Abstract
Iron oxide nanoparticles (IONPS) have been widely investigated as a platform for a new class of multifunctional theranostic agents. They are considered biocompatible, and some formulations are already available in the market for clinical use. However, contradictory results regarding toxicity of IONPs raise a concern about the potential harm of these nanoparticles. Changes in the nanoparticle (NP) physicochemical properties or exposure media can significantly alter their behavior and, as a consequence, their toxic effects. Here, behavior and two-step RT-qPCR were employed to access the potential toxicological effects of dextran-coated IONPs (CLIO-NH2) and uncoated IONPs (UCIO) in zebrafish larvae. Animals were exposed for 7 days to NP solutions ranging from 0.1–100 μg/mL directly mixed to the system water. UCIO showed high decantation and instability in solution, altering zebrafish mortality but showing no alterations in behavior and molecular expression analysis. CLIO-NH2 exposure did not cause significant mortality or changes in hatching rate of zebrafish larvae; however, behavior and expression profiles of the group exposed to lower concentration (1 μg/mL) presented a tendency to decrease the locomotor activity and apoptotic pathway activation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdollah MR, Kalber T, Tolner B et al (2014) Prolonging the circulatory retention of SPIONs using dextran sulfate: in vivo tracking achieved by functionalisation with near-infrared dyes. Faraday Discuss 175:41-58. https://doi.org/10.1039/c4fd00114a
Ahamed M, Akhtar MJ, Khan MAM, Alhadlaq HA, Alshamsan A (2016) Cobalt iron oxide nanoparticles induce cytotoxicity and regulate the apoptotic genes through ROS in human liver cells (HepG2). Colloids Surfaces B Biointerfaces 148:665–673. https://doi.org/10.1016/j.colsurfb.2016.09.047
Akassoglou K, Probert L, Kontogeorgos G, Kollias G (1997) Astrocyte-specific but not neuron-specific transmembrane TNF triggers inflammation and degeneration in the central nervous system of transgenic mice. J Immunol 158(1):438–445
Arami H, Khandhar A, Liggitt D, Krishnan KM (2015) In vivo delivery, pharmacokinetics, biodistribution and toxicity of iron oxide nanoparticles. Chem Soc Rev 44(23):8576–8607. https://doi.org/10.1039/C5CS00541H
Armstrong L, Jordan N, Millar A (1996) Interleukin 10 (IL-10) regulation of tumour necrosis factor alpha (TNF-alpha) from human alveolar macrophages and peripheral blood monocytes. Thorax 51(2):143–149. https://doi.org/10.1136/THX.51.2.143
Ašmonaitė G, Boyer S, de Souza KB et al (2016) Behavioural toxicity assessment of silver ions and nanoparticles on zebrafish using a locomotion profiling approach. Aquat Toxicol 173:143–153. https://doi.org/10.1016/j.aquatox.2016.01.013
Barker AJ, Cage B, Russek S, Stoldt CR (2005) Ripening during magnetite nanoparticle synthesis: resulting interfacial defects and magnetic properties. J Appl Phys 98(6):63528. https://doi.org/10.1063/1.2058191
Bisht G, Rayamajhi S, Kc B et al (2016) Synthesis, characterization, and study of in vitro cytotoxicity of ZnO-Fe3O4 magnetic composite nanoparticles in human breast cancer cell line (MDA-MB-231) and mouse fibroblast (NIH 3T3). Nanoscale Res Lett 11(1):537. https://doi.org/10.1186/s11671-016-1734-9
Bobo D, Robinson KJ, Islam J, Thurecht KJ, Corrie SR (2016) Nanoparticle-based medicines: a review of FDA-approved materials and clinical trials to date. Pharm Res 33(10):2373–2387. https://doi.org/10.1007/s11095-016-1958-5
Bohnsack JP, Assemi S, Miller JD, Furgeson DY (2012) The primacy of physicochemical characterization of nanomaterials for reliable toxicity assessment: A review of the zebrafish nanotoxicology model. Methods Mol Biol 926:261–316. https://doi.org/10.1007/978-1-62703-2-1_19
Boraschi D, Costantino L, Italiani P (2012) Interaction of nanoparticles with immunocompetent cells: nanosafety considerations. Nanomedicine 7(1):121–131. https://doi.org/10.2217/nnm.11.169
Bustin SA, Benes V, Garson JA et al (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622. https://doi.org/10.1373/clinchem.2008.112797s
Capiotti KM, Menezes FP, Nazario LR, Pohlmann JB, de Oliveira GMT, Fazenda L, Bogo MR, Bonan CD, Da Silva RS (2011) Early exposure to caffeine affects gene expression of adenosine receptors, DARPP-32 and BDNF without affecting sensibility and morphology of developing zebrafish (Danio rerio). Neurotoxicol Teratol 33(6):680–685. https://doi.org/10.1016/j.ntt.2011.08.010
Chakraborty C, Sharma AR, Sharma G, Lee S-S (2016) Zebrafish: a complete animal model to enumerate the nanoparticle toxicity. J Nanobiotechnol 14(1):65. https://doi.org/10.1186/s12951-016-0217-6
Chen T-H, Lin C-Y, Tseng M-C (2011) Behavioral effects of titanium dioxide nanoparticles on larval zebrafish (Danio Rerio). Mar Pollut Bull 63(5-12):303–308. https://doi.org/10.1016/j.marpolbul.2011.04.017
Chen L, Miao Y, Chen L, Jin P, Zha Y, Chai Y, Zheng F, Zhang Y, Zhou W, Zhang J, Wen L, Wang M (2013) The role of elevated autophagy on the synaptic plasticity impairment caused by CdSe/ZnS quantum dots. Biomaterials 34(38):10172–10181. https://doi.org/10.1016/j.biomaterials.2013.09.048
Coccini T, Caloni F, Ramírez Cando LJ, De Simone U (2017) Cytotoxicity and proliferative capacity impairment induced on human brain cell cultures after short- and long-term exposure to magnetite nanoparticles. J Appl Toxicol 37(3):361–373. https://doi.org/10.1002/jat.3367
Colwill RM, Creton R (2011) Locomotor behaviors in zebrafish (Danio rerio) larvae. Behav Process 86(2):222–229. https://doi.org/10.1016/j.beproc.2010.12.003
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 (2016) In vitro cytotoxicity of superparamagnetic iron oxide nanoparticles on neuronal and glial cells. Evaluation of nanoparticle interference with viability tests. J Appl Toxicol 36(3):361–372. https://doi.org/10.1002/jat.3213
Couto D, Freitas M, Vilas-Boas V, Dias I, Porto G, Lopez-Quintela MA, Rivas J, Freitas P, Carvalho F, Fernandes E (2014) Interaction of polyacrylic acid coated and non-coated iron oxide nanoparticles with human neutrophils. Toxicol Lett 225(1):57–65. https://doi.org/10.1016/j.toxlet.2013.11.020
Dai Y-J, Jia Y-F, Chen N, Bian WP, Li QK, Ma YB, Chen YL, Pei DS (2014) Zebrafish as a model system to study toxicology. Environ Toxicol Chem 33(1):11–17. https://doi.org/10.1002/etc.2406
Dal Forno GO, Kist LW, de Azevedo MB, Fritsch RS, Pereira TCB, Britto RS, Guterres SS, Külkamp-Guerreiro IC, Bonan CD, Monserrat JM, Bogo MR (2013) Intraperitoneal exposure to nano/microparticles of fullerene (C60) increases acetylcholinesterase activity and lipid peroxidation in adult zebrafish (Danio rerio) brain. Biomed Res Int 2013:623789–623711. https://doi.org/10.1155/2013/623789
Dhakshinamoorthy V, Manickam V, Perumal E (2017) Neurobehavioural toxicity of iron oxide nanoparticles in mice. Neurotox Res 1(2):1–30. https://doi.org/10.1007/s12640-017-9721-1
Digigow RG, Dechézelles J-F, Dietsch H, Geissbühler I, Vanhecke D, Geers C, Hirt AM, Rothen-Rutishauser B, Petri-Fink A (2014) Preparation and characterization of functional silica hybrid magnetic nanoparticles. J Magn Magn Mater 362:72–79. https://doi.org/10.1016/j.jmmm.2014.03.026
Du S, Li J, Du C, Huang Z, Chen G, Yan W (2016) Overendocytosis of superparamagnetic iron oxide particles increases apoptosis and triggers autophagic cell death in human osteosarcoma cell under a spinning magnetic field. Oncotarget 8(6):9410–9424. 10.18632/oncotarget.14114
Dyawanapelly S, Jagtap DD, Dandekar P, Ghosh G, Jain R (2017) Assessing safety and protein interactions of surface-modified iron oxide nanoparticles for potential use in biomedical areas. Colloids Surfaces B Biointerfaces 154:408–420. https://doi.org/10.1016/j.colsurfb.2017.03.050
Fan C-Y, Cowden J, Simmons SO, Padilla S, Ramabhadran R (2010) Gene expression changes in developing zebrafish as potential markers for rapid developmental neurotoxicity screening. Neurotoxicol Teratol 32(1):91–98. https://doi.org/10.1016/j.ntt.2009.04.065
Gajewicz A, Rasulev B, Dinadayalane TC, Urbaszek P, Puzyn T, Leszczynska D, Leszczynski J (2012) Advancing risk assessment of engineered nanomaterials: application of computational approaches. Adv Drug Deliv Rev 64(15):1663–1693. https://doi.org/10.1016/j.addr.2012.05.014
Gatoo MA, Naseem S, Arfat MY, Mahmood Dar A, Qasim K, Zubair S (2014) Physicochemical properties of nanomaterials: implication in associated toxic manifestations. Biomed Res Int 2014(8):498420. https://doi.org/10.1155/2014/498420
Grosse S, Stenvik J, Nilsen AM (2016) Iron oxide nanoparticles modulate lipopolysaccharide-induced inflammatory responses in primary human monocytes. Int J Nanomedicine 11:4625–4642. https://doi.org/10.2147/IJN.S113425
Guo S (2004) Linking genes to brain, behavior and neurological diseases: what can we learn from zebrafish? Genes Brain Behav 3(2):63–74. https://doi.org/10.1046/j.1601-183X.2003.00053.x
Gupta S, Gollapudi S (2005) Molecular mechanisms of TNF-α-induced apoptosis in aging human T cell subsets. Int J Biochem Cell Biol 37(5):1034–1042. https://doi.org/10.1016/j.biocel.2004.08.013
Haddad PS, Santos MC, de Guzzi Cassago CA, Bernardes JS, de Jesus MB, Seabra AB (2016) Synthesis, characterization, and cytotoxicity of glutathione-PEG-iron oxide magnetic nanoparticles. J Nanopart Res 18(12):369. https://doi.org/10.1007/s11051-016-3680-y
Isfort P, Witte H, Slabu I, Penzkofer T, Baumann M, Braunschweig T, Kennes LN, Kuhl CK, Schmitz-Rode T, Mahnken AH, Bruners P (2014) Efficacy of magnetic Thermoablation using SPIO in the treatment of osteoid osteoma in a bovine model compared to radiofrequency and microwave ablation. Cardiovasc Intervent Radiol 37(4):1053–1061. https://doi.org/10.1007/s00270-013-0832-7
Jiménez-Villarreal J, Rivas-Armendáriz DI, Arellano Pérez-Vertti RD, Olivas Calderón E, García-Garza R, Betancourt-Martínez ND, Serrano-Gallardo LB, Morán-Martínez J (2017) Relationship between lymphocyte DNA fragmentation and dose of iron oxide (Fe<sub>2</sub>O<sub>3</sub>) and silicon oxide (SiO<sub>2</sub>) nanoparticles. Genet Mol Res 16(1). https://doi.org/10.4238/gmr16019206
Kim K, Tanguay RL (2014) The role of chorion on toxicity of silver nanoparticles in the embryonic zebrafish assay. Environ Health Toxicol 29:1–6. https://doi.org/10.5620/eht.e2014021
Kim JJ, Lee SB, Park JK, Yoo YD (2010) TNF-α-induced ROS production triggering apoptosis is directly linked to Romo1 and Bcl-XL. Cell Death Differ 17(9):1420–1434. https://doi.org/10.1038/cdd.2010.19
Kim Y, Kong SD, Chen L-H, Pisanic TR II, Jin S, Shubayev VI (2013) In vivo nanoneurotoxicity screening using oxidative stress and neuroinflammation paradigms. Nanomedicine 9(7):1057–1066. https://doi.org/10.1016/j.nano.2013.05.002
Klemm D (ed) (2006) Polysaccharides II, vol 205. Springer, Heidelberg, pp 1–300. https://doi.org/10.1007/11776895
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
Laskar A, Ghosh M, Khattak SI, Li W, Yuan XM (2012) Degradation of superparamagnetic iron oxide nanoparticle-induced ferritin by lysosomal cathepsins and related immune response. Nanomedicine 7(5):705–717. https://doi.org/10.2217/nnm.11.148
Legradi J, el Abdellaoui N, van Pomeren M, Legler J (2015) Comparability of behavioural assays using zebrafish larvae to assess neurotoxicity. Environ Sci Pollut Res 22(21):16277–16289. https://doi.org/10.1007/s11356-014-3805-8
Li W-S, Wang X-J, Zhang S, Hu JB, du YL, Kang XQ, Xu XL, Ying XY, You J, Du YZ (2017) Mild microwave activated, chemo-thermal combinational tumor therapy based on a targeted, thermal-sensitive and magnetic micelle. Biomaterials 131:36–46. https://doi.org/10.1016/j.biomaterials.2017.03.048
MacPhail RC, Hunter DL, Irons TD, Padilla S (2011) Locomotion and behavioral toxicity in larval zebrafish: background, methods, and data. In: Zebrafish. Wiley, Hoboken, pp 151–164. https://doi.org/10.1002/9781118102138.ch12
Magdolenova Z, Drlickova M, Henjum K, Rundén-Pran E, Tulinska J, Bilanicova D, Pojana G, Kazimirova A, Barancokova M, Kuricova M, Liskova A, Staruchova M, Ciampor F, Vavra I, Lorenzo Y, Collins A, Rinna A, Fjellsbø L, Volkovova K, Marcomini A, Amiry-Moghaddam M, Dusinska M (2015) Coating-dependent induction of cytotoxicity and genotoxicity of iron oxide nanoparticles. Nanotoxicology 9(sup1):44–56. https://doi.org/10.3109/17435390.2013.847505
Mehvar R (2000) Dextrans for targeted and sustained delivery of therapeutic and imaging agents. J Control Release 69(1):1–25. https://doi.org/10.1016/S0168-3659(00)00302-3
Micheau O, Tschopp J (2003) Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114(2):181–190. https://doi.org/10.1016/S0092-8674(03)00521-X
Mohammad-Beigi H, Yaghmaei S, Roostaazad R, Bardania H, Arpanaei A (2011) Effect of pH, citrate treatment and silane-coupling agent concentration on the magnetic, structural and surface properties of functionalized silica-coated iron oxide nanocomposite particles. Phys E Low-dimensional Syst Nanostructures 44(3):618–627. https://doi.org/10.1016/j.physe.2011.10.015
Muñoz-Fernández MA, Fresno M (1998) The role of tumour necrosis factor, interleukin 6, interferon-gamma and inducible nitric oxide synthase in the development and pathology of the nervous system. Prog Neurobiol 56(3):307–340. https://doi.org/10.1016/S0301-0082(98)00045-8
Neubert J, Bräuer AU (2015) Superparamagnetic iron oxide nanoparticles: promote neuronal regenerative capacity? Neural Regen Res 10(10):1568–1569. https://doi.org/10.4103/1673-5374.165306
Ng AMC, Guo MY, Leung YH, Chan CMN, Wong SWY, Yung MMN, Ma APY, Djurišić AB, Leung FCC, Leung KMY, Chan WK, Lee HK (2015) Metal oxide nanoparticles with low toxicity. J Photochem Photobiol B Biol 151:17–24. https://doi.org/10.1016/j.jphotobiol.2015.06.020
Niemirowicz K, Piktel E, Wilczewska A, Markiewicz K, Durnaś B, Wątek M, Puszkarz I, Wróblewska M, Niklińska W, Savage P, Bucki R (2016) Core–shell magnetic nanoparticles display synergistic antibacterial effects against <em>Pseudomonas aeruginosa</em> and <em>Staphylococcus aureus</em> when combined with cathelicidin LL-37 or selected ceragenins. Int J Nanomedicine 11:5443–5455. https://doi.org/10.2147/IJN.S113706
de Oliveira GMT, Kist LW, Pereira TCBB 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 C Toxicol Pharmacol 162:77–84. https://doi.org/10.1016/j.cbpc.2014.03.010
Palmacci S, Josephson L (1991) Synthesis of polysaccharide covered superparamagnetic oxide colloids. U.S. Patent # US5262176 A
Park E-J, Umh HN, Kim S-W, Cho MH, Kim JH, Kim Y (2014) ERK pathway is activated in bare-FeNPs-induced autophagy. Arch Toxicol 88(2):323–336. https://doi.org/10.1007/s00204-013-1134-1
Park E-A, Lee W, So YH, Lee YS, Jeon B, Choi KS, Kim E, Myeong WJ (2017) Extremely small pseudoparamagnetic iron oxide nanoparticle as a novel blood pool T1 magnetic resonance contrast agent for 3 T whole-heart coronary angiography in canines. Investig Radiol 52(2):128–133. https://doi.org/10.1097/RLI.0000000000000321
Patil U, Adireddy S, Jaiswal A, Mandava S, Lee B, Chrisey D (2015) In vitro/in vivo toxicity evaluation and quantification of iron oxide nanoparticles. Int J Mol Sci 16(10):24417–24450. https://doi.org/10.3390/ijms161024417
Patitsa M, Karathanou K, Kanaki Z, Tzioga L, Pippa N, Demetzos C, Verganelakis DA, Cournia Z, Klinakis A (2017) Magnetic nanoparticles coated with polyarabic acid demonstrate enhanced drug delivery and imaging properties for cancer theranostic applications. Sci Rep 7(1):775. https://doi.org/10.1038/s41598-017-00836-y
Peszke J, Nowak A, Szade J, Szurko A, Zygadło D, Michałowska M, Krzyściak P, Zygoń P, Ratuszna A, Ostafin MM (2016) Effect of silver/copper and copper oxide nanoparticle powder on growth of gram-negative and gram-positive bacteria and their toxicity against the normal human dermal fibroblasts. J Nanopart Res 18(12):355. https://doi.org/10.1007/s11051-016-3671-z
Pham D-H, De Roo B, Nguyen X-B, Vervaele M, Kecskés A, Ny A, Copmans D, Vriens H, Locquet JP, Hoet P, de Witte PAM (2016) Use of zebrafish larvae as a multi-endpoint platform to characterize the toxicity profile of silica nanoparticles. Sci Rep 6(1):37145. https://doi.org/10.1038/srep37145
Pisanic TR, Blackwell JD, Shubayev VI et al (2007) Nanotoxicity of iron oxide nanoparticle internalization in growing neurons. Biomaterials 28(16):2572–2581. https://doi.org/10.1016/j.biomaterials.2007.01.043
Ploussi AG, Gazouli M, Stathis G, Kelekis NL, Efstathopoulos EP (2015) Iron oxide nanoparticles as contrast agents in molecular magnetic resonance imaging. Cardiol Rev 23(5):229–235. https://doi.org/10.1097/CRD.0000000000000055
Popa CL, Prodan AM, Ciobanu CS, Predoi D (2016) The tolerability of dextran-coated iron oxide nanoparticles during in vivo observation of the rats. Gen Physiol Biophys 35:299–310. https://doi.org/10.4149/gpb_2016004
Revia RA, Zhang M (2016) Magnetite nanoparticles for cancer diagnosis, treatment, and treatment monitoring: recent advances. Mater Today (Kidlington) 19(3):157–168. https://doi.org/10.1016/j.mattod.2015.08.022
Roohi F, Lohrke J, Ide A et al (2012) Studying the effect of particle size and coating type on the blood kinetics of superparamagnetic iron oxide nanoparticles. Int J Nanomedicine 7:4447–4458. https://doi.org/10.2147/IJN.S33120
Ruijter JM, Ramakers C, Hoogaars WMH, Karlen Y, Bakker O, van den Hoff MJB, Moorman AFM (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37(6):e45–e45. https://doi.org/10.1093/nar/gkp045
Saha RN, Liu X, Pahan K (2006) Up-regulation of BDNF in astrocytes by TNF-alpha: a case for the neuroprotective role of cytokine. J NeuroImmune Pharmacol 1(3):212–222. https://doi.org/10.1007/s11481-006-9020-8
Samson JC, Goodridge R, Olobatuyi F, Weis JS (2001) Delayed effects of embryonic exposure of zebrafish (Danio Rerio) to methylmercury (MeHg). Aquat Toxicol 51(4):369–376. https://doi.org/10.1016/S0166-445X(00)00128-4
Selderslaghs IWT, Hooyberghs J, De Coen W, Witters HE (2010) Locomotor activity in zebrafish embryos: a new method to assess developmental neurotoxicity. Neurotoxicol Teratol 32(4):460–471. https://doi.org/10.1016/j.ntt.2010.03.002
Selderslaghs IWT, Hooyberghs J, Blust R, Witters HE (2013) Assessment of the developmental neurotoxicity of compounds by measuring locomotor activity in zebrafish embryos and larvae. Neurotoxicol Teratol 37:44–56. https://doi.org/10.1016/j.ntt.2013.01.003
Shaterabadi Z, Nabiyouni G, Soleymani M (2017) High impact of in situ dextran coating on biocompatibility, stability and magnetic properties of iron oxide nanoparticles. Mater Sci Eng C 75:947–956. https://doi.org/10.1016/j.msec.2017.02.143
Skalska J, Frontczak-Baniewicz M, Strużyńska L (2015) Synaptic degeneration in rat brain after prolonged oral exposure to silver nanoparticles. Neurotoxicology 46:145–154. https://doi.org/10.1016/j.neuro.2014.11.002
Sohail A, Ahmad Z, Bég OA, Arshad S, Sherin L (2017) A review on hyperthermia via nanoparticle-mediated therapy. Bull Cancer 104(5):452–461. https://doi.org/10.1016/j.bulcan.2017.02.003
Srivastava P, Sharma P, Muheem A, Warsi M (2017) Magnetic nanoparticles: a review on stratagems of fabrication and its biomedical applications. Recent Pat Drug Deliv Formul 11(999):1–1. https://doi.org/10.2174/1872211311666170328150747
Stordeur P, Goldman M (1998) Interleukin-10 as a regulatory cytokine induced by cellular stress: molecular aspects. Int Rev Immunol 16(5-6):501–522. https://doi.org/10.3109/08830189809043006
Sukardi H, Chng HT, Chan ECY, Gong Z, Lam SH (2011) Zebrafish for drug toxicity screening: bridging the in vitro cell-based models and in vivo mammalian models. Expert Opin Drug Metab Toxicol 7(5):579–589. https://doi.org/10.1517/17425255.2011.562197
Sun Y, Zhang G, He Z et al (2016) Effects of copper oxide nanoparticles on developing zebrafish embryos and larvae. Int J Nanomedicine 11:905–918. https://doi.org/10.2147/IJN.S100350
Tang R, Dodd A, Lai D et al (2007) Validation of zebrafish (Danio rerio) reference genes for quantitative real-time RT-PCR normalization. Acta Biochim Biophys Sin 39(5):384–390. https://doi.org/10.1111/j.1745-7270.2007.00283.x
Tian L, Lin B, Wu L, Li K, Liu H, Yan J, Liu X, Xi Z (2015) Neurotoxicity induced by zinc oxide nanoparticles: age-related differences and interaction. Sci Rep 5(1):16117. https://doi.org/10.1038/srep16117
Tilton FA, Bammler TK, Gallagher EP (2011) Swimming impairment and acetylcholinesterase inhibition in zebrafish exposed to copper or chlorpyrifos separately, or as mixtures. Comp Biochem Physiol Part C Toxicol Pharmacol 153(1):9–16. https://doi.org/10.1016/j.cbpc.2010.07.008
Toropova YG, Golovkin AS, Malashicheva AB et al (2017) In vitro toxicity of FemOn, FemOn-SiO2 composite, and SiO2-FemOn core-shell magnetic nanoparticles. Int J Nanomedicine 12:593–603. https://doi.org/10.2147/IJN.S122580
Truong L, Harper SL, Tanguay RL (2011) Evaluation of embryotoxicity using the zebrafish model. Methods Mol Biol 691:271–279. https://doi.org/10.1007/978-1-60761-849-2_16
Utkur M, Muslu Y, Saritas EU (2017) Relaxation-based viscosity mapping for magnetic particle imaging. Phys Med Biol 62(9):3422–3439. https://doi.org/10.1088/1361-6560/62/9/3422
Vargas RA, Sarmiento K, Vásquez IC (2015) Zebrafish ( Danio rerio ): a potential model for Toxinological studies. Zebrafish 12(5):320–326. https://doi.org/10.1089/zeb.2015.1102
Vyas D, Lopez-Hisijos N, Gandhi S, el-Dakdouki M, Basson MD, Walsh MF, Huang X, Vyas AK, Chaturvedi LS (2015) Doxorubicin-Hyaluronan conjugated super-paramagnetic iron oxide nanoparticles (DOX-HA-SPION) enhanced cytoplasmic uptake of doxorubicin and modulated apoptosis, IL-6 release and NF-kappaB activity in human MDA-MB-231 breast cancer cells. J Nanosci Nanotechnol 15(9):6413–6422. https://doi.org/10.1166/jnn.2015.10834
Walley KR, Lukacs NW, Standiford TJ, Strieter RM, Kunkel SL (1996) Balance of inflammatory cytokines related to severity and mortality of murine sepsis. Infect Immun 64(11):4733–4738
Wang ZG, Zhou R, Jiang D, Song JE, Xu Q, Si J, Chen YP, Zhou X, Gan L, Li JZ, Zhang H, Liu B (2015) Toxicity of graphene quantum dots in zebrafish embryo. Biomed Environ Sci 28(5):341–351. https://doi.org/10.3967/bes2015.048
Weber GEB, Dal Bosco L, Gonçalves COF, Santos AP, Fantini C, Furtado CA, Parfitt GM, Peixoto C, Romano LA, Vaz BS, Barros DM (2014) Biodistribution and toxicological study of PEGylated single-wall carbon nanotubes in the zebrafish (Danio Rerio) nervous system. Toxicol Appl Pharmacol 280(3):484–492. https://doi.org/10.1016/j.taap.2014.08.018
Wehmas LC, Anders C, Chess J, Punnoose A, Pereira CB, Greenwood JA, Tanguay RL (2015) Comparative metal oxide nanoparticle toxicity using embryonic zebrafish. Toxicol Reports 2:702–715. https://doi.org/10.1016/j.toxrep.2015.03.015
Wilt SG, Milward E, Zhou JM, Nagasato K, Patton H, Rusten R, Griffin DE, O'Connor M, Dubois-Dalcq M (1995) In vitro evidence for a dual role of tumor necrosis factor-? In human immunodeficiency virus type 1 encephalopathy. Ann Neurol 37(3):381–394. https://doi.org/10.1002/ana.410370315
Wong J, Prout J, Seifalian A (2017) Magnetic nanoparticles: new perspectives in drug delivery. Curr Pharm Des 23(20):2908–2917. https://doi.org/10.2174/1381612823666170215104659
Wu W, Wu Z, Yu T, Jiang C, Kim WS (2015) Recent progress on magnetic iron oxide nanoparticles: synthesis, surface functional strategies and biomedical applications. Sci Technol Adv Mater 16(2):23501. https://doi.org/10.1088/1468-6996/16/2/023501
Wu W, Jiang CZ, Roy VAL (2016) Designed synthesis and surface engineering strategies of magnetic iron oxide nanoparticles for biomedical applications. Nano 8(47):19421–19474. https://doi.org/10.1039/c6nr07542h
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(Suppl 2):S304–S306. https://doi.org/10.1016/S1076-6332(03)80210-6
Xie Y, Liu D, Cai C et al (2016) Size-dependent cytotoxicity of Fe3O4 nanoparticles induced by biphasic regulation of oxidative stress in different human hepatoma cells. Int J Nanomedicine 11:3557–3570. https://doi.org/10.2147/IJN.S105575
Xiong F, Wang H, Feng Y, Li Y, Hua X, Pang X, Zhang S, Song L, Zhang Y, Gu N (2015) Cardioprotective activity of iron oxide nanoparticles. Sci Rep 5(1):8579. https://doi.org/10.1038/srep08579
Xiong K, Gao Y, Zhou L, Zhang X (2016) Zero-valent iron particles embedded on the mesoporous silica–carbon for chromium (VI) removal from aqueous solution. J Nanopart Res 18(9):267. https://doi.org/10.1007/s11051-016-3582-z
Zhang Z-Q, Song S-C (2017) Multiple hyperthermia-mediated release of TRAIL/SPION nanocomplex from thermosensitive polymeric hydrogels for combination cancer therapy. Biomaterials 132:16–27. https://doi.org/10.1016/j.biomaterials.2017.03.049
Zhang M, Covar J, Marshall B, Dong Z, Atherton SS (2011) Lack of TNF-α promotes caspase-3–independent apoptosis during murine cytomegalovirus retinitis. Investig Opthalmology Vis Sci 52(3):1800–1808. https://doi.org/10.1167/iovs.10-6904
Zou H, Yang R, Hao J, Wang J, Sun C, Fesik SW, Wu JC, Tomaselli KJ, Armstrong RC (2003) Regulation of the Apaf-1/caspase-9 apoptosome by caspase-3 and XIAP. J Biol Chem 278(10):8091–8098. https://doi.org/10.1074/jbc.M204783200
Acknowledgements
This research was supported by CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico), FINEP (Financiadora de Estudos e Projetos) Research Grant “Implantação, Modernização e Qualificação de Estrutura de Pesquisa da PUCRS” (PUCRSINFRA) #01.11.0014-00 and INCT—Brain Disease Excitotoxicity and Neuroprotection. G.M.T.O and E.M.N.O are recipients of fellowship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). T.C.B.P is recipient from CAPES/PNPD Program. R.M.P. and M.R.B are Research Career Awardees from CNPq.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
Supplementary Fig. 1
Stability over 7 days. Size distribution for (a) CLIO-NH2 and (b) UCIO. Symbols are as follows: (●) Day 1, (□) Day 2, (◊) Day 3, (x) Day 4, (+) Day 5, (▵) Day 6, (◣) Day 7. DLS measurements of hydrodynamic size (c) and Zeta potential (d) of the CLIO-NH2 (blue lines) and UCIO (black lines) solutions measured during 7 days (GIF 434 kb)
Rights and permissions
About this article
Cite this article
de Oliveira, G.M.T., de Oliveira, E.M.N., Pereira, T.C.B. et al. Implications of exposure to dextran-coated and uncoated iron oxide nanoparticles to developmental toxicity in zebrafish. J Nanopart Res 19, 389 (2017). https://doi.org/10.1007/s11051-017-4074-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11051-017-4074-5