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Journal of Nanoparticle Research

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01-04-2020 | Research paper

Developmental toxicity of iron oxide nanoparticles with different coatings in zebrafish larvae

Authors: E. M. N. Oliveira, G. I. Selli, A. von Schmude, C. Miguel, S. Laurent, M. R. M. Vianna, R. M. Papaléo

Published in: Journal of Nanoparticle Research | Issue 4/2020

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Abstract

We report on the effect of different coatings (dextran, chitosan, polyethylene glycol, carboxy-silane, and silica) in the toxicity elicited by superparamagnetic iron oxide nanoparticles (SPIONs) in the developing zebrafish (Danio rerio). Animals were exposed to nanoparticle concentrations ranging from 0.125 to 8.0 mM of Fe during the first 5 days after fertilization. Embryotoxicity parameters (survival, hatching rate, and the incidence of anatomical malformations) and behavioral patterns (locomotion during the exploration of a new environment, thigmotaxis, and the escape response to an aversive stimulus) were evaluated. Exposed embryos hatched between 48 and 72 hpf, as expected for the species, but tendencies of either acceleration or delay were observed, depending on the nanoparticle coating. Malformations in exposed and control groups were similar, independent of the coating. Mortality rates were also not significantly affected by exposure to most of the coated SPIONs, except for animals treated with chitosan-coated nanoparticles, which induced 100% mortality at concentrations higher than 2 mM. A similar trend was observed in the behavioral parameters, in which significant adverse effects were mostly caused by chitosan-coated nanoparticles even at low concentrations. The higher toxicity observed for chitosan-coated particles raises concern and deserves further mechanistic investigations, considering the ample use of this compound in pharmaceutical and biomedical applications.

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Ahmad F et al (2015) An in vivo evaluation of acute toxicity of cobalt ferrite (CoFe2O4) nanoparticles in larval-embryo Zebrafish (Danio rerio). Aquat Toxicol 166(July):21–28. https://doi.org/10.1016/j.aquatox.2015.07.003 CrossRef

Asharani PV et al (2011) Comparison of the toxicity of silver, gold and platinum nanoparticles in developing zebrafish embryos. Nanotoxicology 5(1):43–54. https://doi.org/10.3109/17435390.2010.489207 CrossRef

Bañobre-López M, Teijeiro A, Rivas J (2013) Magnetic nanoparticle-based hyperthermia for cancer treatment. Rep Pract Oncol Radiother 18(6):397–400. https://doi.org/10.1016/j.rpor.2013.09.011 CrossRef

Bellich B et al (2016) ‘“The good, the bad and the ugly” of Chitosans’. Marine Drugs 14(5):99. https://doi.org/10.3390/md14050099

Berry CC, Wells S, Charles S, Aitchison G, Curtis AS (2004) Cell response to dextran-derivatised iron oxide nanoparticles post internalisation. Biomaterials 25(23):5405–5413. https://doi.org/10.1016/j.biomaterials.2003.12.046 CrossRef

Biyani N et al (2014) In vitro toxicity assessment of chitosan oligosaccharide coated iron oxide nanoparticles. Toxicol Rep 2:27–39. https://doi.org/10.1016/j.toxrep.2014.11.002 CrossRef

Boutry S et al (2009) How to quantify iron in an aqueous or biological matrix: a technical note. Contrast Media Mol Imaging 4(6):299–304. https://doi.org/10.1002/cmmi.291 CrossRef

Bridot JL, Stanicki D, Laurent S, Boutry S, Gossuin Y, Leclère P, Lazzaroni R, Vander Elst L, Muller RN (2013) New carboxysilane-coated iron oxide nanoparticles for nonspecific cell labelling. Contrast Media Mol Imaging 8(6):466–474. https://doi.org/10.1002/cmmi.1552 CrossRef

Cai W, Chen X (2007) Nanoplatforms for targeted molecular imaging in living subjects. Small 3(11):1840–1854. https://doi.org/10.1002/smll.200700351 CrossRef

Cambier S, Røgeberg M, Georgantzopoulou A, Serchi T, Karlsson C, Verhaegen S, Iversen TG, Guignard C, Kruszewski M, Hoffmann L, Audinot JN, Ropstad E, Gutleb AC (2018) Fate and effects of silver nanoparticles on early life-stage development of zebrafish (Danio rerio) in comparison to silver nitrate. Sci Total Environ 610–611:972–982. https://doi.org/10.1016/j.scitotenv.2017.08.115 CrossRef

Caro C, Egea-Benavente D, Polvillo R, Royo JL, Pernia Leal M, García-Martín ML (2019) Comprehensive toxicity assessment of PEGylated magnetic nanoparticles for in vivo applications. Colloids Surf B: Biointerfaces 177:253–259. https://doi.org/10.1016/j.colsurfb.2019.01.051 CrossRef

Chen TH, Lin CC, Meng PJ (2014) Zinc oxide nanoparticles alter hatching and larval locomotor activity in zebrafish (Danio rerio). J Hazard Mater 277:134–140. https://doi.org/10.1016/j.jhazmat.2013.12.030 CrossRef

Clemente Z, Castro VL, Moura MA, Jonsson CM, Fraceto LF (2014) Toxicity assessment of TiO2 nanoparticles in zebrafish embryos under different exposure conditions. Aquat Toxicol 147:129–139. https://doi.org/10.1016/j.aquatox.2013.12.024 CrossRef

Colwill RM, Creton R (2011) Imaging escape and avoidance behavior in zebrafish larvae. Rev Neurosci 22(1):63–73. https://doi.org/10.1515/RNS.2011.008 CrossRef

Concea, C. N, De C. De E. A. (2008) Peixes mantidos em instalações de instituições de ensino ou pesquisa científica para fins de estudo biológico ou biomédico I, Guia Brasileiro de Produção, Manutenção ou Utilização de Animais para Atividades de Ensino ou Pesquisa Científica. Available at: https://www.mctic.gov.br/mctic/opencms/institucional/concea/paginas/guia.html. Accessed 15 August 2019

Cornell RM, Schwertmann U (2003) The iron oxides. Wiley. https://doi.org/10.1002/3527602097

Creton R (2012) A novel high-throughput imaging system for automated analyses of avoidance behavior in zebrafish larvae. Behav Brain Res 223(1):135–144. https://doi.org/10.1016/j.bbr.2011.04.033

de Oliveira GMT et al (2017) Implications of exposure to dextran-coated and uncoated iron oxide nanoparticles to developmental toxicity in zebrafish. J Nanopart Res 19(12):1–16. https://doi.org/10.1007/s11051-017-4074-5 CrossRef

De Oliveira GMT et al (2014) Transient modulation of acetylcholinesterase activity caused by exposure to dextran-coated iron oxide nanoparticles in brain of adult zebrafish. Comp Biochem Physiol Part - C: Toxicol Pharmacol 162(1):77–84. https://doi.org/10.1016/j.cbpc.2014.03.010 CrossRef

Duan J, Yu Y, Shi H, Tian L, Guo C, Huang P, Zhou X, Peng S, Sun Z (2013) Toxic effects of silica nanoparticles on zebrafish embryos and larvae. PLoS One 8(9):4–12. https://doi.org/10.1371/journal.pone.0074606 CrossRef

Fifi AP et al (2016) Oxytetracycline delivery in adult female zebrafish by iron oxide nanoparticles. Zebrafish 13(6):495–503. https://doi.org/10.1089/zeb.2016.1302 CrossRef

Forge D et al (2008) Optimization of the synthesis of superparamagnetic contrast agents by the design of experiments method. J Phys Chem C 112(49):19178–19185. https://doi.org/10.1021/jp803832k CrossRef

Geiss KT et al (2005) In vitro toxicity of nanoparticles in BRL 3A rat liver cells. Toxicol in Vitro 19(7):975–983. https://doi.org/10.1016/j.tiv.2005.06.034 CrossRef

George S, Xia T, Rallo R, Zhao Y, Ji Z, Lin S, Wang X, Zhang H, France B, Schoenfeld D, Damoiseaux R, Liu R, Lin S, Bradley KA, Cohen Y, Nel AE (2011) Use of a high-throughput screening approach coupled with in vivo zebrafish embryo screening to develop hazard ranking for engineered nanomaterials. ACS Nano 5(3):1805–1817. https://doi.org/10.1021/nn102734s CrossRef

Hill AJ et al (2005) Zebrafish as a model vertebrate for investigating chemical toxicity. Toxicol Sci 86(1):6–19. https://doi.org/10.1093/toxsci/kfi110 CrossRef

Hu Y et al (2011) Toxicity evaluation of biodegradable chitosan nanoparticles using a zebrafish embryo model. Int J Nanomed (6):3351–3359. https://doi.org/10.2147/IJN.S25853

Hu Q et al (2017) ‘Effects of titanium dioxide nanoparticles exposure on parkinsonism in zebrafish larvae and PC12. Chemosphere. Elsevier Ltd 173:373–379. https://doi.org/10.1016/j.chemosphere.2017.01.063

Josephson L et al (2002) Near-infrared fluorescent nanoparticles as combined MR/optical imaging probes. Bioconjug Chem 13:554–560. https://doi.org/10.1021/bc015555d

Kari G, Rodeck U, Dicker AP (2007) Zebrafish: an emerging model system for human disease and drug discovery. Clin Pharmacol Ther 82(1):70–80. https://doi.org/10.1038/sj.clpt.6100223 CrossRef

Karunaratne DP et al (2017) Developmental toxicity of glycine-coated silica nanoparticles in embryonic zebrafish. Environ Pollut 229:439–447. https://doi.org/10.1016/j.envpol.2017.06.016 CrossRef

Kong B, Seog JH, Graham LM, Lee SB (2011) Experimental considerations on the cytotoxicity of nanoparticles. Nanomedicine 6(5):929–941. https://doi.org/10.2217/nnm.11.77 CrossRef

Koo OM, Rubinstein I, Onyuksel H (2005) Role of nanotechnology in targeted drug delivery and imaging: a concise review. Nanomedicine 1(3):193–212. https://doi.org/10.1016/j.nano.2005.06.004 CrossRef

Kovrižnych JA, Sotníková R, Zeljenková D, Rollerová E, Szabová E, Wimmerová S (2013) Acute toxicity of 31 different nanoparticles to zebrafish (Danio rerio) tested in adulthood and in early life stages - comparative study. Interdiscip Toxicol 6(2):67–73. https://doi.org/10.2478/intox-2013-0012 CrossRef

Lacave JM et al (2016) Effects of metal-bearing nanoparticles (Ag, Au, CdS, ZnO, SiO2) on developing zebrafish embryos. Nanotechnology 27(32):1–15. https://doi.org/10.1088/0957-4484/27/32/325102 CrossRef

Laurent S, Forge D, Port M, Roch A, Robic C, Vander Elst L, Muller RN (2008) Magnetic iron oxide nanoparticles: synthesis, stabilization, vectorization, physicochemical characterizations and biological applications. Chem Rev 108(6):2064–2110. https://doi.org/10.1021/cr068445e CrossRef

Lee N, Yoo D, Ling D, Cho MH, Hyeon T, Cheon J (2015) Iron oxide based nanoparticles for multimodal imaging and magnetoresponsive therapy. Chem Rev 115(19):10637–10689. https://doi.org/10.1021/acs.chemrev.5b00112 CrossRef

Lieschke GJ, Currie PD (2007) Animal models of human disease: zebrafish swim into view. Nat Rev Genet 8(5):353–367. https://doi.org/10.1038/nrg2091 CrossRef

Lin S, Zhao Y, Nel AE, Lin S (2013) Zebrafish: an in vivo model for Nano EHS studies. Small 9(9–10):1608–1618. https://doi.org/10.1002/smll.201202115 CrossRef

Liskova A et al (2017) Immunotoxicity, genotoxicity and epigenetic toxicity of nanomaterials: new strategies for toxicity testing? Food Chem Toxicol 109:797–811. https://doi.org/10.1016/j.fct.2017.08.030 CrossRef

Liu H, Wang X, Wu Y, Hou J, Zhang S, Zhou N, Wang X (2019a) Toxicity responses of different organs of zebrafish (Danio rerio) to silver nanoparticles with different particle sizes and surface coatings. Environ Pollut 246:414–422. https://doi.org/10.1016/j.envpol.2018.12.034 CrossRef

Liu R et al (2012) Automated phenotype recognition for zebrafish embryo based in vivo high throughput toxicity screening of engineered nano-materials. PLoS One 7(4):e35014. https://doi.org/10.1371/journal.pone.0035014 CrossRef

Liu X, Peng M, Li G, Miao Y, Luo H, Jing G, He Y, Zhang C, Zhang F, Fan H (2019b) Ultrasonication-triggered ubiquitous assembly of magnetic janus amphiphilic nanoparticles in cancer theranostic applications. Nano Lett 19(6):4118–4125. https://doi.org/10.1021/acs.nanolett.9b01524 CrossRef

Liu X, Peng M, Li G, Miao Y, Luo H, Jing G, He Y (2019c) ‘Ultrasonication-triggered ubiquitous assembly of magnetic janus amphiphilic nanoparticles in cancer theranostic applications. Nano Lett Am Chem Soc 19:4118–4125. https://doi.org/10.1021/acs.nanolett.9b01524 CrossRef

Magro M, de Liguoro M, Franzago E, Baratella D, Vianello F (2018) The surface reactivity of iron oxide nanoparticles as a potential hazard for aquatic environments: a study on Daphnia magna adults and embryos. Sci Rep 8(1):1–15. https://doi.org/10.1038/s41598-018-31483-6 CrossRef

Mahmoudi M, Sant S, Wang B, Laurent S, Sen T (2011) Superparamagnetic iron oxide nanoparticles (SPIONs): development, surface modification and applications in chemotherapy. Adv Drug Deliv Rev 63(1–2):24–46. https://doi.org/10.1016/j.addr.2010.05.006 CrossRef

Mohammadi-Samani S et al (2013) Preparation and assessment of chitosan-coated superparamagnetic Fe3O4 nanoparticles for controlled delivery of methotrexate. Res Pharm Sci 8(1):25–33

Montet X, Weissleder R, Josephson L (2006) Imaging pancreatic cancer with a peptide-nanoparticle conjugate targeted to normal pancreas. Bioconjug Chem 17(4):905–911. https://doi.org/10.1021/bc060035+ CrossRef

Nery LR et al (2014) ‘Brain intraventricular injection of amyloid-β in zebrafish embryo impairs cognition and increases tau phosphorylation, effects reversed by lithium. PLoS One 9(9):e105862. https://doi.org/10.1371/journal.pone.0105862 CrossRef

Oliveira E et al (2018) Synthesis and nuclear magnetic relaxation properties of composite iron oxide nanoparticles. Química Nova 42(1):57–64. https://doi.org/10.21577/0100-4042.20170309

Osborne OJ, Johnston BD, Moger J, Balousha M, Lead JR, Kudoh T, Tyler CR (2013) Effects of particle size and coating on nanoscale Ag and TiO 2 exposure in zebrafish (Danio rerio) embryos. Nanotoxicology 7(8):1315–1324. https://doi.org/10.3109/17435390.2012.737484 CrossRef

Powers CM et al (2010) Silver exposure in developing zebrafish (Danio rerio): persistent effects on larval behavior and survival. Neurotoxicol Teratol 32(3):391–397. https://doi.org/10.1016/j.ntt.2010.01.009 CrossRef

Powers CM, Slotkin TA, Seidler FJ, Badireddy AR, Padilla S (2011) Silver nanoparticles alter zebrafish development and larval behavior: distinct roles for particle size, coating and composition. Neurotoxicol Teratol 33(6):708–714. https://doi.org/10.1016/j.ntt.2011.02.002 CrossRef

Ramos AP, Cruz MAE, Tovani CB, Ciancaglini P (2017) Biomedical applications of nanotechnology. Biophys Rev 9(2):79–89. https://doi.org/10.1007/s12551-016-0246-2 CrossRef

Reimer P et al (2007) SPIO-enhanced 2D-TOF MR angiography of the portal venous system: results of an intraindividual comparison. J Magn Reson Imaging 7(6):945–949. https://doi.org/10.1002/jmri.1880070602 CrossRef

Samaee SM, Rabbani S, Jovanović B, Mohajeri-Tehrani MR, Haghpanah V (2015) Efficacy of the hatching event in assessing the embryo toxicity of the nano-sized TiO2 particles in zebrafish: a comparison between two different classes of hatching-derived variables. Ecotoxicol Environ Saf 116:121–128. https://doi.org/10.1016/j.ecoenv.2015.03.012 CrossRef

Schnörr SJ, Steenbergen PJ, Richardson MK, Champagne DL (2012) Measuring thigmotaxis in larval zebrafish. Behav Brain Res 228(2):367–374. https://doi.org/10.1016/j.bbr.2011.12.016 CrossRef

Sharifi S, Seyednejad H, Laurent S, Atyabi F, Saei AA, Mahmoudi M (2015) Superparamagnetic iron oxide nanoparticles for in vivo molecular and cellular imaging. Contrast Media Mol Imaging 10(5):329–355. https://doi.org/10.1002/cmmi.1638 CrossRef

Shih YJ, Su CC, Chen CW, Dong CD, Liu WS, Huang CP (2016) Adsorption characteristics of nano-TiO2 onto zebrafish embryos and its impacts on egg hatching. Chemosphere 154:109–117. https://doi.org/10.1016/j.chemosphere.2016.03.061 CrossRef

Soenen SJH et al (2011) Cytotoxic effects of iron oxide nanoparticles and implications for safety in cell labelling. Biomaterials 32(1):195–205. https://doi.org/10.1016/j.biomaterials.2010.08.075 CrossRef

Som C, Wick P, Krug H, Nowack B (2011) Environmental and health effects of nanomaterials in nanotextiles and façade coatings. Environ Int 37(6):1131–1142. https://doi.org/10.1016/j.envint.2011.02.013 CrossRef

Stanicki D et al (2014) Carboxy-silane coated iron oxide nanoparticles: a convenient platform for cellular and small animal imaging. J Mater Chem B 2(4):387–397. https://doi.org/10.1039/c3tb21480j CrossRef

Sun Z et al (2013) Characterization of cellular uptake and toxicity of aminosilane-coated iron oxide nanoparticles with different charges in central nervous system-relevant cell culture models. Int J Nanomedicine 8:961–970. https://doi.org/10.2147/IJN.S39048

Stöber AF (1968) Facial feature extraction using improved deformable templates. J Colloid Interface Sci 26:62–69. https://doi.org/10.1109/ICOSP.2006.345929

van der Merwe D and Pickrell JA (2007) ‘Toxicity of nanomaterials’, in Veterinary Toxicology. Elsevier, pp 319–326. https://doi.org/10.1016/B978-0-12-370467-2.X5095-0

van Pomeren M et al (2019) The biodistribution and immuno-responses of differently shaped non-modified gold particles in zebrafish embryos. Nanotoxicology 13(4):558–571. https://doi.org/10.1080/17435390.2018.1564079 CrossRef

Vu AT et al (2004) First-pass contrast-enhanced magnetic resonance angiography in humans using ferumoxytol, a novel ultrasmall superparamagnetic iron oxide (USPIO)-based blood pool agent. J Magn Reson Imaging 21(1):46–52. https://doi.org/10.1002/jmri.20235 CrossRef

Wang Y et al (2016) Characterization and toxicology evaluation of chitosan nanoparticles on the embryonic development of zebrafish, Danio rerio. Carbohydr Polym 141(1):204–210. https://doi.org/10.1016/j.carbpol.2016.01.012 CrossRef

Wang Y-XJ (2015) Current status of superparamagnetic iron oxide contrast agents for liver magnetic resonance imaging. World J Gastroenterol 21(47):13400. https://doi.org/10.3748/wjg.v21.i47.13400

Wehmas LC, Anders C, Chess J, Punnoose A, Pereira CB, Greenwood JA, Tanguay RL (2015) Comparative metal oxide nanoparticle toxicity using embryonic zebrafish. Toxicol Rep 2:702–715. https://doi.org/10.1016/j.toxrep.2015.03.015 CrossRef

Westerfield M (2000) The zebrafish book. A guide for the laboratory use of zebrafish (Danio rerio). Eugene: University of Oregon Press. Available at: http://zfin.org/zf_info/zfbook/zfbk.html. Accessed 20 August 2001

Wunderbaldinger P, Josephson L, Weissleder R (2002) Crosslinked iron oxides (CLIO): A new platform for the development of targeted MR contrast agents. Acad Radiol 9:304–306. https://doi.org/10.1016/S1076-6332(03)80210-6 CrossRef

Xu J, Zhang Q, Li X, Zhan S, Wang L, Chen D (2017) The effects of copper oxide nanoparticles on dorsoventral patterning, convergent extension, and neural and cardiac development of zebrafish. Aquat Toxicol 188:130–137. https://doi.org/10.1016/j.aquatox.2017.05.002 CrossRef

Xue JY et al (2013) An assessment of the impact of SiO 2 nanoparticles of different sizes on the rest/wake behavior and the developmental profile of zebrafish larvae. Small 9(18):3161–3168. https://doi.org/10.1002/smll.201300430 CrossRef

Xue W, Liu Y, Zhang N, Yao Y, Ma P, Wen H, Huang S, Luo Y, Fan H (2018) Effects of core size and PEG coating layer of iron oxide nanoparticles on the distribution and metabolism in mice. Int J Nanomedicine 13:5719–5731. https://doi.org/10.2147/IJN.S165451 CrossRef

Zhang H, Li L, Liu XL, Jiao J, Ng CT, Yi JB, Luo YE, Bay BH, Zhao LY, Peng ML, Gu N, Fan HM (2017) Ultrasmall ferrite nanoparticles synthesized via dynamic simultaneous thermal decomposition for high-performance and multifunctional T1 magnetic resonance imaging contrast agent. ACS Nano 11(4):3614–3631. https://doi.org/10.1021/acsnano.6b07684 CrossRef

Zhu X, Tian S, Cai Z (2012) Toxicity assessment of iron oxide nanoparticles in zebrafish (Danio rerio) early life stages. PLoS One 7(9):1–6. https://doi.org/10.1371/journal.pone.0046286 CrossRef

Title: Developmental toxicity of iron oxide nanoparticles with different coatings in zebrafish larvae
Authors: E. M. N. Oliveira
G. I. Selli
A. von Schmude
C. Miguel
S. Laurent
M. R. M. Vianna
R. M. Papaléo
Publication date: 01-04-2020
Publisher: Springer Netherlands
Published in: Journal of Nanoparticle Research / Issue 4/2020
Print ISSN: 1388-0764
Electronic ISSN: 1572-896X
DOI: https://doi.org/10.1007/s11051-020-04800-2

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