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Lipase is associated with deltamethrin resistance in Culex pipiens pallens

  • Hong-Xia Hu
  • Dan Zhou
  • Lei Ma
  • Bo Shen
  • Yan SunEmail author
  • Chang-Liang Zhu
Arthropods and Medical Entomology - Original Paper

Abstract

The wide application of pyrethroids has led to the rapid development of insecticide resistance in mosquitoes, leading to a rise in mosquito-borne diseases. We previously identified five differentially expressed lipase family genes upon evaluating the transcriptomes of deltamethrin-resistant and deltamethrin-susceptible strains of Culex pipiens pallens. Herein, the gene expression levels were verified by quantitative real-time PCR, and two lipase family genes, lipase A and pancreatic triacylglycerol lipase A, were chosen for further investigations. Using cell viability assays and Centers for Disease Control and Prevention bottle bioassays, lipase A was found to increase the resistance of mosquitoes against deltamethrin both in vitro and in vivo. Our findings indicate that lipase A is involved in conferring deltamethrin resistance in Cx. pipiens pallens.

Keywords

Lipase Deltamethrin Insecticide resistance Culex pipiens pallens 

Notes

Author contributions

HXH performed the experiments. HXH and DZ wrote the manuscript and prepared the figures. DZ, LM, and BS participated in data analyses. YS and CLZ conceived the idea and coordinated the project. All authors have read and approved the final version of the manuscript for submission.

Funding information

This study was supported by the National Natural Science Foundation of China (Grant No. 81772227, 81672056, and 81672058) and the National S & T Major Program (Grant No. 2017ZX10303404-002-006).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

Not applicable

Supplementary material

436_2019_6489_MOESM1_ESM.docx (40 kb)
ESM 1 (DOCX 40 kb)

References

  1. Araujo RA, Guedes RN, Oliveira MG, Ferreira GH (2008) Enhanced activity of carbohydrate- and lipid-metabolizing enzymes in insecticide-resistant populations of the maize weevil, Sitophilus zeamais. Bull Entomol Res 98(4):417–424.  https://doi.org/10.1017/S0007485308005737 CrossRefPubMedGoogle Scholar
  2. Benelli G, Lo Iacono A, Canale A, Mehlhorn H (2016) Mosquito vectors and the spread of cancer: an overlooked connection? Parasitol Res 115(6):2131–2137.  https://doi.org/10.1007/s00436-016-5037-y CrossRefPubMedGoogle Scholar
  3. Blandin S, Moita LF, Kocher T, Wilm M, Kafatos FC, Levashina EA (2002) Reverse genetics in the mosquito Anopheles gambiae: targeted disruption of the Defensin gene. EMBO Rep 3(9):852–856.  https://doi.org/10.1093/embo-reports/kvf180 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Boeuf P, Drummer HE, Richards JS, Scoullar MJ, Beeson JG (2016) The global threat of Zika virus to pregnancy: epidemiology, clinical perspectives, mechanisms, and impact. BMC Med 14(1):112.  https://doi.org/10.1186/s12916-016-0660-0 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Christeller JT, Amara S, Carriere F (2011) Galactolipase, phospholipase and triacylglycerol lipase activities in the midgut of six species of lepidopteran larvae feeding on different lipid diets. J Insect Physiol 57(9):1232–1239.  https://doi.org/10.1016/j.jinsphys.2011.05.012 CrossRefPubMedGoogle Scholar
  6. Dong Y, Aguilar R, Xi Z, Warr E, Mongin E, Dimopoulos G (2006) Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog 2(6):e52.  https://doi.org/10.1371/journal.ppat.0020052 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Fang F, Wang W, Zhang D, Lv Y, Zhou D, Ma L, Shen B, Sun Y, Zhu C (2015) The cuticle proteins: a putative role for deltamethrin resistance in Culex pipiens pallens. Parasitol Res 114(12):4421–4429.  https://doi.org/10.1007/s00436-015-4683-9 CrossRefPubMedGoogle Scholar
  8. Hirata K, Dichek HL, Cioffi JA, Choi SY, Leeper NJ, Quintana L, Kronmal GS, Cooper AD, Quertermous T (1999) Cloning of a unique lipase from endothelial cells extends the lipase gene family. J Biol Chem 274(20):14170–14175.  https://doi.org/10.1074/jbc.274.20.14170 CrossRefPubMedGoogle Scholar
  9. Holmquist M (2000) Alpha/Beta-hydrolase fold enzymes: structures, functions and mechanisms. Curr Protein Pept Sci 1(2):209–235CrossRefGoogle Scholar
  10. Horne I, Haritos VS, Oakeshott JG (2009) Comparative and functional genomics of lipases in holometabolous insects. Insect Biochem Mol Biol 39(8):547–567.  https://doi.org/10.1016/j.ibmb.2009.06.002 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Liu N (2015) Insecticide resistance in mosquitoes: impact, mechanisms, and research directions. Annu Rev Entomol 60:537–559.  https://doi.org/10.1146/annurev-ento-010814-020828 CrossRefPubMedGoogle Scholar
  12. Lv Y, Wang W, Hong S, Lei Z, Fang F, Guo Q, Hu S, Tian M, Liu B, Zhang D, Sun Y, Ma L, Shen B, Zhou D, Zhu C (2016) Comparative transcriptome analyses of deltamethrin-susceptible and -resistant Culex pipiens pallens by RNA-seq. Mol Genet Genom : MGG 291(1):309–321.  https://doi.org/10.1007/s00438-015-1109-4 CrossRefGoogle Scholar
  13. Main BJ, Everitt A, Cornel AJ, Hormozdiari F, Lanzaro GC (2018) Genetic variation associated with increased insecticide resistance in the malaria mosquito, Anopheles coluzzii. Parasit Vectors 11(1):225.  https://doi.org/10.1186/s13071-018-2817-5 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Mamidala P, Jones SC, Mittapalli O (2011) Metabolic resistance in bed bugs. Insects 2(1):36–48.  https://doi.org/10.3390/insects2010036 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Mitri C, Vernick KD (2012) Anopheles gambiae pathogen susceptibility: the intersection of genetics, immunity and ecology. Curr Opin Microbiol 15(3):285–291.  https://doi.org/10.1016/j.mib.2012.04.001 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Ritter M, Osei-Mensah J, Debrah LB, Kwarteng A, Mubarik Y, Debrah AY, Pfarr K, Hoerauf A, Layland LE (2019) Wuchereria bancrofti-infected individuals harbor distinct IL-10-producing regulatory B and T cell subsets which are affected by anti-filarial treatment. PLoS Negl Trop Dis 13(5):e0007436.  https://doi.org/10.1371/journal.pntd.0007436 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Shepard DS, Undurraga EA, Halasa YA, Stanaway JD (2016) The global economic burden of dengue: a systematic analysis. Lancet Infect Dis 16(8):935–941.  https://doi.org/10.1016/S1473-3099(16)00146-8 CrossRefPubMedGoogle Scholar
  18. Shi L, Hu H, Ma K, Zhou D, Yu J, Zhong D, Fang F, Chang X, Hu S, Zou F, Wang W, Sun Y, Shen B, Zhang D, Ma L, Zhou G, Yan G, Zhu C (2015) Development of resistance to pyrethroid in Culex pipiens pallens population under different insecticide selection pressures. PLoS Negl Trop Dis 9(8):e0003928.  https://doi.org/10.1371/journal.pntd.0003928 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Simma EA et al (2019) 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. Pest Manag Sci.  https://doi.org/10.1002/ps.5374 CrossRefGoogle Scholar
  20. Sumathi ME, Kumar SH, Shashidhar KN, Takkalaki N (2014) Prognostic significance of various biochemical parameters in acute organophosphorus poisoning. Toxicol Int 21(2):167–171.  https://doi.org/10.4103/0971-6580.139800 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Vilibic-Cavlek T et al (2019) Prevalence and molecular epidemiology of West Nile and Usutu virus infections in Croatia in the ‘One health’ context, 2018. Transbound Emerg Dis.  https://doi.org/10.1111/tbed.13225 CrossRefGoogle Scholar
  22. Wahid B, Ali A, Rafique S, Idrees M (2017) Current status of therapeutic and vaccine approaches against Zika virus. Eur J Internal Med 44:12–18.  https://doi.org/10.1016/j.ejim.2017.08.001 CrossRefGoogle Scholar
  23. Wang W, Liu SL, Liu YY, Qiao CL, Chen SL, Cui F (2015) Over-transcription of genes in a parathion-resistant strain of mosquito Culex pipiens quinquefasciatus. Insect science 22(1):150–156.  https://doi.org/10.1111/1744-7917.12106 CrossRefPubMedGoogle Scholar
  24. Xiong C, Fang F, Chen L, Yang Q, He J, Zhou D, Shen B, Ma L, Sun Y, Zhang D, Zhu C (2014) Trypsin-catalyzed deltamethrin degradation. PLoS One 9(3):e89517.  https://doi.org/10.1371/journal.pone.0089517 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Yang T, Liu N (2011) Genome analysis of cytochrome P450s and their expression profiles in insecticide resistant mosquitoes, Culex quinquefasciatus. PLoS One 6(12):e29418.  https://doi.org/10.1371/journal.pone.0029418 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Yang Q, Sun L, Zhang D, Qian J, Sun Y, Ma L, Sun J, Hu X, Tan W, Wang W, Zhu C (2008) Partial characterization of deltamethrin metabolism catalyzed by chymotrypsin. Toxicolo Vitro : Int J Publ Assoc BIBRA 22(6):1528–1533.  https://doi.org/10.1016/j.tiv.2008.05.007 CrossRefGoogle Scholar
  27. Yu X, Sun Q, Li B, Xie Y, Zhao X, Hong J, Sheng L, Sang X, Gui S, Wang L, Shen W, Hong F (2015) Mechanisms of larval midgut damage following exposure to phoxim and repair of phoxim-induced damage by cerium in Bombyx mori. Environ Toxicol 30(4):452–460.  https://doi.org/10.1002/tox.21921 CrossRefPubMedGoogle Scholar
  28. Zhou D, Hao S, Sun Y, Chen L, Xiong C, Ma L, Zhang D, Hong S, Shi L, Gong M, Zhou H, Yu X, Shen B, Zhu C (2012) Cloning and characterization of prophenoloxidase A3 (proPOA3) from Culex pipiens pallens. Comparative Biochem Physiol Part B, Biochem Mol Biol 162(4):57–65.  https://doi.org/10.1016/j.cbpb.2012.04.008 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Pathogen BiologyNanjing Medical UniversityNanjingChina
  2. 2.Department of Clinical Medical LaboratoryThe First Affiliated Hospital, and College of Clinical Medicine of Henan University of Science and TechnologyLuoyangChina

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