journal article·2013-01

The presence of serum alters the properties of iron oxide nanoparticles and lowers their accumulation by cultured brain astrocytes

Mark Geppert, Charlotte Petters, Karsten Thiel, Ralf Dringen

Journal of Nanoparticle Research· Volume 15· Issue 1
Publisher page

Abstract

Iron oxide nanoparticles (IONPs) are considered for various diagnostic and therapeutic applications. Such particles are able to cross the blood–brain barrier and are taken up into brain cells. To test whether serum components affect the properties of IONPs and/or their uptake into brain cells, we have incubated dimercaptosuccinate-coated magnetic IONPs without and with fetal calf serum (FCS) and have exposed cultured brain astrocytes with IONPs in the absence or presence of FCS. Incubation with FCS caused a concentration-dependent increase in the average hydrodynamic diameter of the particles and of their zeta-potential. In the presence of 10 % FCS, the diameter of the IONPs increased from 57 ± 2 to 107 ± 6 nm and the zeta-potential of the particles from −22 ± 5 to −9 ± 1 mV. FCS affected also strongly the uptake of IONPs by cultured astrocytes. The efficient time- and temperature-dependent cellular accumulation of IONPs was lowered with increasing concentration of FCS by up to 90 %. In addition, in the absence of serum, endocytosis inhibitors did not alter the IONP accumulation by astrocytes, while chlorpromazine or wortmannin lowered significantly the accumulation of IONPs in the presence of FCS, suggesting that clathrin-mediated endocytosis and macropinocytosis are involved in astrocytic IONP uptake from serum-containing medium. These data demonstrate that the presence of FCS strongly affects the properties of IONPs as well as their accumulation by cultured brain cells.
Source: openaire · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Nanoparticle-Based Drug Delivery · Nanoparticles: synthesis and applications · Graphene and Nanomaterials Applications

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

References (62)

Show source-provided references
1. Andersson BV, Skoglund C, Uvdal K, Solin N (2012) Preparation of amyloid-like fibrils containing magnetic iron oxide nanoparticles: effect of protein aggregation on proton relaxivity. Biochem Biophys Res Commun 419:682–686. doi: 10.1016/j.bbrc.2012.02.7710.1016/j.bbrc.2012.02.077 ↗
2. Bajaj A, Samanta B, Yan H, Jerry DJ, Rotello VM (2009) Stability, toxicity and differential cellular uptake of protein passivated-Fe3O4 nanoparticles. J Mater Chem 19:6328–633110.1039/b901616c ↗
3. Barros LF, Deitmer JW (2010) Glucose and lactate supply to the synapse. Brain Res Rev 63:149–159. doi: 10.1016/j.brainresrev.2009.10.00210.1016/j.brainresrev.2009.10.002 ↗
4. Bee A, Massart R, Neveu S (1995) Synthesis of very fine maghemite particles. J Magn Magn Mater 149:6–9. doi: 10.1016/0304-8853(95)00317-710.1016/0304-8853(95)00317-7 ↗
5. Bhirde A, Xie J, Swierczewska M, Chen X (2011) Nanoparticles for cell labeling. Nanoscale 3:142–153. doi: 10.1039/c0nr00493f10.1039/C0NR00493F ↗
6. Chen ZP, Zhang Y, Xu K, Xu RZ, Liu JW, Gu N (2008) Stability of hydrophilic magnetic nanoparticles under biologically relevant conditions. J Nanosci Nanotechnol 8:6260–6265. doi: 10.1166/jnn.2008.34310.1166/jnn.2008.343 ↗
7. Chen L, McCrate JM, Lee JC, Li H (2011) The role of surface charge on the uptake and biocompatibility of hydroxyapatite nanoparticles with osteoblast cells. Nanotechnology 22:105708. doi: 10.1088/0957-4484/22/10/10570810.1088/0957-4484/22/10/105708 ↗
8. Chertok B, Moffat BA, David AE, Yu FQ, Bergemann C, Ross BD, Yang VC (2008) Iron oxide nanoparticles as a drug delivery vehicle for MRI monitored magnetic targeting of brain tumors. Biomaterials 29:487–496. doi: 10.1016/j.biomaterials.2007.08.05010.1016/j.biomaterials.2007.08.050 ↗
9. Dausend J, Musyanovych A, Dass M, Walther P, Schrezenmeier H, Landfester K, Mailander V (2008) Uptake mechanism of oppositely charged fluorescent nanoparticles in HeLa cells. Macromol Biosci 8:1135–1143. doi: 10.1002/mabi.20080012310.1002/mabi.200800123 ↗
10. Dringen R, Kussmaul L, Hamprecht B (1998) Detoxification of exogenous hydrogen peroxide and organic hydroperoxides by cultured astroglial cells assessed by microtiter plate assay. Brain Res Brain Res Protoc 2:223–228. doi: 10.1016/S1385-299X(97)00047-010.1016/S1385-299X(97)00047-0 ↗
11. Dringen R, Bishop GM, Koeppe M, Dang TN, Robinson SR (2007) The pivotal role of astrocytes in the metabolism of iron in the brain. Neurochem Res 32:1884–1890. doi: 10.1007/s11064-007-9375-010.1007/s11064-007-9375-0 ↗
12. 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 43:405002–405010. doi: 10.1088/0022-3727/43/40/40500210.1088/0022-3727/43/40/405002 ↗
13. Fauconnier N, Pons JN, Roger J, Bee A (1997) Thiolation of maghemite nanoparticles by dimercaptosuccinic acid. J Colloid Interface Sci 194:427–43310.1006/jcis.1997.5125 ↗
14. Geppert M, Hohnholt M, Gaetjen L, Grunwald I, Bäumer M, Dringen R (2009) Accumulation of iron oxide nanoparticles by cultured brain astrocytes. J Biomed Nanotechnol 5:285–293. doi: 10.1166/jbn.2009.103310.1166/jbn.2009.1033 ↗
15. Geppert M, Hohnholt MC, Thiel K, Nürnberger S, Grunwald I, Rezwan K, Dringen R (2011) Uptake of dimercaptosuccinate-coated magnetic iron oxide nanoparticles by cultured brain astrocytes. Nanotechnology 22:145101–145110. doi: 10.1088/0957-4484/22/14/14510110.1088/0957-4484/22/14/145101 ↗
16. Geppert M, Hohnholt MC, Nürnberger S, Dringen R (2012) Ferritin upregulation and transient ROS production in cultured brain astrocytes after loading with iron oxide nanoparticles. Acta Biomater 8:3832–3839. doi: 10.1016/j.actbio.2012.06.02910.1016/j.actbio.2012.06.029 ↗
17. Greulich C, Diendorf J, Simon T, Eggeler G, Epple M, Koller M (2011) Uptake and intracellular distribution of silver nanoparticles in human mesenchymal stem cells. Acta Biomater 7:347–354. doi: 10.1016/j.actbio.2010.08.00310.1016/j.actbio.2010.08.003 ↗
18. Guarnieri D, Guaccio A, Fusco S, Netti PA (2011) Effect of serum proteins on polystyrene nanoparticle uptake and intracellular trafficking in endothelial cells. J Nanopart Res 13:4295–4309. doi: 10.1007/s11051-011-0375-210.1007/s11051-011-0375-2 ↗
19. Hamprecht B, Löffler F (1985) Primary glial cultures as a model for studying hormone action. Methods Enzymol 109:341–34510.1016/0076-6879(85)09097-8 ↗
20. He C, Hu Y, Yin L, Tang C, Yin C (2010) Effects of particle size and surface charge on cellular uptake and biodistribution of polymeric nanoparticles. Biomaterials 31:3657–3666. doi: 10.1016/j.biomaterials.2010.01.06510.1016/j.biomaterials.2010.01.065 ↗
21. Hirrlinger J, Dringen R (2010) The cytosolic redox state of astrocytes: maintenance, regulation and functional implications for metabolite trafficking. Brain Res Rev 63:177–188. doi: 10.1016/j.brainresrev.2009.10.00310.1016/j.brainresrev.2009.10.003 ↗
22. Hohnholt MC, Geppert M, Nürnberger S, von Byern J, Grunwald I, Dringen R (2010) Advanced biomaterials: accumulation of citrate-coated magnetic iron oxide nanoparticles by cultured brain astrocytes. Adv Eng Mater 12:B690–B694. doi: 10.1002/adem.20108005510.1002/adem.201080055 ↗
23. Huang J, Bu L, Xie J, Chen K, Cheng Z, Li X, Chen X (2010) Effects of nanoparticle size on cellular uptake and liver MRI with polyvinylpyrrolidone-coated iron oxide nanoparticles. ACS Nano 4:7151–7160. doi: 10.1021/nn101643u10.1021/nn101643u ↗
24. Huth US, Schubert R, Peschka-Suss R (2006) Investigating the uptake and intracellular fate of pH-sensitive liposomes by flow cytometry and spectral bio-imaging. J Control Release 110:490–504. doi: 10.1016/j.jconrel.2005.10.01810.1016/j.jconrel.2005.10.018 ↗
25. Ivanov AI (2008) Pharmocological inhibition of endocytotic pathways: is it specific enough to be useful? Methods Mol Biol 440:15–33. doi: 10.1007/978-1-59745-178-9_210.1007/978-1-59745-178-9_2 ↗
26. Iversen TG, Skotland T, Sandvig K (2011) Endocytosis and intracellular transport of nanoparticles: present knowledge and need for future studies. Nano Today 6:176–185. doi: 10.1016/j.nantod.2011.02.00310.1016/j.nantod.2011.02.003 ↗
27. Lamkowsky M, Geppert M, Schmidt MM, Dringen R (2012) Magnetic field-induced acceleration of the accumulation of magnetic iron oxide nanoparticles by cultured brain astrocytes. J Biomed Mater Res A 100:323–334. doi: 10.1002/jbm.a.3326310.1002/jbm.a.33263 ↗
28. Laurent S, Forge D, Port M, Roch A, Robic C, Elst LV, Muller RN (2008) Magnetic iron oxide nanoparticles: synthesis, stabilization, vectorization, physicochemical characterizations, and biological applications. Chem Rev 108:2064–2110. doi: 10.1021/Cr068445e10.1021/cr068445e ↗
29. Lesniak A, Fenaroli F, Monopoli MP, Aberg C, Dawson KA, Salvati A (2012) Effects of the presence or absence of a protein corona on silica nanoparticle uptake and impact on cells. ACS Nano 6:5845–5857. doi: 10.1021/nn300223w10.1021/nn300223w ↗
30. Lévy M, Wilhelm C, Devaud M, Levitz P, Gazeau F (2012) How cellular processing of superparamagnetic nanoparticles affects their magnetic behavior and NMR relaxivity. Contrast Media Mol Imaging 7:373–383. doi: 10.1002/cmmi.50410.1002/cmmi.504 ↗
31. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–27510.1016/S0021-9258(19)52451-6 ↗
32. Lunov O, Syrovets T, Loos C, Beil J, Delacher M, Tron K, Nienhaus GU, Musyanovych A, Mailander V, Landfester K, Simmet T (2011) Differential uptake of functionalized polystyrene nanoparticles by human macrophages and a monocytic cell line. ACS Nano 5:1657–1669. doi: 10.1021/nn200075610.1021/nn2000756 ↗
33. Luther EM, Koehler Y, Diendorf J, Epple M, Dringen R (2011) Accumulation of silver nanoparticles by cultured primary brain astrocytes. Nanotechnology 22:375101–375111. doi: 10.1088/0957-4484/22/37/37510110.1088/0957-4484/22/37/375101 ↗
34. Lynch I, Dawson KA (2008) Protein-nanoparticle interactions. Nano Today 3:40–4710.1016/S1748-0132(08)70014-8 ↗
35. Lynch I, Cedervall T, Lundqvist M, Cabaleiro-Lago C, Linse S, Dawson KA (2007) The nanoparticle-protein complex as a biological entity; a complex fluids and surface science challenge for the 21st century. Adv Coll Interf Sci 134–135:167–174. doi: 10.1016/j.cis.2007.04.02110.1016/j.cis.2007.04.021 ↗
36. Mahmoudi M, Hosseinkhani H, Hosseinkhani M, Boutry S, Simchi A, Journeay WS, Subramani K, Laurent S (2011) Magnetic resonance imaging tracking of stem cells in vivo using iron oxide nanoparticles as a tool for the advancement of clinical regenerative medicine. Chem Rev 111:253–280. doi: 10.1021/cr100183210.1021/cr1001832 ↗
37. Maier-Hauff K, Ulrich F, Nestler D, Niehoff H, Wust P, Thiesen B, Orawa H, Budach V, Jordan A (2011) Efficacy and safety of intratumoral thermotherapy using magnetic iron-oxide nanoparticles combined with external beam radiotherapy on patients with recurrent glioblastoma multiforme. J Neurooncol 103:317–324. doi: 10.1007/s11060-010-0389-010.1007/s11060-010-0389-0 ↗
38. Nel AE, Madler L, Velegol D, Xia T, Hoek EM, Somasundaran P, Klaessig F, Castranova V, Thompson M (2009) Understanding biophysicochemical interactions at the nano-bio interface. Nat Mater 8:543–557. doi: 10.1038/nmat244210.1038/nmat2442 ↗
39. Parpura V, Heneka MT, Montana V, Oliet SH, Schousboe A, Haydon PG, Stout RF Jr, Spray DC, Reichenbach A, Pannicke T, Pekny M, Pekna A, Zorec R, Verkhratsky A (2012) Glial cells in (patho)physiology. J Neurochem 121:4–27. doi: 10.1111/j.1471-4159.2012.07664.x10.1111/j.1471-4159.2012.07664.x ↗
40. 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 68:129–137. doi: 10.1016/j.ejpb.2007.02.02410.1016/j.ejpb.2007.02.024 ↗
41. Pickard MR, Jenkins SI, Koller CJ, Furness DN, Chari DM (2011) Magnetic nanoparticle labeling of astrocytes derived for neural transplantation. Tissue Eng Part C Methods 17:89–99. doi: 10.1089/ten.TEC.2010.017010.1089/ten.tec.2010.0170 ↗
42. Rejman J, Oberle V, Zuhorn IS, Hoekstra D (2004) Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem J 377:159–169. doi: 10.1042/BJ2003125310.1042/bj20031253 ↗
43. Riemer J, Hoepken HH, Czerwinska H, Robinson SR, Dringen R (2004) Colorimetric ferrozine-based assay for the quantitation of iron in cultured cells. Anal Biochem 331:370–375. doi: 10.1016/j.ab.2004.03.04910.1016/j.ab.2004.03.049 ↗
44. Scheiber I, Dringen R (2011) Copper accelerates glycolytic flux in cultured astrocytes. Neurochem Res 36:894–903. doi: 10.1007/s11064-011-0419-010.1007/s11064-011-0419-0 ↗
45. Scheiber I, Schmidt MM, Dringen R (2010) Zinc prevents the copper-induced damage of cultured astrocytes. Neurochem Int 57:314–322. doi: 10.1016/j.neuint.2010.06.01010.1016/j.neuint.2010.06.010 ↗
46. Smith PJ, Giroud M, Wiggins HL, Gower F, Thorley JA, Stolpe B, Mazzolini J, Dyson RJ, Rappoport JZ (2012) Cellular entry of nanoparticles via serum sensitive clathrin-mediated endocytosis, and plasma membrane permeabilization. Int J Nanomedicine 7:2045–2055. doi: 10.2147/IJN.S29334ijn-7-2045
47. Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol 119:7–35. doi: 10.1007/s00401-009-0619-810.1007/s00401-009-0619-8 ↗
48. Tedja R, Lim M, Amal R, Marquis C (2012) Effects of serum adsorption on cellular uptake profile and consequent impact of titanium dioxide nanoparticles on human lung cell lines. ACS Nano 6:4083–4093. doi: 10.1021/nn300484510.1021/nn3004845 ↗
49. Tenzer S, Docter D, Rosfa S, Wlodarski A, Kuharev J, Rekik A, Knauer SK, Bantz C, Nawroth T, Bier C, Sirirattanapan J, Mann W, Treuel L, Zellner R, Maskos M, Schild H, Stauber RH (2011) Nanoparticle size is a critical physicochemical determinant of the human blood plasma corona: a comprehensive quantitative proteomic analysis. ACS Nano 5:7155–7167. doi: 10.1021/nn201950e10.1021/nn201950e ↗
50. Thiesen B, Jordan A (2008) Clinical applications of magnetic nanoparticles for hyperthermia. Int J Hyperther 24:467–474. doi: 10.1080/0265673080210475710.1080/02656730802104757 ↗
51. Valois CR, Braz JM, Nunes ES, Vinolo MA, Lima EC, Curi R, Kuebler WM, Azevedo RB (2010) The effect of DMSA-functionalized magnetic nanoparticles on transendothelial migration of monocytes in the murine lung via a beta2 integrin-dependent pathway. Biomaterials 31:366–374. doi: 10.1016/j.biomaterials.2009.09.05310.1016/j.biomaterials.2009.09.053 ↗
52. Walczyk D, Baldelli Bombelli F, Monopoli MP, Lynch I, Dawson KA (2010) What the cell “sees” in bionanoscience. J Am Chem Soc 132:5761–5768. doi: 10.1021/ja910675v10.1021/ja910675v ↗
53. Wang J, Chen Y, Chen B, Ding J, Xia G, Gao C, Cheng J, Jin N, Zhou Y, Li X, Tang M, Wang XM (2010) Pharmacokinetic parameters and tissue distribution of magnetic Fe3O4 nanoparticles in mice. Int J Nanomedicine 5:861–866. doi: 10.2147/IJN.S13662
54. Weinstein JS, Varallyay CG, Dosa E, Gahramanov S, Hamilton B, Rooney WD, Muldoon LL, Neuwelt EA (2010) Superparamagnetic iron oxide nanoparticles: diagnostic magnetic resonance imaging and potential therapeutic applications in neurooncology and central nervous system inflammatory pathologies, a review. J Cereb Blood Flow Metab 30:15–35. doi: 10.1038/jcbfm.2009.19210.1038/jcbfm.2009.192 ↗
55. Wilhelm C, Billotey C, Roger J, Pons JN, Bacri JC, Gazeau F (2003) Intracellular uptake of anionic superparamagnetic nanoparticles as a function of their surface coating. Biomaterials 24:1001–101110.1016/S0142-9612(02)00440-4 ↗
56. Winer JL, Kim PE, Law M, Liu CY, Apuzzo ML (2011) Visualizing the future: enhancing neuroimaging with nanotechnology. World Neurosurg 75:626–637. doi: 10.1016/j.wneu.2011.02.01610.1016/j.wneu.2011.02.016 ↗
57. Wiogo HTR, Lim M, Bulmus V, Yun J, Amal R (2011) Stabilization of magnetic iron oxide nanoparticles in biological media by fetal bovine serum (FBS). Langmuir 27:843–850. doi: 10.1021/La104278m10.1021/la104278m ↗
58. Yan GP, Robinson L, Hogg P (2007) Magnetic resonance imaging contrast agents: overview and perspectives. Radiography 13:e5–e19. doi: 10.1016/j.radi.2006.07.00510.1016/j.radi.2006.07.005 ↗
59. Yang QQ, Liang JG, Han HY (2009) Probing the interaction of magnetic iron oxide nanoparticles with bovine serum albumin by spectroscopic techniques. J Phys Chem B 113:10454–10458. doi: 10.1021/Jp904004w10.1021/jp904004w ↗
60. Yang X, Hong H, Grailer JJ, Rowland IJ, Javadi A, Hurley SA, Xiao Y, Yang Y, Zhang Y, Nickles RJ, Cai W, Steeber DA, Gong S (2011) cRGD-functionalized, DOX-conjugated, and (64)Cu-labeled superparamagnetic iron oxide nanoparticles for targeted anticancer drug delivery and PET/MR imaging. Biomaterials 32:4151–4160. doi: 10.1016/j.biomaterials.2011.02.00610.1016/j.biomaterials.2011.02.006 ↗
61. Yue ZG, Wei W, Lv PP, Yue H, Wang LY, Su ZG, Ma GH (2011) Surface charge affects cellular uptake and intracellular trafficking of chitosan-based nanoparticles. Biomacromolecules 12:2440–2446. doi: 10.1021/bm101482r10.1021/bm101482r ↗
62. Zhu Y, Li WX, Li QN, Li YG, Li YF, Zhang XY, Huang Q (2009) Effects of serum proteins on intracellular uptake and cytotoxicity of carbon nanoparticles. Carbon 47:1351–1358. doi: 10.1016/j.carbon.2009.01.02610.1016/j.carbon.2009.01.026 ↗