Use of isogenic strains indicates CYP9M10 is linked to permethrin resistance in Culex pipiens quinquefasciatus

Insect Molecular Biology

Volumn 19, Issue 6, 2010, Pages 717-726

  Hardstone, M C ^a   Komagata, O ^b   Kasai, S ^b   Tomita, T ^b   Scott, J G ^a  

^a Department of Molecular Biology and Genetics   (United States)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

cytochrome P450; Insecta; insecticide resistance; mosquito

Indexed keywords

CYTOCHROME B5; CYTOCHROME P450; PERMETHRIN;

ANIMAL; ARTICLE; COMPARATIVE STUDY; CULEX; GENE; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENETICS; GENOTYPE; INSECTICIDE RESISTANCE; LARVA; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SEQUENCE ALIGNMENT;

ANIMALS; BASE SEQUENCE; CULEX; CYTOCHROME P-450 ENZYME SYSTEM; CYTOCHROMES B5; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE FREQUENCY; GENES, INSECT; GENOTYPE; INSECTICIDE RESISTANCE; LARVA; MOLECULAR SEQUENCE DATA; PERMETHRIN; SEQUENCE ALIGNMENT;

CULEX PIPIENS; CULEX PIPIENS QUINQUEFASCIATUS; INSECTA;

EID: 78449297923     PISSN: 09621075     EISSN: 13652583     Source Type: Journal    
DOI: 10.1111/j.1365-2583.2010.01030.x     Document Type: Article

References (54)

1. Amenya, D.A., Naguran, R., Lo, T.-C.M., Ranson, H., Spillings, B.L., Wood, O.R., et al. (2008) Over expression of a cytochrome P450 (CYP6P9) in a major African malaria vector, Anopheles funestus, resistant to pyrethroids. Insect Molec Biol 17: 19 - 25.
2. Amichot, M., Tares, S., Brun-Barale, A., Arthaud, L., Bride, J., and, Berge, J., (2004) Point mutations associated with insecticide resistance in the Drosophila cytochrome P450 Cyp6a2 enable DDT metabolism. Eur J Biochem 271: 1250 - 1257.
3. Amin, A.M., and, Hemingway, J., (1989) Preliminary investigation of the mechanisms of DDT and pyrethroid resistance in Culex quinquefasciatus Say (Diptera: Culicidae) from Saudi Arabia. Bull Ent Res 79: 361 - 366.
4. Berticat, C., Boquien, G., Raymond, M., and, Chevillon, C., (2002) Insecticide resistance genes induce a mating competition cost in Culex pipiens mosquitoes. Genet Res Camb 79: 41 - 47.
5. Bogwitz, M.R., Chung, H., Magoc, L., Rigby, S., Wong, W., O'Keefe, M., et al. (2005) Cyp12a4 confers lufenuron resistance in a natural population of Drosophila melanogaster. PNAS 102: 12807 - 12812.
6. Bradford, M.M., (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochem 72: 248 - 254.
7. Carino, F.A., Koener, J.F., Plapp, F.W. Jr, and, Feyereisen, R., (1994) Constitutive overexpression of the cytochrome P450 gene CYP6A1 in a house fly strain with metabolic resistance to insecticides. Insect Biochem 24: 411 - 418.
8. Chang, T.K.H., Chen, J., Pillay, V., Ho, J.-Y., and, Bandiera, S.M., (2003) Real-time polymerase chain reaction analysis of CYP1B1 gene expression in human liver. Toxiol Sci 71: 11 - 19.
9. Chiu, T.-L., Wen, Z., Rupasinghe, S., and, Schuler, M., (2008) Comparative molecular modeling of Anopheles gambiae CYP6Z1, a mosquito P450 capable of metabolizing DDT. Proc Natl Acad Sci USA 105: 8855 - 8860.
10. Daborn, P., Boundy, S., Yen, J., Pittendrigh, B., and, Ffrench-Constant, R., (2001) DDT Resistance in Drosophila correlates with Cyp6g1 over-expression and confers cross-resistance to the neonicotinoid imidacloprid. Mol Genet Genomics 266: 556 - 563.
11. Daborn, P.J., Lumb, C., Boey, A., Wong, W., Ffrench-Constant, R.H., and, Batterham, P., (2007) Evaluating the insecticide resistance potential of eight Drosophila melanogaster cytochrome P450 genes by transgenic over-expression. Insect Biochem Molec Biol 37: 512 - 519.
12. David, J.-P., Strode, C., Vontas, J., Nikou, D., Vaughan, A., Pignatelli, P.M., et al. (2005) The Anopheles gambiae detoxification chip: A highly specific microarray to study metabolic-based insecticide resistance in malaria vectors. Proc Natl Acad Sci USA 102: 4080 - 4084.
13. Djouaka, R., Bakare, A., Coulibaly, O., Akogbeto, M., Ranson, H., Hemingway, J., et al. (2008a) Expression of the cytochrome P450s, CYP6P3 and CYP6M2 are significantly elevated in multiple pyrethroid resistant populations is Anopheles gambiae s.s. from Southern Benin and Nigeria. BMC Genomics 9: 538 - 547.
14. Djouaka, R.F., Bakare, A.A., Coulibaly, O.N., Akogbeto, M.C., Ranson, H., Hemingway, J., et al. (2008b) Expression of the cytochrome P450s, CYP6P3 and CYP6M2 are significantly elevated in multiple pyrethroid resistant populations of Anopheles gambiae s.s. from Benin and Nigeria. BMC Genomics 9: 538.
15. Georghiou, G.P., Metcalf, R.L., and, Gidden, F.E., (1966) Carbamate resistance in mosquitoes. Selection of Culex pipiens fatigans Weidemann for resistance to Baygon. Bull World Health Org 35: 691 - 708.
16. Ghanim, M., and, Kontsedalov, S., (2007) Gene expression in pyriproxyfen-resistant Bemisia tabaci Q biotype. Pest Manag Sci 63: 776 - 783.
17. Gong, M.-Q., Gu, Y., Hu, X.-B., Sun, Y., Ma, L., Li, X.-L., et al. (2005) Cloning and overexpression of CYP6F1, a cytochrome P450 gene, from deltamethrin-resistant Culex pipiens pallens. Acta Biochim Biophys Sinica 37: 317 - 326.
18. Hardstone, M.C., (2009) Cytochrome P450 monooxygenase-mediated resistance in the southern house mosquito: characterization, genetics and fitness. PhD Thesis, Cornell University, Ithaca, NY.
19. Hardstone, M.C., Leichter, C.A., Harrington, L.C., Kasai, S., Tomita, T., and, Scott, J.G., (2007) Cytochrome P450 monooxygenase-mediated permethrin resistance confers limited and larval specific cross-resistance in the southern house mosquito, Culex pipiens quinquefasciatus. Pestic Biochem Physiol 89: 175 - 184.
20. Hardstone, M.C., Lazzaro, B.P., and, Scott, J.G., (2009) The effect of three environmental conditions on the fitness of cytochrome P450 monooxygenase-mediated permethrin resistance in Culex pipiens quinquefasciatus. BMC Evol Biol 9: 42.
21. Hardstone, M.C., Huang, X., Harrington, L.C., and, Scott, J.G., (2010) Differences in development, glycogen and lipid content associated with cytochrome P450-mediated permethrin resistance in Culex pipiens quinquefasciatus (Diptera: Culicidae). J Med Entomol 47: 188 - 198.
22. Kamiya, E., Yamakawa, M., Shono, T., and, Kono, Y., (2001) Molecular cloning, nucleotide sequences and gene expression of new cytochrome P450s (CYP6A24, CYP6D3v2) from the pyrethroid resistant housefly, Musca domestica L. (Diptera: Muscidae). Appl Entomol Zool 36: 225 - 229.
23. Karunker, I., Benting, J., Lueke, B., Ponge, T., Nauen, R., Roditakis, E., et al. (2008) 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 Molec Biol 38: 634 - 644.
24. Kasai, S., and, Scott, J.G., (2000) Overexpression of cytochrome P450 CYP6D1 is associated with monooxygenase-mediated pyrethroid resistance in house flies from Georgia. Pestic Biochem Physiol 68: 34 - 41.
25. Kasai, S., Weerashinghe, I.S., and, Shono, T., (1998) P450 monooxygenases are an important mechanism of permethrin resistance in Culex quinquefasciatus Say larvae. Arch Insect Biochem Physiol 37: 47 - 56.
26. Kasai, S., Weerashinghe, I.S., Shono, T., and, Yamakawa, M., (2000) Molecular cloning, nucleotide sequence and gene expression of a cytochrome P450 (CYP6F1) from the pyrethroid-resistant mosquito, Culex quinquefasciatus Say. Insect Biochem Mol Biol 30: 163 - 171.
27. Komagata, O., Kasai, S., and, Tomita, T., (2010) Overexpression of cytochrome P450 genes in pyrethroid-resistant Culex quinquefasciatus. Insect Biochem Mol Biol 40: 146 - 152.
28. Lee, S.S.T., and, Scott, J.G., (1989) An improved method for preparation, stabilization and storage of house fly (Diptera: Muscidae) microsomes. J Econ Entomol 82: 1559 - 1563.
29. coh substrate specificity by mutation of a single amino-acid residue. Nature 339: 632 - 634.
30. 5, P450 reductase and monooxygenase activities in LPR house flies, Musca domestica. Biochem Genet 34: 133 - 148.
31. Liu, N., and, Scott, J.G., (1997) Phenobarbital induction of CYP6D1 is due to a trans acting factor on autosome 2 in house flies, Musca domestica. Insect Molec Biol 6: 77 - 81.
32. Liu, N., and, Scott, J.G., (1998) Increased transcription of CYP6D1 causes cytochrome P450-mediated insecticide resistance in house fly. Insect Biochem Molec Biol 28: 531 - 535.
33. Ct method. Methods 25: 402 - 408.
34. Lowe, B., Avila, H.A., Bloom, F.R., Gleeson, M., and, Kusser, W., (2003) Quantitation of gene expression in neural precursors by reverse-transcription polymerase chain reaction using self-quenched, fluorogenic primers. Anal Biochem 315: 95 - 105.
35. Muller, P., Warr, E., Stevenson, B.J., Pignatelli, P.M., Morgan, J.C., Steven, A., et al. (2008) Field-caught permethrin-resistant Anopheles gambiae overexpresses CYP6P3, a P450 that metabolises pyrethroids. PLoS Genet 4: e1000286.
36. Nikou, D., Ranson, H., and, Hemingway, J., (2003) An adult-specific CYP6 P450 gene is overexpressed in a pyrethroid-resistant strain of the malaria vector, Anopheles gambiae. Gene 318: 91 - 102.
37. Omura, T., and, Sato, R., (1964) The carbon monoxide-binding pigment of liver microsomes: I. Evidence for its hemoprotein nature. J Biol Chem 239: 2370 - 2378.
38. Paton, M.G., Karunaratne, S.H.P.P., Giakoumaki, E., Roberts, N., and, Hemingway, J., (2000) Quantitative analysis of gene amplification in insecticide-resistant Culex mosquitoes. Biochem J 346: 17 - 24.
39. Rees, C.B., and, Li, W., (2004) Development and application of a real-time quantitative PCR assay for determining CYP1A transcripts in three genera of salmonids. Aquatic Toxicol 66: 357 - 368.
40. Sasabe, M., Wen, Z., Berenbaum, M.R., and, Schuler, M.A., (2004) Molecular analysis of CYP321A1, a novel cytochrome P450 involved in metabolism of plant allelochemicals (furanocoumarins) and insecticides (cypermethrin) in Helicoverpa zea. Gene 338: 163 - 175.
41. Scott, J.G., (1990) Investigating mechanisms of insecticide resistance: methods, strategies and pitfalls. In Pesticide Resistance in Arthropods (, Roush, R.T., and, Tabashnik, B., eds), pp. 39 - 57. Chapman and Hall, New York.
42. Scott, J.G., (1999) Cytochromes P450 and insecticide resistance. Insect Biochem Mol Biol 29: 757 - 777.
43. Scott, J.G., and, Lee, S.S.T., (1993) Purification and characterization of a cytochrome P-450 from insecticide susceptible and resistant strains of house fly, Musca domestica L. Arch Insect Biochem Physiol 24: 1 - 19.
44. Strode, C., Wondji, C.S., David, J.P., Hawkes, N.J., Lumjuan, N., Nelson, D.R., et al. (2008) Genomic analysis of detoxification genes in the mosquito Aedes aegypti. Insect Biochem Mol Biol 38: 113 - 123.
45. Tomita, T., and, Scott, J.G., (1995) cDNA and deduced protein sequence of CYP6D1: the putative gene for a cytochrome P450 responsible for pyrethroid resistance in house fly. Insect Biochem Molec Biol 25: 275 - 283.
46. Tomita, T., Liu, N., Smith, F.F., Sridhar, P., and, Scott, J.G., (1995) Molecular mechanisms involved in increased expression of a cytochrome P450 responsible for pyrethroid resistance in the housefly, Musca domestica. Insect Molec Biol 4: 135 - 140.
47. Wang, Y., Zolfaghari, R., and, Ross, A.C., (2002) Cloning of rat cytochrome P450RA1 (CYP26) cDNA and regulation of its gene expression by all-trans-retinoic acid in vivo. Arch Biochem Biophysics 401: 235 - 243.
48. Waters, L.C., Zelhof, A.C., Shaw, B.J., and, Ch'ang, L.Y., (1992) Possible involvement of the long terminal repeat of transposable element 17.6 in regulating expression of an insecticide resistance-associated P450 gene in Drosophila. Proc Natl Acad Sci USA 89: 4855 - 4859.
49. Wheelock, C.E., Shan, G., and, Ottea, J., (2005) Overview of carboxylesterases and their role in the metabolism of insecticides. J Pestic Sci 30: 75 - 83.
50. Wheelock, G.D., and, Scott, J.G., (1990) Immunological detection of cytochrome P450 from insecticide resistant and susceptible house flies (Musca domestica). Pestic Biochem Physiol 38: 130 - 139.
51. Wondji, C., Irving, H., Morgan, J., Lobo, N., Collins, F., Hunt, R., et al. (2009) Two duplicated P450 genes are associated with pyrethroid resistance in Anopheles funestus, a major malaria vector. Genome Res 19: 452 - 459.
52. Zhu, F., and, Liu, N., (2008) Differential expression of CYP6A5 and CYP6A5v2 in pyrethroid-resistant house flies, Musca domestica. Arch Insect Biochem Physiol 67: 107 - 119.
53. Zhu, F., Li, T., Zhang, L., and, Liu, N., (2008) Co-up-regulation of three P450 genes in response to permethrin exposure in permethrin resistant house flies, Musca domestica. BMC Physiol 8: 18 - 30.
54. Zhu, Y.C., and, Snodgrass, G.L., (2003) Cytochrome P450 CYP6X1 cDNAs and mRNA expression levels in three strains of the tarnished plant bug Lygus lineolaris (Heteroptera: Miridae) having different susceptibilities to pyrethroid insecticide. Insect Molec Biol 12: 39 - 49.