Identifying genomic changes associated with insecticide resistance in the dengue mosquito <i>Aedes aegypti</i> by deep targeted sequencing

Faucon, Frédéric; Dusfour, Isabelle; Gaude, Thierry; Navratil, Vincent; Boyer, Frédéric; Chandre, Fabrice; Sirisopa, Patcharawan; Thanispong, Kanutcharee; Juntarajumnong, Waraporn; Poupardin, Rodolphe; Chareonviriyaphap, Theeraphap; Girod, Romain; Corbel, Vincent; Reynaud, Stéphane; David, Jean‐Philippe

doi:10.1101/gr.189225.115

Cited by 159 publications

(232 citation statements)

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“…The involvement of detoxification complex enzymes in both resistance and defense to pyrethroids has been documented in several arthropod species, including mosquitoes61112. Among them, cytochromes P450 (CYPs), carboxylesterases (CCEs), glutathione S-transferases (GSTs), UDP-glucuronosyl transferases (UGTs) enzymes, as well as ABC transporters were found differentially expressed between resistant and susceptible strains to pyrethroids1617183031. Likewise, induced up-regulation of detoxifying genes was found in resistant individuals exposed to pyrethroids, such as in the mosquito Anopheles gambiae 30, the cattle tick Rhipicephalus (Boophilus) microplus 32 or the mosquito Culex quinquefasciatus 2425, as well as in susceptible individuals, such as in Panonychus citri 19, Liposcelis bostrychophila 20, and Melita plumulosa 21.…”

Section: Discussionmentioning

confidence: 99%

“…Transcriptomic studies that have focused on single time-points showed that the exposure of individuals to toxicants induces up-regulation of several genes, while several others are down-regulated161718192021. However, these are single snapshots of the defense response that do not allow us to know if and how the differentially expressed genes are modulated during toxicant exposure.…”

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confidence: 99%

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The choreography of the chemical defensome response to insecticide stress: insights into the Anopheles stephensi transcriptome using RNA-Seq

Marco

Sassera

Epis

et al. 2017

Sci Rep

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Animals respond to chemical stress with an array of gene families and pathways termed “chemical defensome”. In arthropods, despite many defensome genes have been detected, how their activation is arranged during toxic exposure remains poorly understood. Here, we sequenced the transcriptome of Anopheles stephensi larvae exposed for six, 24 and 48 hours to the LD50 dose of the insecticide permethrin to monitor transcriptional changes of defensome genes across time. A total of 177 genes involved in insecticide defense were differentially expressed (DE) in at least one time-point, including genes encoding for Phase 0, I, II, III and antioxidant enzymes and for Heat Shock and Cuticular Proteins. Three major patterns emerged throughout time. First, most of DE genes were down-regulated at all time-points, suggesting a reallocation of energetic resources during insecticide stress. Second, single genes and clusters of genes turn off and on from six to 48 hours of treatment, showing a modulated response across time. Third, the number of up-regulated genes peaked at six hours and then decreased during exposure. Our results give a first picture of how defensome gene families respond against toxicants and provide a valuable resource for understanding how defensome genes work together during insecticide stress.

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

The choreography of the chemical defensome response to insecticide stress: insights into the Anopheles stephensi transcriptome using RNA-Seq

Marco

Sassera

Epis

et al. 2017

Sci Rep

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“…aegypti involve target site alterations and metabolic resistance, comprising altered activity of enzymes from three superfamilies, esterases (CCEs), glutathione-s-transferases (GSTs) and cytochrome P450s (CYP450s), although several other enzyme families are likely to be involved [12]. Overexpression of Ae.…”

Section: Introductionmentioning

confidence: 99%

Combined target site (kdr) mutations play a primary role in highly pyrethroid resistant phenotypes of Aedes aegypti from Saudi Arabia

et al. 2017

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BackgroundPyrethroid resistance is a threat to effective vector control of Aedes aegypti, the vector of dengue, Zika and other arboviruses, but there are many major knowledge gaps on the mechanisms of resistance. In Jeddah and Makkah, the principal dengue-endemic areas of Saudi Arabia, pyrethroids are used widely for Ae. aegypti control but information about resistance remains sparse, and the underlying genetic basis is unknown. Findings from an ongoing study in this internationally significant area are reported here.Methods Aedes aegypti collected from each city were raised to adults and assayed for resistance to permethrin, deltamethrin (with and without the synergist piperonyl butoxide, PBO), fenitrothion, and bendiocarb. Two fragments of the voltage-gated sodium channel (Vgsc), encompassing four previously identified mutation sites, were sequenced and subsequently genotyped to determine associations with resistance. Expression of five candidate genes (CYP9J10, CYP9J28, CYP9J32, CYP9M6, ABCB4) previously associated with pyrethroid resistance was compared between assay survivors and controls.ResultsJeddah and Makkah populations exhibited resistance to multiple insecticides and a similarly high prevalence of resistance to deltamethrin compared to a resistant Cayman strain, with a significant influence of age and exposure duration on survival. PBO pre-exposure increased pyrethroid mortality significantly in the Jeddah, but not the Makkah strain. Three potentially interacting Vgsc mutations were detected: V1016G and S989P were in perfect linkage disequilibrium in each strain and strongly predicted survival, especially in the Makkah strain, but were in negative linkage disequilibrium with 1534C, though some females with the Vgsc triple mutation were detected. The candidate gene CYP9J28 was significantly over-expressed in Jeddah compared to two susceptible reference strains, but none of the candidate genes was consistently up-regulated to a significant level in the Makkah strain.ConclusionsDespite their proximity, Makkah and Jeddah exhibit significant differences in pyrethroid resistance phenotypes, with some evidence to suggest a different balance of mechanisms, for example with more impact associated with CYP450s in the Jeddah strain, and the dual kdr mutations 989P and 1016G in the more resistant Makkah strain. The results overall demonstrate a major role for paired target site mutations in pyrethroid resistance and highlight their utility for diagnostic monitoring.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-017-2096-6) contains supplementary material, which is available to authorized users.

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“…). Furthermore, the traditional control method – pesticide – is both indiscriminate and thwarted by the multiple cases of pesticide resistance in Aedes mosquitoes recently reported 8, 9 .…”

Section: Introductionmentioning

confidence: 99%

Preliminary results on the control of Aedes spp. in a remote Guatemalan community vulnerable to dengue, chikungunya and Zika virus: community participation and use of low-cost ecological ovillantas for mosquito control

Ulibarri

Betanzos

et al. 2017

F1000Res

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Objective: To study the effectiveness of an integrated intervention of health worker training, a low-cost ecological mosquito ovitrap, and community engagement on Aedes spp. mosquito control over 10 months in 2015 in an urban remote community in Guatemala at risk of dengue, chikungunya and Zika virus transmission. Methods: We implemented a three-component integrated intervention consisting of: web-based training of local health personnel in vector control, cluster-randomized assignment of an ecological modified ovitrap (ovillantas: ovi=egg, llanta=tire) or standard ovitraps to capture Aedes spp. mosquito eggs (no efforts have been taken to determine the exact Aedes species at this moment), and community engagement to promote participation of community members and health personnel in the understanding and maintenance of ovitraps for mosquito control. The intervention was implemented in local collaboration with Guatemala’s Ministry of Health’s Vector Control Programme, and in international collaboration with the National Institute of Public Health in Mexico. Findings: Eighty percent of the 25 local health personnel enrolled in the training programme received accreditation of their improved knowledge of vector control. When ovillantas were used in a cluster of ovitraps (several in proximity), significantly more eggs were trapped by ecological ovillantas than standard ovitraps over the 10 month (42 week) study period (t=5.2577; p<0.05). Repetitive filtering and recycling of the attractant solution (or water) kept the ovillanta clean, free from algae growth. Among both community members and health workers, the levels of knowledge, interest, and participation in community mosquito control and trapping increased. Recommendations for enhancing and sustaining community mosquito control were identified. Conclusion: Our three-component integrated intervention proved beneficial to this remote community at risk of mosquito-borne diseases such as dengue, chikungunya, and Zika. The combination of training of health workers, cluster use of low-cost ecological ovillanta to destroy the second generation of mosquitoes, and community engagement ensured the project met local needs and fostered collaboration and participation of the community, which can help improve sustainability. The ovillanta intervention and methodology may be modified to target other species such as Culex, should it be established that such mosquitoes carry Zika virus in addition to Aedes.

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Identifying genomic changes associated with insecticide resistance in the dengue mosquito Aedes aegypti by deep targeted sequencing

Cited by 159 publications

References 80 publications

The choreography of the chemical defensome response to insecticide stress: insights into the Anopheles stephensi transcriptome using RNA-Seq

The choreography of the chemical defensome response to insecticide stress: insights into the Anopheles stephensi transcriptome using RNA-Seq

Combined target site (kdr) mutations play a primary role in highly pyrethroid resistant phenotypes of Aedes aegypti from Saudi Arabia

Preliminary results on the control of Aedes spp. in a remote Guatemalan community vulnerable to dengue, chikungunya and Zika virus: community participation and use of low-cost ecological ovillantas for mosquito control

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