2008. Imidacloprid induces neurobehavioral deficits and increases expression of glial fibrillary acidic protein in the motor cortex and hippocampus in offspring rats following in utero exposure. Journal Toxicogical Environment Health A 71:119–130.
   PubMed Web of Science ®Google Scholar
• Agarwal, R., and R. Srinivas. 2007. Severe neuropsychiatric manifestations and rhabdomyolysis in a patient with imidacloprid poisoning. American Journal of Emergency Medicine 25:844–845.
   PubMed Web of Science ®Google Scholar
• Arfat, Y., N. Mahmood, M. U. Tahir, M. Rashid, S. Anjum, F. Zhao, D. Li, Y. Sun, L. Hu, C. Zhihao, C. Yin, P. Shang, and A. R. Qian. 2014. Effect of imidacloprid on hepatotoxicity and nephrotoxicity in male albino mice. Toxicogical Reports 1:554–561.
   PubMedGoogle Scholar
• Bal, R., S. Erdogan, G. Theophilidis, G. Baydas, and M. Naziroglu. 2010. Assessing the effects of the neonicotinoid insecticide imidacloprid in the cholinergic synapses of the stellate cells of the mouse cochlear nucleus using whole-cell patch-clamp recording. Neurotoxicology 31:113–120.
   PubMed Web of Science ®Google Scholar
• Bal, R., M. Naziroglu, G. Turk, O. Yilmaz, T. Kuloglu, E. Etem, and G. Baydas. 2012a. Insecticide imidacloprid induces morphological and DNA damage through oxidative toxicity on the reproductive organs of developing male rats. Cell Biochemistry and Function 30:492–499.
   PubMed Web of Science ®Google Scholar
• Bal, R., G. Turk, M. Tuzcu, O. Yilmaz, T. Kuloglu, R. Gundogdu, S. Gur, A. Agca, M. Ulas, Z. Cambay, Z. Tuzcu, H. Gencoglu, M. Guvenc, A. D. Ozsahin, N. Kocaman, A. Aslan, and E. Etem. 2012b. Assessment of imidacloprid toxicity on reproductive organ system of adult male rats. Journal Environment Sciences Health B: Pest Food Contamination Agricultural Wastes 47:434–444.
   PubMed Web of Science ®Google Scholar
• Bayer. 2018. Avenge. Accessed January 3, 2018. https://bayer.com.au/en/bayerrsquos-products/product-details.php?l1=Bayer+HealthCare&aktion=details&id=676&l1=&l2=Animal%20Health.
   Google Scholar
• Bracht, A., E. L. Ishii-Iwamoto, and C. L. Salgueiro-Pagadigorria. 2003. Estudo do metabolismo energético em mitocôndrias isoladas de tecido animal. In Métodos de Laboratório em Bioquímica, eds. A. Bracht and E. L. Ishii-Iwamoto, 227–247. Barueri, SP: Manole.
   Google Scholar
• Bridges, H. R., A. J. Y. Jones, M. N. Pollak, and J. Hirst. 2014. Effects of metformin and other biguanides on oxidative phosphorylation in mitochondria. Biochemical Journal 462:475–487.
   PubMed Web of Science ®Google Scholar
• Cain, K., and D. N. Skilleter. 1987. Preparation and use of mitochondria in toxicological research. In Biochemical toxicology, eds. K. Snell and B. Mullock., 217–254. Oxford: IRL Press.
   Google Scholar
• Calumpang, S. M., and M. J. Medina. 1996. Applicator exposure to imidacloprid while spraying mangoes. Bulletin Environment Contamination Toxicogical 57:697–704.
   PubMed Web of Science ®Google Scholar
• Chance, B., and G. R. Williams. 1955. The respiratory chain and oxidative phosphorylation. Advancement Enzymology 17:65–134.
   Google Scholar
• Cochran, R. C., and J. H. Ross. 2017. A method for quantitative risk appraisal for pesticide risk assessments. Journal Toxicogical Environment Health A 80:1–17.
   PubMed Web of Science ®Google Scholar
• Danielson, P. B. 2002. The cytochrome P450 superfamily: Biochemistry, evolution and drug metabolism in humans. Current Drug Metabolism 3:561–597.
   PubMed Web of Science ®Google Scholar
• David, D., I. A. George, and J. V. Peter. 2007. Toxicology of the newer neonicotinoid insecticides: Imidacloprid poisoning in a human. Clinical Toxicology 45:485–486.
   PubMed Web of Science ®Google Scholar
• Demsia, G., D. Vlastos, M. Goumenou, and D. P. Matthopoulos. 2007. Assessment of the genotoxicity of imidacloprid and metalaxyl in cultured human lymphocytes and rat bone-marrow. Mutation Research 634:32–39.
   PubMed Web of Science ®Google Scholar
• Desai, B., and P. Parikh. 2013. Biochemical alterations on exposure of imidacloprid and curzate on fresh water fish Oreochromis mossambicus and Labeo rohita. Indian Journal of Forensic Medicine & Toxicology 7:87–91.
   Google Scholar
• Duzguner, V., and S. Erdogan. 2012. Chronic exposure to imidacloprid induces inflammation and oxidative stress in the liver & central nervous system of rats. Pest Biochemical Physiological 104:58–64.
   Web of Science ®Google Scholar
• Dykens, J. A., J. D. Jamieson, L. D. Marroquin, S. Nadanaciva, J. J. Xu, M. C. Dunn, A. R. Smith, and Y. Will. 2008. In vitro assessment of mitochondrial dysfunction and cytotoxicity of nefazodone, trazodone and buspirone. Toxicological Sciences 103:335–345.
   PubMed Web of Science ®Google Scholar
• Fiske, C. H., and Y. Subbarow. 1925. The colorimetric determination of phosphorus. The Journal of Biological Chemistry 66:375–400.
   Google Scholar
• Fossen, M. 2006. Environmental fate of imidacloprid. Sacramento, CA: Environmental Monitoring Department, California Department of Pesticide Regulation.
   Google Scholar
• Goulson, D. 2013. An overview of the environmental risks posed by neonicotinoid insecticides. Journal Applications Ecology 50:977–987.
   Web of Science ®Google Scholar
• Guillouzo, A. 1998. Liver cell models in in vitro toxicology. Environmental Health Perspectives 106:511–532.
   PubMed Web of Science ®Google Scholar
• Han, W., Y. Tian, and X. Shen. 2018. Human exposure to neonicotinoid insecticides and the evaluation of their potential toxicity: An overview. Chemosphere 192:59–65.
   PubMed Web of Science ®Google Scholar
• Huang, N. C., S. L. Lin, C. H. Chou, Y. M. Hung, H. M. Chung, and S. T. Huang. 2006. Fatal ventricular fibrillation in a patient with acute imidacloprid poisoning. American Journal of Emergency Medicine 24:883–885.
   PubMed Web of Science ®Google Scholar
• Hutchinson, M. J., D. E. Jacobs, and N. Mencke. 2001. Establishment of the cat flea (Ctenocephalides felis) on the ferret (Mustelaputorius furo) and its control with imidacloprid. Medical and Veterinary Entomology 15:212–214.
   PubMed Web of Science ®Google Scholar
• Ioannides, C. 2002. Enzyme systems that metabolise drugs and other Xenobiotics, 1st ed. Baffins Lane, Chichester, West Sussex, UK: John Wiley & Sons.
   Google Scholar
• Iyyadurai, R., I. A. George, and J. V. Peter. 2010. Imidacloprid poisoning–Newer insecticide and fatal toxicity. Journal Medica Toxicogical 6:77–78.
   PubMedGoogle Scholar
• Kammon, A. M., R. S. Brar, H. S. Banga, and S. Sodhi. 2010. Patho-biochemical studies on hepatotoxicity and nephrotoxicity on exposure to chlorpyrifos and imidacloprid in layer chickens. Veterinary Arhiv 80:663–672.
   Web of Science ®Google Scholar
• Kapoor, U., M. K. Srivastava, P. Trivedi, V. Garg, and L. P. Srivastava. 2014. Disposition and acute toxicity of imidacloprid in female rats after single exposure. Food and Chemical Toxicology 68:190–195.
   PubMed Web of Science ®Google Scholar
• Kataria, S. K., A. K. Chhillar, A. Kumar, M. Tomar, and V. Malik. 2016. Cytogenetic and hematological alterations induced by acute oral exposure of imidacloprid in female mice. Drug Chemical Toxicogical 39:59–65.
   PubMed Web of Science ®Google Scholar
• Kaur, B., H. Sandhu, and R. Kaur. 2006. Toxic effects of subacute oral exposure of imidacloprid on biochemical parameters in crossbred cow calves. Toxicogical International 13:43.
   Google Scholar
• Kumar, A., A. Verma, and A. Kumar. 2013. Accidental human poisoning with a neonicotinoid insecticide, imidacloprid: A rare case report from rural India with a brief review of literature. Egyptian Journal Forensic Sciences 3:123–126.
   Google Scholar
• Lemasters, J. J., and C. R. Hackenbrock. 1976. Continuous measurement and rapid kinetics of ATP synthesis in rat liver mitochondria, mitoplasts and inner membrane vesicles determined by firefly-luciferase luminescence. European Journal of Biochemistry 67:1–10.
   PubMedGoogle Scholar
• Li, Y., L. Couch, M. Higuchi, J. L. Fang, and L. Guo. 2012. Mitochondrial dysfunction induced by sertraline, an antidepressant agent. Toxicological Sciences 127:582–591.
   PubMed Web of Science ®Google Scholar
• Lin, P.-C., H.-J. Lin, -Y.-Y. Liao, H.-R. Guo, and K.-T. Chen. 2013. Acute poisoning with neonicotinoid insecticides: A case report and literature review. Basic Clinical Pharmacology Toxicogical 112:282–286.
   PubMed Web of Science ®Google Scholar
• Lonare, M., M. Kumar, S. Raut, P. Badgujar, S. Doltade, and A. Telang. 2014. Evaluation of imidacloprid-induced neurotoxicity in male rats: A protective effect of curcumin. Neurochemistry International 78:122–129.
   PubMed Web of Science ®Google Scholar
• Maioli, M. A., D. E. Lemos, M. Guelfi, H. C. D. Medeiros, F. Riet-Correa, R. M. Medeiros, J. M. Barbosa-Filho, and F. E. Mingatto. 2012. Mechanism for the uncoupling of oxidative phosphorylation by juliprosopine on rat brain mitochondria. Toxicon 60:1355–1362.
   PubMed Web of Science ®Google Scholar
• Meyer, S. A., and A. P. Kulkarni. 2001. Hepatotoxicity. In Introduction to biochemical toxicology, eds. E. Hodgson and R. C. Smart, 487–507. New York, NY: John Wiley & Sons.
   Google Scholar
• Mohamed, F., I. Gawarammana, T. A. Robertson, M. S. Roberts, C. Palangasinghe, S. Zawahir, S. Jayamanne, J. Kandasamy, M. Eddleston, N. A. Buckley, A. H. Dawson, and D. M. Roberts. 2009. Acute human self-poisoning with imidacloprid compound: A neonicotinoid insecticide. PLoS One 4:e5127.
   PubMed Web of Science ®Google Scholar
• Mohany, M., G. Badr, I. Refaat, and M. El-Feki. 2011. Immunological and histological effects of exposure to imidacloprid insecticide in male albino rats. African Journal Pharmaceutical Pharmacology 5:2106–2114.
   Google Scholar
• Nadanaciva, S., J. A. Dykens, A. Bernal, R. A. Capaldi, and Y. Will. 2007. Mitochondrial impairment by PPAR agonists and statins identified via immunocaptured OXPHOS complex activities and respiration. Toxicology and Applied Pharmacology 223:277–287.
   PubMed Web of Science ®Google Scholar
• Nicholls, D. G., and S. J. Ferguson. 2013. Bioenergetics 4. London, UK: Academic Press.
   Google Scholar
• Nicodemo, D., M. A. Maioli, H. C. Medeiros, M. Guelfi, K. V. Balieira, D. de Jong, and F. E. Mingatto. 2014. Fipronil and imidacloprid reduce honeybee mitochondrial activity. Environmental Toxicology and Chemistry 33:2070–2075.
   PubMed Web of Science ®Google Scholar
• O’Brien, T. M., P. J. Oliveira, and K. B. Wallace. 2008. Inhibition of the adenine nucleotide translocator by N-acetyl perfluorooctane sulfonamides in vitro. Toxicology and Applied Pharmacology 227:184–195.
   PubMed Web of Science ®Google Scholar
• Pedersen, P. L., J. W. Greenawalt, B. Reynafarje, J. Hullihen, G. L. Decker, J. W. Soper, and E. Bustamente. 1978. Preparation and characterization of mitochondria and submitochondrial particles of rat liver and liver-derived tissues. Methods in cell biology 20:411–481.
   PubMedGoogle Scholar
• Pospischil, R. 2002. Imidacloprid fly bait – A fast acting formulation against flies in livestock. Proceedings of the 4th International Conference on Urban Pests, July 7–10, 457–458. Charleston, South Carolina, Blacksburg: Pocahontas Press.
   Google Scholar
• Preston, B. L. 2002. Indirect effects in aquatic ecotoxicology: Implications for ecological risk assessment. Environmental Management 29:311–323.
   PubMed Web of Science ®Google Scholar
• Proença, P., H. Teixeira, F. Castanheira, J. Pinheiro, P. V. Monsanto, E. P. Marques, and D. N. Vieira. 2005. Two fatal intoxication cases with imidacloprid: LC/MS analysis. Forensic Science International 153:75–80.
   PubMed Web of Science ®Google Scholar
• Qadir, S., A. Latif, M. Ali, and F. Iqbal. 2014. Effects of imidacloprid on the hematological and serum biochemical profile of Labeo rohita. Pakistan Journal Zoological 46:1085–1090.
   Web of Science ®Google Scholar
• Shadnia, S., and H. H. Moghaddam. 2008. Fatal intoxication with imidacloprid insecticide. American Journal of Emergency Medicine 26:631–634.
   Google Scholar
• Shridhar, N. B. 2010. Toxicity of imidacloprid in buffaloes. Indian Journal Animal Researcher 44:224–225.
   Web of Science ®Google Scholar
• Solomon, K. R., and G. L. Stephenson. 2017. Quantitative weight of evidence assessment of risk to honeybee colonies from use of imidacloprid, clothianidin, and thiamethoxam as seed treatments: A postscript. Journal Toxicogical Environment Health B 20:383–386.
   PubMed Web of Science ®Google Scholar
• Soujanya, S., M. Lakshman, A. A. Kumar, and A. G. Reddy. 2013. Evaluation of the protective role of vitamin C in imidacloprid-induced hepatotoxicity in male albino rats. Journal of Natural Science, Biology and Medicine 4:63–67.
   PubMedGoogle Scholar
• Stephenson, G. L., and K. R. Solomon. 2017. Quantitative weight of evidence assessment of higher-tier studies on the toxicity and risks of neonicotinoids in honeybees. 2. Imidacloprid. Journal Toxicogical Environment Health B 20:330–345.
   PubMed Web of Science ®Google Scholar
• Stivaktakis, P. D., M. P. Kavvalakis, M. N. Tzatzarakis, A. K. Alegakis, M. N. Panagiotakis, P. Fragkiadaki, E. Vakonaki, E. Ozcagli, W. A. Hayes, V. N. Rakitskii, and A. M. Tsatsakis. 2016. Long-term exposure of rabbits to imidaclorpid as quantified in blood induces genotoxic effect. Chemosphere 149:108–113.
   PubMed Web of Science ®Google Scholar
• Tavares, M. A., I. D. F. Palma, H. C. D. Medeiros, M. Guelfi, A. T. Santana, and F. E. Mingatto. 2015. Comparative effects of fipronil and its metabolites sulfone and desulfinyl on the isolated rat liver mitochondria. Environmental Toxicology and Pharmacology 40:206–214.
   PubMed Web of Science ®Google Scholar
• Tomizawa, M., D. L. Lee, and J. E. Casida. 2005. Neonicotinoid insecticide toxicology: Mechanisms of selective action. Annual Review of Pharmacology and Toxicology 45:247–268.
   PubMed Web of Science ®Google Scholar
• Toor, H. K., G. K. Sangha, and K. S. Khera. 2013. Imidacloprid induced histological and biochemical alterations in liver of female albino rats. Pest Biochemical Physical 105:1–4.
   PubMed Web of Science ®Google Scholar
• van der Sluijs, J. P., N. Simon-Delso, D. Goulson, L. Maxim, J. M. Bonmatin, and L. P. Belzunces. 2013. Neonicotinoids, bee disorders and the sustainability of pollinator services. Current Opinion Environment Sustainability 5:293–305.
   Web of Science ®Google Scholar
• Wallace, K. B., and A. A. Starkov. 2000. Mitochondrial targets of drug toxicity. Annual Review of Pharmacology and Toxicology 40:353–388.
   PubMed Web of Science ®Google Scholar
• Wu, I. W., J. L. Lin, and E. T. Cheng. 2001. Acute poisoning with the neonicotinoid insecticide imidacloprid in N-methyl pyrrolidone. Journal of Toxicology. Clinical Toxicology 39:617–621.
   PubMed Web of Science ®Google Scholar
• Zanotti, A., and G. F. Azzone. 1980. Safranine as membrane potential probe in rat liver mitochondria. Archives of Biochemistry and Biophysics 201:255–265.
   PubMed Web of Science ®Google Scholar
• Zheng, J., and V. D. Ramirez. 2000. Inhibition of mitochondrial proton F0F1-ATPase/ATP synthase by polyphenolic phytochemicals. British Journal of Pharmacology 130:1115–1123.
   PubMed Web of Science ®Google Scholar