Differential effects of insecticides on mitochondrial membrane fluidity and ATPase activity between the wolf spider and the rice stem borer

Journal of Integrative Agriculture 2015, 14(12): 2574–2580 Available online at www.sciencedirect.com

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RESEARCH ARTICLE

Differential effects of insecticides on mitochondrial membrane fluidity and ATPase activity between the wolf spider and the rice stem borer LI Hai-ping1, 2, CHANG Jing1, 2, FENG Tao1, 3, GAO Xi-wu1 1

Department of Entomology, China Agricultural University, Beijing 100193, P.R.China College of Agronomy, Inner Mongolia Agricultural University, Hohhot 010019, P.R.China 3 College of Life Science, Jianghan University, Wuhan 430056, P.R.China 2

Abstract Differential effects of methamidophos and three pyrethroids on ATPase activity and membrane fluidity of mitochondria were investigated between the wolf spider (Pirata subpiraticus (Boes. et Str.)) and the rice stem borer (Chilo suppressalis (Walker)). Based on a comparison of LD50 values, the toxicities of the tested insecticides were higher to the wolf spider than to the rice stem borer. Cyhalothrin at 1×10–4 mmol L–1 caused inhibition of the mitochondrial Na+-K+-ATPase and Ca2+-Mg2+-ATPase activities, and it’s inhibitions on Na+-K+-ATPase and Ca2+-Mg2+-ATPase activities were significantly higher in the wolf spider (44 and 28%) than in the rice stem borer (19 and 11%). Methamidophos at 1×10–4 mmol L–1 decreased Ca2+-Mg2+-ATPase activity by 16 and 27% in the wolf spider and the rice stem borer, respectively, but no significant effect on the specific activity of Na+-K+-ATPase was observed. The DPH (1,6-diphenyl-1,3,5-hexatriene) fluorescence polarization values of mitochondrial membranes were not significantly affected by methamidophos in either species. However, cyhalothrin and alpha-cypermethrin induced the values of DPH polarization of mitochondrial membrane increasing with the concentration of cyhalothrin and alpha-cypermethrin from 20 to 100 µmol L–1 in the rice stem borer and the wolf spider. Effect of ethofenprox on fluidity of the wolf spider and the rice stem borer was contrary. These results suggest that both inhibition of membrane ATPase and changes of membrane fluidity could be appended to the action mechanisms of pyrethroid insecticides. Keywords: pyrethroids, membrane fluidity, ATPase, wolf spider, rice stem borer

1. Introduction China is one of the original centers of rice cultivation and

Received 12 December, 2014 Accepted 24 April, 2015 LI Hai-ping, Tel: +86-471-4308472, E-mail: lihaiping5820@ hotmail.com; Correspondence GAO Xi-wu, Tel/Fax: +86-1062732974, E-mail: [email protected] © 2015, CAAS. All rights reserved. Published by Elsevier Ltd. doi: 10.1016/S2095-3119(15)61074-7

is currently the largest rice producer in the world. The rice stem borer, Chilo suppressalis (Walker) is a key pest of rice that is present in all rice-producing counties in China. The wolf spider, Pirata subpiraticus (Boes. et Str.), one of the most harmful natural enemies of the rice stem borer, is also widely distributed and found in abundant numbers in Chinese rice paddies. The control of the rice stem borer has been dependent on the application of insecticides, and this pest has developed resistance against the applied insecticides (Zibaee et al. 2009; Hu et al. 2010; Su et al. 2014). Methamidophos was one of the most important insecticides used to control pests in paddy fields in China.

LI Hai-ping et al. Journal of Integrative Agriculture 2015, 14(12): 2574–2580

Due to its high toxicity to mammals, methamidophos has been banned from agricultural use since January 2007 in China (Announcement No. 322 of the Ministry of Agriculture of the People’s Republic of China). Pyrethroids are considered as possible alternative insecticides in production systems that relied on methamidophos previously (Cheng et al. 2010). However, many reports have shown that pyrethroids can cause rapid decreases in spider populations in agroecosystems (Mansour 1987; Wick and Freier 2000; Feng et al. 2007). Synthetic pyrethroid insecticides are divided into two major groups based on their chemical structures: the type I pyrethroids are absent of α–cyano group in chemical structure such as allethrin; the type II pyrethroids include α–cyano group in their chemical structures such as cyhalothrin (Vershoyle and Aldridge 1980; Soderlund et al. 2002). Pyrethroids act primarily on the central nervous system (CNS) of both insects and mammals. The main molecular target of pyrethroids is the voltage-gated sodium channel (VGSC) in neurons (Narahashi 1992; Ogata and Ohishi 2002). These synthetic insecticides keep the sodium channel open for unusually long times, which cause hyperexcitation and paralysis in animals (Narahashi et al. 2000). Membrane bound protein ATPase plays an important role in ionic transfer across membranes and this enzyme has been shown to be one of the targets of pyrethroids (Toshio 1979; Kakko et al. 2003; Li et al. 2009). A growing body of evidence demonstrates that ATPases, including cell membrane-associated Na+-K+-ATPase and Ca2+-Mg2+-ATPase, as well as mitochondrial Mg2+-ATPase, and Ca2+-ATPase, can be inhibited by pyrethroids (Clark and Matsumura 1982; Luo and Bodnaryk 1988; Al-Rajhi 1990; Li et al. 2006a, b; Vani et al. 2011). Some insecticides have been testified to partition into membranes and cause changes in membrane fluidity (Antunes-Mederia and Maderia 1979; Rosita et al. 2002; Cinzia et al. 2003; Li et al. 2012). Extensive studies on the interaction of insecticides with membranes have been conducted with DDT (Dichlorodiphenyltrichloroethane) (Antunes-Mederia and Maderia 1984), Lindane (Antunes-Mederia and Maderia 1989), fenvalerate (Sarkar et al. 1993), and deltamethrin (Braguini et al. 2004; Li et al. 2009).

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Several reports have examined the comparative toxicities of insecticides to pest insects and their natural enemies. These studies also exhibited the differential responses of the biochemical mechanisms of these compounds in both the pest and the natural enemy species (Croft and Brown 1982; Mullin et al. 1982). Our previous study has exhibited the differential effects on fluidity of mitochondrial membrane from C. suppressalis (Walker) among pyrethroids and endosulfan (Li et al. 2009). In this paper, we report differential effects of methamidophos and three pyrethroids on mitochondrial membrane fluidity and ATPase activity between the wolf spider and the rice stem borer. These results will be essential in the rational application of pyrethroids in rice paddy systems.

2. Results 2.1. Bioassays The susceptibilities of the rice stem borer and the wolf spider to the insecticides tested are shown in Table 1. The LD50 value of methamidophos to the wolf spider was 0.01100 µg/individual. The LD50 value of methamidophos to the rice stem borer was 0.0338 µg/individual. In three pyrethroids tested, the rice stem borer was the most sensitive to alpha-cypermethrin, with LD50 value of 0.0036 µg/individual; the wolf spider was most sensitive to cyhalothrin, with LD50 value of 0.00078 µg/individual. In general, based on comparison of LD50 values, the toxicities of these organophosphorus and pyrethroid insecticides were higher to the wolf spider than to the rice stem borer.

2.2. Effect of insecticides on mitochondrial membrane fluidity Fig. 1 shows the changes of DPH (1,6-diphenyl-1,3,5-hexatriene) fluorescence polarization values (P) in the wolf spider and the rice stem borer mitochondrial membranes as altered by the treatments using different concentrations of cyhalothrin, alpha-cypermethrin, ethofenprox, and methamidophos. The fluorescence polarization value of mitochondrial membrane was larger in the wolf spider (P=0.309)

Table 1 Susceptibility of the wolf spider and the rice stem borer to insecticides Insecticide Cyhalothrin Alpha-cypermethrin Ethofenprox Methamidophos 1)

Slope±SE 2.237±0.353 2.853±0.535 2.593±0.383 2.761±0.427

The wolf spider LD50 (µg/induvidual, 95% confidence level) 0.00078 (0.00058-0.00100) 0.00143 (0.00101-0.00203) 0.00955 (0.00728-0.01255) 0.01100 (0.00870-0.01500)

RR, LD50 of the rice stem borer/LD50 of the wolf spider.

The rice stem borer LD50 (µg/induvidual, Slope±SE 95% confidence level) 2.558±0.559 0.0042 (0.0034-0.0062) 4.695±1.151 0.0036 (0.0031-0.0062) 2.329±0.282 0.0127 (0.0101-0.0161) 1.956±0.387 0.0338 (0.0300-0.0370)

RR1) 5.38 2.52 1.57 3.07

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A

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0.36 Fluorescence polarization

ization values and the fluidity of mitochondrial membranes increased significantly after the treatment by cyhalothrin or alpha-cypermethrin in both the wolf spider and the rice stem borer; the values increased with the concentration (from 20 to 100 µmol L–1) of cyhalothrin or alpha-cypermethrin. The action of ethofenprox was different from the above two pyrethroids in changes of the DPH polarization values and the fluidity of mitochondrial membranes. Ethofenprox increased the fluidity of the mitochondrial membranes of rice stem borer, but decreased the fluidity of the mitochondrial membranes of wolf spider; these changes were proportional with increasing ethofenprox concentrations.

0.37 Cyhalothrin Methamidophos Ethofenprox Alpha-cypermethrin

0.35 0.34 0.33 0.32 0.31 0.3 0.29 0.28

B

0

20

60

80

100

120

Concentration (μmol L–1)

2.3. Cyhalothrin and methamidophos inhibition of ATPase activity

0.28 Cyhalothrin Methamidophos Ethofenprox Alpha-cypermethrin

0.27 Fluorescence polarization

40

0.26 0.25 0.24 0.23 0.22 0.21 0.2

0

20

40

60

80

100

120

Concentration (μmol L–1)

Fig. 1 Changes of fluidity of mitochondrial membrane depending on the concentrations of three pyrethroids and methamidophos in the wolf spider (A) and the rice stem borer (B).

than in the rice stem borer (P=0.226) in the control. The DPH fluorescence polarization values of mitochondrial membranes were hardly affected by methamidophos in the wolf spider or the rice stem borer. However, the DPH polar-

Three pyrethroids caused greater inhibition of the mitochondrial Na+-K+-ATPase and Ca2+-Mg2+-ATPase activities in the wolf spider than in the rice stem borer (Table 2). The inhibition ratios of cyhalothrin on activities of Na+-K+-ATPase and Ca2+-Mg2+-ATPase were 44.32 and 28.82% in the wolf spider, significantly higher than in the rice stem borer, the inhibition ratios were only 19.49 and 11.64%, respectively when the final concentration of cyhalothrin was 100 mmol L–1. No significant difference in the inhibition on the above two ATPases by methamidophos was observed between the wolf spider and the rice stem borer. However, the inhibition of mitochondrial Ca2+-Mg2+-ATPase activity by methamidophos was significantly greater in the rice stem borer than in the wolf spider. As shown in Fig. 2, we can observe that the inhibition of cyhalothrin against the Na+K+-ATPase activity exhibited a concentration-dependent manner in the wolf spider and the rice stem borer. The inhibition of methamidophos against the Ca2+-Mg2+-ATPase activity showed a similar concentration-dependent manner for the above two animals.

3. Discussion The previous studies have showed that the main target

Table 2 In vitro comparison of the inhibition of mitochondrial ATPase by insecticides in the wolf spider and the rice stem borer Insecticides (10–4 mol L–1) Cyhalothrin Alpha-cypermethrin Ethofenprox Methamidophos 1)

Percentage of inhibition (%) The wolf spider The rice stem borer Ca2+-Mg2+-ATPase Na+-K+-ATPase Ca2+-Mg2+-ATPase Na+-K+-ATPase 11.64±4.93 b1) 44.32±0.21 a 28.82±1.06 a 19.49±7.04 b1) 36.72±0.94 a 27.82±4.59 a 12.84±4.18 b 24.65±6.80 a 23.76±5.24 a 16.71±0.28 a 22.23±1.57 a 6.77±2.60 b 27.16±2.60 b1) 5.78±0.87 a 16.16±1.61 a 6.78±0.87 a1)

Data are from previous study of Li et al. (2006b). Data are means±SE of three replications. Within columns, data by the same letter do not differ significantly between the wolf spider and the rice stem borer (Turkey’ test, P≤0.05).

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of pyrethroids appears to act on the ionic channels of biomembranes, and organophosphate is one type of potent neurotoxic molecules, which are robust inhibitors of AChE (Acetylcholinesterase). Pyrethroids are known to be more damaging to natural enemies than to pest insects (Mansour 1987; Easterbrook 1997; Wick 2000; Feng 2007). The results of our study showed that three pyrethroid insecticides were more harmful to the wolf spider than to the rice stem borer, and cyhalothrin was the mostharmful in the tested insecticides to the wolf spider. Pyrethroids, because of their damage to natural enemies and their highly toxic effects on freshwater fish and bees, even at very low concentrations (Edwards and Millburn 1985), must be subjected to further experimentation before they can be registered and used in rice paddies in China. Ethofenprox, which is registered for application of rice paddies in Japan, is quite different from conventional pyrethroids in molecular structure (Fan 1993), and is an ether chemical in fact. Ethofenprox was different from other three insecticides in toxicity. LD50 value was 0.00955 µg/individual to the wolf spider and 0.0127 µg/ individual to the rice stem borer, and the RR (relative ratio) of them was 1.57 respectively in this study. Our results indicated that ethofenprox may be suitable as an alternative insecticide for use in the rice paddies in China in the future. The plasma membrane is an important discriminating filter for cell physiology changes in phospholipids, fatty acids, and in the cholesterol content function to modulate membrane fluidity, which in turn influences enzymatic activity (Nasuti et al. 2003; Ramon et al. 2014). Our results clearly showed that cyhalothrin and alpha-cypermethrin decreased mitochondrial membrane fluidity, but that methamidophos had almost no effect on membrane fluidity. Braguini et al. (2004) measured the effects of deltamethrin on native and synthetic model membranes, and found that deltamethrin increased the fluorescence polarization of DPH in native membranes. These effects are similar to those observed for the pyrethroids tested in our study. Many studies have shown that decreases in membrane fluidity are associated with decreases in ATPase activity (Keeffe et al. 1979; Schachter 1984; Brown et al. 1988; Kim et al. 1988). In our study, treatment with pyrethroids decreased membrane fluidity and inhibited ATPase activity. ATPase can hydrolyze the terminal pyrophosphate bond of ATP to provide energy for ion-pump to drive the membrane transport of mono- and divalent-ions. There is an evidence that ATP-utilizing enzymes and ion pumps may be involved in the neurotoxic action of types I and II pyrethroids and DDT (Soderlund and Bloomquist 1989; Husain et al. 1994; Kakko et al. 2000). Our results showed that the inhibition of Na+K+-ATPase and Ca2+-Mg2+-ATPase activities resulting from treatment with the three pyrethroids was greater in the wolf

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spider than in the rice stem borer. And these inhibitions by the three pyrethroids were in agreement with the toxicities of them to the wolf spider and the rice stem borer. Our results support the theory that membrane ATPases are targets of pyrethroid action. Methamidophos is an organophosphate, and is very different from pyrethroids in molecular structure. We observed that methamidophos mainly decreased Ca2+-Mg2+-ATPase activity, and had little effect on membrane fluidity and Na+-K+-ATPase. In conclusion, the tested insecticides were more toxic to the wolf spider than to the rice stem borer. The three pyrethroids decreased mitochondrial membrane fluidity and ATPase activity. Song et al. (1996) found that the toxicity of pyrethroids was correlated to the structure of sodium channels. We hypothesize that the selective toxicity of pyrethroids between the wolf spider and the rice stem borer may be related to differences in sodium channel structures. Finally, the results of our study revealed the serious risk to spiders of pyrethroids application in paddy fields. The best way to protect spiders from pyrethroids is to develop accurate damage threshold levels and to reduce the number of insecticide applications.

4. Conclusion The toxicities of four tested insecticides including cyhalothrin, alpha-cypermethrin, ethofenprox, and methamidophos were higher to the wolf spider than to the rice stem borer. The pyrethroids inhibited the Na+-K+-ATPase and Ca2+-Mg2+ATPase activities and affected the fluidity of mitochondrial membrane on two animals. But the significant effect of methamidophos on the specific activity of Na+-K+-ATPase and member fluidity were not observed.

5. Materials and methods 5.1. Chemicals Methamidophos (70% purity) was obtained from Shandong Huayang Technology Co., Tai’an, China (www.huayang. com). Cyhalothrin (97% purity), alpha-cypermethrin (93.2% purity), and ethofenprox (95.6% purity) were got from Jiangsu Yangnong Chemical Group Co., Yangzhou, China (www.yangnong.com.cn). Coomassie brilliant blue G-250 was purchased from Sigma, USA (www.sigmaaldrich.com). DPH (1,6-diphenyl-1,3,5-hexatriene) (99% purity) and ouabain were purchased from Fluca, USA (www.sigmaaldrich.com). ATP (adenosine triphosphate) was purchased from Boehringer Mannheim GmbH, Germany (www.boehringer-ingelheim.com). Other reagents used in this study were of analytical grade and were manufactured in China.

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5.2. Animals The rice stem borer and the wolf spider populations used in this study were cultured continuously in laboratory conditions, without exposure to insecticides. Cultural conditions for rearing were (27±1)°C, 80–90% relative humidity, and a photoperiod of 16 h L:8 h D. The larvae of the rice stem borer were reared on rice seedlings, and the wolf spider was reared with adults of housefly.

5.3. Bioassay The toxicity of the various insecticides to the rice stem borer was determined by the micro-topical application technique reported by the FAO Method No. 3,1980 (FAO 1980) with some modifications. Insecticides were diluted into a series of concentrations with acetone. Before treatment, rice stem borer larvae were taken from rice seedlings and held in 30-mL plastic cups. Larvae (9 to 11 mg; 4th instar) were treated. The insecticides in 0.05 mL acetone or 0.05 mL of acetone (for controls) was delivered topically on the dorsum of the thorax using a hand microapplicator (Burkard Manufacturing, Richmansworth, England). After treatment, the larvae were placed on fresh rice seedlings in the cups in a growth chamber at room temperature of (27±1)°C, and examined for mortality after 48 h. The inability of the larvae to move or change position after being prodded was used as the criterion of mortality. In all experiments, a minimum of at least 30 larvae were tested per dose and 3 replications were done alone. Toxicity of insecticides to the wolf spider was measured using a topical application according to that described by Peng (2000). The adults of the wolf spider were anesthetized by diethyl ether before dropping topically. Each wolf spider was treated topically on the tergum with the compounds in 0.05 mL of acetone using a hand microapplicator, and was moved in a small plastic cup (5 cm in diameter, 12 cm in height) individually. The humidity in the plastic cup was kept by the sponge with enough water, and the cups were kept in a growth chamber at room temperature of (27±1)°C. A minimum of at least 30 wolf spiders were tested per dose and 3 replications were done alone. Controls were treated with 0.05 mL of acetone. The mortality of wolf spider was scored at 48 h after treatment. The inability of the wolf spider to move or change position after being prodded was used as the criterion of mortality.

5.4. Mitochondrial membrane preparation Fourth-instar larvae of the rice stem borer or wolf spider adults were homogenized in 2 mL of ice cold extraction solution (10 mmol L –1 Tris-HCl, 0.1 mmol

L–1 EDTA, 250 mmol L–1 sucrose, NaCl 0.8 g %, BSA (bovine serum albumin) 0.5 g %, pH 7.4) with a grinder (teflon pestle). The homogenate was centrifuged at 3 000× g for 10 min. The supernatant was centrifuged at 10 000× g for 30 min at 4°C. The resulting sediment was then suspended in 2 mL ice-cold sucrose extraction solution and stored at –20°C. The extraction solution (10 mmol L–1 Tris-HCl, 0.1 mmol L–1 EDTA, 250 mmol L–1 sucrose, NaCl 0.8 g %, BSA 0.5 g %, pH7.4) used in the enzymatic assays did not contain BSA. Protein content was determined with a Bradford assay using bovine serum albumin as a standard (Bradford 1976).

5.5. Fluorescence measurement A solution of DPH (2 mmol L–1) in tetrahydrofuran was diluted 1 000-fold by injection into a vigorously stirred solution of 20 mmol L–1 imidazole, pH 7.4, and stirred for 1 h before use. Steady-state fluorescence polarization measurements were performed using a Model LS-55 polarization spectrophotometer (Perkin-Elmer, Britain) equipped with two photo multipliers to separately detect each polarized component of the fluorescent light. A thermostated circulating-water pump was used to control the temperature of the cuvettes. The excitation was set at 362 nm and the emission was 432 nm for the rice stem borer, and at 360 and 430 nm for the wolf spider. Polarization is inversely proportional to fluidity; relative fluidity was expressed as 1/P. The degree of fluorescence polarization (P) was calculated according to the following equation: P=IⅡ-GIⅠ/IⅡ+GIⅠ Where, G is an instrumental correction factor, and IⅠand IⅡ are, respectively, the intensities measured with the polarization plane parallel and perpendicular to the exciting beam. The experimental data are expressed as mean values±SE of experiments performed in triplicate.

5.6. Enzymatic assays ATPase activity was determined by measuring the initial rate of release of P (phosphorus) from ATP. Na+-K+-ATPase activity was to measure ouabain sensitive ATP hydrolysis using the method of Muszbek et al. (1977) and Cheng (1977) with minor modifications. The malachite green-ammonium molybdate reagent was used to detect free inorganic phosphat. A working solution (0.5 mL) contained 150 mmol L–1 NaCl, 5 mmol L–1 KCl, 2.5 mmol L–1 MgCl2, 2.5 mmol L–1 ATP, 20 mg of homogenate protein, and 20 mmol L–1 imidazole. The total ATPase activity was assayed in this solution. Ca2+-Mg2+-ATPase was detected in a nearly identical medium that contained 1 mmol L–1 ouabain. The difference

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between the two reactions, with and without ouabain, represented the Na+-K+-ATPase. Incubations were carried out at 37°C for 15 min. The reaction was stopped with 100 mL of ice-cold 35% (w/v) trichloroacetic acid. 20 mL aliquots were analyzed for inorganic phosphate. Eliminating the enzyme from the control assays enabled monitoring of spontaneous hydrolysis of ATP. Percentage of inhibition was calculated as: Percentage of inhibition=(ATPase activity of control– ATPase activity with insecticides)/ATPase activity of control×100%

5.7. Statistical analysis A minimum of five doses for each compound were used to determine the LD50 using Polo program (POLO-PC, Leora software, 1987). Two LD50 values were considered to be significantly different (P<0.01) if their 95% fiducial limits did not overlap. Other experimental data are expressed as means±SE of experiments performed in triplicate. The Student’s t-test was used to carry out statistical analysis. Differences were considered significant at P<0.05.

Acknowledgements This work was supported by the National Basic Research Program of China (2012CB114103).

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