Abstract
The field of nanotechnology had enormous developments, resulting in new methods for the controlled synthesis of a wide variety of nanoscale materials with unique properties. Efficient methods such as thermal decomposition for efficient size control have been developed in recent years for the synthesis of oleic acid (OA)-coated magnetite (Fe3O4) nanoparticles (MNP-OA). These nanostructures can be a source of pollution when emitted in the aquatic environment and could be accumulated by vulnerable marine species such as crustaceans. In this work, we synthesized and characterized MNP-OA of three different diameters (5, 8, and 12 nm) by thermal decomposition. These nanoparticles were remarkably stable after treatment with high affinity iron chelators (calcein, fluorescent desferrioxamine, and fluorescent apotransferrin); however, they displayed pro-oxidant activity after being challenged with ascorbate under two physiological buffers. Free or nanoparticle iron displayed low toxicity to four types of hepatopancreatic cells (E, R, F, and B) of the mangrove crab Ucides cordatus; however, they were promptly bioavailable, posing the risk of ecosystem disruption due to the release of excess nutrients.
Similar content being viewed by others
References
Ahearn GA, Mandal APK, Mandal AA (2004) Mechanisms of heavy-metal sequestration and detoxification in crustaceans: a review. https://doi.org/10.1007/s00360-004-0438-0
Ahmadi R, Malek M, Hosseini HRM, Shokrgozar MA, Oghabian MA, Masoudi A, Gu N, Zhang Y (2011) Ultrasonic-assisted synthesis of magnetite based MRI contrast agent using cysteine as the biocapping coating. Mater Chem Phys 131:170–177. https://doi.org/10.1016/j.matchemphys.2011.04.083
Aizawa H (2009) Morphology of polysorbate 80 (tween 80) micelles in aqueous 1,4-dioxane solutions. J Appl Crystallogr 42:592–596. https://doi.org/10.1107/S002188980902295X
Andrews NC (2000) Iron homeostasis: insights from genetics and animal models. Nat Rev Genet 1:208–217. https://doi.org/10.1038/35042073
Ankamwar B, Lai TC, Huang JH, Liu RS, Hsiao M, Chen CH, Hwu YK (2010) Biocompatibility of Fe 3 O 4 nanoparticles evaluated by in vitro cytotoxicity assays using normal, glia and breast cancer cells. Nanotechnology 21:075102. https://doi.org/10.1088/0957-4484/21/7/075102
Arelaro AD, Lima E, Rossi LM et al (2008) Ion dependence of magnetic anisotropy in MFe2O4 (MFe, co, Mn) nanoparticles synthesized by high-temperature reaction. J Magn Magn Mater 320:e335–e338. https://doi.org/10.1016/j.jmmm.2008.02.066
Bae KH, Park M, Do MJ, Lee N, Ryu JH, Kim GW, Kim CG, Park TG, Hyeon T (2012) Chitosan oligosaccharide-stabilized Ferrimagnetic Iron oxide Nanocubes for magnetically modulated Cancer hyperthermia. ACS Nano 6:5266–5273. https://doi.org/10.1021/nn301046w
Barbeta VB, Jardim RF, Kiyohara PK, Effenberger FB, Rossi LM (2010) Magnetic properties of Fe3O4 nanoparticles coated with oleic and dodecanoic acids. J Appl Phys 107:073913. https://doi.org/10.1063/1.3311611
Blinova I, Kanarbik L, Irha N, Kahru A (2017) Ecotoxicity of nanosized magnetite to crustacean Daphnia magna and duckweed Lemna minor. Hydrobiologia 798:141–149. https://doi.org/10.1007/s10750-015-2540-6
Breuer W, Cabantchik ZI (2001) A fluorescence-based one-step assay for serum non-transferrin-bound iron. Anal Biochem 299:194–202. https://doi.org/10.1006/abio.2001.5378
Breuer W, Epsztejn S, Cabantchik ZI (1995) Iron acquired from transferrin by K562 cells is delivered into a cytoplasmic Pool of Chelatable Iron(II). J Biol Chem 270:24209–24215. https://doi.org/10.1074/jbc.270.41.24209
Bruce IJ, Taylor J, Todd M, Davies MJ, Borioni E, Sangregorio C, Sen T (2004) Synthesis, characterisation and application of silica-magnetite nanocomposites. J Magn Magn Mater 284:145–160. https://doi.org/10.1016/j.jmmm.2004.06.032
Cheng FY, Su CH, Yang YS, Yeh CS, Tsai CY, Wu CL, Wu MT, Shieh DB (2005) Characterization of aqueous dispersions of Fe3O4 nanoparticles and their biomedical applications. Biomaterials 26:729–738
Cornell RM, Schwertmann U (2003) The Iron oxides: structure, properties, reactions, occurrences and uses
Doke SK, Dhawale SC (2015) Alternatives to animal testing: a review. Saudi Pharm J 23:223–229. https://doi.org/10.1016/j.jsps.2013.11.002
Duarte LF de A, Souza CA, Nobre CR et al (2016) Multi-level biological responses in Ucides cordatus (Linnaeus, 1763) (Brachyura, Ucididae) as indicators of conservation status in mangrove areas from the western Atlantic. Ecotoxicol Environ Saf 133:176–187. https://doi.org/10.1016/j.ecoenv.2016.07.018
Effenberger FB, Couto RA, Kiyohara PK, Machado G, Masunaga SH, Jardim RF, Rossi LM (2017) Economically attractive route for the preparation of high quality magnetic nanoparticles by the thermal decomposition of iron(III) acetylacetonate. Nanotechnology 28:115603. https://doi.org/10.1088/1361-6528/aa5ab0
Espósito BP, Epsztejn S, Breuer W, Cabantchik ZI (2002) A review of fluorescence methods for assessing labile Iron in cells and biological fluids. Anal Biochem 304:1–18. https://doi.org/10.1006/abio.2002.5611
Esposito BP, Breuer W, Sirankapracha P et al (2003) Labile plasma iron in iron overload: redox activity and susceptibility to chelation. Blood 102:2670–2677. https://doi.org/10.1182/blood-2003-03-0807
Faller B, Nick H (1994) Kinetics and mechanism of iron(III) removal from citrate by desferrioxamine B and 3-hydroxy-1,2-dimethyl-4-pyridone. J Am Chem Soc 116:3860–3865
Fukumura H, Sato M, Kezuka K, Sato I, Feng X, Okumura S, Fujita T, Yokoyama U, Eguchi H, Ishikawa Y, Saito T (2012) Effect of ascorbic acid on reactive oxygen species production in chemotherapy and hyperthermia in prostate cancer cells. J Physiol Sci 62:251–257. https://doi.org/10.1007/s12576-012-0204-0
Gregor C, Hermanek M, Jancik D, Pechousek J, Filip J, Hrbac J, Zboril R (2010) The effect of surface area and crystal structure on the catalytic efficiency of Iron(III) oxide nanoparticles in hydrogen peroxide decomposition. Eur J Inorg Chem 2010:2343–2351. https://doi.org/10.1002/ejic.200901066
Jahn MR, Nawroth T, Fütterer S, Wolfrum U, Kolb U, Langguth P (2012) Iron oxide/hydroxide nanoparticles with negatively charged shells show increased uptake in Caco-2 cells. Mol Pharm 9:1628–1637. https://doi.org/10.1021/mp200628u
Jeng HA, Swanson J (2006) Toxicity of metal oxide nanoparticles in mammalian cells. J Environ Sci Health A 41:2699–2711. https://doi.org/10.1080/10934520600966177
Karlsson HL, Cronholm P, Gustafsson J, Möller L (2008) Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes. Chem Res Toxicol 21:1726–1732. https://doi.org/10.1021/tx800064j
Könczöl M, Ebeling S, Goldenberg E et al (2011) Cytotoxicity and genotoxicity of size-fractionated iron oxide (magnetite) in A549 human lung epithelial cells: role of ROS, JNK, and NF-κB. Chem Res Toxicol 24:1460–1475. https://doi.org/10.1021/tx200051s
Kontoghiorghes G (1995) Comparative efficacy and toxicity of desferrioxamine, deferiprone and other iron and aluminium chelating drugs. Toxicol Lett 80:1–18. https://doi.org/10.1016/0378-4274(95)03415-H
Martin RB, Savory J, Brown S, Bertholf RL, Wills MR (1987) Transferrin binding Al3+ and Fe3+. Clin Chem 33:405–407
Masthoff I-C, Kraken M, Menzel D, Litterst FJ, Garnweitner G (2016) Study of the growth of hydrophilic iron oxide nanoparticles obtained via the non-aqueous sol–gel method. J Sol-Gel Sci Technol 77:553–564. https://doi.org/10.1007/s10971-015-3883-1
Morales MP, Roca AG, Serna CJ (2006) Synthesis of monodispersed magnetite particles from different organometallic precursors. In: INTERMAG 2006 - IEEE International Magnetics Conference. p 555
Moya C, Batlle X, Labarta A (2015) The effect of oleic acid on the synthesis of Fe3O4 nanoparticles over a wide size range. Phys Chem Chem Phys 17:27373–27379. https://doi.org/10.1039/c5cp03395k
Murphy H (1991) The use of whole animals versus isolated organs or cell culture in research
Muxworthy AR, Dunlop DJ, Williams W (2003) High-temperature magnetic stability of small magnetite particles. J Geophys Res Solid Earth 108. https://doi.org/10.1029/2002JB002195
Obi I, Wells AL, Ortega P, Patel D, Farah L, Zanotto FP, Ahearn GA (2011) 3H-L-leucine transport by the promiscuous crustacean dipeptide-like cotransporter. J Exp Zool A Ecol Genet Physiol 315:465–475. https://doi.org/10.1002/jez.694
Ortega P, e Sá MG, Custódio MR, Zanotto FP (2011) Separation and viability of gill and hepatopancreatic cells of a mangrove crab Ucides cordatus. Vitr Cell Dev Biol Anim 47:346–349. https://doi.org/10.1007/s11626-011-9402-y
Ortega P, Custódio MR, Zanotto FP (2014a) Characterization of cadmium plasma membrane transport in gills of a mangrove crab Ucides cordatus. Aquat Toxicol 157:21–29. https://doi.org/10.1016/j.aquatox.2014.09.006
Ortega P, Santos RA, Lacouth P, Rozas EE, Custódio MR, Zanotto FP (2014b) Cytochemical characterization of gill and hepatopancreatic cells of the crab Ucides cordatus (Crustacea, Brachyura) validated by cell metal transport. Iheringia Série Zool 104:347–354. https://doi.org/10.1590/1678-476620141043347354
Ortega P, Vitorino HA, Moreira RG, Pinheiro MAA, Almeida AA, Custódio MR, Zanotto FP (2016) Physiological differences in the crab Ucides cordatus from two populations inhabiting mangroves with different levels of cadmium contamination. Environ Toxicol Chem 9999:1–11. https://doi.org/10.1002/etc.3537
Ortega P, Custódio MR, Zanotto FP (2017) Characterization of cadmium transport in hepatopancreatic cells of a mangrove crab Ucides cordatus: the role of calcium. Aquat Toxicol 188:92–99. https://doi.org/10.1016/j.aquatox.2017.04.012
Patil RM, Thorat ND, Shete PB, Bedge PA, Gavde S, Joshi MG, Tofail SAM, Bohara RA, (2018) Comprehensive cytotoxicity studies of superparamagnetic iron oxide nanoparticles. Biochemistry and Biophysics Reports 13:63–72
Patterson A (1939) The Scherrer formula for X-ray particle size determination. Phys Rev 56:978–982. https://doi.org/10.1103/PhysRev.56.978
Petcharoen K, Sirivat A (2012) Synthesis and characterization of magnetite nanoparticles via the chemical co-precipitation method. Mater Sci Eng B 177:421–427. https://doi.org/10.1016/j.mseb.2012.01.003
Pinheiro MA, Silva PP, Duarte LF et al (2012) Accumulation of six metals in the mangrove crab Ucides cordatus (Crustacea: Ucididae) and its food source, the red mangrove Rhizophora mangle (Angiosperma: Rhizophoraceae). Ecotoxicol Environ Saf 81:114–121. https://doi.org/10.1016/j.ecoenv.2012.05.004
Rocchini G (1994) Magnetite stability in aqueous solutions as a function of temperature. Corros Sci 36:2043–2061. https://doi.org/10.1016/0010-938X(94)90007-8
Sá MG, Zanotto FP (2013) Characterization of copper transport in gill cells of a mangrove crab Ucides cordatus. Aquat Toxicol 144–145:275–283. https://doi.org/10.1016/j.aquatox.2013.10.018
Saville SL, Stone RC, Qi B, Mefford OT (2012) Investigation of the stability of magnetite nanoparticles functionalized with catechol based ligands in biological media. J Mater Chem 22:24909. https://doi.org/10.1039/c2jm34902g
Scherer C, Figueiredo Neto AM (2005) Ferrofluids: properties and applications. Braz J Phys 35:718–727. https://doi.org/10.1590/S0103-97332005000400018
Shang L, Nienhaus K, Nienhaus GU (2014) Engineered nanoparticles interacting with cells: size matters. J Nanobiotechnol 12:5. https://doi.org/10.1186/1477-3155-12-5
Shen S, Liu Y, Huang P, Wang J (2009) In vitro cellular uptake and effects of Fe3O4 magnetic nanoparticles on HeLa cells. J Nanosci Nanotechnol 9:2866–2871
Shen Y, Huang Z, Liu X, Qian J, Xu J, Yang X, Sun A, Ge J (2015) Iron-induced myocardial injury: an alarming side effect of superparamagnetic iron oxide nanoparticles. J Cell Mol Med 19:2032–2035. https://doi.org/10.1111/jcmm.12582
Song SE, Seo BK, Cho KR, Woo O, Son G, Kim C, Cho S, Kwon SS (2015) Computer-aided detection (CAD) system for breast MRI in assessment of local tumor extent, nodal status, and multifocality of invasive breast cancers: preliminary study. Cancer Imaging 15(1):1. https://doi.org/10.1186/s40644-015-0036-2
Sponza DT, Işik M (2002) Decolorization and azo dye degradation by anaerobic/aerobic sequential process. Enzym Microb Technol 31:102–110. https://doi.org/10.1016/S0141-0229(02)00081-9
Su B-L, Moniotte N, Nivarlet N, Tian G, Desmet J (2010) Design and synthesis of fluorescence-based siderophore sensor molecules for FeIII ion determination. Pure Appl Chem 82:2199–2216. https://doi.org/10.1351/PAC-CON-10-02-05
Su B-L, Moniotte N, Nivarlet N, Chen LH, Fu ZY, Desmet J, Li J (2011) Fl–DFO molecules@mesoporous silica materials: highly sensitive and selective nanosensor for dosing with iron ions. J Colloid Interface Sci 358:136–145. https://doi.org/10.1016/j.jcis.2011.02.050
Sun S, Zeng H (2002) Size-controlled synthesis of magnetite nanoparticles. J Am Chem Soc 124:8204–8205. https://doi.org/10.1021/ja026501x
Sun S, Zeng H, Robinson DB, Raoux S, Rice PM, Wang SX, Li G (2004) Monodisperse MFe2O4 (M = Fe, Co, Mn) nanoparticles. J Am Chem Soc 126:273–279. https://doi.org/10.1021/ja0380852
Thomas F, Serratrice G, Beguin C et al (1999) Calcein as a fluorescent probe for ferric Iron: application to iron nutrition in plant cells. J Biol Chem 274:13375–13383. https://doi.org/10.1074/jbc.274.19.13375
Thurber GM, Figueiredo J-L, Weissleder R (2010) Detection limits of intraoperative near infrared imaging for tumor resection. J Surg Oncol 102:758–764. https://doi.org/10.1002/jso.21735
Treuel L, Jiang X, Nienhaus GU (2013) New views on cellular uptake and trafficking of manufactured nanoparticles. J R Soc Interface 10:20120939. https://doi.org/10.1098/rsif.2012.0939
Turdean GL (2011) Design and development of biosensors for the detection of heavy metal toxicity. Int J Electrochem 2011:1–15. https://doi.org/10.4061/2011/343125
Vaslet A, Phillips DL, France C et al (2012) The relative importance of mangroves and seagrass beds as feeding areas for resident and transient fishes among different mangrove habitats in Florida and Belize: evidence from dietary and stable-isotope analyses. J Exp Mar Bio Ecol 434:81–93
Vikesland PJ, Rebodos RL, Bottero JY, Rose J, Masion A (2016) Aggregation and sedimentation of magnetite nanoparticle clusters. Environ Sci Nano 3:567–577. https://doi.org/10.1039/C5EN00155B
Vitorino HA, Mantovanelli L, Zanotto FP, Espósito BP (2015) Iron metallodrugs: stability, redox activity and toxicity against Artemia salina. PLoS One 10:e0121997. https://doi.org/10.1371/journal.pone.0121997
Vitorino HA, Pastrana RYA, Pastrana ECA, Ortega P (2017) Hepatopancreatic cells of a stone crab Menippe frontalis from Perú: separation, viability study, and evaluation of lipoperoxidation against cadmium contamination. Vitr Cell Dev Biol Anim 53:778–781. https://doi.org/10.1007/s11626-017-0168-8
Watts AJR, Lewis C, Goodhead RM, Beckett SJ, Moger J, Tyler CR, Galloway TS (2014) Uptake and retention of microplastics by the shore crab Carcinus maenas. Environ Sci Technol 48:8823–8830. https://doi.org/10.1021/es501090e
Watts AJR, Urbina MA, Goodhead R, Moger J, Lewis C, Galloway TS (2016) Effect of microplastic on the gills of the shore crab Carcinus maenas. Environ Sci Technol 50:5364–5369. https://doi.org/10.1021/acs.est.6b01187
Wu H, Yin J-J, Wamer WG, Zeng M, Lo YM (2014) Reactive oxygen species-related activities of nano-iron metal and nano-iron oxides. J Food Drug Anal 22:86–94. https://doi.org/10.1016/j.jfda.2014.01.007
Xu Z, Shen C, Hou Y, Gao H, Sun S (2009) Oleylamine as both reducing agent and stabilizer in a facile synthesis of magnetite nanoparticles. Chem Mater 21:1778–1780
Zanotto FP, Baptista BB (2011) ATP pulse and calcium homeostasis in cells from hepatopancreas of Dilocarcinus pagei, a freshwater crab. Comp Biochem Physiol A Mol Integr Physiol 158:432–437. https://doi.org/10.1016/j.cbpa.2010.11.025
Zhu X, Tian S, Cai Z (2012) Toxicity assessment of iron oxide nanoparticles in zebrafish (Danio rerio) early life stages. PLoS One 7:e46286. https://doi.org/10.1371/journal.pone.0046286
Funding
This work was financially supported by CAPES and FAPESP (Brazilian government agencies).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible editor: Philippe Garrigues
Rights and permissions
About this article
Cite this article
Vitorino, H.A., Ortega, P., Alta, R.Y.P. et al. Magnetite nanoparticles coated with oleic acid: accumulation in hepatopancreatic cells of the mangrove crab Ucides cordatus. Environ Sci Pollut Res 25, 35672–35681 (2018). https://doi.org/10.1007/s11356-018-3480-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-018-3480-2