{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,25]],"date-time":"2026-09-25T06:01:42Z","timestamp":1790316102385,"version":"4.1.0"},"reference-count":64,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2023,8,15]],"date-time":"2023-08-15T00:00:00Z","timestamp":1692057600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"CDC\u2019s Advanced Molecular Detection (AMD) program","award":["AMD-159"],"award-info":[{"award-number":["AMD-159"]}]},{"name":"CDC\u2019s Advanced Molecular Detection (AMD) program","award":["NU60OE000104"],"award-info":[{"award-number":["NU60OE000104"]}]},{"name":"Association of Public Health Laboratories (APHL)","award":["AMD-159"],"award-info":[{"award-number":["AMD-159"]}]},{"name":"Association of Public Health Laboratories (APHL)","award":["NU60OE000104"],"award-info":[{"award-number":["NU60OE000104"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Genes"],"abstract":"<jats:p>Aedes aegypti transmits major arboviruses of public health importance, including dengue, chikungunya, Zika, and yellow fever. The use of insecticides represents the cornerstone of vector control; however, insecticide resistance in Ae. aegypti has become widespread. Understanding the molecular basis of insecticide resistance in this species is crucial to design effective resistance management strategies. Here, we applied Illumina RNA-Seq to study the gene expression patterns associated with resistance to three widely used insecticides (malathion, alphacypermethrin, and lambda-cyhalothrin) in Ae. aegypti populations from two sites (Manat\u00ed and Isabela) in Puerto Rico (PR). Cytochrome P450s were the most overexpressed detoxification genes across all resistant phenotypes. Some detoxification genes (CYP6Z7, CYP28A5, CYP9J2, CYP6Z6, CYP6BB2, CYP6M9, and two CYP9F2 orthologs) were commonly overexpressed in mosquitoes that survived exposure to all three insecticides (independent of geographical origin) while others including CYP6BY1 (malathion), GSTD1 (alpha-cypermethrin), CYP4H29 and GSTE6 (lambda-cyhalothrin) were uniquely overexpressed in mosquitoes that survived exposure to specific insecticides. The gene ontology (GO) terms associated with monooxygenase, iron binding, and passive transmembrane transporter activities were significantly enriched in four out of six resistant vs. susceptible comparisons while serine protease activity was elevated in all insecticide-resistant groups relative to the susceptible strain. Interestingly, cuticular-related protein genes (chinase and chitin) were predominantly downregulated, which was also confirmed in the functional enrichment analysis. This RNA-Seq analysis presents a detailed picture of the candidate detoxification genes and other pathways that are potentially associated with pyrethroid and organophosphate resistance in Ae. aegypti populations from PR. These results could inform development of novel molecular tools for detection of resistance-associated gene expression in this important arbovirus vector and guide the design and implementation of resistance management strategies.<\/jats:p>","DOI":"10.3390\/genes14081626","type":"journal-article","created":{"date-parts":[[2023,8,15]],"date-time":"2023-08-15T11:06:16Z","timestamp":1692097576000},"page":"1626","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["Comparative Transcriptomic Analysis of Insecticide-Resistant Aedes aegypti from Puerto Rico Reveals Insecticide-Specific Patterns of Gene Expression"],"prefix":"10.3390","volume":"14","author":[{"given":"Dieunel","family":"Derilus","sequence":"first","affiliation":[{"name":"Entomology Branch, Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, GA 30329, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lucy Mackenzie","family":"Impoinvil","sequence":"additional","affiliation":[{"name":"Entomology Branch, Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, GA 30329, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ephantus J.","family":"Muturi","sequence":"additional","affiliation":[{"name":"Entomology Branch, Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, GA 30329, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Janet","family":"McAllister","sequence":"additional","affiliation":[{"name":"Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, CO 80521, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6761-4272","authenticated-orcid":false,"given":"Joan","family":"Kenney","sequence":"additional","affiliation":[{"name":"Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, CO 80521, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Steven E.","family":"Massey","sequence":"additional","affiliation":[{"name":"Biology Department, University of Puerto Rico-Rio Piedras, San Juan, PR 00925, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ryan","family":"Hemme","sequence":"additional","affiliation":[{"name":"Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, San Juan, PR 00920, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Linda","family":"Kothera","sequence":"additional","affiliation":[{"name":"Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, CO 80521, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Audrey","family":"Lenhart","sequence":"additional","affiliation":[{"name":"Entomology Branch, Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, GA 30329, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,8,15]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Sharp, T.M., Quandelacy, T.M., Adams, L.E., Aponte, J.T., Lozier, M.J., Ryff, K., Flores, M., Rivera, A., Santiago, G.A., and Mu\u00f1oz-Jord\u00e1n, J.L. (2020). Epidemiologic and spatiotemporal trends of Zika Virus disease during the 2016 epidemic in Puerto Rico. PLoS Negl. Trop. Dis., 14.","DOI":"10.1371\/journal.pntd.0008532"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1959","DOI":"10.3201\/eid2510.181847","article-title":"Rapid Screening of Aedes aegypti Mosquitoes for Susceptibility to Insecticides as Part of Zika Emergency Response, Puerto Rico","volume":"25","author":"Hemme","year":"2019","journal-title":"Emerg. Infect. Dis."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1146\/annurev-ento-010814-020828","article-title":"insecticide resistance in mosquitoes: Impact, mechanisms and research directions","volume":"60","author":"Liu","year":"2015","journal-title":"Annu. Rev. Entomol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1016\/j.ibmb.2004.03.018","article-title":"The molecular basis of insecticide resistance in mosquitoes","volume":"34","author":"Hemingway","year":"2004","journal-title":"Insect. Biochem. Mol. Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1186\/1756-3305-6-280","article-title":"Review of insecticide resistance and behavioral avoidance of vectors of human diseases in Thailand","volume":"6","author":"Chareonviriyaphap","year":"2013","journal-title":"Parasit. Vectors"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1808","DOI":"10.1002\/ps.5374","article-title":"Genome-wide gene expression profiling reveals that cuticle alterations and P450 detoxification are associated with deltamethrin and DDT resistance in Anopheles arabiensis populations from Ethiopia","volume":"75","author":"Simma","year":"2019","journal-title":"Pest. Manag. Sci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1186\/1475-2875-6-111","article-title":"Detection of knockdown resistance (kdr) mutations in Anopheles gambiae: A comparison of two new high-throughput assays with existing methods","volume":"6","author":"Bass","year":"2007","journal-title":"Malar. J."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1186\/1475-2875-10-10","article-title":"Spatial and temporal variation in the kdr allele L1014S in Anopheles gambiae s.s. and phenotypic variability in susceptibility to insecticides in Western Kenya","volume":"10","author":"Mathias","year":"2011","journal-title":"Malar. J."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1365-2583.2004.00452.x","article-title":"The unique mutation in ace-1 giving high insecticide resistance is easily detectable in mosquitoes","volume":"13","author":"Weill","year":"2004","journal-title":"Insect. Mol. Biol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1146\/annurev.ento.51.110104.151104","article-title":"Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics","volume":"52","author":"Li","year":"2007","journal-title":"Annu. Rev. Entomol."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Ishak, I.H., Kamgang, B., Ibrahim, S.S., Riveron, J.M., Irving, H., and Wondji, C.S. (2017). Pyrethroid Resistance in Malaysian Populations of Dengue Vector Aedes aegypti Is Mediated by CYP9 Family of Cytochrome P450 Genes. PLoS Negl. Trop. Dis., 11.","DOI":"10.1371\/journal.pntd.0005302"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1819","DOI":"10.1534\/g3.117.040147","article-title":"Genome-Wide Transcription and Functional Analyses Reveal Heterogeneous Molecular Mechanisms Driving Pyrethroids Resistance in the Major Malaria Vector Anopheles funestus Across Africa","volume":"7","author":"Riveron","year":"2017","journal-title":"G3"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"20120429","DOI":"10.1098\/rstb.2012.0429","article-title":"Role of cytochrome P450s in insecticide resistance: Impact on the control of mosquito-borne diseases and use of insecticides on Earth","volume":"368","author":"David","year":"2013","journal-title":"Philos. Trans. R. Soc. Lond. B Biol. Sci."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Schluep, S.M., and Buckner, E.A. (2021). Metabolic resistance in permethrin-resistant Florida Aedes aegypti (Diptera: Culicidae). Insects, 12.","DOI":"10.3390\/insects12100866"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1590\/S0074-02762004000200015","article-title":"Aedes aegypti resistance to temephos during 2001 in several municipalities in the states of Rio de Janeiro, Sergipe, and Alagoas, Brazil","volume":"99","author":"Braga","year":"2004","journal-title":"Mem. Inst. Oswaldo Cruz"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1016\/j.pestbp.2012.05.008","article-title":"Insecticide resistance in the major dengue vectors Aedes albopictus and Aedes aegypti","volume":"104","author":"Vontas","year":"2012","journal-title":"Pestic. Biochem. Physiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1186\/s13071-018-2899-0","article-title":"Pyrethroid resistance in the dengue vector Aedes aegypti in Southeast Asia: Present situation and prospects for management","volume":"11","author":"Chen","year":"2018","journal-title":"Parasit. Vectors"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1240","DOI":"10.4269\/ajtmh.18-0607","article-title":"Transcriptome Sequencing and Analysis of Changes Associated with Insecticide Resistance in the Dengue Mosquito (Aedes aegypti) in Vietnam","volume":"100","author":"Lien","year":"2019","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"David, J.P., Faucon, F., Chandor-Proust, A., Poupardin, R., Riaz, M.A., Bonin, A., Navratil, V., and Reynaud, S. (2014). Comparative analysis of response to selection with three insecticides in the dengue mosquito Aedes aegypti using mRNA sequencing. BMC Genom., 15.","DOI":"10.1186\/1471-2164-15-174"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1347","DOI":"10.1101\/gr.189225.115","article-title":"Identifying genomic changes associated with insecticide resistance in the dengue mosquito Aedes aegypti by deep targeted sequencing","volume":"25","author":"Faucon","year":"2015","journal-title":"Genome Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/j.ibmb.2007.09.007","article-title":"Genomic analysis of detoxification genes in the mosquito Aedes aegypti","volume":"38","author":"Strode","year":"2008","journal-title":"Insect Biochem. Mol. Biol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1186\/1756-3305-4-5","article-title":"Insecticide resistance in Aedes aegypti populations from Cear\u00e1, Brazil","volume":"4","author":"Lima","year":"2011","journal-title":"Parasit. Vectors"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"146","DOI":"10.1016\/j.actatropica.2018.12.021","article-title":"Mechanisms of pyrethroid resistance in Aedes (Stegomyia) aegypti from Colombia","volume":"191","author":"Aponte","year":"2019","journal-title":"Acta Tropica"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Badolo, A., Sombi\u00e9, A., Pignatelli, P.M., Sanon, A., Yam\u00e9ogo, F., Wangrawa, D.W., Sanon, A., Kanuka, H., McCall, P.J., and Weetman, D. (2019). Insecticide resistance levels and mechanisms in Aedes aegypti populations in and around Ouagadougou, Burkina Faso. PLoS Negl. Trop. Dis., 13.","DOI":"10.1371\/journal.pntd.0007439"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Saavedra-Rodriguez, K., Campbell, C.L., Lozano, S., Penilla-Navarro, P., Lopez-Solis, A., Solis-Santoyo, F., Rodriguez, A.D., Perera, R., and Black Iv, W.C. (2021). Permethrin resistance in Aedes aegypti: Genomic variants that confer knockdown resistance, recovery, and death. PLoS Genet., 17.","DOI":"10.1371\/journal.pgen.1009606"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Sene, N.M., Mavridis, K., Ndiaye, E.H., Diagne, C.T., Gaye, A., Ngom, E.H.M., Ba, Y., Diallo, D., Vontas, J., and Dia, I. (2021). Insecticide resistance status and mechanisms in Aedes aegypti populations from Senegal. PLoS Negl. Trop. Dis., 15.","DOI":"10.1371\/journal.pntd.0009393"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"988907","DOI":"10.3389\/fphys.2022.988907","article-title":"Metabolic detoxification and ace-1 target site mutations associated with acetamiprid resistance in Aedes aegypti L.","volume":"13","author":"Samal","year":"2022","journal-title":"Front. Physiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1111\/j.1948-7134.2010.00077.x","article-title":"Transcription analysis of differentially expressed genes in insecticide-resistant Aedes aegypti mosquitoes after deltamethrin exposure","volume":"35","author":"Lertkiatmongkol","year":"2010","journal-title":"J. Vector Ecol."},{"key":"ref_29","unstructured":"Brogdon, W., and Chan, A. (2010). Guideline for Evaluating Insecticide Resistance in Vectors Using the CDC Bottle Bioassay, CDC."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1101","DOI":"10.1038\/nprot.2008.73","article-title":"Analyzing real-time PCR data by the comparative C(T) method","volume":"3","author":"Schmittgen","year":"2008","journal-title":"Nat. Protoc."},{"key":"ref_31","unstructured":"Andrews, S. (2021, September 03). FastQC: A Quality Control Tool for High Throughput Sequence Data. Version 0.11.2. Available online: https:\/\/www.bioinformatics.babraham.ac.uk\/projects\/fastqc\/."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"i884","DOI":"10.1093\/bioinformatics\/bty560","article-title":"fastp: An ultra-fast all-in-one FASTQ preprocessor","volume":"34","author":"Chen","year":"2018","journal-title":"Bioinformatics"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"D707","DOI":"10.1093\/nar\/gku1117","article-title":"VectorBase: An updated bioinformatics resource for invertebrate vectors and other organisms related with human diseases","volume":"43","author":"Emrich","year":"2015","journal-title":"Nucleic Acids Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"e108","DOI":"10.1093\/nar\/gkt214","article-title":"The Subread aligner: Fast, accurate and scalable read mapping by seed-and-vote","volume":"41","author":"Liao","year":"2013","journal-title":"Nucleic Acids Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2078","DOI":"10.1093\/bioinformatics\/btp352","article-title":"The Sequence Alignment\/Map format and SAMtools","volume":"25","author":"Li","year":"2009","journal-title":"Bioinformatics"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1093\/bioinformatics\/btp616","article-title":"edgeR: A Bioconductor package for differential expression analysis of digital gene expression data","volume":"26","author":"Robinson","year":"2010","journal-title":"Bioinformatics"},{"key":"ref_37","unstructured":"Chen, Y., McCarthy, D., Ritchie, M., Robinson, M., Smyth, G., and Hall, E. (2021, September 20). edgeR: Differential Analysis of Sequence Read Count Data User\u2019s Guide, Available online: https:\/\/www.ncbi.nlm.nih.gov\/pmc\/articles\/PMC2796818\/."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"e47","DOI":"10.1093\/nar\/gkv007","article-title":"limma powers differential expression analyses for RNA-sequencing and microarray studies","volume":"43","author":"Ritchie","year":"2015","journal-title":"Nucleic Acids Res."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1038\/s41586-018-0692-z","article-title":"Improved reference genome of Aedes aegypti informs arbovirus vector control","volume":"563","author":"Matthews","year":"2018","journal-title":"Nature"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"D211","DOI":"10.1093\/nar\/gkn785","article-title":"InterPro: The integrative protein signature database","volume":"37","author":"Hunter","year":"2008","journal-title":"Nucleic Acids Res."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1236","DOI":"10.1093\/bioinformatics\/btu031","article-title":"InterProScan 5: Genome-scale protein function classification","volume":"30","author":"Jones","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"10872","DOI":"10.1038\/s41598-018-28948-z","article-title":"GOATOOLS: A Python library for Gene Ontology analyses","volume":"8","author":"Klopfenstein","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/j.cois.2018.03.001","article-title":"Insect cuticle: A critical determinant of insecticide resistance","volume":"27","author":"Balabanidou","year":"2018","journal-title":"Curr. Opin. Insect. Sci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1186\/1756-3305-3-67","article-title":"Cuticle thickening associated with pyrethroid resistance in the major malaria vector Anopheles funestus","volume":"3","author":"Wood","year":"2010","journal-title":"Parasit. Vectors"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"9268","DOI":"10.1073\/pnas.1608295113","article-title":"Cytochrome P450 associated with insecticide resistance catalyzes cuticular hydrocarbon production in Anopheles gambiae","volume":"113","author":"Balabanidou","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1111\/j.1365-2583.2005.00582.x","article-title":"Gene expression in insecticide resistant and susceptible Anopheles gambiae strains constitutively or after insecticide exposure","volume":"14","author":"Vontas","year":"2005","journal-title":"Insect. Mol. Biol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/j.abb.2005.03.021","article-title":"Serine proteinase over-expression in relation to deltamethrin resistance in Culex pipiens pallens","volume":"438","author":"Gong","year":"2005","journal-title":"Arch. Biochem. Biophys."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"584","DOI":"10.1186\/s13071-021-05091-9","article-title":"Functional characterization of two clip domain serine proteases in innate immune responses of Aedes aegypti","volume":"14","author":"Wang","year":"2021","journal-title":"Parasites Vectors"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1159\/000527974","article-title":"Serine Protease Networks Mediate Immune Responses in Extra-Embryonic Tissues of Eggs in the Tobacco Hornworm, Manduca sexta","volume":"15","author":"Shan","year":"2022","journal-title":"J. Innate Immun."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"El Moussawi, L., Nakhleh, J., Kamareddine, L., and Osta, M.A. (2019). The mosquito melanization response requires hierarchical activation of non-catalytic clip domain serine protease homologs. PLoS Pathog., 15.","DOI":"10.1371\/journal.ppat.1008194"},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Kasai, S., Komagata, O., Itokawa, K., Shono, T., Ng, L.C., Kobayashi, M., and Tomita, T. (2014). Mechanisms of pyrethroid resistance in the dengue mosquito vector, Aedes aegypti: Target site insensitivity, penetration, and metabolism. PLoS Negl. Trop. Dis., 8.","DOI":"10.1371\/journal.pntd.0002948"},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Dusfour, I., Zorrilla, P., Guidez, A., Issaly, J., Girod, R., Guillaumot, L., Robello, C., and Strode, C. (2015). Deltamethrin Resistance Mechanisms in Aedes aegypti Populations from Three French Overseas Territories Worldwide. PLoS Negl. Trop. Dis., 9.","DOI":"10.1371\/journal.pntd.0004226"},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Bariami, V., Jones, C.M., Poupardin, R., Vontas, J., and Ranson, H. (2012). Gene amplification, ABC transporters and cytochrome P450s: Unraveling the molecular basis of pyrethroid resistance in the dengue vector, Aedes aegypti. PLoS Negl. Trop. Dis., 6.","DOI":"10.1371\/journal.pntd.0001692"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1603\/ME13228","article-title":"Transcriptional analysis of four family 4 P450s in a Puerto Rico strain of Aedes aegypti (Diptera: Culicidae) compared with an Orlando strain and their possible functional roles in permethrin resistance","volume":"51","author":"Reid","year":"2014","journal-title":"J. Med. Entomol."},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Moyes, C.L., Vontas, J., Martins, A.J., Ng, L.C., Koou, S.Y., Dusfour, I., Raghavendra, K., Pinto, J., Corbel, V., and David, J.P. (2017). Contemporary status of insecticide resistance in the major Aedes vectors of arboviruses infecting humans. PLoS Negl. Trop. Dis., 11.","DOI":"10.1371\/journal.pntd.0005625"},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Epelboin, Y., Wang, L., Giai Gianetto, Q., Choumet, V., Gaborit, P., Issaly, J., Guidez, A., Douche, T., Chaze, T., and Matondo, M. (2021). CYP450 core involvement in multiple resistance strains of Aedes aegypti from French Guiana highlighted by proteomics, molecular and biochemical studies. PLoS ONE, 16.","DOI":"10.1371\/journal.pone.0243992"},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Marcombe, S., Poupardin, R., Darriet, F., Reynaud, S., Bonnet, J., Strode, C., Brengues, C., Y\u00e9bakima, A., Ranson, H., and Corbel, V. (2009). Exploring the molecular basis of insecticide resistance in the dengue vector Aedes aegypti: A case study in Martinique Island (French West Indies). BMC Genom., 10.","DOI":"10.1186\/1471-2164-10-494"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1111\/j.1365-2583.2011.01113.x","article-title":"Transcription of detoxification genes after permethrin selection in the mosquito Aedes aegypti","volume":"21","author":"Suarez","year":"2012","journal-title":"Insect. Mol. Biol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"192","DOI":"10.1093\/jme\/tjab179","article-title":"Expansive and Diverse Phenotypic Landscape of Field Aedes aegypti (Diptera: Culicidae) Larvae with Differential Susceptibility to Temephos: Beyond Metabolic Detoxification","volume":"59","author":"Morgan","year":"2022","journal-title":"J. Med. Entomol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1042\/bj3590295","article-title":"Identification of a novel class of insect glutathione S-transferases involved in resistance to DDT in the malaria vector Anopheles gambiae","volume":"359","author":"Ranson","year":"2001","journal-title":"Biochem. J."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"27876","DOI":"10.1016\/S0021-9258(18)46868-8","article-title":"Biochemical characterization of Drosophila glutathione S-transferases D1 and D21","volume":"269","author":"Tang","year":"1994","journal-title":"J. Biol. Chem."},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Faucon, F., Gaude, T., Dusfour, I., Navratil, V., Corbel, V., Juntarajumnong, W., Girod, R., Poupardin, R., Boyer, F., and Reynaud, S. (2017). In the hunt for genomic markers of metabolic resistance to pyrethroids in the mosquito Aedes aegypti: An integrated next-generation sequencing approach. PLoS Negl. Trop. Dis., 11.","DOI":"10.1371\/journal.pntd.0005526"},{"key":"ref_63","unstructured":"Eldefrawi, M.E., and Eldefrawi, A.T. (2021, September 03). Insecticide Actions on Gaba Receptors and Voltage-Dependent Chloride Channels. Available online: https:\/\/api.semanticscholar.org\/CorpusID:92680854."},{"key":"ref_64","unstructured":"World Health Organization (1998). The World Health Report: 1998: Life in the 21st Century: A Vision for All: Report of the Director-General, World Health Organization."}],"container-title":["Genes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4425\/14\/8\/1626\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:33:51Z","timestamp":1760128431000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4425\/14\/8\/1626"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,8,15]]},"references-count":64,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2023,8]]}},"alternative-id":["genes14081626"],"URL":"https:\/\/doi.org\/10.3390\/genes14081626","relation":{},"ISSN":["2073-4425"],"issn-type":[{"value":"2073-4425","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,8,15]]}}}