Dissecting the mechanisms responsible for the multiple insecticide resistance phenotype in Anopheles gambiae s.s., M form, from Vallée du Kou, Burkina Faso

Rachel M Kwiatkowska,Naomi Platt,Rodolphe Poupardin,Helen Irving,Roch K Dabire,Sara Mitchell,Christopher M Jones,Abdoulaye Diabaté,Hilary Ranson,Charles S Wondji

doi:10.1016/j.gene.2013.01.036

Rachel M Kwiatkowska, Naomi Platt + Show 8 more

Open Access

https://doi.org/10.1016/j.gene.2013.01.036

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Abstract

With the exception of target site mutations, insecticide resistance mechanisms in the principle malaria vector Anopheles gambiae, remains largely uncharacterized in Burkina Faso.Here we detected high prevalence of resistance in Vallée du Kou (VK) to pyrethroids, DDT and dieldrin, moderate level for carbamates and full susceptibility to organophosphates. High frequencies of L1014F kdr (75%) and Rdl (87%) mutations were observed showing strong correlation with pyrethroids/DDT and dieldrin resistance. The frequency of ace1R mutation was low even in carbamate resistant mosquitoes. Microarray analysis identified genes significantly over-transcribed in VK. These include the cytochrome P450 genes, CYP6P3 and CYP6Z2, previously associated with pyrethroid resistance. Gene Ontology (GO) enrichment analysis suggested that elevated neurotransmitter activity is associated with resistance, with the over-transcription of target site resistance genes such as acetylcholinesterase and the GABA receptor. A rhodopsin receptor gene previously associated with pyrethroid resistance in Culex pipiens pallens was also over-transcribed in VK.This study highlights the complex network of mechanisms conferring multiple resistance in malaria vectors and such information should be taken into account when designing and implementing resistance control strategies.

Highlights

Malaria is endemic in Burkina Faso (West Africa) where it is the main cause of morbidity and mortality (MoH, Burkina Faso)
Vallée du Kou is surrounded by agricultural land which has long been exposed to pesticides, contributing to the Abbreviations: VK, Vallée du Kou; DDT, dichlorodiphenyltrichloroethane; kdr, knockdown resistance; RDL, resistance to dieldrin; GO, Gene Ontology; MoH, Ministry of Health; IRS, indoor residual spraying; long lasting insecticides nets (LLINs), long lasting insecticide nets; AChE, acetylcholinesterase; GSTs, glutathione-S-transferases; WHO, World Health Organization; SINE, short interspersed element; FC, fold change; sHSP, small Heat Shock Protein; qRT-PCR, quantitative reverse transcriptase polymerase chain reaction; GABA, gammaaminobutyric acid
All bioassay tests were carried out using F1 mosquitoes generated from indoor-collected blood-fed female A. gambiae s.l. from VK1 (n = 226), VK2 (= 241), VK3 (n = 292), VK6 (n = 311) and VK7 (n= 225)

Summary

Introduction

Malaria is endemic in Burkina Faso (West Africa) where it is the main cause of morbidity and mortality (MoH, Burkina Faso). Current efforts to control malaria in Burkina Faso, as elsewhere in Africa, rely on vector control methods such as long lasting insecticides nets (LLINs) and indoor residual spraying (IRS) (Dabiré et al, 2012). Insecticide resistance in malaria vectors is widely reported in Burkina Faso and has been linked to the heavy agricultural use of insecticides (Dabiré et al, 2012; Diabate et al, 2002a). Vallée du Kou is surrounded by agricultural land which has long been exposed to pesticides, contributing to the Abbreviations: VK, Vallée du Kou; DDT, dichlorodiphenyltrichloroethane; kdr, knockdown resistance; RDL, resistance to dieldrin; GO, Gene Ontology; MoH, Ministry of Health; IRS, indoor residual spraying; LLINs, long lasting insecticide nets; AChE, acetylcholinesterase; GSTs, glutathione-S-transferases; WHO, World Health Organization; SINE, short interspersed element; FC, fold change; sHSP, small Heat Shock Protein; qRT-PCR, quantitative reverse transcriptase polymerase chain reaction; GABA, gammaaminobutyric acid.

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