The effects of fenvalerate on hepatic and cerebral xenobiotic metabolizing enzymes in selenium and/or iodine deficient rats

Document Type : Original Article

Authors

Hacettepe University, Faculty of Pharmacy, Department of Toxicology, Ankara 06100 Turkey

Abstract

Objective(s): Particularly in developing countries, selenium and/or iodine deficiencies are encountered and use of pesticides in agriculture are not well-controlled. Fenvalerate is a pyrethroid insectide used in agriculture and has applications against a wide range of pests. This study was designed to evaluate the effects of fenvalerate on hepatic and cerebral xenobiotic metabolizing enzyme activities in the presence of iodine and/or selenium deficiency on a rat model.
Materials and Methods: Iodine and/or selenium deficiency was induced by feeding  three-week-old Wistar rats with a diet containing <0.005 mg selenium kg-1, and/or administering 1% sodium perchlorate in drinking water for 7 weeks. Test groups received fenvalerate (100 mg kg-1 BW IP) for the last 7 days. Hepatic and cerebral microsomal aniline hydroxylase (CYP2E1) and cytosolic glutathione S-transferase (GST) activities were determined. Besides, hepatic NADPH-cytochrome P450 reductase (P450R), ethoxyresorufin O-deethylase (EROD, CYP1A1/1A2) and penthoxyresorufin O-depenthylase (PROD, CYP2B1/2B2), activities were also measured.
Results: Fenvalerate had a general inductive effect on the hepatic and cerebral xenobiotic metabolizing enzyme activities. Moreover, enzyme activities were also altered by iodine and/or selenium deficiency, but the effects seemed to be enzyme- and tissue-specific.
Conclusion: The inductive effect of fenvalerate, particularly in high dose exposures, may change the metabolism of several xenobiotics, including drugs, as well as endogenous substrates. The effects may vary depending on the selenium and/or iodine status of individual.

Keywords


1.Saillenfait AM, Ndiaye D, Sabaté JP. Pyrethroids: exposure and health effects--an update. Int J Hyg Environ Health 2015; 218:281-292.
2.Casida, JE. Curious about pesticide action. J Agric Food Chem 2011; 59:2762-2769.
3.Kaneko H. Pyrethroids: mammalian metabolism and toxicity. J Agric Food Chem 2011; 59: 2786-2791.
4.Soderlund DM, Clark JM, Sheets LP, Mullin LS, Piccirillo VJ, Sargent D. Mechanism of pyrethroid neurotoxicity: implications for cumulative risk assessment. Toxicology 2002; 171:3-59.
5.Ware GW, editor. The pesticide book. 5th ed. Fresno:Thomson. 2000. p.66-88.
6.Costa LG. The neurotoxicity of organochlorine and pyrethroid pesticides. Handb Clin Neurol 2015; 131:135-148.
7.Narahashi T. Neuronal ion channels as target sites of insecticides. Pharmacol Toxicol 1996; 79:1-14.
8.UN/WHO. Environmental Health Criteria 95, Fenvalerate. Geneva: UN/WHO; 1990.
9.Bradberry SM, Cage SA, Proudfoot AT, Vale JA. Poisoning due to pyrethroids. Toxicol Rev 2005; 24:93-106.
10.Misra S, Sharma CB. Metabolism and bioaccu-mulation of fenvalerate and its metabolites in rat organs. Biomed Chromatogr 1997; 11:50-53.
11.Cabral JRP, Galendo D. Carcinogenecity study of the pesticide fenvalerate in mice. Cancer Lett 1990; 49:13-18.
12.Parker CM, Patterson DR, Van Gelder GA, Gordon EB, Valerio MG, Hall WC. Chronic toxicity and carcinogenecity evaluation of fenvalerate in rats. J Toxicol Environ Health 1984; 13:83-97.
13.Ecobichon JD. The basic science of posions. In: Amdur MO, Doull J, Klassen CD, editors. Casarett and Doull’s Toxicology. New York: Macmillan Publishing Company. 1992. p.565-622.
14.International programme on chemical safety. Environmental health criteria 95, fenvalerate. geneva: World Health Organization. 1990.
15.Giray B, Hıncal F. Fenvalerate induced hepatic oxidative stress in selenium- and/or iodine deficient rats. Hum Exp Toxicol 2011; 30:1575-1583.
16.Arena AC, Fernandez CD, Porto EM, Bissacot DZ, Pereira OC, Kempinas WG. Fenvalerate, a pyrethroid insecticide, adversely affects sperm production and storage in male rats. J Toxicol Environ Health Part A 2008; 71:1550-1558.
17.Balbaa M, Abdelhamid EME, Bassiouny K. Enhancement of lysosomal enzymes by the pyrethroids fenvalerate and trans-cypermethrin. Jpn J Toxicol Environ Health 1998; 44:83-91.
18.Garey J, Wolff MS. Estrogenic and anti-progestagenic activities of pyrethroid insecticides. Biochem Biophys Res Commun 1998; 251:855-859.
19.Hemming H, Flodstrom S, Warngard L. Enhancement of altered hepatic foci in rat liver and inhibition of intercellular communication in vitro by the pyrethroid insecticides fenvalerate, flucythrinate and cypermethrin. Carcinogenesis 1993; 14:2531-2535.
20.Maiti PK, Kar A. Dual role of testosterone in fenvalerate-treated mice with respect to thyroid function and lipid peroxidation. J Appl Toxicol 1997; 17:127-131.
21.Maiti PK, Kar A. Is triiodothyronine capable of ameliorating pyrethroid-induced thyroid dysfunction and lipid peroxidation? J Appl Toxicol 1998; 18:125-128.
22.Catinot R, Hoellinger H, Sonnier M, Do-Cao-Thang, Pichon J, Nguyen-Hoang-Nam. In vitro covalent binding of the pyrethroids cismethrin, cypermethrin and deltamethrin to rat liver homogenate and microsomes. Arch Toxicol 1989; 63:214-220.
23.Heder AF, Hirsch-Ernst KI, Bauer D, Kahl GF, Desel H. Induction of cytochrome P450 2B1 by pyrethroids in primary rat hepatocyte cultures. Biochem Pharmacol 2001; 62:71-79.
24.Dayal M, Parmar D, Ali M, Dhawan A, Dwivedi UN, Seth PK. Induction of rat brain cytochrome P450s (P450s) by deltamethrin: regional specificity and correlation with neurobehavioral toxicity. Neurotox Res 2001; 3:351-357.
25.Ranasinghe C, Hobbs AA. Isolation and characterisation of a cytochrome b5 cDNA clone from Helicoverpa armigera (Hubner): possible involvement of cytochrome b5 in cytochrome P450 CYP6B7 activity towards pyrethroids. Insect Biochem Mol Biol 1999; 29:145-151.
26.Morisseau C, Derbel M, Lane TR, Stoutamire D, Hammock BD. Differential induction of hepatic drug-metabolizing enzymes by fenvaleric acid in male rats. Toxicol Sci 1999; 52:148-153.
27.Riviere JL, Bach J, Grollceau G. Effects of pyrethroid insecticides and N-(3,5-dichlorophenyl)-dicarboximide fungucides on microsomal-drug metabolizing enzymes in the Japanase quail (Coturnix coturnix). Bull Environ Contam Toxicol 1983; 31:479-485.
28.Schomburg L, Köhrle J. On the importance of selenium and iodine metabolism for thyroid hormone biosynthesis and human health. Mol Nutr Food Res 2008; 52:1235-1246.
29.Steinbrenner H, Sies H. Protection against reactive oxygen species by selenoproteins. Biochim Biophys Acta 1790:1478-1485.
30.Giray B, Hıncal F. Selenium status in Turkey-possible link between status of selenium, iodine, antioxidant enzymes and oxidative DNA damage. J Radioanal Nucl Chem 2004; 259:447-451.
31.Giray B, Hıncal F, Teziç T, Ökten A, Gedik Y. Antioxidant enzyme activities and selenium status in various stages of goiter. FABAD J Pharm Sci 2001; 26:13-19.
32.Hıncal F, Giray B. Selenium status in Turkey. In: Hıncal F, Çavdar A, Giray B, editors. Selenium in health and disease. Ankara: Pozitif Matbaacılık. 2006.
33.Yetgin S, Ataçeri N. Selenium status in Turkey. I.Serum selenium levels in infants and children in Ankara. Biol Trace Elem Res 1989; 20:161-167.
34.Hodgson E, Levi PE. Thyroid hormones. In: Hodgson E, Levi PE, editors. Biochemical toxicology.  Norwalk, Connecticut: Appleton & Lange. 1994.  p. 139.
35.Raheja KL, Linscheer WG, Chijiiwa K, Iba M. Inhibitory effect of propylthiouracil-induced hypothyroidism in rat on oxidative drug metabolism. Comp Biochem Physiol C 1985; 82:17-19.
36.Arthur JR, Morrice PC, Nicol F, Beddows SE, Boyd R, Hayes JD, Beckett GJ. The effects of selenium and copper deficiencies on glutathione S-transferase and glutathione peroxidase in rat liver. Biochem J 1987; 248:539-44.
37.Beckett GJ, Nicol F, Proudfoot D, Dyson K, Loucaides G, Arthur JR. The changes in hepatic enzyme expression caused by selenium deficiency and hypothyroidism in rats are produced by independent mechanisms. Biochem J 1990; 266:743-747.
38.Burk RF, Masters BSS. Some effects of selenium deficiency on the hepatic microsomal cytochrome P-450 system in the rat. Arch Biochem Biophys 1975; 170:124-131.
39.Combs GF Jr. Impact of selenium and cancer-prevention findings on the nutrition-health paradigm. Nutr Cancer 2001; 40:6-11.
40.Olsson U, Lundgren B, Segura-Aguilar J, Messing-Eriksson A, Andersson K, Becedas L, De Pierre JW. Effects of selenium deficiency on xenobiotic-metabolizing and other enzymes in rat liver. Int J Vitam Nutr Res 1992; 63:31-37.
41.Lalonde L, Jean Y, Roberts KD, Chapdelaine A, Bleau G. Fluorometry of selenium in serum or urine. Clin Chem 1982; 28:172-174.
42.Philips AH, Langdon RG. Hepatic triphosphopyridine nucleotide-cytochrome c reductase: isolation, charac-terization and kinetic studies. J Biol Chem 1962; 237:2652-2660.
43.Burke MD, Thompson S, Elcombe CR, Halpert J, Haaparanta T, Mayer RT. Ethoxy-, pentoxy- and benzyloxyphenoxazones and homologues: a series of substrates to distinguish between different induced cytochromes P-450. Biochem Pharmacol 1985; 34:3337-3345.
44.Burke MD, Thompson S, Weaver RJ, Wolf CR, Mayer RT. Cytochrome P450 specificities of alkoxyresorufin O-dealkylation in human and rat liver. Biochem Pharmacol 1994; 48:923-936.
45.Imai Y, Ito A, Sato R. Evidence for biochemically different types of vesicles in the hepatic microsomal fraction. J Biochem 1996; 60:417-428.
46.Habig WH, Pabst MJ, Jakoby WB. Glutathione S-transferases, the first enzymatic step in mercapturic acid formation. J Biol Chem 1974; 249:7130-7139.
47.Lowry OH, Rosebrough NJ, Faar AL, Randall RJ. Protein measurement with the folin-phenol reagents.  J Biol Chem 1951; 193:265-275.
48.El-Banna SG, Attia AM, Nomeir FR, El-Besrawy SK, Koriem AA. Role of antioxidant micronutrients on induction of rat liver and brain cytochrome P450 enzymes by fenvalerate. Slovak J Anim Sci 2008; 41:140-145.
49.Habazin-Novak V, Plestina R. The effect of deltamethrin on induction of hepatic microsomal cytochrome P450 in rats. Period Biol 1984; 86:315-316.
50.Xi-Wen H, Wei-Hua Z, Jing LU, Tao CUI, Guang Yun XIE. Inductive effect of fenvalerate on cytochrome P450 2B1/2B2. Chinese J Pharmacol Toxicol 1999; 13:222-226.
51.Price RJ, Giddings AM, Scott MP, Walters DG, Capen CC, Osimitz TG, Lake BG. Effect of pyrethrins on cytochrome P450 forms in cultured rat and human hepatocytes. Toxicology 2008; 243:84-95.
52.Morisseau C, Derbel M, Lane TR, Stoutamire D, Hammock BD. Differential induction of hepatic drug-metabolizing enzymes by fenvaleric acid in male rats. Toxicol Sci 1999; 52:148-153.
53.Tang CA, Ma T, Liu Y. Effects of deltamethrin on hepatic microsomal enzymes in rats. Acta Scientiae Circumstantiae 1987; 7:176-180.
54.Carlson GP, Schoenig GP. Induction of liver microsomal NADPH cytochrome c reductase and cytochrome P-450 by some new synthetic pyrethroids. Toxicol Appl Pharmacol 1990; 52:507-512.
55.Krechniak J, Wrzesniowska K. Effects of pyrethroid insecticides on hepatic microsomal enzymes in rats. Environ Res 1991; 55:129-134.
56.Kale M, Rathore N, John S, Bhatnagar D. Lipid peroxidative damage on pyrethroid exposure and alterations in antioxidant status in rat erythrocytes: a possible involvement of reactive oxygen species. Toxicol Lett 1999; 105:197-205.
57.Reiter R, Wendel A. Selenium and drug metabolism – I. Multiple modulations of mouse liver enzymes. Biochem Pharmacol 1983; 32:3063-3067.
58.O'Leary KA, Li HC, Ram PA, McQuiddy P, Waxman DJ, Kasper CB. Thyroid regulation of NADPH: cytochrome P450 oxidoreductase: identification of a thyroid-responsive element in the 5'-flank of the oxidoreductase gene. Mol Pharmacol 1997; 52:46-53.
59.Erkekoglu P, Giray BK, Caglayan A, Hincal F. Selenium and/or iodine deficiency alters hepatic xenobiotic metabolizing enzyme activities in rats. J Trace Elem Med Biol 2012; 26:36-41.
60.Ram PA, Waxman DJ. Hepatic P450 expression in hypothyroid rats: differential responsiveness of male-specific P450 forms 2a (IIIA2), 2c (IIC11), and RLM2 (IIA2) to thyroid hormone. Mol Endocrinol. 1991; 5:13-20.
61.Martignoni M, Groothuis GM, de Kanter R. Species differences between mouse, rat, dog, monkey and human CYP-mediated drug metabolism, inhibition and induction. Expert Opin Drug Metab Toxicol 2006; 2:875-94.
62.Andersen ME, Clewell HJ 3rd, Gargas ML, Smith FA, Reitz RH. Physiologically based pharmacokinetics and the risk assessment process for methylene chloride. Toxicol Appl Pharmacol. 1987; 87:185-205.
63.Reitz RH, Mendrala AL, Guengerich FP. In vitro metabolism of methylene chloride in human and animal tissues: use in physiologically based pharmacokinetic models. Toxicol Appl Pharmacol 1989; 97:230-46.
64.Giray B, Cağlayan A, Erkekoğlu P, Hincal F. Fenvalerate exposure alters thyroid hormone status in selenium- and/or iodine-deficient rats. Biol Trace Elem Res. 2010; 135:233-41.
65.Pascoe GA, Sakai-Wong J, Soliven E, Correia MA. Regulation of intestinal cytochrome P-450 and heme by dietary nutrients. Critical role of selenium. Biochem Pharmacol 1983; 2:3027-3035.
66.Brigelius-Flohé R, Kipp AP. Selenium in the redox regulation of the Nrf2 and the Wnt pathway. Methods Enzymol 2013; 527:65-86.
67.Wrighton SA, Elswick B. Modulation of the induction of rat hepatic cytochromes P-450 by selenium deficiency. Biochem Pharmacol 1989; 38:3767-771.
68.Ram PA, Waxman DJ. Thyroid hormone stimulation of NADPH P-450 reductase expression in liver and extrahepatic tissues. J Biol Chem 1992; 267:3294-3301.