The effects of iron oxide nanoparticles on antioxidant capacity and response to oxidative stress in Mozambique tilapia (Oreochromis mossambicus, Peters 1852)

Puthan Variyam Vidya Balakrishnan; Goran Gajski; Kumari Chidambaran Chitra

doi:10.2478/aiht-2024-75-3826

Abstract

Recent research has raised concern about the biocompatibility of iron oxide nanoparticles (IONPs), as they have been reported to induce oxidative stress and inflammatory responses, whilst prolonged exposure to high IONP concentrations may lead to cyto-/genotoxicity. Besides, there is concern about its environmental impact. The aim of our study was to investigate the effects of IONPs on the antioxidant defence system in freshwater fish Mozambique tilapia (Oreochromis mossambicus, Peters 1852). The fish were exposed to IONP concentration of 15 mg/L over 1, 3, 4, 15, 30, and 60 days and the findings compared to a control, unexposed group. In addition, we followed up the fish for 60 days after exposure had stopped to estimate the stability of oxidative stress induced by IONPs. Exposure affected the activity of antioxidant and marker enzymes and increased the levels of hydrogen peroxide and lipid peroxidation in the gill, liver, and brain tissues of the fish. Even after 60 days of depuration, adverse effects remained, indicating long-term nanotoxicity. Moreover, IONPs accumulated in the gill, liver, and brain tissues. Our findings underscore the potential health risks posed to non-target organisms in the environment, and it is imperative to establish appropriate guidelines for safe handling and disposal of IONPs to protect the aquatic environment.

References

Noqta OA, Aziz AA, Usman IA, Bououdina M. Recent advances in iron oxide nanoparticles (IONPs): synthesis and surface modification for biomedical applications. J Supercond Nov Magn 2019;32:779–95. doi: 10.1007/s10948-018-4939-6
Open DOI Search in Google Scholar Back to article
Jjagwe J, Olupot PW, Carrara S. Iron oxide nanoparticles/nanocomposites derived from steel and iron wastes for water treatment: A review. J Environ Manage 2023;343:118236. doi: 10.1016/J.JENVMAN.2023.118236
Open DOI Search in Google Scholar Back to article
Baabu PRS, Kumar HK, Gumpu MB, Babu KJ, Kulandaisamy AJ, Rayappan JBB. Iron oxide nanoparticles: A Review on the province of its compounds, properties and biological applications. Materials (Basel) 2022;16(1):59. doi: 10.3390/ma16010059
Open DOI Search in Google Scholar Back to article
Patiño-Ruiz DA, Meramo-Hurtado SI, González-Delgado ÁD, Herrera A. Environmental sustainability evaluation of iron oxide nanoparticles synthesized via green synthesis and the coprecipitation method: A comparative life cycle assessment study. ACS Omega 2021;6:12410–23. doi: 10.1021/acsomega.0c05246
Open DOI Search in Google Scholar Back to article
Tai VC, Che HX, Kong XY, Ho KC, Ng WM. Decoding iron oxide nanoparticles from design and development to real world application in water remediation. J Ind Eng Chem 2023;127:82–100. doi: 10.1016/J.JIEC.2023.07.038
Open DOI Search in Google Scholar Back to article
Oberdörster G, Oberdörster E, Oberdörster J. Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect 2005;113:823–39. doi: 10.1289/ehp.7339
Open DOI Search in Google Scholar Back to article
Piccinno F, Gottschalk F, Seeger S, Nowack B. Industrial production quantities and uses of ten engineered nanomaterials in Europe and the world. J Nanoparticle Res 2012;14:1109. doi: 10.1007/s11051-012-1109-9
Open DOI Search in Google Scholar Back to article
Zhang C, Liu T, Gao J, Su Y, Shi C. Recent development and application of magnetic nanoparticles for cell labeling and imaging. Mini Rev Med Chem 2010;10:194–203. doi: 10.2174/138955710791185073
Open DOI Search in Google Scholar Back to article
Xuan L, Ju Z, Skonieczna M, Zhou P, Huang R. Nanoparticles-induced potential toxicity on human health: Applications, toxicity mechanisms, and evaluation models. MedComm 2023;4(4):e327. doi: 10.1002/mco2.327
Open DOI Search in Google Scholar Back to article
Tao Z, Zhou Q, Zheng T, Mo F, Ouyang S. Iron oxide nanoparticles in the soil environment: Adsorption, transformation, and environmental risk. J Hazard Mater 2023;459:132107. doi: 10.1016/J.JHAZMAT.2023.132107
Open DOI Search in Google Scholar Back to article
Caixeta MB, Araújo PS, Rodrigues CC, Gonçalves BB, Araújo OA, Bevilaqua GB, Malafaia G, Silva LD, Rocha TL. Risk assessment of iron oxide nanoparticles in an aquatic ecosystem: A case study on Biomphalaria glabrata. J Hazard Mater 2021;401:123398. doi: 10.1016/J.JHAZMAT.2020.123398
Open DOI Search in Google Scholar Back to article
Cotin G, Piant S, Mertz D, Felder-Flesch D, Begin-Colin S. Iron oxide nanoparticles for biomedical applications: synthesis, functionalization, and application. In: Mahmoudi M, Laurent S, editors. Iron oxide nanoparticles biomedical application. Chapter 2. Amsterdam: Elsevier; 2018. p. 43–88. doi: 10.1016/B978-0-08-101925-2.00002-4
Open DOI Search in Google Scholar Back to article
Mahmoudi M, Laurent S. Iron Oxide Nanoparticles for Biomedical Applications : Synthesis, Functionalization and Application. 1^st ed. Imprint: Elsevier; 2017.
Search in Google Scholar Back to article
Cedervall T, Hansson L-A, Lard M, Frohm B, Linse S. Food chain transport of nanoparticles affects behaviour and fat metabolism in fish. PLoS One 2012;7:e32254. doi: 10.1371/journal.pone.0032254
Open DOI Search in Google Scholar Back to article
Maharramov AM, Hasanova UA, Suleymanova IA, Osmanova GE, Hajiyeva NE. The engineered nanoparticles in food chain: potential toxicity and effects. SN Appl Sci 2019;1:1362. doi: 10.1007/s42452-019-1412-5
Open DOI Search in Google Scholar Back to article
Forest V. Combined effects of nanoparticles and other environmental contaminants on human health - an issue often overlooked. NanoImpact 2021;23:100344. doi: 10.1016/J.IMPACT.2021.100344
Open DOI Search in Google Scholar Back to article
Li M, Liu W, Slaveykova VI. Effects of mixtures of engineered nanoparticles and metallic pollutants on aquatic organisms. Environments 2020;7(4):27. doi: 10.3390/environments7040027
Open DOI Search in Google Scholar Back to article
Zhang F, Wang Z, Peijnenburg WJGM, Vijver MG. Review and prospects on the ecotoxicity of mixtures of nanoparticles and hybrid nanomaterials. Environ Sci Technol 2022;56:15238–50. doi: 10.1021/acs.est.2c03333
Open DOI Search in Google Scholar Back to article
Remya AS, Ramesh M, Saravanan M, Poopal RK, Bharathi S, Nataraj D. Iron oxide nanoparticles to an Indian major carp, Labeo rohita: Impacts on hematology, iono regulation and gill Na⁺/K⁺ ATPase activity. J King Saud Univ - Sci 2015;27:151–60. doi: 10.1016/J.JKSUS.2014.11.002
Open DOI Search in Google Scholar Back to article
Li H, Zhou Q, Wu Y, Fu J, Wang T, Jiang G. Effects of waterborne nano-iron on medaka (Oryzias latipes): Antioxidant enzymatic activity, lipid peroxidation and histopathology. Ecotoxicol Environ Saf 2009;72:684–92. doi: 10.1016/J.ECOENV.2008.09.027
Open DOI Search in Google Scholar Back to article
Villacis RAR, Filho JS, Piña B, Azevedo RB, Pic-Taylor A, Mazzeu JF, Grisolia CK. Integrated assessment of toxic effects of maghemite (γ-Fe₂O₃) nanoparticles in zebrafish. Aquat Toxicol 2017;191:219–25. doi: 10.1016/J.AQUATOX.2017.08.004
Open DOI Search in Google Scholar Back to article
Ucar A, Parlak V, Ozgeris FB, Yeltekin AC, Arslan ME, Alak G, Turkez H, Kocaman EM, Atamanalp M. Magnetic nanoparticles-induced neurotoxicity and oxidative stress in brain of rainbow trout: Mitigation by ulexite through modulation of antioxidant, anti-inflammatory, and antiapoptotic activities. Sci Total Environ 2022;838:155718. doi: 10.1016/J.SCITOTENV.2022.155718
Open DOI Search in Google Scholar Back to article
Committee for the Purpose of Control and Supervision of Experiments on Animals (CPCSEA). Guidelines of CPCSEA for Experimentation on Fishes [displayed 20 May 2024]. Available at https://ccsea.gov.in/WriteReadData/userfiles/file/Guidelines%20of%20CPCSEA%20for%20Experimentation%20on%20Fishes-2021.pdf
Search in Google Scholar Back to article
Rice EW, Baird RB, Eaton AD, editors. Standard Methods for the Examination of Water and Wastewater. 23^rd ed. Washington (DC): American Public Health Association; 2017.
Search in Google Scholar Back to article
Organisation for Economic Co-operation and Development (OECD). Test No. 122: Determination of pH, Acidity and Alkalinity. Paris: OECD; 2013. doi: 10.1787/9789264203686-en
Open DOI Search in Google Scholar Back to article
Vidya PV, Chitra KC. Irreversible histopathological modifications induced by iron oxide nanoparticles in the fish, Oreochromis mossambicus (Peters, 1852). Biol Forum-An Int J 2019;11:1–6.
Search in Google Scholar Back to article
Vidya PV, Chitra KC. Evaluation of genetic damage in Oreochromis mossambicus exposed to selected nanoparticles by using micronucleus and comet bioassays. Croat J Fish 2018;76:115–24. doi: 10.2478/cjf-2018-0015
Open DOI Search in Google Scholar Back to article
Arslan Z, Ates M, McDuffy W, Agachan MS, Farah IO, Yu WW, Bednar AJ. Probing metabolic stability of CdSe nanoparticles: Alkaline extraction of free cadmium from liver and kidney samples of rats exposed to CdSe nanoparticles. J Hazard Mater 2011;192:192–9. doi: 10.1016/J.JHAZMAT.2011.05.003
Open DOI Search in Google Scholar Back to article
Lowry O, Rosebrough N, Farr AL, Randall R. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265–75. doi: 10.1016/S0021-9258(19)52451-6
Open DOI Search in Google Scholar Back to article
Marklund S, Marklund G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 1974;47:469–74. doi: 10.1111/j.1432-1033.1974.tb03714.x
Open DOI Search in Google Scholar Back to article
Claiborne A. Catalase activity. In: Greenwald RA, editors. CRC Handbook of methods for oxygen radical research. Boca Raton (FL): CRC Press; 1985. p. 283–4.
Search in Google Scholar Back to article
Carlberg I, Mannervik B. Purification and characterization of the flavoenzyme glutathione reductase from rat liver. J Biol Chem 1975;250:5475–80. doi: 10.1016/S0021-9258(19)41206-4
Open DOI Search in Google Scholar Back to article
Mohandas J, Marshall JJ, Duggin GG, Horvath JS, Tiller DJ. Low activities of glutathione-related enzymes as factors in the genesis of urinary bladder cancer1. Cancer Res 1984;44:5086–91. PMID: 6149017
Search in Google Scholar Back to article
Pick E, Keisari Y. Superoxide anion and hydrogen peroxide production by chemically elicited peritoneal macrophages–induction by multiple nonphagocytic stimuli. Cell Immunol 1981;59:301–18. doi: 10.1016/0008-8749(81)90411-1
Open DOI Search in Google Scholar Back to article
Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979;95:351–8. doi: 10.1016/0003-2697(79)90738-3
Open DOI Search in Google Scholar Back to article
Bessey OA, Lowry OH, Brock MJ. A method for the rapid determination of alkaline phosphatase with five cubic millimeters of serum. J Biol Chem 1946;164:321–9. doi: 10.1016/S0021-9258(18)43072-4
Open DOI Search in Google Scholar Back to article
Ellman GL, Courtney KD, Andres V, Featherstone RM. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 1961;7:88–95. doi: 10.1016/0006-2952(61)90145-9
Open DOI Search in Google Scholar Back to article
Ates M, Demir V, Adiguzel R, Arslan Z. Bioaccumulation, subacute toxicity, and tissue distribution of engineered titanium dioxide (TiO₂) nanoparticles in goldfish (Carassius auratus). J Nanomater 2013;2013:460518. doi: 10.1155/2013/460518
Open DOI Search in Google Scholar Back to article
Kalman J, Connolly M, Abdolahpur-Monikh F, Fernández-Saavedra R, Cardona-García AI, Conde-Vilda E, Martínez-Morcillo S, Peijnenburg WJGM, Rucandio I, Fernández-Cruz ML. Bioaccumulation of CuO nanomaterials in rainbow trout: Influence of exposure route and particle shape. Chemosphere 2023;310:136894. doi: 10.1016/J.CHEMOSPHERE.2022.136894
Open DOI Search in Google Scholar Back to article
Ates M, Demir V, Arslan Z, Kaya H, Yılmaz S, Camas M. Chronic exposure of tilapia (Oreochromis niloticus) to iron oxide nanoparticles: Effects of particle morphology on accumulation, elimination, hematology and immune responses. Aquat Toxicol 2016;177:22–32. doi: 10.1016/J.AQUATOX.2016.05.005
Open DOI Search in Google Scholar Back to article
Murali M, Suganthi P, Athif P, Sadiq Bukhari A, Syed Mohamed HE, Basu H, Singhal RK. Histological alterations in the hepatic tissues of Al₂O₃ nanoparticles exposed freshwater fish Oreochromis mossambicus. J Trace Elem Med Biol 2017;44:125–31. doi: 10.1016/J.JTEMB.2017.07.001
Open DOI Search in Google Scholar Back to article
Martínez-Álvarez RM, Morales AE, Sanz A. Antioxidant defenses in fish: biotic and abiotic factors. Rev Fish Biol Fish 2005;15:75–88. doi: 10.1007/s11160-005-7846-4
Open DOI Search in Google Scholar Back to article
Sumi N, Chitra K. Effects of fullerene (C₆₀) on antioxidant enzyme activities and lipid peroxidation in gill of the cichlid fish, Pseudetroplus maculatus (Bloch, 1795). J Zool Stud 2016;3:31–7.
Search in Google Scholar Back to article
Sumi N, Chitra K. Acute exposure to fullerene (C₆₀) altered antioxidant defence system in hepatocytes of the cichlid fish, Pseudetroplus maculatus. Int J Res 2017;4:953–62.
Search in Google Scholar Back to article
Mahmoudi M, Shokrgozar MA, Sardari S, Moghadam MK, Vali H, Laurent S, Stroeve P. Irreversible changes in protein conformation due to interaction with superparamagnetic iron oxide nanoparticles. Nanoscale 2011;3:1127–38. doi: 10.1039/c0nr00733a
Open DOI Search in Google Scholar Back to article
Déciga-Alcaraz A, Delgado-Buenrostro NL, Ispanixtlahuatl-Meráz O, Freyre-Fonseca V, Flores-Flores JO, Ganem-Rondero A, Vaca-Paniagua F, Pilar Ramos-Godinez M del, Morales-Barcenas R, Sánchez-Pérez Y, García-Cuéllar CM, Chirino YI. Irreversible disruption of the cytoskeleton as induced by non-cytotoxic exposure to titanium dioxide nanoparticles in lung epithelial cells. Chem Biol Interact 2020;323:109063. doi: 10.1016/J.CBI.2020.109063
Open DOI Search in Google Scholar Back to article
Lochbaum CA, Chew AK, Zhang X, Rotello V, Van Lehn RC, Pedersen JA. Lipophilicity of cationic ligands promotes irreversible adsorption of nanoparticles to lipid bilayers. ACS Nano 2021;15:6562–72. doi: 10.1021/acsnano.0c09732
Open DOI Search in Google Scholar Back to article
Federici G, Shaw BJ, Handy RD. Toxicity of titanium dioxide nanoparticles to rainbow trout (Oncorhynchus mykiss): gill injury, oxidative stress, and other physiological effects. Aquat Toxicol 2007;84:415–30. doi: 10.1016/J.AQUATOX.2007.07.009
Open DOI Search in Google Scholar Back to article
Afifi M, Saddick S, Abu Zinada OA. Toxicity of silver nanoparticles on the brain of Oreochromis niloticus and Tilapia zillii. Saudi J Biol Sci 2016;23:754–60. doi: 10.1016/J.SJBS.2016.06.008
Open DOI Search in Google Scholar Back to article
Vidya PV, Chitra KC. Elevation of reactive oxygen species in hepatocytes of tilapian fish when exposed to silicon dioxide: a potential environmental impact of nanomaterial. Int J Recent Sci Res 2015;6:2990–5.
Search in Google Scholar Back to article
Green MR, Sambrook J. Alkaline phosphatase. Cold Spring Harb Protoc 2020;2020:pdb.top100768. doi: 10.1101/pdb.top100768
Open DOI Search in Google Scholar Back to article
Temiz Ö, Kargın F. Toxicological impacts on antioxidant responses, stress protein, and genotoxicity parameters of aluminum oxide nanoparticles in the liver of Oreochromis niloticus. Biol Trace Elem Res 2022;200:1339–46. doi: 10.1007/s12011-021-02723-0
Open DOI Search in Google Scholar Back to article
Khan GB, Akhtar N, Khan MF, Ullah Z, Tabassum S, Tedesse Z. Toxicological impact of Zinc Nano Particles on tilapia fish (Oreochromis mossambicus). Saudi J Biol Sci 2022;29:1221–6. doi: 10.1016/J.SJBS.2021.09.044
Open DOI Search in Google Scholar Back to article
Wei X, Jiang W, Yu J, Ding L, Hu J, Jiang G. Effects of SiO₂ nanoparticles on phospholipid membrane integrity and fluidity. J Hazard Mater 2015;287:217–24. doi: 10.1016/J.JHAZMAT.2015.01.063
Open DOI Search in Google Scholar Back to article
Zhao X, Wang S, Wu Y, You H, Lv L. Acute ZnO nanoparticles exposure induces developmental toxicity, oxidative stress and DNA damage in embryo-larval zebrafish. Aquat Toxicol 2013;136–137:49–59. doi: 10.1016/J.AQUATOX.2013.03.019
Open DOI Search in Google Scholar Back to article
Wolf-Grosse S, Mollnes TE, Ali S, Stenvik J, Nilsen AM. Iron oxide nanoparticles enhance Toll-like receptor-induced cytokines in a particle size- and actin-dependent manner in human blood. Nanomedicine 2018;13:1773–85. doi: 10.2217/nnm-2017-0362
Open DOI Search in Google Scholar Back to article
Wu X, Zhang Y, Mao H, Zhang M. Toxic effects of iron oxide nanoparticles on human umbilical vein endothelial cells. Int J Nanomedicine 2010;5:385–99. doi: 10.2147/IJN.S10458
Open DOI Search in Google Scholar Back to article
Palacios-Hernandez T, Diaz-Diestra DM, Nguyen AK, Skoog SA, Vijaya Chikkaveeraiah B, Tang X, Wu Y, Petrochenko PE, Sussman EM, Goering PL. Cytotoxicity, cellular uptake and apoptotic responses in human coronary artery endothelial cells exposed to ultrasmall superparamagnetic iron oxide nanoparticles. J Appl Toxicol 2020;40:918–30. doi: 10.1002/jat.3953
Open DOI Search in Google Scholar Back to article
Costa C, Brandão F, Bessa MJ, Costa S, Valdiglesias V, Kiliç G, Fernández-Bertólez N, Quaresma P, Pereira E, Pásaro E, Laffon B, Teixeira JP. In vitro cytotoxicity of superparamagnetic iron oxide nanoparticles on neuronal and glial cells. Evaluation of nanoparticle interference with viability tests. J Appl Toxicol 2016;36:361–72. doi: 10.1002/jat.3213
Open DOI Search in Google Scholar Back to article
Dwivedi S, Siddiqui MA, Farshori NN, Ahamed M, Musarrat J, Al-Khedhairy AA. Synthesis, characterization and toxicological evaluation of iron oxide nanoparticles in human lung alveolar epithelial cells. Colloids Surfaces B Biointerfaces 2014;122:209–15. doi: 10.1016/J.COLSURFB.2014.06.064
Open DOI Search in Google Scholar Back to article
Couto D, Freitas M, Vilas-Boas V, Dias I, Porto G, Lopez-Quintela MA, Rivas J, Freitas P, Carvalho F, Fernandes E. Interaction of polyacrylic acid coated and non-coated iron oxide nanoparticles with human neutrophils. Toxicol Lett 2014;225:57–65. doi: 10.1016/J.TOXLET.2013.11.020
Open DOI Search in Google Scholar Back to article
Fernández-Bertólez N, Costa C, Brandão F, Kiliç G, Duarte JA, Teixeira JP, Pásaro E, Valdiglesias V, Laffon B. Toxicological assessment of silica-coated iron oxide nanoparticles in human astrocytes. Food Chem Toxicol 2018;118:13–23. doi: 10.1016/J.FCT.2018.04.058
Open DOI Search in Google Scholar Back to article

The effects of iron oxide nanoparticles on antioxidant capacity and response to oxidative stress in Mozambique tilapia (Oreochromis mossambicus, Peters 1852)

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