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Photothermal Depletion of Cancer-Associated Fibroblasts Normalizes Tumor Stiffness in Desmoplastic Cholangiocarcinoma

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    Photothermal Depletion of Cancer-Associated Fibroblasts Normalizes Tumor Stiffness in Desmoplastic Cholangiocarcinoma
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    • Alba Nicolás-Boluda
      Alba Nicolás-Boluda
      Laboratoire Matière et Systèmes Complexes (MSC), Université de Paris, CNRS-UMR 7057, Paris 75013, France
      Institut Cochin, Université de Paris, INSERM U1016/CNRS UMR 8104, Paris 75014, France
      More by Alba Nicolás-Boluda
    • Javier Vaquero
      Javier Vaquero
      Sorbonne Université, INSERM, Centre de Recherche Saint-Antoine, CRSA, Paris 75012, France
      Oncobell Program, Bellvitge Biomedical Research Institute (IDIBELL), Barcelona, Spain
      CIBEREHD, National Biomedical Research Institute on Liver and Gastrointestinal Diseases, Instituto de Salud Carlos III, Madrid, Spain
      More by Javier Vaquero
    • Gautier Laurent
      Gautier Laurent
      Institut UTINAM, CNRS UMR 6213, Université Bourgogne Franche-Comté, Besançon 25010, France
      More by Gautier Laurent
    • Gilles Renault
      Gilles Renault
      Institut Cochin, Université de Paris, INSERM U1016/CNRS UMR 8104, Paris 75014, France
      More by Gilles Renault
    • Rana Bazzi
      Rana Bazzi
      Institut UTINAM, CNRS UMR 6213, Université Bourgogne Franche-Comté, Besançon 25010, France
      More by Rana Bazzi
    • Emmanuel Donnadieu
      Emmanuel Donnadieu
      Institut Cochin, Université de Paris, INSERM U1016/CNRS UMR 8104, Paris 75014, France
      More by Emmanuel Donnadieu
    • Stéphane Roux
      Stéphane Roux
      Institut UTINAM, CNRS UMR 6213, Université Bourgogne Franche-Comté, Besançon 25010, France
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      Orcidhttp://orcid.org/0000-0002-5198-1916
    • Laura Fouassier*
      Laura Fouassier
      Sorbonne Université, INSERM, Centre de Recherche Saint-Antoine, CRSA, Paris 75012, France
      *Email: [email protected]
      More by Laura Fouassier
    • Florence Gazeau*
      Florence Gazeau
      Laboratoire Matière et Systèmes Complexes (MSC), Université de Paris, CNRS-UMR 7057, Paris 75013, France
      *Email: [email protected]
      More by Florence Gazeau
      Orcidhttp://orcid.org/0000-0002-6482-3597
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    ACS Nano

    Cite this: ACS Nano 2020, 14, 5, 5738–5753
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    https://doi.org/10.1021/acsnano.0c00417
    Published April 27, 2020
    Copyright © 2020 American Chemical Society
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    Abstract

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    Physical oncology recognizes tissue stiffness mediated by activation of cancer-associated fibroblasts (CAF) and extracellular matrix remodeling as an active modulator of tumorigenesis, treatment resistance, and clinical outcome. Cholangiocarcinoma (CCA) is a highly aggressive and chemoresistant desmoplastic cancer enriched in CAF. CCA’s stroma mechanical properties are considered responsible for its chemoresistant character. To normalize tumor mechanics, we propose a physical strategy based on remotely light-activated nanohyperthermia to modulate the tumor microenvironment. In this study, we report the use of multifunctional iron oxide nanoflowers decorated with gold nanoparticles (GIONF) as efficient nanoheaters to achieve complete tumor regression following three sessions of mild hyperthermia. The preferential uptake of GIONF by CAF allowed targeting this cell population, which resulted in a significant early reduction of tumor stiffness followed by tumor regression. In conclusion, our study highlights a spatially and temporally controlled physical strategy, GIONF-mediated photothermal therapy to deplete CAF and normalize the tumor mechanics that may apply to desmoplastic cancer and CCA treatment.

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    • Supplementary Figures S1–S9 . Figure S1, UV–vis-NIR absorption spectra of GIONF and IONF at different concentrations. Figure S2, IONF and GIONF are not cytotoxic to EGI-1, hTERT-HSC, RAW 264.7 and HUVEC cells. Figure S3, GIONF and IONF do not induce hemolysis in red blood cells. Figure S4, Quantification of gold in EGI-1 cells by ICP-AES. Figure S5, Analysis of the components of the stromal compartment in EGI-1 tumor using IHC. Figure S6, Laser power used in the in vivo experiments. Figure S7, Normalized tumor volume of GIONF mediated PTT. Figure S8, Histological (HES, Perls and Sirius Red staining) and IHC (F4/80 and αSMA labeling) analysis of GIONF injected tumors after one PTT session, after the three PTT sessions. Figure S9, GIONF-mediated PTT does not induce collagen denaturation (PDF)

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    Cite this: ACS Nano 2020, 14, 5, 5738–5753
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