Transcriptome Profiling and Genetic Study Reveal Amplified Carboxylesterase Genes Implicated in Temephos Resistance, in the Asian Tiger Mosquito Aedes albopictus

PLoS Neglected Tropical Diseases

Volumn 9, Issue 5, 2015, Pages

  Grigoraki, Linda ^a,b   Lagnel, Jacques ^c   Kioulos, Ilias ^d   Kampouraki, Anastasia ^a   Morou, Evangelia ^a   Labbé, Pierrick ^e   Weill, Mylene ^e   Vontas, John ^b,d  

^a UNIVERSITY OF CRETE   (Greece)

^b INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

^c INSTITUTE OF OCEANOGRAPHY   (Greece)

^d AGRICULTURAL UNIVERSITY OF ATHENS   (Greece)

^e UNIV MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

1 NAPHTHYL ACETATE; ABC TRANSPORTER; BETA NAPHTHYL ACETATE; CARBOXYLESTERASE; COMPLEMENTARY DNA; CYTOCHROME P450; GENOMIC DNA; GLUCURONOSYLTRANSFERASE; GLUTATHIONE TRANSFERASE; NAPHTHALENE DERIVATIVE; RNA; TEMEFOS; TRANSCRIPTOME; UNCLASSIFIED DRUG; INSECT PROTEIN; INSECTICIDE;

AEDES ALBOPICTUS; ARTICLE; DETOXIFICATION; ENZYME ACTIVITY; GENE AMPLIFICATION; GENE DOSAGE; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; LC50; LIPOGENESIS; NONHUMAN; PESTICIDE RESISTANCE; REAL TIME POLYMERASE CHAIN REACTION; SURVIVAL; AEDES; ANIMAL; DNA SEQUENCE; DRUG EFFECTS; ENZYMOLOGY; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETICS; HIGH THROUGHPUT SEQUENCING; INSECT VECTOR; INSECTICIDE RESISTANCE; MALE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; UPREGULATION;

AEDES; ANIMALS; BASE SEQUENCE; CARBOXYLESTERASE; FEMALE; GENE AMPLIFICATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE LIBRARY; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; INSECT PROTEINS; INSECT VECTORS; INSECTICIDE RESISTANCE; INSECTICIDES; MALE; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; TEMEFOS; UP-REGULATION;

EID: 84930644553     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0003771     Document Type: Article

References (40)

1. Adhami J, Reiter P, Introduction and establishment of Aedes (Stegomyia) albopictus Skuse (Diptera: Culicidae) in Albania. J Am Mosq Control Assoc. 1998; 14: 340–343. 9813831
2. Bonizzoni M, Gasperi G, Chen XG, James AA, The invasive mosquito species Aedes albopictus: current knowledge and future perspectives. Trends Parasitol. 2013; 29: 460–468. doi: 10.1016/j.pt.2013.07.003 23916878
3. Briegel H, Timmermann SE, Aedes albopictus (Diptera: Culicidae): Physiological aspects of development and reproduction. J Medl Entomol.2001; 38: 566–571.
4. Gratz NG, Critical review of the vector status of Aedes albopictus. Med Vet Entomol. 2004; 18: 215–227. 15347388
5. Enserink M, Infectious diseases. Massive outbreak draws fresh attention to little known virus. Science. 2006; 311: 1085. 16497896
6. Ranson H, Burhani J, Lumjuan N, Black W. Insecticide resistance in dengue vectors. TropIKAnet. 2010. http://journal.tropika.net/scielo.php?script=sci_arttext&pid=s2078-86062010000100003&lng=en.
7. Vontas J, Kioulos E, Pavlidi N, Morou E, della Torre A, et al. Insecticide resistance in the major dengue vectors Aedes albopictus and Aedes aegypti. Pestic Biochem Physiol. 2012; 104: 126–131.
8. Li XC, Schuler MA, Berenbaum MR, Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol. 2007; 52: 231–253. 16925478
9. Linton KJ, Structure and function of ABC transporters. Physiology. 2007; 22: 122–130. 17420303
10. Ahn SJ, Dermauw W, Wybouw N, Heckel DG, Van Leeuwen T, Bacterial origin of a diverse family of UDP-glycosyltransferase genes in the Tetranychus urticae genome. Insect Biochem Mol Biol. 2014; 50: 43–57. doi: 10.1016/j.ibmb.2014.04.003 24727020
11. Weill M, Lutfalla G, Mogensen K, Chandre F, Berthomieu A, et al. Insecticide resistance in mosquito vectors. Nature. 2003; 423: 136–137. 12736674
12. Weill M, Berthomieu A, Berticat C, Lutfalla G, Negre V, et al. Insecticide resistance: a silent base prediction. Curr Biol. 2004; 14: 552–553.
13. Poupardin R, Srisukontarat W, Yunta C, Ranson H. Identification of Carboxylesterase Genes Implicated in Temephos Resistance in the Dengue Vector Aedes Aegypti. Plos Negl Trop Dis. 2014; doi: 10.1371/journal.pntd.0002743
14. Guillemaud T, Makate N, Raymond M, Hirst B, Callaghan A, Esterase gene amplification in Culex pipiens. Insect Mol Biol. 1997; 6: 319–327. 9359574
15. Hemingway J, Karunaratne SH, Mosquito carboxylesterases: a review of the molecular biology and biochemistry of a major insecticide resistance mechanism. Med Vet Entomol. 1998; 12: 1–12. 9513933
16. Ishak I, Jaal Z, Ranson H, Wondji C. Contrasting patterns of insecticide resistance and knockdown resistance (kdr) in the dengue vectors Aedes aegypti and Aedes albopictus from Malaysia. Parasit Vectors. 2015; In press.
17. WHO Division of Vector Biology and Control. Instructions for determining the susceptibility or resistance of mosquito larvae to insecticides. Geneva: World Health Organization. 1981. http://www.who.int/iris/handle/10665/69615
18. Milesi P, Pocquet N, P L BioRssay: a R script for bioassay analyses. http://wwwisemuniv-montp2fr/recherche/equipes/genomique-de-ladaptation/personnel/labbe-pierrick/.
19. Brogdon WG, Mosquito protein microassay. I. Protein determinations from small portions of single-mosquito homogenates. Comp Biochem Physiol B. 1984; 79: 457–459. 6509934
20. Brogdon WG, Microassay of acetylcholinesterase activity in small portions of single mosquito homogenates. Comp Biochem Physiol C. 1988; 90: 145–150. 2904854
21. Navajas M, Lagnel J, Fauvel G, De Moraes G, Sequence variation of ribosomal internal transcribed spacers (ITS) in commercially important phytoseiidae mites. Exp Appl Acarol.1999; 23: 851–859. 10668860
22. Schmieder R, Edwards R, Quality control and preprocessing of metagenomic datasets. Bioinformatics. 2011; 27: 863–864. doi: 10.1093/bioinformatics/btr026 21278185
23. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011; 29: 644–652. doi: 10.1038/nbt.1883 21572440
24. Langmead B, Salzberg SL, Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012; 9: 357–359. doi: 10.1038/nmeth.1923 22388286
25. Parra G, Bradnam K, Korf I, CEGMA: a pipeline to accurately annotate core genes in eukaryotic genornes. Bioinformatics. 2007; 23: 1061–1067. 17332020
26. Lagnel J, Tsigenopoulos CS, Iliopoulos I, NOBLAST and JAMBLAST: New Options for BLAST and a Java Application Manager for BLAST results. Bioinformatics. 2009; 25: 824–826. doi: 10.1093/bioinformatics/btp067 19181685
27. Robinson MD, McCarthy DJ, Smyth GK, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010; 26: 139–140. doi: 10.1093/bioinformatics/btp616 19910308
28. Zhou XB, Lindsay H, Robinson MD. Robustly detecting differential expression in RNA sequencing data using observation weights. Nucleic Acids Res. 2014.
29. Reynolds JA, Poelchau MF, Rahman Z, Armbruster PA, Denlinger DL, Transcript profiling reveals mechanisms for lipid conservation during diapause in the mosquito, Aedes albopictus. J Insect Physiol. 2012; 58: 966–973. doi: 10.1016/j.jinsphys.2012.04.013 22579567
30. Pfaffl MW, A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001; 29: 2002–2007.
31. Strode C, de Melo-Santos M, Magalhaes T, Araujo A, Ayres C. Expression Profile of Genes during Resistance Reversal in a Temephos Selected Strain of the Dengue Vector, Aedes aegypti. Plos One. 2012.
32. Fort P, Albertini A, Van-Hua A, Berthomieu A, Roche S, et al. Fossil Rhabdoviral Sequences Integrated into Arthropod Genomes: Ontogeny, Evolution, and Potential Functionality. Mol Biol Evol. 2012; 29: 381–390. doi: 10.1093/molbev/msr226 21917725
33. Flalconer D, Introduction to quantitative genetics. Edinburgh: Oliver and Boyd; 1964.
34. Kioulos I, Kampouraki A, Morou E, Skavdis G, Vontas J, Insecticide resistance status in the major West Nile virus vector Culex pipiens from Greece. Pest Manag Sci. 2014; 70: 623–627. doi: 10.1002/ps.3595 23788440
35. Field LM, Devonshire AL, Structure and organization of amplicons containing the E4 esterase genes responsible for insecticide resistance in the aphid Myzus persicae (Sulzer). Biochem J. 1997; 322: 867–871. 9148762
36. Vontas JG, Small GJ, Hemingway J, Comparison of esterase gene amplification, gene expression and esterase activity in insecticide susceptible and resistant strains of the brown planthopper, Nilaparvata lugens (Stal). Insect Mol Biol. 2000; 9: 655–660. 11122475
37. Mouches C, Pasteur N, Berge JB, Hyrien O, Raymond M, et al. Amplification of an Esterase Gene Is Responsible for Insecticide Resistance in a California Culex Mosquito. Science. 1986; 233: 778–780. 3755546
38. Paton MG, Karunaratne SH, Giakoumaki E, Roberts N, Hemingway J, Quantitative analysis of gene amplification in insecticide-resistant Culex mosquitoes. Biochem J. 2000; 346: 17–24. 10657234
39. Callaghan A, Guillemaud T, Makate N, Raymond M, Polymorphisms and fluctuations in copy number of amplified esterase genes in Culex pipiens mosquitoes. Insect Mol Biol. 1998; 7: 295–300. 9662480
40. David JP, Ismail HM, Chandor-Proust A, Paine MJI. Role of cytochrome P450s in insecticide resistance: impact on the control of mosquito-borne diseases and use of insecticides on Earth. Philos Trans R Soc Lond B Biol Sc. 2013.