journal article·2014-07Open access

Enhanced stability of superparamagnetic iron oxide nanoparticles in biological media using a pH adjusted-BSA adsorption protocol

Si-Ming Yu, Anna Laromaine, Anna Roig

Journal of Nanoparticle Research· Volume 16· Issue 7

Abstract

Superparamagnetic iron oxide nanoparticles (SPIONs) are widely used for biological applications due to their unique properties compared to their bulk counterparts, simplified SPIONs stabilization protocols applicable for a wide spectra of biological media remains a challenging issue. In this work, SPIONs with different surface coatings, tetramethylammonium hydroxide-coated SPIONs (T-SPIONs), and citrate-coated SPIONs (C-SPIONs) were synthesized by a facile, rapid and cost effective microwave-assisted method. C-SPIONs show robust stability in biological media of phosphate buffered saline and Roswell Park Memorial Institute Medium, while destabilize in DMEM. T-SPIONs were found to aggregate rapidly and significantly in all tested media. Then, a modified pH adjusted-BSA adsorption protocol and an addition of excess trisodium citrate dihydrate (Na3Cit) were used to enhance their stability in the media. The BSA adsorption protocol showed great efficiency in stabilizing the dispersed state of both SPIONs in the tested media, while the addition of excess Na3Cit showed limited effect, and it was only applicable for C-SPIONs. The formed BSA layer on SPIONs could be imaged by negative staining TEM, and revealed by Cryo-TEM, FTIR, DLS, and the zeta potential measurements. Results indicated that BSA forms a monolayer of a thickness of about 3 ± 1 nm and BSA interacts with C-SPIONs and T-SPIONs through their coating, rather than by replacing them. This synthetic method and stabilization protocol offer a general methodology to obtain SPIONs with a variety of surfactants, stable in different biological media in few minutes. © 2014 Springer Science+Business Media.
Source: openaire · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Characterization and Applications of Magnetic Nanoparticles · Nanoparticle-Based Drug Delivery · Iron oxide chemistry and applications

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (63)

Show source-provided references
1. Allouni ZE, Cimpan MR, Høl PJ, Skodvin T, Gjerdet NR (2009) Agglomeration and sedimentation of TiO2 nanoparticles in cell culture medium. Colloid Surf B 68(1):83–87. doi: 10.1016/j.colsurfb.2008.09.01410.1016/j.colsurfb.2008.09.014 ↗
2. Andrade ÂL, Valente MA, Ferreira JMF, Fabris JD (2012) Preparation of size-controlled nanoparticles of magnetite. J Magn Magn Mater 324(10):1753–1757. doi: 10.1016/j.jmmm.2011.12.03310.1016/j.jmmm.2011.12.033 ↗
3. Baghbanzadeh M, Carbone L, Cozzoli PD, Kappe CO (2011) Microwave-assisted synthesis of colloidal inorganic nanocrystals. Angew Chem Int Edit 50(48):11312–11359. doi: 10.1002/anie.20110127410.1002/anie.201101274 ↗
4. Brewer SH, Glomm WR, Johnson MC, Knag MK, Franzen S (2005) Probing BSA binding to citrate-coated gold nanoparticles and surfaces. Langmuir 21(20):9303–9307. doi: 10.1021/la050588t10.1021/la050588t ↗
5. Butoescu N, Jordan O, Burdet P, Stadelmann P, Petri-Fink A, Hofmann H, Doelker E (2009) Dexamethasone-containing biodegradable superparamagnetic microparticles for intra-articular administration: physicochemical and magnetic properties, in vitro and in vivo drug release. Eur J Pharm Biopharm 72(3):529–538. doi: 10.1016/j.ejpb.2009.03.00310.1016/j.ejpb.2009.03.003 ↗
6. Carenza E, Barceló V, Morancho A, Levander L, Boada C, Laromaine A, Roig A, Montaner J, Rosell A (2014a) In vitro angiogenic performance and in vivo brain targeting of magnetized endothelial progenitor cells for neurorepair therapies. Nanomed Nanotechnol 10(1):225–234. doi: 10.1016/j.nano.2013.06.00510.1016/j.nano.2013.06.005 ↗
7. Carenza E, Barceló V, Morancho A, Montaner J, Rosell A, Roig A (2014b) Rapid synthesis of water-dispersable SPIONs by microwave assisted route for safe labeling of endothelial progenitor cells. Acta Biomater. doi: 10.1016/j.actbio.2014.04.010
8. Casals E, Pfaller T, Duschl A, Oostingh GJ, Puntes V (2010) Time evolution of the nanoparticle protein corona. ACS Nano 4(7):3623–3632. doi: 10.1021/nn901372t10.1021/nn901372t ↗
9. Corti M, Lascialfari A, Marinone M, Masotti A, Micotti E, Orsini F, Ortaggi G, Poletti G, Innocenti C, Sangregorio C (2008a) Magnetic and relaxometric properties of polyethylenimine-coated superparamagnetic MRI contrast agents. J Magn Magn Mater 320(14):e316–e319. doi: 10.1016/j.jmmm.2008.02.11510.1016/j.jmmm.2008.02.115 ↗
10. Corti M, Lascialfari A, Micotti E, Castellano A, Donativi M, Quarta A, Cozzoli PD, Manna L, Pellegrino T, Sangregorio C (2008b) Magnetic properties of novel superparamagnetic MRI contrast agents based on colloidal nanocrystals. J Magn Magn Mater 320(14):e320–e323. doi: 10.1016/j.jmmm.2008.02.06410.1016/j.jmmm.2008.02.064 ↗
11. Deng Y, Wang L, Yang W, Fu S, Elaïssari A (2003) Preparation of magnetic polymeric particles via inverse microemulsion polymerization process. J Magn Magn Mater 257(1):69–78. doi: 10.1016/S0304-8853(02)00987-310.1016/S0304-8853(02)00987-3 ↗
12. Di Corato R, Piacenza P, Musarò M, Buonsanti R, Cozzoli PD, Zambianchi M, Barbarella G, Cingolani R, Manna L, Pellegrino T (2009) Magnetic-fluorescent colloidal nanobeads: preparation and exploitation in cell separation experiments. Macromol Biosci 9(10):952–958. doi: 10.1002/mabi.20090015410.1002/mabi.200900154 ↗
13. Dominguez-Medina S, Blankenburg J, Olson J, Landes CF, Link S (2013) Adsorption of a protein monolayer via hydrophobic interactions prevents nanoparticle aggregation under harsh environmental conditions. ACS Sustain Chem Eng 1(7):833–842. doi: 10.1021/sc400042h10.1021/sc400042h ↗
14. Eberbeck D, Kettering M, Bergemann C, Zirpel P, Hilger I, Trahms L (2010) Quantification of the aggregation of magnetic nanoparticles with different polymeric coatings in cell culture medium. J Phys D Appl Phys 43(40):1–9. doi: 10.1088/0022-3727/43/40/40500210.1088/0022-3727/43/40/405002 ↗
15. Euliss LE, Grancharov SG, O’Brien S, Deming TJ, Stucky GD, Murray CB, Held GA (2003) Cooperative Assembly of Magnetic Nanoparticles and Block Copolypeptides in Aqueous Media. Nano Lett 3(11):1489–1493. doi: 10.1021/nl034472y10.1021/nl034472y ↗
16. Figuerola A, Fiore A, Di Corato R, Falqui A, Giannini C, Micotti E, Lascialfari A, Corti M, Cingolani R, Pellegrino T, Cozzoli PD, Manna L (2008) One-pot synthesis and characterization of size-controlled bimagnetic FePt–iron oxide heterodimer nanocrystals. J Am Chem Soc 130(4):1477–1487. doi: 10.1021/ja078034v10.1021/ja078034v ↗
17. Freese C, Uboldi C, Gibson M, Unger R, Weksler B, Romero I, Couraud P-O, Kirkpatrick C (2012) Uptake and cytotoxicity of citrate-coated gold nanospheres: comparative studies on human endothelial and epithelial cells. Part Fibre Toxicol 9(1):23. doi: 10.1186/1743-8977-9-2310.1186/1743-8977-9-23 ↗
18. Geppert M, Petters C, Thiel K, Dringen R (2012) The presence of serum alters the properties of iron oxide nanoparticles and lowers their accumulation by cultured brain astrocytes. J Nanopart Res 15(1):1–15. doi: 10.1007/s11051-012-1349-8
19. Grief AD, Richardson G (2005) Mathematical modelling of magnetically targeted drug delivery. J Magn Magn Mater 293(1):455–463. doi: 10.1016/j.jmmm.2005.02.04010.1016/j.jmmm.2005.02.040 ↗
20. Guiot C, Spalla O (2012) Stabilization of TiO2 nanoparticles in complex medium through a pH adjustment protocol. Environ Sci Technol 47(2):1057–1064. doi: 10.1021/es304073610.1021/es3040736 ↗
21. Gupta AK, Gupta M (2005) Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials 26(18):3995–4021. doi: 10.1016/j.biomaterials.2004.10.01210.1016/j.biomaterials.2004.10.012 ↗
22. He XM, Carter DC (1992) Atomic structure and chemistry of human serum albumin. Nature 358(6383):209–215. doi: 10.1038/358209a010.1038/358209a0 ↗
23. Hergt R, Dutz S (2007) Magnetic particle hyperthermia—biophysical limitations of a visionary tumour therapy. J Magn Magn Mater 311(1):187–192. doi: 10.1016/j.jmmm.2006.10.115610.1016/j.jmmm.2006.10.1156 ↗
24. Hondow N, Brydson R, Wang P, Holton M, Brown MR, Rees P, Summers H, Brown A (2012) Quantitative characterization of nanoparticle agglomeration within biological media. J Nanopart Res 14(7):1–15. doi: 10.1007/s11051-012-0977-310.1007/s11051-012-0977-3 ↗
25. Hoskins C, Wang L, Cheng W, Cuschieri A (2012) Dilemmas in the reliable estimation of the in vitro cell viability in magnetic nanoparticle engineering: which tests and what protocols? Nanoscale Res Lett 7(1):77. doi: 10.1186/1556-276X-7-7710.1186/1556-276X-7-77 ↗
26. Janes KA, Calvo P, Alonso MJ (2001) Polysaccharide colloidal particles as delivery systems for macromolecules. Adv Drug Deliver Rev 47(1):83–97. doi: 10.1016/S0169-409X(00)00123-X10.1016/S0169-409X(00)00123-X ↗
27. Ji Z, Jin X, George S, Xia T, Meng H, Wang X, Suarez E, Zhang H, Hoek EMV, Godwin H, Nel AE, Zink JI (2010) Dispersion and stability optimization of TiO2 nanoparticles in cell culture media. Environ Sci Technol 44(19):7309–7314. doi: 10.1021/es100417s10.1021/es100417s ↗
28. Kah JCY, Chen J, Zubieta A, Hamad-Schifferli K (2012) Exploiting the protein corona around gold nanorods for loading and triggered release. ACS Nano 6(8):6730–6740. doi: 10.1021/nn301389c10.1021/nn301389c ↗
29. Khullar P, Singh V, Mahal A, Dave PN, Thakur S, Kaur G, Singh J, Singh Kamboj S, Singh Bakshi M (2012) Bovine serum albumin bioconjugated gold nanoparticles: synthesis, hemolysis, and cytotoxicity toward cancer cell lines. J Phys Chem C 116(15):8834–8843. doi: 10.1021/jp300585d10.1021/jp300585d ↗
30. Kim DK, Zhang Y, Kehr J, Klason T, Bjelke B, Muhammed M (2001) Characterization and MRI study of surfactant-coated superparamagnetic nanoparticles administered into the rat brain. J Magn Magn Mater 225(1–2):256–261. doi: 10.1016/S0304-8853(00)01255-510.1016/S0304-8853(00)01255-5 ↗
31. Kircheis R, Wightman L, Wagner E (2001) Design and gene delivery activity of modified polyethylenimines. Adv Drug Deliv Rev 53(3):341–358. doi: 10.1016/S0169-409X(01)00202-210.1016/S0169-409X(01)00202-2 ↗
32. Kohli I, Alam S, Patel B, Mukhopadhyay A (2013) Interaction and diffusion of gold nanoparticles in bovine serum albumin solutions. Appl Phys Lett 102 (20):203705-203705-203704. doi: 10.1063/1.480767210.1063/1.4807672 ↗
33. Lee P, Knight R, Smit JM, Wilschut J, Griffin DE (2002) A single mutation in the E2 glycoprotein important for neurovirulence influences binding of sindbis virus to neuroblastoma cells. J Virol 76(12):6302–6310. doi: 10.1128/jvi.76.12.6302-631-.200210.1128/JVI.76.12.6302-631-.2002 ↗
34. Levy M, Quarta A, Espinosa A, Figuerola A, Wilhelm C, García-Hernández M, Genovese A, Falqui A, Alloyeau D, Buonsanti R, Cozzoli PD, García MA, Gazeau F, Pellegrino T (2011) Correlating magneto-structural properties to hyperthermia performance of highly monodisperse iron oxide nanoparticles prepared by a seeded-growth route. Chem Mater 23(18):4170–4180. doi: 10.1021/cm201078f10.1021/cm201078f ↗
35. Liu G, Hong RY, Guo L, Li YG, Li HZ (2011) Preparation, characterization and MRI application of carboxymethyl dextran coated magnetic nanoparticles. Appl Surf Sci 257(15):6711–6717. doi: 10.1016/j.apsusc.2011.02.11010.1016/j.apsusc.2011.02.110 ↗
36. Lu A-H, Salabas EL, Schüth F (2007) Magnetic nanoparticles: synthesis, protection, functionalization, and application. Angew Chem Int Ed 46(8):1222–1244. doi: 10.1002/anie.20060286610.1002/anie.200602866 ↗
37. Luciani N, Gazeau F, Wilhelm C (2009) Reactivity of the monocyte/macrophage system to superparamagnetic anionic nanoparticles. J Mater Chem 19(35):6373–6380. doi: 10.1039/B903306H10.1039/b903306h ↗
38. McBain SC, Griesenbach U, Xenariou S, Keramane A, Batich CD, Alton EWFW, Dobson J (2008) Magnetic nanoparticles as gene delivery agents: enhanced transfection in the presence of oscillating magnet arrays. Nanotechnology 19(40):405102. doi: 10.1088/0957-4484/19/40/40510210.1088/0957-4484/19/40/405102 ↗
39. Metin C, Lake L, Miranda C, Nguyen Q (2011) Stability of aqueous silica nanoparticle dispersions. J Nanopart Res 13(2):839–850. doi: 10.1007/s11051-010-0085-110.1007/s11051-010-0085-1 ↗
40. Moulin AM, O’Shea SJ, Badley RA, Doyle P, Welland ME (1999) Measuring surface-induced conformational changes in proteins. Langmuir 15(26):8776–8779. doi: 10.1021/la990416u10.1021/la990416u ↗
41. Nakata S, Kido N, Hayashi M, Hara M, Sasabe H, Sugawara T, Matsuda T (1996) Chemisorption of proteins and their thiol derivatives onto gold surfaces: characterization based on electrochemical nonlinearity. Biophys Chem 62(1–3):63–72. doi: 10.1016/S0301-4622(96)02208-910.1016/S0301-4622(96)02208-9 ↗
42. Namduri H, Nasrazadani S (2008) Quantitative analysis of iron oxides using Fourier transform infrared spectrophotometry. Corros Sci 50(9):2493–2497. doi: 10.1016/j.corsci.2008.06.03410.1016/j.corsci.2008.06.034 ↗
43. Natte K, Friedrich JF, Wohlrab S, Lutzki J, von Klitzing R, Österle W, Orts-Gil G (2013) Impact of polymer shell on the formation and time evolution of nanoparticle–protein corona. Colloid Surf B 104:213–220. doi: 10.1016/j.colsurfb.2012.11.01910.1016/j.colsurfb.2012.11.019 ↗
44. Nigam S, Barick KC, Bahadur D (2011) Development of citrate-stabilized Fe3O4 nanoparticles: conjugation and release of doxorubicin for therapeutic applications. J Magn Magn Mater 323(2):237–243. doi: 10.1016/j.jmmm.2010.09.00910.1016/j.jmmm.2010.09.009 ↗
45. Ouasri A, Rhandour A, Dhamelincourt MC, Dhamelincourt P, Mazzah A (2002) Vibrational study of (CH3)4NSbCl6 and [(CH3)4N]2SiF6. Spectrochim Acta A 58(12):2779–2788. doi: 10.1016/S1386-1425(02)00019-710.1016/S1386-1425(02)00019-7 ↗
46. Pamme N, Wilhelm C (2006) Continuous sorting of magnetic cells via on-chip free-flow magnetophoresis. Lab Chip 6(8):974–980. doi: 10.1039/B604542A10.1039/b604542a ↗
47. Pascu O, Carenza E, Gich M, Estradé S, Peiró F, Herranz G, Roig A (2012) Surface reactivity of iron oxide nanoparticles by microwave-assisted synthesis; comparison with the thermal decomposition route. J Phys Chem C 116(28):15108–15116. doi: 10.1021/jp303204d10.1021/jp303204d ↗
48. Petri-Fink A, Steitz B, Finka A, Salaklang J, Hofmann H (2008) Effect of cell media on polymer coated superparamagnetic iron oxide nanoparticles (SPIONs): Colloidal stability, cytotoxicity, and cellular uptake studies. Eur J Pharm Biopharm 68(1):129–137. doi: 10.1016/j.ejpb.2007.02.02410.1016/j.ejpb.2007.02.024 ↗
49. Porter D, Sriram K, Wolfarth M, Jefferson A, Schwegler-Berry D, Andrew ME, Castranova V (2008) A biocompatible medium for nanoparticle dispersion. Nanotoxicology 2(3):144–154. doi: 10.1080/1743539080231834910.1080/17435390802318349 ↗
50. Pratten MK, Lloyd JB (1986) Pinocytosis and phagocytosis: the effect of size of a particulate substrate on its mode of capture by rat peritoneal macrophages cultured in vitro. BBA-Gen Subjects 881(3):307–313. doi: 10.1016/0304-4165(86)90020-610.1016/0304-4165(86)90020-6 ↗
51. Safi M, Sarrouj H, Sandre O, Mignet N, Berret JF (2010) Interactions between sub-10-nm iron and cerium oxide nanoparticles and 3T3 fibroblasts: the role of the coating and aggregation state. Biomaterials 21(14):145103. doi: 10.1088/0957-4484/21/14/145103
52. Safi M, Courtois J, Seigneuret M, Conjeaud H, Berret JF (2011) The effects of aggregation and protein corona on the cellular internalization of iron oxide nanoparticles. Biomaterials 32(35):9353–9363. doi: 10.1016/j.biomaterials.2011.08.04810.1016/j.biomaterials.2011.08.048 ↗
53. Sager TM, Porter DW, Robinson VA, Lindsley WG, Schwegler-Berry DE, Castranova V (2007) Improved method to disperse nanoparticles for in vitro and in vivo investigation of toxicity. Nanotoxicology 1(2):118–129. doi: 10.1080/1743539070138159610.1080/17435390701381596 ↗
54. Sasidharan S, Jayasree A, Fazal S, Koyakutty M, Nair SV, Menon D (2013) Ambient temperature synthesis of citrate stabilized and biofunctionalized, fluorescent calcium fluoride nanocrystals for targeted labeling of cancer cells. Biomater Sci 1(3):294–305. doi: 10.1039/C2BM00127F10.1039/C2BM00127F ↗
55. Sen T, Mandal S, Haldar S, Chattopadhyay K, Patra A (2011) Interaction of gold nanoparticle with human serum albumin (HSA) protein using surface energy transfer. J Phys Chem C 115(49):24037–24044. doi: 10.1021/jp207374g10.1021/jp207374g ↗
56. Soenen SJH, Himmelreich U, Nuytten N, De Cuyper M (2011) Cytotoxic effects of iron oxide nanoparticles and implications for safety in cell labelling. Biomaterials 32(1):195–205. doi: 10.1016/j.biomaterials.2010.08.07510.1016/j.biomaterials.2010.08.075 ↗
57. Sun S, Zeng H (2002) Size-controlled synthesis of magnetite nanoparticles. J Am Chem Soc 124(28):8204–8205. doi: 10.1021/ja026501x10.1021/ja026501x ↗
58. Uboldi C, Bonacchi D, Lorenzi G, Hermanns MI, Pohl C, Baldi G, Unger R, Kirkpatrick CJ (2009) Gold nanoparticles induce cytotoxicity in the alveolar type-II cell lines A549 and NCIH441. Part Fibre Toxicol 6(1):18. doi: 10.1186/1743-8977-6-1810.1186/1743-8977-6-18 ↗
59. Walczyk D, Bombelli FB, Monopoli MP, Lynch I, Dawson KA (2010) What the cell “Sees” in bionanoscience. J Am Chem Soc 132(16):5761–5768. doi: 10.1021/ja910675v10.1021/ja910675v ↗
60. Wei X, Wei Z, Zhang L, Liu Y, He D (2011) Highly water-soluble nanocrystal powders of magnetite and maghemite coated with gluconic acid: Preparation, structure characterization, and surface coordination. J Colloid Interf Sci 354(1):76–81. doi: 10.1016/j.jcis.2010.10.04910.1016/j.jcis.2010.10.049 ↗
61. Wells MA, Abid A, Kennedy IM, Barakat AI (2012) Serum proteins prevent aggregation of Fe2O3 and ZnO nanoparticles. Nanotoxicology 6(8):837–846. doi: 10.3109/17435390.2011.62513110.3109/17435390.2011.625131 ↗
62. Wiogo HTR, Lim M, Bulmus V, Gutiérrez L, Woodward RC, Amal R (2012) Insight into serum protein interactions with functionalized magnetic nanoparticles in biological media. Langmuir 28(9):4346–4356. doi: 10.1021/la204740t10.1021/la204740t ↗
63. Ye A, Flanagan J, Singh H (2006) Formation of stable nanoparticles via electrostatic complexation between sodium caseinate and gum arabic. Biopolymers 82(2):121–133. doi: 10.1002/bip.2046510.1002/bip.20465 ↗