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Imidacloprid-induced pathophysiological damage in the midgut of Locusta migratoria (Orthoptera: Acrididae) in the field

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Abstract

Neonicotinoids are modern insecticides widely used in agriculture worldwide. Their impact on target (nervous system) and non-target (midgut) tissues has been well studied in beneficial insects including honeybees under controlled conditions. However, their detailed effects on pest insects on the field are missing to date. Here, we have studied the effects of the neonicotinoid imidacloprid on the midgut of the pest insect Locusta migratoria caught in the field. We found that in the midgut of imidacloprid-exposed locusts the activity of enzymes involved in reactive oxygen metabolism was perturbed. By contrast, the activity of P450 enzymes that have been shown to be activated in a detoxification response and that were also reported to produce reactive oxygen species was elevated. Probably as a consequence, markers of oxidative stress including protein carbonylation and lipid peroxidation accumulated in midgut samples of these locusts. Histological analyses revealed that their midgut epithelium is disorganized and that the brush border of the epithelial cells is markedly reduced. Indeed, microvilli are significantly shorter, misshapen and possibly non-functional in imidacloprid-treated locusts. We hypothesize that imidacloprid induces oxidative stress in the locust midgut, thereby changing the shape of midgut epithelial cells and probably in turn compromising their physiological function. Presumably, these effects reduce the survival rate of imidacloprid-treated locusts and the damage they cause in the field.

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Change history

  • 07 July 2022

    Author name tagging correction of the 5th Author.

References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

  • Amezian D, Nauen R, Le Goff G (2021) Transcriptional regulation of xenobiotic detoxification genes in insects—an overview. Pestic Biochem Physiol 174:104822

    Article  CAS  Google Scholar 

  • Anderson M (1989) Enzymatic and chemical methods for the determination of glutathione. In: Glutathione: chemical, biochemical and medical aspects. John Wiley & Sons Inc, pp 339–365

  • Arthidoro de Castro MB, Martinez LC, Cossolin JFS, Serra RS, Serrao JE (2020) Cytotoxic effects on the midgut, hypopharyngeal, glands and brain of Apis mellifera honey bee workers exposed to chronic concentrations of lambda-cyhalothrin. Chemosphere 248:126075

    Article  CAS  Google Scholar 

  • Bass C, Field LM (2018) Neonicotinoids. Curr Biol 28:R772–R773

    Article  CAS  Google Scholar 

  • Bierkens JG (2000) Applications and pitfalls of stress-proteins in biomonitoring. Toxicology 153:61–72

    Article  CAS  Google Scholar 

  • Brogdon W, Chan A (2010) Guidelines for evaluating insecticide resistance in vectors using the CDC bottle bioassay/methods in Anopheles research. CDC Atlanta USA CDC Tech Rep 1:1–28

    Google Scholar 

  • Buckingham S, Lapied B, Corronc H, Sattelle F (1997) Imidacloprid actions on insect neuronal acetylcholine receptors. J Exp Biol 200:2685–2692

    Article  CAS  Google Scholar 

  • Carmagnol F, Sinet PM, Rapin J, Jerome H (1981) Glutathione-S-transferase of human red blood cells; assay, values in normal subjects and in two pathological circumstances: hyperbilirubinemia and impaired renal function. Clin Chim Acta 117:209–217

    Article  CAS  Google Scholar 

  • Carneiro LS, Martinez LC, Oliveira AH, Cossolin JFS, Resende M, Goncalves WG, Medeiros-Santana L, Serrao JE (2022) Acute oral exposure to imidacloprid induces apoptosis and autophagy in the midgut of honey bee Apis mellifera workers. Sci Total Environ 815:152847

    Article  CAS  Google Scholar 

  • Casida JE, Durkin KA (2013) Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annu Rev Entomol 58:99–117

    Article  CAS  Google Scholar 

  • Castro B, Martinez LC, Plata-Rueda A, Soares MA, Tavares WS, Serrao JE, Zanuncio JC (2019) Chlorantraniliprole degenerates microvilli goblet cells of the Anticarsia gemmatalis (Lepidoptera: Noctuidae) midgut. Chemosphere 229:525–528

    Article  CAS  Google Scholar 

  • Chu F-F, Doroshow JH, Esworthy RS (1993) Expression, characterization, and tissue distribution of a new cellular selenium-dependent glutathione peroxidase, GSHPx-GI. J Biol Chem 268:2571–2576

    Article  CAS  Google Scholar 

  • Cui X, Wang C, Wang X, Li G, Liu Z, Wang H, Guo X, Xu B (2020) Molecular mechanism of the UDP-glucuronosyltransferase 2B20-like gene (AccUGT2B20-like) in pesticide resistance of Apis cerana cerana. Front Genet 11:592595

    Article  CAS  Google Scholar 

  • Dalle-Donne I, Rossi R, Giustarini D, Milzani A, Colombo R (2003) Protein carbonyl groups as biomarkers of oxidative stress. Clin Chim Acta 329:23–38

    Article  CAS  Google Scholar 

  • Delkash-Roudsari S, Chicas-Mosier AM, Goldansaz SH, Talebi-Jahromi K, Ashouri A, Abramson CI (2020) Assessment of lethal and sublethal effects of imidacloprid, ethion, and glyphosate on aversive conditioning, motility, and lifespan in honey bees (Apis mellifera L). Ecotoxicol Environ Saf 204:111108

    Article  CAS  Google Scholar 

  • Diaz P, Jeong SC, Lee S, Khoo C, Koyyalamudi SR (2012) Antioxidant and anti-inflammatory activities of selected medicinal plants and fungi containing phenolic and flavonoid compounds. Chinese Medicine 7:26

    Article  Google Scholar 

  • Elbert A, Haas M, Springer B, Thielert W, Nauen R (2008) Applied aspects of neonicotinoid uses in crop protection. Pest Manag Sci 64:1099–1105

    Article  CAS  Google Scholar 

  • El-Gendy AH, Augustyniak M, Toto NA, Al Farraj S, El-Samad LM (2020) Oxidative stress parameters, DNA damage and expression of HSP70 and MT in midgut of Trachyderma hispida (Forskal, 1775) (Coleoptera: Tenebrionidae) from a textile industry area. Environ Pollut 267:115661

    Article  CAS  Google Scholar 

  • Ellman GL, Courtney KD, Andres V Jr, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95

    Article  CAS  Google Scholar 

  • El-Saad AM, Kheirallah DA, El-Samad LM (2017) Biochemical and histological biomarkers in the midgut of Apis mellifera from polluted environment at Beheira Governorate. Egypt Environ Sci Pollut Res Int 24:3181–3193

    Article  CAS  Google Scholar 

  • Gao J, Jin SS, He Y, Luo JH, Xu CQ, Wu YY, Hou CS, Wang Q, Diao QY (2020) Physiological analysis and transcriptome analysis of Asian honey bee (Apis cerana cerana) in response to sublethal neonicotinoid imidacloprid. Insects 11(753):1–20

  • Hermes-Lima M, Willmore WG, Storey KB (1995) Quantification of lipid peroxidation in tissue extracts based on Fe (III) xylenol orange complex formation. Free Radical Biol Med 19:271–280

    Article  CAS  Google Scholar 

  • Jeschke P, Nauen R (2008) Neonicotinoids—from zero to hero in insecticide chemistry. Pest Manag Sci 64:1084–1098

    Article  CAS  Google Scholar 

  • Jeschke P, Nauen R, Schindler M, Elbert A (2011) Overview of the status and global strategy for neonicotinoids. J Agric Food Chem 59:2897–2908

    Article  CAS  Google Scholar 

  • Johnston G (1995) The study of interactive effects of pollutants: a biomarker approach. Sci Total Environ 171:205–212

    Article  CAS  Google Scholar 

  • King AM, MacRae TH (2015) Insect heat shock proteins during stress and diapause. Annu Rev Entomol 60:59–75

    Article  CAS  Google Scholar 

  • Lackie RE, Maciejewski A, Ostapchenko VG, Marques-Lopes J, Choy WY, Duennwald ML, Prado VF, Prado MAM (2017) The Hsp70/Hsp90 chaperone machinery in neurodegenerative diseases. Front Neurosci 11:254

    Article  Google Scholar 

  • Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz A-G, Ahn B-W, Shaltiel S, Stadtman ER (1990) [49] Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186:464–478

    Article  CAS  Google Scholar 

  • Lewis S, Handy RD, Cordi B, Billinghurst Z, Depledge MH (1999) Stress proteins (HSP’s): methods of detection and their use as an environmental biomarker. Ecotoxicology 8:351–368

    Article  CAS  Google Scholar 

  • Li X, Deng Z, Chen X (2021) Regulation of insect P450s in response to phytochemicals. Curr Opin Insect Sci 43:108–116

    Article  Google Scholar 

  • Liu T (1984) Ultrastructure of the midgut of the worker honey bee Apis mellifera heavily infected with Nosema apis. J Invertebr Pathol 44:282–291

    Article  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Lu K, Song Y, Zeng R (2021) The role of cytochrome P450-mediated detoxification in insect adaptation to xenobiotics. Curr Opin Insect Sci 43:103–107

    Article  Google Scholar 

  • Martelli F, Zhongyuan Z, Wang J, Wong CO, Karagas NE, Roessner U, Rupasinghe T, Venkatachalam K, Perry T, Bellen HJ, Batterham P (2020) Low doses of the neonicotinoid insecticide imidacloprid induce ROS triggering neurological and metabolic impairments in Drosophila. Proc Natl Acad Sci U S A 117:25840–25850

    Article  CAS  Google Scholar 

  • Matsuda K, Ihara M, Sattelle DB (2020) Neonicotinoid insecticides: molecular targets, resistance, and toxicity. Annu Rev Pharmacol Toxicol 60:241–255

    Article  CAS  Google Scholar 

  • Morakchi S, Maiza A, Farine P, Aribi N, Soltani N (2005) Effects of a neonicotinoid insecticide (acetamiprid) on acetylcholinesterase activity and cuticular hydrocarbons profil in German cockroaches. Commun Agric Appl Biol Sci 70:843–848

    CAS  Google Scholar 

  • Nebot C, Moutet M, Huet P, Xu J-Z, Yadan J, Chaudiere J (1993) Spectrophotometric assay of superoxide dismutase activity based on the activated autoxidation of a tetracyclic catechol. Anal Biochem 214:442–451

    Article  CAS  Google Scholar 

  • Palli SR (2020) CncC/Maf-mediated xenobiotic response pathway in insects. Archives of Insect Biochem Physiol 104:e21674

    Article  CAS  Google Scholar 

  • Parkinson RH, Little JM, Gray JR (2017) A sublethal dose of a neonicotinoid insecticide disrupts visual processing and collision avoidance behaviour in Locusta migratoria. Sci Rep 7:936

    Article  CAS  Google Scholar 

  • Parkinson RH, Zhang S, Gray JR (2020) Neonicotinoid and sulfoximine pesticides differentially impair insect escape behavior and motion detection. Proc Natl Acad Sci U S A 117:5510–5515

    Article  CAS  Google Scholar 

  • Peachey LD (1958) Thin sections. I. A study of section thickness and physical distortion produced during microtomy. J Biophys Biochem Cytol 4:233–242

    Article  CAS  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J CELL BIOL 17:208–212

    Article  CAS  Google Scholar 

  • Scandalios JG (2005) Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Braz J Med Biol Res 38:995–1014

    Article  CAS  Google Scholar 

  • Shapiro HM (2005) Practical flow cytometry. John Wiley & Sons

    Google Scholar 

  • Smith IK, Vierheller TL, Thorne CA (1988) Assay of glutathione reductase in crude tissue homogenates using 5, 5′-dithiobis (2-nitrobenzoic acid). Anal Biochem 175:408–413

    CAS  Google Scholar 

  • Suchail S, De Sousa G, Rahmani R, Belzunces LP (2004) In vivo distribution and metabolisation of 14C-imidacloprid in different compartments of Apis mellifera L. Pest Manag Sci 60:1056–1062

    Article  CAS  Google Scholar 

  • Tahmasebi P, Javadpour F, Sahimi M (2015) Three-dimensional stochastic characterization of shale SEM images. Transp Porous Media 110:521–531

    Article  Google Scholar 

  • Thompson DA, Lehmler HJ, Kolpin DW, Hladik ML, Vargo JD, Schilling KE, LeFevre GH, Peeples TL, Poch MC, LaDuca LE, Cwiertny DM, Field RW (2020) A critical review on the potential impacts of neonicotinoid insecticide use: current knowledge of environmental fate, toxicity, and implications for human health. Environ Sci Process Impacts 22:1315–1346

    Article  CAS  Google Scholar 

  • Tomizawa M, Casida JE (2005) Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu Rev Pharmacol Toxicol 45:247–268

    Article  CAS  Google Scholar 

  • Wang H-S, Zhou C-S, Guo W, Kang L (2006) Thermoperiodic acclimations enhance cold hardiness of the eggs of the migratory locust. Cryobiology 53:206–217

    Article  CAS  Google Scholar 

  • Wang HS, Wang XH, Zhou CS, Huang LH, Zhang SF, Guo W, Kang L (2007) cDNA cloning of heat shock proteins and their expression in the two phases of the migratory locust. Insect Mol Biol 16:207–219

    Article  CAS  Google Scholar 

  • Wang X, Anadon A, Wu Q, Qiao F, Ares I, Martinez-Larranaga MR, Yuan Z, Martinez MA (2018) Mechanism of neonicotinoid toxicity: impact on oxidative stress and metabolism. Annu Rev Pharmacol Toxicol 58:471–507

    Article  CAS  Google Scholar 

  • Wang H, Lu Z, Li M, Fang Y, Qu J, Mao T, Chen J, Li F, Sun H, Li B (2020) Responses of detoxification enzymes in the midgut of Bombyx mori after exposure to low-dose of acetamiprid. Chemosphere 251:126438

    Article  CAS  Google Scholar 

  • Wood TJ, Goulson D (2017) The environmental risks of neonicotinoid pesticides: a review of the evidence post 2013. Environ Sci Pollut Res Int 24:17285–17325

    Article  CAS  Google Scholar 

  • Wu K, Li S, Wang J, Ni Y, Huang W, Liu Q, Ling E (2020) Peptide hormones in the insect midgut. Front Physiol 11:191

    Article  Google Scholar 

  • Zhang L, Wang X, Cueto R, Effi C, Zhang Y, Tan H, Qin X, Ji Y, Yang X, Wang H (2019) Biochemical basis and metabolic interplay of redox regulation. Redox Biol 26:101284

    Article  CAS  Google Scholar 

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Funding

The contribution of BM was financed by the German Research Foundation (DFG MO1714/9).

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Authors and Affiliations

  1. Department of Zoology, Faculty of Science, Alexandria University, Alexandria, Egypt

    Lamia M. El-Samad

  2. Department of Zoology, Faculty of Science, Damanhour University, Damanhour, Egypt

    Mohamed S. El-Gerbed

  3. Department of Applied Entomology and Zoology, Faculty of Agriculture, Alexandria University, Alexandria, Egypt

    Hanaa S. Hussein

  4. Interfaculty Institute for Cell Biology, Eberhard-Karls Universität Tübingen, Tübingen, Germany

    Justin Flaven-Pouchon

  5. Department of Biological and Geological Sciences, Faculty of Education, Alexandria University, Alexandria, Egypt

    Abeer El Wakil

  6. Université Côte d’Azur, INRAE, CNRS, Institut Sophia Agrobiotech, Sophia Antipolis, France

    Bernard Moussian

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  1. Lamia M. El-Samad
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  2. Mohamed S. El-Gerbed
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  3. Hanaa S. Hussein
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  4. Justin Flaven-Pouchon
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  5. Abeer El Wakil
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  6. Bernard Moussian
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Contributions

L.M.E.-S. conceptualization, project administration, validation, formal analysis, supervision, revising the draft, M.S. E.-G. methodology, formal analysis, data curation, revising the draft, H.S.H. methodology, formal analysis, data curation, revising the draft, J.F.-P. formal statistical analysis, data curation, revising the draft, A.E.W. project administration, validation, supervision, reviewing and editing the draft, B.M. validation, formal statistical analysis, data curation, writing—original draft, reviewing and editing the draft.

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Correspondence to Bernard Moussian.

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El-Samad, L.M., El-Gerbed, M.S., Hussein, H.S. et al. Imidacloprid-induced pathophysiological damage in the midgut of Locusta migratoria (Orthoptera: Acrididae) in the field. Environ Sci Pollut Res 29, 57644–57655 (2022). https://doi.org/10.1007/s11356-022-19804-9

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