دورية أكاديمية

Environmentally Relevant Concentrations of the Insecticide Fipronil Modulated Molecular Response in Chironomus riparius.

التفاصيل البيبلوغرافية
العنوان: Environmentally Relevant Concentrations of the Insecticide Fipronil Modulated Molecular Response in Chironomus riparius.
المؤلفون: Pinto TJDS; PPG-SEA and NEEA/CRHEA/SHS, São Carlos Engineering School, University of São Paulo, São Carlos, Brazil.; Analytical Chemistry Department, Institute of Chemistry, University of Campinas, Campinas, São Paulo, Brazil., Martínez-Guitarte JL; Department of Physics, Mathematics, and Fluids, National Distance Education University, Madrid, Spain., Amaral Dias M; Analytical Chemistry Department, Institute of Chemistry, University of Campinas, Campinas, São Paulo, Brazil., Montagner CC; Analytical Chemistry Department, Institute of Chemistry, University of Campinas, Campinas, São Paulo, Brazil., Espindola ELG; PPG-SEA and NEEA/CRHEA/SHS, São Carlos Engineering School, University of São Paulo, São Carlos, Brazil., Muñiz-González AB; Department of Physics, Mathematics, and Fluids, National Distance Education University, Madrid, Spain.; Department of Environment and Planning & CESAM, University of Aveiro, Aveiro, Portugal.
المصدر: Environmental toxicology and chemistry [Environ Toxicol Chem] 2024 Feb; Vol. 43 (2), pp. 405-417.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: SETAC Press Country of Publication: United States NLM ID: 8308958 Publication Model: Print Cited Medium: Internet ISSN: 1552-8618 (Electronic) Linking ISSN: 07307268 NLM ISO Abbreviation: Environ Toxicol Chem Subsets: MEDLINE
أسماء مطبوعة: Publication: Pensacola, FL : SETAC Press
Original Publication: New York : Pergamon Press, c1982-
مواضيع طبية MeSH: Insecticides*/toxicity , Chironomidae*/genetics , Water Pollutants, Chemical*/toxicity , Pyrazoles*, Animals ; Acetylcholinesterase/metabolism ; Larva/metabolism
مستخلص: Pesticides employed worldwide for crop protection easily reach aquatic systems, which act as the main reservoirs, and become a risk factor for aquatic fauna. Fipronil is a broad-spectrum insecticide acting on the insect nervous system; however, other effects and systems unrelated to this mechanism could be affected in non-target organisms. Thus, the present study aimed to assess the impact of fipronil on the suborganismal response (gene expression and enzymatic activity) of Chironomus riparius larvae as a model organism in ecotoxicology. To this end, short-term toxicity tests were carried out with fourth-instar larvae exposed to 0.001, 0.01, and 0.1 µg L -1 of fipronil for 24 and 96 h. Messenger RNA levels of 42 genes related to diverse metabolic pathways were analyzed by real-time polymerase chain reaction, complemented with catalase (CAT), glutathione S-transferase (GST), and acetylcholinesterase (AChE) activities. Few effects were observed at 24 h; however, after longer exposure (96 h), genes involved in the endocrine, detoxification, stress, and immune response pathways were altered. Moreover, fipronil at 96 h increased CAT and GST activity at 0.01 µg L -1 and AChE at the highest concentrations. The results demonstrate that even low environmentally relevant fipronil concentrations can modulate the molecular response of several cellular pathways in C. riparius after short-term exposure. These results bring new information about the underlying response of fipronil and its mode of action on a key aquatic invertebrate. Despite no effects on mortality, strong modulation at the suborganismal level emphasizes the advantage of biomarkers as early damage responses and the harmful impact of this pesticide on freshwater organisms. Environ Toxicol Chem 2024;43:405-417. © 2023 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.
(© 2023 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.)
References: Bavisotto, C. C., Alberti, G., Vitale, A. M., Paladino, L., Campanella, C., Rappa, F., Gorska, M., Conway de Macario, E., Cappello, F., Macario, A. J. L., & Gammazza, A. M. (2020). Hsp60 post-translational modifications: Functional and pathological consequences. Frontiers in Molecular Biosciences, 7, Article 95. https://doi.org/10.3389/fmolb.2020.00095.
Belles, X. (2020). Krüppel homolog 1 and E93: The doorkeeper and the key to insect metamorphosis. Archives of Insect Biochemistry and Physiology, 103(3), Article e21609. https://doi.org/10.1002/arch.21609.
Berenbaum, M. R., & Johnson, R. M. (2015). Xenobiotic detoxification pathways in honey bees. Current Opinion in Insect Science, 10, 51-58. https://doi.org/10.1016/j.cois.2015.03.005.
Bisthoven, L. G. J., Timmermans, K. R., & Ollevier, F. (1992). The concentration of cadmium, lead, copper and zinc in Chironomus grthummi larvae (Diptera, Chironomidae) with deformed versus normal menta. Hydrobiologia, 239(3), 141-149. https://doi.org/10.1007/BF00007671.
Bonmatin, J.-M., Giorio, C., Girolami, V., Goulson, D., Kreutzweiser, D. P., Krupke, C., Liess, M., Long, E., Marzaro, M., Mitchell, E. A. D., Noome, D. A., Simon-Delso, N., & Tapparo, A. (2015). Environmental fate and exposure; neonicotinoids and fipronil. Environmental Science and Pollution Research, 22(1), 35-67. https://doi.org/10.1007/s11356-014-3332-7.
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1), 248-254. https://doi.org/10.1016/0003-2697(76)90527-3.
Cahill, M. A. (2007). Progesterone receptor membrane component 1: An integrative review. The Journal of Steroid Biochemistry and Molecular Biology, 105(1), 16-36. https://doi.org/10.1016/j.jsbmb.2007.02.002.
Defelipe, L. A., Dolghih, E., Roitberg, A. E., Nouzova, M., Mayoral, J. G., Noriega, F. G., & Turjanski, A. G. (2011). Juvenile hormone synthesis: “Esterify then epoxidize” or “epoxidize then esterify”? Insights from the structural characterization of juvenile hormone acid methyltransferase. Insect Biochemistry and Molecular Biology, 41(4), 228-235. https://doi.org/10.1016/j.ibmb.2010.12.008.
de Souza, R. M., Seibert, D., Quesada, H. B., de Jesus Bassetti, F., Fagundes-Klen, M. R., & Bergamasco, R. (2020). Occurrence, impacts and general aspects of pesticides in surface water: A review. Process Safety and Environmental Protection, 135, 22-37. https://doi.org/10.1016/j.psep.2019.12.035.
Fang, W., Peng, Y., Muir, D., Lin, J., & Zhang, X. (2019). A critical review of synthetic chemicals in surface waters of the US, the EU and China. Environment International, 131, Article 104994. https://doi.org/10.1016/j.envint.2019.104994.
Farooq, M., & Freed, S. (2018). Mortality, biological, and biochemical response of Musca domestica (Diptera: Muscidae) to selected insecticides. Journal of Entomological Science, 53(1), 27-45. https://doi.org/10.18474/JES17-22.1.
Gao, H., Lin, X., Yang, B., & Liu, Z. (2021). The roles of GSTs in fipronil resistance in Nilaparvata lugens: Over-expression and expression induction. Pesticide Biochemistry and Physiology, 177, Article 104880. https://doi.org/10.1016/j.pestbp.2021.104880.
Ghorab, M. A., & Khalil, M. S. (2015). Toxicological effects of organophosphates pesticides. International Journal of Environmental Monitoring and Analysis, 3(4), 218-220. https://doi.org/10.11648/j.ijema.20150304.13.
Gilbert, L. I. (2004). Halloween genes encode P450 enzymes that mediate steroid hormone biosynthesis in Drosophila melanogaster. Molecular and Cellular Endocrinology, 215(1), 1-10. https://doi.org/10.1016/j.mce.2003.11.003.
Goff, A. D., Saranjampour, P., Ryan, L. M., Hladik, M. L., Covi, J. A., Armbrust, K. L., & Brander, S. M. (2017). The effects of fipronil and the photodegradation product fipronil desulfinyl on growth and gene expression in juvenile blue crabs, Callinectes sapidus, at different salinities. Aquatic Toxicology, 186, 96-104. https://doi.org/10.1016/j.aquatox.2017.02.027.
Goulart, B. V., Vizioli, B. D. C., Espindola, E. L. G., & Montagner, C. C. (2020). Matrix effect challenges to quantify 2,4-D and fipronil in aquatic systems. Environmental Monitoring and Assessment, 192(12), Article 797. https://doi.org/10.1007/s10661-020-08776-3.
Guittard, E., Blais, C., Maria, A., Parvy, J.-P., Pasricha, S., Lumb, C., Lafont, R., Daborn, P. J., & Dauphin-Villemant, C. (2011). CYP18A1, a key enzyme of Drosophila steroid hormone inactivation, is essential for metamorphosis. Developmental Biology, 349(1), 35-45. https://doi.org/10.1016/j.ydbio.2010.09.023.
Gunasekara, A. S., Truong, T., Goh, K. S., Spurlock, F., & Tjeerdema, R. S. (2007). Environmental fate and toxicology of fipronil. Journal of Pesticide Science, 32(3), 189-199. https://doi.org/10.1584/jpestics.R07-02.
Gupta, S. C., Sharma, A., Mishra, M., Mishra, R. K., & Chowdhuri, D. K. (2010). Heat shock proteins in toxicology: How close and how far? Life Sciences, 86(11), 377-384. https://doi.org/10.1016/j.lfs.2009.12.015.
Hodges, R. E., & Minich, D. M. (2015). Modulation of metabolic detoxification pathways using foods and food-derived components: A scientific review with clinical application. Journal of Nutrition and Metabolism, 2015, Article 760689. https://doi.org/10.1155/2015/760689.
Ighodaro, O. M., & Akinloye, O. A. (2018). First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alexandria Journal of Medicine, 54(4), 287-293. https://doi.org/10.1016/j.ajme.2017.09.001.
Lee, Y. H., Park, J. C., Hwang, U.-K., Lee, J.-S., & Han, J. (2018). Adverse effects of the insecticides chlordecone and fipronil on population growth and expression of the entire cytochrome P450 (CYP) genes in the freshwater rotifer Brachionus calyciflorus and the marine rotifer Brachionus plicatilis. Aquatic Toxicology, 202, 181-187. https://doi.org/10.1016/j.aquatox.2018.07.014.
Li, Y., & Schellhorn, H. E. (2007). Rapid kinetic microassay for catalase activity. Journal of Biomolecular Techniques, 18(4), 185-187.
Liu, Y., Yu, M., Cui, J., Du, Y., Teng, X., & Zhang, Z. (2021). Heat shock proteins took part in oxidative stress-mediated inflammatory injury via NF-κB pathway in excess manganese-treated chicken livers. Ecotoxicology and Environmental Safety, 226, Article 112833. https://doi.org/10.1016/j.ecoenv.2021.112833.
Lu, K., Song, Y., & Zeng, R. (2021). The role of cytochrome P450-mediated detoxification in insect adaptation to xenobiotics. Current Opinion in Insect Science, 43, 103-107. https://doi.org/10.1016/j.cois.2020.11.004.
Marchesan, E., Sartori, G. M. S., de Avila, L. A., Machado, S. L. O., Zanella, R., Primel, E. G., Macedo, V. R. M., & Marchezan, M. G. (2010). Residues of pesticides in the water of the Depression Central rivers in the state of Rio Grande do Sul, Brazil. Ciência Rural, 40, 1053-1059. https://doi.org/10.1590/S0103-84782010005000078.
Martínez-Guitarte, J.-L. (2018). Transcriptional activity of detoxification genes is altered by ultraviolet filters in Chironomus riparius. Ecotoxicology and Environmental Safety, 149, 64-71. https://doi.org/10.1016/j.ecoenv.2017.11.017.
Monteiro, H. R., Pestana, J. L. T., Novais, S. C., Leston, S., Ramos, F., Soares, A. M. V. M., Devreese, B., & Lemos, M. F. L. (2019). Assessment of fipronil toxicity to the freshwater midge Chironomus riparius: Molecular, biochemical, and organismal responses. Aquatic Toxicology, 216, Article 105292. https://doi.org/10.1016/j.aquatox.2019.105292.
Moreira, R. A., Araújo, C. V. M., Junio da Silva Pinto, T., Menezes da Silva, L. C., Goulart, B. V., Viana, N. P., Montagner, C. C., Fernandes, M. N., & Gaeta Espindola, E. L. (2021). Fipronil and 2,4-D effects on tropical fish: Could avoidance response be explained by changes in swimming behavior and neurotransmission impairments. Chemosphere, 263, Article 127972. https://doi.org/10.1016/j.chemosphere.2020.127972.
Mota, M. B. S., Carvalho, M. A., Monteiro, A. N. A., & Mesquita, R. D. (2019). DNA damage response and repair in perspective: Aedes aegypti, Drosophila melanogaster and Homo sapiens. Parasites & Vectors, 12(1), Article 533. https://doi.org/10.1186/s13071-019-3792-1.
Muñiz-González, A.-B. (2021). Ibuprofen as an emerging pollutant on non-target aquatic invertebrates: Effects on Chironomus riparius. Environmental Toxicology and Pharmacology, 81, Article 103537. https://doi.org/10.1016/j.etap.2020.103537.
Muñiz-González, A.-B., & Martínez-Guitarte, J.-L. (2020). Combined effects of benzophenone-3 and temperature on gene expression and enzymatic activity in the aquatic larvae Chironomus riparius. Science of the Total Environment, 698, Article 134292. https://doi.org/10.1016/j.scitotenv.2019.134292.
Muñiz-González, A.-B., Novo, M., & Martínez-Guitarte, J.-L. (2021). Persistent pesticides: Effects of endosulfan at the molecular level on the aquatic invertebrate Chironomus riparius. Environmental Science and Pollution Research, 28, 31431-31446. https://doi.org/10.1007/s11356-021-12669-4.
Mutzner, L., Furrer, V., Castebrunet, H., Dittmer, U., Fuchs, S., Gernjak, W., Gromaire, M.-C., Matzinger, A., Mikkelsen, P. S., Selbig, W. R., & Vezzaro, L. (2022). A decade of monitoring micropollutants in urban wet-weather flows: What did we learn? Water Research, 223, Article 118968. https://doi.org/10.1016/j.watres.2022.118968.
Nikonorov, Y. M., Syrtlanova, L. A., Kitaev, K. A., & Benkovskaya, G. V. (2018). Transcription activity of genes involved in diapause regulation in the Colorado potato beetle and its change under a fipronil impact. Russian Journal of Genetics: Applied Research, 8(1), 80-86. https://doi.org/10.1134/S2079059718010100.
Noorimotlagh, Z., Mirzaee, S. A., Ahmadi, M., Jaafarzadeh, N., & Rahim, F. (2018). The possible DNA damage induced by environmental organic compounds: The case of nonylphenol. Ecotoxicology and Environmental Safety, 158, 171-181. https://doi.org/10.1016/j.ecoenv.2018.04.023.
Organisation for Economic Co-operation and Development. (2011). Test No. 235: Chironomus sp., acute immobilisation test. OECD guidelines for the testing of chemicals. https://www.oecd-ilibrary.org/content/publication/9789264122383-en.
Peret, A. M., Oliveira, L. F., Bianchini, I., Seleghim, M. H. R., Peret, A. C., & Mozeto, A. A. (2010). Dynamics of fipronil in Óleo Lagoon in Jataí Ecological Station, São Paulo-Brazil. Chemosphere, 78(10), 1225-1229. https://doi.org/10.1016/j.chemosphere.2009.12.060.
Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 29(9), Article e45.
Pfaffl, M. W., Tichopad, A., Prgomet, C., & Neuvians, T. P. (2004). Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations. Biotechnology Letters, 26(6), 509-515. https://doi.org/10.1023/b:bile.0000019559.84305.47.
Pinto, T. J. S., Moreira, R. A., Silva, L. C. M., da Yoshii, M. P. C., Goulart, B. V., Fraga, P. D., Montagner, C. C., Daam, M. A., & Espindola, E. L. G. (2021). Impact of 2,4-D and fipronil on the tropical midge Chironomus sancticaroli (Diptera: Chironomidae). Ecotoxicology and Environmental Safety, 209, Article 111778. https://doi.org/10.1016/j.ecoenv.2020.111778.
Pinto, T. J. S., Rocha, G. S., Moreira, R. A., Silva, L. C. M., da Yoshii, M. P. C., Goulart, B. V., Montagner, C. C., Daam, M. A., & Espindola, E. L. G. (2021). Multi-generational exposure to fipronil, 2,4-D, and their mixtures in Chironomus sancticaroli: Biochemical, individual, and population endpoints. Environmental Pollution, 283, Article 117384. https://doi.org/10.1016/j.envpol.2021.117384.
R: A language and environment for statistical computing (Version 3.6.0) [Computer software]. (2019). R Foundation for Statistical Computing.
Rao, M. A., Scelza, R., Acevedo, F., Diez, M. C., & Gianfreda, L. (2014). Enzymes as useful tools for environmental purposes. Chemosphere, 107, 145-162. https://doi.org/10.1016/j.chemosphere.2013.12.059.
Roat, T. C., Carvalho, S. M., Palma, M. S., & Malaspina, O. (2017). Biochemical response of the Africanized honeybee exposed to fipronil. Environmental Toxicology and Chemistry, 36(6), 1652-1660. https://doi.org/10.1002/etc.3699.
Sheehan, G., Garvey, A., Croke, M., & Kavanagh, K. (2018). Innate humoral immune defences in mammals and insects: The same, with differences? Virulence, 9(1), 1625-1639. https://doi.org/10.1080/21505594.2018.1526531.
Singh, N. S., Sharma, R., Singh, S. K., & Singh, D. K. (2021). A comprehensive review of environmental fate and degradation of fipronil and its toxic metabolites. Environmental Research, 199, Article 111316. https://doi.org/10.1016/j.envres.2021.111316.
Soin, T., & Smagghe, G. (2007). Endocrine disruption in aquatic insects: A review. Ecotoxicology, 16(1), 83-93. https://doi.org/10.1007/s10646-006-0118-9.
Soreq, H., & Seidman, S. (2001). Acetylcholinesterase-New roles for an old actor. Nature Reviews Neuroscience, 2(4), 294-302. https://doi.org/10.1038/35067589.
Stratman, K. N., Wilson, P. C., Overholt, W. A., Cuda, J. P., & Netherland, M. D. (2013). Toxicity of fipronil to the midge, Cricotopus lebetis Sublette. Journal of Toxicology and Environmental Health, Part A, 76(12), 716-722. https://doi.org/10.1080/15287394.2013.802266.
Thuyet, D. Q., Watanabe, H., & Ok, J. (2013). Effect of pH on the degradation of imidacloprid and fipronil in paddy water. Journal of Pesticide Science, 38, 223-227. https://doi.org/10.1584/jpestics.D12-080.
Truman, J. W. (2019). The evolution of insect metamorphosis. Current Biology, 29(23), R1252-R1268. https://doi.org/10.1016/j.cub.2019.10.009.
Tsakas, S., & Marmaras, V. J. (2010). Insect immunity and its signalling: An overview. Invertebrate Survival Journal, 7(2), 228-238.
Verheijen, M., Tong, W., Shi, L., Gant, T. W., Seligman, B., & Caiment, F. (2020). Towards the development of an omics data analysis framework. Regulatory Toxicology and Pharmacology, 112, Article 104621. https://doi.org/10.1016/j.yrtph.2020.104621.
Zaluski, R., Kadri, S. M., Alonso, D. P., Martins Ribolla, P. E., & de Oliveira Orsi, R. (2015). Fipronil promotes motor and behavioral changes in honey bees (Apis mellifera) and affects the development of colonies exposed to sublethal doses. Environmental Toxicology and Chemistry, 34(5), 1062-1069. https://doi.org/10.1002/etc.2889.
Zininga, T., Ramatsui, L., & Shonhai, A. (2018). Heat shock proteins as immunomodulants. Molecules, 23(11), Article 2846. https://doi.org/10.3390/molecules23112846.
معلومات مُعتمدة: PRINT/CAPES 88887.576780/2020-00 Coordenação de Aperfeiçoamento de Pessoal de Nível Superior; RTI2018-094598-B-100 Ministerio de Universidades; REGAGE21e00018296847 Universidad Nacional de Educación a Distancia
فهرسة مساهمة: Keywords: Aquatic toxicity; Chironomids; Insecticides; Molecular response; Pesticides; Real-time polymerase chain reaction (RT-PCR)
المشرفين على المادة: 0 (Insecticides)
QGH063955F (fipronil)
EC 3.1.1.7 (Acetylcholinesterase)
0 (Water Pollutants, Chemical)
0 (Pyrazoles)
تواريخ الأحداث: Date Created: 20231129 Date Completed: 20240125 Latest Revision: 20240125
رمز التحديث: 20240125
DOI: 10.1002/etc.5798
PMID: 38018734
قاعدة البيانات: MEDLINE
الوصف
تدمد:1552-8618
DOI:10.1002/etc.5798