| |
A single mutation in the GSTe2 gene allows tracking of metabolically based insecticide resistance in a major malaria vector
- 作者:Jacob M Riveron (1)
Cristina Yunta (1) (2) Sulaiman S Ibrahim (1) Rousseau Djouaka (3) Helen Irving (1) Benjamin D Menze (1) (4) Hanafy M Ismail (1) Janet Hemingway (1) Hilary Ranson (1) Armando Albert (2) Charles S Wondji (1)
- 刊名:Genome Biology
- 出版年:2014
- 出版时间:February 2014
- 年:2014
- 卷:15
- 期:2
- 全文大小:1,482 KB
- 参考文献:1. World Health Organization: / Global Plan for Insecticide Resistance Management (GPIRM). Geneva, Switzerland; 2012.
2. Hemingway J, Ranson H: g class="a-plus-plus">Insecticide resistance in insect vectors of human disease.g> / Annual Review Entomol 2000, g class="a-plus-plus">45:g>369鈥?89. g/10.1146/annurev.ento.45.1.371" target="_blank" title="It opens in new window">CrossRef 3. David JP, Strode C, Vontas J, Nikou D, Vaughan A, Pignatelli PM, Louis C, Hemingway J, Ranson H: g class="a-plus-plus">Theg> g class="a-plus-plus">Anopheles gambiaeg> g class="a-plus-plus">detoxification chip: a highly specific microarray to study metabolic-based insecticide resistance in malaria vectors.g> / Proc Natl Acad Sci USA 2005, g class="a-plus-plus">102:g>4080鈥?084. g/10.1073/pnas.0409348102" target="_blank" title="It opens in new window">CrossRef 4. Muller P, Warr E, Stevenson BJ, Pignatelli PM, Morgan JC, Steven A, Yawson AE, Mitchell SN, Ranson H, Hemingway J, Paine MJ, Donnelly MJ: g class="a-plus-plus">Field-caught permethrin-resistantg> g class="a-plus-plus">Anopheles gambiaeg> g class="a-plus-plus">overexpress CYP6P3, a P450 that metabolises pyrethroids.g> / PLoS Genet 2008, g class="a-plus-plus">4:g>e1000286. g/10.1371/journal.pgen.1000286" target="_blank" title="It opens in new window">CrossRef 5. Riveron JM, Irving H, Ndula M, Barnes KG, Ibrahim SS, Paine MJ, Wondji CS: g class="a-plus-plus">Directionally selected cytochrome P450 alleles are driving the spread of pyrethroid resistance in the major malaria vectorg> g class="a-plus-plus">Anopheles funestusg> g class="a-plus-plus">.g> / Proc Natl Acad Sci USA 2013, g class="a-plus-plus">110:g>252鈥?57. g/10.1073/pnas.1216705110" target="_blank" title="It opens in new window">CrossRef 6. Djouaka R, Irving H, Tukur Z, Wondji CS: g class="a-plus-plus">Exploring mechanisms of multiple insecticide resistance in a population of the malaria vectorg> g class="a-plus-plus">Anopheles funestusg> g class="a-plus-plus">in Benin.g> / PLoS One 2011, g class="a-plus-plus">6:g>e27760. g/10.1371/journal.pone.0027760" target="_blank" title="It opens in new window">CrossRef 7. Ranson H, Rossiter L, Ortelli F, Jensen B, Wang X, Roth CW, Collins FH, Hemingway J: g class="a-plus-plus">Identification of a novel class of insect glutathione S-transferases involved in resistance to DDT in the malaria vectorg> g class="a-plus-plus">Anopheles gambiaeg> g class="a-plus-plus">.g> / Biochem J 2001, g class="a-plus-plus">359:g>295鈥?04. g/10.1042/0264-6021:3590295" target="_blank" title="It opens in new window">CrossRef 8. Lumjuan N, Rajatileka S, Changsom D, Wicheer J, Leelapat P, Prapanthadara LA, Somboon P, Lycett G, Ranson H: g class="a-plus-plus">The role of theg> g class="a-plus-plus">Aedes aegyptig> g class="a-plus-plus">epsilon glutathione transferases in conferring resistance to DDT and pyrethroid insecticides.g> / Insect Biochem Mol Biol 2011, g class="a-plus-plus">41:g>203鈥?09. g/10.1016/j.ibmb.2010.12.005" target="_blank" title="It opens in new window">CrossRef 9. Morgan JC, Irving H, Okedi LM, Steven A, Wondji CS: g class="a-plus-plus">Pyrethroid resistance in ang> g class="a-plus-plus">Anopheles funestusg> g class="a-plus-plus">population from Uganda.g> / PLoS One 2010, g class="a-plus-plus">5:g>e11872. g/10.1371/journal.pone.0011872" target="_blank" title="It opens in new window">CrossRef 10. Ramphul U, Boase T, Bass C, Okedi LM, Donnelly MJ, Muller P: g class="a-plus-plus">Insecticide resistance and its association with target-site mutations in natural populations ofg> g class="a-plus-plus">Anopheles gambiaeg> g class="a-plus-plus">from eastern Uganda.g> / Trans R Soc Trop Med Hyg 2009, g class="a-plus-plus">103:g>1121鈥?126. g/10.1016/j.trstmh.2009.02.014" target="_blank" title="It opens in new window">CrossRef 11. Chiu TL, Wen Z, Rupasinghe SG, Schuler MA: g class="a-plus-plus">Comparative molecular modeling ofg> g class="a-plus-plus">Anopheles gambiaeg> g class="a-plus-plus">CYP6Z1, a mosquito P450 capable of metabolizing DDT.g> / Proc Natl Acad Sci USA 2008, g class="a-plus-plus">105:g>8855鈥?860. g/10.1073/pnas.0709249105" target="_blank" title="It opens in new window">CrossRef 12. Mitchell SN, Stevenson BJ, Muller P, Wilding CS, Egyir-Yawson A, Field SG, Hemingway J, Paine MJ, Ranson H, Donnelly MJ: g class="a-plus-plus">Identification and validation of a gene causing cross-resistance between insecticide classes ing> g class="a-plus-plus">Anopheles gambiaeg> g class="a-plus-plus">from Ghana.g> / Proc Natl Acad Sci USA 2012, g class="a-plus-plus">109:g>6147鈥?152. g/10.1073/pnas.1203452109" target="_blank" title="It opens in new window">CrossRef 13. Daborn PJ, Lumb C, Boey A, Wong W, Ffrench-Constant RH, Batterham P: g class="a-plus-plus">Evaluating the insecticide resistance potential of eightg> g class="a-plus-plus">Drosophila melanogasterg> g class="a-plus-plus">cytochrome P450 genes by transgenic over-expression.g> / Insect Biochem Mol Biol 2007, g class="a-plus-plus">37:g>512鈥?19. g/10.1016/j.ibmb.2007.02.008" target="_blank" title="It opens in new window">CrossRef 14. Kostaropoulos I, Papadopoulos AI, Metaxakis A, Boukouvala E, Papadopoulou-Mourkidou E: g class="a-plus-plus">Glutathione S-transferase in the defence against pyrethroids in insects.g> / Insect Biochem Mol Biol 2001, g class="a-plus-plus">31:g>313鈥?19. g/10.1016/S0965-1748(00)00123-5" target="_blank" title="It opens in new window">CrossRef 15. Vontas JG, Small GJ, Hemingway J: g class="a-plus-plus">Glutathione S-transferases as antioxidant defence agents confer pyrethroid resistance ing> g class="a-plus-plus">Nilaparvata lugensg> g class="a-plus-plus">.g> / Biochem J 2001, g class="a-plus-plus">357:g>65鈥?2. g/10.1042/0264-6021:3570065" target="_blank" title="It opens in new window">CrossRef 16. Daborn PJ, Yen JL, Bogwitz MR, Le Goff G, Feil E, Jeffers S, Tijet N, Perry T, Heckel D, Batterham P, Feyereisen R, Wilson TG, ffrench-Constant RH: g class="a-plus-plus">A single p450 allele associated with insecticide resistance ing> g class="a-plus-plus">Drosophilag> g class="a-plus-plus">.g> / Science 2002, g class="a-plus-plus">297:g>2253鈥?256. g/10.1126/science.1074170" target="_blank" title="It opens in new window">CrossRef 17. Campbell PM, Newcomb RD, Russell RJ, Oakeshott JG: g class="a-plus-plus">Two different amino acid substitutions in the ali-esterase, E3, confer alternative types of organophosphorus insecticide resistance in the sheep blowfly,g> g class="a-plus-plus">Lucilia cuprinag> g class="a-plus-plus">.g> / Insect Biochem Mol Biol 1998, g class="a-plus-plus">28:g>139鈥?50. g/10.1016/S0965-1748(97)00109-4" target="_blank" title="It opens in new window">CrossRef 18. Claudianos C, Russell RJ, Oakeshott JG: g class="a-plus-plus">The same amino acid substitution in orthologous esterases confers organophosphate resistance on the house fly and a blowfly.g> / Insect Biochem Mol Biol 1999, g class="a-plus-plus">29:g>675鈥?86. g/10.1016/S0965-1748(99)00035-1" target="_blank" title="It opens in new window">CrossRef 19. Okoye PN, Brooke BD, Koekemoer LL, Hunt RH, Coetzee M: g class="a-plus-plus">Characterisation of DDT, pyrethroid and carbamate resistance ing> g class="a-plus-plus">Anopheles funestusg> g class="a-plus-plus">from Obuasi, Ghana.g> / Trans R Soc Trop Med Hyg 2008, g class="a-plus-plus">102:g>591鈥?98. g/10.1016/j.trstmh.2008.02.022" target="_blank" title="It opens in new window">CrossRef 20. Wondji CS, Dabire RK, Tukur Z, Irving H, Djouaka R, Morgan JC: g class="a-plus-plus">Identification and distribution of a GABA receptor mutation conferring dieldrin resistance in the malaria vectorg> g class="a-plus-plus">Anopheles funestusg> g class="a-plus-plus">in Africa.g> / Insect Biochem Mol Biol 2011, g class="a-plus-plus">41:g>484鈥?91. g/10.1016/j.ibmb.2011.03.012" target="_blank" title="It opens in new window">CrossRef 21. Cuamba N, Morgan JC, Irving H, Steven A, Wondji CS: g class="a-plus-plus">High level of pyrethroid resistance in ang> g class="a-plus-plus">Anopheles funestusg> g class="a-plus-plus">population of the Chokwe District in Mozambique.g> / PLoS One 2010, g class="a-plus-plus">5:g>e11010. g/10.1371/journal.pone.0011010" target="_blank" title="It opens in new window">CrossRef 22. Wondji CS, Coleman M, Kleinschmidt I, Mzilahowa T, Irving H, Ndula M, Rehman A, Morgan J, Barnes KG, Hemingway J: g class="a-plus-plus">Impact of pyrethroid resistance on operational malaria control in Malawi.g> / Proc Natl Acad Sci USA 2012, g class="a-plus-plus">109:g>19063鈥?9070. g/10.1073/pnas.1217229109" target="_blank" title="It opens in new window">CrossRef 23. Huang H, Yao H, Liu JY, Samra AI, Kamita SG, Cornel AJ, Hammock BD: g class="a-plus-plus">Development of pyrethroid-like fluorescent substrates for glutathione S-transferase.g> / Anal Biochem 2012, g class="a-plus-plus">431:g>77鈥?3. g/10.1016/j.ab.2012.09.011" target="_blank" title="It opens in new window">CrossRef 24. Biswas S, Akey JM: g class="a-plus-plus">Genomic insights into positive selection.g> / Trends Genet 2006, g class="a-plus-plus">22:g>437鈥?46. g/10.1016/j.tig.2006.06.005" target="_blank" title="It opens in new window">CrossRef 25. Schlenke TA, Begun DJ: g class="a-plus-plus">Strong selective sweep associated with a transposon insertion ing> g class="a-plus-plus">Drosophila simulansg> g class="a-plus-plus">.g> / Proc Natl Acad Sci USA 2004, g class="a-plus-plus">101:g>1626鈥?631. g/10.1073/pnas.0303793101" target="_blank" title="It opens in new window">CrossRef 26. Michel AP, Ingrasci MJ, Schemerhorn BJ, Kern M, Le Goff G, Coetzee M, Elissa N, Fontenille D, Vulule J, Lehmann T, Sagnon N, Costantini C, Besansky NJ: g class="a-plus-plus">Rangewide population genetic structure of the African malaria vectorg> g class="a-plus-plus">Anopheles funestusg> g class="a-plus-plus">.g> / Mol Ecol 2005, g class="a-plus-plus">14:g>4235鈥?248. g/10.1111/j.1365-294X.2005.02754.x" target="_blank" title="It opens in new window">CrossRef 27. Wang Y, Qiu L, Ranson H, Lumjuan N, Hemingway J, Setzer WN, Meehan EJ, Chen L: g class="a-plus-plus">Structure of an insect epsilon class glutathione S-transferase from the malaria vectorg> g class="a-plus-plus">Anopheles gambiaeg> g class="a-plus-plus">provides an explanation for the high DDT-detoxifying activity.g> / J Struct Biol 2008, g class="a-plus-plus">164:g>228鈥?35. g/10.1016/j.jsb.2008.08.003" target="_blank" title="It opens in new window">CrossRef 28. Schmittgen TD, Livak KJ: g class="a-plus-plus">Analyzing real-time PCR data by the comparative C (T) method.g> / Nat Protoc 2008, g class="a-plus-plus">3:g>1101鈥?108. g/10.1038/nprot.2008.73" target="_blank" title="It opens in new window">CrossRef 29. Markstein M, Pitsouli C, Villalta C, Celniker SE, Perrimon N: g class="a-plus-plus">Exploiting position effects and the gypsy retrovirus insulator to engineer precisely expressed transgenes.g> / Nat Genet 2008, g class="a-plus-plus">40:g>476鈥?83. g/10.1038/ng.101" target="_blank" title="It opens in new window">CrossRef 30. Thompson JD, Higgins DG, Gibson TJ: g class="a-plus-plus">CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.g> / Nucleic Acids Res 1994, g class="a-plus-plus">22:g>4673鈥?680. g/10.1093/nar/22.22.4673" target="_blank" title="It opens in new window">CrossRef 31. Rozas J: g class="a-plus-plus">DNA sequence polymorphism analysis using DnaSP.g> / Methods Mol Biol 2009, g class="a-plus-plus">537:g>337鈥?50. g/10.1007/978-1-59745-251-9_17" target="_blank" title="It opens in new window">CrossRef 32. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: g class="a-plus-plus">MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.g> / Mol Biol Evol 2011, g class="a-plus-plus">28:g>2731鈥?739. g/10.1093/molbev/msr121" target="_blank" title="It opens in new window">CrossRef 33. Clement M, Posada D, Crandall KA: g class="a-plus-plus">TCS: a computer program to estimate gene genealogies.g> / Mol Ecol 2000, g class="a-plus-plus">9:g>1657鈥?659. g/10.1046/j.1365-294x.2000.01020.x" target="_blank" title="It opens in new window">CrossRef 34. Kwiatkowska RM, Platt N, Poupardin R, Irving H, Dabire RK, Mitchell S, Jones CM, Diabate A, Ranson H, Wondji CS: g class="a-plus-plus">Dissecting the mechanisms responsible for the multiple insecticide resistance phenotype ing> g class="a-plus-plus">Anopheles gambiaeg> g class="a-plus-plus">s.s., M form, from Vallee du Kou, Burkina Faso.g> / Gene 2013, g class="a-plus-plus">519:g>98鈥?06. g/10.1016/j.gene.2013.01.036" target="_blank" title="It opens in new window">CrossRef 35. Hudson RR, Slatkin M, Maddison WP: g class="a-plus-plus">Estimation of levels of gene flow from DNA sequence data.g> / Genetics 1992, g class="a-plus-plus">132:g>583鈥?89. 36. Zhang Z, Li J, Zhao XQ, Wang J, Wong GK, Yu J: g class="a-plus-plus">KaKs_calculator: calculating Ka and Ks through model selection and model averaging.g> / Genomics Proteomics Bioinformatics 2006, g class="a-plus-plus">4:g>259鈥?63. g/10.1016/S1672-0229(07)60007-2" target="_blank" title="It opens in new window">CrossRef 37. Nei M, Gojobori T: g class="a-plus-plus">Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions.g> / Mol Biol Evol 1986, g class="a-plus-plus">3:g>418鈥?26. 38. Kabsch W: g class="a-plus-plus">Xds.g> / Acta Crystallogr D Biol Crystallogr 2010, g class="a-plus-plus">66:g>125鈥?32. g/10.1107/S0907444909047337" target="_blank" title="It opens in new window">CrossRef 39. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ: g class="a-plus-plus">Phaser crystallographic software.g> / J Appl Crystallogr 2007, g class="a-plus-plus">40:g>658鈥?74. g/10.1107/S0021889807021206" target="_blank" title="It opens in new window">CrossRef 40. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH: g class="a-plus-plus">PHENIX: a comprehensive Python-based system for macromolecular structure solution.g> / Acta Crystallogr D Biol Crystallogr 2010, g class="a-plus-plus">66:g>213鈥?21. g/10.1107/S0907444909052925" target="_blank" title="It opens in new window">CrossRef
- 作者单位:Jacob M Riveron (1)
Cristina Yunta (1) (2) Sulaiman S Ibrahim (1) Rousseau Djouaka (3) Helen Irving (1) Benjamin D Menze (1) (4) Hanafy M Ismail (1) Janet Hemingway (1) Hilary Ranson (1) Armando Albert (2) Charles S Wondji (1)
1. Vector Biology Department, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool, L3 5QA, United Kingdom 2. Departamento de Cristalograf铆a y Biolog铆a Estructural, Instituto de Qu铆mica-F铆sica 鈥淩ocasolano鈥? CSIC, C/Serrano 119, Madrid, E-28006, Spain 3. International Institute of Tropical Agriculture, 08 BP, 0932, Cotonou, Benin 4. Organisation de Coordination pour la lutte contre les End茅mies en Afrique Centrale, PO Box 288, Yaound茅, Cameroon
- ISSN:1465-6906
文摘
Background Metabolic resistance to insecticides is the biggest threat to the continued effectiveness of malaria vector control. However, its underlying molecular basis, crucial for successful resistance management, remains poorly characterized. Results Here, we demonstrate that the single amino acid change L119F in an upregulated glutathione S-transferase gene, GSTe2, confers high levels of metabolic resistance to DDT in the malaria vector Anopheles funestus. Genome-wide transcription analysis revealed that GSTe2 was the most over-expressed detoxification gene in DDT and permethrin-resistant mosquitoes from Benin. Transgenic expression of GSTe2 in Drosophila melanogaster demonstrated that over-transcription of this gene alone confers DDT resistance and cross-resistance to pyrethroids. Analysis of GSTe2 polymorphism established that the point mutation is tightly associated with metabolic resistance to DDT and its geographical distribution strongly correlates with DDT resistance patterns across Africa. Functional characterization of recombinant GSTe2 further supports the role of the L119F mutation, with the resistant allele being more efficient at metabolizing DDT than the susceptible one. Importantly, we also show that GSTe2 directly metabolizes the pyrethroid permethrin. Structural analysis reveals that the mutation confers resistance by enlarging the GSTe2 DDT-binding cavity, leading to increased DDT access and metabolism. Furthermore, we show that GSTe2 is under strong directional selection in resistant populations, and a restriction of gene flow is observed between African regions, enabling the prediction of the future spread of this resistance. Conclusions This first DNA-based metabolic resistance marker in mosquitoes provides an essential tool to track the evolution of resistance and to design suitable resistance management strategies.
| |
NGLC 2004-2010.National Geological Library of China All Rights Reserved.
Add:29 Xueyuan Rd,Haidian District,Beijing,PRC. Mail Add: 8324 mailbox 100083
For exchange or info please contact us via email.
| |