|Year : 2017 | Volume
| Issue : 3 | Page : 226-232
Esterases are responsible for malathion resistance in Anopheles stephensi: A proof using biochemical and insecticide inhibition studies
Kona Madhavinadha Prasad1, Kamaraju Raghavendra1, Vaishali Verma1, Poonam Sharma Velamuri1, Veena Pande2
1 ICMR–National Institute of Malaria Research, New Delhi, India
2 Department of Biotechnology, Kumaun University, Nainital, Uttarakhand, India
|Date of Submission||16-Mar-2017|
|Date of Acceptance||24-Aug-2017|
|Date of Web Publication||7-Nov-2017|
Scientist ‘G’, ICMR-National Institute of Malaria Research, New Delhi–110 077
Source of Support: None, Conflict of Interest: None
Background & objectives: Increase in prevalence and intensity of insecticide-resistance in vectors of vector-borne diseases is a major threat to sustainable disease control; and, for their effective management, studies on resistance mechanisms are important to come out with suitable strategies. Esterases are major class of detoxification enzymes in mosquitoes, which confers protection against insecticides in causing resistance. This study was aimed at biochemical characterization of esterases responsible for malathion resistance in Anopheles stephensi mosquitoes, along with its validation through biochemical techniques and native-PAGE assays.
Methods: Laboratory maintained susceptible and resistant An. stephensi mosquitoes were used for assessing the activity and effect of α- and β-esterases on malathion. Bioassay, synergist bioassay, biochemical assay and native- PAGE were employed to characterize the role of esterases in conferring malathion-resistance.
Results: Notably significant (p < 0.0001) enhancement in α- and β-esterases activity was observed with 2-fold increase in resistant An. stephensiGOA compared to susceptible An. stephensiBB native-PAGE depicted two major bands ‘a’ (Rf = 0.80) and ‘b’ (Rf = 0.72) in susceptible An. stephensiBB while one intense band ‘b’ (Rf = 0.72) was visible in resistant An. stephensiGOA. Inhibition assay revealed complete inhibition of α- and β-esterases activity in presence of 1 mM malathion in susceptible strain compared to observed partial inhibition in resistant strain on native-PAGE.
Interpretation & conclusion: This study provides a better understanding on the role of esterase enzyme (carboxylesterase) in conferring malathion-resistance in An. stephensi mosquitoes, as evident from the native-PAGE assay results. The study results could be used in characterizing the resistance mechanisms in vectors and for suggesting alternative chemical insecticide based resistance management strategies for effective vector-borne disease control.
Keywords: Anopheles stephensi; esterases; malathion; native-PAGE; triphenyl phosphate
|How to cite this article:|
Prasad KM, Raghavendra K, Verma V, Velamuri PS, Pande V. Esterases are responsible for malathion resistance in Anopheles stephensi: A proof using biochemical and insecticide inhibition studies. J Vector Borne Dis 2017;54:226-32
|How to cite this URL:|
Prasad KM, Raghavendra K, Verma V, Velamuri PS, Pande V. Esterases are responsible for malathion resistance in Anopheles stephensi: A proof using biochemical and insecticide inhibition studies. J Vector Borne Dis [serial online] 2017 [cited 2019 Nov 11];54:226-32. Available from: http://www.jvbd.org/text.asp?2017/54/3/226/217613
| Introduction|| |
Insecticide based vector control is crucial for management of vector-borne diseases in public health programme . However, the continuous and unrestricted use of the insecticides leads to development of insecticide resistance in vectors. Anopheles stephensi is a major urban malaria vector in India, responsible for about 12% of malaria cases annually; it is also an important malaria vector in Pakistan and Iran. The insecticide resistance data for An. stephensi is meager in India. It has been reported resistant to DDT, dieldrin and malathion in Chennai (Tamil Nadu), Belgaum and Dharward (Karnataka), and Banaskantha and Amerli districts (Gujarat) in a study carried out by Roop Kumari et al in 1998. However, in a recent review on insecticide resistance carried out by Raghavendra et al, this species was reported resistant only to malathion in three districts, namely Gandhinagar, Jamnagar, Surat (Gujarat); and double resistant to DDT+malathion in seven districts, namely northwest Delhi, north Goa, Kutch (Gujarat), Ramanagar (Karnataka), Kolkata (West Bengal), Bikaner, Jodhpur (Rajasthan), and to malathion+deltamethrin in one district, i.e. Dakshina Kannada (Mangalore) in India. At present, IRS is not targeted for the control of An. stephensi, as a strategy for vector control in India, except in Rajasthan where this species is reported as primary vector of malaria. An. stephensi has been reported completely susceptible to malathion in Iran.
To date, four types of insecticide resistance mechanisms have been reported in mosquitoes, i.e. point mutations in target site genes to insecticides, elevation in enzyme levels or mutations in the coding regions of detoxification enzyme, changes in cuticle architecture, and behavioural changes. The detoxifying enzyme based resistance occurs mainly due to qualitative or quantitative changes in three main enzymes: Esterases, glutathione-S-transferases and monooxygenases, a cytochrome P450 super family enzyme. In mosquitoes showing metabolic resistance mechanism(s), it is important to measure levels of specific detoxification enzyme that confer the resistance, and also to infer cross-resistance. Esterases are major family of enzymes that are responsible for insecticide resistance in disease vectors and agriculture pests. Nonspecific and general esterases are reported responsible for organophosphates (OPs), carbamate and pyrethroids resistance,. In a study carried out in Mysore, India, Ganesh et al reported that elevated levels of β-esterase are responsible for conferring resistance to organophosphates (malathion) in An. stephensi. Carboxylesterases are most abundant protein family in the insects. Insect carboxylesterases play important physiological role in lipid metabolism and xenobiotic metabolism. They are frequently implicated for the resistance in insects to OPs, carbamates and pyrethroids through quantitative or qualitative change in the enzyme or combination of these mechanisms.
In the present study, the susceptibility status of laboratory reared An. stephensi populations to malathion and synergistic effect of carboxylesterase specific synergist, triphenyl phosphate (TPP) with malathion were determined. Synergist bioassays can not provide definitive proof of the resistance mechanisms; and needs to be combined with other assays, such as electrophoresis to provide better biochemical characteristics of resistance in an insect population. Quantitative microplate biochemical assays are performed to assess the levels of α- and β-esterases and native-polyacrylamide gel electrophoresis (PAGE) for localization of α- and β-esterases in susceptible- and resistant-An. stephensi. This study would provide a better understanding of the role of esterase enzyme in malathion-resistance and provide additional evidence to show esterase mediated malathion metabolism through native-PAGE in Indian An. stephensi. Based on literature search, this appears first such study on An. stephensi mosquitoes, which provides information on the OP resistance mechanism using native-PAGE.
| Material & Methods|| |
The mosquito strains used in this study are maintained at the insectariums of the National Institute of Malaria Research, New Delhi, India. Insecticide susceptibility assays were ascertained quarterly, each year since 2011 following WHO method.
Black Brown (BB) skin colored An. stephensi mosquitoes, collected from district Sonepat, Haryana, India, were established in the year 1996. This strain is found to be susceptible to DDT, malathion and deltamethrin in the range of 95–100, 92–100 and 98–100 respectively.
An. stephensi mosquitoes collected from Goa, India were established in the year 2009. This strain is found to be resistant to DDT, malathion and deltamethrin in the range of 12–60, 10–80 and 54–92 respectively.
Chemicals, insecticides and equipment
For biochemical assays, analytical grade chemicals purchased from Sigma Chemicals Co. (USA), and for protein estimation, reagents from Bio-Rad Laboratories, Inc. (USA) were used. Malathion (5%) insecticide impregnated papers were purchased from the Vector Control Research Unit (VCRU), University Sains Malaysia, Malaysia (www.usm.my). Technical grade malathion (96%) were ingratiated from the Hindustan Insecticides Ltd, India. NanoQuant Infinite® M200 PRO ELISA reader (Tecan Group Ltd., Switzerland) with inbuilt Magellan 7.2 software, and SCIE-PLAS electrophoresis apparatus (England) were used in the study.
Insecticide susceptibility assay
Three to five days old sugar fed female An. stephensiBB (n=116) and An. stephensiGOA (n=129) mosquitoes were exposed in replicates (20–25 mosquitoes per replicate) for 1 h to 5% malathion impregnated paper along with control replicates by using standard WHO method and kit provided by VCRU. Then mosquitoes were transferred to holding tubes and kept in climatic chamber maintained at 27±2°C and 80±10% relative humidity for 24 h. Then, dead mosquitoes were scored and percent mortality calculated as follows.
If, the mortality in control replicates was found between 5 and 20%, it was corrected using Abbott’s formula, and if the morality in control replicates was >20%, the test was rejected.
For studying synergistic effect of a specific synergist carboxylesterase, i.e. TPP, the 3–5 days old sugar fed female susceptible An. stephensiBB (n = 119) and resistant An. stephensiGOA (n = 147) mosquitoes were pre-exposed to TPP (10%) impregnated paper, for 1 h and then exposed to the malathion (5%) insecticide impregnated WHO papers for 1 h. Mortality was scored after 24 h holding period as described in insecticide susceptibility assay.
Interpretation of insecticide susceptibility and synergist data
Insecticide susceptibility status was designated on the basis of WHO criteria: > 98% mortality–Susceptible, 91 to 97% mortality–Possible resistance, and < 90% mortality–Resistant. For determining the synergistic effect, the difference in percent mortality after exposure to malathion alone and TPP + malathion was noted.
Esterase activity assay
The adult non-blood fed 1–3 days old live or −80°C/ Liquid N2 stored female susceptible and resistant An. stephensi mosquitoes were used for 96 well microplate assays. Individual mosquitoes were homogenized in 50 μl of distilled water in 1.5 ml centrifuge tube on ice and made up to a final volume of 200 μl. Homogenate was centrifuged at 14,000 rpm for 30 sec at 4°C. The supernatant was used for α- and β-esterase activity assays. Esterase activity assays were performed as described by Penilla et al with minor modifications in 96 well microplate. For α-esterase assay, 200 μl α-naphthyl acetate (NA) solution (100 μl of 30 mM α-NA in acetone in 10 ml of 0.02 M sodium phosphate buffer, pH 7.2) was added to 10 μl of homogenate in a well. Similarly, for β-esterase assay, 200 μl of β-NA solution (100 μl of 30 mM β-NA in acetone in 10 ml of 0.02 M sodium phosphate buffer pH 7.2) was added to 10 μl of homogenate in another well, simultaneously. The reactions were incubated for 15 min at room temperature and to stop the reaction, 50 μl of o-dianisidine stain (a mixture of 22.5 mg o-dianisidine in 2.25 ml distilled water and 5.25 ml of 5% sodium lauryl sulphate in 0.1 M sodium phosphate buffer, pH 7.0) was added to each well. Control wells contained 10 μl distilled water in place of homogenate, 200 μl of α-NA or β-NA solution and 50 μl of o-dianisidine stain. End point enzyme activity was measured at 570 nm in ELISA reader.
The total protein of the individual mosquitoes was estimated following Bradford method using Bio-Rad reagent, following manufacture’s protocol. The activities of α- and β-esterase of the individual mosquitoes were expressed as mmoles of product formed/min/mg protein based on the α-and β-naphthol standard curves respectively. The activity data was compared between susceptible and resistant strains using Mann-Whitney U-test.
Esterase microplate inhibition assay
A pooled homogenate of five mosquitoes from the susceptible An. stephensiBB and resistant An. stephensiGOA population were prepared separately in 1.5 ml centrifuge vials containing 50 μl of 0.02 M sodium phosphate buffer (pH 7.2) and made up to a final volume of 1.0 ml , and centrifuged at 14,000 rpm for 30 sec at 4 °C. Resistant- and susceptible-An. stephensi mosquito homogenates (10 μ1) were incubated individually in 96 well microplates with 10 μl of different concentrations of technical malathion (96%) (serial dilution of 10 mM to 0.001 mM malathion in sodium phosphate buffer, pH 7.2) for 15 min at room temperature. After incubation, α- and β-NA assay was performed as described in esterase activity assay and the end point enzyme activity was measured at 570 nm in ELISA reader. The activities of α- and β-esterase were expressed as mmoles of product formed /min/mg protein.
Esterase native polyacrylamide gel electrophoresis
Native-PAGE was performed for determining α- and β-esterase profile of the susceptible and resistant strains of An. stephensi following Gopalan et al method with minor modifications, i.e. 8% resolving and 5% stacking gel. Single mosquito from susceptible An. stephensiBB and resistant An. stephensiGOA was homogenized in 150 μl of 0.02 M sodium phosphate buffer (pH 7.2) and centrifuged at 14,000 rpm for 30 sec at 4°C in individual vials, and the protein was estimated from the supernatant. Volume of homogenate equivalent to 8 μg of protein was loaded on the gel and electrophoresed initially at 50 V for 30 min and increased to 75 V for 3 h with continuous cooling at 4°C to localize the enzymes. After electrophoresis, the gels were incubated separately in Petri dish More Detailses containing 0.1 M sodium phosphate buffer (pH 6.0) at 4°C for 10 min. After incubation, the buffer in the petri dishes were replaced with 0.1 M sodium phosphate buffer, pH 6.0 containing 1 mM α- or β- NA (30 mM stock in acetone) substrate solution for 20 min at 37°C and stained with 0.025% o-dianisidine (in DD H2O) to localize α- and β-esterase activity on the gel, washed with DDW and analyzed.
Esterase inhibition on native-PAGE
The malathion inhibition effect on α- and β-esterase activity was then assessed by using native-PAGE. Pooled homogenate of five mosquitoes each from the susceptible An. stephensiBB and resistant An. stephensiGOA population were prepared in 1.5 ml centrifuge vials in 50 μl of 0.02 M sodium phosphate buffer (pH 7.2), made up to 750 μl with 0.02 M sodium phosphate buffer (pH 7.2), and centrifuged at 14,000 rpm for 30 sec at 4 °C. The protein was estimated from the supernatant using Bio-Rad reagent. Volume of homogenate equivalent to 8 μg of protein was loaded on the gel and electrophoresed as described in previous section. Gels were pre-incubated with 0.1 M sodium phosphate buffer (pH 6.0) for 10 min followed by incubation in 1 mM malathion (dissolved in 0.1 M sodium phosphate buffer pH 6.0) for 20 min at room temperature before detecting the esterase activity. Control gels were processed without malathion incubation.
| Results|| |
Adult susceptibility and synergist assay
The malathion-susceptible An. stephensiBB showed 100% mortality while malathion-resistant An. stephensiGOA reported 82% mortality. The TPP synergistic assay revealed increase in the malathion susceptibility in the resistant line from 82 to 97% showing synergism of carboxylesterase, thereby indicating the possible involvement of this enzyme in conferring malathion resistance. The average control % mortality in control exposures with susceptible An. stephensiBB was 8.7% while in resistant An. stephensiGOA it was nil.
Esterase activity assay
The mean value of α- and β-esterase activity (mmol/ min/mg) of An. stephensiBB (susceptible strain) and An. stephensiGOA (resistant strain) are shown in [Table 1]. There was a significant increase in α- and β-esterase activity of resistant An. stephensi&æ (1.85 and 2.18 mmol/min/mg protein) compared to the α- and β-esterase activity of susceptible An. stephensiBB (0.87 and 0.88 mmol/min/mg protein) (p < 0.0001; Mann-Whitney U-test). The α- and β-esterase activity increased by 2.12 and 2.47 times in resistant strain compared to susceptible strain. The susceptibility threshold of α- and β-esterase activity in susceptible population was 2 mmol/min/mg. The proportion of population showing activity beyond this susceptibility threshold was considered resistant. About 30% of resistant An. stephensiGOA population showed activity beyond this threshold [Figure 1].
|Table 1: Mean α- and β-esterases activity (mmol/min/mg) in An. stephensiBB and An. stephensiGOA|
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|Figure 1: (a) α-esterase activity, and (b) β-esterase activity in An. stephensiBB and An. stephensiGOA (Susceptibility threshold 2 mmol/min/mg).|
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Esterase microplate inhibition assay
Dose dependent inhibition of α- and β-esterases activity with technical malathion (96%) in susceptible An. stephensiBB [Figure 2]a and resistant An. stephensiQQK [Figure 2]b were observed. However, the strains showed differential inhibition activity and >90% inhibition was observed beyond 1.2 mM malathion concentration. The activities of α- and β-esterase in susceptible and resistant strains were respectively ~1.3 and >2 mmol/min/mg.
|Figure 2: Inhibition of α- and β-esterases activity (mmol/min/mg) with different concentrations of malathion in susceptible An. stephensiBB and resistant An. stephensiGOA.|
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Esterase native polyacrylamide gel electrophoresis
The α- and β-esterase activity profiles were localized on native-PAGE [Figure 3]. In An. stephensiBB two major bands ‘a’ [Retention factor (Rf) = 0.80] and ‘b’ (Rf = 0.72) were observed based on its mobility. In An. stephensiGOA only one band ‘b’ (Rf= 0.72) was observed which was common to both the strains. The intensity of ‘b’ was relatively more in resistant strain than in susceptible strain [Figure 3].
|Figure 3: The α- and β-esterases activity in An. stephensiBB [Two bands observed 'a' (Rf = 0.80) and 'b' (Rf = 0.72)]; and An. stephensiGOA [One intense band observed 'b' (Rf = 0.72)] detected on native-PAGE.|
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Esterase inhibition on native-PAGE
The α- and β-esterases activity inhibition were studied in presence of inhibitor malathion in An. stephensiBB and An. stephensiGOAon native-PAGE assay [Figure 4]. The α- and β-esterases bands ofAn. stephensiBBwere completely inhibited by malathion [Figure 4]a however, the intensity of ‘b’ in An. stephensiGOAdecreased [Figure 4]a compared to uninhibited samples (Control) [Figure 4]b.
|Figure 4: Inhibition of α- and β-esterases activity in An. stephensiBB and An. stephensiGOA with (a) Malathion; and (b) without Malathion (Control).|
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| Discussion|| |
Involvement of elevated carboxylesterase activity has been observed in many insecticide-resistant insects of agriculture and public health importance viz. multi-insecticide resistant peach-potato aphids to organophosphates, carbamates and pyrethroids, chloropyrifos resistant Culex species, organophosphate resistant Lygus hesperus, rice brown plant hopper Nilaparvata lugens Stal, rice green leafhopper Nephotettix cincticeps Uhler and in German cockroaches. Involvement of malathion specific carboxylesterase has been reported in An. culicifacies sensu lato from India and Sri lanka, An. arabiensis from Sudan, An. stephensi from Pakistan and India (K. Raghavendra, personal communication).
The synergist study on malathion-resistant-An. stephensiGOA showed strong synergism to 10% TPP, indicating the involvement of carboxylesterase mediated mechanism of malathion-resistance. The malathion susceptibility increased from 82% in malathion alone exposures, to 97% with TPP and malathion exposure indicating involvement of carboxylesterase in conferring malathion-resistance.
In the present study, microplate biochemical assays showed 2.12 and 2.47 times elevated levels of α- and β-esterases, respectively in resistant An. stephensiGOA strain compared to the levels in susceptible An. stephensiBB strain and supported increased synergism with TPP, thereby substantiating the involvement of carboxylesterase in conferring malathion-resistance. Similar results have been reported in peach-potato aphids (Myzus persicae), Culex quinquefasciatus,, Cx. pipiens and in An. culicifacies for organophos-phate resistance.
The esterase activity was also analyzed through native-PAGE by staining with α- and β-NA substrates. Two major bands were observed in the An. stephensiBB namely, ‘a’ (Rf = 0.80) and ‘b’ (Rf = 0.72), while in malathion-resistant An. stephensiGOA only one intense band ‘b’ was seen. Gopalan et al have identified intense carboxylesterase in malathion selected line of Cx. quinquefasciatus. In a similar study by Ganesh et al, increased levels of carboxylesterase activity were found on native-PAGE in deltamethrin tolerant An. stephensi larvae. In this study, native-PAGE also illustrated complete inhibition of esterases by malathion at 1.0 mM concentration in susceptible An. stephensiBB; however, in resistant An. stephensiGOA esterase inhibition was relatively less at this concentration, which further suggested involvement of esterases in conferring malathion-resistance.
| Conclusion|| |
The study showed that levels of esterases are higher in resistant An. stephensiGOA strains compared to susceptible An. stephensiBB. The results indicated unequivocal evidence for major involvement of malathion carboxylesterase (MCE) mediated malathion-resistance mechanism in Indian strain of An. stephensi. This information could be of immense use in suggesting alternative chemical insecticide based resistance management strategies for effective disease vector control.
Conflict of interest
The authors declare no conflict of interest.
| Acknowledgements|| |
The authors express sincere thanks to the Director, National Institute of Malaria Research (NIMR) for her continuous encouragement for this study and support for providing laboratory facilities. The authors sincerely thank technical assistance rendered by Mr. Narender Sharma, Mr. Kamal Dev, Mr. Om Prakash and Mr. Rajinder Singh for completing the work.
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