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Confining Iron Oxide Nanocubes inside Submicrometric Cavities as a Key Strategy To Preserve Magnetic Heat Losses in an Intracellular Environment

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    Research Article

    Confining Iron Oxide Nanocubes inside Submicrometric Cavities as a Key Strategy To Preserve Magnetic Heat Losses in an Intracellular Environment
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    • Mikhail V. Zyuzin
      Mikhail V. Zyuzin
      Istituto Italiano di Tecnologia, Via Morego 30, 16163 Genova, Italy
      Faculty of Physics and Engineering, ITMO University, Lomonosova 9, 191023 St. Petersburg, Russia
      More by Mikhail V. Zyuzin
    • Marco Cassani
      Marco Cassani
      Istituto Italiano di Tecnologia, Via Morego 30, 16163 Genova, Italy
      Dipartimento di Chimica, Università di Genova, Via Dodecaneso 33, 16146 Genova, Italy
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    • Markus J. Barthel
      Markus J. Barthel
      Istituto Italiano di Tecnologia, Via Morego 30, 16163 Genova, Italy
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    • Helena Gavilan
      Helena Gavilan
      Istituto Italiano di Tecnologia, Via Morego 30, 16163 Genova, Italy
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    • Niccolò Silvestri
      Niccolò Silvestri
      Istituto Italiano di Tecnologia, Via Morego 30, 16163 Genova, Italy
      Dipartimento di Chimica, Università di Genova, Via Dodecaneso 33, 16146 Genova, Italy
      More by Niccolò Silvestri
    • Alberto Escudero
      Alberto Escudero
      Leibniz Institute for New Materials, Campus D2 2, D-66123 Saarbrücken, Germany
      Departamento de Química Inorgánica and Instituto de Investigaciones Químicas (IIQ), Universidad de Sevilla−CSIC, Calle Américo Vespucio 49, E-41092 Seville, Spain
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      Orcidhttp://orcid.org/0000-0002-0850-6589
    • Alice Scarpellini
      Alice Scarpellini
      Istituto Italiano di Tecnologia, Via Morego 30, 16163 Genova, Italy
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    • Federica Lucchesi
      Federica Lucchesi
      Istituto Italiano di Tecnologia, Via Morego 30, 16163 Genova, Italy
      Dipartimento di Informatica,B ioingegneria, Robotica e Ingegneria dei Sistemi (DIBRIS), Via all’Opera Pia, 13, 16145 Genova, Italy
      More by Federica Lucchesi
    • Francisco J. Teran
      Francisco J. Teran
      iMdea Nanociencia, Campus Universitario de Cantoblanco, 28049 Madrid, Spain
      Nanobiotecnología (iMdea-Nanociencia), Unidad Asociada al Centro Nacional de Biotecnología (CSIC), 28049 Madrid, Spain
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      Orcidhttp://orcid.org/0000-0002-2466-6208
    • Wolfgang J. Parak*
      Wolfgang J. Parak
      Faculty of Physics and Chemistry and CHyN, Universität Hamburg, 20146 Hamburg, Germany
      *E-mail for W.J.P.: [email protected]
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      Orcidhttp://orcid.org/0000-0003-1672-6650
    • Teresa Pellegrino*
      Teresa Pellegrino
      Istituto Italiano di Tecnologia, Via Morego 30, 16163 Genova, Italy
      *E-mail for T.P.: teresa.pellegrino@iit
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      Orcidhttp://orcid.org/0000-0001-5518-1134
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    ACS Applied Materials & Interfaces

    Cite this: ACS Appl. Mater. Interfaces 2019, 11, 45, 41957–41971
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    https://doi.org/10.1021/acsami.9b15501
    Published October 4, 2019
    Copyright © 2019 American Chemical Society
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    Abstract

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    The design of magnetic nanostructures whose magnetic heating efficiency remains unaffected at the tumor site is a fundamental requirement to further advance magnetic hyperthermia in the clinic. This work demonstrates that the confinement of magnetic nanoparticles (NPs) into a sub-micrometer cavity is a key strategy to enable a certain degree of nanoparticle motion and minimize aggregation effects, consequently preserving the magnetic heat loss of iron oxide nanocubes (IONCs) under different conditions, including intracellular environments. We fabricated magnetic layer-by-layer (LbL) self-assembled polyelectrolyte sub-micrometer capsules using three different approaches, and we studied their heating efficiency as obtained in aqueous dispersions and after internalization by tumor cells. First, IONCs were added to the hollow cavities of LbL submicrocapsules, allowing the IONCs to move to a certain extent in the capsule cavities. Second, IONCs were coencapsulated into solid calcium carbonate cores coated with LbL polymer shells. Third, IONCs were incorporated within the polymer layers of the LbL capsule walls. In aqueous solution, higher specific absorption rate (SAR) values were related to those of free IONCs, while lower SAR values were recorded for capsule/core assemblies. However, after uptake by cancer cell lines (SKOV-3 cells), the SAR values of the free IONCs were significantly lower than those observed for capsule/core assemblies, especially after prolonged incubation periods (24 and 48 h). These results show that IONCs packed into submicrocavities preserve the magnetic losses, as the SAR values remained almost invariable. Conversely, free IONCs without the protective capsule shell agglomerated and their magnetic losses were strongly reduced. Indeed, IONC-loaded capsules and free IONCs reside inside endosomal and lysosomal compartments after cellular uptake and show strongly reduced magnetic losses due to the immobilization and aggregation in centrosymmetrical structures in the intracellular vesicles. The confinement of IONCs into sub-micrometer cavities is a key strategy to provide a sustained and predictable heating dose inside biological matrices.

    Copyright © 2019 American Chemical Society

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    Supporting Information

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsami.9b15501.

    • Ligand exchange procedure, synthesis of nitrodopamine, synthesis of α–ω-carboxypoly(ethylene glycol), synthesis of α-N-hydroxysuccinimide-ω-carboxypoly(ethylene glycol), synthesis of α-nitrodopamine-ω-carboxypoly(ethylene glycol), and IONC/capsule characterization, including TEM, DLS, LDA, and bright field microscopy (PDF)

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    This article is cited by 48 publications.

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    ACS Applied Materials & Interfaces

    Cite this: ACS Appl. Mater. Interfaces 2019, 11, 45, 41957–41971
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acsami.9b15501
    Published October 4, 2019
    Copyright © 2019 American Chemical Society
    Request reuse permissions

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