Multiple-P450 Gene Co-Up-Regulation in the Development of Permethrin Resistance in the House Fly,

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2023 Feb 25

PMID 36834582

Authors

Ming Li

Xuechun Feng

William R Reid

Fang Tang

Nannan Liu

Affiliations

Soon will be listed here.

Abstract

This paper reports a study conducted at the whole transcriptome level to characterize the P450 genes involved in the development of pyrethroid resistance, utilizing expression profile analyses of 86 cytochrome P450 genes in house fly strains with different levels of resistance to pyrethroids/permethrin. Interactions among the up-regulated P450 genes and possible regulatory factors in different autosomes were examined in house fly lines with different combinations of autosomes from a resistant house fly strain, ALHF. Eleven P450 genes that were significantly up-regulated, with levels > 2-fold those in the resistant ALHF house flies, were in CYP families 4 and 6 and located on autosomes 1, 3 and 5. The expression of these P450 genes was regulated by trans- and/or cis-acting factors, especially on autosomes 1 and 2. An in vivo functional study indicated that the up-regulated P450 genes also conferred permethrin resistance in transgenic lines. An in vitro functional study confirmed that the up-regulated P450 genes are able to metabolize not only cis- and trans-permethrin, but also two metabolites of permethrin, PBalc and PBald. In silico homology modeling and the molecular docking methodology further support the metabolic capacity of these P450s for permethrin and substrates. Taken together, the findings of this study highlight the important function of multi-up-regulated P450 genes in the development of insecticide resistance in house flies.

Citing Articles

Unveiling the Role of Two Rhodopsin-like GPCR Genes in Insecticide-Resistant House Flies, .

Xin J, Brown D, Wang Y, Wang X, Li M, Li T Int J Mol Sci. 2024; 25(19).

PMID: 39408947 PMC: 11477390. DOI: 10.3390/ijms251910618.

The P450-Monooxygenase Activity and CYP6D1 Expression in the Chlorfenapyr-Resistant Strain of L.

Krestonoshina K, Melnichuk A, Kinareikina A, Maslakova K, Yangirova L, Silivanova E Insects. 2024; 15(6).

PMID: 38921174 PMC: 11203901. DOI: 10.3390/insects15060461.

Biological Fitness Cost, Demographic Growth Characteristics, and Resistance Mechanism in Alpha-Cypermethrin-Resistant (Diptera: Muscidae).

Hafez A, Abbas N Biology (Basel). 2023; 12(7).

PMID: 37508450 PMC: 10376271. DOI: 10.3390/biology12071021.

References

Mugenzi L, Menze B, Tchouakui M, Wondji M, Irving H, Tchoupo M . Cis-regulatory CYP6P9b P450 variants associated with loss of insecticide-treated bed net efficacy against Anopheles funestus. Nat Commun. 2019; 10(1):4652. PMC: 6789023. DOI: 10.1038/s41467-019-12686-5. View

Kalsi M, Palli S . Transcription factors, CncC and Maf, regulate expression of CYP6BQ genes responsible for deltamethrin resistance in Tribolium castaneum. Insect Biochem Mol Biol. 2015; 65:47-56. DOI: 10.1016/j.ibmb.2015.08.002. View

Yang T, Liu N . Genome analysis of cytochrome P450s and their expression profiles in insecticide resistant mosquitoes, Culex quinquefasciatus. PLoS One. 2012; 6(12):e29418. PMC: 3248432. DOI: 10.1371/journal.pone.0029418. View

Pavlidi N, Vontas J, Van Leeuwen T . The role of glutathione S-transferases (GSTs) in insecticide resistance in crop pests and disease vectors. Curr Opin Insect Sci. 2018; 27:97-102. DOI: 10.1016/j.cois.2018.04.007. View

Chen S, Li X . Transposable elements are enriched within or in close proximity to xenobiotic-metabolizing cytochrome P450 genes. BMC Evol Biol. 2007; 7:46. PMC: 1852546. DOI: 10.1186/1471-2148-7-46. View

Gong Y, Li T, Zhang L, Gao X, Liu N . Permethrin induction of multiple cytochrome P450 genes in insecticide resistant mosquitoes, Culex quinquefasciatus. Int J Biol Sci. 2013; 9(9):863-71. PMC: 3805894. DOI: 10.7150/ijbs.6744. View

Liu N . Insecticide resistance in mosquitoes: impact, mechanisms, and research directions. Annu Rev Entomol. 2015; 60:537-59. DOI: 10.1146/annurev-ento-010814-020828. View

Ma K, Tang Q, Zhang B, Liang P, Wang B, Gao X . Overexpression of multiple cytochrome P450 genes associated with sulfoxaflor resistance in Aphis gossypii Glover. Pestic Biochem Physiol. 2019; 157:204-210. DOI: 10.1016/j.pestbp.2019.03.021. View

Brun-Barale A, Hema O, Martin T, Suraporn S, Audant P, Sezutsu H . Multiple P450 genes overexpressed in deltamethrin-resistant strains of Helicoverpa armigera. Pest Manag Sci. 2010; 66(8):900-9. DOI: 10.1002/ps.1960. View

10.

Stevenson B, Bibby J, Pignatelli P, Muangnoicharoen S, ONeill P, Lian L . Cytochrome P450 6M2 from the malaria vector Anopheles gambiae metabolizes pyrethroids: Sequential metabolism of deltamethrin revealed. Insect Biochem Mol Biol. 2011; 41(7):492-502. DOI: 10.1016/j.ibmb.2011.02.003. View

11.

Hu B, Huang H, Hu S, Ren M, Wei Q, Tian X . Changes in both trans- and cis-regulatory elements mediate insecticide resistance in a lepidopteron pest, Spodoptera exigua. PLoS Genet. 2021; 17(3):e1009403. PMC: 7978377. DOI: 10.1371/journal.pgen.1009403. View

12.

Cojocaru V, Winn P, Wade R . The ins and outs of cytochrome P450s. Biochim Biophys Acta. 2006; 1770(3):390-401. DOI: 10.1016/j.bbagen.2006.07.005. View

13.

Tange S, Fujimoto N, Uramaru N, Sugihara K, Ohta S, Kitamura S . In vitro metabolism of cis- and trans-permethrin by rat liver microsomes, and its effect on estrogenic and anti-androgenic activities. Environ Toxicol Pharmacol. 2014; 37(3):996-1005. DOI: 10.1016/j.etap.2014.03.009. View

14.

Li T, Liu N . The Function of G-Protein-Coupled Receptor-Regulatory Cascade in Southern House Mosquitoes (Diptera: Culicidae). J Med Entomol. 2018; 55(4):862-870. PMC: 6025232. DOI: 10.1093/jme/tjy022. View

15.

Gotoh O . Substrate recognition sites in cytochrome P450 family 2 (CYP2) proteins inferred from comparative analyses of amino acid and coding nucleotide sequences. J Biol Chem. 1992; 267(1):83-90. View

16.

Irwin J, Sterling T, Mysinger M, Bolstad E, Coleman R . ZINC: a free tool to discover chemistry for biology. J Chem Inf Model. 2012; 52(7):1757-68. PMC: 3402020. DOI: 10.1021/ci3001277. View

17.

Rosen R, Lebedev G, Kontsedalov S, Ben-Yakir D, Ghanim M . A De Novo Transcriptomics Approach Reveals Genes Involved in Thrips Tabaci Resistance to Spinosad. Insects. 2021; 12(1). PMC: 7828677. DOI: 10.3390/insects12010067. View

18.

Cao C, Sun L, Du H, Moural T, Bai H, Liu P . Physiological functions of a methuselah-like G protein coupled receptor in Lymantria dispar Linnaeus. Pestic Biochem Physiol. 2019; 160:1-10. DOI: 10.1016/j.pestbp.2019.07.002. View

19.

Wilding C, Smith I, Lynd A, Yawson A, Weetman D, Paine M . A cis-regulatory sequence driving metabolic insecticide resistance in mosquitoes: functional characterisation and signatures of selection. Insect Biochem Mol Biol. 2012; 42(9):699-707. DOI: 10.1016/j.ibmb.2012.06.003. View

20.

Ibrahim S, Riveron J, Stott R, Irving H, Wondji C . The cytochrome P450 CYP6P4 is responsible for the high pyrethroid resistance in knockdown resistance-free Anopheles arabiensis. Insect Biochem Mol Biol. 2015; 68:23-32. PMC: 4717123. DOI: 10.1016/j.ibmb.2015.10.015. View