A single mutation in the GSTe2 gene allows tracking of metabolically based insecticide resistance in a major malaria vector

Genome Biology

Volumn 15, Issue 2, 2014, Pages

  Riveron, Jacob M ^a   Yunta, Cristina ^a,b   Ibrahim, Sulaiman S ^a   Djouaka, Rousseau ^c   Irving, Helen ^a   Menze, Benjamin D ^a,d   Ismail, Hanafy M ^a   Hemingway, Janet ^a   Ranson, Hilary ^a   Albert, Armando ^b   Wondji, Charles S ^a  

^a LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^b INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

^c INTERNATIONAL INSTITUTE OF TROPICAL AGRICULTURE   (Benin)

^d Organisation Coord Pour Lutte C   (Cameroon)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORPHENOTANE; GLUTATHIONE TRANSFERASE; PERMETHRIN; PYRETHROID;

ADULT; ANOPHELES FUNESTUS; ARTICLE; BINDING SITE; CONTROLLED STUDY; CROSS RESISTANCE; DISEASE CARRIER; DROSOPHILA MELANOGASTER; FEMALE; GENE FLOW; GENE INTERACTION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC MARKER; GENETIC POLYMORPHISM; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; GLUTATHIONE S TRANSFERASE EPSILON 2 GENE; HAPLOTYPE; INSECTICIDE RESISTANCE; MALARIA; METABOLIC ACTIVITY ASSAY; MICROARRAY ANALYSIS; MOLECULAR EVOLUTION; NONHUMAN; POINT MUTATION; POPULATION GENETIC STRUCTURE; RECOMBINANT GENE; STRUCTURE ANALYSIS; TRANSGENIC ANIMAL; UPREGULATION; AFRICA; ALLELE; ANIMAL; ANOPHELES; CHEMISTRY; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MUTATION; TOXICITY; TRANSMISSION; X RAY CRYSTALLOGRAPHY;

ANOPHELES FUNESTUS; DROSOPHILA MELANOGASTER;

AFRICA; ALLELES; ANIMALS; ANOPHELES; CRYSTALLOGRAPHY, X-RAY; DDT; GLUTATHIONE TRANSFERASE; HUMANS; INSECT VECTORS; INSECTICIDE RESISTANCE; MALARIA; MOLECULAR SEQUENCE DATA; MUTATION; PYRETHRINS;

EID: 84904544930     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2014-15-2-r27     Document Type: Article

References (40)

1. World Health Organization: Global Plan for Insecticide Resistance Management (GPIRM). Geneva, Switzerland 2012.
2. Hemingway J, Ranson H: Insecticide resistance in insect vectors of human disease. Annual Review Entomol 2000, 45:369-389.
3. David JP, Strode C, Vontas J, Nikou D, Vaughan A, Pignatelli PM, Louis C, Hemingway J, Ranson H: The Anopheles gambiae detoxification chip: a highly specific microarray to study metabolic-based insecticide resistance in malaria vectors. Proc Natl Acad Sci USA 2005, 102:4080-4084.
4. Muller P, Warr E, Stevenson BJ, Pignatelli PM, Morgan JC, Steven A, Yawson AE, Mitchell SN, Ranson H, Hemingway J, Paine MJ, Donnelly MJ: Field-caught permethrin-resistant Anopheles gambiae overexpress CYP6P3, a P450 that metabolises pyrethroids. PLoS Genet 2008, 4:e1000286.
5. Riveron JM, Irving H, Ndula M, Barnes KG, Ibrahim SS, Paine MJ, Wondji CS: Directionally selected cytochrome P450 alleles are driving the spread of pyrethroid resistance in the major malaria vector Anopheles funestus. Proc Natl Acad Sci USA 2013, 110:252-257.
6. Djouaka R, Irving H, Tukur Z, Wondji CS: Exploring mechanisms of multiple insecticide resistance in a population of the malaria vector Anopheles funestus in Benin. PLoS One 2011, 6:e27760.
7. Ranson H, Rossiter L, Ortelli F, Jensen B, Wang X, Roth CW, Collins FH, Hemingway J: Identification of a novel class of insect glutathione S-transferases involved in resistance to DDT in the malaria vector Anopheles gambiae. Biochem J 2001, 359:295-304.
8. Lumjuan N, Rajatileka S, Changsom D, Wicheer J, Leelapat P, Prapanthadara LA, Somboon P, Lycett G, Ranson H: The role of the Aedes aegypti epsilon glutathione transferases in conferring resistance to DDT and pyrethroid insecticides. Insect Biochem Mol Biol 2011, 41:203-209.
9. Morgan JC, Irving H, Okedi LM, Steven A, Wondji CS: Pyrethroid resistance in an Anopheles funestus population from Uganda. PLoS One 2010, 5:e11872.
10. Ramphul U, Boase T, Bass C, Okedi LM, Donnelly MJ, Muller P: Insecticide resistance and its association with target-site mutations in natural populations of Anopheles gambiae from eastern Uganda. Trans R Soc Trop Med Hyg 2009, 103:1121-1126.
11. Chiu TL, Wen Z, Rupasinghe SG, Schuler MA: Comparative molecular modeling of Anopheles gambiae CYP6Z1, a mosquito P450 capable of metabolizing DDT. Proc Natl Acad Sci USA 2008, 105:8855-8860.
12. Mitchell SN, Stevenson BJ, Muller P, Wilding CS, Egyir-Yawson A, Field SG, Hemingway J, Paine MJ, Ranson H, Donnelly MJ: Identification and validation of a gene causing cross-resistance between insecticide classes in Anopheles gambiae from Ghana. Proc Natl Acad Sci USA 2012, 109:6147-6152.
13. Daborn PJ, Lumb C, Boey A, Wong W, Ffrench-Constant RH, Batterham P: Evaluating the insecticide resistance potential of eight Drosophila melanogaster cytochrome P450 genes by transgenic over-expression. Insect Biochem Mol Biol 2007, 37:512-519.
14. Kostaropoulos I, Papadopoulos AI, Metaxakis A, Boukouvala E, Papadopoulou-Mourkidou E: Glutathione S-transferase in the defence against pyrethroids in insects. Insect Biochem Mol Biol 2001, 31:313-319.
15. Vontas JG, Small GJ, Hemingway J: Glutathione S-transferases as antioxidant defence agents confer pyrethroid resistance in Nilaparvata lugens. Biochem J 2001, 357:65-72.
16. Daborn PJ, Yen JL, Bogwitz MR, Le Goff G, Feil E, Jeffers S, Tijet N, Perry T, Heckel D, Batterham P, Feyereisen R, Wilson TG, ffrench-Constant RH: A single p450 allele associated with insecticide resistance in Drosophila. Science 2002, 297:2253-2256.
17. Campbell PM, Newcomb RD, Russell RJ, Oakeshott JG: Two different amino acid substitutions in the ali-esterase, E3, confer alternative types of organophosphorus insecticide resistance in the sheep blowfly, Lucilia cuprina. Insect Biochem Mol Biol 1998, 28:139-150.
18. Claudianos C, Russell RJ, Oakeshott JG: The same amino acid substitution in orthologous esterases confers organophosphate resistance on the house fly and a blowfly. Insect Biochem Mol Biol 1999, 29:675-686.
19. Okoye PN, Brooke BD, Koekemoer LL, Hunt RH, Coetzee M: Characterisation of DDT, pyrethroid and carbamate resistance in Anopheles funestus from Obuasi, Ghana. Trans R Soc Trop Med Hyg 2008, 102:591-598.
20. Wondji CS, Dabire RK, Tukur Z, Irving H, Djouaka R, Morgan JC: Identification and distribution of a GABA receptor mutation conferring dieldrin resistance in the malaria vector Anopheles funestus in Africa. Insect Biochem Mol Biol 2011, 41:484-491.
21. Cuamba N, Morgan JC, Irving H, Steven A, Wondji CS: High level of pyrethroid resistance in an Anopheles funestus population of the Chokwe District in Mozambique. PLoS One 2010, 5:e11010.
22. Wondji CS, Coleman M, Kleinschmidt I, Mzilahowa T, Irving H, Ndula M, Rehman A, Morgan J, Barnes KG, Hemingway J: Impact of pyrethroid resistance on operational malaria control in Malawi. Proc Natl Acad Sci USA 2012, 109:19063-19070.
23. Huang H, Yao H, Liu JY, Samra AI, Kamita SG, Cornel AJ, Hammock BD: Development of pyrethroid-like fluorescent substrates for glutathione S-transferase. Anal Biochem 2012, 431:77-83.
24. Biswas S, Akey JM: Genomic insights into positive selection. Trends Genet 2006, 22:437-446.
25. Schlenke TA, Begun DJ: Strong selective sweep associated with a transposon insertion in Drosophila simulans. Proc Natl Acad Sci USA 2004, 101:1626-1631.
26. Michel AP, Ingrasci MJ, Schemerhorn BJ, Kern M, Le Goff G, Coetzee M, Elissa N, Fontenille D, Vulule J, Lehmann T, Sagnon N, Costantini C, Besansky NJ: Rangewide population genetic structure of the African malaria vector Anopheles funestus. Mol Ecol 2005, 14:4235-4248.
27. Wang Y, Qiu L, Ranson H, Lumjuan N, Hemingway J, Setzer WN, Meehan EJ, Chen L: Structure of an insect epsilon class glutathione S-transferase from the malaria vector Anopheles gambiae provides an explanation for the high DDT-detoxifying activity. J Struct Biol 2008, 164:228-235.
28. Schmittgen TD, Livak KJ: Analyzing real-time PCR data by the comparative C (T) method. Nat Protoc 2008, 3:1101-1108.
29. Markstein M, Pitsouli C, Villalta C, Celniker SE, Perrimon N: Exploiting position effects and the gypsy retrovirus insulator to engineer precisely expressed transgenes. Nat Genet 2008, 40:476-483.
30. Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22:4673-4680.
31. Rozas J: DNA sequence polymorphism analysis using DnaSP. Methods Mol Biol 2009, 537:337-350.
32. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
33. Clement M, Posada D, Crandall KA: TCS: a computer program to estimate gene genealogies. Mol Ecol 2000, 9:1657-1659.
34. Kwiatkowska RM, Platt N, Poupardin R, Irving H, Dabire RK, Mitchell S, Jones CM, Diabate A, Ranson H, Wondji CS: Dissecting the mechanisms responsible for the multiple insecticide resistance phenotype in Anopheles gambiae s.s., M form, from Vallee du Kou, Burkina Faso. Gene 2013, 519:98-106.
35. Hudson RR, Slatkin M, Maddison WP: Estimation of levels of gene flow from DNA sequence data. Genetics 1992, 132:583-589.
36. Zhang Z, Li J, Zhao XQ, Wang J, Wong GK, Yu J: KaKs_calculator: calculating Ka and Ks through model selection and model averaging. Genomics Proteomics Bioinformatics 2006, 4:259-263.
37. Nei M, Gojobori T: Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 1986, 3:418-426.
38. Kabsch W: Xds. Acta Crystallogr D Biol Crystallogr 2010, 66:125-132.
39. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ: Phaser crystallographic software. J Appl Crystallogr 2007, 40:658-674.
40. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH: PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 2010, 66:213-221.