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Permethrin induction of multiple cytochrome P450 genes in insecticide resistant mosquitoes, Culex quinquefasciatus.

ABSTRACT: The expression of some insect P450 genes can be induced by both exogenous and endogenous compounds and there is evidence to suggest that multiple constitutively overexpressed P450 genes are co-responsible for the development of resistance to permethrin in resistant mosquitoes. This study characterized the permethrin induction profiles of P450 genes known to be constitutively overexpressed in resistant mosquitoes, Culex quinquefasciatus. The gene expression in 7 of the 19 P450 genes CYP325K3v1, CYP4D42v2, CYP9J45, (CYP) CPIJ000926, CYP325G4, CYP4C38, CYP4H40 in the HAmCqG8 strain, increased more than 2-fold after exposure to permethrin at an LC50 concentration (10 ppm) compared to their acetone treated counterpart; no significant differences in the expression of these P450 genes in susceptible S-Lab mosquitoes were observed after permethrin treatment. Eleven of the fourteen P450 genes overexpressed in the MAmCqG6 strain, CYP9M10, CYP6Z12, CYP9J33, CYP9J43, CYP9J34, CYP306A1, CYP6Z15, CYP9J45, CYPPAL1, CYP4C52v1, CYP9J39, were also induced more than doubled after exposure to an LC50 (0.7 ppm) dose of permethrin. No significant induction in P450 gene expression was observed in the susceptible S-Lab mosquitoes after permethrin treatment except for CYP6Z15 and CYP9J39, suggesting that permethrin induction of these two P450 genes are common to both susceptible and resistant mosquitoes while the induction of the others are specific to insecticide resistant mosquitoes. These results demonstrate that multiple P450 genes are co-up-regulated in insecticide resistant mosquitoes through both constitutive overexpression and induction mechanisms, providing additional support for their involvement in the detoxification of insecticides and the development of insecticide resistance.

SUBMITTER: Gong Y

PROVIDER: S-EPMC3805894 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Permethrin induction of multiple cytochrome P450 genes in insecticide resistant mosquitoes, Culex quinquefasciatus.

Gong Youhui Y Li Ting T Zhang Lee L Gao Xiwu X Liu Nannan N

International journal of biological sciences 20130905 9

The expression of some insect P450 genes can be induced by both exogenous and endogenous compounds and there is evidence to suggest that multiple constitutively overexpressed P450 genes are co-responsible for the development of resistance to permethrin in resistant mosquitoes. This study characterized the permethrin induction profiles of P450 genes known to be constitutively overexpressed in resistant mosquitoes, Culex quinquefasciatus. The gene expression in 7 of the 19 P450 genes CYP325K3v1, C ...[more]

PMID: 24155662

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Project description:BackgroundThe Culex quinquefasciatus mosquito, a major pest and vector of filariasis and arboviruses in the tropics, has developed multiple resistance mechanisms to the main insecticide classes currently available in public health. Among them, the insensitive acetylcholinesterase (ace-1(R) allele) is widespread worldwide and confers cross-resistance to organophosphates and carbamates. Fortunately, in an insecticide-free environment, this mutation is associated with a severe genetic cost that can affect various life history traits. Salivary proteins are directly involved in human-vector contact during biting and therefore play a key role in pathogen transmission.Methods and resultsAn original proteomic approach combining 2D-electrophoresis and mass spectrometry was adopted to compare the salivary expression profiles of two strains of C. quinquefasciatus with the same genetic background but carrying either the ace-1(R) resistance allele or not (wild type). Four salivary proteins were differentially expressed (>2 fold, P<0.05) in susceptible (SLAB) and resistant (SR) mosquito strains. Protein identification indicated that the D7 long form, a major salivary protein involved in blood feeding success, presented lower expression in the resistant strain than the susceptible strain. In contrast, three other proteins, including metabolic enzymes (endoplasmin, triosephosphate isomerase) were significantly over-expressed in the salivary gland of ace-1(R) resistant mosquitoes. A catalogue of 67 salivary proteins of C. quinquefasciatus sialotranscriptome was also identified and described.ConclusionThe "resistance"-dependent expression of salivary proteins in mosquitoes may have considerable impact on biting behaviour and hence on the capacity to transmit parasites/viruses to humans. The behaviour of susceptible and insecticide-resistant mosquitoes in the presence of vertebrate hosts and its impact on pathogen transmission urgently requires further investigation.Data depositionAll proteomic data will be deposited at PRIDE (http://www.ebi.ac.uk/pride/).

Project description:To gain valuable insights into the gene interaction and the complex regulation system involved in the development of insecticide resistance in mosquitoes Culex quinquefasciatus, we conducted a whole transcriptome analysis of Culex mosquitoes following permethrin selection. Gene expression profiles for the lower resistant parental mosquito strain HAmCq(G0) and their permethrin-selected high resistant offspring HAmCq(G8) were compared and a total of 367 and 3982 genes were found to be up- and down-regulated, respectively, in HAmCq(G8), indicating that multiple genes are involved in response to permethrin selection. However, a similar overall cumulative gene expression abundance was identified between up- and down-regulated genes in HAmCq(G8) mosquitoes following permethrin selection, suggesting a homeostatic response to insecticides through a balancing of the up- and down-regulation of the genes. While structural and/or cuticular structural functions were the only two enriched GO terms for down-regulated genes, the enriched GO terms obtained for the up-regulated genes occurred primarily among the catalytic and metabolic functions where they represented three functional categories: electron carrier activity, binding, and catalytic activity. Interestingly, the functional GO terms in these three functional categories were overwhelmingly overrepresented in P450s and proteases/serine proteases. The important role played by P450s in the development of insecticide resistance has been extensively studied but the function of proteases/serine proteases in resistance is less well understood. Hence, the characterization of the functions of these proteins, including their digestive, catalytic and proteinase activities; regulation of signaling transduction and protein trafficking, immunity and storage; and their precise function in the development of insecticide resistance in mosquitoes will provide new insights into how genes are interconnected and regulated in resistance.

Project description:The mosquito Culex quinquefasciatus (Say) is a vector of human disease and a world-wide biting nuisance. Organophosphorus insecticides (OPs) have been widely used to control C. quinquefasciatus populations and this has led to the emergence of OP-resistance. Predominantly, resistance is caused by increased production of two non-specific carboxylesterases, Estalpha2(1) and Estbeta2(1). Increased abundance of these esterases is associated with the amplification of their respective genes. The estalpha21 and estbeta21 genes were cloned and sequenced from OP-resistant Sri Lankan C. quinquefasciatus; the two adjacent genes are in a head to head configuration, within a single amplification unit (amplicon). The homology between the two genes suggests that they arose from an ancient duplication event. The two genes have different numbers of exons (estalpha21 has seven and estbeta21 has four); however, the intron/exon boundaries in estbeta21 are all conserved in estalpha21. The two genes are co-amplified in three other mosquito strains with the elevated Estalpha2(1)/Estbeta2(1) phenotype. Their complete linkage disequilibrium is explained by the location of the two genes involved in resistance within a single amplicon. In insecticide-susceptible C. quinquefasciatus, the non-amplified estalpha and estbeta gene loci are also found in a similar head to head configuration, but the size of the intergenic non-coding region is approx. 1 kb less than in the amplicon. The smaller intergenic spacer is also found in a strain with amplified estbeta11, which suggests that extensive laboratory selection for this amplified esterase has not eliminated the non-amplified genes. The intergenic spacer regions have been subcloned and sequenced. They contain numerous possible TATA boxes, promoters and a number of possible regulatory elements with high homology to the consensus sequence of the Barbie box. These latter putative regulatory elements are more numerous in the larger intergenic spacer, which differs from the non-amplified spacer by two large (>>420 bp) and one small (5 bp) insertions.

Dataset Information

Permethrin induction of multiple cytochrome P450 genes in insecticide resistant mosquitoes, Culex quinquefasciatus.

Publications

Permethrin induction of multiple cytochrome P450 genes in insecticide resistant mosquitoes, Culex quinquefasciatus.

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