Using Drosophila melanogaster to validate metabolism-based insecticide resistance from insect pests

Insect Biochemistry and Molecular Biology

Volumn 42, Issue 12, 2012, Pages 918-924

  Daborn, Phillip J ^a   Lumb, Christopher ^a   Harrop, Thomas W R ^a   Blasetti, Alex ^a   Pasricha, Shivani ^a   Morin, Shai ^b   Mitchell, Sara N ^c   Donnelly, Martin J ^c   Müller, Pie ^c,d,e   Batterham, Philip ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^d SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^e UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Carboxylesterase; Cytochrome P450; Glutathione S transferase; Insecticide resistance

Indexed keywords

ANIMAL; ANIMAL MODEL; ANOPHELES GAMBIAE; ARTICLE; DROSOPHILA MELANOGASTER; ENZYMOLOGY; FEMALE; GENE; GENETICS; HEMIPTERA; INSECTICIDE RESISTANCE; MALE; METABOLISM; TRANSGENE; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANOPHELES GAMBIAE; DROSOPHILA MELANOGASTER; FEMALE; GENES, INSECT; HEMIPTERA; INSECTICIDE RESISTANCE; MALE; MODELS, ANIMAL; TRANSGENES;

ALEYRODIDAE; ANOPHELES GAMBIAE; BEMISIA TABACI; CALLIPHORIDAE; DROSOPHILA MELANOGASTER; HEXAPODA; LUCILIA CUPRINA; OVIS ARIES;

EID: 84868474056     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2012.09.003     Document Type: Article

References (56)

1. Bass C., Field L.M. Gene amplification and insecticide resistance. Pest Manag. Sci. 2011, 67:886-890.
2. Bautista M.A., Miyata T., Miura K., Tanaka T. RNA interference-mediated knockdown of a cytochrome P450, CYP6BG1, from the diamondback moth, Plutella xylostella, reduces larval resistance to permethrin. Insect Biochem. Mol. Biol. 2009, 39:38-46.
3. Bischof J., Maeda R.K., Hediger M., Karch F., Basler K. An optimized transgenesis system for Drosophila using germ-line-specific varphiC31 integrases. Proc. Natl. Acad. Sci. U S A 2007, 104:3312-3317.
4. Bogwitz M.R., Chung H., Magoc L., Rigby S., Wong W., O'Keefe M., McKenzie J.A., Batterham P., Daborn P.J. Cyp12a4 confers lufenuron resistance in a natural population of Drosophila melanogaster. Proc. Natl. Acad. Sci. U S A 2005, 102:12807-12812.
5. Campbell P.M., Newcomb R.D., Russell R.J., Oakeshott J.G. 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.
6. Carbone A., Zinovyev A., Kepes F. Codon adaptation index as a measure of dominating codon bias. Bioinformatics 2003, 19:2005-2015.
7. Chung H., Bogwitz M.R., McCart C., Andrianopoulos A., ffrench-Constant R.H., Batterham P., Daborn P.J. Cis-regulatory elements in the Accord retrotransposon result in tissue-specific expression of the Drosophila melanogaster insecticide resistance gene Cyp6g1. Genetics 2007, 175:1071-1077.
8. Claudianos C., Russell R.J., Oakeshott J.G. 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.
9. Daborn P., Boundy S., Yen J., Pittendrigh B., ffrench-Constant R. DDT resistance in Drosophila correlates with Cyp6g1 over-expression and confers cross-resistance to the neonicotinoid imidacloprid. Mol. Genet. Genomics 2001, 266:556-563.
10. Daborn P.J., Yen J.L., Bogwitz M.R., Le Goff G., Feil E., Jeffers S., Tijet N., Perry T., Heckel D., Batterham P., Feyereisen R., Wilson T.G., ffrench-Constant R.H. A single P450 allele associated with insecticide resistance in Drosophila. Science 2002, 297:2253-2256.
11. Daborn P.J., Lumb C., Boey A., Wong W., ffrench-Constant R.H., 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.
12. David J.P., Strode C., Vontas J., Nikou D., Vaughan A., Pignatelli P.M., 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. U S A 2005, 102:4080-4084.
13. Feyereisen R. Arthropod CYPomes illustrate the tempo and mode in P450 evolution. Biochim. Biophys. Acta 2010, 1814:19-28.
14. ffrench-Constant R., Roush R.T., Carino F.A. Drosophila as a tool for investigating the molecular genetics of insecticide resistance. Molecular Approaches to Fundamental and Applied Entomology. Springer Series in Experimental Entomology 1992, 1-37. Springer, New York. J.G. Oakeshott, M.J. Whitten (Eds.).
15. Fonseca-Gonzalez I., Quinones M.L., Lenhart A., Brogdon W.G. Insecticide resistance status of Aedes aegypti (L.) from Colombia. Pest Manag. Sci. 2011, 67:430-437.
16. Grote A., Hiller K., Scheer M., Munch R., Nortemann B., Hempel D.C., Jahn D. JCat: a novel tool to adapt codon usage of a target gene to its potential expression host. Nucleic Acids Res. 2005, 33:W526-W531.
17. Guzov V.M., Unnithan G.C., Chernogolov A.A., Feyereisen R. CYP12A1, a mitochondrial cytochrome P450 from the house fly. Arch. Biochem. Biophys. 1998, 359:231-240.
18. Huvenne H., Smagghe G. Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. J. Insect Physiol. 2010, 56:227-235.
19. Karunker I., Benting J., Lueke B., Ponge T., Nauen R., Roditakis E., Vontas J., Gorman K., Denholm I., Morin S. Over-expression of cytochrome P450 CYP6CM1 is associated with high resistance to imidacloprid in the B and Q biotypes of Bemisia tabaci (Hemiptera: aleyrodidae). Insect Biochem. Mol. Biol. 2008, 38:634-644.
20. Karunker I., Morou E., Nikou D., Nauen R., Sertchook R., Stevenson B.J., Paine M.J., Morin S., Vontas J. Structural model and functional characterization of the Bemisia tabaci CYP6CM1vQ, a cytochrome P450 associated with high levels of imidacloprid resistance. Insect Biochem. Mol. Biol. 2009, 39:697-706.
21. Korytko P.J., MacLntyre R.J., Scott J.G. Expression and activity of a house-fly cytochrome P450, CYP6D1, in Drosophila melanogaster. Insect Mol. Biol. 2000, 9:441-449.
22. Lee T., Luo L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 1999, 22:451-461.
23. Li X., Schuler M.A., Berenbaum M.R. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu. Rev. Entomol. 2007, 52:231-253.
24. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
25. Low W.Y., Ng H.L., Morton C.J., Parker M.W., Batterham P., Robin C. Molecular evolution of glutathione S-transferases in the genus Drosophila. Genetics 2007, 177:1363-1375.
26. Low W.Y., Feil S.C., Ng H.L., Gorman M.A., Morton C.J., Pyke J., McConville M.J., Bieri M., Mok Y.F., Robin C., Gooley P.R., Parker M.W., Batterham P. Recognition and detoxification of the insecticide DDT by Drosophila melanogaster glutathione S-transferase D1. J. Mol. Biol. 2010, 399:358-366.
27. Lumjuan N., McCarroll L., Prapanthadara L.A., Hemingway J., Ranson H. Elevated activity of an Epsilon class glutathione transferase confers DDT resistance in the dengue vector, Aedes aegypti. Insect Biochem. Mol. Biol. 2005, 35:861-871.
28. Lumjuan N., Rajatileka S., Changsom D., Wicheer J., Leelapat P., Prapanthadara L.A., 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.
29. Mao Y.B., Cai W.J., Wang J.W., Hong G.J., Tao X.Y., Wang L.J., Huang Y.P., Chen X.Y. Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat. Biotechnol. 2007, 25:1307-1313.
30. Morton R.A. Evolution of Drosophila insecticide resistance. Genome 1993, 36:1-7.
31. Muller P., Warr E., Stevenson B.J., Pignatelli P.M., Morgan J.C., Steven A., Yawson A.E., Mitchell S.N., Ranson H., Hemingway J., Paine M.J., Donnelly M.J. Field-caught permethrin-resistant Anopheles gambiae overexpress CYP6P3, a P450 that metabolises pyrethroids. PLoS Genet. 2008, 4:e1000286.
32. Nauen R., Denholm I. Resistance of insect pests to neonicotinoid insecticides: current status and future prospects. Arch. Insect Biochem. Physiol. 2005, 58:200-215.
33. Nauen R., Stumpf N., Elbert A. Toxicological and mechanistic studies on neonicotinoid cross resistance in Q-type Bemisia tabaci (Hemiptera: aleyrodidae). Pest Manag. Sci. 2002, 58:868-874.
34. Newcomb R.D., Campbell P.M., Ollis D.L., Cheah E., Russell R.J., Oakeshott J.G. 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 1997, 94:7464-7468.
35. Newcomb R.D., Gleeson D.M., Yong C.G., Russell R.J., Oakeshott J.G. 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. 2005, 60:207-220.
36. Oakeshott J.G., Claudianos C., Campbell P.M., Newcomb R.D., Russell R.J. Biochemical genetics and genomics of insect esterases. Compr. Mol. Insect Science 2005, 309-381. Elservier. L. Gilbert, K. Iatrou, S. Gill (Eds.).
37. Ortelli F., Rossiter L.C., Vontas J., Ranson H., Hemingway J. Heterologous expression of four glutathione transferase genes genetically linked to a major insecticide-resistance locus from the malaria vector Anopheles gambiae. Biochem. J. 2003, 373:957-963.
38. Pedra J.H., McIntyre L.M., Scharf M.E., Pittendrigh B.R. Genome-wide transcription profile of field- and laboratory-selected dichlorodiphenyltrichloroethane (DDT)-resistant Drosophila. Proc. Natl. Acad. Sci. U S A 2004, 101:7034-7039.
39. Perry T., McKenzie J.A., Batterham P. A Dalpha6 knockout strain of Drosophila melanogaster confers a high level of resistance to spinosad. Insect Biochem. Mol. Biol. 2007, 37:184-188.
40. Perry T., Batterham P., Daborn P.J. The biology of insecticidal activity and resistance. Insect Biochem. Mol. Biol. 2011, 41:411-422.
41. Ranson H., Prapanthadara L., Hemingway J. Cloning and characterization of two glutathione S-transferases from a DDT-resistant strain of Anopheles gambiae. Biochem. J. 1997, 324(Pt 1):97-102.
42. Ranson H., Jensen B., Wang X., Prapanthadara L., Hemingway J., Collins F.H. Genetic mapping of two loci affecting DDT resistance in the malaria vector Anopheles gambiae. Insect Mol. Biol. 2000, 9:499-507.
43. Ranson H., Rossiter L., Ortelli F., Jensen B., Wang X., Roth C.W., Collins F.H., 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.
44. Ranson H., Claudianos C., Ortelli F., Abgrall C., Hemingway J., Sharakhova M.V., Unger M.F., Collins F.H., Feyereisen R. Evolution of supergene families associated with insecticide resistance. Science 2002, 298:179-181.
45. Russell R.M., Preisler H.K., Savin N.E., Robertson J.L. Bioassays with Arthropods 2007, CRC Press, Florida. second ed.
46. Sabourault C., Guzov V.M., Koener J.F., Claudianos C., Plapp F.W., Feyereisen R. Overproduction of a P450 that metabolizes diazinon is linked to a loss-of-function in the chromosome 2 ali-esterase (MdalphaE7) gene in resistant house flies. Insect Mol. Biol. 2001, 10:609-618.
47. Sakuma M. Probit analysis of preference data. Appl. Entomol. Zool. 1998, 33:339-347.
48. Schmidt J.M., Good R.T., Appleton B., Lydall J., Raymant G.C., Bogwitz M.R., Martin J., Fair J., Daborn P.J., Goddard M., Batterham P., Robin C. Copy number variation and transposable elements feature in recent, ongoing adaptation at the Cyp6g1 locus. PLoS Genet. 2010, 6:e1000998.
49. Smyth K.A., Boyce T.M., Russell R.J., Oakeshott J.G. MCE activities and malathion resistances in field populations of the Australian sheep blowfly (Lucilia cuprina). Heredity 2000, 84(Pt 1):63-72.
50. Stevenson B.J., Bibby J., Pignatelli P., Muangnoicharoen S., O'Neill P.M., Lian L.Y., Muller P., Nikou D., Steven A., Hemingway J., Sutcliffe M.J., Paine M.J. Cytochrome P450 6M2 from the malaria vector Anopheles gambiae metabolizes pyrethroids: sequential metabolism of deltamethrin revealed. Insect Biochem. Mol. Biol. 2011, 41:492-502.
51. Strode C., Wondji C.S., David J.P., Hawkes N.J., Lumjuan N., Nelson D.R., Drane D.R., Karunaratne S.H., Hemingway J., Black W.C.t., Ranson H. Genomic analysis of detoxification genes in the mosquito Aedes aegypti. Insect Biochem. Mol. Biol. 2008, 38:113-123.
52. Vontas J., David J.P., Nikou D., Hemingway J., Christophides G.K., Louis C., Ranson H. Transcriptional analysis of insecticide resistance in Anopheles stephensi using cross-species microarray hybridization. Insect Mol. Biol. 2007, 16:315-324.
53. Wang J., Kean L., Yang J., Allan A.K., Davies S.A., Herzyk P., Dow J.A. Function-informed transcriptome analysis of Drosophila renal tubule. Genome Biol. 2004, 5:R69.
54. Wang Y., Qiu L., Ranson H., Lumjuan N., Hemingway J., Setzer W.N., Meehan E.J., 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.
55. Williams R.T. Detoxification Mechanisms 1959, J. Wiley and Sons, NewYork.
56. Zhu F., Parthasarathy R., Bai H., Woithe K., Kaussmann M., Nauen R., Harrison D.A., Palli S.R. A brain-specific cytochrome P450 responsible for the majority of deltamethrin resistance in the QTC279 strain of Tribolium castaneum. Proc. Natl. Acad. Sci. U S A 2010, 107:8557-8562.