AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home Nano Research Article
Article Link
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article

Real-time in situ magnetic measurement of the intracellular biodegradation of iron oxide nanoparticles in a stem cell-spheroid tissue model

Aurore Van de Walle1( ), Alexandre Fromain1, Anouchka Plan Sangnier1,2, Alberto Curcio1, Luc Lenglet3, Laurence Motte2( ), Yoann Lalatonne2,4( ), Claire Wilhelm1( )
Laboratoire Matière et Systèmes, Complexes MSC, UMR 7057, CNRS & University of Paris, 75205, Paris Cedex 13, France
Inserm, U1148, Laboratory for Vascular Translational Science, Sorbonne Paris Nord, Sorbonne Paris Cité, F-93017 Bobigny, France
Normafin Sàrl, 8 rue Mathilde Girault, 92300 Levallois-Perret, France
Services de Biochimie et Médecine Nucléaire, Hôpital Avicenne Assistance Publique-Hôpitaux de Paris, F-93009 Bobigny, France
Show Author Information

Graphical Abstract

Abstract

The use of magnetic nanoparticles in nanomedicine keeps expanding and, for most applications, the nanoparticles are internalized in cells then left within, bringing the need for accurate, fast, and easy to handle methodologies to assess their behavior in the cellular environment. Herein, a benchtop-size magnetic sensor is introduced to provide real-time precise measurement of nanoparticle magnetism within living cells. The values obtained with the sensor, of cells loaded with different doses of magnetic nanoparticles, are first compared to conventional vibrating sample magnetometry (VSM), and a strong correlation remarkably validates the use of the magnetic sensor as magnetometer to determine the nanoparticle cellular uptake. The sensor is then used to monitor the progressive intracellular degradation of the nanoparticles, over days. Importantly, this real-time in situ measure is performed on a stem cell-spheroid tissue model and can run continuously on a same spheroid, with cells kept alive within. Besides, such continuous magnetic measurement of cell magnetism at the tissue scale does not impact either tissue formation, viability, or stem cell function, including differentiation and extracellular matrix production.

Keywords

magnetic nanoparticlesmagnetometryreal-time in operando measuresbiodegradationstem cells

Electronic Supplementary Material

Download File(s)
12274_2020_2631_MOESM1_ESM.pdf (3.9 MB)

References

[1]
Wei, H.; Bruns, O. T.; Kaul, M. G.; Hansen, E. C.; Barch, M.; Wiśniowska, A.; Chen, O.; Chen, Y.; Li, N.; Okada, S. et al. Exceedingly small iron oxide nanoparticles as positive MRI contrast agents. Proc. Natl. Acad. Sci. U.S.A 2017, 114, 2325-2330.
Crossref Google Scholar
[2]
Hachani, R.; Lowdell, M.; Birchall, M.; Hervault, A.; Mertz, D.; Begin-Colin, S.; Thanh, N. T. K. Polyol synthesis, functionalisation, and biocompatibility studies of superparamagnetic iron oxide nanoparticles as potential MRI contrast agents. Nanoscale 2016, 8, 3278-3287.
Crossref Google Scholar
[3]
Blanco-Andujar, C.; Walter, A.; Cotin, G.; Bordeianu, C.; Mertz, D.; Felder-Flesch, D.; Begin-Colin, S. Design of iron oxide-based nanoparticles for MRI and magnetic hyperthermia. Nanomedicine 2016, 11, 1889-1910.
Crossref Google Scholar
[4]
Cotin, G.; Blanco-Andujar, C.; Nguyen, D. V.; Affolter, C.; Boutry, S.; Boos, A.; Ronot, P.; Uring-Lambert, B.; Choquet, P.; Zorn, P. E. et al. Dendron based antifouling, MRI and magnetic hyperthermia properties of different shaped iron oxide nanoparticles. Nanotechnology 2019, 30, 374002.
Crossref Google Scholar
[5]
Cortajarena, A. L.; Ortega, D.; Ocampo, S. M.; Gonzalez-García, A.; Couleaud, P.; Miranda, R.; Belda-Iniesta, C.; Ayuso-Sacido, A. Engineering iron oxide nanoparticles for clinical settings. Nanobiomedicine 2014, 1, 2.
Crossref Google Scholar
[6]
Johannsen, M.; Thiesen, B.; Wust, P.; Jordan, A. Magnetic nanoparticle hyperthermia for prostate cancer. Int. J. Hyperthermia 2010, 26, 790-795.
Crossref Google Scholar
[7]
Blanco-Andujar, C.; Teran, F. J.; Ortega, D. Current outlook and perspectives on nanoparticle-mediated magnetic hyperthermia. In Iron Oxide Nanoparticles for Biomedical Applications. Mahmoudi, M.; Laurent, S., Eds.; Metal Oxides: Elsevier, 2018; pp 197-245.
Crossref
[8]
Maier-Hauff, K.; Ulrich, F.; Nestler, D.; Niehoff, H.; Wust, P.; Thiesen, B.; Orawa, H.; Budach, V.; Jordan, A. Efficacy and safety of intratumoral thermotherapy using magnetic iron-oxide nanoparticles combined with external beam radiotherapy on patients with recurrent glioblastoma multiforme. J. Neurooncol. 2011, 103, 317-324.
Crossref Google Scholar
[9]
Espinosa, A.; Kolosnjaj-Tabi, J.; Abou-Hassan, A.; Sangnier, A. P.; Curcio, A.; Silva, A. K. A.; Di Corato, R.; Neveu, S.; Pellegrino, T.; Liz-Marzán, L. M. et al. Magnetic (Hyper)thermia or photothermia? Progressive comparison of iron oxide and gold nanoparticles heating in water, in cells, and in vivo. Adv. Funct. Mater. 2018, 28, 1803660.
Crossref Google Scholar
[10]
Kakwere, H.; Leal, M. P.; Materia, M. E.; Curcio, A.; Guardia, P.; Niculaes, D.; Marotta, R.; Falqui, A.; Pellegrino, T. Functionalization of strongly interacting magnetic nanocubes with (thermo)responsive coating and their application in hyperthermia and heat-triggered drug delivery. ACS Appl. Mater. Interfaces 2015, 7, 10132-10145.
Crossref Google Scholar
[11]
Sandre, O.; Genevois, C.; Garaio, E.; Adumeau, L.; Mornet, S.; Couillaud, F. In vivo imaging of local gene expression induced by magnetic hyperthermia. Genes 2017, 8, 61.
Crossref Google Scholar
[12]
Cazares-Cortes, E.; Cabana, S.; Boitard, C.; Nehlig, E.; Griffete, N.; Fresnais, J.; Wilhelm, C.; Abou-Hassan, A.; Ménager, C. Recent insights in magnetic hyperthermia: From the “hot-spot” effect for local delivery to combined magneto-photo-thermia using magneto-plasmonic hybrids. Adv. Drug Deliv. Rev. 2019, 138, 233-246.
Crossref Google Scholar
[13]
Blanco-Andujar, C.; Ortega, D.; Southern, P.; Pankhurst, Q. A.; Thanh, N. T. K. High performance multi-core iron oxide nanoparticles for magnetic hyperthermia: Microwave synthesis, and the role of core-to-core interactions. Nanoscale 2015, 7, 1768-1775.
Crossref Google Scholar
[14]
Asensio, J. M.; Marbaix, J.; Mille, N.; Lacroix, L. M.; Soulantica, K.; Fazzini, P. F.; Carrey, J.; Chaudret, B. To heat or not to heat: A study of the performances of iron carbide nanoparticles in magnetic heating. Nanoscale 2019, 11, 5402-5411.
Crossref Google Scholar
[15]
Hallali, N.; Clerc, P.; Fourmy, D.; Gigoux, V.; Carrey, J. Influence on cell death of high frequency motion of magnetic nanoparticles during magnetic hyperthermia experiments. Appl. Phys. Lett. 2016, 109, 032402.
Crossref Google Scholar
[16]
Plan Sangnier, A.; Preveral, S.; Curcio, A.; Silva, A. K. A.; Lefèvre, C. T.; Pignol, D.; Lalatonne, Y.; Wilhelm, C. Targeted thermal therapy with genetically engineered magnetite magnetosomes@RGD: Photothermia is far more efficient than magnetic hyperthermia. J. Control. Release 2018, 279, 271-281.
Crossref Google Scholar
[17]
Chu, M. Q.; Shao, Y. X.; Peng, J. L.; Dai, X. Y.; Li, H. K.; Wu, Q. S.; Shi, D. L. Near-infrared laser light mediated cancer therapy by photothermal effect of Fe3O4 magnetic nanoparticles. Biomaterials 2013, 34, 4078-4088.
Crossref Google Scholar
[18]
Zhou, Z. G.; Sun, Y. N.; Shen, J. C.; Wei, J.; Yu, C.; Kong, B.; Liu, W.; Yang, H.; Yang, S. P.; Wang, W. Iron/iron oxide core/shell nanoparticles for magnetic targeting MRI and near-infrared photothermal therapy. Biomaterials 2014, 35, 7470-7478.
Crossref Google Scholar
[19]
Shen, S.; Wang, S.; Zheng, R.; Zhu, X. Y.; Jiang, X. G.; Fu, D. L.; Yang, W. L. Magnetic nanoparticle clusters for photothermal therapy with near-infrared irradiation. Biomaterials 2015, 39, 67-74.
Crossref Google Scholar
[20]
Ye, D. W.; Li, Y.; Gu, N. Magnetic labeling of natural lipid encapsulations with iron-based nanoparticles. Nano Res. 2018, 11, 2970-2991.
Crossref Google Scholar
[21]
Ulbrich, K.; Holá, K.; Šubr, V.; Bakandritsos, A.; Tuček, J.; Zbořil, R. Targeted drug delivery with polymers and magnetic nanoparticles: Covalent and noncovalent approaches, release control, and clinical studies. Chem. Rev. 2016, 116, 5338-5431.
Crossref Google Scholar
[22]
Carregal-Romero, S.; Guardia, P.; Yu, X.; Hartmann, R.; Pellegrino, T.; Parak, W. J. Magnetically triggered release of molecular cargo from iron oxide nanoparticle loaded microcapsules. Nanoscale 2015, 7, 570-576.
Crossref Google Scholar
[23]
Mertz, D.; Sandre, O.; Bégin-Colin, S. Drug releasing nanoplatforms activated by alternating magnetic fields. Biochim. Biophys. Acta Gen. Subj. 2017, 1861, 1617-1641.
Crossref Google Scholar
[24]
Adedoyin, A. A.; Ekenseair, A. K. Biomedical applications of magneto-responsive scaffolds. Nano Res. 2018, 11, 5049-5064.
Crossref Google Scholar
[25]
Souza, G. R.; Molina, J. R.; Raphael, R. M.; Ozawa, M. G.; Stark, D. J.; Levin, C. S.; Bronk, L. F.; Ananta, J. S.; Mandelin, J.; Georgescu, M. M. et al. Three-dimensional tissue culture based on magnetic cell levitation. Nat. Nanotechnol, 2010, 5, 291-296.
Crossref Google Scholar
[26]
Mattix, B.; Olsen, T. R.; Gu, Y.; Casco, M.; Herbst, A.; Simionescu, D. T.; Visconti, R. P.; Kornev, K. G.; Alexis, F. Biological magnetic cellular spheroids as building blocks for tissue engineering. Acta Biomater. 2014, 10, 623-629.
Crossref Google Scholar
[27]
Hachani, R.; Lowdell, M.; Birchall, M.; Thanh, N. T. K. Tracking stem cells in tissue-engineered organs using magnetic nanoparticles. Nanoscale 2013, 5, 11362-11373.
Crossref Google Scholar
[28]
Pham, B. T. T.; Colvin, E. K.; Pham, N. T. H.; Kim, B. J.; Fuller, E. S.; Moon, E. A.; Barbey, R.; Yuen, S.; Rickman, B. H.; Bryce, N. S. et al. Biodistribution and clearance of stable superparamagnetic maghemite iron oxide nanoparticles in mice following intraperitoneal administration. Int. J. Mol. Sci. 2018, 19, 205.
Crossref Google Scholar
[29]
Bargheer, D.; Giemsa, A.; Freund, B.; Heine, M.; Waurisch, C.; Stachowski, G. M.; Hickey, S. G.; Eychmüller, A.; Heeren, J.; Nielsen, P. The distribution and degradation of radiolabeled superparamagnetic iron oxide nanoparticles and quantum dots in mice. Beilstein J. Nanotechnol. 2015, 6, 111-123.
Crossref Google Scholar
[30]
Freund, B.; Tromsdorf, U. I.; Bruns, O. T.; Heine, M.; Giemsa, A.; Bartelt, A.; Salmen, S. C.; Raabe, N.; Heeren, J.; Ittrich, H. et al. A simple and widely applicable method to 59Fe-radiolabel monodisperse superparamagnetic iron oxide nanoparticles for in vivo quantification studies. ACS Nano 2012, 6, 7318-7325.
Crossref Google Scholar
[31]
Singh, S. P.; Rahman, M. F.; Murty, U. S. N.; Mahboob, M.; Grover, P. Comparative study of genotoxicity and tissue distribution of nano and micron sized iron oxide in rats after acute oral treatment. Toxicol. Appl. Pharmacol. 2013, 266, 56-66.
Crossref Google Scholar
[32]
Gu, L.; Fang, R. H.; Sailor, M. J.; Park, J. H. In vivo clearance and toxicity of monodisperse iron oxide nanocrystals. ACS Nano 2012, 6, 4947-4954.
Crossref Google Scholar
[33]
Mazuel, F.; Espinosa, A.; Luciani, N.; Reffay, M.; Le Borgne, R.; Motte, L.; Desboeufs, K.; Michel, A.; Pellegrino, T.; Lalatonne, Y. et al. Massive intracellular biodegradation of iron oxide nanoparticles evidenced magnetically at single-endosome and tissue levels. ACS Nano 2016, 10, 7627-7638.
Crossref Google Scholar
[34]
Plan Sangnier, A.; Van De Walle, A. B.; Curcio, A.; Le Borgne, R.; Motte, L.; Lalatonne, Y.; Wilhelm, C. Impact of magnetic nanoparticle surface coating on their long-term intracellular biodegradation in stem cells. Nanoscale 2019, 11, 16488-16498.
Crossref Google Scholar
[35]
Van De Walle, A.; Plan Sangnier, A.; Abou-Hassan, A.; Curcio, A.; Hémadi, M.; Menguy, N.; Lalatonne, Y.; Luciani, N.; Wilhelm, C. Biosynthesis of magnetic nanoparticles from nano-degradation products revealed in human stem cells. Proc. Natl. Acad. Sci. USA 2019, 116, 4044-4053.
Crossref Google Scholar
[36]
Hemery, G.; Garanger, E.; Lecommandoux, S.; Wong, A. D.; Gillies, E. R.; Pedrono, B.; Bayle, T.; Jacob, D.; Sandre, O. Thermosensitive polymer-grafted iron oxide nanoparticles studied by in situ dynamic light backscattering under magnetic hyperthermia. J. Phys. D.: Appi. Phys. 2015, 48, 494001.
Crossref Google Scholar
[37]
Wang, L.; Wang, Z. J.; Li, X. M.; Zhang, Y.; Yin, M.; Li, J.; Song, H. Y.; Shi, J. Y.; Ling, D. S.; Wang, L. H. et al. Deciphering active biocompatibility of iron oxide nanoparticles from their intrinsic antagonism. Nano Res. 2018, 11, 2746-2755.
Crossref Google Scholar
[38]
Wilhelm, C.; Gazeau, F. Universal cell labelling with anionic magnetic nanoparticles. Biomaterials 2008, 29, 3161-3174.
Crossref Google Scholar
[39]
Negi, H.; Takeuchi, S.; Kamei, N.; Yanada, S.; Adachi, N.; Ochi, M. In vitro safety and quality of magnetically labeled human mesenchymal stem cells preparation for cartilage repair. Tissue Eng. Part C: Methods 2019, 25, 324-333.
Crossref Google Scholar
[40]
Van De Walle, A.; Faissal, W.; Wilhelm, C.; Luciani, N. Role of growth factors and oxygen to limit hypertrophy and impact of high magnetic nanoparticles dose during stem cell chondrogenesis. Comput. Struct. Biotechnol. J. 2018, 16, 532-542.
Crossref Google Scholar
[41]
Chang, Y. K.; Liu, Y. P.; Ho, J. H.; Hsu, S. C.; Lee, O. K. Amine-surface-modified superparamagnetic iron oxide nanoparticles interfere with differentiation of human mesenchymal stem cells. J. Orthop. Res. 2012, 30, 1499-1506.
Crossref Google Scholar
[42]
Chen, Y. C.; Hsiao, J. K.; Liu, H. M.; Lai, I. Y.; Yao, M.; Hsu, S. C.; Ko, B. S.; Chen, Y. C.; Yang, C. S.; Huang, D. M. The inhibitory effect of superparamagnetic iron oxide nanoparticle (Ferucarbotran) on osteogenic differentiation and its signaling mechanism in human mesenchymal stem cells. Toxicol. Appl. Pharmacol. 2010, 245, 272-279.
Crossref Google Scholar
[43]
Huang, D. M.; Hsiao, J. K.; Chen, Y. C.; Chien, L. Y.; Yao, M.; Chen, Y. K.; Ko, B. S.; Hsu, S. C.; Tai, L. A.; Cheng, H. Y. The promotion of human mesenchymal stem cell proliferation by superparamagnetic iron oxide nanoparticles. Biomaterials 2009, 30, 3645-3651.
Crossref Google Scholar
[44]
Roeder, E.; Henrionnet, C.; Goebel, J. C.; Gambier, N.; Beuf, O.; Grenier, D.; Chen, B. L.; Vuissoz, P. A.; Gillet, P.; Pinzano, A. Dose-response of superparamagnetic iron oxide labeling on mesenchymal stem cells chondrogenic differentiation: A multi-scale in vitro study. PLoS One 2014, 9, e98451.
Crossref Google Scholar
[45]
Nikitin, P. I.; Vetoshko, P. M.; Ksenevich, T. I. New type of biosensor based on magnetic nanoparticle detection. J. Magn. Magn. Mater. 2007, 311, 445-449.
Crossref Google Scholar
[46]
Lenglet, L.; Motte, L. Neel effect: Exploiting the nonlinear behavior of superparamagnetic nanoparticles for applications in life sciences up to electrical engineering. In Novel Magnetic Nanostructures. Domracheva, N.; Caporali, M.; Rentschler, E., Eds.; Elsevier: Amsterdam, 2018; pp 247-265.
Crossref
[47]
Richard, S.; Eder, V.; Caputo, G.; Journé, C.; Ou, P.; Bolley, J.; Louedec, L.; Guenin, E.; Motte, L.; Pinna, N. et al. USPIO size control through microwave nonaqueous sol-gel method for neoangiogenesis T2 MRI contrast agent. Nanomedicine (Lond) 2016, 11, 2769-2779.
Crossref Google Scholar
[48]
Motte, L.; Benyettou, F.; De Beaucorps, C.; Lecouvey, M.; Milesovic, I.; Lalatonne, Y. Multimodal superparamagnetic nanoplatform for clinical applications: Immunoassays, imaging & therapy. Faraday Discuss. 2011, 149, 211-225.
Crossref Google Scholar
[49]
Kostura, L.; Kraitchman, D. L.; Mackay, A. M.; Pittenger, M. F.; Bulte, J. W. M. Feridex labeling of mesenchymal stem cells inhibits chondrogenesis but not adipogenesis or osteogenesis. NMR Biomed. 2004, 17, 513-517.
Crossref Google Scholar
[50]
Assa, F.; Jafarizadeh-Malmiri, H.; Ajamein, H.; Anarjan, N.; Vaghari, H.; Sayyar, Z.; Berenjian, A. A biotechnological perspective on the application of iron oxide nanoparticles. Nano Res. 2016, 9, 2203-2225.
Crossref Google Scholar
[51]
Tamion, A.; Hillenkamp, M.; Hillion, A.; Maraloiu, V. A.; Vlaicu, I. D.; Stefan, M.; Ghica, D.; Rositi, H.; Chauveau, F.; Blanchin, M. G. et al. Ferritin surplus in mouse spleen 14 months after intravenous injection of iron oxide nanoparticles at clinical dose. Nano Res. 2016, 9, 2398-2410.
Crossref Google Scholar
[52]
Nikitin, P. I.; Vetoshko, P. M.; Ksenevich, T. I. Magnetic immunoassays. Sens. Lett. 2007, 5, 296-299.
Crossref Google Scholar
[53]
Guénin, E.; Lalatonne, Y.; Bolley, J.; Milosevic, I.; Platas-Iglesias, C.; Motte, L. Catechol versus bisphosphonate ligand exchange at the surface of iron oxide nanoparticles: Towards multi-functionalization. J. Nanopart. Res. 2014, 16, 2596.
Crossref Google Scholar
[54]
Milosevic, I.; Warmont, F.; Lalatonne, Y.; Motte, L. Magnetic metrology for iron oxide nanoparticle scaled-up synthesis. RSC Adv. 2014, 4, 49086-49089.
Crossref Google Scholar
[55]
Geinguenaud, F.; Souissi, I.; Fagard, R.; Motte, L.; Lalatonne, Y. Electrostatic assembly of a DNA superparamagnetic nano-tool for simultaneous intracellular delivery and in situ monitoring. Nanomedicine 2012, 8, 1106-1115.
Crossref Google Scholar
[56]
Geinguenaud, F.; Souissi, I.; Fagard, R.; Lalatonne, Y.; Motte, L. Easily controlled grafting of oligonucleotides on γFe2O3 Nanoparticles: Physicochemical characterization of DNA organization and biological activity studies. J. Phys. Chem. B 2014, 118, 1535-1544.
Crossref Google Scholar
[57]
Benyettou, F.; Fahs, H.; Elkharrag, R.; Bilbeisi, R. A.; Asma, B.; Rezgui, R.; Motte, L.; Magzoub, M.; Brandel, J.; Olsen, J. C. et al. Selective growth inhibition of cancer cells with doxorubicin-loaded CB[7]-modified iron-oxide nanoparticles. RSC Adv. 2017, 7, 23827-23834.
Crossref Google Scholar
[58]
Nikitin, M. P.; Vetoshko, P. M.; Brusentsov, N. A.; Nikitin, P. I. Highly sensitive room-temperature method of non-invasive in vivo detection of magnetic nanoparticles. J. Magn. Magn. Mater. 2009, 321, 1658-1661.
Crossref Google Scholar
[59]
Nikitin, M.; Yuriev, M.; Brusentsov, N.; Vetoshko, P.; Nikitin, P. Non-invasive in vivo mapping and long-term monitoring of magnetic nanoparticles in different organs of animals. AIP Conf. Proc. 2010, 1311, 452-457.
Crossref Google Scholar
[60]
De Montferrand, C.; Hu, L.; Milosevic, I.; Russier, V.; Bonnin, D.; Motte, L.; Brioude, A.; Lalatonne, Y. Iron oxide nanoparticles with sizes, shapes and compositions resulting in different magnetization signatures as potential labels for multiparametric detection. Acta Biomater. 2013, 9, 6150-6157.
Crossref Google Scholar
[61]
Arbab, A. S.; Wilson, L. B.; Ashari, P.; Jordan, E. K.; Lewis, B. K.; Frank, J. A. A model of lysosomal metabolism of dextran coated superparamagnetic iron oxide (SPIO) nanoparticles: Implications for cellular magnetic resonance imaging. NMR Biomed. 2005, 18, 383-389.
Crossref Google Scholar
[62]
Gutiérrez, L.; Romero, S.; Da Silva, G. B.; Costo, R.; Vargas, M. D.; Ronconi, C. M.; Serna, C. J.; Veintemillas-Verdaguer, S.; Del Puerto Morales, M. Degradation of magnetic nanoparticles mimicking lysosomal conditions followed by AC susceptibility. Biomed. Tech. (Berl) 2015, 60, 417-425.
Crossref Google Scholar
[63]
Soenen, S. J. H.; Himmelreich, U.; Nuytten, N.; Pisanic II, T. R.; Ferrari, A.; De Cuyper, M. Intracellular nanoparticle coating stability determines nanoparticle diagnostics efficacy and cell functionality. Small 2010, 6, 2136-2145.
Crossref Google Scholar
[64]
Garcés, V.; Rodríguez-Nogales, A.; González, A.; Gálvez, N.; Rodríguez-Cabezas, M. E.; García-Martin, M. L.; Gutiérrez, L.; Rondón, D.; Olivares, M.; Gálvez, J. et al. Bacteria-carried iron oxide nanoparticles for treatment of anemia. Bioconjugate Chem. 2018, 29, 1785-1791.
Crossref Google Scholar
Nano Research
Volume 13 Issue 2,
February 2020
Pages 467-476
DOI: 10.1007/s12274-020-2631-1
Cite this article:
Van de Walle A, Fromain A, Sangnier AP, et al. Real-time in situ magnetic measurement of the intracellular biodegradation of iron oxide nanoparticles in a stem cell-spheroid tissue model. Nano Research, 2020, 13(2): 467-476. https://doi.org/10.1007/s12274-020-2631-1
Topics:
BiodegradationCytologyIron oxidesMagnetic sensorsMedical nanotechnologyNanoparticlesStem cellsTissue

750

Views

16

Crossref

N/A

Web of Science

15

Scopus

0

CSCD

Altmetrics
Received: 21 November 2019
Revised: 19 December 2019
Accepted: 27 December 2019
Published: 18 January 2020
© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature 2020
Return