Skip to main content
SpringerLink
Log in

Inductions of a CYP6 cluster conferring deltamethrin resistance in colonized and field-collected Culex pipiens pallens

  • Arthropods and Medical Entomology - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Mosquitoes transmit many damaging vector-borne diseases. Unfortunately, the rise of insecticide resistance has become a major obstacle to mosquito control. A preliminary study showed that a CYP6 cluster is significant for deltamethrin resistance in colonized Culex pipiens pallens. Here, several field strains were collected to explore the association of the cluster in deltamethrin tolerance. We examined the effect of deltamethrin treatment on the cluster expression at a deltamethrin concentration of LC50 in these strains using five time points. As a result, both P450 induction and constitutive overexpression were associated with deltamethrin resistance. Deltamethrin could stimulate different expression sets in the P450 cluster in different strains, predominately correlated with the resistance level of the strain. Our results will offer more insight into working with the characterization of P450s related to insecticide resistance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

Not applicable.

Code availability

Not applicable.

References

  • Arensburger P, Megy K et al (2010) Sequencing of Culex quinquefasciatus establishes a platform for mosquito comparative genomics. Science 330(6000):86–88

    Article  CAS  Google Scholar 

  • Cardo MV, Rubio A et al (2018) Heterogeneous distribution of Culex pipiens, Culex quinquefasciatus and their hybrids along the urbanisation gradient. Acta Trop 178:229–235

    Article  CAS  Google Scholar 

  • Carvalho RA, Azeredo-Espin AM et al (2010) Deep sequencing of New World screw-worm transcripts to discover genes involved in insecticide resistance. BMC Genomics 11:695

    Article  CAS  Google Scholar 

  • Chaimanee V, Evans JD et al (2016) Sperm viability and gene expression in honey bee queens (Apis mellifera) following exposure to the neonicotinoid insecticide imidacloprid and the organophosphate acaricide coumaphos. J Insect Physiol 89:1–8

    Article  CAS  Google Scholar 

  • Chen HL, Lin LL et al (2017) Using Next-generation sequencing to detect differential expression genes in Bradysia odoriphaga after exposure to insecticides. Int J Mol Sci 18(11):2445

    Article  Google Scholar 

  • Cui PH, Lee AC et al (2010) Impaired transactivation of the human CYP2J2 arachidonic acid epoxygenase gene in HepG2 cells subjected to nitrative stress. Br J Pharmacol 159(7):1440–1449

    Article  CAS  Google Scholar 

  • Fang F, Wang W et al (2015) The cuticle proteins: a putative role for deltamethrin resistance in Culex pipiens pallens. Parasitol Res 114(12):4421–4429

    Article  Google Scholar 

  • Festucci-Buselli RA, Carvalho-Dias AS et al (2005) Expression of Cyp6g1 and Cyp12d1 in DDT resistant and susceptible strains of Drosophila melanogaster. Insect Mol Biol 14(1):69–77

    Article  CAS  Google Scholar 

  • Giraudo M, Hilliou F et al (2015) Cytochrome P450s from the fall armyworm (Spodoptera frugiperda): responses to plant allelochemicals and pesticides. Insect Mol Biol 24(1):115–128

    Article  CAS  Google Scholar 

  • Gong Y, Li T et al (2013) Permethrin induction of multiple cytochrome P450 genes in insecticide resistant mosquitoes, Culex quinquefasciatus. Int J Biol Sci 9(9):863–871

    Article  CAS  Google Scholar 

  • Ishak, I. H., B. Kamgang, et al. (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(1): e0005302.

  • Kirby GM, Nichols KD et al (2011) CYP2A5 induction and hepatocellular stress: an adaptive response to perturbations of heme homeostasis. Curr Drug Metab 12(2):186–197

    Article  CAS  Google Scholar 

  • Li F, Ni M et al (2015) Expression profile analysis of silkworm P450 family genes after phoxim induction. Pestic Biochem Physiol 122:103–109

    Article  CAS  Google Scholar 

  • Liu NN, Li M et al (2015) Cytochrome P450s-Their expression, regulation, and role in insecticide resistance. Pestic Biochem Physiol 120:77–81

    Article  CAS  Google Scholar 

  • Liu H, Xie L et al (2019) Trends in insecticide resistance in Culex pipiens pallens over 20 years in Shandong, China. Parasit Vectors 12(1):167

    Article  Google Scholar 

  • Lv Y, Wang W et al (2015) Comparative transcriptome analyses of deltamethrin-susceptible and -resistant Culex pipiens pallens by RNA-seq. Mol Genet Genomics 291(1):309–321

    Article  Google Scholar 

  • Muller C (2018) Impacts of sublethal insecticide exposure on insects – facts and knowledge gaps. Basic Appl Ecol 30:1–10

    Article  Google Scholar 

  • Nkya TE, Akhouayri I et al (2013) Impact of environment on mosquito response to pyrethroid insecticides: facts, evidences and prospects. Insect Biochem Mol Biol 43(4):407–416

    Article  CAS  Google Scholar 

  • Pavlidi N, Kampouraki A et al (2018) Molecular characterization of pyrethroid resistance in the olive fruit fly Bactrocera oleae. Pestic Biochem Physiol 148:1–7

    Article  CAS  Google Scholar 

  • Poupardin R, Reynaud S et al (2008) Cross-induction of detoxification genes by environmental xenobiotics and insecticides in the mosquito Aedes aegypti: impact on larval tolerance to chemical insecticides. Insect Biochem Mol Biol 38(5):540–551

    Article  CAS  Google Scholar 

  • Poupardin R, Riaz MA et al (2010) Transcription profiling of eleven cytochrome P450s potentially involved in xenobiotic metabolism in the mosquito Aedes aegypti. Insect Mol Biol 19(2):185–193

    Article  CAS  Google Scholar 

  • Scott JG, Yoshimizu MH et al (2015) Pyrethroid resistance in Culex pipiens mosquitoes. Pestic Biochem Phys 120:68–76

    Article  CAS  Google Scholar 

  • Smith, L. B., R. Tyagi, et al. (2018).  CYP-mediated permethrin resistance in Aedes aegypti and evidence for trans-regulation. PLoS Negl Trop Dis 12(11): e0006933.

  • Terhzaz S, Cabrero P et al (2015) A novel role of Drosophila cytochrome P450–4e3 in permethrin insecticide tolerance. Insect Biochem Mol Biol 67:38–46

    Article  CAS  Google Scholar 

  • Tian M, Liu B et al (2016) MiR-285 targets P450 (CYP6N23) to regulate pyrethroid resistance in Culex pipiens pallens. Parasitol Res 115(12):4511–4517

    Article  Google Scholar 

  • Wang W, Lv Y et al (2015) Identification of proteins associated with pyrethroid resistance by iTRAQ-based quantitative proteomic analysis in Culex pipiens pallens. Parasit Vectors 8:95

    Article  Google Scholar 

  • WHO (2005) Guidelines for laboratory and field testing of mosquito larvicides. World Health Organization, Geneva

    Google Scholar 

  • WHO (2012) Global plan for insecticide resistance management in malaria vectors. World Health Organization, Geneva

    Google Scholar 

  • WHO (2016) Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. World Health Organization, Geneva

    Google Scholar 

  • WHO (2017) Vector-borne diseases. World health Organization, Geneva

    Google Scholar 

  • WHO (2018) Neglected tropical diseases. World health Organization, Geneva

    Google Scholar 

  • Xu, J. B., X. H. Su, et al. (2018). Comparative transcriptome analysis and RNA interference reveal CYP6A8 and SNPs related to pyrethroid resistance in Aedes albopictus. Plos Neglected Tropical Diseases 12(11): e0006828.

  • Yang T, Liu N (2014) Permethrin resistance variation and susceptible reference line isolation in a field population of the mosquito, Culex quinquefasciatus (Diptera: Culicidae). Insect Sci 21(5):659–666

    Article  CAS  Google Scholar 

  • Yang, T. and N. N. Liu (2011). Genome analysis of cytochrome P450s and their expression profiles in insecticide resistant mosquitoes, Culex quinquefasciatus. Plos One 6(12): e29418.

  • Yang YX, Yu N et al (2018) Induction of P450 genes in Nilaparvata lugens and Sogatella furcifera by two neonicotinoid insecticides. Insect Sci 25(3):401–408

    Article  CAS  Google Scholar 

  • Yanola J, Chamnanya S et al (2015) Insecticides resistance in the Culex quinquefasciatus populations from northern Thailand and possible resistance mechanisms. Acta Trop 149:232–238

    Article  Google Scholar 

  • Zhang X, Kang X et al (2018) Transcriptome-wide survey, gene expression profiling and exogenous chemical-induced transcriptional responses of cytochrome P450 superfamily genes in migratory locust (Locusta migratoria). Insect Biochem Mol Biol 100:66–77

    Article  CAS  Google Scholar 

  • Zhang YX, Yibin Z (2003) The application of the pyrethroid in rice field modern agrochemicals. Mod Agroch 2:9–13

    CAS  Google Scholar 

  • Zhou D, Hao S et al (2012) Cloning and characterization of prophenoloxidase A3 (proPOA3) from Culex pipiens pallens. Comp Biochem Physiol B Biochem Mol Biol 162(4):57–65

    Article  CAS  Google Scholar 

  • Zhu F, Li T et al (2008) Co-up-regulation of three P450 genes in response to permethrin exposure in permethrin resistant house flies, Musca domestica. BMC Physiol 8:18

    Article  Google Scholar 

  • Zou, F., C. Chen, et al. (2015). Identification of QTLs conferring resistance to deltamethrin in Culex pipiens pallens. PLoS One 10(10): e0140923.

  • Zou FF, Guo Q et al (2016) Identification of protease m1 zinc metalloprotease conferring resistance to deltamethrin by characterization of an AFLP marker in Culex pipiens pallens. Parasit Vectors 9:172

    Article  CAS  Google Scholar 

  • Zou F, Guo Q et al (2019) A cluster of CYP6 gene family associated with the major quantitative trait locus is responsible for the pyrethroid resistance in Culex pipiens pallen. Insect Mol Biol 28(4):528–536

    CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China [Grant Number 81672058, 81971970, and 81471984], the National Institutes of Health of US (NIH) [Grant Number R01A1075746], the Natural Science Foundation of Jiangsu Province Fund [Grant Number BK20180824], and the Natural Science Research Project of Jiangsu Higher Education Institutions [19KJB310011].

Author information

Authors and Affiliations

  1. School of Medicine & Holistic Integrative Medicine, Nanjing University of Chinese Medicine, 138 Xianlin Road, Nanjing, Jiangsu, 210023, People’s Republic of China

    Feifei Zou, Wei Zhang, Miao Jiang & Wei Dong

  2. Department of Clinical Laboratory, The Affiliated Hospital of Jiangnan University, Wuxi, China

    Qin Guo

  3. Department of Pathogen Biology, Nanjing Medical University, 101 Longmian Avenue, Jiangning District, Nanjing, 211166, People’s Republic of China

    Xiaoshan Yang & Bo Shen

Authors
  1. Feifei Zou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qin Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiaoshan Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Miao Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wei Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bo Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

FFZ, XSY, and QG performed the experiments. FFZ, QG, and BS wrote the manuscript and prepared the figures. FFZ, QG, WZ, WD, and MJ participated in data analyses. FFZ and BS conceived the idea and coordinated the project. All authors have read and approved the final version of the manuscript for submission.

Corresponding author

Correspondence to Bo Shen.

Ethics declarations

Ethics approval

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

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Conflict of interest

The authors declare no competing interests.

Additional information

Section Editor: Guido Favia

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Feifei Zou and Qin Guo contributed equally to this work.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zou, F., Guo, Q., Yang, X. et al. Inductions of a CYP6 cluster conferring deltamethrin resistance in colonized and field-collected Culex pipiens pallens. Parasitol Res 121, 75–85 (2022). https://doi.org/10.1007/s00436-021-07351-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-021-07351-0

Keywords

Search

Navigation