Mosquito-borne diseases, the most well known of which is malaria, are among the leading causes of human deaths worldwide. Vector control is a very important part of the global strategy for management of mosquito-associated diseases, and insecticide application is the most important component in this effort. However, mosquito-borne diseases are now resurgent, largely because of the insecticide resistance that has developed in mosquito vectors and the drug resistance of pathogens. A large number of studies have shown that multiple, complex resistance mechanisms—in particular, increased metabolic detoxification of insecticides and decreased sensitivity of the target proteins—or genes are likely responsible for insecticide resistance. Gene overexpression and amplification, and mutations in protein-coding-gene regions, have frequently been implicated as well. However, no comprehensive understanding of the resistance mechanisms or regulation involved has yet been developed. This article reviews current knowledge of the molecular mechanisms, genes, gene interactions, and gene regulation governing the development of insecticide resistance in mosquitoes and discusses the potential impact of the latest research findings on the basic and practical aspects of mosquito resistance research.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Alon M, Alon F, Nauen R, Morin S. 1.  2008. Organophosphates' resistance in the B-biotype of Bemisia tabaci (Hemiptera: Aleyrodidae) is associated with a point mutation in an ace1-type acetylcholinesterase and overexpression of carboxylesterase. Insect Biochem. Mol. Biol. 38:940–49 [Google Scholar]
  2. Alout H, Djogbénou L, Berticat C, Chandre F, Weill M. 2.  2008. Comparison of Anopheles gambiae and Culex pipiens acetycholinesterase 1 biochemical properties. Comp. Biochem. Physiol. B 150:271–77 [Google Scholar]
  3. Alout H, Weill M. 3.  2008. Amino-acid substitutions in acetylcholinesterase 1 involved in insecticide resistance in mosquitoes. Chem. Biol. Int. 175:138–41 [Google Scholar]
  4. Amenya DA, Naguran R, Lo T-CM, Ranson H, Spillings BL. 4.  et al. 2008. Over expression of a cytochrome P450 (CYP6P9) in a major African malaria vector, Anopheles Funestus, resistant to pyrethroids. Insect Mol. Biol. 17:19–25 [Google Scholar]
  5. Anazawa Y, Tomita T, Aiki Y, Kozaki T, Kono Y. 5.  2003. Sequence of a cDNA encoding acetylcholinesterase from susceptible and resistant two-spotted spider mite, Tetranychus urticae. Insect Biochem. Mol. Biol. 33:509–14 [Google Scholar]
  6. Arensburger P, Megy K, Waterhouse RM, Abrudan J, Amedeo P. 6.  et al. 2010. Sequencing of Culex quinquefasciatus establishes a platform for mosquito comparative genomics. Science 330:86–88 [Google Scholar]
  7. Bariami V, Jones CM, Poupardin R, Vontas J, Ranson H. 7.  2012. Gene amplification, ABC transporters and cytochrome P450s: unraveling the molecular basis of pyrethroid resistance in the dengue vector, Aedes aegypti. PLOS Negl. Trop. Dis. 6:e1692 [Google Scholar]
  8. Berenbaum MR. 8.  1991. Coumarins. Herbivores: Their Interaction with Secondary Plant Metabolites GA Rosenthal, MR Berenbaum 221–49 New York: Academic [Google Scholar]
  9. Blättler SM, Rencurel F, Kaufmann MR, Meyer UA. 9.  2007. In the regulation of cytochrome P450 genes, phenobarbital targets LKB1 for necessary activation of AMP-activated protein kinase. Proc. Natl. Acad. Sci. USA 104:1045–50 [Google Scholar]
  10. Bloomquist JR. 10.  2003. Chloride channels as tools for developing selective insecticides. Insect Biochem. Physiol. 54:145–56 [Google Scholar]
  11. Boonsuepsakul S, Luepromchai E, Rongnoparut P. 11.  2008. Characterization of Anopheles minimus CYP6AA3 expressed in a recombinant baculovirus system. Arch. Insect Biochem. Physiol. 69:13–21 [Google Scholar]
  12. Brogdon WG, McAllister JC, Corwin AM, Cordon-Rosales C. 12.  1999. Independent selection of multiple mechanisms for pyrethroid resistance in Guatemalan Anopheles albimanus (Diptera: Culicidae). J. Econ. Entomol. 92:298–302 [Google Scholar]
  13. Brown RP, Berenbaum MR, Schuler MA. 13.  2004. Transcription of a lepidopteran cytochrome P450 promoter is modulated by multiple elements in its 5′ UTR and repressed by 20-hydroxyecdysone. Insect Mol. Biol. 13:337–47 [Google Scholar]
  14. Butler D. 14.  2011. Mosquitoes score in chemical war. Nature 475:19 [Google Scholar]
  15. Carino FA, Koener JF, Plapp FW Jr, Feyereisen R. 15.  1994. Constitutive overexpression of the cytochrome P450 gene CYP6A1 in a house fly strain with metabolic resistance to insecticides. Insect Biochem. Mol. Biol. 24:411–18 [Google Scholar]
  16. Casida JE, Durkin KA. 16.  2013. Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annu. Rev. Entomol. 58:99–117 [Google Scholar]
  17. Casimiro S, Coleman M, Mohloai P, Hemingway J, Sharp B. 17.  2006. Insecticide resistance in Anopheles funestus (Diptera: Culicidae) from Mozambique. J. Med. Entomol. 43:267–75 [Google Scholar]
  18. 18. Cent. Dis. Control Prev. (CDC) 2013. CDC releases final West Nile virus national surveillance data for 2012. Media Advis., May 13, Cent. Dis. Control Prev., Atlanta, GA
  19. Chang C, Shen WK, Wang T-T, Lin Y-H, Hsu E-L. 19.  et al. 2009. A novel amino acid substitution in a voltage-gated sodium channel is associated with knockdown resistance to permethrin in Aedes aegypti. Insect Biochem. Mol. Biol. 39:272–78 [Google Scholar]
  20. Chiu TL, Wen Z, Rupasinghe SG, Schuler MA. 20.  2008. Comparative molecular modeling of Anopheles gambiae CYP6Z1, a mosquito P450 capable of metabolizing DDT. Proc. Natl. Acad. Sci. USA 105:8855–60 [Google Scholar]
  21. Cole LM, Nicholson RT, Casida JE. 21.  1993. Action of phenylpyrazole insecticides at the GABA-gated chloride channel. Pestic. Biochem. Physiol 46:47–54 [Google Scholar]
  22. Cole LM, Roush TT, Casida JE. 22.  1995. Drosophila GABA-gated chloride channel: modified [3H]EBOB binding site associated with Ala → Ser or Gly mutants of Rdl subunit. Life Sci 56:757–65 [Google Scholar]
  23. Coetzee M,, Koekemoer LL. 23.  2013. Molecular systematics and insecticide resistance in the major African malaria vector Anopheles funestus. Annu. Rev. Entomol. 58:393–412 [Google Scholar]
  24. Cuamba N, Morgan JC, Irving H, Steven A, Wondji CS. 24.  2010. High level of pyrethroid resistance in an Anopheles funestus population of the Chokwe District in Mozambique. PLOS ONE 5:e11010 [Google Scholar]
  25. Daborn PJ, Lumb C, Harrop TWR, Blasetti A, Pasricha S. 25.  et al. 2012. Using Drosophila melanogaster to validate metabolism-based insecticide resistance from insect pets. Insect Biochem. Mol. Biol. 42:918–24 [Google Scholar]
  26. Davari B, Vatandoost H, Oshaghi MA, Ladonni H, Enayati AA. 26.  et al. 2007. Selection of Anopheles stephensi with DDT and dieldrin and cross-resistance spectrum to pyrethroids and fipronil. Pestic. Biochem. Physiol. 89:97–103 [Google Scholar]
  27. David JP, Faucon F, Chandor-Proust A, Poupardin R, Riaz MA. 27.  et al. 2014. Comparative analysis of response to selection with three insecticides in the dengue mosquito Aedes aegypti using mRNA sequencing. BMC Genomics 15:174 [Google Scholar]
  28. David JP, Strode C, Vontas J, Nikou D, Vaughan A. 28.  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 102:4080–84 [Google Scholar]
  29. Davies TGE, Field LM, Usherwood PNR, Williamson MS. 29.  2007. DDT, pyrethrins, pyrethroids and insect sodium channels. IUBMB Life 59:151–62 [Google Scholar]
  30. Deb S, Bandiera SM. 30.  2011. Regulation of cytochrome P450 1B1 expression by luteinizing hormone in mouse MA-10 and rat R2C Leydig cells: role of protein kinase A. Biol. Reprod. 85:89–96 [Google Scholar]
  31. Dimopoulos G, Casavant TL, Chang S, Scheetz T, Roberts C. 31.  et al. 2000. Anopheles gambiae pilot gene discovery project: identification of mosquito innate immunity genes from expressed sequence tags generated from immune-competent cell lines. Proc. Natl. Acad. Sci. USA 97:6619–24 [Google Scholar]
  32. Ding Y, Ortelli F, Rossiter LC, Hemingway J, Ranson H. 32.  2003. The Anopheles gambiae glutathione transferase supergene family: annotation, phylogeny and expression profiles. BMC Genomics 4:35 [Google Scholar]
  33. Djouaka RF, Bakare AA, Coulibaly ON, Akogbeto MC, Ranson H. 33.  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 9:538 [Google Scholar]
  34. Dong K. 34.  2007. Insect sodium channels and insecticide resistance. Invert. Neurosci. 7:17–30 [Google Scholar]
  35. Dorsam RT, Gutkind JS. 35.  2007. G-protein-coupled receptors and cancer. Nat. Rev. Cancer 7:79–94 [Google Scholar]
  36. Du W, Awolola TS, Howell P, Koekemoer LL, Brooke BD. 36.  et al. 2005. Independent mutations in the Rdl locus confer dieldrin resistance to Anopheles gambiae and An. arabiensis. Insect Mol. Biol. 14:179–83 [Google Scholar]
  37. Du Y, Nomura Y, Satar G, Hu Z, Nauen R. 37.  et al. 2013. Molecular evidence for dual pyrethroid receptor sites on a mosquito sodium channel. Proc. Natl. Acad. Sci. USA 110:11785–90 [Google Scholar]
  38. Duangkaew P, Pethuan S, Kaewpa D, Boonsuepsakul S, Sarapusit S, Rongnoparut P. 38.  2011. Characterization of mosquito CYP6P7 and CYP6AA3: differences in substrate preference and kinetic properties. Arch. Insect Biochem. Physiol. 76:236–48 [Google Scholar]
  39. Enayati AA, Vatandoost H, Ladonni H, Townson H, Hemingway J. 39.  2003. Molecular evidence for a kdr-like pyrethroid resistance mechanism in the malaria vector mosquito Anopheles stephensi. Med. Vet. Entomol. 17:138–44 [Google Scholar]
  40. Feenstra KA, Starikov EB, Urlacher VB, Commandeur JN, Vermeulen NP. 40.  2007. Combining substrate dynamics, binding statistics, and energy barriers to rationalize regioselective hydroxylation of octane and lauric acid by CYP102A1 and mutants. Protein Sci. 16:420–31 [Google Scholar]
  41. Feyereisen R. 41.  2005. Insect cytochrome P450. Comprehensive Molecular Insect Science LI Gilbert, K Iatrou, SS Gill 41–77 Amsterdam, Neth.: Elsevier BV [Google Scholar]
  42. ffrench-Constant RH, Anthony N, Aronstein K, Rocheleau T, Stilwell G. 42.  2000. Cyclodiene insecticide resistance: from molecular to population genetics. Annu. Rev. Entomol. 45:449–66 [Google Scholar]
  43. ffrench-Constant RH, Rocheleau TA, Steichen JC, Chalmers AE. 43.  1993. A point mutation in a Drosophila GABA receptor confers insecticide resistance. Nature 363:449–51 [Google Scholar]
  44. Gjullen CM, Peters RF. 44.  1952. Recent studies of mosquito resistance to insecticides in California. Mosq. News 12:1–7 [Google Scholar]
  45. Gong MQ, Gu Y, Hu XB, Sun Y, Ma L. 45.  et al. 2005. Cloning and overexpression of CYP6F1, a cytochrome P450 gene, from deltamethrin-resistant Culex pipiens pallens. Acta Biochim. Biophys. Sin. 37:317–26 [Google Scholar]
  46. Gotoh O. 46.  1992. Substrate recognition sites in cytochrome P450 family 2 (CYP2) proteins inferred from comparative analyses of amino acid and coding nucleotide sequences. J. Biol. Chem. 267:83–90 [Google Scholar]
  47. Grant DF, Hammock BD. 47.  1992. Genetic and molecular evidence for a trans-acting regulatory locus controlling glutathione S-tranferase-2 expression in Aedes aegypti. Mol. Gen. Genet. 234:169–76 [Google Scholar]
  48. Gunasekaran K, Muthukumaravel S, Sahu SS, Vijayakumar T, Jambulingam P. 48.  2011. Glutathione S transferase activity in Indian vectors of malaria: a defense mechanism against DDT. J. Med. Entomol. 48:561–69 [Google Scholar]
  49. Gupta SK, Majumdar S, Bhattacharya TK, Ghosh TC. 49.  2000. Studies on the relationships between the synonymous codon usage and protein secondary structural units. Biochem. Biophys. Res. Commun. 269:692–96 [Google Scholar]
  50. Hemingway J, Field L, Vontas J. 50.  2002. An overview of insecticide resistance. Science 298:96–97 [Google Scholar]
  51. Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R. 51.  et al. 2002. The genome sequence of the malaria mosquito Anopheles gambiae. Science 298:129–49 [Google Scholar]
  52. Hsu MH, Savas Ü, Lasker JM, Johson EF. 52.  2011. Genistein, resveratrol, and 5-aminoimidazole-4-carboxamide-1-β-D-ribofuranoside induce cytochrome P450 4F2 expression through an AMP-activated protein kinase-dependent pathway. J. Pharmacol. Exp. Ther. 337:125–136 [Google Scholar]
  53. Irving H, Riveron JM, Ibrahim SS, Lobo NF, Wondji CS. 53.  2012. Positional cloning of rp2 QTL associates the P450 genes CYP6Z1, CYP6Z3 and CYP6M7 with pyrethroid resistance in the malaria vector Anopheles funestus. Heredity 109:383–92 [Google Scholar]
  54. Itokawa K, Komagata O, Kasai S, Okamura Y, Masada M. 54.  et al. 2010. Genomic structures of Cyp9m10 in pyrethroid resistant and susceptible strains of Culex quinquefasciatus. Insect Biochem. Mol. Biol. 40:631–40 [Google Scholar]
  55. Jones CM, Liyanapathirana M, Agossa FR, Weetman D, Ranson H. 55.  et al. 2012. Footprints of positive selection associated with a mutation (N1575Y) in the voltage-gated sodium channel of Anopheles gambiae. Proc. Natl. Acad. Sci. USA 109:6614–19 [Google Scholar]
  56. Kasai S, Shono T, Yamakawa M. 56.  1998. Molecular cloning and nucleotide sequence of a cytochrome P450 cDNA from a pyrethroid-resistant mosquito, Culex quinquefasciatus Say. Insect Mol. Biol. 7:185–90 [Google Scholar]
  57. Kasai S, Weerashinghe IS, Shono T. 57.  1998. P450 monooxygenases are an important mechanism of permethrin resistance in Culex quinquefasciatus Say larvae. Arch. Insect Biochem. Physiol. 37:47–56 [Google Scholar]
  58. Kelvin AA. 58.  2011. Outbreak of Chikungunya in the Republic of Congo and the global picture. J. Infect. Dev. Ctries. 5:441–44 [Google Scholar]
  59. Ketterman AJ, Saisawang C, Wongsantichon J. 59.  2011. Insect glutathione transferases. Drug Metab. Rev. 43:253–65 [Google Scholar]
  60. Kimchi-Sarfaty C, Oh JM, Kim IW, Sauna ZE, Calcagno AM. 60.  et al. 2007. A “silent” polymorphism in the MDR1 gene changes substrate specificity. Science 315:525–28 [Google Scholar]
  61. Knipple DC, Doyle KE, Marsella-Herrick PA, Soderlund DM. 61.  1991. Tight genetic linkage between the kdr insecticide resistance trait and a voltage-sensitive sodium channel gene in the house fly. Proc. Natl. Acad. Sci. USA 91:2483–87 [Google Scholar]
  62. Lagerstrom MC, Schioth HB. 62.  2008. Structural diversity of G protein-coupled receptors and significance for drug discovery. Nat. Rev. Drug Discov. 7:339–57 [Google Scholar]
  63. Lertkiatmongkol P, Jenwitheesuk E, Rongnoparut P. 63.  2011. Homology modeling of mosquito cytochrome P450 enzymes involved in pyrethroid metabolism: insights into differences in substrate selectivity. BMC Res. Notes 4:321 [Google Scholar]
  64. Li M, Reid WR, Zhang L, Scott JG, Gao X. 64.  et al. 2013. A whole transcriptiomal linkage analysis of gene co-regulation in insecticide resistant house flies, Musca domestica. BMC Genomics 14:803 [Google Scholar]
  65. Li T, Liu L, Zhang L, Liu N. 65.  2014. Role of G-protein-coupled receptor-related genes in insecticide resistance of the mosquito, Culex quinquefasciatus. Sci. Rep. 4:6474 [Google Scholar]
  66. Li T, Liu N. 66.  2010. Genetics and inheritance of permethrin resistance in the mosquito Culex quinquefasciatus. J. Med. Entomol. 47:1127–34 [Google Scholar]
  67. Li T, Zhang L, Reid WR, Xu Q, Dong K, Liu N. 67.  2012. Multiple mutations and mutation combinations in the sodium channel of permethrin resistant mosquitoes, Culex quinquefasciatus. Sci. Rep. 2:781 [Google Scholar]
  68. Li X, Schuler MA, Berenbaum MR. 68.  2007. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu. Rev. Entomol. 52:231–53 [Google Scholar]
  69. Liu H, Cupp EW, Micher KM, Guo A, Liu N. 69.  2004. Insecticide resistance and cross-resistance in Alabama and Florida strains of Culex quinquefasciatus. J. Med. Entomol. 41:408–13 [Google Scholar]
  70. Liu H, Xu Q, Zhang L, Liu N. 70.  2005. Chlorpyrifos resistance in the mosquito Culex quinquefasciatus. J. Med. Entomol. 42:815–20 [Google Scholar]
  71. Liu N, Li T, Reid WR, Yang T, Zhang L. 71.  2011. Multiple cytochrome P450 genes: their constitutive overexpression and permethrin induction in insecticide resistant mosquitoes, Culex quinquefasciatus. PLOS ONE 6:e23403 [Google Scholar]
  72. Liu N, Liu H, Zhu F, Zhang L. 72.  2007. Differential expression of genes in pyrethroid resistant and susceptible mosquitoes, Culex quinquefasciatus. Gene 394:61–68 [Google Scholar]
  73. Liu N, Scott JG. 73.  1997. Inheritance of CYP6D1-mediated pyrethroid resistance in house fly (Diptera: Muscidae). J. Econ. Entomol. 90:1478–81 [Google Scholar]
  74. Liu N, Scott JG. 74.  1997. Phenobarbital induction of CYP6D1 is due to a trans acting factor on autosome 2 in house flies, Musca domestica. Insect Mol. Biol. 6:77–81 [Google Scholar]
  75. Lumjuan N, Rajatileka S, Changsom D, Wicheer J, Leelapat P. 75.  et al. 2011. The role of the Aedes aegypti Epsilon glutathione transferases in conferring resistance to DDT and pyrethroid insecticides. Insect Biochem. Mol. Biol. 41:203–9 [Google Scholar]
  76. Lycett GJ, McLaughlin LA, Ranson H, Hemingway J, Kafatos FC. 76.  et al. 2006. Anopheles gambiae P450 reductase is highly expressed in oenocytes and in vivo knockdown increases permethrin susceptibility. Insect Mol. Biol. 15:321–27 [Google Scholar]
  77. Maitra S, Dombrowski SM, Basu M, Raustol O, Waters LC. 77.  et al. 2000. Factors on the third chromosome affect the level of Cyp6a2 and Cyp6a8 expression in Drosophila melanogaster. Gene 248:147–56 [Google Scholar]
  78. Marcombe S, Mathieu RB, Pocquet N, Riaz M-A, Poupardin R. 78.  et al. 2012. Insecticide resistance in the dengue vector Aedes aegypti from Martinique: distribution, mechanisms and relations with environmental factors. PLOS ONE 7:e30989 [Google Scholar]
  79. Marinotti O, Cerqueita GC, de Almeida LGP, Ferro MIT, da Silva Loreto EL. 79.  et al. 2013. The genome of Anopheles darlingi, the main neotropical malaria vector. Nucleic Acids Res. 41:7387–400 [Google Scholar]
  80. Marshall E. 80.  2000. A renewed assault on an old and deadly foe. Science 290:428–30 [Google Scholar]
  81. Martinez-Torres D, Chandre F, Williamson MS, Darriet F, Bergé JB. 81.  et al. 1998. Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s.s. Insect Mol. Biol. 7:179–84 [Google Scholar]
  82. McAbee RD, Kang KD, Stanich MA, Christiansen JA, Wheelock CE. 82.  et al. 2004. Pyrethroid tolerance in Culex pipiens pipiens var molestus from Marin County, California. Pest Manag. Sci. 60:359–68 [Google Scholar]
  83. McDonnell CM, Brown RP, Berenbaum MR, Schuler MA. 83.  2004. Conserved regulatory elements in the promoters of two allelochemical-inducible cytochrome P450 genes differentially regulate transcription. Insect Biochem. Mol. Biol. 34:1129–39 [Google Scholar]
  84. Mitchell SN, Stevenson BJ, Müller P, Wilding CS, Egyir-Yawson A. 84.  et al. 2012. Identification and validation of a gene causing cross-resistance between insecticide classes in Anopheles gambiae from Ghana. Proc. Natl. Acad. Sci. USA 109:6147–52 [Google Scholar]
  85. Morou E, Dowd AJ, Rajatileka S, Steven A, Hemingway J. 85.  et al. 2010. A simple colorimetric assay for specific detection of glutathione-S transferase activity associated with DDT resistance in mosquitoes. PLOS Negl. Trop. Dis. 4:e808 [Google Scholar]
  86. Mouches C, Pasteur N, Berge JB, Hyrien O, Raymond M. 86.  et al. 1986. Amplification of an esterase gene is responsible for insecticide resistance in a California Culex mosquito. Science 233:778–80 [Google Scholar]
  87. Müller P, Donnelly MJ, Ranson H. 87.  2007. Transcription profiling of a recently colonised pyrethroid resistant Anopheles gambiae strain from Ghana. BMC Genomics 8:36 [Google Scholar]
  88. Müller P, Warr E, Stevenson BJ, Pignatelli PM, Morgan JC. 88.  et al. 2008. Field-caught permethrin-resistant Anopheles gambiae overexpress CYP6P3, a P450 that metabolises pyrethroids. PLOS Genet. 4:e1000286 [Google Scholar]
  89. Nabeshima T, Mori A, Kozaki T, Iwata Y, Hidoh O. 89.  et al. 2004. An amino acid substitution attributable to insecticide-insensitivity of acetylcholinesterase in a Japanese encephalitis vector mosquito, Culex tritaeniorhynchus. Biochem. Biophys. Res. Commun. 313:794–801 [Google Scholar]
  90. Narahashi T. 90.  1988. Molecular and cellular approaches to neurotoxicology: past, present and future. Neurotox '88: Molecular Basis of Drug and Pesticide Action GG Lunt 563–82 New York: Elsevier [Google Scholar]
  91. Nene V, Wortman JR, Lawson D, Haas B, Kodira C. 91.  et al. 2007. Genome sequence of Aedes aegypti, a major arbovirus vector. Science 316:1718–23 [Google Scholar]
  92. Nikou D, Ranson H, Hemingway J. 92.  2003. An adult-specific CYP6 P450 gene is overexpressed in a pyrethroid-resistant strain of the malaria vector, Anopheles gambiae. Gene 318:91–102 [Google Scholar]
  93. Oliveira EE, Du Y, Nomura Y, Dong K. 93.  2013. A residue in the transmembrane segment 6 of domain I in insect and mammalian sodium channels regulate differential sensitivities to pyrethroid insecticides. Neurotoxicology 38:42–50 [Google Scholar]
  94. Ortelli F, Rossiter LC, Vontas J, Ranson H, Hemingway J. 94.  2003. Heterologous expression of four glutathione transferase genes genetically linked to a major insecticide-resistance locus from the malaria vector Anopheles gambiae. Biochem. J. 373:957–63 [Google Scholar]
  95. Pasteur N, Raymond M. 95.  1996. Insecticide resistance genes in mosquitoes: their mutations, migration, and selection in field populations. J. Hered. 87:444–49 [Google Scholar]
  96. Pavlidi N, Monastirioti M, Daborn P, Livadaras I, Van Leeuwen T, Vontas J. 96.  2012. Transgenic expression of the Aedes aegypti CYP9J28 confers pyrethroid resistance in Drosophila melanogaster. Pestic. Biochem. Physiol. 104:132–35 [Google Scholar]
  97. Petersen RA, Niamsup H, Berenbaum MR, Schuler MA. 97.  2003. Transcriptional response elements in the promoter of CYP6B1, an insect P450 gene regulated by plant chemicals. Biochim. Biophys. Acta 1619:269–82 [Google Scholar]
  98. Ranson H, Claudianos C, Ortelli F, Abgrall C, Hemingway J. 98.  et al. 2002. Evolution of supergene families associated with insecticide resistance. Science 298:179–81 [Google Scholar]
  99. Ranson H, Hemingway J. 99.  2005. Mosquito glutathione transferases. Method Enzymol. 401:226–41 [Google Scholar]
  100. Ranson H, N'Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V. 100.  2011. Pyrethroid resistance in African anopheline mosquitoes: What are the implications for malaria control. Trends Parasitol. 27:91–98 [Google Scholar]
  101. Ranson H, Rossiter L, Ortelli F, Jensen B, Wang X. 101.  et al. 2001. Identification of a novel class of insect glutathione S-transferases involved in resistance to DDT in the malaria vector Anopheles gambiae. Biochem. J. 359:295–304 [Google Scholar]
  102. Raymond M, Chevillon C, Guillemaud T, Lenormand T, Pasteur N. 102.  1998. An overview of the evolution of overproduced esterases in the mosquito Culex pipiens. Philos. Trans. R. Soc. Lond. B 353:1707–11 [Google Scholar]
  103. Reenan RA. 103.  2005. Molecular determinants and guided evolution of species-specific RNA editing. Nature 434:409–13 [Google Scholar]
  104. Reid WR, Zhang L, Liu N. 104.  2012. The whole genome transcriptome analysis of the mosquito Culex quinquefasciatus following permethrin selection. PLOS ONE 7:e47163 [Google Scholar]
  105. Rencurel F, Stenhouse A, Hawley SA, Friedberg T, Hardie DG. 105.  et al. 2005. AMP-activated protein kinase mediates phenobarbital induction of CYP2B gene expression in hepatocytes and a newly derived human hepatoma cell line. J. Biol. Chem. 280:4367–73 [Google Scholar]
  106. Rinkevich FD, Du Y, Dong K. 106.  2013. Diversity and convergence of sodium channel mutations involved in resistance to pyrethroids. Pestic. Biochem. Physiol. 106:93–100 [Google Scholar]
  107. Riveron JM, Irving H, Ndula M, Barnes KG, Ibrahim SS. 107.  et al. 2013. Directionally selected cytochrome P450 alleles are driving the spread of pyrethroid resistance in the major malaria vector Anopheles funestus. Proc. Natl. Acad. Sci. USA 110:252–57 [Google Scholar]
  108. Rongnoparut P, Boonsuepsakul S, Chareonviriyaphap T, Thanomsing N. 108.  2003. Cloning of cytochrome P450, CYP6P5, and CYP6AA2 from Anopheles minimus resistant to deltamethrin. J. Vector Ecol. 28:150–58 [Google Scholar]
  109. Roush RT. 109.  1990. Genetics and management of insecticide resistance: lessons for resistance in internal parasites?. Resistance of Parasites to Antiparasitic Drugs: Round Table Conf. ICOPA VII, Paris JC Boray, M Fernex, PJ Martin, RT Roush 197–211 Rahway, NJ: MSD Agvet [Google Scholar]
  110. Schuler MA. 110.  1996. The role of cytochrome P450 monooxygenases in plant-insect interactions. Plant Physiol. 112:1411–19 [Google Scholar]
  111. Schuler MA. 111.  2011. P450s in plant-insect interactions. Biochem. Biophys. Acta 1814:36–45 [Google Scholar]
  112. Schuler MA, Berenbaum MR. 112.  2013. Structure and function of cytochrome P450S in insect adaptation to natural and synthetic toxins: Insights gained from molecular modeling. J. Chem. Ecol. 39:1232–45 [Google Scholar]
  113. Scott JA, Collins FH, Feyereisen R. 113.  1994. Diversity of cytochrome P450 genes in the mosquito, Anopheles albimanus. Biochem. Biophys. Res. Commun. 205:1452–59 [Google Scholar]
  114. Scott JG. 114.  1999. Cytochromes P450 and insecticide resistance. Insect Biochem. Mol. Biol. 29:757–77 [Google Scholar]
  115. Scott JG, Michel K, Bartholomay LC, Siegfried BD, Hunter WB. 115.  et al. 2013. Towards the elements of successful insect RNAi. J. Insect Physiol. 59:1212–21 [Google Scholar]
  116. Severson DW, Behura SK. 116.  2012. Mosquito genomics: progress and challenges. Annu. Rev. Entomol. 57:143–66 [Google Scholar]
  117. Singh OP, Dykes CL, Das MK, Pradhan S, Bhatt RM. 117.  et al. 2010. Presence of two alternative kdr-like mutations, L1014F and L1014S, and a novel mutation, V1010L, in the voltage gated Na+ channel of Anopheles culicifacies from Orissa, India. Malar. J. 9:146 [Google Scholar]
  118. Soderlund DM. 118.  2005. Sodium channels. Comprehensive Molecular Insect Science LI Gilbert, K Iatrou, SS Gill 51–24 Amsterdam, Neth.: Elsevier BV [Google Scholar]
  119. Soderlund DM, Bloomquist JR. 119.  1990. Molecular mechanisms of insecticide resistance. Pesticide Resistance in Arthropods RT Roush, BE Tabashnik 58–96 New York: Chapman & Hall [Google Scholar]
  120. Soderlund DM, Knipple DC. 120.  2003. The molecular biology of knockdown resistance to pyrethroid insecticides. Insect Biochem. Mol. Biol. 33:563–77 [Google Scholar]
  121. Srisawat R, Komalamisra N, Eshita Y, Zheng M, Ono K. 121.  et al. 2010. Point mutations in domain II of the voltage-gated sodium channel gene in deltamethrin-resistant Aedes aegypti (Diptera: Culicidae). Appl. Entomol. Zool. 45:275–82 [Google Scholar]
  122. Steinberg SF, Brunton L. 122.  2001. Compartmentation of G protein-coupled signaling pathways in cardiac myocytes. Annu. Rev. Pharmacol. Toxicol. 41:751–73 [Google Scholar]
  123. Stevenson BJ, Bibby J, Pignatelli P, Muangnoicharoen S, O'Neill PM. 123.  et al. 2011. Cytochrome P450 6M2 from the malaria vector Anopheles gambiae metabolizes pyrethroids: sequential metabolism of deltamethrin revealed. Insect Biochem. Mol. Biol. 41:492–502 [Google Scholar]
  124. Stevenson BJ, Pignatelli P, Nikou D, Paine MJ. 124.  2012. Pinpointing P450s associated with pyrethroid metabolism in the dengue vector, Aedes aegypti: developing new tools to combat insecticide resistance. PLOS Negl. Trop. Dis. 6:e1595 [Google Scholar]
  125. Strode C, Wondji CS, David J-P, Hawkes NJ, Lumjuan N. 125.  et al. 2008. Genomic analysis of detoxification genes in the mosquito Aedes aegypti. Insect Biochem. Mol. Biol. 38:113–23 [Google Scholar]
  126. SupYoon K, Symington SB, Lee SH, Soderlund DM, Clark JM. 126.  2008. Three mutations identified in the voltage-sensitive sodium channel α-subunit gene of permethrin-resistant human head lice reduce the permethrin sensitivity of house fly Vssc1 sodium channels expressed in Xenopus oocytes. Insect Biochem. Mol. Biol. 38:296–306 [Google Scholar]
  127. Tian L, Cao C, He L, Li M, Zhang L. 127.  et al. 2011. Autosomal interactions and mechanisms of pyrethroid resistance in house flies, Musca domestica. Int. J. Biol. Sci. 7:902 [Google Scholar]
  128. Vaughan A, Hemingway J. 128.  1995. Mosquito carboxylesterase Estα21 (A2): Cloning and sequence of the full-length cDNA for a major insecticide resistance gene worldwide in the mosquito Culex quinquefasciatus. J. Biol. Chem. 270:17044–49 [Google Scholar]
  129. Vontas J, Blass C, Koutsos JAC, David P, Kafatos FC. 129.  et al. 2005. Gene expression in insecticide resistant and susceptible Anopheles gambiae strains constitutively or after insecticide exposure. Insect Mol. Biol. 14:509–21 [Google Scholar]
  130. Vulule JM, Beach RF, Atieli FK, McAllister JC, Brogdon WG. 130.  et al. 1999. Elevated oxidase and esterase levels associated with permethrin tolerance in Anopheles gambiae from Kenyan villages using permethrin-impregnated nets. Med. Vet. Entomol. 13:239–44 [Google Scholar]
  131. Wang D, Johnson AD, Papp AC, Kroetz DL, Sadee W. 131.  2005. Multidrug resistance polypeptide 1 (MDR1, ABCB1) variant 3435C>T affects mRNA stability. Pharmacogenetics Genomics 15:693–704 [Google Scholar]
  132. Wang W, Liu S-L, Liu Y-Y, Qiao C-L, Chen S-L, Cui F. 132.  2014. Over-transcription of genes in a parathion-resistant strain of mosquito Culex pipiens quinquefasciatus. Insect Sci. In press. doi: 10.1111/1744-7917.12106 [Google Scholar]
  133. Weill M, Fort P, Berthomieu A, Dubois MP, Pasteur N. 133.  et al. 2002. A novel acetylcholinesterase gene in mosquitoes codes for the insecticide target and is non-homologous to the ace gene in Drosophila. Proc. R. Soc. Lond. B 269:2007–16 [Google Scholar]
  134. Weill M, Lutfalla G, Mogensen K, Chandre F, Berthomieu A. 134.  et al. 2003. Insecticide resistance in mosquito vectors. Nature 423:136–37 [Google Scholar]
  135. Wilding CS, Smith I, Lynd A, Yawson AE, Weetman D. 135.  et al. 2012. A cis-regulatory sequence driving metabolic insecticide resistance in mosquitoes: functional characterisation and signatures of selection. Insect Biochem. Mol. Biol. 42:699–707 [Google Scholar]
  136. Williamson MS, Martinez-Torres D, Hick CA, Devonshire AL. 136.  1996. Identification of mutations in the house fly para-type sodium channel gene associated with knockdown resistance (kdr) to pyrethroid insecticides. Mol. Gen. Genet. 252:51–60 [Google Scholar]
  137. Wondji CS, Dabire RK, Tukur Z, Irving H, Djouaka R. 137.  et al. 2011. Identification and distribution of a GABA receptor mutation conferring dieldrin resistance in the malaria vector Anopheles funestus in Africa. Insect Biochem. Mol. Biol. 41:484–91 [Google Scholar]
  138. Wondji CS, Irving H, Morgan J, Lobo NF, Collins FH. 138.  et al. 2009. Two duplicated P450 genes are associated with pyrethroid resistance in Anopheles funestus, a major malaria vector. Genome Res. 19:452–59 [Google Scholar]
  139. 139. World Health Organ. (WHO) 1957. Expert committee on insecticides. WHO Tech. Rep. Ser. No. 125, 7th Rep., WHO, Geneva [Google Scholar]
  140. 140. World Health Organ. (WHO) 2007. Long-lasting insecticidal nets for malaria prevention—a manual for malaria programme managers Trial Ed., WHO, Geneva. http://www.who.int/malaria/publications/atoz/insecticidal_nets_malaria/en/ [Google Scholar]
  141. 141. World Health Organ. (WHO) 2009. WHO recommended long-lasting insecticidal mosquito nets. WHO, Geneva [Google Scholar]
  142. 142. World Health Organ. (WHO) 2013. Malaria: core vector control methods WHO, Geneva. http://www.who.int/malaria/areas/vector_control/core_methods/en/ [Google Scholar]
  143. 143. World Health Organ. (WHO) 2013. Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. WHO, Geneva. http://apps.who.int/iris/bitstream/10665/80139/1/9789241505154_eng.pdf [Google Scholar]
  144. 144. World Health Organ. (WHO) 2014. Dengue and severe dengue Fact Sheet Number 117, WHO, Genveva. http://www.who.int/mediacentre/factsheets/fs117/en/ [Google Scholar]
  145. 145. World Health Organ. (WHO) 2014. Malaria Fact Sheet Number 94, WHO, Geneva. http://www.who.int/mediacentre/factsheets/fs094/en/ [Google Scholar]
  146. Xu Q, Liu H, Zhang L, Liu N. 146.  2005. Resistance in the mosquito, Culex quinquefasciatus (S.), and possible mechanisms for resistance. Pest Manag. Sci. 61:1096–102 [Google Scholar]
  147. Xu Q, Wang H, Zhang L, Liu N. 147.  2006. Kdr allelic variation in pyrethroid resistant mosquitoes, Culex quinquefasciatus (S.). Biochem. Biophys. Res. Commun. 345:774–80 [Google Scholar]
  148. Xu Q, Wang H, Zhang L, Liu N. 148.  2006. Sodium channel gene expression associated with pyrethroid resistant house flies and German cockroaches. Gene 379:62–67 [Google Scholar]
  149. Xu Q, Zhang L, Li T, Zhang L, He L. 149.  et al. 2012. Evolutionary adaption of the amino acid and codon usage of the mosquito sodium channel following permethrin selection. PLOS ONE 7:e47609 [Google Scholar]
  150. Yan L, Yang P, Jiang F, Cui N, Ma E. 150.  et al. 2012. Transcriptomic and phylogenetic analysis of Culex pipiens quinquefasciatus for three detoxification gene families. BMC Genomics 13:609 [Google Scholar]
  151. Yang T, Liu N. 151.  2011. Genome analysis of cytochrome P450s and their expression profiles in insecticide resistant mosquitoes, Culex quinquefasciatus. PLOS ONE 6:e29418 [Google Scholar]
  152. Yang T, Liu N. 152.  2014. Permethrin resistance variation and susceptible reference line isolation in a field population of the mosquito, Culex quinquefasciatus (Diptera: Culicidae). Insect Sci. 21659–66 [Google Scholar]
  153. Zaim M, Guillet P. 153.  2002. Alternative insecticides: an urgent need. Trends Parasitol. 18:161–63 [Google Scholar]
  154. Zhu F, Moural TW, Shah K, Palli SR. 154.  2013. Integrated analysis of cytochrome P450 gene superfamily in the red flour beetle, Tribolium castaneum. BMC Genomics 14:174 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error