single mutation in the GSTe2 gene allows tracking of metabolically based insecticide resistance in a major malaria vector

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 ac...

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Published in:	Genome biology Vol. 15; no. 2; pp. R27 - 27
Main Authors:	Riveron, Jacob M, Yunta, Cristina, Ibrahim, Sulaiman S, Djouaka, Rousseau, Irving, Helen, Menze, Benjamin D, Ismail, Hanafy M, Hemingway, Janet, Ranson, Hilary, Albert, Armando, Wondji, Charles S
Format:	Journal Article
Language:	English
Published:	London Springer-Verlag 25.02.2014 BioMed Central
Subjects:	Africa Alleles Animal Genetics and Genomics Animals Anopheles - drug effects Anopheles - genetics Anopheles funestus Benin Bioinformatics Biomedical and Life Sciences cross resistance Crystallography, X-Ray DDT (pesticide) DDT - toxicity Drosophila melanogaster evolution Evolutionary Biology gene expression regulation gene flow gene overexpression genes geographical distribution glutathione transferase Glutathione Transferase - chemistry Glutathione Transferase - genetics Human Genetics Humans Insect Vectors - drug effects Insect Vectors - genetics insecticide resistance Insecticide Resistance - genetics Life Sciences malaria Malaria - genetics Malaria - transmission Microbial Genetics and Genomics Molecular Sequence Data Mutation permethrin Plant Genetics and Genomics point mutation Pyrethrins - metabolism resistance management vector control Benin Africa Root Mean Square Deviation Pyrethroid Resistance Indoor Residual Spray Deltamethrin L119F Mutation
ISSN:	1465-6906, 1474-760X, 1465-6914, 1474-760X
Online Access:	Get full text
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Abstract	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.
AbstractList	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. 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.BACKGROUNDMetabolic 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.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.RESULTSHere, 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.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.CONCLUSIONSThis 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. 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. 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. 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. 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.
ArticleNumber	R27
Author	Ismail, Hanafy M Menze, Benjamin D Djouaka, Rousseau Yunta, Cristina Riveron, Jacob M Ranson, Hilary Albert, Armando Irving, Helen Ibrahim, Sulaiman S Wondji, Charles S Hemingway, Janet
AuthorAffiliation	2 Departamento de Cristalografía y Biología Estructural, Instituto de Química-Física “Rocasolano”, CSIC, C/Serrano 119 Madrid E-28006, Spain 1 Vector Biology Department, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, United Kingdom 4 Organisation de Coordination pour la lutte contre les Endémies en Afrique Centrale, PO Box 288, Yaoundé, Cameroon 3 International Institute of Tropical Agriculture, 08 BP 0932 Cotonou, Benin
AuthorAffiliation_xml	– name: 2 Departamento de Cristalografía y Biología Estructural, Instituto de Química-Física “Rocasolano”, CSIC, C/Serrano 119 Madrid E-28006, Spain – name: 4 Organisation de Coordination pour la lutte contre les Endémies en Afrique Centrale, PO Box 288, Yaoundé, Cameroon – name: 3 International Institute of Tropical Agriculture, 08 BP 0932 Cotonou, Benin – name: 1 Vector Biology Department, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, United Kingdom
Author_xml	– sequence: 1 fullname: Riveron, Jacob M – sequence: 2 fullname: Yunta, Cristina – sequence: 3 fullname: Ibrahim, Sulaiman S – sequence: 4 fullname: Djouaka, Rousseau – sequence: 5 fullname: Irving, Helen – sequence: 6 fullname: Menze, Benjamin D – sequence: 7 fullname: Ismail, Hanafy M – sequence: 8 fullname: Hemingway, Janet – sequence: 9 fullname: Ranson, Hilary – sequence: 10 fullname: Albert, Armando – sequence: 11 fullname: Wondji, Charles S
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/24565444$$D View this record in MEDLINE/PubMed
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Snippet	BACKGROUND: Metabolic resistance to insecticides is the biggest threat to the continued effectiveness of malaria vector control. However, its underlying... Background Metabolic resistance to insecticides is the biggest threat to the continued effectiveness of malaria vector control. However, its underlying... Metabolic resistance to insecticides is the biggest threat to the continued effectiveness of malaria vector control. However, its underlying molecular basis,... Background: Metabolic resistance to insecticides is the biggest threat to the continued effectiveness of malaria vector control. However, its underlying...
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SubjectTerms	Africa Alleles Animal Genetics and Genomics Animals Anopheles - drug effects Anopheles - genetics Anopheles funestus Benin Bioinformatics Biomedical and Life Sciences cross resistance Crystallography, X-Ray DDT (pesticide) DDT - toxicity Drosophila melanogaster evolution Evolutionary Biology gene expression regulation gene flow gene overexpression genes geographical distribution glutathione transferase Glutathione Transferase - chemistry Glutathione Transferase - genetics Human Genetics Humans Insect Vectors - drug effects Insect Vectors - genetics insecticide resistance Insecticide Resistance - genetics Life Sciences malaria Malaria - genetics Malaria - transmission Microbial Genetics and Genomics Molecular Sequence Data Mutation permethrin Plant Genetics and Genomics point mutation Pyrethrins - metabolism resistance management vector control
Title	single mutation in the GSTe2 gene allows tracking of metabolically based insecticide resistance in a major malaria vector
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