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Sex-, tissue-, and exposure duration-dependent effects of imidacloprid modulated by piperonyl butoxide and menadione in rats. Part I: oxidative and neurotoxic potentials


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1. Tomizawa M, Casida JE. Neonicotinoid insecticides: highlights of a symposium on strategic molecular designs. J Agric Food Chem 2011;59:2883-6. doi: 10.1021/jf103856c10.1021/jf103856cSearch in Google Scholar

2. Kovganko NV, Kashkan ZhN. Advances in the synthesis of neonicotinoids. Russ J Org Chem 2004;40:1709-26. doi: 10.1007/s11178-005-0089-y10.1007/s11178-005-0089-ySearch in Google Scholar

3. Tomizawa M, Casida JE. Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu Rev Pharmacol Toxicol 2005;45:247-68. doi: 10.1146/annurev. pharmtox.45.120403.095930Search in Google Scholar

4. EPA. Imidacloprid Summary Document Registration Review: Initial Docket December 2008. EPA-HQ-OPP-2008-0844 [displayed 7 July 2014]. Available at http://agri-pulse.com/uploaded/EPA_2008_Imidacloprid.pdfSearch in Google Scholar

5. Tomizawa M, Casida JE. Selective toxicity of neonicotinoids attributable to specificity of insect and mammalian nicotinic receptors. Annu Rev Entomol 2003;48:339-64. doi: 10.1146/ annurev.ento.48.091801.11273110.1146/annurev.ento.48.091801.112731Search in Google Scholar

6. Chao SL, Casida JE. Interaction of imidacloprid metabolites and analogs with the nicotinic acetylcholine receptor of mouse brain in relation to toxicity. Pestic Biochem Physiol 1997;58:77-88. doi: 10.1006/pest.1997.228410.1006/pest.1997.2284Search in Google Scholar

7. Tomizawa M, Casida JE. Imidacloprid, thiacloprid, and their imine derivatives up-regulate the α4β2 nicotinic acetylcholine receptor in M10 cells. Toxicol Appl Pharmacol 2000;169:114-20. doi: 10.1006/taap.2000.905710.1006/taap.2000.9057Search in Google Scholar

8. Honda H, Tomizawa M, Casida JE. Neonicotinoid metabolic activation and inactivation established with coupled nicotinic receptor-CYP3A4 and -aldehyde oxidase systems. Toxicol Lett 2006;161:108-14. doi: 10.1016/j.toxlet.2005.08.00410.1016/j.toxlet.2005.08.004Search in Google Scholar

9. Costa C, Silvari V, Melchini A, Catania S, Heffron JJ, Trovato A, De Pasquale R. Genotoxicity of imidacloprid in relation to metabolic activation and composition of the commercial product. Mutat Res 2009;672:40-4. doi: 10.1016/j. mrgentox.2008.09.018Search in Google Scholar

10. Schulz-Jander DA, Casida JE. Imidacloprid insecticide metabolism: human cytochrome P450 isozymes differ in selectivity for imidazolidine oxidation versus nitroimine reduction. Toxicol Lett 2002;132:65-70. PMID: 1208462110.1016/S0378-4274(02)00068-1Search in Google Scholar

11. Dick RA, Kanne DB, Casida JE. Identification of aldehyde oxidase as the neonicotinoid nitroreductase. Chem Res Toxicol 2005;18:317-23. PMID: 1572013810.1021/tx049737i15720138Search in Google Scholar

12. Capowiez Y, Rault M, Mazzia C, Belzunces L. Earthworm behaviour as a biomarker - a case study using imidacloprid. Pedobiologia 2003;47:542-7. doi: 10.1078/0031-4056-0022610.1078/0031-4056-00226Search in Google Scholar

13. Abou-Donia MB, Goldstein LB, Bullman S, Tu T, Khan WA, Dechkovskaia AM, Abdel-Rahman AA. 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. J Toxicol Environ Health Part A 2008;71:119-30. doi: 10.1080/1528739070161314010.1080/1528739070161314018080902Search in Google Scholar

14. Bhardwaj S, Srivastava MK, Kapoor U, Srivastava LP. A 90 days oral toxicity of imidacloprid in female rats: Morphological, biochemical and histopathological evaluations. Food Chem Toxicol 2010;48:1185-90. doi: 10.1016/j.fct.2010.02.00910.1016/j.fct.2010.02.00920146932Search in Google Scholar

15. Dondero F, Negri A, Boatti L, Marsano F, Mignone F, Viarengo A. Transcriptomic and proteomic effects of a neonicotinoid insecticide mixture in the marine mussel (Mytilus galloprovincialis, Lam.). Sci Total Environ 2010;408:3775-86. doi: 10.1016/j.scitotenv.2010.03.04010.1016/j.scitotenv.2010.03.04020417955Search in Google Scholar

16. Duzguner V, Erdogan S. Acute oxidant and inflammatory effects of imidacloprid on the mammalian central nervous system and liver in rats. Pestic Biochem Physiol 2010;97:13-8. doi: 10.1016/j.pestbp.2009.11.00810.1016/j.pestbp.2009.11.008Search in Google Scholar

17. El-Gendy KS, Aly NM, Mahmoud FH, Kenawy A, El-Sebae AH. The role of vitamin C as antioxidant in protection of oxidative stress induced by imidacloprid. Food Chem Toxicol 2010;48:215-21. doi: 10.1016/j.fct.2009.10.00310.1016/j.fct.2009.10.00319833166Search in Google Scholar

18. Kapoor U, Srivastava MK, Bhardwaj S, Srivastava LP. Effect of imidacloprid on antioxidant enzymes lipid peroxidation in female rats to derive its No Observed Effect Level (NOEL). J Toxicol Sci 2010;35:577-81. PMID: 2068634510.2131/jts.35.57720686345Search in Google Scholar

19. Kapoor U, Srivastava MK, Srivastava LP. Toxicological impact of technical imidacloprid on ovarian morphology, hormones and antioxidant enzymes in female rats. Food Chem Toxicol 2011;49:3086-9. doi: 10.1016/j.fct.2011.09.00910.1016/j.fct.2011.09.00921946071Search in Google Scholar

20. Nebbia C. Biotransformation enzymes as determinants of xenobiotic toxicity in domestic animals. Vet J 2001;161:238-52. doi: 10.1053/tvjl.2000.056110.1053/tvjl.2000.056111352482Search in Google Scholar

21. Ghanayem BI, Hoffler U. Investigation of xenobiotics metabolism, genotoxicity, and carcinogenicity using cyp2e1-/- mice. Curr Drug Metab 2007;8:728-49. PMID: 1797966110.2174/13892000778210976017979661Search in Google Scholar

22. Sivori JL, Casabé N, Zerba EN, Wood EJ. Induction of glutathione S-transferase activity in Triatoma infestans. Mem Inst Oswaldo Cruz 1997;92:797-802. PMID: 956621210.1590/S0074-02761997000600013Search in Google Scholar

23. Bingham G, Strode C, Tran L, Khoa PT, Jamet HP. Can piperonyl butoxide enhance the efficacy of pyrethroids against pyrethroid-resistant Aedes aegypti? Trop Med Int Health 2011;16:492-500. doi: 10.1111/j.1365-3156.2010. 02717.xSearch in Google Scholar

24. Urek SY, Baydan E, Yurdakök B, Akaydin Y, Kozlu T, Tunca A. Subacute toxicity of piperonyl butoxide and resmethrin in mice. Afr J Pharm Pharmacol 2012;6:2083-7. doi: 10.5897/ AJPP12.851Search in Google Scholar

25. Abe K, Saito H. Menadione toxicity in cultured rat cortical astrocytes. Jpn J Pharmacol 1996;72:299-306. doi: 10.1254/ jjp.72.29910.1254/jjp.72.2999015738Search in Google Scholar

26. Chung JH, Seo DC, Chung SH, Lee JY, Seung SA. Metabolism and cytotoxicity of menadione and its metabolite in rat platelets. Toxicol Appl Pharmacol 1997;142:378-85. PMID: 907036110.1006/taap.1996.8048Search in Google Scholar

27. Cui D, Rankin G, Harvison PJ. Transamination in the metabolism of the nephrotoxicant n-(3,5-dichlorophenyl) succinimide in rats. Drug Metab Dispos 2005;33:1765-70. doi: 10.1124/dmd.105.00659310.1124/dmd.105.006593Search in Google Scholar

28. Kerver ED, Vogels IMC, Bosch KS, Vreeling-Sindelarova H, Van Den Munckhof RJM, Frederiks WM. In situ detection of spontaneous superoxide anion and singlet oxygen production by mitochondria in rat liver and small intestine. Histochem J 1997;29:229-37. PMID: 9472385Search in Google Scholar

29. Al-Omar MA, Al-Arifi MN. Comparative effects of scopoletin and menadione on aldehyde oxidase activity of guinea pig liver. J Biol Sci 2005;5:525-31. doi: 10.3923/ jbs.2005.525.53110.3923/jbs.2005.525.531Search in Google Scholar

30. Sanmartín-Suárez C, Soto-Otero R, Sánchez-Sellero I, Méndez-Álvarez E. Antioxidant properties of dimethyl sulfoxide and its viability as a solvent in the evaluation of neuroprotective antioxidants. J Pharmacol Toxicol Methods 2011;63:209-15. doi: 10.1016/j.vascn.2010.10.00410.1016/j.vascn.2010.10.004Search in Google Scholar

31. IPCS/INCHEM. Pesticide residues in food. Toxicological evaluations: imidacloprid. 2001. [displayed 7 July 2014]. Available at http://www.inchem.org/documents/jmpr/jmpmono/2001pr07.htmSearch in Google Scholar

32. Anderson ME. Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol 1985;113:548-55. PMID: 408807410.1016/S0076-6879(85)13073-9Search in Google Scholar

33. Beutler E. Red Cell Metabolism: A Manual of Biochemical Methods. 2nd Ed. New York (NY): Grune and Starton; 1984.Search in Google Scholar

34. Habig WH, Pabst MJ, Jakoby WB. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 1974;249:7130-9. PMID:443630010.1016/S0021-9258(19)42083-8Search in Google Scholar

35. Wills ED. Mechanism of lipid peroxide formation in animal tissues. Biochem J 1966; 99:667-76. PMID: 596496310.1042/bj0990667Search in Google Scholar

36. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with Folin-phenol reagent. J Biol Chem 1951;193:265-75. PMID: 1490771310.1016/S0021-9258(19)52451-6Search in Google Scholar

37. Ellman GL, Courtney KD, Andres V, Featherstone RM. A new and rapid colorimetric determination of acetycholinesterase activity. Biochem Pharmacol 1961;7:88-95. doi: 10.1016/0006-2952(61)90145-910.1016/0006-2952(61)90145-9Search in Google Scholar

38. Rankin GO. Kidney. In: Wexler P, editor. Encylopedia of toxicology. 2nd ed. New York (NY): Academic Press; 2005. p. 666-89.10.1016/B0-12-369400-0/00550-0Search in Google Scholar

39. Broznić D, Marinić J, Tota M, Čanadi Jurešić G, Milin C. Kinetic evaluation of imidacloprid degradation in mice organs treated with olive oil polyphenols extract. Croat Chem Acta 2008;81:203-9.Search in Google Scholar

40. EMEA. European Medicines Agency, Scientific Discussion, CVMP/0297/03 2009 [displayed 7 July 2014]. Available at http://www.ema.europa.eu/docs/en_GB/document_library/EPAR_-_Scientific_Discussion/veterinary/000076/WC500060915.pdfSearch in Google Scholar

41. Yildiz D, Ercal N, Armstrong DW. Nicotine enantiomers and oxidative stress. Toxicology 1998;130:155-65. doi: 10.1016/ S0300-483X(98)00105-X10.1016/S0300-483X(98)00105-XSearch in Google Scholar

42. Kyerematen GA, Owens GF, Chattopadhyay B, de Bethizy JD, Vesell ES. Sexual dimorphism of nicotine metabolism and distribution in the rat, studies in vivo and in vitro. Drug Metab Dispos 1988;16:823-8. PMID: 2907460Search in Google Scholar

43. Kammerer B, Scheible H, Albrecht W, Gleiter CH, Laufer S. Pharmacokinetics of ML3403 ({4-[5-(4-fluorophenyl)-2- methylsulfanyl-3H-imidazol-4-yl]-pyridin-2-yl}-(1- phenylethyl)-amine), a 4-Pyridinylimidazole-type p38 mitogen-activated protein kinase inhibitor. Drug Metab Dispos 2007;35:875-83. doi: 10.1124/dmd.106.01340910.1124/dmd.106.013409Search in Google Scholar

44. Sundseth SS, Waxman DJ. Sex-dependent expression and clofibrate inducibility of cytochrome P450 4A fatty acid a-hydroxylases. J Biol Chem 1992;267:3915-21. PMID: 174043910.1016/S0021-9258(19)50613-5Search in Google Scholar

45. Kundu TK, Velayutham M, Zweier JL. Aldehyde oxidase functions as a superoxide generating NADH oxidase: an important redox regulated pathway of cellular oxygen radical formation. Biochemistry 2012;51:2930-9. doi: 10.1021/ bi300087910.1021/bi3000879Search in Google Scholar

46. Huh K, Shin US, Choi JW, Lee SI. Effect of sex hormones on lipid peroxidation in rat liver. Arch Pharm Res 1994;17:109-14. PMID: 1031914110.1007/BF02974233Search in Google Scholar

47. Ventura SM, Dachtler SL. Effects of sex hormones on hepatic aldehyde oxidase activity in C57BL/6J mice. Horm Res 1981;14:250-9. PMID: 730898210.1159/000179395Search in Google Scholar

48. Kimura-Kuroda J, Komuta Y, Kuroda Y, Hayashi M, Kawano H. Nicotine-like effects of the neonicotinoid insecticides acetamiprid and imidacloprid on cerebellar neurons from neonatal rats. PLoS One 2012;7:e32432. doi: 10.1371/ journal.pone.003243210.1371/journal.pone.0032432Search in Google Scholar

49. Yeboah MM, Xue X, Javdan M, Susin M, Metz CN. Nicotinic acetylcholine receptor expression and regulation in the rat kidney after ischemia-reperfusion injury. Am J Physiol Renal Physiol 2008;295:654-61. doi: 10.1152/ajprenal.90255.200810.1152/ajprenal.90255.2008Search in Google Scholar

50. Bond CE, Patel P, Crouch L, Tetlow N, Day T, Abu-Hayyeh S, Williamson C, Greenfield SA. Astroglia up-regulate transcription and secretion of ‘readthrough’ acetylcholinesterase following oxidative stress. Eur J Neurosci 2006;24:381-6. PMID: 1690384810.1111/j.1460-9568.2006.04898.xSearch in Google Scholar

51. Yang ZP, Morrow J, Wu A, Roberts LJ, Dettbarn WD. Diisopropylphosphofluoridate-induced muscle hyperactivity associated with enhanced lipid peroxidation in vivo. Biochem Pharmacol 1996;52:357-61. PMID: 869486110.1016/0006-2952(96)00214-6Search in Google Scholar

52. García-Ayllón MS, Silveyra MX, Candela A, Compañ A, Clària J, Jover R, Pérez-Mateo M, Felipo V, Martínez S, Galcerán J, Sáez-Valero J. Changes in liver and plasma acetylcholinesterase in rats with cirrhosis induced by bile duct ligation. Hepatology 2006;43:444-53. PMID: 1649634910.1002/hep.21071Search in Google Scholar

53. Hazarika A, Sarkar SN. Subacute toxicity of anilofos, a new organophosphorus herbicide, in male rats: Effect on some physical attributes and acetylcholinesterase activity. Indian J Exp Biol 2001;39:1107-12. PMID: 11906102Search in Google Scholar

54. Borges HE, Martins ACP, Mathias PCF, Esteves RZ. Atividade colinesterásica em tireóide de ratos: resposta a uma sobrecarga de iodo [Cholinesterase activity in rat thyroid in response to iodine overload, in Portuguese]. Arq Bras Endocrinol Metab 2000;44:347-51.10.1590/S0004-27302000000400011Search in Google Scholar

55. Berninsone P, Katz E, Napp M, Azcurra J. Acetylcholinesterase and nonspecific cholinesterase activities in rat liver: subcellular localization, molecular forms, and some extraction properties. Biochem Cell Biol 1989;67:817-22. doi: 10.1139/o89-121 10.1139/o89-121Search in Google Scholar

56. Shih T-M. Comparison of several oximes on reactivation of soman-inhibited blood, brain and tissue cholinesterase activity in rats. Arch Toxicol 1993;67:637-46. doi: 10.1007/ BF0197407110.1007/BF01974071Search in Google Scholar

57. Kaur B, Khera A, Sandhir R. Attenuation of cellular antioxidant defense mechanisms in kidney of rats intoxicated with carbofuran. J Biochem Mol Toxicol 2012;26:393-8. doi: 10.1002/jbt.2143310.1002/jbt.21433Search in Google Scholar

58. Iwata H, Inoue A, Tomoi M. Enhancement of brain thiamine diphosphatase activity of rats by injection of cholinergıc drugs. J Neurochem 1971;18:1371-7. doi: 10.1111/j.1471-4159.1971.tb00001.x10.1111/j.1471-4159.1971.tb00001.xSearch in Google Scholar

59. Obregon ADC, Schetinger MRC, Correa MM, Morsch VM, da Silva JEP, Martins MAP, Bonacorso HG, Zanatta N. Effects per se of organic solvents in the cerebral acetylcholinesterase of rats. Neurochem Res 2005;30:379-84. doi: 10.1007/s11064-005-2612-510.1007/s11064-005-2612-5Search in Google Scholar

60. Carr RL, Nail CA. Effect of different administration paradigms on cholinesterase inhibition following repeated chlorpyrifos exposure in late preweanling rats. Toxicol Sci 2008;106:186-92. doi: 10.1093/toxsci/kfn16410.1093/toxsci/kfn164Search in Google Scholar

61. Debnath D, Mandal TK. Study of quinalphos (an environmental oestrogenic insecticide) formulation (Ekalux 25 E.C.)-induced damage of the testicular tissues and antioxidant defence systems in Sprague-Dawley albino rats. J Appl Toxicol 2000;20:197-204. PMID: 1079747210.1002/(SICI)1099-1263(200005/06)20:3<197::AID-JAT634>3.0.CO;2-7Search in Google Scholar

62. Cnubben NHP, Rietjens IMCM, Wortelboer H, Zanden JV, van Bladeren PJ. The interplay of glutathione-related processes in antioxidant defense. Environ Toxicol Pharmacol 2001;10:141-52. PMID: 2178257010.1016/S1382-6689(01)00077-1Search in Google Scholar

63. Butera L, Fenfeld DA, Bhargava M. Sex differences in the subunits of glutathione-S-transferase isoenzyme from rat and human kidney. Enzyme 1990;43:175-82. PMID: 210179710.1159/000468728Search in Google Scholar

64. Valentovic MA, Lo HH, Brown PI, Rankin GO. 3,5-Dichloroaniline toxicity in Fischer 344 rats pretreated with inhibitors and inducers of cytochrome P450. Toxicol Lett 1995;78:207-14. PMID: 762489110.1016/0378-4274(95)03249-KSearch in Google Scholar

65. Baliga R, Zhang Z, Shah SV. Role of cytochrome P-450 in hydrogen peroxide-induced cytotoxicity to LLC-PK1 cells. Kidney Int 1996;50:1118-24. doi: 10.1038/ki.1996.41810.1038/ki.1996.4188887268Search in Google Scholar

66. Muguruma M, Unami A, Kanki M, Kuroiwa Y, Nishimura J, Dewa Y, Umemura T, Oishi Y, Mitsumori K. Possible involvement of oxidative stress in piperonyl butoxide induced hepatocarcinogenesis in rats. Toxicology 2007;236:61-75. PMID: 1749885910.1016/j.tox.2007.03.02517498859Search in Google Scholar

67. Torda C, Wolff HG. Effect of vitamin K (menadione) on choline esterase activity, acetylcholine synthesis, and striated muscle. Exp Biol Med 1944;57:236-9. doi: 10.3181/00379727-57-1476610.3181/00379727-57-14766Search in Google Scholar

68. Kitamura S, Suzuki T, Ohta S, Fujimoto N. Antiandrojenic activity and metabolism of the organophosphorus pesticide fenthion and related compounds. Environ Health Perspect 2003;111:503-8. doi: 10.1289/ehp.591710.1289/ehp.5917124143512676606Search in Google Scholar

69. Sidorova YA, Grishanova AY. Dose- and time-dependent effects of menadione on enzymes of xenobiotics in rat liver. Bull Exp Biol Med 2004;137:231-4. PMID: 15232626 10.1023/B:BEBM.0000031556.47763.04Search in Google Scholar

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