Skip to main content
SpringerLink
Log in

Utilization of piperonyl butoxide and 1-aminobenzotriazole for metabolic studies of toxic chemicals in Daphnia magna and Chironomus yoshimatsui

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Daphnids and chironomids have been used to assess the ecological effects of chemicals released into water bodies; however, the toxicity mechanisms in organisms are generally difficult to identify. Here, we developed a system capable of estimating the contribution of cytochrome P450 (CYP) to the metabolism of test substances in Daphnia magna and Chironomus yoshimatsui based on toxicity differences in the absence and presence of the CYP inhibitors piperonyl butoxide (PBO) and 1-aminobenzotriazole (ABT). The optimum concentrations of PBO and ABT that could effectively reduce the toxicity of diazinon, which is toxic after oxidative metabolism in vivo, were determined as 0.5 and 0.6 mg/L for D. magna, and 2.0 and 40.0 mg/L for C. yoshimatsui, respectively. Acute immobilization tests of 15 insecticides were conducted for D. magna and C. yoshimatsui, with and without the optimum concentrations of PBO or ABT. In the presence of either inhibitor, chlorpyrifos and chlorfenapyr toxicity was reduced in both organisms, whereas those of thiocyclam, nereistoxin, and silafluofen were enhanced in C. yoshimatsui. Liquid chromatography-mass spectrometry analysis of D. magna and C. yoshimatsui samples exposed to chlorfenapyr confirmed that the level of the active metabolite produced by CYP was decreased by PBO or ABT in both organisms. The system to which the test substance was co-exposed to PBO or ABT will be valuable for estimating the contribution of CYPs to metabolism and elucidating the toxicity mechanism in daphnids and chironomids.

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

Similar content being viewed by others

Data availability

The datasets generated and/or analyzed during the current study are available from the corresponding author upon reasonable request.

References

  • Akkanen J, Kukkonen JVK (2003) Biotransformation and bioconcentration of pyrene in Daphnia magna. Aquat Toxicol 64:53–61

    Article  CAS  Google Scholar 

  • Ankley GT, Dierkes JR, Jensen DA, Peterson JS (1991) Piperonyl butoxide as a tool in aquatic toxicological research with organophosphate insecticides. Ecotoxicol Environ Safe 21:266–274

    Article  CAS  Google Scholar 

  • Ankley GT, Collyard SA (1995) Influence of piperonyl butoxide on the toxicity of organophosphate insecticides to three species of freshwater benthic invertebrates. Comp Biochem Physiol Part C 110:149–155

    Google Scholar 

  • Baldwin WS, Marko PB, Nelson DR (2009) The cytochrome P450 (CYP) gene super family in Daphnia pulex. BMC Genom 10:169

    Article  Google Scholar 

  • Brock TCM, Wijngaarden RPAV (2012) Acute toxicity tests with Daphnia magna, Americamysis bahia, Chironomus riparius, and Gammarus pulex, and implications of new EU requirements for the aquatic effect assessment of insecticides. Environ Sci Pollut Res 19:3610–3618

    Article  CAS  Google Scholar 

  • European Food Safety Authority (EFSA), European Union (2013) Guidance on tiered risk assessment for plant protection products for aquatic organisms in edge-of-field surface waters. EFSA J 11:3290

  • Farnham AW (1999) The mode of action of piperonyl butoxide with reference to studying pesticide resistance. In: Jones DG (ed) Piperonyl butoxide: The insecticide synergist, 1st edn. Elsevier, pp 199–213. https://doi.org/10.1016/B978-0-12-286975-4.X5000-1

  • Federal Government of the United States. Code of federal regulations (2022) Title 40: protection of environment. Chapter I: Environmental Protection Agency. https://www.ecfr.gov/current/title-40/chapter-I/

  • Gunning RV, Moores GD, Devonshire AL (1998) Inhibition of action resistance-related esterases by piperonyl butoxide in Helicoverpa armigera (Lepidoptera: Noctuidae) and Aphis gossypii (Hemiptera: Aphididae). In: Piperonyl butoxide: The insecticide synergist, 1st edn. Elsevier, p 215–226. https://doi.org/10.1016/B978-0-12-286975-4.X5000-1

  • Hamm JT, Wilson BW, Hinton DE (2001) Increased uptake and bioactivation with development positively modulate diazinon toxicity in early life stage medaka (Oryzias latipes). Toxicol Sci 61:304–313

    Article  CAS  Google Scholar 

  • Hatano R, Scott JG (1993) Anti-P450lpr antiserum inhibits the activation of chlorpyrifos to chlorpyrifos oxon in house fly microsomes. Pestic Biochem Physiol 45:228–233

    Article  CAS  Google Scholar 

  • Hodgson E, Levi PE (1998). Interactions of piperonyl butoxide with cytochrome p450. In: Piperonyl butoxide: The insecticide synergist, 1st edn. Elsevier, p 41–53. https://doi.org/10.1016/B978-0-12-286975-4.X5000-1

  • Insecticide Resistance Action Committee (IRAC) (2022) Mode of Action Classification. Version 10.3. https://irac-online.org/mode-of-action/

  • Ishimota M, Tomiyama N (2021) Generational sensitivity alteration in Chironomus yoshimatsui to carbamate and pharmaceutical chemicals and the effect on Catalase, CYP450, and hemoglobin gene transcription. Ecotoxicology 30:2119–2131

    Article  CAS  Google Scholar 

  • Iwasa T, Motoyama N, Ambrose JT, Roe RM (2004) Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee Apis mellifera. Crop Prot 23:371–378

    Article  CAS  Google Scholar 

  • Kashian DR (2004) Toxaphene detoxification and acclimation in Daphnia magna: Do cytochrome P-450 enzymes play a role? Comp Biochem Physiol Part C 137:53–63

    Google Scholar 

  • Kim RO, Jo MA, Song J, Kim IC, Yoon S, Kim WK (2018) Novel approach for evaluating pharmaceuticals toxicity using Daphnia model: Analysis of the mode of cytochrome P450-generated metabolite action after acetaminophen exposure. Aquat Toxicol 196:35–42

    Article  CAS  Google Scholar 

  • Le TH, Lim ES, Lee SK, Choi YW, Kim YH, Min J (2010) Effects of glyphosate and methidathion on the expression of the Dhb, Vtg, Arnt, CYP4 and CYP314 in Daphnia magna. Chemosphere 79:67–71

    Article  CAS  Google Scholar 

  • Lee BY, Choi BS, Kim MS, Park JC, Jeong CB, Han J, Lee JS (2019) The genome of the freshwater water flea Daphnia magna: A potential use for freshwater molecular ecotoxicology. Aquat Toxicol 210:69–84

    Article  CAS  Google Scholar 

  • Marsden PJ, Kuwano E, Fukuto TR (1982) Metabolism of carbosulfan [2,3-dihydro-2,2-dimethylbenzofuran-7-yl (di-n-butylaminothio) methylcarbamate] in the rat and house fly. Pesti Biochem Physiol 18:38–48

  • Matsumura F (1975) Modes of action of insecticides. In: Matsumura F (ed) Toxicology of insecticides, Springer, pp 105–163 https://doi.org/10.1007/978-1-4613-4410-0

  • McCarty LS, Mackay D (1993) Enhancing ecotoxicological modeling and assessment. Body residues and modes of toxic action. Environ Sci Technol 27:1718–1728

    Article  CAS  Google Scholar 

  • Ministry of Agriculture, Forestry and Fisheries (MAFF), Japan (2019) No. 30-shouan-6278, 29 March 2019

  • Montellano PRO (2018) 1-Aminobenzotriazole: A mechanism-based cytochrome p450 inhibitor and probe of cytochrome p450 biology. Med Chem 8:3. https://doi.org/10.4172/2161-0444.1000495

    Article  Google Scholar 

  • Nagai T (2016) Ecological effect assessment by species sensitivity distribution for 68 pesticides used in Japanese paddy fields. J Pestic Sci 41:6–14

    Article  CAS  Google Scholar 

  • Nair PM, Park SY, Choi J (2013) Characterization and expression of cytochrome p450 cDNA (CYP9AT2) in Chironomus riparius fourth instar larvae exposed to multiple xenobiotics. Environ Toxicol Pharmacol 36:1133–1140

    Article  CAS  Google Scholar 

  • Nelson DR, Nebert DW (2018) Cytochrome P450 (CYP) Gene Superfamily. eLS. https://doi.org/10.1002/9780470015902.a0005667.pub3

  • OECD (2004a) OECD guideline for testing of chemicals ‘Daphnia sp., acute immobilization test’. 13 April 2004.

  • OECD (2004b) OECD guideline for testing of chemicals ‘Sediment-Water Chironomid Toxicity Using Spiked Sediment’. 13 April 2004.

  • OECD (2004c) OECD guideline for testing of chemicals ‘Sediment-Water Chironomid Toxicity Using Spiked Water’. 13 April 2004.

  • OECD (2010) OECD guideline for testing of chemicals ‘Sediment-Water Chironomid Life-Cycle Toxicity Test Using Spiked Water or Spiked Sediment’. 22 July 2010.

  • OECD (2011) OECD guideline for testing of chemicals ‘Chironomus sp., acute immobilization test’. 28 July 2011.

  • Ohnuki S, Saika O, Matsumoto T, Baba K, Fujikake N (2016) Relationship between ecotoxicity and mode of action classification of insecticides and acaricides. Jpn J Environ Toxicol 19:59–70

    Google Scholar 

  • Pflugmacher S, Sandermann Jr. H (1998) Cytochrome p450 monooxygenases for fatty acids and xenobiotics in marine macroalgae. Plant Physiol 117:123–128

    Article  CAS  Google Scholar 

  • Pimprale SS, Besco CL, Bryson PK, Brown TM (1997) Increased susceptibility of pyrethroid-resistant tobacco budworm (Lepidoptera: Noctuidae) to chlorfenapyr. J Econ Entomol 90:49–54

    Article  CAS  Google Scholar 

  • Rakotondravelo ML, Anderson TD, Charlton RE, Zhu KY (2006) Sublethal effects of three pesticides on activities of selected target and detoxification enzymes in the aquatic midge, Chironomus tentans (diptera: chironomidae). Arch Environ Contam Toxicol 51:360–366

    Article  CAS  Google Scholar 

  • Religia P, Nguyen ND, Nong QD, Matsuura T, Kato Y, Watanabe H (2021) Mutation of the cytochrome p450 CYP360A8 gene increases sensitivity to paraquat in Daphnia magna. Environ Toxicol Chem 40:1279–1288

    Article  CAS  Google Scholar 

  • Roberts TR (1999) Nereistoxin precursor. In: Plimmer J (ed.) Metabolic pathways of agrochemicals. Part 2: Insecticides and fungicides, RSC publishing, pp 127–138

  • Schmidt AM, Sengupta N, Saski CA, Noorai RE, Baldwin WS (2017) RNA sequencing indicates that atrazine induces multiple detoxification genes in Daphnia magna and this is a potential source of its mixture interactions with other chemicals. Chemosphere 189:699–708

    Article  CAS  Google Scholar 

  • Scott JG, Liu N, Wen Z (1998) Insect cytochromes P450: diversity, insecticide resistance and tolerance to plant toxins. Comp Biochem Physiol Part C 121:147–155

    CAS  Google Scholar 

  • Scott JG (1999) Cytochromes P450 and insecticide resistance. Insect Biochem Mol Biol 29:757–777

    Article  CAS  Google Scholar 

  • Scott JG, Leichter CA, Rinkevich FD (2004) Insecticide resistant strains of house flies (Musca domestica) show limited cross-resistance to chlorfenapyr. Pestic Sci 292:124–126

    Article  Google Scholar 

  • Selby TP, George PL, Stevenson TM, Hughes KA, Cordova D, Annan IB, Barry JD, Benner EA, Currie MJ, Pahutski TF (2013) Discovery of cyantraniliprole, a potent and selective anthranilic diamide ryanodine receptor activator with cross-spectrum insecticidal activity. Bioorg Med Chem Lett 23:6341–6345

    Article  CAS  Google Scholar 

  • Tang G, Yao J, Li D, He Y, Zhu YC, Zhang X, Zhu KY (2017) Cytochrome p450 genes from the aquatic midge Chironomus tentans: atrazine-induced up-regulation of CtCYP6EX3 enhanced the toxicity of chlorpyrifos. Chemosphere 186:68–77

    Article  CAS  Google Scholar 

  • Tang G, Yao J, Zhang X, Lu N, Zhu KY (2018) Comparision of gene expression profiles in the aquatic midge (Chironomus tentans) larvae exposed to two major agricultural pesticides. Chemosphere 194:745–754

    Article  CAS  Google Scholar 

  • Taxak N, Kalra S, Bharatam PV (2013) Carbene generation by cytochromes and electronic structure of heme-iron-porphyrin-carbene complex: a quantum chemical study. Inorg Chem 52:5097–5109

    Article  CAS  Google Scholar 

  • Thies F, Backhaus T, Bossmann B, Grimme LH (1996) Xenobiotic biotransformation in unicellular green algae (involvement of cytochrome p450 in the activation and selectivity of the pyridazinone pro-herbicide metflurazon). Plant Physiol 112:361–370

    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 

  • Uno T, Ishizuka M, Itakura T (2012) Cytochrome p450 (CYP) in fish. Environ Toxicol Pharmacol 34:1–13

    Article  CAS  Google Scholar 

  • Usui M, Umezu K (1986) Metabolism of the insecticide benfuracarb in the housefly. J Pestic Sci 11:401–408

    Article  CAS  Google Scholar 

  • Wang L, Peng Y, Nie X, Pan B, Ku P, Bao S (2016) Gene response of CYP360A, CYP314, and GST and whole-organism changes in Daphnia magna exposed to Ibuprofen. Comp Biochem Physiol Part C 110:49–56

    Google Scholar 

  • Watanabe H, Kobayashi K, Kato Y, Oda S, Abe R, Tatarazako N, Iguchi T (2008) Transcriptome profiling in crustaceans as a tool for ecotoxicogenomics: Daphnia magna DNA microarray. Cell Biol Toxicol 24:641–647

    Article  CAS  Google Scholar 

  • Wickham J (1998) The use of synergized pyrethroids to control insect pests in and around domestic, industrial and food-handling premises. In: Jones DG (ed.) Piperonyl butoxide: The insecticide synergist, 1st edn. Elsevier, pp 239–260. https://doi.org/10.1016/B978-0-12-286975-4.X5000-1

  • Williams JA, Hyland R, Jones BC, Smith DA, Hurst S, Goosen TC, Peterkin V, Koup JR, Ball SE (2004) Drug-drug interactions for UDP-glucronosyltransferase substrates: a pharmacokinetic explanation for typically observed low exposure (AUC I /AUC) ratios. Drug Metab Dispos 32:1201–1208

    Article  CAS  Google Scholar 

  • Young SJ, Gunning RV, Moores GD (2005) The effect of piperonyl butoxide on pyrethroid-resistance-associated esterases in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Pest Manag Sci 61:397–401

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank the members of the Insecticide Group, Department of Biological Research, Odawara Research Center, Nippon Soda Co., Ltd., Japan for providing detailed information on the actual use of insecticides. This study was supported by the Promotion and Mutual Aid Corporation for Private Schools of Japan. The authors are indebted to Editage (www.editage.com) for correcting the English version of this manuscript.

Author information

Authors and Affiliations

  1. School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, 1432-1, Horinouchi, Hachioji, Tokyo, 192-0392, Japan

    Shinpei Ohnuki, Shinichi Tokishita & Shoko Fujiwara

  2. Odawara Research Center, Nippon Soda Co., Ltd., 345, Takada, Odawara, Kanagawa, 250-0280, Japan

    Shinpei Ohnuki, Yoko Osawa & Takeru Matsumoto

Authors
  1. Shinpei Ohnuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yoko Osawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Takeru Matsumoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shinichi Tokishita
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shoko Fujiwara
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shoko Fujiwara.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

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

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ohnuki, S., Osawa, Y., Matsumoto, T. et al. Utilization of piperonyl butoxide and 1-aminobenzotriazole for metabolic studies of toxic chemicals in Daphnia magna and Chironomus yoshimatsui. Ecotoxicology 32, 25–37 (2023). https://doi.org/10.1007/s10646-022-02617-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-022-02617-4

Keywords

Search

Navigation