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Evolutionary adaptation of the amino acid and codon usage of the mosquito sodium channel following insecticide selection in the field mosquitoes.

ABSTRACT: Target site insensitivity resulting from point mutations within the voltage-gated sodium channel of the insect nervous system is known to be of primary importance in the development of resistance to pyrethroid insecticides. This study shifts current research paradigms by conducting, for the first time, a global analysis of all the naturally occurring mutations, both nonsynonymous and synonymous mutations, as well as mutation combinations in the entire mosquito sodium channel of Culex quinquefasciatus and analyzing their evolutionary and heritable feature and roles in insecticide resistance. Through a systematic analysis of comparing nucleotide polymorphisms in the entire sodium channel cDNAs of individuals between susceptible and resistant mosquito strains, between field parental mosquitoes and their permethrin selected offspring, and among different mosquito groups categorized by their levels of tolerance to specific permethrin concentrations within and among the mosquito strains of the field parental strains and their permethrin selected offspring, 3 nonsynonymous (A(109)S, L(982)F, and W(1573)R) and 6 synonymous (L(852), G(891), A(1241), D(1245), P(1249), and G(1733)) mutations were identified. The co-existence of all 9 mutations, both nonsynonymous and synonymous, and their homozygousity were found to be important factors for high levels of resistance. Our study, for the first time, provide a strong case demonstrating the co-existence of both nonsynonymous and synonymous mutations in the sodium channel of resistant mosquitoes in response to insecticide resistance and the inheritance of these mutations in the offspring of field mosquito strains following insecticide selection.

SUBMITTER: Xu Q

PROVIDER: S-EPMC3474719 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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Evolutionary adaptation of the amino acid and codon usage of the mosquito sodium channel following insecticide selection in the field mosquitoes.

Xu Qiang Q Zhang Lee L Li Ting T Zhang Lan L He Lin L Dong Ke K Liu Nannan N

PloS one 20121017 10

Target site insensitivity resulting from point mutations within the voltage-gated sodium channel of the insect nervous system is known to be of primary importance in the development of resistance to pyrethroid insecticides. This study shifts current research paradigms by conducting, for the first time, a global analysis of all the naturally occurring mutations, both nonsynonymous and synonymous mutations, as well as mutation combinations in the entire mosquito sodium channel of Culex quinquefasc ...[more]

PMID: 23082181

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Project description:Ebola virus (EBOV) has caused several outbreaks as the consequence of spillover events from zoonotic sources and has resulted in huge death tolls. In spite of considerable progress, a thorough know-how regarding EBOV adaptation in various host species and detailed information about the potential reservoirs of EBOV still remains obscure. The present study was executed to examine the patterns of codon usage and its associated influence in the adaptation of EBOV to potential hosts that dwell in Africa, the origin of the viral outbreaks. Correspondence analysis (CA) revealed that the codon usage signature in EBOV is a complex interplay of factors including compositional bias and natural selection, with the latter having a more pronounced impact. Low codon usage bias in EBOV indicates a flexibility of the viruses in adapting to diverse range of hosts with different codon usage architectures. EBOV adaptation in potential hosts, as estimated by codon adaptation index (CAI) and relative codon deoptimization index (RCDI), revealed that the viruses were relatively better adapted to African primates than other mammals examined, which might account for the high fatality rate of primates owing to EBOV infection. Bats have been speculated as natural reservoirs of EBOV. In the present analysis it was interesting to note that EBOV displayed lower degrees of adaptation, as estimated by CAI and RCDI, with bats in comparison to the primate hosts. Lower degrees of adaptation might contribute to long-term co-existence and circulation of the viral pathogens in bat populations. Codon usage patterns of EBOV isolates associated with different outbreaks varied significantly, with discrete patterns between the West and Central African isolates. Additional evolutionary analyses indicated that the West African Epidemic began with an initial spillover infection and there was more than one population of EBOV circulating in the natural reservoir in the Democratic Republic of the Congo. The present study yields valuable information regarding the possible circulation of EBOV in various African mammals.

Project description:Mosquitoes host and pass on to humans a variety of disease-causing pathogens such as infectious viruses and other parasitic microorganisms. The emergence and spread of insecticide resistance is threatening the effectiveness of current control measures for common mosquito vector borne diseases, such as malaria, dengue and Zika. Therefore, the emerging resistance to the widely used pyrethroid insecticides is an alarming problem for public health. Herein we demonstrated the use of RNA interference (RNAi) to increase susceptibility of adult mosquitoes to a widely used pyrethroid insecticide.Experiments were performed on a field-collected pyrethroid resistant strain of Ae. aegypti (Rio de Janeiro; RJ). Larvae from the resistant Ae. aegypti population were soaked with double-stranded RNAs (dsRNAs) that correspond either to voltage-gate sodium channel (VGSC), P-glycoprotein, or P450 detoxification genes and reared to adulthood. Adult mortality rates in the presence of various Deltamethrin pyrethroid concentrations were used to assess mosquito insecticide susceptibility.We characterized the RJ Ae. aegypti strain with regard to its level of resistance to a pyrethroid insecticide and found that it was approximately 6 times more resistant to Deltamethrin compared to the laboratory Rockefeller strain. The RJ strain displayed a higher frequency of Val1016Ile and Phe1534Cys substitutions of the VGSC gene. The resistant strain also displayed a higher basal expression level of VGSC compared to the Rockefeller strain. When dsRNA-treated mosquitoes were subjected to a standard pyrethroid contact bioassay, only dsRNA targeting VGSC increased the adult mortality of the pyrethroid resistant strain. The dsRNA treatment proved effective in increasing adult mosquito susceptibility over a range of pyrethroid concentrations and these results were associated with dsRNA-specific small interfering RNAs in treated adults, and the corresponding specific down regulation of VGSC gene expression level. Finally, we demonstrated that the efficiency of our approach was further improved by 'tiling' along the VGSC gene in order to identify the most potent dsRNA sequences.These results demonstrate that dsRNA applied to mosquito larvae retains its biological activity into adulthood. Thus, the RNAi system reported here could be a useful approach to control the widespread insecticide resistance in mosquitoes and other insect vectors of human diseases.

Dataset Information

Evolutionary adaptation of the amino acid and codon usage of the mosquito sodium channel following insecticide selection in the field mosquitoes.

Publications

Evolutionary adaptation of the amino acid and codon usage of the mosquito sodium channel following insecticide selection in the field mosquitoes.

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