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Differential expression of carboxylesterases in larva and adult of Culex quinquefasciatus Say (Diptera: Culicidae) from sub-Himalayan West Bengal, India

Published online by Cambridge University Press:  02 August 2018

Minu Bharati  and
Dhiraj Saha
Minu Bharati
Affiliation:
Insect Biochemistry and Molecular Biology Laboratory, Department of Zoology, University of North Bengal, Raja Ramohunpur, PO North Bengal University, Darjeeling, Siliguri, 734013, West Bengal, India
Dhiraj Saha*
Affiliation:
Insect Biochemistry and Molecular Biology Laboratory, Department of Zoology, University of North Bengal, Raja Ramohunpur, PO North Bengal University, Darjeeling, Siliguri, 734013, West Bengal, India
*
*E-mail: dhirajsaha.nbu@gmail.com; dhirajsaha@nbu.ac.in
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Abstract

Culex quinquefasciatus Say, a widely distributed mosquito in tropical and subtropical areas, is the most important vector of the filarial parasite Wuchereria bancrofti, the causative agent of lymphatic filariasis. In India, filariasis is endemic in 17 States and six Union Territories, putting about 553 million people at risk of infection. Vector control, which aims to prevent pathogen transmission through interventions targeting adult mosquito vectors, is a significant component of control of the disease. Chemical-based control represents a chief strategy in the management of mosquito vectors; however, continuous application of insecticides has led to the development of resistance in many mosquito vectors around the world. The current study aims to observe the variability of expression of carboxylesterase isozymes that play a role in detoxifying insecticides into non-toxic compounds, in different life stages of Culex mosquitoes, to understand levels of insecticide susceptibility that may be used in integrated mosquito management for efficient vector control. C. quinquefasciatus were collected from different localities of sub-Himalayan West Bengal, India, and adult and larval bioassays were performed against one organophosphate insecticide (chlorpyrifos) and two synthetic pyrethroid insecticides (deltamethrin and lambda-cyhalothrin). The activity of α- and β-carboxylesterases (quantitative assay) were measured in larvae and adults of C. quinquefasciatus using a microplate assay, and measured qualitative expression by native polyacrylamide gel electrophoresis. The study shows a differential activity of α- and β-carboxylesterases both in quantitative and qualitative assays. The quantitative assay reveals that larvae exhibit a 12.2-fold higher level activity of α-carboxylesterase and about 5.0-fold higher level of activity of β-carboxylesterase than adults. Some carboxylesterase isozymes, i.e., α-Est I-IV, α-Est VII and α-Est XI-XV were exclusively expressed in larvae, whereas α-Est V-VI and α-Est IX were expressed only in adults. In larvae, all β-Est I-IX were expressed, while in adults only β-Est IV-V was expressed. The results of adult and larval insecticide bioassay are also as per the above findings showing an LC90 value of 0.017 ppm, 0.097 ppm and 0.072 ppm in the larva, and LC90 value of 0.0015 ppm, 0.721 ppm, 0.364 ppm in adults against chlorpyrifos, deltamethrin and lambda-cyhalothrin, respectively.

Keywords

Culex quinquefasciatuscarboxylesterasesinsecticide resistancedifferential expressionlarvaedetoxifying enzymes' activity
Type
Research Paper
Information
International Journal of Tropical Insect Science , Volume 38 , Issue 4 , December 2018 , pp. 303 - 312
Copyright
Copyright © icipe 2018 

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References

Aldridge, W. N. (1953) Serum esterases. 1. Two types of esterases (A and B) hydrolysing p-nitrophenyl acetate, propionate and butyrate, and a method for their determination. Biochemical Journal 53, 110–117.Google Scholar
Alvarez, L. C., Ponce, G., Oviedo, M., Lopez, B. and Flores, A. E. (2013) Resistance to malathion and deltamethrin in Aedes aegypti (Diptera: Culicidae) from western Venezuela. Journal of Medical Entomology 50, 1031–1039.Google Scholar
Anonymous (2010) IRAC: Prevention and management of insecticide resistance in vectors of public health importance. Insecticide Resistance Action Committee 2, 72–143.Google Scholar
Avise, J. C. and McDonald, J. F. (1976) Enzyme changes during development of holo- and hemi-metabolic insects. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry 53, 393–397.Google Scholar
Bouvier, J. C., Boivin, T., Beslay, D. and Sauphanor, B. (2002) Age-dependent response to insecticides and enzyme variation in susceptible and resistant codling moth larvae. Archives of Insect Biochemistry and Physiology 51, 55–66.Google Scholar
Brady, J. P. and Richmond, R. C. (1990) Molecular analysis of evolutionary changes in the expression of Drosophila esterases. Proceedings of the National Academy of Sciences of the United States of America 87, 8217–8221.Google Scholar
Chouaïbou, M., Etang, J., Brévault, T., Nwane, P., Hinzoumbé, C. K., Mimpfoundi, R. and Simard, F. (2008) Dynamics of insecticide resistance in the malaria vector Anopheles gambiae s.l. from an area of extensive cotton cultivation in Northern Cameroon. Tropical Medicine & International Health 13, 476–486.Google Scholar
Davidson, G. (1957) Insecticide resistance in Anopheles sundaicus. Nature 180, 1333–1335.Google Scholar
de Carvalho, V. M., Marques, R. M., Lapenta, A. S. and Machado, M. F. P. S. (2003) Functional classification of esterases from leaves of Aspidosperma polyneuron M. Arg. (Apocynaceae). Genetics and Molecular Biology 26, 195–198.Google Scholar
de Kort, C. A. D. and Granger, N. A. (1981) Regulation of the juvenile hormone titer. Annual Review of Entomology 26, 1–28.Google Scholar
Diabate, A., Baldet, T., Chandre, F., Akoobeto, M., Guiguemdé, T. R., Darriet, F., Brengues, C., Guillet, P., Hemingway, J., Small, G. J. and Hougard, J. M. (2002) The role of agricultural use of insecticides in resistance to pyrethroids in Anopheles gambiaes s.l. in Burkina Faso. American Journal of Tropical Medicine and Hygiene 67, 617–622.Google Scholar
dos Santos, J. M., Contel, E. P. and Kerr, W. E. (1985) Biology of amazonian mosquitoes. III. Esterase isozymes in Anopheles darlingi. Acta Amazonia 15, 167–178.Google Scholar
Dusfour, I., Zorrilla, P., Guidez, A., Issaly, J., Girod, R., Guillaumot, L., Robello, C. and Strode, C. (2015) Deltamethrin resistance mechanisms in Aedes aegypti populations from three French overseas territories worldwide. PLOS Neglected Tropical Diseases 9 (11), e0004226.Google Scholar
Forattini, O. P., Kakitani, I., Massad, E. and Marucci, D. (1993) Studies on mosquitoes (Diptera: Culicidae) and anthropic environment. 4 – Survey of resting adults and synanthropic behaviour in south-eastern Brazil. Revista de Saúde Pública, São Paulo 27, 398–411.Google Scholar
Fournier, D., Mutero, A., Pralavorio, M. and Bride, J.-M. (1993) Drosophila acetylcholinesterase: Mechanisms of resistance to organophosphates. Chemico-Biological Interactions 87, 233–238.Google Scholar
Georghiou, G. P., Pasteur, N. and Hawley, M. K. (1980) Linkage relationship between organophosphate resistance and a highly active esterase-B in Culex quinquefasciatus from California. Journal of Economic Entomology 73, 301–305.Google Scholar
Hemingway, J. (1982) The biochemical nature of malathion resistance in Anopheles stephensi from Pakistan. Pesticide Biochemistry and Physiology 17, 149–155.Google Scholar
Hemingway, J. (1983) Biochemical studies on malathion resistance in Anopheles arabiensis from Sudan. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 477–480.Google Scholar
Hemingway, J. and Karunaratne, S. H. P. P. (1998) Mosquito carboxylesterases: a review of the molecular biology and biochemistry of a major insecticide resistance mechanism. Medical and Veterinary Entomology 12, 1–12.Google Scholar
Hemingway, J., Field, L. and Vontas, J. (2002) An overview of insecticide resistance. Science 298, 96–97.Google Scholar
Heymann, E. and Jakoby, W. B. (1980) Carboxylesterases and amidases, pp. 291–323. In Enzymatic Basis of Detoxification Vol. 2 (edited by Jakoby, W. B.). Academic Press, New York.Google Scholar
Johnson, F. M., Kanapi, C. G., Richardson, R. H., Wheeler, M. R. and Stone, W. S. (1966) An operational classification of Drosophila esterases for species comparison. University of Texas Publishing 6615, 517–532.Google Scholar
Jones, B. R. and Brancoft, H. R. (1986) Distribution and probable physiological role of esterases in reprodutive, digestive, and fat-body tissues of the adult cotton boll weevil, Anthonomus grandis Boh. Biochemical Genetics 24, 499–508.Google Scholar
Kamita, S. G. and Hammock, B. D. (2010) Juvenile hormone esterase: biochemistry and structure. Journal of Pesticide Science 35, 265–274.Google Scholar
Kamita, S. G., Hinton, A. C., Wheelock, C. E., Wogulis, M. D., Wilson, D. K., Wolf, N. M., Stok, J. E., Hock, B. and Hammock, B. D. (2003) Juvenile hormone (JH) esterase: why are you so JH specific? Insect Biochemistry and Molecular Biology 33, 1261–1273.Google Scholar
Kapin, M. A. and Ahmad, S. (1980) Esterases in larval tissues of gypsy moth, Lymantria dispar (L): Optimum assay conditions, quantification and characterization. Insect Biochemistry 10, 331–337.Google Scholar
Karlekar, S. R., Deshpande, M. M. and Andrew, R. J. (2013) Present susceptibility status of Culex quinquefasciatus Say to three insecticides in Nagpur District of India. Indian Journal of Scientific Research and Technology 1, 12–14.Google Scholar
Karunaratne, S. H. P. P. and Hemingway, J. (1996) Different insecticides select multiple carboxylesterase isozymes and different resistance levels from a single population of Culex quinquefasciatus. Pesticide Biochemistry and Physiology 54, 4–11.Google Scholar
Karunaratne, S. H. P. P. and Hemingway, J. (2001) Malathion resistance and prevalence of the malathon carboxylesterase mechanism in populations of mosquito vectors of disease in Sri Lanka. Bulletin of the World Health Organization : the International Journal of Public Health 79 (11), 1060–1064.Google Scholar
Khambay, B. P. S. and Jewess, P. J. (2010) Pyrethroids, pp. 1–29. In Insect Control: Biological and Synthetic Agents, 2nd edn (edited by Gilbert, L. I. and Gill, S. S.). Academic Press, London.Google Scholar
Koutsos, A. C., Blass, C., Meister, S., Schmidt, S., MacCallum, R. M., Soares, M. B., Collins, F. H., Benes, V., Zdobnov, E., Kafatos, F. C. and Christophides, G. K. (2007) Life cycle transcriptome of the malaria mosquito Anopheles gambiae and comparison with the fruitfly Drosophila melanogaster. Proceedings of the National Academy of Sciences of the USA 104, 11304–11309.Google Scholar
Li, C.-X., Guo, X.-X., Zhang, Y.-M., Dong, Y.-D., Xing, D., Yan, T., Wang, G., Zhang, H.-D. and Zhao, T.-Y. (2016) Identification of genes involved in pyrethroid-, propoxur-, and dichlorvos- insecticides resistance in the mosquitoes, Culex pipiens complex (Diptera: Culicidae). Acta Tropica 157, 84–95.Google Scholar
Lima-Catelani, A. R. A., Ceron, C. R. and Bicudo, H. E. M. C. (2004) Variation of genetic expression during development, revealed by esterase patterns in Aedes aegypti (Diptera: Culicidae). Biochemical Genetics 42, 69–84.Google Scholar
Lowry, O. H., Rosebrough, N. J., Farr, A. L. and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 265–275.Google Scholar
Mane, S. D., Tompkins, L. and Richmond, R. C. (1983) Male esterase 6 catalyzes the synthesis of a sex pheromone in Drosophila melanogaster females. Science 222, 419–421.Google Scholar
Montella, I. R., Schama, R. and Valle, D. (2012) The classification of esterases: an important gene family involved in insecticide resistance—A review. Memórias do Instituto Oswaldo Cruz 107, 437–449.Google Scholar
Motoyama, M. and Dauterman, C. (1974) Role of nonoxidative metabolism in organophosphorous resistance. Journal of Agricultural and Food Chemistry 22, 350–356.Google Scholar
Peiris, H. T. R. and Hemingway, J. (1993) Characterisation and inheritance of elevated esterases in organophosphorus and carbamate insecticide resistant Culex quinquefasciatus (Diptera: Culicidae) from Sri Lanka. Bulletin of Entomological Research 83, 127–132.Google Scholar
Perez-Mendoza, J., Fabrick, J. A., Zhu, K. Y. and Baker, J. E. (2000) Alterations in esterases are associated with malathion resistance in Habrobracon hebetor (Hymenoptera: Braconidae). Journal of Economic Entomology 93, 31–37.Google Scholar
Ramaiah, K. D., Das, P. K., Michael, E. and Guyatt, H. L. (2000) The economic burden of lymphatic filariasis in India. Parasitology Today 16, 251–253.Google Scholar
Raymond, M., Callaghan, A., Fort, P. and Pasteur, N. (1991) World-wide migration of amplified insecticide resistance genes in mosquitoes. Nature 350, 151–153.Google Scholar
Raymond, M., Chevillon, C., Guillemaud, T., Lenormand, T. and Pasteur, N. (1998) An overview of the evolution of overproduced esterases in the mosquito Culex pipiens. Philosophical Transactions of the Royal Society B: Biological Sciences 353, 1707–1711.Google Scholar
Raymond, M., Fournier, D., Bride, J. M., Cuany, A., Berge, J., Magnin, M. and Pasteur, N. (1986) Identification of resistance mechanisms in Culex pipiens (Diptera: Culicidae) from southern France: Insensitive acetylcholinesterase and detoxifying oxidases. Journal of Economic Entomology 79, 1452–1458.Google Scholar
Richmond, R. C., Gilbert, D. G., Sheehan, K. B., Gromko, M. H. and Butterworth, F. M. (1980) Esterase 6 and reproduction in Drosophila melanogaster. Science 207, 1483–1485.Google Scholar
Rodríguez, M. M., Bisset, J. A., Armas, Y. D. and Ramos, F. (2005) Pyrethroid insecticide-resistant strain of Aedes aegypti from Cuba induced by deltamethrin selection. Journal of the American Mosquito Control Association 21, 437–445.Google Scholar
Saavedra-Rodriguez, K., Strode, C., Flores, A. E., Garcia-Luna, S., Reyes-Solis, G., Ranson, H., Hemingway, J. and Black, W. C. IV (2014) Differential transcription profiles in Aedes aegypti detoxification genes after temephos selection. Insect Molecular Biology 23, 199–215.Google Scholar
Sabesan, S., Vanamail, P., Raju, K. H. K. and Jambulingam, P. (2010) Lymphatic filariasis in India: Epidemiology and control measures. Journal of Postgraduate Medicine 56, 232–238.Google Scholar
Scott, J. G. (1999) Cytochromes P450 and insecticide resistance. Insecticide Biochemistry and Molecular Biology 29, 757–777.Google Scholar
Shanmugavelu, M., Baytan, A. R., Chesnut, J. D. and Bonning, B. C. (2000) A novel protein that binds juvenile hormone esterase in fat body tissue and pericardial cells of the tobacco hornworm Manduca sexta L. Journal of Biological Chemistry 275, 1802–1806.Google Scholar
Siegfried, B. D. and Ono, M. (1993) Mechanisms of parathion resistance in the greenbug Schizaphis graminum (Rondani). Pesticide Biochemistry and Physiology 45, 24–33.Google Scholar
Sirivanakarn, S. (1976) Medical Entomology studies-III. A revision of the subgenus Culex in the Oriental region (Diptera: Culicidae). Contributions of the American Entomological Institute 12 (2), 1–272.Google Scholar
Steiner, W. W. M. and Johnson, W. E. (1973) Techniques for electrophoresis of Hawaiian Drosophila. Island Ecosystems IRP, U.S. International Biological Program, Honolulu (HI). International Biological Program Technical Report 30. 21 pages.Google Scholar
van Asperen, K. (1962) A study of housefly esterases by means of a sensitive colorimetric method. Journal of Insect Physiology 8, 401–414, IN3, 415–416.Google Scholar
Vedbrat, S. S. and Whitt, G. S. (1975) Isozyme ontogeny of the mosquito. Anopheles albimanus. Isozymes: Developmental Biology 3, 131–143.Google Scholar
WHO [World Health Organization, Division of Vector Biology and Control] (1981) Instructions for determining the susceptibility or resistance of mosquito larvae to insecticides. World Health Organization, Geneva. http://www.who.int/iris/handle/10665/69615.Google Scholar
WHO [World Health Organization] (2006) Guidelines for testing mosquito adulticides for indoor residual spraying and treatment of mosquito nets. WHO/ CDS/NTD/WHOPES/ GCDPP/3. World Health Organization, Geneva, Switzerland. Available at: http://apps.who.int/iris/bitstream/handle/10665/69296/WHO_CDS_NTD_WHOPES_GCDPP_2006.3_eng.pdf?sequence=1.Google Scholar
Yadouleton, A. W. M., Asidi, A., Djouaka, R. F., Braïma, J., Agossou, C. D. and Akogbeto, M. C. (2009) Development of vegetable farming: a cause of the emergence of insecticide resistance in populations of Anopheles gambiae in urban areas of Benin. Malaria Journal 8, 103.Google Scholar
Yadouleton, A., Martin, T., Padonou, G., Chandre, F., Asidi, A., Djogbenou, L., Dabiré, R., Aïkpon, R., Boko, M., Glitho, I. and Akogbeto, M. (2011) Cotton pest management practices and the selection of pyrethroid resistance in Anopheles gambiae population in Northern Benin. Parasites & Vectors 4, 60.Google Scholar
Yang, W.-J., Xu, K.-K., Shang, F., Dou, W. and Wang, J.-J. (2016) Identification and characterization of three juvenile hormone genes from Bactrocera dorsalis (Diptera: Tephritidae). Florida Entomologist 99, 648–657.Google Scholar