Molecular and functional characterization of three novel carboxylesterases in the detoxification of permethrin in the mosquito, Culex quinquefasciatus.


Journal

Insect science
ISSN: 1744-7917
Titre abrégé: Insect Sci
Pays: Australia
ID NLM: 101266965

Informations de publication

Date de publication:
Feb 2022
Historique:
revised: 20 03 2021
received: 07 09 2020
accepted: 24 03 2021
pubmed: 29 5 2021
medline: 19 2 2022
entrez: 28 5 2021
Statut: ppublish

Résumé

Carboxylesterases (CarEs) belong to a super family of multifunctional enzymes associated with the degradation of endogenous and exogenous compounds. Many insect CarEs are known to play important roles in catalyzing the hydrolysis of organophosphates (OPs), carbamates, and synthetic pyrethroids (SPs). The elevation of esterase activity through gene amplification and overexpression of estα2 and estβ2 genes contributes to the development of resistance to OP insecticides in the mosquito Culex quinquefasciatus. Three additional CarE genes are upregulated in permethrin-resistant Cx. quinquefasciatus according to an RNA-seq analysis, but their function remains unknown. In this study, we, for the first time, characterized the function of these three novel genes using in vitro protein expression, an insecticide metabolism study and molecular docking analysis. All three CarE genes were significantly overexpressed in resistant mosquito larvae, but not adults, compared to susceptible strain. No gene copy differences in these three genes were found in the mosquitoes tested. In vitro high-performance liquid chromatography (HPLC) revealed that CPIJ018231, CPIJ018232, and CPIJ018233 metabolized 30.4% ± 2.9%, 34.7% ± 6.8%, and 23.2% ± 2.2% of the permethrin, respectively. No mutations in resistant strains might significantly affect their CarE hydrolysis ability. A docking analysis further confirmed that these three CarEs from resistant strain all potentially metabolize permethrin. Taken together, these three carboxylesterase genes could play important roles in the development of permethrin resistance in Cx. quinquefasciatus larvae through transcriptional overexpression, metabolism, and detoxification.

Identifiants

pubmed: 34048147
doi: 10.1111/1744-7917.12927
doi:

Substances chimiques

Insecticides 0
Permethrin 509F88P9SZ
Carboxylic Ester Hydrolases EC 3.1.1.-

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

199-214

Informations de copyright

© 2021 Institute of Zoology, Chinese Academy of Sciences.

Références

Aerts, J.L., Gonzales, M.I. and Topalian, S.L. (2004) Selection of appropriate control genes to assess expression of tumor antigens using real-time RT-PCR. Bio Techniques, 36, 84-86.
Alon, M., Alon, F., Nauen, R. and Morin, S. (2008) Organophosphates'resistance in the B-biotype of Bemisiatabaci (Hemiptera: Aleyrodidae) is associated with a point mutation in an ace1-type acetylcholinesterase and overexpression of carboxylesterase. Insect Biochemistry and Molecular Biology, 38, 940-949.
Baffi, M.A., de Souza, G.R., de Sousa, C.S., Ceron, C.R., Bonetti, A.M. and Baf, M.A. (2008) Esterase enzymes involved in pyrethroid and organophosphate resistance in a Brazilian population of Rhiphicephallus (Boophilus) microplus (Acari, Ixodidae). Molecular and Biochemical Parasitology, 160, 70-73.
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, 248-254
Campbell, P.M., Newcomb, R.D., Russell, R.J. and Oakeshott, J.G. (1998) Two different amino acid substitutions in the ali-esterase, E3, confer alternative types of organophosphorus insecticide resistance in the sheep blowfly, Lucilia cuprina. Insect Biochemistry and Molecular Biology, 28, 139-150.
Cao, C.W., Zhang, J. and Gao, X.W. (2008) Overexpression of carboxylesterase gene associated with organophosphorous insecticide resistance in cotton aphids, Aphis gossypii (Glover). Pesticide Biochemistry and Physiology, 90, 175-180.
Choi, J., Rose, R.L. and Hodgson, E. (2002) In vitro human metabolism of permethrin: the role of human alcohol and aldehyde dehydrogenases. Pesticide Biochemistry and Physiology, 73, 117-128.
Cui, F., Lin, Z., Wang, H.S., Liu, S.L., Chang, H.J., Reeck, G. et al. (2010) Two single mutations commonly cause qualitative change of nonspecific carboxylesterases in insects. Insect Biochemistry and Molecular Biology, 41, 1-8.
DeLano, W.L. (2002) The PyMOL Molecular Graphics System. DeLano Scientific, SanCarlos, CA.
Devonshire, A.L., Heidari, R., Huang, H.Z., Hammock, B.D., Russell, R.J. and Oakeshot, J.G. (2007) Hydrolysis of individual isomers of fluorogenic pyrethroid analogs by mutant carboxylesterases from Lucilia cuprina. Insect Biochemistry and Molecular Biology, 37, 891-902.
Devonshire, A.L. and Sawicki, R.M. (1979) Insecticide resistant Myzus persicae as an example of evolution by gene duplication. Nature, 280, 140-141.
Enayati, A.A., Asgarian, F., Amouei, A., Sharif, M., Mortazavi, H., Boujhmehrani, H. et al. (2010) Pyrethroid insecticide resistance in Rhipicephalus bursa (Acari, Ixodidae). Pesticide Biochemistry and Physiology, 97, 243-248.
Feng, X.C. and Liu, N.N. (2020) Functional analyses of house Fly carboxylesterases involved in insecticide resistance. Frontiers in Physiology, 11, 595009.
Feng, Y.N., Jin, Y., Sun, W., Zhao, S., Lu, W.C., Li, M. et al. (2011) Transcription and induction profiles of two esterase genes in susceptible and acaricide-resistant Tetranychus cinnabarinus. Pesticide Biochemistry and Physiology, 100, 70-73.
Field, L.M., Blackman, R.L., Tyler-Smith, C. and Devonshire, A.L. (1999) Relationship between amount of esterase and gene copy number in insecticide-resistant Myzus persicae (Sulzer). Biochemical Journal, 399, 737-742.
Gan, Q., Schones, D.E., Eun, S.H., Wei, G., Cui, K.R., Zhao, K.J. et al. (2010) Monovalent and unpoised status of most genes in undifferentiated cell-enriched Drosophila testis. Genome Biology, 11, R42.
Gong, Y.H., Ai, G.M., Li, M., Shi, X.Y., Diao, Q.Y. and Gao, X.W. (2017a) Functional characterization of carboxylesterase gene mutations involved in Aphis gossypii resistance to organophosphate insecticides. Insect Molecular Biology, 26, 702-714.
Gong, Y.H., Li, T., Feng, Y.C. and Liu, N.N. (2017b) The function of two P450s, CYP9M10 and CYP6AA7, in the permethrin resistance of Culex quinquefasciatus. Scientific Reports, 7, 587
Grigoraki, L., Lagnel, J., Kioulos, I., Kampouraki, A., Morou, E., Labbé, P. et al. (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, e0003771.
Grigoraki, L., Pipini, D., Labbé, P., Chaskopoulou, A., Weill, M. and Vontas, J. (2017) Carboxylesterase gene amplifications associated with insecticide resistance in Aedes albopictus: geographical distribution and evolutionary origin. PLoS Neglected Tropical Diseases, 11, e0005533.
Guerrero, F.D. (2000) Cloning of a horn fly cDNA, HiaE7, encoding an esterase whose transcript concentration is elevated in diazinon-resistant flies. Insect Biochemistry and Molecular Biology, 30, 1107-1115.
Gullemaud, T., Makate, N., Raymond, M., Hirst, B. and Callaghan, A. (1997) Esterase gene amplification in Culex pipiens. Insect Molecular Biology, 6, 319-327.
Gunning, R.V., Moores, G.D. and Devonshire, A.L. (1997) Esterases and fenvalerate resistance in a field population of Helicoverpa punctigera (Lepidoptera: Noctuidae) in Australia. Pesticide Biochemistry and Physiology, 58, 155-162.
Heidari, R., Devonshire, A.L., Campbell, B.E., Dorrian, S.J., Oakeshott, J.G. and Russell, R.J. (2005) Hydrolysis of pyrethroids by carboxylesterases from Lucilia cuprina and Drosophila melanogaster with active sites modified by in vitro mutagenesis. Insect Biochemistry and Molecular Biology, 35, 597-609.
Hemingway, J. and Karunaratne, S. (1998) Mosquito carboxylesterases: a review of the molecular biology and biochemistry of a major insecticide resistance mechanism. Medical and Veterinary Entomology, 12, 1-12.
Hopkins, D.H., Fraser, N.J., Mabbitt, P.D., Carr, P.D., Oakeshott, J.G. and Jackson, C.J. (2017) Structure of an insecticide sequestering carboxylesterase from the disease vector Culex quinquefasciatus: what makes an enzyme a good insecticide sponge? Biochemistry, 56, 5512-5525.
Hosokawa, M. (2008) Structure and catalytic properties of carboxylesterase isozymes involved in metabolic activation of prodrugs. Molecules, 13, 412-431.
Irwin, J.J., Sterling, T., Mysinger, M.M., Bolstad, E.S. and Coleman, R.G. (2012) ZINC: a free tool to discover chemistry for biology. Journal of Chemical Information and Modeling, 52, 1757-1768.
Itokawa, K., Komagata, O., Kasai, S., Ogawa, K. and Tomita, T. (2016) Testing the causality between CYP9M10 and pyrethroid resistance using the TALEN and CRISPR/Cas9 technologies. Scientific Reports, 6, 24652.
Jackson, C.J., Liu, J.W., Carr, P.D., Younus, F., Coppin, C.W., Meirelles, T. et al. (2013) The aEsterase-7 carboxylesterase (E3) from the blowfly Lucilia cuprina: engineering, crystal structure, natural substrate preference and the structural basis for insecticide resistance. Proceedings of the National Academy of Sciences USA, 110, 10177-10182.
Ketterman, A.J., Karunaratne, S.H.P.P., Jayawardena, K.G.I. and Hemingway, J. (1993) Qualitative differences between populations of Culex quinquefasciatus in both the esterases A2 and B2 which are involved in insecticide resistance. Pesticide Biochemistry and Physiology, 47, 142-148.
Laskowski, R.A., MacArthur, M.W., Moss, D.S. and Thornton, J.M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. Journal of Applied Crystallography, 26, 283-291.
Li, T. and Liu, N.N. (2010) Inheritance of permethrin resistance in Culex quinquefasciatus. Journal of Medical Entomology, 47, 1127-1134.
Li, Y., Farnsworth, C.A., Coppin, C.W., Teese, M.G., Liu, J.W., Scott, C. et al. (2013) Organophosphate and pyrethroid hydrolase activities of mutant esterases from the cotton bollworm Helicoverpa armigera. PLoS ONE, 8, e77685.
Lilly, D.G., Dang, K., Webb, C.E. and Doggett, S.L. (2016) Evidence for metabolic pyrethroid resistancein the common bed bug (Hemiptera: Cimicidae). Journal of Economic Entomology, 109, 1364-1368.
Liu, H., Cupp, E.W., Micher, K.M., Guo, A. and Liu, N.N. (2004) Insecticide resistance and cross-resistance in Alabama and Florida strains ofCulex quinquefasciatus (S.). Journal of Medical Entomology, 41, 408-413.
Liu, N.N. and Scott, J.G. (1997) Phenobarbital induction of CYP6D1 is due to a transacting factor on autosome 2 in house flies, Musca domestica. Insect Molecular Biology, 6, 77-81.
Liu, N.N., Xu, Q., Zhu, F. and Zhang, L. (2006) Pyrethroid resistance in mosquitoes. Insect Science, 13, 159-166.
Livak, K.J. and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods (San Diego, Calif.), 25, 402-408.
Morris, G.M., Huey, R., Lindstrom, W., Sanner, M.F., Belew, R.K., Goodsell, D.S. et al. (2009) AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. Journal of Computational Chemistry, 30, 2785-2791.
Mutunga, J.M., Anderson, T.D., Craft, D.T., Gross, A.D., Swale, D.R., Tong, F. et al. (2015) Carbamate and pyrethroid resistance in the Akron strain of Anopheles gambiae. Pesticide Biochemistry and Physiology, 121, 116-121.
Nandi, A., Jyoti, S. H. and Singh, N.K. (2015) Esterase and glutathione S-transferase levels associated with synthetic pyrethroid resistance in Hyalomma anatolicum and Rhipicephalus microplusticks from Punjab, India. Experimental and Applied Acarology, 66, 141-157.
Newcomb, R.D., Campbell, P.M., Ollis, D.L., Cheah, E., Russell, R.J. and Oakeshott, J.G. (1997) A single amino acid substitution converts a carboxylesterase to an organophosphorus hydrolase and confers insecticide resistance on a blowfly. Proceedings of the National Academy of Sciences USA, 94, 7464-7468.
Oakeshott, J.G., Claudianos, C., Campbell, P.M., Newcomb, R.D. and Russell, R.J. (2005) Biochemical genetics and genomics of insect esterases. Comprehensive Molecular Insect Science (eds. L.I. Gilbert, K. Iatrou & S.S. Gill), pp. 309-361.Elsevier Science Publishers, London.
Pan, Y.O., Guo, H.L. and Gao, X.W. (2009) Carboxylesterase activity, cDNA sequence, and gene expression in malathion susceptible and resistant strains of the cotton aphid, Aphis gossypii. Comparative Biochemistry and Physiology Part B, 152, 266-270.
Paton, M.G., Karunaratne, S.H.P.P., Giakoumaki, E., Roberts, N. and Hemingway, J. (2000) Quantitative analysis of gene amplification in insecticide resistant Culex mosquitoes. Biochemical Journal, 346, 17-24.
Poupardin, R., Srisukontarat, W., Yunta, C. and Ranson, H. (2014) Identification of carboxylesterase genes implicated in temephos resistance in the dengue vector Aedes aegypti. PLoS Neglected Tropical Diseases, 8(3), e2743.
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 of London, Series B, 353, 1707-1711.
Reid, W.R., Zhang, L., Liu, F. and Liu, N.N. (2012) The transcriptome profile of the mosquito Culex quinquefasciatus following permethrin selection. PLoS ONE, 7, e47163.
Robert, X. and Gouet, P. (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Research, 42, W320-W324.
Roy, A., Kucukural, A. and Zhang, Y. (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nature Protocols, 5, 725-738.
Shi, L., Wei, P., Wang, X., Shen, G., Zhang, J., Xiao, W. et al. (2016) Functional analysis of esteraseTCE2 gene from Tetranychus cinnabarinus (Boisduval) involved in acaricide resistance. Scientific Reports, 6, 18646.
Sippl, M.J. (1993) Recognition of errors in three-dimensional structures of proteins. Proteins, 17, 355-362.
Small, G.J. and Hemingway, J. (2000) Molecular characterization of the amplified carboxylesterase gene associated with organophosphorus insecticide resistance in the brown planthopper, Nilaparvata lugens. Insect Molecular Biology, 9, 647-653.
Stevenson, B.J., Pignatelli, P., Nikou, D. and Paine, M.J.I. (2012) Pinpointing P450s associated with pyrethroid metabolism in the Dengue Vector, Aedes aegypti developing new tools to Combat Insecticide Resistance. PLoS Neglected Tropical Diseases, 6, e1595.
Strode, C., Wondji, C.S., David, J.P., Hawkes, N.J., Lumjuan, N., Nelson, D. et al. (2008) Genomic analysis of detoxification genes in the mosquito Aedes aegypti. Insect Biochemistry and Molecular Biology, 38, 113-123
Sun, W., Xue, C.H., He, L., Lu, W.C., Li, M., Cao, X.F. et al. (2010) Molecular characterization of two novel esterase genes from carmine spider mite, Tetranychus cinnabarinus (Acarina: Tetranychidae). Insect Science, 17, 91-100.
Vaughan, A.M., Hawkes, N.J. and Hemingway, J. (1997) Co-amplification explains linkage disequilibrium of two mosquito esterase genes in insecticide resistant Culex quinquefasciatus. Biochemical Journal, 325, 359-365.
van Asperen, K. (1962) A study of housefly esterase by means of a sensitive colorimetric method. Journal of Insect Physiology, 8, 401-416.
Vontas, J.G., Small, G.J. and Hemingway, J. (2000) Comparison of esterasegene amplification, geneexpression and esterase activity in insecticide susceptible and resistant strains of the brown planthopper, Nilaparvata lugens (Stål). Insect Molecular Biology, 9, 655-660.
Wheelock, C.E., Shan, G. and Ottea, J. (2005) Overview of carboxylesterases and their role in the metabolism of insecticides. Journal of Pest Science, 30, 75-83.
Wiederstein, M. and Sippl, M.J. (2007) ProSa-web: interactiveweb service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Research, 35, 407-410.
Wittwer, C.T., Herrmann, M.G., Moss, A.A. and Rasmussen, R.P. (1997) Continuous fluorescence monitoring of rapid cycle DNA amplification. Biotechniques, 22, 130-131.
Wu, S.W., Yang, Y.H., Yuan, G.R., Campbell, P.M., Teese, M.G., Russell, R.J. et al. (2011) Overexpressed esterases in a fenvalerate resistant strain of the cotton bollworm, Helicoverpa armigera. Insect Biochemistry and Molecular Biology, 41, 14-21.
Wu, X.M., Xu, B.Y., Si, F.L., Li, J., Yan, Z.T., Yan, Z.W. et al. (2018) Identification of carboxylesterase genes associated with pyrethroid resistance in the malaria vector Anopheles sinensis (Diptera: Culicidae). Pest Management Science, 74, 159-169.
Xu, Q., Wang, H., Zhang, L. and Liu, N. (2006) Kdr allelic variation in pyrethroid resistant mosquitoes, Culex quinquefasciatus (S). Biochemical and Biophysical Research Communications, 345, 774-780.
Yan, L.Z., Yang, P.C., Jiang, F., Cui, N., Ma, E., Qiao, C. et al. (2012) Transcriptomic and phylogenetic analysis of Culex pipiens quinquefasciatus for three detoxification gene families. BMC Genomics [Electronic Resource], 13, 609.
Zhang, Y. (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics, 9, 40.
Zhu, F., Feng, J.N., Zhang, L. and Liu, N.N. (2008) Characterization of two novel cytochrome P450 genes in insecticide-resistant house-flies. Insect Molecular Biology, 17, 27-37.

Auteurs

Youhui Gong (Y)

Department of Entomology and Plant Pathology, Auburn University, Auburn, Alabama, USA.
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China.

Ming Li (M)

Department of Entomology and Plant Pathology, Auburn University, Auburn, Alabama, USA.
Department of Biology Sciences, University of California, San Diego, California, USA.

Ting Li (T)

Department of Entomology and Plant Pathology, Auburn University, Auburn, Alabama, USA.

Nannan Liu (N)

Department of Entomology and Plant Pathology, Auburn University, Auburn, Alabama, USA.

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