Overcoming insecticide resistance through computational inhibitor design

Proceedings of the National Academy of Sciences of the United States of America

Volumn 116, Issue 42, 2019, Pages 21012-21021

  Correy, Galen J ^a,f   Zaidman, Daniel ^b   Harmelin, Alon ^b   Carvalho, Silvia ^b   Mabbitt, Peter D ^a,g   Calaora, Viviane ^c   James, Peter J ^d   Kotze, Andrew C ^e   Jackson, Colin J ^a   London, Nir ^b  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c BioTransfer   (France)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e CSIRO   (Australia)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Carboxylesterase; Covalent docking; Insecticide resistance; Lucilia cuprina; Organophosphates

Indexed keywords

CHLORPYRIFOS; DIMPYLATE; HYDROLASE; INSECTICIDE; MALATHION; ACETYLCHOLINESTERASE; CARBOXYLESTERASE; ORGANOPHOSPHATE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHEMICAL PEST CONTROL; COMPUTER MODEL; CONTROLLED STUDY; CRYSTALLOGRAPHY; ENZYME INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INSECTICIDE RESISTANCE; LUCILIA CUPRINA; MOLECULAR DOCKING; MOUSE; MYZUS PERSICAE; NONHUMAN; PRIORITY JOURNAL; SCREENING; STRUCTURE ANALYSIS; TOXICITY TESTING; ANIMAL; APHID; C57BL MOUSE; CELL LINE; DRUG EFFECT; FEMALE; GENETICS; HEK293 CELL LINE;

ACETYLCHOLINESTERASE; ANIMALS; APHIDS; CARBOXYLIC ESTER HYDROLASES; CELL LINE; DIAZINON; FEMALE; HEK293 CELLS; HUMANS; INSECTICIDE RESISTANCE; INSECTICIDES; MALATHION; MICE; MICE, INBRED C57BL; ORGANOPHOSPHATES;

EID: 85073315143     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1909130116     Document Type: Article

References (68)

1. J. Cooper, H. Dobson, The benefits of pesticides to mankind and the environment. Crop Prot. 26, 1337–1348 (2007).
2. World Health Organization, Integrated Vector Management: Strategic Framework for the Eastern Mediterranean Region 2004–2010 (The WHO Regional Office for the Eastern Mediterranean, Cairo, Egypt, 2004).
3. World Health Organization, Pesticides and Their Application for the Control of Vectors and Pests of Public Health Importance (World Health Organization, Geneva, Switzerland, ed. 6, 2006).
4. M. E. Whalon, D. Mota-Sanchez, R. M. Hollingworth, Global Pesticide Resistance in Arthropods, M. E. Whalon, D. Mota-Sanchez, R. M. Hollingworth, Eds. (Cabi International, London, United Kingdom, 2008).
5. T. C. Sparks, R. Nauen, IRAC: Mode of action classification and insecticide resistance management. Pestic. Biochem. Physiol. 121, 122–128 (2015).
6. M. Eddleston et al., Pesticide poisoning in the developing world–A minimum pesticides list. Lancet 360, 1163–1167 (2002).
7. D. Atwood, C. Paisley-Jones, Pesticides Industry Sales and Usage 2008–2012 Market Estimates (US Environmental Protection Agency, 2017).
8. T. R. Fukuto, Mechanism of action of organophosphorus and carbamate insecticides. Environ. Health Perspect. 87, 245–254 (1990).
9. J. Tafuri, J. Roberts, Organophosphate poisoning. Ann. Emerg. Med. 16, 193–202 (1987).
10. J. G. Oakeshott, C. Claudianos, P. M. Campbell, R. D. Newcomb, R. J. Russell, “Biochemical genetics and genomics of insect esterases” in Comprehensive Molecular Insect Science–Pharmacology, L. I. Gilbert, S. S. Gill, Eds. (Elsevier B.V., Oxford, United Kingdom, 2005), pp. 309–381.
11. A. L. Devonshire, L. M. Field, Gene amplification and insecticide resistance. Annu. Rev. Entomol. 36, 1–23 (1991).
12. R. D. Newcomb, D. M. Gleeson, C. G. Yong, R. J. Russell, J. G. Oakeshott, Multiple mutations and gene duplications conferring organophosphorus insecticide resistance have been selected at the Rop-1 locus of the sheep blowfly, Lucilia cuprina. J. Mol. Evol. 60, 207–220 (2005).
13. C. Claudianos, R. J. Russell, J. G. Oakeshott, The same amino acid substitution in orthologous esterases confers organophosphate resistance on the house fly and a blowfly. Insect Biochem. Mol. Biol. 29, 675–686 (1999).
14. G. J. Shanahan, Development of a changed response in Lucilia cuprina (Wied.) to organophosphorus insecticides in New South Wales. Bull. Entomol. Res. 57, 93–100 (1966).
15. R. D. Newcomb et al., A single amino acid substitution converts a carboxylesterase to an organophosphorus hydrolase and confers insecticide resistance on a blowfly. Proc. Natl. Acad. Sci. U.S.A. 94, 7464–7468 (1997).
16. J. A. McKenzie, Dieldrin and diazinon resistance in populations of the Australian sheep blowfly, Lucilia cuprina, from sheep-grazing areas and rubbish tips. Aust. J. Biol. Sci. 37, 367–374 (1984).
17. R. A. de Carvalho, T. T. Torres, A. M. L. de Azeredo-Espin, A survey of mutations in the Cochliomyia hominivorax (Diptera: Calliphoridae) esterase E3 gene associated with organophosphate resistance and the molecular identification of mutant alleles. Vet. Parasitol. 140, 344–351 (2006).
18. R. Birner-Gruenberger et al., Functional fat body proteomics and gene targeting reveal in vivo functions of Drosophila melanogaster α-Esterase-7. Insect Biochem. Mol. Biol. 42, 220–229 (2012).
19. Y.-B. Mao et al., Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat. Biotechnol. 25, 1307–1313 (2007).
20. D. R. Swale et al., An insecticide resistance-breaking mosquitocide targeting inward rectifier potassium channels in vectors of Zika virus and malaria. Sci. Rep. 6, 36954 (2016).
21. H. B. Matthews, J. E. Casida, Properties of housefly microsomal cytochromes in relation to sex, strain, substrate specificity, and apparent inhibition and induction by synergist and insecticide chemicals. Life Sci. I 9, 989–1001 (1970).
22. J. E. Casida, Mixed-function oxidase involvement in the biochemistry of insecticide synergists. J. Agric. Food Chem. 18, 753–772 (1970).
23. N. London et al., Covalent docking of large libraries for the discovery of chemical probes. Nat. Chem. Biol. 10, 1066–1072 (2014).
24. N. London et al., Covalent docking predicts substrates for haloalkanoate dehalogenase superfamily phosphatases. Biochemistry 54, 528–537 (2015).
25. C. J. Jackson et al., Structure and function of an insect α-carboxylesterase (αEsterase7) associated with insecticide resistance. Proc. Natl. Acad. Sci. U.S.A. 110, 10177–10182 (2013).
26. K. A. Koehler, G. E. Lienhard, 2-phenylethaneboronic acid, a possible transition-state analog for chymotrypsin. Biochemistry 10, 2477–2483 (1971).
27. D. B. Diaz, A. K. Yudin, The versatility of boron in biological target engagement. Nat. Chem. 9, 731–742 (2017).
28. P. D. Mabbitt et al., Conformational disorganization within the active site of a recently evolved organophosphate hydrolase limits its catalytic efficiency. Biochemistry 55, 1408–1417 (2016).
29. D. Leung, C. Hardouin, D. L. Boger, B. F. Cravatt, Discovering potent and selective reversible inhibitors of enzymes in complex proteomes. Nat. Biotechnol. 21, 687–691 (2003).
30. W. A. Kappers, R. J. Edwards, S. Murray, A. R. Boobis, Diazinon is activated by CYP2C19 in human liver. Toxicol. Appl. Pharmacol. 177, 68–76 (2001).
31. Z. Chen, R. Newcomb, E. Forbes, J. McKenzie, P. Batterham, The acetylcholinesterase gene and organophosphorus resistance in the Australian sheep blowfly, Lucilia cuprina. Insect Biochem. Mol. Biol. 31, 805–816 (2001).
32. S. Whyard, R. J. Russell, V. K. Walker, Insecticide resistance and malathion carboxylesterase in the sheep blowfly, Lucilia cuprina. Biochem. Genet. 32, 9–24 (1994).
33. M. J. Hatfield et al., Carboxylesterases: General detoxifying enzymes. Chem. Biol. Interact. 259, 327–331 (2016).
34. J. A. Crow et al., Inhibition of recombinant human carboxylesterase 1 and 2 and monoacylglycerol lipase by chlorpyrifos oxon, paraoxon and methyl paraoxon. Toxicol. Appl. Pharmacol. 258, 145–150 (2012).
35. W. K. Marshall, J. R. Roberts, “Ecotoxicology of chlorpyrifos” (Publication no. NRCC 16079, National Research Council of Canada, NRC Associate Committee on Scientific Criteria for Environmental Quality, Subcommittee on Pesticides and Related Compounds, Ottawa, ON, Canada, 1978).
36. Pfizer, “Material safety data sheet” (Version 4.0, Pfizer Pharmaceuticals Group, New York, NY, 2010), pp. 1–7.
37. J. Lian, R. Nelson, R. Lehner, Carboxylesterases in lipid metabolism: From mouse to human. Protein Cell 9, 178–195 (2018).
38. G. W. Levot, N. Sales, New high level resistance to diflubenzuron detected in the Australian sheep blowfly, Lucilia cuprina (Wiedemann) (Diptera: Calliphoridae). Gen. Appl. Entomol. 31, 43–46 (2002).
39. A. C. Kotze et al., Histone deacetylase enzymes as drug targets for the control of the sheep blowfly, Lucilia cuprina. Int. J. Parasitol. Drugs Drug Resist. 5, 201–208 (2015).
40. K. A. Smyth, T. M. Boyce, R. J. Russell, J. G. Oakeshott, MCE activities and malathion resistances in field populations of the australian sheep blowfly (Lucilia cuprina). Heredity 84, 63–72 (2000).
41. G. W. Levot, Resistance and the control of sheep ectoparasites. Int. J. Parasitol. 25, 1355–1362 (1995).
42. G. W. Levot, N. Sales, I. Barchia, In vitro larvicidal efficacy of flystrike dressings against the Australian sheep blowfly. Aust. J. Exp. Agric. 39, 457–464 (1999).
43. A. L. Devonshire, Insecticide resistance in Myzus persicae: From field to gene and back again. Pestic. Sci. 26, 375–382 (1989).
44. Nature Chemical Biology, Probing questions. Nat. Chem. Biol. 11, 533 (2015).
45. B. K. Shoichet, Virtual screening of chemical libraries. Nature 432, 862–865 (2004).
46. W. Yang, X. Gao, B. Wang, Boronic acid compounds as potential pharmaceutical agents. Med. Res. Rev. 23, 346–368 (2003).
47. W. G. Lewis et al., Click chemistry in situ: Acetylcholinesterase as a reaction vessel for the selective assembly of a femtomolar inhibitor from an array of building blocks. Angew. Chem. Int. Ed. Engl. 41, 1053–1057 (2002).
48. J. Cheung et al., Structures of human acetylcholinesterase in complex with pharma-cologically important ligands. J. Med. Chem. 55, 10282–10286 (2012).
49. L. G. Tsurkan, M. J. Hatfield, C. C. Edwards, J. L. Hyatt, P. M. Potter, Inhibition of human carboxylesterases hCE1 and hiCE by cholinesterase inhibitors. Chem. Biol. Interact. 203, 226–230 (2013).
50. S. Bencharit et al., Multisite promiscuity in the processing of endogenous substrates by human carboxylesterase 1. J. Mol. Biol. 363, 201–214 (2006).
51. C. H. Walker, M. I. Mackness, “A” esterases and their role in regulating the toxicity of organophosphates. Arch. Toxicol. 60, 30–33 (1987).
52. C. E. Furlong et al., Role of paraoxonase (PON1) status in pesticide sensitivity: Genetic and temporal determinants. Neurotoxicology 26, 651–659 (2005).
53. K. Lorentz, W. Wirtz, T. Weiss, Continuous monitoring of arylesterase in human serum. Clin. Chim. Acta 308, 69–78 (2001).
54. R. J. Russell et al., Two major classes of target site insensitivity mutations confer resistance to organophosphate and carbamate insecticides. Pestic. Biochem. Physiol. 79, 84–93 (2004).
55. E. Gasteiger et al., “Protein identification and analysis tools on the ExPASy server” in The Proteomics Protocols Handbook, J. M. Walker, Ed. (Humana Press, Inc., Totowa, NJ, 2005), pp. 571–607.
56. Y. Cheng, W. H. Prusoff, Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem. Pharmacol. 22, 3099–3108 (1973).
57. G. L. Ellman, K. D. Courtney, V. Andres Jr, R. M. Feather-Stone, A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 7, 88–95 (1961).
58. Z. Radic, N. A. Pickering, D. C. Vellom, S. Camp, P. Taylor, Three distinct domains in the cholinesterase molecule confer selectivity for acetyl- and butyrylcholinesterase inhibitors. Biochemistry 32, 12074–12084 (1993).
59. N. J. Fraser et al., Evolution of protein quaternary structure in response to selective pressure for increased thermostability. J. Mol. Biol. 428, 2359–2371 (2016).
60. W. Kabsch, XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125–132 (2010).
61. P. A. Karplus, K. Diederichs, Linking crystallographic model and data quality. Science 336, 1030–1033 (2012).
62. K. Diederichs, P. A. Karplus, Better models by discarding data? Acta Crystallogr. D Biol. Crystallogr. 69, 1215–1222 (2013).
63. A. J. McCoy et al., Phaser crystallographic software. J. Appl. Cryst. 40, 658–674 (2007).
64. G. J. Correy et al., Mapping the accessible conformational landscape of an insect carboxylesterase using conformational ensemble analysis and kinetic crystallography. Structure 24, 977–987 (2016).
65. P. Emsley, B. Lohkamp, W. G. Scott, K. Cowtan, Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486–501 (2010).
66. P. V. Afonine et al., Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr. D Biol. Crystallogr. 68, 352–367 (2012).
67. P. D. Adams et al., PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213–221 (2010).
68. R. D. Newcomb, P. M. Campbell, R. J. Russell, J. G. Oakeshott, cDNA cloning, baculovirus-expression and kinetic properties of the esterase, E3, involved in organophosphorus resistance in Lucilia cuprina. Insect Biochem. Mol. Biol. 27, 15–25 (1997).