magnetic polyion complex micelle; cytotoxicity; cell internalization
Abstract :
[en] Magnetic nanoparticles (MNPs) of magnetite (Fe3O4) were prepared using a polystyrene-graft-poly(2-vinylpyridine) copolymer (denoted G0PS-g-P2VP or G1) as template. These MNPs were subjected to self-assembly with a poly(acrylic acid)-block-poly(2-hydroxyethyl acrylate) double-hydrophilic block copolymer (DHBC), PAA-b-PHEA, to form water-dispersible magnetic polyion complex (MPIC) micelles. Large Fe3O4 crystallites were visualized by transmission electron microscopy (TEM) and magnetic suspensions of MPIC micelles exhibited improved colloidal stability in aqueous environments over a wide pH and ionic strength range. L929 and U87 cell lines incubated for 48 h with MPIC micelles at the highest concentration (1250 µg of Fe3O4 per mL) had a cell viability of 91%, as compared with 51% when incubated with bare (unprotected) MNPs. Cell internalization, visualized by confocal laser scanning microscopy (CLSM) and TEM, exhibited strong dependence on the MPIC micelle concentration and incubation time, as also evidenced by fluorescence-activated cell sorting (FACS). The usefulness of MPIC micelles for cellular radiofrequency magnetic field hyperthermia (MFH) was also confirmed, as the MPIC micelles showed a dual dose-dependent effect (concentration and duration of magnetic field exposure) on the viability of L929 mouse fibroblasts and U87 human glioblastoma epithelial cells.
Research Center/Unit :
MolSys - Molecular Systems - ULiège
Disciplines :
Life sciences: Multidisciplinary, general & others
Author, co-author :
Nguyen, Vo Thu An; University Bordeaux > UMR 5629 > Laboratoire de Chimie des Polymères Organiques
Gillet, Marie-Claire ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Histologie - Cytologie
Gauthier, Mario; University of Waterloo > Department of Chemistry
Sandre, Olivier; University Bordeaux > CNRS > Laboratoire de Chimie des Polymères Organiques
Language :
English
Title :
Magnetic Polyion Complex Micelles for Cell Toxicity Induced by Radiofrequency Magnetic Field Hyperthermia
Publication date :
06 December 2018
Journal title :
Nanomaterials
eISSN :
2079-4991
Publisher :
MDPI AG, Basel, Switzerland
Special issue title :
Magnetic Nanoparticles in Biological Applications
Volume :
8
Issue :
12
Pages :
1014
Peer reviewed :
Peer Reviewed verified by ORBi
Name of the research project :
Multifunctional Nanoparticles for Magnetic Hyperthermia and Indirect Radiation Therapy
Mancarella, S.; Greco, V.; Baldassarre, F.; Vergara, D.; Maffia, M.; Leporatti, S. Polymer-Coated Magnetic Nanoparticles for Curcumin Delivery to Cancer Cells. Macromol. Biosci. 2015, 15, 1365–1374. [CrossRef]
Estelrich, J.; Escribano, E.; Queralt, J.; Busquets, M. Iron Oxide Nanoparticles for Magnetically-Guided and Magnetically-Responsive Drug Delivery. Int. J. Mol. Sci. 2015, 16, 8070–8101. [CrossRef]
Mertz, D.; Sandre, O.; Bégin-Colin, S. Drug releasing nanoplatforms activated by alternating magnetic fields. Biochim. Biophys. Acta (BBA) Gen. Subj. 2017, 1861, 1617–1641. [CrossRef] [PubMed]
Corti, M.; Lascialfari, A.; Micotti, E.; Castellano, A.; Donativi, M.; Quarta, A.; Cozzoli, P.D.; Manna, L.; Pellegrino, T.; Sangregorio, C. Magnetic properties of novel superparamagnetic MRI contrast agents based on colloidal nanocrystals. J. Magn. Magn. Mater. 2008, 320, e320–e323. [CrossRef]
Laurent, S.; Forge, D.; Port, M.; Roch, A.; Robic, C.; Vander Elst, L.; Muller, R.N. Magnetic Iron Oxide Nanoparticles: Synthesis, Stabilization, Vectorization, Physicochemical Characterizations, and Biological Applications. Chem. Rev. 2008, 108, 2064–2110. [CrossRef] [PubMed]
Gupta, A.K.; Gupta, M. Synthesis and Surface Engineering of Iron Oxide Nanoparticles for Biomedical Applications. Biomaterials 2005, 26, 3995–4021. [CrossRef] [PubMed]
Hervault, A.; Thanh, N.T.K. Magnetic nanoparticle-based therapeutic agents for thermo-chemotherapy treatment of cancer. Nanoscale 2014, 6, 11553–11573. [CrossRef] [PubMed]
Périgo, E.A.; Hemery, G.; Sandre, O.; Ortega, D.; Garaio, E.; Plazaola, F.; Teran, F.J. Fundamentals and advances in magnetic hyperthermia. Appl. Phys. Rev. 2015, 2, 041302. [CrossRef]
Massart, R.; Cabuil, V. Effect of Some Parameters on the Formation of Colloidal Magnetite in Alkaline Medium: Yield and Particle Size Control. J. Chim. Phys.Phys.-Chim. Biol. 1987, 84, 967–973. [CrossRef]
Akbarzadeh, A.; Samiei, M.; Davaran, S. Magnetic Nanoparticles: Preparation, Physical Properties, and Applications In Biomedicine. Nanoscale Res. Lett. 2012, 7, 1–13. [CrossRef]
Nguyen, V.T.A.; Gauthier, M.; Sandre, O. Templated Synthesis of Magnetic Nanoparticles Through the Self-Assembly of Polymers and Surfactants. Nanomaterials 2014, 4, 628–685. [CrossRef] [PubMed]
Gauthier, M.; Munam, A. Arborescent Polystyrene-graft-Poly(2-vinylpyridine) Copolymers: Solution Polyelectrolyte Behavior. RSC Adv. 2012, 2, 3100–3108. [CrossRef]
Bae, J.-E.; Huh, M.-I.; Ryu, B.-K.; Do, J.-Y.; Jin, S.-U.; Moon, M.-J.; Jung, J.-C.; Chang, Y.; Kim, E.; Chi, S.-G.; et al. The effect of static magnetic fields on the aggregation and cytotoxicity of magnetic nanoparticles. Biomaterials 2011, 32, 9401–9414. [CrossRef] [PubMed]
Wilhelm, C.; Billotey, C.; Roger, J.; Pons, J.N.; Bacri, J.C.; Gazeau, F. Intracellular Uptake of Anionic Superparamagnetic Nanoparticles as a Function of Their Surface Coating. Biomaterials 2003, 24, 1001–1011. [CrossRef]
Gupta, A.K.; Wells, S. Surface-Modified Superparamagnetic Nanoparticles for Drug Delivery: Preparation, Characterization, and Cytotoxicity Studies. IEEE Trans. NanoBiosc. 2004, 3, 66–73. [CrossRef]
Hahn, P.F.; Stark, D.D.; Lewis, J.M.; Saini, S.; Elizondo, G.; Weissleder, R.; Fretz, C.J.; Ferrucci, J.T. First Clinical Trial of a New Superparamagnetic Iron Oxide for Use as an Oral Gastrointestinal Contrast Agent in MR Imaging. Radiology 1990, 175, 695–700. [CrossRef]
Cole, A.J.; Yang, V.C.; David, A.E. Cancer theranostics: The rise of targeted magnetic nanoparticles. Trends Biotechnol. 2011, 29, 323–332. [CrossRef]
Wang, Y.-X.; Hussain, S.; Krestin, G. Superparamagnetic Iron Oxide Contrast Agents: Physicochemical Characteristics and Applications in MR Imaging. Eur. Radiol. 2001, 11, 2319–2331. [CrossRef]
Berry, C.C.; Wells, S.; Charles, S.; Curtis, A.S.G. Dextran and Albumin Derivatised Iron Oxide Nanoparticles: Influence on Fibroblasts In Vitro. Biomaterials 2003, 24, 4551–4557. [CrossRef]
Pisanic Ii, T.R.; Blackwell, J.D.; Shubayev, V.I.; Fiñones, R.R.; Jin, S. Nanotoxicity of iron oxide nanoparticle internalization in growing neurons. Biomaterials 2007, 28, 2572–2581. [CrossRef] [PubMed]
Laurent, S.; Burtea, C.; Thirifays, C.; Häfeli, U.O.; Mahmoudi, M. Crucial Ignored Parameters on Nanotoxicology: The Importance of Toxicity Assay Modifications and “Cell Vision”. PLoS ONE 2012, 7, e29997. [CrossRef] [PubMed]
Kurlyandskaya, V.G.; Litvinova, S.L.; Safronov, P.A.; Schupletsova, V.V.; Tyukova, S.I.; Khaziakhmatova, G.O.; Slepchenko, B.G.; Yurova, A.K.; Cherempey, G.E.; Kulesh, A.N.; et al. Water-Based Suspensions of Iron Oxide Nanoparticles with Electrostatic or Steric Stabilization by Chitosan: Fabrication, Characterization and Biocompatibility. Sensors 2017, 17, 2605. [CrossRef] [PubMed]
Soenen, S.J.; De Cuyper, M. Assessing iron oxide nanoparticle toxicity in vitro: Current status and future prospects. Nanomedicine 2010, 5, 1261–1275. [CrossRef] [PubMed]
Nguyen, V.T.A.; Gillet, M.-C.D.-P.; Gauthier, M.; Sandre, O. Biocompatible Polyion Complex Micelles Synthesized from Arborescent Polymers. Langmuir 2016, 32, 13482–13492. [CrossRef] [PubMed]
Huang, Y.-S.; Bertrand, V.; Bozukova, D.; Pagnoulle, C.; Labrugère, C.; De Pauw, E.; De Pauw-Gillet, M.-C.; Durrieu, M.-C. RGD Surface Functionalization of the Hydrophilic Acrylic Intraocular Lens Material to Control Posterior Capsular Opacification. PLoS ONE 2014, 9, e114973. [CrossRef]
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]
Fortin, J.-P.; Gazeau, F.; Wilhelm, C. Intracellular Heating of Living Cells through Néel Relaxation of Magnetic Nanoparticles. Eur. Biophys. J. 2008, 37, 223–228. [CrossRef]
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 Appl. Phys. 2015, 48, 494001. [CrossRef]
Liu, J.; Detrembleur, C.; Debuigne, A.; De Pauw-Gillet, M.-C.; Mornet, S.; Vander Elst, L.; Laurent, S.; Labrugère, C.; Duguet, E.; Jérôme, C. Poly(acrylic acid)-block-poly(vinyl alcohol) anchored maghemite nanoparticles designed for multi-stimuli triggered drug release. Nanoscale 2013, 5, 11464–11477. [CrossRef]
Tsourkas, A.; Josephson, L. Magnetic Nanoparticles. In Molecular Imaging: Principles and Practice; Weissleder, R., Ross, B.D., Rehemtulla, A., Gambhir, S.S., Eds.; People’s Medical Publishing House-USA: Shelton, CT, USA, 2010; pp. 523–541.
Ortega, D. Structure and Magnetism in Magnetic Nanoparticles. In Magnetic Nanoparticles From Fabrication to Clinical Applications; Thanh, N.T., Ed.; CRC Press; Taylor & Francis Group: Boca Raton, FL, USA, 2012; pp. 3–44.
Zhu, R.; Jiang, W.; Pu, Y.; Luo, K.; Wu, Y.; He, B.; Gu, Z. Functionalization of Magnetic Nanoparticles with Peptide Dendrimers. J. Mater. Chem. 2011, 21, 5464–5474. [CrossRef]
Shang, H.; Chang, W.-S.; Kan, S.; Majetich, S.A.; Lee, G.U. Synthesis and Characterization of Paramagnetic Microparticles through Emulsion-Templated Free Radical Polymerization. Langmuir 2006, 22, 2516–2522. [CrossRef] [PubMed]
Zhang, Q.; Wang, C.; Qiao, L.; Yan, H.; Liu, K. Superparamagnetic Iron Oxide Nanoparticles Coated with a Folate-Conjugated Polymer. J. Mater. Chem. 2009, 19, 8393–8402. [CrossRef]
Arosio, P.; Thevenot, J.; Orlando, T.; Orsini, F.; Corti, M.; Mariani, M.; Bordonali, L.; Innocenti, C.; Sangregorio, C.; Oliveira, H.; et al. Hybrid Iron Oxide-Copolymer Micelles and Vesicles as Contrast Agents for MRI: Impact of the Nanostructure on the Relaxometric Properties. J. Mater. Chem. B 2013, 1, 5317–5328. [CrossRef]
Magonov, S.N.; Elings, V.; Whangbo, M.H. Phase Imaging and Stiffness in Tapping-Mode Atomic Force Microscopy. Surf. Sci. 1997, 375, L385–L391. [CrossRef]
Leclère, P.; Lazzaroni, R.; Brédas, J.L.; Yu, J.M.; Dubois, P.; Jérôme, R. Microdomain Morphology Analysis of Block Copolymers by Atomic Force Microscopy with Phase Detection Imaging. Langmuir 1996, 12, 4317–4320. [CrossRef]
Safi, M.; Courtois, J.; Seigneuret, M.; Conjeaud, H.; Berret, J.F. The effects of aggregation and protein corona on the cellular internalization of iron oxide nanoparticles. Biomaterials 2011, 32, 9353–9363. [CrossRef]
Gupta, A.K.; Gupta, M. Cytotoxicity Suppression and Cellular Uptake Enhancement of Surface Modified Magnetic Nanoparticles. Biomaterials 2005, 26, 1565–1573. [CrossRef]
Petri-Fink, A.; Chastellain, M.; Juillerat-Jeanneret, L.; Ferrari, A.; Hofmann, H. Development of Functionalized Superparamagnetic Iron Oxide Nanoparticles for Interaction with Human Cancer Cells. Biomaterials 2005, 26, 2685–2694. [CrossRef] [PubMed]
Wan, S.; Huang, J.; Guo, M.; Zhang, H.; Cao, Y.; Yan, H.; Liu, K. Biocompatible Superparamagnetic Iron Oxide Nanoparticle Dispersions Stabilized with Poly(ethylene glycol)–Oligo(aspartic acid) Hybrids. J. Biomed. Mater. Res. Part A 2007, 80A, 946–954. [CrossRef] [PubMed]
Cole, A.J.; David, A.E.; Wang, J.; Galbán, C.J.; Yang, V.C. Magnetic brain tumor targeting and biodistribution of long-circulating PEG-modified, cross-linked starch-coated iron oxide nanoparticles. Biomaterials 2011, 32, 6291–6301. [CrossRef] [PubMed]
Lamanna, G.; Kueny-Stotz, M.; Mamlouk-Chaouachi, H.; Ghobril, C.; Basly, B.; Bertin, A.; Miladi, I.; Billotey, C.; Pourroy, G.; Begin-Colin, S.; et al. Dendronized iron oxide nanoparticles for multimodal imaging. Biomaterials 2011, 32, 8562–8573. [CrossRef] [PubMed]
Soenen, S.J.; Himmelreich, U.; Nuytten, N.; Pisanic, T.R.; Ferrari, A.; De Cuyper, M. Intracellular Nanoparticle Coating Stability Determines Nanoparticle Diagnostics Efficacy and Cell Functionality. Small 2010, 6, 2136–2145. [CrossRef]
Lu, C.-W.; Hung, Y.; Hsiao, J.-K.; Yao, M.; Chung, T.-H.; Lin, Y.-S.; Wu, S.-H.; Hsu, S.-C.; Liu, H.-M.; Mou, C.-Y.; et al. Bifunctional Magnetic Silica Nanoparticles for Highly Efficient Human Stem Cell Labeling. Nano Lett. 2006, 7, 149–154. [CrossRef]
Sanchez, C.; El Hajj Diab, D.; Connord, V.; Clerc, P.; Meunier, E.; Pipy, B.; Payré, B.; Tan, R.P.; Gougeon, M.; Carrey, J.; et al. Targeting a G-Protein-Coupled Receptor Overexpressed in Endocrine Tumors by Magnetic Nanoparticles To Induce Cell Death. ACS Nano 2014, 8, 1350–1363. [CrossRef]
Asin, L.; Goya, G.F.; Tres, A.; Ibarra, M.R. Induced Cell Toxicity Originates Dendritic Cell Death Following Magnetic Hyperthermia Treatment. Cell Death Dis. 2013, 4, e596. [CrossRef]
Song, C.W. Effect of Local Hyperthermia on Blood Flow and Microenvironment: A Review. Cancer Res. 1984, 44, 4721s–4730s.
Petryk, A.A.; Giustini, A.J.; Gottesman, R.E.; Trembly, B.S.; Hoopes, P.J. Comparison of magnetic nanoparticle and microwave hyperthermia cancer treatment methodology and treatment effect in a rodent breast cancer model. Int. J. Hyperth. 2013, 29, 819–827. [CrossRef]
Kolosnjaj-Tabi, J.; Di Corato, R.; Lartigue, L.; Marangon, I.; Guardia, P.; Silva, A.K.A.; Luciani, N.; Clément, O.; Flaud, P.; Singh, J.V.; et al. Heat-Generating Iron Oxide Nanocubes: Subtle “Destructurators” of the Tumoral Microenvironment. ACS Nano 2014, 8, 4268–4283. [CrossRef] [PubMed]
Creixell, M.; Bohórquez, A.C.; Torres-Lugo, M.; Rinaldi, C. EGFR-Targeted Magnetic Nanoparticle Heaters Kill Cancer Cells without a Perceptible Temperature Rise. ACS Nano 2011, 5, 7124–7129. [CrossRef] [PubMed]
Rabin, Y. Is intracellular hyperthermia superior to extracellular hyperthermia in the thermal sense? Int. J. Hyperth. 2002, 18, 194–202. [CrossRef] [PubMed]
Baffou, G.; Rigneault, H.; Marguet, D.; Jullien, L. A critique of methods for temperature imaging in single cells. Nat. Methods 2014, 11, 899–901. [CrossRef] [PubMed]
Connord, V.; Clerc, P.; Hallali, N.; El Hajj Diab, D.; Fourmy, D.; Gigoux, V.; Carrey, J. Real-Time Analysis of Magnetic Hyperthermia Experiments on Living Cells under a Confocal Microscope. Small 2015, 11, 2437–2445. [CrossRef]
Wydra, R.J.; Rychahou, P.G.; Evers, B.M.; Anderson, K.W.; Dziubla, T.D.; Hilt, J.Z. The role of ROS generation from magnetic nanoparticles in an alternating magnetic field on cytotoxicity. Acta Biomater. 2015, 25, 284–290. [CrossRef] [PubMed]
Sanz, B.; Calatayud, M.P.; Torres, T.E.; Fanarraga, M.L.; Ibarra, M.R.; Goya, G.F. Magnetic hyperthermia enhances cell toxicity with respect to exogenous heating. Biomaterials 2017, 114, 62–70. [CrossRef]
