Cellular uptake of magnetic nanoparticles imaged and quantified by magnetic particle imaging.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
05 02 2020
05 02 2020
Historique:
received:
23
07
2019
accepted:
21
01
2020
entrez:
7
2
2020
pubmed:
7
2
2020
medline:
21
11
2020
Statut:
epublish
Résumé
Magnetic particle imaging (MPI) is a non-invasive, non-ionizing imaging technique for the visualization and quantification of magnetic nanoparticles (MNPs). The technique is especially suitable for cell imaging as it offers zero background contribution from the surrounding tissue, high sensitivity, and good spatial and temporal resolutions. Previous studies have demonstrated that the dynamic magnetic behaviour of MNPs changes during cellular binding and internalization. In this study, we demonstrate how this information is encoded in the MPI imaging signal. Through MPI imaging we are able to discriminate between free and cell-bound MNPs in reconstructed images. This technique was used to image and quantify the changes that occur in-vitro when free MNPs come into contact with cells and undergo cellular-uptake over time. The quantitative MPI results were verified by colorimetric measurements of the iron content. The results showed a mean relative difference between the MPI results and the reference method of 23.8% for the quantification of cell-bound MNPs. With this technique, the uptake of MNPs in cells can be imaged and quantified directly from the first MNP cell contact, providing information on the dynamics of cellular uptake.
Identifiants
pubmed: 32024926
doi: 10.1038/s41598-020-58853-3
pii: 10.1038/s41598-020-58853-3
pmc: PMC7002802
doi:
Substances chimiques
Magnetite Nanoparticles
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1922Références
Gleich, B. & Weizenecker, J. Tomographic imaging using the nonlinear response of magnetic particles. Nature 435(no. 7046), 1214–1217 (2005).
pubmed: 15988521
doi: 10.1038/nature03808
Wells, J. et al. Standardisation of magnetic nanoparticles in liquid suspension, J. Phys. D. Appl. Phys. vol. 50, no. 38, p. 383003, Sep. (2017).
doi: 10.1088/1361-6463/aa7fa5
Weizenecker, J. et al. Three-dimensional real-time in vivo magnetic particle imaging. Phys. Med. Biol. 54(no. 5), L1–L10 (2009).
pubmed: 19204385
doi: 10.1088/0031-9155/54/5/L01
Rahmer, J. et al. Nanoparticle encapsulation in red blood cells enables blood-pool magnetic particle imaging hours after injection, Phys. Med. Biol. vol. 58, no. 12, pp. 3965–3977, Jun. (2013).
pubmed: 23685712
doi: 10.1088/0031-9155/58/12/3965
Sedlacik, J. et al. Magnetic Particle Imaging for High Temporal Resolution Assessment of Aneurysm Hemodynamics, PLoS One vol. 11, no. 8, p. e0160097, Aug. (2016).
pubmed: 27494610
pmcid: 4975468
doi: 10.1371/journal.pone.0160097
Zheng, B. et al. Quantitative magnetic particle imaging monitors the transplantation, biodistribution, and clearance of stem cells in vivo. Theranostics 6(no. 3), 291–301 (2016).
pubmed: 26909106
pmcid: 4737718
doi: 10.7150/thno.13728
Yu, E. Y. et al. Magnetic Particle Imaging: A Novel in Vivo Imaging Platform for Cancer Detection. Nano Lett. 17(no. 3), 1648–1654 (2017).
pubmed: 28206771
pmcid: 5724561
doi: 10.1021/acs.nanolett.6b04865
Arami, H. et al. Tomographic Magnetic Particle Imaging of Cancer Targeted Nanoparticles, Nanoscale (2017).
Tay, Z. W. et al. In vivo tracking and quantification of inhaled aerosol using magnetic particle imaging towards inhaled therapeutic monitoring. Theranostics 8(no. 13), 3676–3687 (2018).
pubmed: 30026874
pmcid: 6037024
doi: 10.7150/thno.26608
Finas, D. et al. Sentinel lymphnode detection in breast cancer by magnetic particle imaging using superparamagnetic nanoparticles, In Magnetic Nanoparticles pp. 205–210 (2010).
Bulte, J. W. M. et al. Developing Cellular Mpi: Initial Experience, In Magnetic Nanoparticles pp. 201–204 (2010).
Kool, M. E. et al. Accumulation of ultrasmall superparamagnetic particles of iron oxide in human atherosclerotic plaques can be detected by in vivo magnetic resonance imaging, Circulation vol. 107, no. 19, pp. 2453–2458, May (2003).
Howarth, S. P. S. et al. Utility of USPIO-enhanced MR imaging to identify inflammation and the fibrous cap: A comparison of symptomatic and asymptomatic individuals, Eur. J. Radiol. vol. 70, no. 3, pp. 555–560, Jun. (2009).
pubmed: 18356000
doi: 10.1016/j.ejrad.2008.01.047
Makowski, M. R. et al. Noninvasive assessment of atherosclerotic plaque progression in ApoE −/− mice using susceptibility gradient mapping, Circ. Cardiovasc. Imaging vol. 4, no. 3, pp. 295–303, May (2011).
Ludwig, A. et al. Rapid binding of electrostatically stabilized iron oxide nanoparticles to THP-1 monocytic cells via interaction with glycosaminoglycans, Basic Res. Cardiol. vol. 108, no. 2, p. 328, Mar. (2013).
Poller, W. C. et al. Uptake of citrate-coated iron oxide nanoparticles into atherosclerotic lesions in mice occurs via accelerated transcytosis through plaque endothelial cells, Nano Res. vol. 9, no. 11, pp. 3437–3452, Nov. (2016).
doi: 10.1007/s12274-016-1220-9
Ruehm, S. G., Corot, C., Vogt, P., Kolb, S. & Debatin, J. F. Magnetic Resonance Imaging of Atherosclerotic Plaque With Ultrasmall Superparamagnetic Particles of Iron Oxide in Hyperlipidemic Rabbits, Circulation vol. 103, no. 3, pp. 415–422, Jan. (2001).
Scharlach, C. et al. Synthesis of acid-stabilized iron oxide nanoparticles and comparison for targeting atherosclerotic plaques: Evaluation by MRI, quantitative MPS, and TEM alternative to ambiguous Prussian blue iron staining, Nanomedicine Nanotechnology, Biol. Med. vol. 11, no. 5, pp. 1085–1095, Jul. (2015).
doi: 10.1016/j.nano.2015.01.002
Lendon, C. L., Davies, M. J., Born, G. V & Richardson, P. D. Atherosclerotic plaque caps are locally weakened when macrophages density is increased. Atherosclerosis vol. 87, no. 1, pp. 87–90, Mar. (1991).
Libby, P., Geng, Y. J., Sukhova, G. K., Simon, D. I. & Lee, R. T. Molecular determinants of atherosclerotic plaque vulnerability, in Annals of the New York Academy of Sciences, vol. 811, no. 1 Atheroscleros, pp. 134–145 (1997).
Martinet, W., Schrijvers, D. M. & De, G. R. Y. Meyer Molecular and cellular mechanisms of Macrophage survival in atherosclerosis, Basic Research in Cardiology vol. 107, no. 6. Springer-Verlag, p. 297, 12-Nov (2012).
Loewa, N. et al. Cellular uptake of magnetic nanoparticles quantified by magnetic particle spectroscopy, IEEE Trans. Magn. vol. 49, no. 1, pp. 275–278, Jan. (2013).
doi: 10.1109/TMAG.2012.2218223
Poller, W. C. et al. Magnetic particle spectroscopy reveals dynamic changes in the magnetic behavior of very small superparamagnetic iron oxide nanoparticles during cellular uptake and enables determination of cell-labeling efficacy. J. Biomed. Nanotechnol. 12(no. 2), 337–346 (2016).
pubmed: 27305767
doi: 10.1166/jbn.2016.2204
Poller, W. C. et al. Very small superparamagnetic iron oxide nanoparticles: Long-term fate and metabolic processing in atherosclerotic mice, Nanomedicine Nanotechnology, Biol. Med. vol. 14, no. 8, pp. 2575–2586, Nov. (2018).
doi: 10.1016/j.nano.2018.07.013
Löwa, N., Seidel, M., Radon, P. & Wiekhorst, F. Magnetic nanoparticles in different biological environments analyzed by magnetic particle spectroscopy, J. Magn. Magn. Mater. vol. 427, no. 4 Pt 1, pp. 133–138, Apr. (2017).
Teeman, E., Shasha, C., Evans, J. E. & Krishnan, K. M. Intracellular dynamics of superparamagnetic iron oxide nanoparticles for magnetic particle imaging, Nanoscale (2019).
Markov, D. E. et al. Human erythrocytes as nanoparticle carriers for magnetic particle imaging, Phys. Med. Biol. vol. 55, no. 21, pp. 6461–6473, Nov. (2010).
Shah, S. A., Reeves, D. B., Ferguson, R. M., Weaver, J. B. & Krishnan, K. M. Mixed Brownian alignment and Néel rotations in superparamagnetic iron oxide nanoparticle suspensions driven by an ac field, Phys. Rev. B - Condens. Matter Mater. Phys. vol. 92, no. 9, p. 094438, Sep. (2015).
Arami, H. & Krishnan, K. M. Intracellular performance of tailored nanoparticle tracers in magnetic particle imaging. J. Appl. Phys. 115(no. 17), 3–5 (2014).
doi: 10.1063/1.4867756
Rahmer, J., Halkola, A., Gleich, B., Schmale, I. & Borgert, J. First experimental evidence of the feasibility of multi-color magnetic particle imaging. Phys. Med. Biol. 60(no. 5), 1775–1791 (2015).
pubmed: 25658130
doi: 10.1088/0031-9155/60/5/1775
Stehning, C., Gleich, B. & Rahmer, J. Simultaneous magnetic particle imaging (MPI) and temperature mapping using multi-color MPI. IJMPI 2(no. 2), 1–6 (2016).
Möddel, M., Meins, C., Dieckhoff, J. & Knopp, T. Viscosity quantification using multi-contrast magnetic particle imaging. New J. Phys. 20(no. 8), 083001 (2018).
doi: 10.1088/1367-2630/aad44b
Paysen, H. et al. Improved sensitivity and limit-of-detection using a receive-only coil in magnetic particle imaging, Phys. Med. Biol. vol. 63, no. 13, p. 13NT02, Jul. (2018).
Straub, M. & Schulz, V. Joint reconstruction of tracer distribution and background in magnetic particle imaging. IEEE Trans. Med. Imaging 37(no. 5), 1192–1203 (2018).
pubmed: 29727282
doi: 10.1109/TMI.2017.2777878
Knopp, T., Gdaniec, N., Rehr, R., Graeser, M. & Gerkmann, T. Correction of linear system drifts in magnetic particle imaging, Phys. Med. Biol. May (2019).
Weber, A., Werner, F., Weizenecker, J., Buzug, T. M. & Knopp, T. Artifact free reconstruction with the system matrix approach by overscanning the field-free-point trajectory in magnetic particle imaging. Phys. Med. Biol. 61(no. 2), 475–487 (2016).
pubmed: 26682648
doi: 10.1088/0031-9155/61/2/475
Arbab, A. S. et al. A Model of Lysosomal Metabolism of Dextran Coated Superparamagnetic Iron Oxide (SPIO) Nanoparticles: Implications for Cellular Magnetic Resonance Imaging, NMR Biomed. vol. 11, no. 6, p. 2003, Oct. (2003).
Graeser, M. et al. Towards Picogram Detection of Superparamagnetic Iron-Oxide Particles Using a Gradiometric Receive Coil. Sci. Rep. 7(no. 1), 1–13 (2017).
doi: 10.1038/s41598-017-06992-5
Monopoli, M. P., Åberg, C., Salvati, A. & Dawson, K. A. Biomolecular coronas provide the biological identity of nanosized materials, Nat. Nanotechnol. vol. 7, no. 12, pp. 779–786, Dec. (2012).
Gräfe, C. et al. Intentional formation of a protein corona on nanoparticles: Serum concentration affects protein corona mass, surface charge, and nanoparticle-cell interaction. Int. J. Biochem. Cell Biol. 75, 196–202 (2016).
pubmed: 26556312
doi: 10.1016/j.biocel.2015.11.005
Lesniak, A. et al Effects of the presence or absence of a protein corona on silica nanoparticle uptake and impact on cells, ACS Nano vol. 6, no. 7, pp. 5845–5857, Jul. (2012).
pubmed: 22721453
pmcid: 22721453
doi: 10.1021/nn300223w
Kim, J. A., Aberg, C., Salvati, A. & Dawson, K. A. Role of cell cycle on the cellular uptake and dilution of nanoparticles in a cell population. Nat. Nanotechnol. 7(no. 1), 62–68 (2012).
doi: 10.1038/nnano.2011.191
Kuhlpeter, R. et al. R2 and R2* Mapping for Sensing Cell-bound Superparamagnetic Nanoparticles: In Vitro and Murine in Vivo Testing, Radiology vol. 245, no. 2, pp. 449–457, Nov. (2007).
Girard, O. M., Ramirez, R., Mccarty, S. & Mattrey, R. F. Toward absolute quantification of iron oxide nanoparticles as well as cell internalized fraction using multiparametric MRI, Contrast Media Mol. Imaging vol. 7, no. 4, pp. 411–417, Jul. (2012).
Paysen, H. et al. Imaging and quantification of magnetic nanoparticles: Comparison of magnetic resonance imaging and magnetic particle imaging, J. Magn. Magn. Mater. vol. 475, pp. 382–388, Apr. (2019).
doi: 10.1016/j.jmmm.2018.10.082