Abstract
The role of ATP-binding cassette (ABC) transporters in conferring insecticide resistance has received much attention recently. Here we identify ABC transporters differentially expressed in insecticide-resistant populations of the malaria vector, Anopheles gambiae. Although we found little evidence that the orthologues of the multidrug resistance proteins described in other species are associated with resistance in An.gambiae we did identify a subset of ABC proteins consistently differentially expressed in pyrethroid-resistant populations from across Africa. We present information on the phylogenetic relationship, primary sites of expression and potential role of ABC transporters in mediating the mosquito's response to insecticides. Furthermore we demonstrate that a paralogous group of eight ABCG transporters, clustered on chromosome 3R, are highly enriched in the legs of An.gambiae mosquitoes, consistent with a proposed role for this ABC subfamily in transport of lipids to the outer surface of the cuticle. Finally, antibodies raised against one of the most highly expressed ABC transporters in adult females, ABCG7 (AGAP009850), localized this transporter to the pericardial cells. These data will help prioritize members of this gene family for further localization and functional validation studies to identify the in vivo function of these transporters in the mosquito and determine whether elevated expression of members of this family contribute to insecticide resistance.
Highlights
The mosquito species Anopheles gambiae is responsible for the majority of malaria transmission in Africa and has been subject to extensive control efforts using insecticides
In this study we provide an updated catalogue of the ATP-binding cassette (ABC) transporters in An. gambiae and, via a metaanalysis of multiple microarray datasets comparing gene expression in pyrethroid resistant and susceptible populations of this species, identify members of this gene family that are repeatedly found up-regulated in pyrethroid-resistant populations
Much has been written about the role of ABC transporters in conferring resistance to insecticides, in many cases the evidence is largely limited to correlations with whole body gene expression, which may miss significant hits and gives little insight into the mechanisms by which these transporters might contribute to the resistance phenotype
Summary
The mosquito species Anopheles gambiae is responsible for the majority of malaria transmission in Africa and has been subject to extensive control efforts using insecticides. ABC transporters are transmembrane ATP-dependent efflux pumps that mediate the transport of compounds out of the cell or into cellular organelles They can transport a wide range of endogenous and exogenous compounds and some members of this family have nontransport functions, such as control of protein biosynthesis (Dean et al, 2001). Further studies have shown that exposure to the ABC inhibitor verapamil synergizes the activity of insecticides in some insect species (Figueira-Mansur et al, 2013; Epis et al, 2014; Lima et al, 2014) Whilst these studies are supportive of the hypothesis that over-expression of ABC transporters can protect insects against insecticides by protecting tissues few have directly demonstrated that insect ABC transporters can transport insecticides and only a small number of studies have considered the tissue distribution of these transporters. By phylogenetic comparisons to other dipteran ABC gene families, reference to both an excellent recent review on the ABCs in other arthropod species (Dermauw & Van Leeuwen, 2014), and published transcriptomic studies (Pitts et al, 2011; Gabrieli et al, 2014; Matthews et al, 2016), and by conducting quantitative PCR (qPCR) and immunolocalization experiments on a subset of this gene family, we provide new insights into the tissue localization and putative functions of members of this gene family
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