Functional Characterization of two Carboxylesterase Genes Involved in Pyrethroid Detoxification in Helicoverpa armigera.

Insect carboxylesterases are major enzymes involved in metabolism of xenobiotics including insecticides. Two carboxylesterase genes, CarE001A and CarE001H, were cloned from the destructive agricultural pest Helicoverpa armigera. Quantitative Real-Time PCR showed that CarE001A and CarE001H were predominantly expressed in fat body and midgut, respectively; developmental expression analyses found that the expression levels of both CarEs were significantly higher in fifth- instar larvae than in other life stages. Recombinant CarE001A and CarE001H expressed in the Escherichia coli exhibited high enzymatic activity toward α-naphthyl acetate. Inhibition assays showed that organophosphates had strong inhibition on CarEs activity compared to pyrethroids. Metabolism assays indicated that CarE001A and CarE001H were able to metabolize β-cypermethrin and λ-cyhalothrin. Homology modeling and molecular docking analyses demonstrated that β-cypermethrin could fit nicely into the active pocket of both carboxylesterases. These results suggested that CarE001A and CarE001H could play important roles in the detoxification of pyrehtroids in H. armigera.

[1]  Zhi-Qing Ma,et al.  Identification and biochemical characterization of carboxylesterase 001G associated with insecticide detoxification in Helicoverpa armigera. , 2019, Pesticide biochemistry and physiology.

[2]  Yulin Gao,et al.  Cytochrome P450-Mediated λ-Cyhalothrin-Resistance in a Field Strain of Helicoverpa armigera from Northeast China. , 2019, Journal of agricultural and food chemistry.

[3]  Xueqing Yang,et al.  CpGSTd3 is a lambda-Cyhalothrin Metabolizing Glutathione S-Transferase from Cydia pomonella (L.). , 2019, Journal of agricultural and food chemistry.

[4]  Xianchun Li,et al.  Expressional divergences of two desaturase genes determine the opposite ratios of two sex pheromone components in Helicoverpa armigera and Helicoverpa assulta. , 2017, Insect biochemistry and molecular biology.

[5]  G. Smagghe,et al.  Functional characterization of BdB1, a well-conserved carboxylesterase among tephritid fruit flies associated with malathion resistance in Bactrocera dorsalis (Hendel). , 2017, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[6]  J. Oakeshott,et al.  Structure of an Insecticide Sequestering Carboxylesterase from the Disease Vector Culex quinquefasciatus: What Makes an Enzyme a Good Insecticide Sponge? , 2017, Biochemistry.

[7]  Q. Diao,et al.  Functional characterization of carboxylesterase gene mutations involved in Aphis gossypii resistance to organophosphate insecticides , 2017, Insect molecular biology.

[8]  K. C. Worley,et al.  Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species , 2017, BMC Biology.

[9]  Dong Liu,et al.  CYP6B6 is involved in esfenvalerate detoxification in the polyphagous lepidopteran pest, Helicoverpa armigera. , 2017, Pesticide biochemistry and physiology.

[10]  Chong-lin Cai,et al.  Bacterial Expression and Kinetic Analysis of Carboxylesterase 001D from Helicoverpa armigera , 2016, International journal of molecular sciences.

[11]  Sudhir Kumar,et al.  MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. , 2016, Molecular biology and evolution.

[12]  J. Oakeshott,et al.  An antennal carboxylesterase from Drosophila melanogaster, esterase 6, is a candidate odorant-degrading enzyme toward food odorants , 2015, Front. Physiol..

[13]  G. Smagghe,et al.  Overexpression of two α‐esterase genes mediates metabolic resistance to malathion in the oriental fruit fly, Bactrocera dorsalis (Hendel) , 2015, Insect molecular biology.

[14]  Jianzhen Zhang,et al.  Two homologous carboxylesterase genes from Locusta migratoria with different tissue expression patterns and roles in insecticide detoxification. , 2015, Journal of insect physiology.

[15]  Michael J E Sternberg,et al.  The Phyre2 web portal for protein modeling, prediction and analysis , 2015, Nature Protocols.

[16]  M. Arif,et al.  Multiple Resistances Against Formulated Organophosphates, Pyrethroids, and Newer-Chemistry Insecticides in Populations of Helicoverpa armigera (Lepidoptera: Noctuidae) from Pakistan , 2015, Journal of economic entomology.

[17]  S. Turk,et al.  Discovery, biological evaluation, and crystal structure of a novel nanomolar selective butyrylcholinesterase inhibitor. , 2014, Journal of medicinal chemistry.

[18]  S. Dong,et al.  An antennae‐enriched carboxylesterase from Spodoptera exigua displays degradation activity in both plant volatiles and female sex pheromones , 2014, Insect molecular biology.

[19]  Ji Yuan Liu,et al.  Key Amino Acid Associated with Acephate Detoxification by Cydia pomonella Carboxylesterase Based on Molecular Dynamics with Alanine Scanning and Site-Directed Mutagenesis , 2014, J. Chem. Inf. Model..

[20]  Ya-jun Gong,et al.  Correlation between Pesticide Resistance and Enzyme Activity in the Diamondback Moth, Plutella xylostella , 2013, Journal of insect science.

[21]  W. T. Tay,et al.  A Brave New World for an Old World Pest: Helicoverpa armigera (Lepidoptera: Noctuidae) in Brazil , 2013, PloS one.

[22]  J. Oakeshott,et al.  How many genetic options for evolving insecticide resistance in heliothine and spodopteran pests? , 2013, Pest management science.

[23]  J. Oakeshott,et al.  Structure and function of an insect α-carboxylesterase (αEsterase7) associated with insecticide resistance , 2013, Proceedings of the National Academy of Sciences.

[24]  J. Oakeshott,et al.  Proteomic and molecular analyses of esterases associated with monocrotophos resistance in Helicoverpa armigera , 2012 .

[25]  D. Heckel,et al.  Resistance of Australian Helicoverpa armigera to fenvalerate is due to the chimeric P450 enzyme CYP337B3 , 2012, Proceedings of the National Academy of Sciences.

[26]  Wim F Vranken,et al.  ACPYPE - AnteChamber PYthon Parser interfacE , 2012, BMC Research Notes.

[27]  P. Hart,et al.  Testing the evolvability of an insect carboxylesterase for the detoxification of synthetic pyrethroid insecticides. , 2012, Insect biochemistry and molecular biology.

[28]  Duncan Poole,et al.  Routine Microsecond Molecular Dynamics Simulations with AMBER on GPUs. 1. Generalized Born , 2012, Journal of chemical theory and computation.

[29]  J. Oakeshott,et al.  Overexpressed esterases in a fenvalerate resistant strain of the cotton bollworm, Helicoverpa armigera. , 2011, Insect biochemistry and molecular biology.

[30]  T. Martin,et al.  Multiple P450 genes overexpressed in deltamethrin-resistant strains of Helicoverpa armigera. , 2010, Pest management science.

[31]  Yidong Wu,et al.  Molecular cloning, genomic structure, and genetic mapping of two Rdl-orthologous genes of GABA receptors in the diamondback moth, Plutella xylostella. , 2010, Archives of insect biochemistry and physiology.

[32]  A. A. El-latif,et al.  Pyrethroid resistance and esterase activity in three strains of the cotton bollworm, Helicoverpa armigera (Hübner). , 2010 .

[33]  Xueyan Shi,et al.  HPLC assay for characterizing alpha-cyano-3-phenoxybenzyl pyrethroids hydrolytic metabolism by Helicoverpa armigera (Hubner) based on the quantitative analysis of 3-phenoxybenzoic acid. , 2010, Journal of agricultural and food chemistry.

[34]  Arthur J. Olson,et al.  AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading , 2009, J. Comput. Chem..

[35]  David S. Goodsell,et al.  AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility , 2009, J. Comput. Chem..

[36]  V. Beneš,et al.  The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. , 2009, Clinical chemistry.

[37]  Xiwu Gao,et al.  Differential mRNA expression levels and gene sequences of carboxylesterase in both deltamethrin resistant and susceptible strains of the cotton aphid, Aphis gossypii , 2008 .

[38]  Xiwu Gao,et al.  Beta-cypermethrin resistance associated with high carboxylesterase activities in a strain of house fly, Musca domestica (Diptera: Muscidae) , 2007 .

[39]  J. Oakeshott,et al.  Biochemical Genetics and Genomics of Insect Esterases , 2005, Reference Module in Life Sciences.

[40]  C. Wheelock,et al.  Overview of Carboxylesterases and Their Role in the Metabolism of Insecticides , 2005 .

[41]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[42]  J. Hemingway,et al.  Molecular characterization of the amplified carboxylesterase gene associated with organophosphorus insecticide resistance in the brown planthopper, Nilaparvata lugens , 2000, Insect molecular biology.

[43]  J. Oakeshott,et al.  A single amino acid substitution converts a carboxylesterase to an organophosphorus hydrolase and confers insecticide resistance on a blowfly. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[44]  A. Devonshire,et al.  Esterases and Esfenvalerate Resistance in AustralianHelicoverpa armigera(Hübner) Lepidoptera:Noctuidae , 1996 .

[45]  Daniel M. Bender,et al.  Quantitative kinetic assays for glutathione S-transferase and general esterase in individual mosquitoes using an EIA reader , 1989 .

[46]  M. A. Hamilton,et al.  Trimmed Spearman-Karber Method for Estimating Median Lethal Concentrations in Toxicity Bioassays , 1977 .