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Overexpression of cytochrome P450 and esterase genes involved in permethrin resistance in larvae and adults of Culex quinquefasciatus

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Abstract

Mosquitoes are important vectors of several arthropod-borne diseases, which remain a priority for epidemiological research. Mosquito vector control strategies have traditionally relied on chemical insecticides such as synthetic pyrethroids. However, the indiscriminate use of pesticides has resulted in the development of resistance in many mosquito species. In insects, resistance evolves primarily through the overexpression of one or more gene products from the cytochrome P450, carboxylesterase, and glutathione superfamilies. The current study examined the expression of cytochrome P450 CYP6M2, CYP6AA7, CYP6Z2, CYP9J34, α-Esterase, Esterase B1, and neuroactin genes in larvae and adults of a permethrin-resistant (PerRes) and susceptible (Sus) Culex quinquefasciatus strains. The results showed that the CYP6AA7 gene was overexpressed (10-fold) in larvae and adults with PerRes (p < 0.01) followed by CYPJ34 (9.0-fold) and CYP6Z2 (5.0-fold) compared to the Sus, whereas fewer changes in CYP6M gene expression were observed in PerRes adults (p < 0.05), and no expression was found in larvae. The esterase gene was overexpressed in PerRes larvae (9.0-fold) followed by adults (2.5-fold) compared to the susceptible strain. Based on data, the present study suggests that cytochrome P450, CYP6AA7, CYP6Z2, CYP9J34, α-Esterase, Esterase B1, and neuroactin genes were involved in permethrin resistance in larval and adult Cx. quinquefasciatus.

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References

  • Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267

    Article  CAS  Google Scholar 

  • Arensburger P, Megy K, Waterhouse RM, Abrudan J, Amedeo P, Antelo B, Bartholomay L, Bidwell S, Caler E, Camara F, Campbell CL, Campbell KS, Casola C, Castro MT, Chandramouliswaran I, Chapman SB, Christley S, Costas J, Eisenstadt E, Feschotte C, Fraser-Liggett C, Guigo R, Haas B, Hammond M, Hansson BS, Hemingway J, Hill SR, Howarth C, Ignell R, Kennedy RC, Kodira CD, Lobo NF, Mao C, Mayhew G, Michel K, Mori A, Liu N, Naveira H, Nene V, Nguyen N, Pearson MD, Pritham EJ, Puiu D, Qi Y, Ranson H, Ribeiro JM, Roberston HM, Severson DW, Shumway M, Stanke M, Strausberg RL, Sun C, Sutton G, Tu ZJ, Tubio JM, Unger MF, Vanlandingham DL, Vilella AJ, White O, White JR, Wondji CS, Wortman J, Zdobnov EM, Birren B, Christensen BM, Collins FH, Cornel A, Dimopoulos G, Hannick LI, Higgs S, Lanzaro GC, Lawson D, Lee NH, Muskavitch MA, Raikhel AS, Atkinson PW (2010) Sequencing of Culex quinquefasciatus establishes a platform for mosquito comparative genomics. Science 330(6000):86–8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brogdon WG, Chan A (2010) Guideline for evaluating insecticide resistance in vectors using the CDC bottle bioassay. Centers for Disease Control and Prevention, Atlanta, pp 1–28

  • Brogdon WG, McAllister JC (1998) Simplification of adult mosquito bioassays through use of time-mortality determinations in glass bottles. J Am Mosq Contr Assoc 14:159–164

    CAS  Google Scholar 

  • Chareonviriyaphap T, Bangs MJ, Suwonkerd W, Kongmee M, Corbel V, Ngoen-Klan R (2013) Review of insecticide resistance and behavioral avoidance of vectors of human diseases in Thailand. Parasites Vectors 6(1):1–28

    Article  Google Scholar 

  • Claudianos C, Ranson H, Johnson R, Biswas S, Schuler M, Berenbaum M, Feyereisen R, Oakeshott JG (2006) A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Mol Biol 15(5):615–636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • David JP, Strode C, Vontas J, Nikou D, Vaughan A, Pignatelli PM, Louis C, Hemingway J, Ranson H (2005) The Anopheles gambiae detoxification chip: a highly specific microarray to study metabolic-based insecticide resistance in malaria vectors. Proc Natl Acad Sci 102(11):4080–4084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Djouaka RF, Bakare AA, Coulibaly ON, Akogbeto MC, Ranson H, Hemingway J, Strode C (2008) Expression of the cytochrome P450s, CYP6P3 and CYP6M2 are significantly elevated in multiple pyrethroid resistant populations of Anopheles gambiae ss. from Southern Benin and Nigeria. BMC Genomics 9(1):1–10

    Article  Google Scholar 

  • Donnelly MJ, Corbel V, Weetman D, Wilding CS, Williamson MS, Black WC IV (2009) Does kdr genotype predicts insecticide-resistance phenotype in mosquitoes. Trends Parasitol 25(5):213–219

    Article  CAS  PubMed  Google Scholar 

  • Feyereisen R (2006) Evolution of insect P450. Biochem Soc Trans 34:1252–1255

    Article  CAS  PubMed  Google Scholar 

  • Gong Y, Li T, Feng Y, Liu N (2017) The function of two P450s, CYP9M10 and CYP6AA7, in the permethrin resistance of Culex quinquefasciatus. Sci Rep 7:587

    Article  PubMed  PubMed Central  Google Scholar 

  • Guntay O, Yikilmaz MS, Ozaydin H, Izzetoglu S, Suner A (2018) Evaluation of pyrethroid susceptibility in Culex pipiens of Northern Izmir Province, Turkey. J Arthropod Borne Dis 12(4):370–377

    PubMed  PubMed Central  Google Scholar 

  • Hemingway J, Ranson H (2000) Insecticide resistance in insect vectors of human disease. Annual Rev Entomol 45(1):371–391

    Article  CAS  Google Scholar 

  • Komagata O, Kasai S, Tomita T (2010) Overexpression of cytochrome P450 genes in pyrethroid-resistant Culex quinquefasciatus. Insect Biochem Mol Biol 40(2):146–152

    Article  CAS  PubMed  Google Scholar 

  • Liu N (2015) Insecticide resistance in mosquitoes: impact, mechanisms, and research directions. Annu Rev Entomol 60:537–559

    Article  CAS  PubMed  Google Scholar 

  • Liu CG, Calin GA, Meloon B, Gamliel N, Sevignani C, Ferracin M, Dumitru CD, Shimizu M, Zupo S, Dono M (2004) An oligonucleotide microchip for genome-wide microRNA profiling in human and mouse tissues. Proc Natl Acad Sci 101(26):9740–9744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu N, Li T, Reid WR, Yang T, Zhang L (2011) Multiple cytochrome P450 genes: their constitutive overexpression and permethrin induction in insecticide resistant mosquitoes, Culex quinquefasciatus. PLoS One 6:e23403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mamatha V, Muthusamy R, Murugan JM, Kweka EJ (2020) Effect of cypermethrin on worker and soldier termites of subterranean termites Odontotermes brunneus (Hagen)(Termitidae: Isoptera). Proc Zool Soc 73:40–45

    Article  Google Scholar 

  • Marcombe S, Fustec B, Cattel J, Chonephetsarath S, Thammavong P, Phommavanh N, David JP, Corbel V, Sutherland IW, Hertz JC, Brey PT (2019) Distribution of insecticide resistance and mechanisms involved in the arbovirus vector Aedes aegypti in Laos and implication for vector control. PLoS Negl Trop Dis 13(12):e0007852

    Article  PubMed  PubMed Central  Google Scholar 

  • Martins WFS, Wilding CS, Isaacs AT, Rippon EJ, Megy K, Donnelly MJ (2019) Transcriptomic analysis of insecticide resistance in the lymphatic filariasis vector Culex quinquefasciatus. Sci Rep 9(1):1–13

    Google Scholar 

  • Mueller P, Chouaibou M, Pignatelli P, Etang J, Walker ED, Donnelly MJ, Simard F, Ranson H (2008) Pyrethroid tolerance is associated with elevated expression of antioxidants and agricultural practice in Anopheles arabiensis sampled from an area of cotton fields in Northern Cameroon. Mol Ecol 17(4):1145–1155

    Article  Google Scholar 

  • Muthusamy R, Shivakumar MS (2015a) Involvement of metabolic resistance and F1534C kdr mutation in the pyrethroid resistance mechanisms of Aedes aegypti in India. Acta Tropica 148:137–141

    Article  CAS  PubMed  Google Scholar 

  • Muthusamy R, Shivakumar MS (2015b) Resistance selection and molecular mechanisms of cypermethrin resistance in red hairy caterpillar (Amsacta albistriga Walker). Pestic Biochem Physiol 117:54–61

    Article  CAS  PubMed  Google Scholar 

  • Muthusamy R, Vishnupriya M, Shivakumar MS (2014) Biochemical mechanism of chlorantraniliprole resistance in Spodoptera litura (Fab) (Lepidoptera: Noctuidae). J Asia-Pac Entomol 17(4):865–869

    Article  CAS  Google Scholar 

  • Narayanan M, Muthusamy R, Shivakumar MS, Suresh K, Sabariswaran K (2020) Toxicity of cypermethrin and enzyme inhibitor synergists in red hairy caterpillar Amsacta albistriga (Lepidoptera: Arctiidae). J Basic Appl Zool 81(1):1–8

    Article  Google Scholar 

  • Omotayo AI, Dogara MM, Sufi D, Shuaibu T, Balogun J, Dawaki S, Muktar B, Adeniyi K, Garba N, Namadi I, Adam HA, Adamu S, Abdullahi H, Sulaiman A, Oduola AO (2022) High pyrethroid-resistance intensity in Culex quinquefasciatus (Say) (Diptera: Culicidae) populations from Jigawa, North-West, Nigeria. PLoS Negl Trop Dis 16(6):e0010525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prasannakumar NR, Jyothi N, Ramkumar G, Asokan R, Sridhar V (2021) Assessment of cross-resistance in South American tomato moth, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Pest Manag Hortic Ecosyst 27(2):265–269

    Google Scholar 

  • Prasannakumar NR, Rao VK, Jyothi N, Saroja S, Lokesha AN, Ramkumar G (2023) Evaluation of insecticidal properties of botanicals for sustainable management of sucking pests of horticultural crops. J Appl Entomol 147:105–115

    Article  CAS  Google Scholar 

  • Ramkumar G, Shivakumar MS (2015) Laboratory development of permethrin resistance and cross-resistance pattern of Culex quinquefasciatus to other insecticides. Parasitol Res 114(7):2553–2560

    Article  PubMed  Google Scholar 

  • Ramkumar G, Asokan R, Prasannakumar NR, Kariyanna B, Karthi S, Alwahibi MS, Elshikh MS, Abdel-Megeed A, Ghaith A, Senthil-Nathan S, Kalaivani K (2021) RNA interference suppression of V-ATPase B and juvenile hormone binding protein genes through topically applied DsRNA on tomato leaves: developing biopesticides to control the South American pinworm, Tuta Absoluta (Lepidoptera: Gelechiidae). Front Physiol 12:742871

    Article  PubMed  PubMed Central  Google Scholar 

  • Ramkumar G, Muthusamy R, Narayanan M, Dhanapal R, Karthik C, Shivakumar MS, Malathi G, Kariyanna B (2022) Pretreatment of mosquito larvae with ultraviolet-B and nitropolycyclic aromatic hydrocarbons induces increased sensitivity to permethrin toxicity. Heliyon 8(10):e11094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shyam-Sundar N, Ramasubramanian R, Karthi S, Senthil-Nathan S, Chanthini KMP, Sivanesh H, Stanley-Raja V, Ramkumar G, Narayanan KR, Mahboob S, Al-Ghanim KA (2022) Effects of phytocompound Precocene 1 on the expression and functionality of the P450 gene in λ-cyhalothrin-resistant Spodoptera litura (Fab.). Front Physiol 13:900570

    Article  PubMed  PubMed Central  Google Scholar 

  • Sowndarya P, Ramkumar G, Shivakumar MS (2017) Green synthesis of selenium nanoparticles conjugated Clausena dentata plant leaf extract and their insecticidal potential against mosquito vectors. Artif Cells Nanomed Biotechnol 45(8):1490–1495

    Article  CAS  PubMed  Google Scholar 

  • Talipouo A, Mavridis K, Nchoutpouen E, Djiappi-Tchamen B, Fotakis EA, Kopya E, Bamou R, Kekeunou S, Awono-Ambene P, Balabanidou V, Balaska S, Wondji CS, Vontas J, Antonio-Nkondjio C (2021) High insecticide resistance mediated by different mechanisms in Culex quinquefasciatus populations from the city of Yaoundé, Cameroon. Sci Rep 11(1):7322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vivekanandhan P, Ayyavu T, Kweka EJ, Mahande AM (2021) Resistance to temephos in Anopheles stephensi larvae is associated with increased cytochrome P450 and α-esterase genes overexpression. Int J Trop Insect Sci 41(4):2543–2548

    Article  Google Scholar 

  • Wang K, Huang Y, Li X, Chen M (2018) Functional analysis of a carboxylesterase gene associated with isoprocarb and cyhalothrin resistance in Rhopalosiphum padi (L.). Front Physiol 9:992

    Article  PubMed  PubMed Central  Google Scholar 

  • Weedall GD, Mugenzi LM, Menze BD, Tchouakui M, Ibrahim SS, Amvongo-Adjia N, Irving H, Wondji MJ, Tchoupo M, Djouaka R (2019) A cytochrome P450 allele confers pyrethroid resistance on a major African malaria vector, reducing insecticide-treated bednet efficacy. Sci Trans Med 11:484

    Article  Google Scholar 

  • Weetman D, Djogbenou LS, Lucas E (2018) Copy number variation (CNV) and insecticide resistance in mosquitoes: evolving knowledge or an evolving problem. Curr Opin Insect Sci 27:82–88

    Article  PubMed  PubMed Central  Google Scholar 

  • Wei DD, He W, Miao ZQ, Tu YQ, Wang L, Dou W, Wang JJ (2020) Characterization of esterase genes involving malathion detoxification and establishment of an RNA interference method in Liposcelis bostrychophila. Front Physiol 11:274

    Article  PubMed  PubMed Central  Google Scholar 

  • Wheelock CE, Shan G, Ottea J (2005) Overview of carboxylesterases and their role in the metabolism of insecticides. J Pestic Sci 30(2):75–83

    Article  CAS  Google Scholar 

  • WHO (1981) Instructions for determining the susceptibility or resistance of adult mosquitoes to organochlorine, organophosphate and carbamate insecticides, WHO/VBC/81.805. World Health Organization, Geneva

  • Wilding CS (2018) Regulating resistance: CncC: Maf, antioxidant response elements and the overexpression of detoxification genes in insecticide resistance. Curr Opin Insect Sci 27:89–96

    Article  PubMed  Google Scholar 

  • Wilding CS, Smith I, Lynd A, Yawson AE, Weetman D, Paine MJ, Donnelly MJ (2012) A cis-regulatory sequence driving metabolic insecticide resistance in mosquitoes: functional characterization and signatures of selection. Insect Biochem Mol Biol 42(9):699–707

    Article  CAS  PubMed  Google Scholar 

  • Yang T, Li T, Feng X, Li M, Liu S, Liu N (2021) Multiple cytochrome P450 genes: conferring high levels of permethrin resistance in mosquitoes, Culex quinquefasciatus. Sci Rep 11:9041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Zhang B, Yan D, Dong W, Yang W, Li Q, Zeng L, Wang J, Wang L, Hicks LM (2011) Two Arabidopsis cytochrome P450 monooxygenases, CYP714A1 and CYP714A2, function redundantly in plant development through gibberellins deactivation. Plant J 67(2):342–353

    Article  CAS  PubMed  Google Scholar 

  • Zhu F, Feng JN, Zhang L, Liu N (2008) Characterization of two novel cytochrome P450 genes in insecticide-resistant house-flies. Insect Mol Biol 17(1):27–37

    Article  PubMed  Google Scholar 

  • Zhu F, Li T, Zhang L, Liu N (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  PubMed  Google Scholar 

  • Zhu F, Parthasarathy R, Bai H, Woithe K, Kaussmann M, Nauen R, Harrison DA, Palli SR (2010) A brain-specific cytochrome P450 responsible for the majority of deltamethrin resistance in the QTC279 strain of Tribolium castaneum. Proc Natl Acad Sci 107(19):8557–8562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu F, Moural TW, Shah K, Palli SR (2013) Integrated analysis of cytochrome P450 gene superfamily in the red flour beetle, Tribolium castaneum. BMC Genomics 14(1):1–12

    Article  CAS  Google Scholar 

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Acknowledgements

The authors thank the Department of Biotechnology, Periyar University, Salem, Tamil Nadu, India, and PG and Research Center for Biotechnology, MGR College, Hosur, India, for providing the infrastructural facility. The authors would also like to thank the reviewer of this draft for valuable suggestions and changes.

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Govindaraju Ramkumar: Planned and conducted research, analyzed the data and wrote the original manuscript; Mathiyazhagan Narayanan: Help with RT-PCR analysis; Ranganathan Muthusamy: planning the research and editing the manuscript; Muthugoundar Subramanian Shivakumar: planning and supervising the research work; Eliningaya J. Kweka: Edited and reviewed the language and draft manuscript.

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Correspondence to Ranganathan Muthusamy.

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Ramkumar, G., Muthusamy, R., Narayanan, M. et al. Overexpression of cytochrome P450 and esterase genes involved in permethrin resistance in larvae and adults of Culex quinquefasciatus. Parasitol Res 122, 3205–3212 (2023). https://doi.org/10.1007/s00436-023-08010-2

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