Malathion Residue in Wheat Kernels Is Degraded by Thion Organophosphorus Pesticide-Specific Carboxylesterase

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Malathion Residue in Wheat Kernels Is Degraded by Thion Organophosphorus Pesticide-Specific Carboxylesterase Journal of Health Science, 52(3) 221–227 (2006) 221 Malathion Residue in Wheat Kernels is Degraded by Thion Organophosphorus Pesticide-Specific Carboxylesterase Kimihiko Yoshii,*, a Yasuhide Tonogai,b Hitoshi Ueno,c and Katsuhiko Nakamuroc aOsaka Prefectural Government, Pharmaceutical Affairs Division, Department of Public Health and Welfare, Otemae 2, Chuo-ku, Osaka 540–8570, Japan, bOsaka Pharmaceutical Association, 1–3–8 Izumi-cho, Chuo-ku, Osaka 540–0019, Japan, and cFaculty of Phar- maceutical Sciences, Setsunan University, 45–1 Nagaotoge-cho, Hirakata, Osaka 573–0101, Japan (Received December 2, 2005; Accepted February 20, 2006) We earlier reported that malathion residue in wheat kernels is enzymatically eliminated by adding water to swell the sample as pretreatment in the official method set forth in the Food Sanitation Law of Japan. We examined the activities of monooxygenase, organophosphorus hydrolase, methyltransferase, and carboxylesterase as possible malathion-degradable enzymes in wheat kernels. GC/MS analysis resulted in no activity of monooxygenase in wheat kernels, because malaoxon was not produced in the reaction mixture of the homogenate incubated with malathion for 4 hr. When five organophosphorus pesticides that have a thioether group (P-S-C) were reacted with the wheat kernel homogenate, no formation of thiol groups was detected with the 5,5′-Dithiobis(2-nitro-benzoic acid) (DTNB) reagent, indicating that there was no activity of organophosphorus hydrolase in the kernels. Pesticides that do not have a carboxylester group but do have a dimethyl thio- or dimethyl dithio-phosphate group were not decomposed by the homogenate, suggesting that there is no contribution of methyltransferase to malathion degradation. Among the organophosphorus pesticides with a carboxylester group, only the thion compounds malathion, phenthoate, and methacrifos were enzymatically decomposed by the homogenate. Malathion was also demonstrated to be the sub- strate of carboxylesterase, as the pesticide competitively inhibited the activity with p-nitrophenyl acetate as the typical substrate. Conversely, oxon organophosphorus pesticides were not degraded in the homogenate, the carboxylesterase of which was noncompetitively inhibited. These results suggest that malathion degradation in wheat kernels is caused by the thion organophosphorus pesticide-specific carboxylesterase. Key words —–— malathion residue, wheat kernel, carboxylesterase, malathion degradation, thion organophosphorus pesticide INTRODUCTION mum residue limits (MRLs) in the Food Sanitation Law were set for applied crops on the basis of the Since the first report on parathion was published acceptable daily intake (ADI) value. According to in 1944,1) many types of organophosphorus pesti- the official method referred to in the Law for the cides have been developed and widely used. Measurement of Residual Pesticides, the powdered Malathion is one of the most common of these pes- cereals used as samples are generally allowed to ticides, because of its selective toxicity to insects swell with water for 2 hr as a pretreatment for ex- and low toxicity to mammals.1) Malathion is also traction with organic solvent to improve the extrac- used for pest control in agriculture as a postharvest tion efficiency.3) However, we previously found that pesticide and for malaria vector control in place of malathion residue is eliminated by this pretreat- the organochlorine pesticide DDT.2) In Japan, ment.4) The elimination appeared to be caused by malathion is used for various crops, and its maxi- enzymatic reaction in the kernel homogenate, be- cause the reaction is stopped by boiling the homo- genate. *To whom correspondence should be addressed: Osaka Prefec- tural Government, Pharmaceutical Affairs Division, Department Many investigators have reported the enzymatic 5) 6,7) of Public Health and Welfare, Otemae 2, Chuo-ku, Osaka 540– degradation of malathion by microorganisms, 8,9) 10,11) 12,13) 8570, Japan. Tel.: +81-6-6941-0351; Fax: +81-6-6944-6701; E- insects, mammals, and humans. In those mail: [email protected] reports, four major metabolites, malaoxon, diethyl 222 Vol. 52 (2006) Table 1. Structures of Organophosphorus Pesticides Examined Pesticide X Z R R¼ Malathion S S CH3O-CH(CH2COOC2H5)COOC2H5 Phenthoate S S CH3O -CH(COOC2H5)C6H5 Methacrifos S O CH3O-CH2CH(CH3)COOCH3 Crotoxyphos O O CH3O -C(CH3)=CHCOOCH(CH3)C6H5 Mevinphos O O CH3O -C(CH3)=CHCOOCH3 Malaoxon O S CH3O-CH(CH2COOC2H5)COOC2H5 Methidathion S S CH3O Chlorpyrifos-methyl S O CH3O Dimethoate S S CH3O-CH2CONHCH3 thiomalate, malathion monocarboxylic acid, and the metabolites expected from malathion and related desmethyl malathion were shown to be produced by compounds. Methyltransferase and carboxylesterase monooxygenase,2,13) organophosphorus hydrolase,7) were examined based on the degradability of nine carboxylesterase,6,8,10,12) and methyltransferase,11) re- organophosphorus pesticides in the kernel homoge- spectively. Mostafa et al. estimated that the degra- nate. dation of malathion sprayed on cotton and broad beans in field experiments was mainly caused by the carboxylesterases in the crops, judging from the MATERIALS AND METHODS formation of malathion monocarboxylic acid.14) Re- ports of such enzymatic degradation by plants are Materials —–— Pesticide standards of phenthoate, fewer, however, than reports of that by microorgan- methacrifos, and methidathion, sodium dihydrogen isms, insects, and mammals. It is known that wheat phosphate, and disodium hydrogen phosphate were has oxidase, phosphatase, glutathione S-transferase, purchased from Wako Pure Chemical Industries Co., and lipase activities,15) and there is a possibility of Ltd. (Osaka, Japan). 5,5′-Dithiobis(2-nitro-benzoic corresponding to monooxygenase, organophosphate acid) (DTNB) was from Dojindo Laboratories hydrolase, methyltransferase, and carboxylesterase (Kumamoto, Japan). Pesticide standards of activities as malathion-degrading enzymes, respec- malaoxon, crotoxyphos, mevinphos, malathion, tively. chrolpyrifos methyl, and dimethoate were from The aim of this paper was to identify the wheat Riedel-de Haën Sigma-Aldrich Laborchemikalien kernel enzymes contributing to malathion elimina- GmbH (Seelze, Germany). Paraoxon was from tion when measuring the malathion residue in wheat Sigma-Aldrich (St. Louis, MO, U.S.A.). Thiomalic kernels using the official Japanese method. We ex- acid and p-nitrophenyl acetate were from Tokyo amined the activities of monooxygenase, organo- Kasei Kogyo Co., Ltd. (Tokyo, Japan). These orga- phosphorus hydrolase, methyltransferase, and nophosphorus pesticides are presented in Table 1. carboxylesterase as possible enzymes that decom- Apparatus and Analytical Conditions —–— Pesti- pose malathion in the kernel homogenate. The ac- cides were measured with a Shimadzu GC/MS tivities of monooxygenase and organophosphorus QP-5050 attached to a DB-5 GC column (5%- hydrolase were detected based on the formation of phenylmethylsiloxane, 30 m × 0.25 mm i.d., with a No. 3 223 film thickness of 0.25 mm, J&W Scientific, Folsom, buffer 30 mM, pH 7.6, was preincubated at 36°C for CA, U.S.A.). The detector and the injector tempera- 2 min and 7.5 µl of malathion 3.0 mM in acetone ture were maintained at 280°C. The column was held was added to the mixture to initiate the reaction (fi- isothermally at an initial temperature of 50°C for nal concentration of malathion was 43.3 µM). An 1 min, then temperature-programmed at 25°C/min aliquot of 10 µl was sequentially taken and mixed to 125°C and next programmed at 10°C/min from with 90 µl of acetonitrile including 4.5 µM of par- 125 to 280°C with a final hold time of 10.5 min. athion as an internal standard. The mixture was cen- Injection volume was 2 µl. trifuged at 6000 g for 3 min, and the malathion in A microplate reader, Tecan (Maennedorf, Swit- the supernatant was measured using GC/MS. Other zerland) Sunrise Rainbow Thermo, was used to de- organophosphorus pesticides were determined fol- termine enzyme activities colorimetrically. lowing the same procedure. Enzyme Assay —–— The supernatant of wheat ker- nel homogenate was prepared as follows: 5 g of wheat kernels was homogenized in 10 ml of sodium RESULTS phosphate buffer 30 mM, pH 7.6, with an Ika Ultra Turrax homogenizer. The homogenate was centri- Possible Malathion-Degradable Enzymes in fuged at 6000 g for 10 min. Protein concentration Wheat Kernels of the obtained supernatant was adjusted to 5.3 mg/ Four types of malathion-degradable enzymes ml, and it was referred to as the “wheat kernel ho- mentioned in the “Introduction” were proposed to mogenate.” be the wheat enzymes that decompose malathion. Organophosphorus Hydrolase Activity7) —–— The enzymes examined were monooxygenase, or- Malathion, phenthoate, dimethoate, malaoxon, and ganophosphorus hydrolase, methyltransferase, and methidathion were characterized by quantifying the carboxylesterase, and the cleavage patterns of en- formation of free thiol groups during hydrolysis, zymatic degradation of malathion were oxidation of utilizing DTNB reagent, in phosphate buffer 30 mM, the thion group (P = S) into oxon (P = O), hydroly- pH 7.6, at 36°C. The free thiol groups of 5′-thiol-2- sis of the P-S bond in the thioether group (P-S-C), nitrobenzoate-anion produced were detected at demethylation of the dimethyl dithio- or dimethyl 412 nm. The hydrolysis reaction was initiated by ad- thio-phosphate group, and/or hydrolysis of carboxyl dition of 10 µl of organophosphorus pesticide ac-
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