Metabolic and target-site mechanisms combine to confer strong DDT resistance in Anopheles gambiae

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Mitchell, Sara N ^a   Rigden, Daniel J ^b   Dowd, Andrew J ^a   Lu, Fang ^b   Wilding, Craig S ^a   Weetman, David ^a   Dadzie, Samuel ^a,c   Jenkins, Adam M ^d   Regna, Kimberly ^d   Boko, Pelagie ^a   Djogbenou, Luc ^e   Muskavitch, Marc A T ^d,f   Ranson, Hilary ^a   Paine, Mark J I ^a   Mayans, Olga ^b   Donnelly, Martin J ^a,g  

^a LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c University of Ghana   (Ghana)

^d BOSTON COLLEGE   (United States)

^e UNIVERSITY OF ABOMEY CALAVI   (Benin)

^f HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^g WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORPHENOTANE; GLUTATHIONE TRANSFERASE; GSTE2 PROTEIN; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL; INSECTICIDE; PROTEIN BINDING; RECOMBINANT PROTEIN;

AMINO ACID SUBSTITUTION; ANOPHELES GAMBIAE; ARTICLE; BINDING SITE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; HETEROLOGOUS EXPRESSION; INSECTICIDE RESISTANCE; INTROGRESSION; MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY; AFRICA; ALLELE; ANIMAL; CATALYSIS; CHEMICAL STRUCTURE; DRUG EFFECTS; ENZYME ACTIVATION; FEMALE; GENE; GENE EXPRESSION; GENETIC VARIABILITY; GENETICS; HAPLOTYPE; METABOLISM; PHYLOGEOGRAPHY; PROTEIN CONFORMATION; PROTEIN DOMAIN;

AFRICA; ALLELES; AMINO ACID SUBSTITUTION; ANIMALS; ANOPHELES GAMBIAE; CATALYSIS; DDT; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION; GENES, INSECT; GENETIC VARIATION; HAPLOTYPES; INSECTICIDE RESISTANCE; INSECTICIDES; MODELS, MOLECULAR; MUTATION; PHYLOGEOGRAPHY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECOMBINANT PROTEINS;

EID: 84899796045     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092662     Document Type: Article

References (52)

1. Newcomb RD, Campbell PM, Ollis DL, Cheah E, Russell RJ, et al. (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 of the United States of America 94: 7464-7468.
2. Ffrench-Constant R, Rocheleau T, Steichen J, Chalmers A (1993) A point mutation in a Drosophila GABA receptor confers insecticide resistance. Nature (London) 363: 449-451. (Pubitemid 23179390)
3. Weill M, Chandre F, Brengues C, Manguin S, Akogbeto M, et al. (2000) The kdr mutation occurs in the Mopti form of Anopheles gambiae s.s. through introgression. Insect Molecular Biology 9: 451-455.
4. Reimer L, Fondjo E, Patchoke S, Diallo B, Lee Y, et al. (2008) Relationship between kdr mutation and resistance to pyrethroid and DDT insecticides in natural populations of Anopheles gambiae. Journal of Medical Entomology 45: 260-266. (Pubitemid 351421734)
5. Jones C, Liyanapathirana M, Agossa F, Weetman D, Ranson H, et al. (2012) Footprints of positive selection associated with a novel mutation (N1575Y) in the voltage gated sodium channel of Anopheles gambiae. Proceedings of the National Academy of Sciences of the United States of America 109: 6614-6619.
6. Weetman D, Wilding CS, Steen K, Morgan JC, Simard F, et al. (2010) Association mapping of insecticide resistance in wild Anopheles gambiae populations: major variants identified in a low-linkage disequilbrium genome. PLoS ONE 5: e13140.
7. David JP, Strode C, Vontas J, Nikou D, Vaughan A, et al. (2005) The Anopheles gambiae detoxification chip: a highly specific microarray to study metabolic-based insecticide resistance in malaria vectors. Proceedings of the National Academy of Sciences of the United States of America 102: 4080-4084. (Pubitemid 40388558)
8. Mitchell S, Stevenson B, Müller P, Wilding C, Yawson A, et al. (2012) Identification and validation of a gene causing cross-resistance between insecticide classes in Anopheles gambiae from Ghana. Proceedings of the National Academy of Sciences of the United States of America 109: 6147-6152
9. Müller P, Warr E, Stevenson BJ, Pignatelli PM, Morgan JC, et al. (2008) Field-caught permethrin-resistant Anopheles gambiae overexpress CYP6P3, a P450 that metabolises pyrethroids. PLoS Genetics 4: e1000286.
10. Prapanthadara L, Hemingway J, Ketterman A (1993) Partial purification and characterization of glutathione S-transferases involved in DDT resistance from the mosquito Anopheles gambiae. Pesticide Biochemistry and Physiology 47: 119-133. (Pubitemid 223042852)
11. Lumjuan N, McCarroll L, Prapanthadara LA, 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: 861-871. (Pubitemid 41556949)
12. Ranson H, Rossiter L, Ortelli F, Jensen B, Wang XL, et al. (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: 295-304. (Pubitemid 32999773)
13. Ding YC, Ortelli F, Rossiter LC, Hemingway J, Ranson HI (2003) The Anopheles gambiae glutathione transferase supergene family: annotation, phylogeny and expression profiles. BMC Genomics 4: art. no. -35.
14. Ding YC, Hawkes N, Meredith J, Eggleston P, Hemingway J, et al. (2005) Characterization of the promoters of Epsilon glutathione transferases in the mosquito Anopheles gambiae and their response to oxidative stress. Biochemical Journal 387: 879-888. (Pubitemid 40685725)
15. Wang Y, Qiu L, Ranson H, Lumjuan N, Hemingway J, et al. (2008) Structure of an insect epsilon class glutathione S-transferase from the malaria vector Anopheles gambiae provides an explanation for the high DDT-detoxifying activity. Journal of Structural Biology 164: 228-235.
16. Vincent F, Davies GJ, Brannigan JA (2005) Structure and kinetics of a monomeric glucosamine 6-phosphate deaminase. Journal of Biological Chemistry 280: 19649-19655.
17. Lin Y, Lu P, Tang C, Mei Q, Sandig G, et al. (2001) Substrate inhibition kinetics for cytochrome P450-catalyzed reactions. Drug Metabolism and Disposition 29: 368-374. (Pubitemid 32275548)
18. Donnelly MJ, Townson HI (2000) Evidence for extensive genetic differentiation among populations of the malaria vector Anopheles arabiensis in Eastern Africa. Insect Molecular Biology 9: 357-367.
19. Mosca R, Schneider RT (2008) RAPIDO: a web server for the alignment of protein structures in the presence of conformational changes. Nucleic Acids Research 36: w42-46.
20. Joosten RP, Joosten K, Murshudov GN, Perrakis A (2012) PDB-REDO: constructive validation, more than just looking for errors. Acta Crystallographica Section D-Biological Crystallography 68: 484-496.
21. WHO (2012) Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. Geneva: World Health Organization. ISBN 978 92 4 150515 4 ISBN 978 92 4 150515 4.
22. Djouaka RF, Bakare AA, Coulibaly ON, Akogbeto MC, Ranson H, et al. (2008) Expression of the cytochrome P450s, CYP6P3 and CYP6M2 are significantly elevated in multiple pyrethroid resistant populations of Anopheles gambiae s.s. from Southern Benin and Nigeria. BMC Genomics 9: e538.
23. Amenya DA, Naguran R, Lo TCM, Ranson H, Spillings BL, et al. (2008) Over expression of a cytochrome p450 (CYP6P9) in a major African malaria vector, Anopheles funestus, resistant to pyrethroids. Insect Molecular Biology 17: 19-25. (Pubitemid 351171296)
24. Le Goff G, Boundy S, Daborn PJ, Yen JL, Sofer L, et al. (2003) Microarray analysis of cytochrome P450 mediated insecticide resistance in Drosophila. Insect Biochemistry and Molecular Biology 33: 701-708. (Pubitemid 36821095)
25. Puinean AM, Foster SP, Oliphant L, Denholm I, Field LM, et al. (2010) Amplification of a cytochrome P450 gene is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. PLoS Genetics 6: e1000999.
26. Ortelli F, Rossiter LC, Vontas J, Ranson H, Hemingway J (2003) Heterologous expression of four glutathione transferase genes genetically linked to a major insecticide-resistance locus from the malaria vector Anopheles gambiae. Biochemical Journal 373: 957-963. (Pubitemid 36981107)
27. Wilkins EE, Marcet PL, Sutcliffe AC, Howell PI (2009) Authentication scheme for routine verification of genetically similar laboratory colonies: a trial with Anopheles gambiae. BMC Biotechnology 9.
28. Claudianos C, Russell RJ, Oakeshott JG (1999) The same amino acid substitution in orthologous esterases confers organophosphate resistance on the house fly and a blowfly. Insect Biochemistry and Molecular Biology 29: 675-686. (Pubitemid 29347310)
29. Daborn PJ, Lumb C, Harrop TWR, Blasetti A, Pasricha S, et al. (2012) Using Drosophila melanogaster to validate metabolism-based insecticide resistance from insect pests. Insect Biochemistry and Molecular Biology 42: 918-924.
30. Smith DT, Hosken DJ, Rostant WG, Yeo M, Griffin RM, et al. (2011) DDT resistance, epistasis and male fitness in flies. Journal of Evolutionary Biology 24: 1351-1362.
31. Sterner R, Liebl W (2001) Thermophilic adaptation of proteins. Critical Reviews in Biochemistry and Molecular Biology 36: 39-106. (Pubitemid 32202690)
32. Jaenicke R (1991) Protein stability and molecular adaptation to extreme conditions. European Journal of Biochemistry 202: 715-728.
33. Schlee S, Deuss M, Bruning M, Ivens A, Schwab T, et al. (2009) Activation of anthranilate phosphoribosyltransferase from Sulfolobus solfataricus by removal of magnesium inhibition and acceleration of product rlease. Biochemistry 48: 5199-5209.
34. Merz A, Yee MC, Szadkowski H, Pappenberger G, Crameri A, et al. (2000) Improving the catalytic activity of a thermophilic enzyme at low temperatures. Biochemistry 39: 880-889. (Pubitemid 30075314)
35. Dehouck Y, Kwasigroch J, Gilis D, Rooman M (2011) PoPMuSiC 2.1: a web server for the estimation of protein stability changes upon mutation and sequence optimality. BMC Bioinformatics 12: e151.
36. Dehouck Y, Grosfils A, Folch B, Gilis D, Bogaerts P, et al. (2009) Fast and accurate predictions of protein stability changes upon mutations using statistical potentials and neural networks: PoPMuSiC-2.0. Bioinformatics 25: 2537-2543.
37. Prapanthadara L, Hemingway J, Ketterman AJIAT (1995) DDT resistance in Anopheles gambiae (Diptera, Culicidae) from Zanzibar, Tanzania, based on increased DDT dehydrochlorinase activity of Glutathione S-Transferases. Bulletin of Entomological Research 85: 267-274.
38. Ranson H, Jensen B, Wang X, Prapanthadara L, Hemingway J, et al. (2000) Genetic mapping of two loci affecting DDT resistance in the malaria vector Anopheles gambiae. Insect Molecular Biology 9: 499-507.
39. Fanello C, Santolamazza F, della Torre AI (2002) Simultaneous identification of species and molecular forms of the Anopheles gambiae complex by PCR-RFLP. Medical and Veterinary Entomology 16: 461-464. (Pubitemid 36016904)
40. Bradford MM (1976) Rapid and sensitive method for quantitation of microgram quanitities of protein utilizing principle of protein-dye binding. Analytical Biochemistry 72: 248-254.
41. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione-s-transferases - first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry 249: 7130-7139.
42. R-Core-Team (2012) R: A Language and Environment for Statistical Computing.
43. Kabsch W (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. Journal of Applied Crystallography 26: 795-800.
44. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. Journal of Applied Crystallography 40.
45. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallographica Section D Biological Crystallography 69: 2126-2132. (Pubitemid 41742764)
46. Murshudov GN, Skubák P, Lebedev AA, Pannu NS, Steiner RA, et al. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallographica Section D Biological Crystallography 67: 355-367.
47. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy A, et al. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallographica Section D Biological Crystallography 58: 1948-1954. (Pubitemid 35337293)
48. Venken KJT, He Y, Hoskins RA, Bellen HJ (2006) P[acman] : A BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster . Science 314: 1747-1751. (Pubitemid 44969080)
49. Badolo A, Traore A, Jones CM, Sanou A, Flood L, et al. (2012) Three years of insecticide resistance monitoring in Anopheles gambiae in Burkina Faso: resistance on the rise? Malaria Journal 11: e232.
50. Bass C, Nikou D, Donnelly M, Williamson M, Ranson H, et al. (2007) Detection of knockdown resistance (kdr) mutations in Anopheles gambiae: a comparison of two new high-throughput assays with existing methods. Malaria Journal 6: 111.
51. Hood GM (2010) PopTools version 3.2.5.
52. Barrett JC, Fry B, Maller J, Daly MJW (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21: 263-265. (Pubitemid 40202029)