EFFECT OF XENOBIOTIC CHALLENGE ON ENZYMATIC ACTIVITY OF DETOXIFICATION ENZYMES AT DIFFERENT EXPOSURE PERIODS IN Aedes albopictus (SKUSE) (DIPTERA: CULICIDAE)
Abstract
The xenobiotics including insecticides such as malathion and permethrin induce the activities of detoxification enzymes and potentially leading to the development of resistance. In this study, biochemical analysis was used to characterize the time-dependent malathion and permethrin induction profile of Glutathione S-transferase (GST), α-esterase (α-est), β-esterase (β-est), Cytochrome P450 (Cyt P450) and Acetylcholinesterase (AChE), enzymes which are known to contribute to metabolic resistance in Aedes albopictus. Time-dependent induction of early fourth instar larvae with the sub-lethal concentration (LC50) of malathion (0.099 mg/L) and permethrin (0.0023 mg/L) was done at 6, 12 and 24 hours to observe the effect on the enzymatic activity under toxicological challenges. Total protein content of larvae was most elevated when the larvae were exposed to both insecticides for 24 hours. The level of total enzyme activity and specific activity of GST, as well as Cyt P450 were found to be most elevated whereas the level of α-est and β-est total enzyme and specific activity were decreased at 24 hours of treatment with malathion. A different pattern was observed for permethrin induction whereby the total enzyme and specific activity of all enzymes except Cyt P450 were highly elevated upon 24 hours of acute exposure. The level of total enzyme activity and specific activity of almost all enzymes upon acute induction with malathion and permethrin were statistically significant (p˂0.05) when compared between the induced hours and to its susceptible strain. Conclusively, these findings indicate that the continuous and prolonged exposure to sub-lethal concentration of malathion and permethrin influenced the induction of GST, α-est, β-est, Cyt P450 as well as AChE enzymatic activities.
Full Text:
PDFReferences
Amelia-Yap, Z.H., Chen, C.D., Sofian-Azirun, M. & Low, V.L. 2018. Pyrethroid resistance in the dengue vector Aedes aegypti in the Southeast Asia: Present situation in the prospects for management. Parasites & Vectors 11(1): 332.
Avicor, S.W., Wajidi, M.F., El-garj, F.M., Jaal, Z. & Yahaya, Z.S. 2014. Insecticidal activity and expression of cytochrome P450 family 4 genes in Aedes albopictus after exposure to pyrethroid mosquito coils. The Protein Journal 33(5): 457-464.
Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical biochemistry 72(1-2): 248-254.
Brogdon, W.G., McAllister, J.C. & Vulule, J. 1997. Heme-peroxidase activity measured in single mosquitoes identifies individuals expressing an elevated oxidase for insecticide resistance. Journal of the American Mosquito Control Association 13(3): 233-237.
Brogdon, W.G. & McAllister, J.C. 1998. Insecticide resistance and vector control. Emerging infectious diseases 4(4): 605.
Caminade, C., Medlock, J.M., Els Ducheyne, E., McIntyre, K.M., Leach, S., Baylis, M. & Morse, A.P. 2012. Suitability of European climate for the Asian tiger mosquito Aedes albopictus: recent trends and future scenarios. Journal of the Royal Society Interface 9(75): 2708-2717.
Chen, C.D., Nazni, W.A., Lee, H.L. & Sofian-Azirun, M. 2013. Temephos resistance in field Aedes (Stegomyia) albopictus (Skuse) from Selangor, Malaysia. Tropical Biomedicine 30 (2): 220-230.
Chua, K.B., Chua, I.L., Chua, I.E. & Chua, K.H. 2005. Effect of chemical fogging on immature Aedes mosquitoes in natural field conditions. Singapore Medical Journal 46(11): 639.
Davies, T.G.E., Field, L.M., Usherwood, P.N.R. & Williamson, M S. 2007. DDT, pyrethrins, pyrethroids and insect sodium channels. International Union of Biochemistry and Molecular Biology Life 59(3): 151-162.
Dou, W., Wu, S., Hassan, M.W. & Wang, J.J. 2009. Purification and biochemical characterization of glutathione S-transferases from three strains of Liposcelis bostrychophila Badonnel (Psocoptera: Liposcelididae): Implication of insecticide resistance. Pesticide Biochemistry and Physiology 94(1): 10-14.
El-garj, F.M.A., Avicor, S.W., Wajidi, M.F.F. & Jaal, Z. 2015. Comparative efficacy of spatial repellents containing d-allethrin and d-trans allethrin against the major dengue vector Aedes aegypti (Linnaeus). Asian Biomedicine 9(3): 313-320.
El-garj, F.M.A., Wajidi, M.F.F., & Avicor, S.W. 2016a. Allelic variants of cytochrome P450 monooxygenases: Constitutive and insecticide-mediated expression in a Malaysian strain of the dengue vector, Aedes aegypti (Diptera: Culicidae). European Journal of Entomology 113: 507-515.
El-garj, F.M.A., Avicor, S.W. & Wajidi, M.F.F. 2016b. Xenobiotic-induced expression of detoxification genes, CYP4H28v2 and CYP4H31v2 in the dengue mosquito Aedes aegypti. Tropical Biomedicine 33(3): 409-419.
Emtithal, A.E.S. & Thanaa, A.E.B. 2012. Efficacy of some insecticides on field populations of Culex pipiens (Linnaeus) from Egypt. The Journal of Basic & Applied Zoology 65(1): 62-73.
Enayati, A.A., Ranson, H. & Hemingway, J. 2005. Insect glutathione transferases and insecticide resistance. Insect molecular biology 14(1): 3-8.
Etang, J., Manga, L., Toto, J.C., Guillet, P., Fondjo, E. & Chandre, F. 2007. Spectrum of metabolic-based resistance to DDT and pyrethroids in Anopheles gambiae sl populations from Cameroon. Journal of Vector Ecology 32(1): 123-134.
Farouk, S.A., Jaal, Z. & Hamzah, S.N. 2019. Effect of nutrient and density against the susceptibility status of Aedes aegypti and Aedes albopictus towards diagnostic dose of malathion and permethrin. Serangga 24(1): 58-69.
Gratz, N.G. 2004. Critical review of the vector status of Aedes albopictus. Medical and Veterinary Entomology 18(3): 215-227.
Grigoraki, L., Lagnel, J., Kioulos, I., Kampouraki, A., Morou, E., Labbé, P., Weill, M. & Vontas, J. 2015. Transcriptome profiling and genetic study reveal amplified carboxylesterase genes implicated in temephos resistance, in the Asian tiger mosquito Aedes albopictus. PLoS neglected Tropical Diseases 9(5): e0003771.
Guzman, M.G., Halstead, S.B., Artsob, H., Buchy, P., Farrar, J., Gubler, D.J., Hunsperger, E., Kroeger, A., Margolis, H.S., Martínez, E. & Nathan, M.B. 2010. Dengue: a continuing global threat. Nature Reviews Microbiology 8(12 supp): S7.
Hamzah, S.N. & Alias, Z. 2016a. Purification, expression and partial characterisation of glutathione s-transferases (GSTs) from three different strains of Aedes albopictus (Diptera: Culicidae). Tropical Biomedicine 33: 335-347.
Hamzah, S.N. & Alias, Z. 2016b. Developmental expression and oxidative stress induction of proteome of glutathione S-transferases in Aedes albopictus (Diptera: Culicidae). Journal of Asia-Pacific Entomology 19(3): 869-875.
Hamzah, S.N., Farouk, S.A., & Alias, Z. 2019. Isoenzymes of Aedes albopictus (Diptera: Culicidae) glutathione s-transferases: Isolation and expression after acute insecticide treatment. Pesticide Biochemistry and Physiology 15 : 116-121.
Hemingway, J. 1998. Techniques to detect insecticide resistance mechanism (field and laboratory manual). Geneva: World Health Organization.
Hemingway, J., Hawkes, N.J., McCarroll, L. & Ranson, H. 2004. The molecular basis of insecticide resistance in mosquitoes. Insect Biochemistry and Molecular Biology 34(7): 653-665.
Ishak, I.H., Riveron, J.M., Ibrahim, S.S., Stott, R., Longbottom, J., Irving, H. & Wondji, C.S. 2016. The Cytochrome P450 gene CYP6P12 confers pyrethroid resistance in kdr-free Malaysian populations of the dengue vector Aedes albopictus. Scientific Reports 6: 24707.
Kasai, S., Komagata, O., Itokawa, K., Shono, T., Ng, L. C., Kobayashi, M. & Tomita, T. 2014. Mechanisms of pyrethroid resistance in the dengue mosquito vector, Aedes aegypti: target site insensitivity, penetration, and metabolism. PLoS Neglected Tropical Diseases 8(6): e2948.
Koou, S.Y., Chong, C.S., Vythilingam, I., Lee, C.Y., & Ng, L.C. 2014. Insecticide resistance and its underlying mechanisms in field populations of Aedes aegypti adults (Diptera: Culicidae) in Singapore. Parasites & vectors 7(1): 471.
Latif, M.A., Omar, M.Y., Tan, S.G., Siraj, S.S., & Ismail, A.R. 2010. Biochemical studies on malathion resistance, inheritance and association of carboxylesterase activity in brown planthopper, Nilaparvata lugens complex in Peninsular Malaysia. Insect Science 17(6): 517-526.
Li, X., Schuler, M.A. & Berenbaum, M.R. 2007. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review in Entomology (52): 231-253.
Liu, N., Xu, Q., Zhu, F. & Zhang, L.E.E. 2006. Pyrethroid resistance in mosquitoes. Insect Science 13(3): 159-166.
Lumjuan, N., McCarroll, L., Prapanthadara, L. A., Hemingway, J. & Ranson, H. 2005. Elevated activity of an Epsilon class glutathione transferase confers DDT resistance in the dengue vector, Aedes aegypti. Insect biochemistry and molecular biology 35(8): 861-871.
Lumjuan, N., Rajatileka, S., Changsom, D., Wicheer, J., Leelapat, P., Prapanthadara, L.A., Somboon, P., Lycett, G. & Ranson, H. 2011. The role of the Aedes aegypti Epsilon glutathione transferases in conferring resistance to DDT and pyrethroid insecticides. Insect Biochemistry and Molecular Biology 41: 203-209.
Mazzarri, M.B. & Georghiou, G.P. 1995. Characterization of resistance to organophosphate, carbamate, and pyrethroid insecticides in field populations of Aedes aegypti from Venezuela. Journal of the American Mosquito Control Association-Mosquito News 11(3): 315-322.
Melo-Santos, M.A.V., Varjal-Melo, J.J.M., Araújo, A.P., Gomes, T.C.S., Paiva, M.H.S., Regis, L.N., Furtado, A.F., Magalhaes, T., Macoris, M.L.G., Andrighetti, M.T.M. & Ayres, C. F.J. 2010. Resistance to the organophosphate temephos: Mechanisms, evolution and reversion in an Aedes aegypti laboratory strain from Brazil. Acta Tropica 113(2): 180-189.
Montella, I.R., Martins, A.J., Viana-Medeiros, P.F., Lima, J.B.P., Braga, I.A. & Valle, D. 2007. Insecticide resistance mechanisms of Brazilian Aedes aegypti populations from 2001 to 2004. The American Journal of Tropical Medicine and Hygiene 77(3): 467-477.
Ngoagouni, C., Kamgang, B., Brengues, C., Yahouedo, G., Paupy, C., Nakouné, E., Kazanji, M. & Chandre, F. 2016. Susceptibility profile and metabolic mechanisms involved in Aedes aegypti and Aedes albopictus resistant to DDT and deltamethrin in the Central African Republic. Parasites & Vectors 9: 599.
Nkya, T.E., Akhouayri, I., Kisinza, W. & David, J.P. 2013. Impact of environment on mosquito response to pyrethroid insecticides: Facts, evidences and prospects. Insect Biochemistry and Molecular Biology 43(4): 407-416.
Paiva, M.H., Lovin, D.D., Mori, A., Melo-Santos, M.A., Severson, D.W. & Ayres, C.F. 2016. Identification of a major quantitative trait locus determining resistance to the organophosphate temephos in the dengue vector mosquito Aedes aegypti. Genomics 107(1): 40-48.
Pang, E.L. & Loh, H.S. 2016. Current perspectives on dengue episode in Malaysia. Asian Pacific Journal of Tropical Medicine 9(4): 395-401.
Panini, M., Manicardi, G.C., Moores, G.D. & Mazzoni, E. 2016. An overview of the main pathways of metabolic resistance in insects. Invertebrate Survival Journal 13(1): 326-335.
Poupardin, R., Reynaud, S., Strode, C., Ranson, H., Vontas, J. & David, J.P. 2008. Cross-induction of detoxification genes by environmental xenobiotics and insecticides in the mosquito Aedes aegypti: Impact on larval tolerance to chemical insecticides. Insect Biochemistry and Molecular Biology 38(5): 540-551.
Ranson, H., Rossier, L., Ortelli, F., Jensen, B., Xuelan, W., Collins, F.H. & Hemingway, J. 2001. Identification of a novel class of insect glutathione S-transferases involved in resistance to DDT in the malaria vector Anopheles gambiae. Biochemical Journal, 359(2): 295-304.
Ranson, H., N’Guessan, R., Lines, J., Moiroux, N., Nkuni, Z. & Corbel, V. 2011. Pyrethroid resistance in African anopheline mosquitoes: What are the implications for malaria control? Trends in parasitology 27(2): 91-98.
Rozilawati, H., Mohd Masri, S., Tanaselvi, K., Mohd Zahari, T.H., Zairi, J., Nazni, W.A. & Lee, H.L. 2017. Life table characteristics of Malaysian strain Aedes albopictus (Skuse). Serangga 22(1): 85-121.
Sabchareon, A., Wallace, D., Sirivichayakul, C., Limkittikul, K., Chanthavanich, P., Suvannadabba, S., Jiwariyavej, V., Dulyachai, W., Pengsaa, K., Wartel, T.A. & Moureau, A. 2012. Protective efficacy of the recombinant, live-attenuated, CYD tetravalent dengue vaccine in Thai schoolchildren: a randomised, controlled phase 2b trial. The Lancet 380(9853): 1559-1567.
Saelim, V., Brogdon, W.G., Rojanapremsuk, J., Suvannadabba, S., Pandii, W., Jones, J.W. & Sithiprasasna, R. 2005. Bottle and Biochemical Assays on Temephos Resistance in Aedes aegypti in Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 36(2) : 417-425.
Smith. L.B., Kasai. S., & Scott. J.G. 2016. Pyrethroid resistance in Aedes aegypti and Aedes albopictus: Important mosquito vectors of human diseases. Pesticide Biochemistry and Physiology 133: 1-12.
Sokhna. C., Ndiath. M.O. & Rogier. C. 2013. The changes in mosquito vector behaviour and the emerging resistance to insecticides will challenge the decline of malaria. Clinical Microbiology and Infection 19: 902–907.
Somwang, P., Yanola, J., Suwan, W., Walton, C., Lumjuan, N., Prapanthadara, L.A. & Somboon, P. 2011. Enzymes-based resistant mechanism in pyrethroid resistant and susceptible Aedes aegypti strains from northern Thailand. Parasitology Research 109(3): 531-537.
Ullah, S., Li, Z., Hasan, Z., Khan, S.U. & Fahad, S. 2018. Malathion induced oxidative stress leads to histopathological and biochemical toxicity in the liver of rohu (Labeo rohita, Hamilton) at acute concentration. Ecotoxicology and Environmental Safety 161: 270-280.
Vanlerberghe, V.E., Toledo, M.E., Rodriguez, M., Gomez, D., Baly, A., Benitez, J. R. & Van Der Stuyft, P. 2009. Community involvement in dengue vector control: Cluster randomised trial. British Medical Journal 338: b1959.
Vontas. J.G., Small. G.J. & Hemingway, J. 2001. Glutathione S-transferases as antioxidant defence agents confer pyrethroid resistance in Nilaparvata lugens. Biochemical Journal 357: 65–72.
Vulule, J.M., Beach, R.F., Atieli, F.K., McAllister, J.C., Brogdon, W.G., Roberts, J.M., Mwangi, R.W. & Hawley, W.A. 1999. Elevated oxidase and esterase levels associated with permethrin tolerance in Anopheles gambiae from Kenyan villages using permethrin‐impregnated nets. Medical and Veterinary Entomology 13(3): 239-244.
Wan-Norafikah, O., Nazni, W.A., Lim, L., Dhang, C., Wan-Norjuliana, W.M., Azahari, A.H. & Mohd, S.A. 2008. Detection of permethrin resistance in Aedes albopictus Skuse, Collected from Titiwangsa zone, Kuala Lumpur, Malaysia. Proceedings of the Third ASEAN Congress of Tropical Medicine and Parasitology 3: 69-77.
Wan-Norafikah, O., Nazni, W.A., Lee, H.L., Zainol-Ariffin, P. & Sofian-Azirun, M. 2013. Susceptibility of Aedes albopictus Skuse (Diptera: Culicidae) to permethrin in Kuala Lumpur, Malaysia. Asian Biomedicine 7(1): 51-62
Wang, X., Martínez, M.A., Dai, M., Chen, D., Ares, I., Romero, A., Castellano, V., Martinez, M., Rodriguez, J.L., Martínez-Larrañaga, M.R. & Anadón, A. 2016. Permethrin-induced oxidative stress and toxicity and metabolism. A review. Environmental Research 149: 86-104.
Wei, S.H., Clark, A.G. & Syvanen, M. 2001. Identification and cloning of a key insecticide-metabolizing glutathione S-transferase (MdGST-6A) from a hyper insecticide-resistant strain of the housefly Musca domestica. Insect Biochemistry and Molecular Biology 31(12): 1145-1153.
WHO (World Health Organization). 1981. Instructions for Determining the Susceptibility or Resistance of Mosquito Larvae to Insecticides (No. WHO/VBC/81.807). Geneva: World Health Organization.
WHO (World Health Organization). 2005. Guidelines for Laboratory and Field Testing of Mosquito Larvicides (No. WHO/CDS/WHOPES/GCDPP/2005.13). Geneva: World Health Organization.
WHO (World Health Organization). 2009. Dengue: Guidelines for Diagnosis, Treatment, Prevention and Control. Geneva: World Health Organization.
Yaicharoen, R., Kiatfuengfoo, R., Chareonviriyaphap, T. & Rongnoparut, P. 2005. Characterization of deltamethrin resistance in field populations of Aedes aegypti in Thailand. Journal of Vector Ecology 30(1): 144.
Yang, M.L., Zhang, J.Z., Zhu, K.Y., Xuan, T., Liu, X.J., Guo, Y.P. & Ma, E.B. 2009. Mechanisms of organophosphate resistance in a field population of oriental migratory locust, Locusta migratoria manilensis (Meyen). Archives of Insect Biochemistry and Physiology: Published in Collaboration with the Entomological Society of America 71(1): 3-15.
Refbacks
- There are currently no refbacks.