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Environmental Science and Pollution Research

, Volume 25, Issue 35, pp 35672–35681 | Cite as

Magnetite nanoparticles coated with oleic acid: accumulation in hepatopancreatic cells of the mangrove crab Ucides cordatus

  • Hector Aguilar Vitorino
  • Priscila Ortega
  • Roxana Y. Pastrana Alta
  • Flavia Pinheiro Zanotto
  • Breno Pannia Espósito
Research Article
  • 68 Downloads

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.

Keywords

Iron Magnetite Ucides cordatus Fluorescence Hepatopancreas Mangrove crab 

Notes

Funding information

This work was financially supported by CAPES and FAPESP (Brazilian government agencies).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 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
  2. 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 CrossRefGoogle Scholar
  3. 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 CrossRefGoogle Scholar
  4. Andrews NC (2000) Iron homeostasis: insights from genetics and animal models. Nat Rev Genet 1:208–217.  https://doi.org/10.1038/35042073 CrossRefGoogle Scholar
  5. 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 CrossRefGoogle Scholar
  6. 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 CrossRefGoogle Scholar
  7. 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 CrossRefGoogle Scholar
  8. 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 CrossRefGoogle Scholar
  9. 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 CrossRefGoogle Scholar
  10. 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 CrossRefGoogle Scholar
  11. 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 CrossRefGoogle Scholar
  12. 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 CrossRefGoogle Scholar
  13. 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 26:729–738CrossRefGoogle Scholar
  14. Cornell RM, Schwertmann U (2003) The Iron oxides: structure, properties, reactions, occurrences and usesCrossRefGoogle Scholar
  15. 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 CrossRefGoogle Scholar
  16. 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 CrossRefGoogle Scholar
  17. 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 CrossRefGoogle Scholar
  18. 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 CrossRefGoogle Scholar
  19. 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 CrossRefGoogle Scholar
  20. 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 116:3860–3865CrossRefGoogle Scholar
  21. 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 CrossRefGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. 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 CrossRefGoogle Scholar
  24. 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 CrossRefGoogle Scholar
  25. 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 CrossRefGoogle Scholar
  26. 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 CrossRefGoogle Scholar
  27. 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 CrossRefGoogle Scholar
  28. Martin RB, Savory J, Brown S, Bertholf RL, Wills MR (1987) Transferrin binding Al3+ and Fe3+. Clin Chem 33:405–407Google Scholar
  29. 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 CrossRefGoogle Scholar
  30. Morales MP, Roca AG, Serna CJ (2006) Synthesis of monodispersed magnetite particles from different organometallic precursors. In: INTERMAG 2006 - IEEE International Magnetics Conference. p 555Google Scholar
  31. 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 CrossRefGoogle Scholar
  32. Murphy H (1991) The use of whole animals versus isolated organs or cell culture in researchGoogle Scholar
  33. 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
  34. 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 CrossRefGoogle Scholar
  35. 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 CrossRefGoogle Scholar
  36. 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 CrossRefGoogle Scholar
  37. 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 CrossRefGoogle Scholar
  38. 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 CrossRefGoogle Scholar
  39. 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 CrossRefGoogle Scholar
  40. 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 13:63–72CrossRefGoogle Scholar
  41. 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 CrossRefGoogle Scholar
  42. 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 CrossRefGoogle Scholar
  43. 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 CrossRefGoogle Scholar
  44. 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 CrossRefGoogle Scholar
  45. 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 CrossRefGoogle Scholar
  46. 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 CrossRefGoogle Scholar
  47. Scherer C, Figueiredo Neto AM (2005) Ferrofluids: properties and applications. Braz J Phys 35:718–727.  https://doi.org/10.1590/S0103-97332005000400018 CrossRefGoogle Scholar
  48. 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 CrossRefGoogle Scholar
  49. 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 9:2866–2871CrossRefGoogle Scholar
  50. 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 CrossRefGoogle Scholar
  51. 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 CrossRefGoogle Scholar
  52. 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 CrossRefGoogle Scholar
  53. 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 CrossRefGoogle Scholar
  54. 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 CrossRefGoogle Scholar
  55. Sun S, Zeng H (2002) Size-controlled synthesis of magnetite nanoparticles. J Am Chem Soc 124:8204–8205.  https://doi.org/10.1021/ja026501x CrossRefGoogle Scholar
  56. 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 CrossRefGoogle Scholar
  57. 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 CrossRefGoogle Scholar
  58. 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 CrossRefGoogle Scholar
  59. 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 CrossRefGoogle Scholar
  60. 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 CrossRefGoogle Scholar
  61. 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 434:81–93CrossRefGoogle Scholar
  62. 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 CrossRefGoogle Scholar
  63. 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 CrossRefGoogle Scholar
  64. 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 CrossRefGoogle Scholar
  65. 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 CrossRefGoogle Scholar
  66. 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 CrossRefGoogle Scholar
  67. 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 CrossRefGoogle Scholar
  68. 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 21:1778–1780CrossRefGoogle Scholar
  69. 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 CrossRefGoogle Scholar
  70. 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 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Fundamental Chemistry, Institute of ChemistryUniversity of São PauloSão PauloBrazil
  2. 2.Institute of BiosciencesUniversity of São PauloSão PauloBrazil
  3. 3.Faculty of ScienceNational University of EngineeringLimaPeru

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