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Remote Manipulation of Ligand Nano-Oscillations Regulates Adhesion and Polarization of Macrophages in Vivo
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    Remote Manipulation of Ligand Nano-Oscillations Regulates Adhesion and Polarization of Macrophages in Vivo
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    † # ¶ □ Department of Biomedical Engineering, Department of Orthopaedics and Traumatology, Faculty of Medicine, #Shun Hing Institute of Advanced Engineering, Shenzhen Research Institute, Centre for Novel Biomaterials, The Chinese University of Hong Kong, Hong Kong, China
    ‡ ∥ Department of Materials Science and Engineering, NUANCE Center, Northwestern University, Evanston, Illinois 60208, United States
    § International Institute for Nanotechnology, Evanston, Illinois 60208, United States
    China Orthopedic Regenerative Medicine Group (CORMed), Hangzhou, China
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    Nano Letters

    Cite this: Nano Lett. 2017, 17, 10, 6415–6427
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    https://doi.org/10.1021/acs.nanolett.7b03405
    Published September 6, 2017
    Copyright © 2017 American Chemical Society

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    Macrophages play crucial roles in various immune-related responses, such as host defense, wound healing, disease progression, and tissue regeneration. Macrophages perform distinct and dynamic functions in vivo, depending on their polarization states, such as the pro-inflammatory M1 phenotype and pro-healing M2 phenotype. Remote manipulation of the adhesion of host macrophages to the implants and their subsequent polarization in vivo can be an attractive strategy to control macrophage polarization-specific functions but has rarely been achieved. In this study, we grafted RGD ligand-bearing superparamagnetic iron oxide nanoparticles (SPIONs) to a planar matrix via a long flexible linker. We characterized the nanoscale motion of the RGD-bearing SPIONs grafted to the matrix, in real time by in situ magnetic scanning transmission electron microscopy (STEM) and in situ atomic force microscopy. The magnetic field was applied at various oscillation frequencies to manipulate the frequency-dependent ligand nano-oscillation speeds of the RGD-bearing SPIONs. We demonstrate that a low oscillation frequency of the magnetic field stimulated the adhesion and M2 polarization of macrophages, whereas a high oscillation frequency suppressed the adhesion of macrophages but promoted their M1 polarization, both in vitro and in vivo. Macrophage adhesion was also temporally regulated by switching between the low and high frequencies of the oscillating magnetic field. To the best of our knowledge, this is the first demonstration of the remote manipulation of the adhesion and polarization phenotype of macrophages, both in vitro and in vivo. Our system offers the promising potential to manipulate host immune responses to implanted biomaterials, including inflammation or tissue reparative processes, by regulating macrophage adhesion and polarization.

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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/acs.nanolett.7b03405.

    • Characterizations of the surface charges and chemical bonds of the SPIONs and RGD-bearing SPIONs, the changes in the surface chemistry and surface hydrophilicity for the matrix-grafting of the RGD-bearing SPIONs, characterization control of nanoscale displacement of the matrix-grafted RGD-bearing SPIONs, macrophage adhesion on the oscillating non-RGD-bearing SPIONs, integrin β1 binding analysis to the oscillating RGD-bearing SPIONs, distribution of RGD-bearing SPIONs on the matrix used for in vivo implantation, host macrophage polarization and neutrophils analyses by the quantitative gene expression and immunofluorescent staining with and without the injection of M2-polarizing cytokines (PDF)

    • Movies for the no frequency dependent oscillations of the RGD-bearing SPIONs (AVI)

    • Movies for the low frequency dependent oscillations of the RGD-bearing SPIONs (AVI)

    • Movies for the medium frequency dependent oscillations of the RGD-bearing SPIONs (AVI)

    • Movies for the high frequency dependent oscillations of the RGD-bearing SPIONs (AVI)

    • Movie for the real-time nanoscale motion of the RGD-bearing SPIONs on the matrix by in situ magnetic high-angle annular dark-field scanning transmission electron microscopy (HAADF-STEM) imaging with the setup descriptions (AVI)

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    Nano Letters

    Cite this: Nano Lett. 2017, 17, 10, 6415–6427
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.nanolett.7b03405
    Published September 6, 2017
    Copyright © 2017 American Chemical Society

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