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CYP6 P450 Enzymes and Duplication Produce Extreme and Multiple Insecticide Resistance in the Malaria Mosquito


Malaria control depends heavily on only four classes of insecticide to which Anopheles mosquitoes are increasingly resistant. It is important to manage insecticide application carefully to minimise increases in resistance, for example by using different compounds in combination or rotation. Recently, mosquitoes resistant to all available insecticides have been found in Tiassalé, West Africa, which could be problematic for resistance management, particularly if common genetic mechanisms are responsible (‘cross-resistance’). Tiassalé mosquitoes also exhibit extreme levels of resistance to the two most important classes, pyrethroids and carbamates. We investigated the genetic basis of extreme carbamate resistance and cross-resistance in Tiassalé, and the applicability of results in an additional population from Togo. We find that specific P450 enzymes are involved in both extreme and cross-resistance, including one, CYP6M2, which can cause resistance to three insecticide classes. However, amplification of a mutated version of the gene which codes for acetycholinesterase, the target site of both the carbamate and organophosphate insecticides, also plays an important role. Mechanisms involved in both extreme resistance and cross resistance are likely to be very resilient to insecticide management practices, and represent an alarming scenario for mosquito-targeted malaria control.


Vyšlo v časopise: CYP6 P450 Enzymes and Duplication Produce Extreme and Multiple Insecticide Resistance in the Malaria Mosquito. PLoS Genet 10(3): e32767. doi:10.1371/journal.pgen.1004236
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004236

Souhrn

Malaria control depends heavily on only four classes of insecticide to which Anopheles mosquitoes are increasingly resistant. It is important to manage insecticide application carefully to minimise increases in resistance, for example by using different compounds in combination or rotation. Recently, mosquitoes resistant to all available insecticides have been found in Tiassalé, West Africa, which could be problematic for resistance management, particularly if common genetic mechanisms are responsible (‘cross-resistance’). Tiassalé mosquitoes also exhibit extreme levels of resistance to the two most important classes, pyrethroids and carbamates. We investigated the genetic basis of extreme carbamate resistance and cross-resistance in Tiassalé, and the applicability of results in an additional population from Togo. We find that specific P450 enzymes are involved in both extreme and cross-resistance, including one, CYP6M2, which can cause resistance to three insecticide classes. However, amplification of a mutated version of the gene which codes for acetycholinesterase, the target site of both the carbamate and organophosphate insecticides, also plays an important role. Mechanisms involved in both extreme resistance and cross resistance are likely to be very resilient to insecticide management practices, and represent an alarming scenario for mosquito-targeted malaria control.


Zdroje

1. WHO (2011) WHO Global Malaria Programme. World malaria report. World Health Organization report, Geneva.

2. van den BergH, ZaimM, YadavRS, SoaresA, AmeneshewaB, et al. (2012) Global trends in the use of insecticides to control vector-borne diseases. Environ Health Perspect 120: 577–582.

3. BadoloA, TraoreA, JonesCM, SanouA, FloodL, et al. (2012) Three years of insecticide resistance monitoring in Anopheles gambiae in Burkina Faso: resistance on the rise? Malar J 11: 232.

4. RansonH, AbdallahH, BadoloA, GuelbeogoWM, Kerah-HinzoumbéC, et al. (2009) Insecticide resistance in Anopheles gambiae: data from the first year of a multi-country study highlight the extent of the problem. Malar J 8: 299.

5. RansonH, N'guessanR, LinesJ, MoirouxN, NkuniZ, et al. (2011) Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol 27: 91–98.

6. WHO (2012) Global Plan for Insecticide Resistance Management (GPIRM). (World Health Organization, Geneva).

7. IRAC (2011) Prevention and Management of Insecticide Resistance in Vectors of Public Health Importance. Available: http://www.irac-online.org/content/uploads/2009/09/VM-Layout-v2.6_LR.pdf

8. QiuX, SunW, McDonnellCM, Li-ByarlayH, SteeleLD, et al. (2012) Genome-wide analysis of genes associated with moderate and high DDT resistance in Drosophila melanogaster. Pest Manag Sci in press. doi:10.1002/ps.3454

9. NamountougouM, SimardF, BaldetT, DiabatéA, OuédraogoJB, et al. (2012) Multiple insecticide resistance in Anopheles gambiae s.l. populations from Burkina Faso, West Africa. PLoS One 7: e48412.

10. CorbelV, N'GuessanR, BrenguesC, ChandreF, DjogbenouL, et al. (2007) Multiple insecticide resistance mechanisms in Anopheles gambiae and Culex quinquefasciatus from Benin, West Africa. Acta Trop 101: 207–216.

11. EdiCV, KoudouGB, JonesCM, WeetmanD, RansonH (2012) Multiple-insecticide resistance in Anopheles gambiae mosquitoes, Southern Cote d'Ivoire. Emerg Infect Dis 18: 1508–1511.

12. OduolaAO, IdowuET, OyebolaMK, AdeogunAO, OlojedeJB, et al. (2012) Evidence of carbamate resistance in urban populations of Anopheles gambiae s.s. mosquitoes resistant to DDT and deltamethrin insecticides in Lagos, South-Western Nigeria. Parasit Vectors 5: 116.

13. OkoyePN, BrookeBD, KoekemoerLL, HuntRH, CoetzeeM (2008) Characterisation of DDT, pyrethroid and carbamate resistance in Anopheles funestus from Obuasi, Ghana. Trans R Soc Trop Med Hyg 102: 591–598.

14. Martinez-TorresD, ChandreF, WilliamsonMS, DarrietF, BergéJB, et al. (1998) Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s.s.. Insect Mol Biol 7: 179–184.

15. RansonH, JensenB, VululeJM, WangX, HemingwayJ, et al. (2000) Identification of a point mutation in the voltage-gated sodium channel gene of Kenyan Anopheles gambiae associated with resistance to DDT and pyrethroids. Insect Mol Biol 9: 491–497.

16. JonesCM, LiyanapathiranaM, AgossaFR, WeetmanD, RansonH, 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: 6614–6619.

17. AkogbétoMC, PadonouGG, GbénouD, IrishS, YadouletonA (2010) Bendiocarb, a potential alternative against pyrethroid resistant Anopheles gambiae in Benin, West Africa. Malar J 9: 204.

18. AkogbétoM, PadonouG, BankoléH, Kindé GazardD, GbédjissiG (2011) Dramatic decline of malaria transmission after implementation of large-scale Indoor Residual Spraying using bendiocarb in Bénin, West Africa, an area of high Anopheles gambiae resistance to pyrethroids. Am J Trop Med Hyg 85: 586–593.

19. SharpBL, RidlFC, GovenderD, KuklinskiJ, KleinschmidtI (2007) Malaria vector control by indoor residual insecticide spraying on the tropical island of Bioko, Equatorial Guinea. Malar J 6: 52.

20. KigoziR, BaxiSM, GasasiraA, SserwangaA, KakeetoS, et al. (2012) Indoor Residual Spraying of insecticide and malaria morbidity in a high transmission intensity area of Uganda. PLoS ONE 7: e42857.

21. WeillM, LutfallaG, MogensenK, ChandreF, BerthomieuA, et al. (2003) Insecticide resistance in mosquito vectors. Nature 423: 136–137.

22. WeillM, MalcolmC, ChandreF, MogensenK, BerthomieuA, et al. (2004) The unique mutation in ace-1 giving high insecticide resistance is easily detectable in mosquito vectors. Insect Mol Biol 13: 1–7.

23. DjogbénouL, ChandreF, BerthomieuA, DabiréR, KoffiA, et al. (2008) Evidence of introgression of the ace-1(R) mutation and of the ace-1 duplication in West African Anopheles gambiae s.s. PLoS ONE 3: e2172.

24. DabiréKR, DiabatéA, NamontougouM, DjogbenouL, KengneP, et al. (2009) Distribution of insensitive acetylcholinesterase (ace-1R) in Anopheles gambiae s.l. populations from Burkina Faso (West Africa). Trop Med Int Health 14: 396–403.

25. Ahoua AlouLP, KoffiAA, AdjaMA, TiaE, KouassiPK, et al. (2010) Distribution of ace-1R and resistance to carbamates and organophosphates in Anopheles gambiae s.s. populations from Côte d'Ivoire. Malar J 9: 167.

26. DjogbénouL, WeillM, HougardJM, RaymondM, AkogbétoM, et al. (2007) Characterization of insensitive acetyleholinesterase (ace-1(R)) in Anopheles gambiae (Diptera: Culicidae): resistance levels and dominance. J Med Entomol 44: 805–810.

27. LenormandT, BourguetD, GuillemaudT, RaymondM (1999) Tracking the evolution of insecticide resistance in the mosquito Culex pipiens. Nature 400: 861–864.

28. LabbéP, BerticatC, BerthomieuA, UnalS, BernardC, et al. (2007) Forty years of erratic insecticide resistance evolution in the mosquito Culex pipiens. PLoS Genet 3: e205.

29. DjogbenouL, NoelV, AgnewP (2010) Costs of insensitive acetylcholinesterase insecticide resistance for the malaria vector Anopheles gambiae homozygous for the G119S mutation. Malar J 9: 12.

30. LabbéP, BerthomieuA, BerticatC, AloutH, RaymondM, et al. (2007) Independent duplications of the acetylcholinesterase gene conferring insecticide resistance in the mosquito Culex pipiens. Mol Biol Evol 24: 1056–1067.

31. GassmannAJ, OnstadDW, PittendrighBR (2009) Evolutionary analysis of herbivorous insects in natural and agricultural environments. Pest Manag Sci 65: 1174–1181.

32. MitchellSN, StevensonBJ, MüllerP, WildingCS, Egyir-YawsonA, 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: 6147–6152.

33. DjouakaRF, BakareAA, CoulibalyON, AkogbetoMC, RansonH, 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.

34. MüllerP, WarrE, StevensonBJ, PignatelliPM, MorganJC, et al. (2008) Field-caught permethrin-resistant Anopheles gambiae overexpress CYP6P3, a P450 that metabolises pyrethroids. PLoS Genet 4: e1000286.

35. StevensonBJ, BibbyJ, PignatelliP, MuangnoicharoenS, O'NeillPM, 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.

36. CoetzeeM, HuntRH, WilkersonR, TorreA, della CoulibalyMB, et al. (2013) Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa 3619: 246–274.

37. NPIC (2002) Bendiocarb technical fact sheet. National Pesticide Information Centre, Oregon State University. Available: http://npic.orst.edu/factsheets/bendiotech.pdf

38. BakerDA, NolanT, FischerB, PinderA, CrisantiA, et al. (2011) A comprehensive gene expression atlas of sex- and tissue-specificity in the malaria vector, Anopheles gambiae. BMC Genomics 12: 296.

39. KoffiAA, Ahoua AlouLP, AdjaMA, ChandreF, PennetierC (2013) Insecticide resistance status of Anopheles gambiae s.s population from M'Be': a WHOPES-labelled experimental station, 10 years after the political crisis in Côte d'Ivoire. Malar J 12: 151.

40. BrookeBD, KlokeG, HuntRH, KoekemoerLL, TemuEA, et al. (2001) Bioassay and biochemical analyses of insecticide resistance in southern African Anopheles funestus (Diptera: Culicidae). Bull Entomol Res 91: 265–272.

41. Farnham AW (1998) The mode of action of piperonyl butoxide with reference to studying pesticide resistance. In: Jones DG, editor. Piperonyl butoxide, the insecticide synergist. Academic, London. pp. 199–213.

42. Gunning RV, Moores GD, Devonshire AL (1998) Inhibition of resistance-related esterase by piperonyl butoxide in Helicoverpa armigera (Hübner) (Lepidopdera: Noctoidae) and Aphis gossypii (Hempitera: Aphididae). In: Jones DG, editor. Piperonyl butoxide, the insecticide synergist. Academic, London. pp. 215–226.

43. YoungSJY, GunningRV, MooresGD (2005) The effect of piperonyl butoxide on pyrethroid- resistance-associated esterases in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Pest Manag Sci 61: 397–401.

44. WondjiCS, IrvingH, MorganJ, LoboNF, CollinsFH, et al. (2009) Two duplicated P450 genes are associated with pyrethroid resistance in Anopheles funestus, a major malaria vector. Genome Res 19: 452–459.

45. RiveronJM, IrvingH, NdulaM, BarnesKG, IbrahimSS, 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: 252–257.

46. ChiuTL, WenZ, RupasingheSG, SchulerMA (2008) Comparative molecular modeling of Anopheles gambiae CYP6Z1, a mosquito P450 capable of metabolizing DDT. Proc Natl Acad Sci USA 105: 8855–8860.

47. Fossog TeneB, PoupardinR, CostantiniC, Awono-AmbeneP, WondjiCS, et al. (2013) Resistance to DDT in an urban setting: common mechanisms implicated in both M and S forms of Anopheles gambiae in the city of Yaoundé, Cameroon. PLoS ONE 8: e61408.

48. LiuN, ScottJG (1996) Genetic analysis of factors controlling high-level expression of cytochrome P450, CYP6D1, cytochrome b5, P450 reductase, and monooxygenase activities in LPR house flies, Musca domestica. Biochem Genet 34: 133–148.

49. DavidJP, IsmailHM, Chandor-ProustA, PaineMJ (2013) Role of cytochrome P450s in insecticide resistance: impact on the control of mosquito-borne diseases and use of insecticides on Earth. Philos Trans R Soc Lond B Biol Sci 368: 20120429.

50. Chandor-ProustA, BibbyJ, Régent-KloecknerM, RouxJ, Guittard-CrilatE, et al. (2013) The central role of mosquito cytochrome P450 CYP6Zs in insecticide detoxification revealed by functional expression and structural modelling. Biochem J 455: 75–85.

51. PuineanAM, FosterSP, OliphantL, DenholmI, FieldLM, et al. (2010) Amplification of a cytochrome P450 gene is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. PLoS Genet 6: e1000999.

52. SchmidtJM, GoodRT, AppletonB, SherrardJ, RaymantGC, et al. (2010) Copy number variation and transposable elements feature in recent, ongoing adaptation at the Cyp6g1 locus. PLoS Genet 6: e1000998.

53. CarvalhoR, YangYiHua, FieldLM, GormanK, MooresG, et al. (2012) Chlorpyrifos resistance is associated with mutation and amplification of the acetylcholinesterase-1 gene in the tomato red spider mite, Tetranychus evansi. Pestic Biochem Physiol 104: 143–149.

54. DabornP, BoundyS, YenJ, PittendrighB, ffrench-ConstantR (2001) DDT resistance in Drosophila correlates with Cyp6g1 over-expression and confers cross-resistance to the neonicotinoid imidacloprid. Mol Genet Genomics 266: 556–563.

55. LinGG-H, ScottJG (2011) Investigations of the constitutive overexpression of CYP6D1 in the permethrin resistantLPR strain of house fly (Musca domestica). Pestic Biochem Physiol 100: 130–134.

56. LinesJD, NassorNS (1991) DDT resistance in Anopheles gambiae declines with mosquito age. Med Vet Entomol 5: 261–265.

57. ChouaibouMS, ChabiJ, BinghamGV, KnoxTB, N'driL, et al. (2012) Increase in susceptibility to insecticides with aging of wild Anopheles gambiae mosquitoes from Côte d'Ivoire. BMC Infectious Diseases 12: 214.

58. JonesCM, SanouA, GuelbeogoWM, SagnonN, JohnsonPC, et al. (2012) Aging partially restores the efficacy of malaria vector control in insecticide-resistant populations of Anopheles gambiae s.l. from Burkina Faso. Malar J 11: 24.

59. AloutH, LabbéP, BerthomieuA, DjogbénouL, LeonettiJP, et al. (2012) Novel AChE Inhibitors for sustainable insecticide resistance management. PLoS ONE 7: e47125.

60. WongDM, LiJ, ChenQH, HanQ, MutungaJM, et al. (2012) Select small core structure carbamates exhibit high contact toxicity to “carbamate-resistant” strain malaria mosquitoes, Anopheles gambiae (Akron). PLoS ONE 7: e46712.

61. SantolamazzaF, ManciniE, SimardF, QiY, TuZ, et al. (2008) Insertion polymorphisms of SINE200 retrotransposons within speciation islands of Anopheles gambiae molecular forms. Malar J 7: 163.

62. BassC, NikouD, VontasJ, WilliamsonMS, FieldLM (2010) Development of high-throughput real-time PCR assays for the identification of insensitive acetylcholinesterase (ace-1R) in Anopheles gambiae. Pestic Biochem Physiology 96: 80–85.

63. SchmittgenTD, LivakKJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101–1108.

64. CuiX, ChurchillG (2003) Statistical tests for differential expression in cDNA microarray experiments. Genome Biology 4: 210.

65. Wu H, Kerr K, Cui X, Churchill G (2002) MAANOVA: a software package for the analysis of spotted cDNA microarray experiments. In: Parmigiani G, Garrett ES, Irizarry R, Zeger S, editors. The Analysis of Gene Expression Data: Methods and Software. New York: Springer pp. 313–341.

66. KooperbergC, AragakiA, StrandAD, OlsonJM (2005.) Significance testing for small microarray experiments. Stat Med 24: 2281–2298.

67. Huang daW, ShermanBT, TanQ, KirJ, LiuD, et al. (2007) DAVID Bioinformatics Resources: expanded annotation database and novel algorithms to better extract biology from large gene lists. Nucleic Acids Research 35 (suppl 2) 169–175.

68. WangJ-W, BeckES, McCabeBD (2012) A modular toolset for recombination transgenesis and neurogenetic analysis of Drosophila. PLoS ONE 7: e42102.

69. PontonF, ChapuisMP, PerniceM, SwordGA, SimpsonSJ (2011) Evaluation of potential reference genes for reverse transcription-qPCR studies of physiological responses in Drosophila melanogaster. J Insect Physiol 57: 840–850.

70. DulinF, Halm-LemeilleMP, LozanoS, LepailleurA, SantosJS, et al. (2012) Interpretation of honeybees contact toxicity associated to acetylcholinesterase inhibitors. Ecotoxicology and Environmental Safety 79: 13–21.

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