Additional Selection for Insecticide Resistance in Urban Malaria Vectors: DDT Resistance in Anopheles arabiensis from Bobo-Dioulasso, Burkina Faso

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Jones, Christopher M ^a   Toé, Hyacinthe K ^a,b,c   Sanou, Antoine ^c   Namountougou, Moussa ^b   Hughes, Angela ^a   Diabaté, Abdoulaye ^b   Dabiré, Roch ^b   Simard, Frederic ^b,d   Ranson, Hilary ^a  

^a LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^b CENTRE MURAZ   (Burkina Faso)

^c Burkina Faso   (Burkina Faso)

^d University de Montpellier   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; CYTOCHROME P450; GLUTATHIONE TRANSFERASE; VASCULOTROPIN RECEPTOR 2;

ABC TRANSPORTER GENE; ANOPHELES ARABIENSIS; ANOPHELES GAMBIAE; ARTICLE; BURKINA FASO; CONTROLLED STUDY; CYTOCHROME P450 GENE; DISEASE CARRIER; GENE; GENE EXPRESSION; GENE FREQUENCY; GLUTATHIONE TRANSFERASE GENE; INSECT GENETICS; INSECTICIDE RESISTANCE; KDR GENE; MUTATION RATE; MUTATOR GENE; NONHUMAN; RURAL AREA; URBAN AREA;

ANIMALS; ANOPHELES; BIOLOGICAL ASSAY; BURKINA FASO; CULICIDAE; DDT; FEMALE; GENE FREQUENCY; GENOTYPE; GLUTATHIONE TRANSFERASE; HUMANS; INSECTICIDE RESISTANCE; INSECTICIDES; MODELS, GENETIC; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SPECIES SPECIFICITY; TRANSCRIPTION, GENETIC; URBANIZATION;

ANOPHELES (GENUS); ANOPHELES ARABIENSIS; ANOPHELES GAMBIAE; JOTURUS PICHARDI;

EID: 84866716350     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045995     Document Type: Article

References (66)

1. World Urbanization Prospects: the 2011 Revision [http://esa.un.org/unpd/wup/unup/index_panel1.html] Accessed September 4, 2012.
2. Hay SI, Guerra CA, Tatem AJ, Atkinson PM, Snow RW, (2005) Urbanization, malaria transmission and disease burden in Africa. Nat Rev Microbiol 3(1): 81-90.
3. Keiser J, Utzinger J, De Castro MC, Smith TA, Tanner M, et al. (2004) Urbanization in sub-Saharan Africa and implication for malaria control. Am J of Trop Med Hyg 71(2): 118-127.
4. Donnelly MJ, McCall PJ, Lengeler C, Bates I, D'Alessandro U, et al. (2005) Malaria and urbanization in sub-Saharan Africa. Malar J 4: 12.
5. Coetzee M, Craig M, le Sueur D, (2000) Distribution of African malaria mosquitoes belonging to the Anopheles gambiae complex. Parasitol Today 16(2): 74-77.
6. Coluzzi M, Sabatini A, Petrarca V, Dideco MA, (1979) Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. Trans R Soc Trop Med Hyg 73(5): 483-497.
7. Kerah-Hinzoumbé C, Peka M, Antonio-Nkondjio C, Donan-Gouni I, Awono-Ambene P, et al. (2009) Malaria vectors and transmission dynamics in Goulmoun, a rural city in south-western Chad. BMC Infect Dis 9: 71.
8. Sattler MA, Mtasiwa D, Kiama M, Premji Z, Tanner M, et al. (2005) Habitat characterization and spatial distribution of Anopheles sp. mosquito larvae in Dar es Salaam (Tanzania) during an extended dry period. Malar J 4: 4.
9. Fournet F, Cussac M, Ouari A, Meyer PE, Toé HK, et al. (2010) Diversity in anopheline larval habitats and adult composition during the dry and wet seasons in Ouagadougou (Burkina Faso). Malar J 2010 9: 78.
10. Kristan M, Fleischmann H, della Torre A, Stich A, Curtis CF, (2003) Pyrethroid resistance/susceptibility and differential urban/rural distribution of Anopheles arabiensis and An. gambiae s.s. malaria vectors in Nigeria and Ghana. Med Vet Ent 17(3): 326-332.
11. della Torre A, Tu ZJ, Petrarca V, (2005) On the distribution and genetic differentiation of Anopheles gambiae s.s. molecular forms. Insect Biochem Molec Biol 35(7): 755-769.
12. Chinery WA, (1984) Effects of ecological changes on the malaria vectors Anopheles funestus and the Anopheles gambiae complex of mosquitoes in Accra, Ghana. J Trop Med Hyg 87(2): 75-81.
13. Chouaïbou M, Etang J, Brévault T, Nwane P, Hinzoumbé CK, et al. (2008) Dynamics of insecticide resistance in the malaria vector Anopheles gambiae s.l. from an area of extensive cotton cultivation in Northern Cameroon. Trop Med Int Health 13(4): 476-486.
14. World Malaria Report (2010) World Health Organisation.
15. Ranson H, N'Guessan R, Lines J, Moiroux N, Nkuni Z, et al. (2011) Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol 27(2): 91-98.
16. van den Berg H, Zaim M, Yadav RS, Soares A, Ameneshewa B, et al. (2012) Global trends in the use of insecticides for vector-borne diseases. Environ Health Perspect 120(4): 577-582.
17. Alou LPA, Koffi AA, Adja MA, Tia E, Kouassi PK, 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.
18. Dabiré KR, Diabate A, Namountougou M, Toé KH, Ouari A, et al. (2009) Distribution of pyrethroid and DDT resistance and the L1014F kdr mutation in Anopheles gambiae s.l. from Burkina Faso (West Africa). Trans R Soc Trop Med Hyg 103(11): 1113-1120.
19. Yewhalaw D, Wassie F, Steurbaut W, Spanoghe P, Van Bortel, (2011) Multiple Insecticide Resistance: An Impediment to Insecticide-Based Malaria Vector Control Program. PLoS ONE 6(1): 10.1371/journal.pone.0016066.
20. Davies TGE, Field LM, Usherwood PNR, Williamson MS, (2007) DDT, pyrethrins, pyrethroids and insect sodium channels. IUBMB Life 59(3): 151-162.
21. Donnelly MJ, Corbel V, Weetman D, Wilding CS, Williamson MS, et al. (2009) Does kdr genotype predict insecticide-resistance phenotype in mosquitoes? Trends Parasitol. 25(5): 213-219.
22. Jones CM, Liyanapathirana M, Agossa FR, Weetman D, Ranson H, 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(17): 6614-6619.
23. Lynd A, Weetman D, Barbosa S, Yawson AE, Mitchell S, et al. (2010) Field, Genetic, and Modeling Approaches Show Strong Positive Selection Acting upon an Insecticide Resistance Mutation in Anopheles gambiae s.s. Mol Biol Evol 27(5): 1117-1125.
24. Diabaté A, Baldet T, Chandre E, Dabiré KR, Simard F, et al. (2004) First report of a kdr mutation in Anopheles arabiensis from Burkina Faso, West Africa. J Am Mosq Control Assoc 20(2): 195-196.
25. Djégbé I, Boussari O, Sidick A, Martin T, Ranson H, et al. (2011) Dynamics of insecticide resistance in malaria vectors in Benin: first evidence of the presence of L1014S kdr mutation in Anopheles gambiae from West Africa. Malar J 10: 261.
26. Santolamazza F, Calzetta M, Etang J, Barrese E, Dia I, et al. (2008) Distribution of knock-down resistance mutations in Anopheles gambiae molecular forms in west and west-central Africa. Malar J 7: 74.
27. Daborn PJ, Yen JL, Bogwitz MR, Le Goff G, Feil E, et al. (2002) A single P450 allele associated with insecticide resistance in Drosophila. Science 297(5590): 2253-2256.
28. Puinean AM, Foster SP, Oliphant L, Denholm I, Field LM, et al. (2010) Amplification of a Cytochrome P450 Gene Is Associated with Resistance to Neonicotinoid Insecticides in the Aphid Myzus persicae. PLoS Genetics 6(6): 10.1371/journal.pgen.1000999.
29. Muller P, Warr E, Stevenson BJ, Pignatelli PM, Morgan JC, et al. (2008) Field-Caught Permethrin-Resistant Anopheles gambiae Overexpress CYP6P3, a P450 That Metabolises Pyrethroids. PLoS Genetics 2008 4(11): 10.1371/journal.pgen.1000286.
30. Chiu TL, Wen ZM, Rupasinghe SG, Schuler MA, (2008) Comparative molecular modeling of Anopheles gambiae CYP6Z1, a mosquito P450 capable of metabolizing DDT. Proc Natl Acad Sci USA 105(26): 8855-8860.
31. Stevenson BJ, Bibby J, Pignatelli P, Muangnoicharoen S, O'Neill PM, et al. (2011) Cytochrome P450 6M2 from the malaria vector Anopheles gambiae metabolizes pyrethroids: Sequential metabolism of deltamethrin revealed. Insect Biochem Molec Biol 41(7): 492-502.
32. Ranson H, Rossiter L, Ortelli F, Jensen B, Wang XL, 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.
33. Mitchell SN, Stevenson BJ, Müller P, Wilding CS, Egyir-Yawson A, et al. (2012) Identification and validation of a gene causing cross-resistance between insecticide classes in Anopheles gambiae from Ghana. Proc Natl Acad Sci 109(16): 6147-6152.
34. Diabaté A, Baldet T, Chandre F, Akogbeto M, Guiguemde TR, et al. (2002) The role of agricultural use of insecticides in resistance to pyrethroids in Anopheles gambiae s.l. in Burkina Faso. Am J Trop Med Hyg 67(6): 617-622.
35. Djogbenou L, Dabiré R, Diabaté A, Kengne P, Akogbeto M, et al. (2008) Identification and geographic distribution of the ace-1R mutation in the malaria vector Anopheles gambiae in south-western Burkina Faso, West Africa. Am J Trop Med Hyg 78(2): 298-302.
36. World Health Organisation (1998) Test procedures for insecticide resistance monitoring in malaria vectors, bio-efficacy and persistence of insecticides on treated surfaces.
37. Scott JA, Brogdon WG, Collins FH, (1993) Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg 49(4): 520-529.
38. Bass C, Nikou D, Donnelly MJ, Williamson MS, Ranson H, et al. (2007) Detection of knockdown resistance (kdr) mutations in Anopheles gambiae: a comparison of two new high-throughput assays with existing methods. Malar J 6: 111.
39. Rodriguez S, Gaunt TR, Day INM, (2009) Hardy-Weinberg Equilibrium Testing of Biological Ascertainment for Mendelian Randomization Studies. Am J Epidemiol 169(4): 505-514.
40. David JP, Strode C, Vontas J, Nikou D, Vaughan A, 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(11): 4080-4084.
41. Huang DW, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1): 44-57.
42. Schmittgen TD, Livak KJ, (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3(6): 1101-1108.
43. Tarr PT, Tarling EJ, Bojanic DD, Edwards PA, Baldan A, (2009) Emerging new paradigms for ABCG transporters. BBA-Mol Cell Biol L 1791(7): 584-593.
44. Sarkadi B, Homolya L, Szakacs G, Varadi A, (2006) Human multidrug resistance ABCB and ABCG transporters: Participation in a chemoimmunity defense system. Physiol Rev 86(4): 1179-1236.
45. Marcombe S, Poupardin R, Darriet F, Reynaud S, Bonnet J, et al. (2009) Exploring the molecular basis of insecticide resistance in the dengue vector Aedes aegypti: a case study in Martinique Island (French West Indies). BMC Genomics 2009 10; 494.
46. Onyabe D, Conn JE, (2001) The Distribution of Two Major Malaria Vectors, Anopheles gambiae and Anopheles arabiensis, in Nigeria. Mem Inst Oswaldo Cruz, Rio de Janeiro 2001 98(8): 1081-1084.
47. Poupardin R, Riaz MA, Jones CM, Chandor-Proust A, Reynaud S, et al. (2012) Do pollutants affect insecticide-driven gene selection in mosquitoes? Experimental evidence from transcriptomics. Aquat Toxicol 114-115: 49-57.
48. Antonio-Nkondjio C, Fossog BT, Ndo C, Djantio BM, Togouet SZ, et al. (2011) Anopheles gambiae distribution and insecticide resistance in the cities of Douala and Yaounde (Cameroon): influence of urban agriculture and pollution. Malar J 10: 154.
49. Dongus S, Nyika D, Kannady K, Mtasiwa D, Mshinda H, et al. (2009) Urban agriculture and Anopheles habitats in Dar es Salaam, Tanzania. Geospatial Health 3(2): 189-210.
50. Badolo A, Traore A, Jones CM, Sanou A, Flood L, et al. (2012) Three years of insecticide resistance monitoring in Anopheles gambiae from Burkina Faso: resistance on the rise? Malar J 11: 232.
51. Himeidan YE, Chen H, Chandre F, Donnelly MJ, Yan G, (2007) Permethrin and DDT resistance in the malaria vector Anopheles arabiensis from eastern Sudan. Am J Trop Medicine Hyg 77(6): 1066-1068.
52. Ramphul U, Boase T, Bass C, Okedi LM, Donnelly MJ, et al. (2009) Insecticide resistance and its association with target-site mutations in natural populations of Anopheles gambiae from eastern Uganda. Trans R Soc Trop Med and Hyg 103(11): 1121-1126.
53. Stump AD, Atieli FK, Vulule JM, Besansky NJ, (2004) Dynamics of the pyrethroid knockdown resistance allele in western Kenyan populations of Anopheles gambiae in response to insecticide-treated bed net trials. Am J Trop Med Hyg 70(6): 591-596.
54. Djogbenou L, Pasteur N, Akogbeto M, Weill M, Chandre F, (2011) Insecticide resistance in the Anopheles gambiae complex in Benin: a nationwide survey. Med Vet Ent 25(3): 256-267.
55. Ranson H, Jensen B, Vulule JM, Wang X, Hemingway J, 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(5): 491-497.
56. Protopopoff N, Verhaeghen K, Van Bortel W, Roelants P, Marcotty T, et al. (2008) A significant increase in kdr in Anopheles gambiae is associated with an intensive vector control intervention in Burundi highlands. Trop Med Int Health 13(12): 1479-1487.
57. Burton MJ, Mellor IR, Duce IR, Davies TGE, Field LM, et al. (2011) Differential resistance of insect sodium channels with kdr mutations to deltamethrin, permethrin and DDT. Insect Biochem Mol Biol 41(9): 723-732.
58. Vontas J, David JP, Nikou D, Hemingway J, Christophides GK, et al. (2007) Transcriptional analysis of insecticide resistance in Anopheles stephensi using cross-species microarray hybridization. Insect Mol Biol 16(3): 315-324.
59. Muller P, Chouaibou M, Pignatelli P, Etang J, Walker ED, et al. (2008) Pyrethroid tolerance is associated with elevated expression of antioxidants and agricultural practice in Anopheles arabiensis sampled from an area of cotton fields in Northern Cameroon. Mol Ecol 17(4): 1145-1155.
60. Karunker I, Benting J, Lueke B, Ponge T, Nauen R, 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 Mol Biol 38(6): 634-644.
61. Prapanthadara LA, Hemingway J, Ketterman AJ, (1993) Partial purification and characterisation of glutathione s-transferases involved in DDT resistance from the mosquito Anopheles gambiae. Pest Biochem Physiol 47(2): 119-133.
62. Grant DF, Dietze EC, Hammock BD, (1991) Glutathione-S-transferase isozymes in Aedes aegypti- purification, characterization, and isozyme-specific regulation. Insect Biochem 21(4): 421-433.
63. Tang AH, Tu CPD, (1994) Biochemical characterization of Drosophila glutathione S-transferases D1 and D21. J Biol Chem 269(45): 27876-27884.
64. Gahan LJ, Pauchet Y, Vogel H, Heckel DG: An ABC Transporter Mutation Is Correlated with Insect Resistance to Bacillus thuringiensis Cry1Ac Toxin. PLoS Genetics 6(12): 10.1371/journal.pgen.1001248.
65. Buss DS, Callaghan A, (2008) Interaction of pesticides with p-glycoprotein and other ABC proteins: A survey of the possible importance to insecticide, herbicide and fungicide resistance. Pest Biochem Physiol 90(3): 141-153.
66. Bariami V, Jones CM, Poupardin R, Vontas J, Ranson H, (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(6): e1692.