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Brush-Induced Orientation of Collagen Fibers in Layer-by-Layer Nanofilms: A Simple Method for the Development of Human Muscle Fibers

  • Muhammad Haseeb Iqbal
    Muhammad Haseeb Iqbal
    Université de Strasbourg, CNRS, Institut Charles Sadron, UPR 22, Strasbourg Cedex 2, 67034, France
  • Faratiana Jeanne Rosine Revana
    Faratiana Jeanne Rosine Revana
    Université de Strasbourg, CNRS, Institut Charles Sadron, UPR 22, Strasbourg Cedex 2, 67034, France
  • Emeline Pradel
    Emeline Pradel
    Université de Strasbourg, CNRS, Institut Charles Sadron, UPR 22, Strasbourg Cedex 2, 67034, France
  • Varvara Gribova
    Varvara Gribova
    Centre de Recherche en Biomédecine de Strasbourg, Institut National de la Santé et de la Recherche Médicale, UMR 1121, Biomatériaux et Bioingénierie, Strasbourg Cedex, 67085, France
    Université de Strasbourg, Faculté de Chirurgie Dentaire, Strasbourg 67000, France
  • Kamel Mamchaoui
    Kamel Mamchaoui
    Sorbonne Université, INSERM UMRS 974, Centre for Research in Myology, Batiment Babinski, GH Pitié-Salpêtrière 47 bd de l’Hôpital, F-75013 Paris, France
  • Catherine Coirault
    Catherine Coirault
    Sorbonne Université, INSERM UMRS 974, Centre for Research in Myology, Batiment Babinski, GH Pitié-Salpêtrière 47 bd de l’Hôpital, F-75013 Paris, France
  • Florent Meyer
    Florent Meyer
    Centre de Recherche en Biomédecine de Strasbourg, Institut National de la Santé et de la Recherche Médicale, UMR 1121, Biomatériaux et Bioingénierie, Strasbourg Cedex, 67085, France
    Université de Strasbourg, Faculté de Chirurgie Dentaire, Strasbourg 67000, France
  • , and 
  • Fouzia Boulmedais*
    Fouzia Boulmedais
    Université de Strasbourg, CNRS, Institut Charles Sadron, UPR 22, Strasbourg Cedex 2, 67034, France
    *Email: [email protected]
Cite this: ACS Nano 2022, 16, 12, 20034–20043
Publication Date (Web):October 27, 2022
https://doi.org/10.1021/acsnano.2c06329
Copyright © 2022 American Chemical Society

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    Abstract

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    The engineering of skeletal muscle tissue, a highly organized structure of myotubes, is promising for the treatment of muscle injuries and muscle diseases, for replacement, or for pharmacology research. Muscle tissue development involves differentiation of myoblasts into myotubes with parallel orientation, to ultimately form aligned myofibers, which is challenging to achieve on flat surfaces. In this work, we designed hydrogen-bonded tannic acid/collagen layer-by-layer (TA/COL LbL) nanofilms using a simple brushing method to address this issue. In comparison to films obtained by dipping, brushed TA/COL films showed oriented COL fibers of 60 nm diameter along the brushing direction. Built at acidic pH due to COL solubility, TA/COL films released TA in physiological conditions with a minor loss of thickness. After characterization of COL fibers’ orientation, human myoblasts (C25CL48) were seeded on the oriented TA/COL film, ended by COL. After 12 days in a differentiation medium without any other supplement, human myoblasts were able to align on brushed TA/COL films and to differentiate into long aligned myotubes (from hundreds of μm up to 1.7 mm length) thanks to two distinct properties: (i) the orientation of COL fibers guiding myoblasts’ alignment and (ii) the TA release favoring the differentiation. This simple and potent brushing process allows the development of anisotropic tissues in vitro which can be used for studies of drug discovery and screening or the replacement of damaged tissue.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acsnano.2c06329.

    • Optimization of the TA/COL brushing method, AFM topography/cross section of isolated COL fibers on mica, hydrodynamic size of TA, “OrientationJ” color coded analysis of the AFM topography images of brushed and dipped TA/COL films, AFM topography and OrientationJ analysis of oriented (TA/COL)4, (TA/COL)8, and (TA/COL)16, in vitro cytotoxicity of TA on human myoblasts, AFM topography/orientation of oriented TA/COL after 3 days incubation in DMEM medium, myoblasts after 12 days of differentiation on oriented TA/COL and TCPS, morphology of myoblasts after 12 days of differentiation, TA release from the TA/COL films, morphology of isolated nuclei on differentiation day 12, differentiation/orientation of myoblasts oriented TA/COL_PBS films, quantitative information for oriented TA/COL_PBS films and controls on differentiation day 12, and physicochemical characterization of the nonoriented (TA/COL)3 and myoblasts after 12 days of differentiation (PDF)

    • Buildup of brushed TA/COL films performed manually on silicon or glass substrate using a nylon paintbrush at each deposition of TA and COL, alternating with a rinsing step and a drying step (AVI)

    • Myoblasts movement recorded by time-lapse video for the first 48 h in contact with the oriented TA/COL films in the growth medium (AVI)

    • Myoblasts movement recorded by time-lapse video for the first 48 h in contact with the nonoriented TA/COL films in the growth medium (AVI)

    • Myoblasts movement recorded by time-lapse video for the first 48 h in contact with the uncoated glass surface in the growth medium (AVI)

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    Cited By

    This article is cited by 3 publications.

    1. Yan Guo, Xinyue Zhai, Na Li, Xingjie Zan. Recent Progress in Protein-Polyphenol Assemblies for Biomedical Applications. Langmuir 2024, 40 (4) , 2005-2014. https://doi.org/10.1021/acs.langmuir.3c03244
    2. Katsuhiko Ariga. Chemistry of Materials Nanoarchitectonics for Two-Dimensional Films: Langmuir–Blodgett, Layer-by-Layer Assembly, and Newcomers. Chemistry of Materials 2023, 35 (14) , 5233-5254. https://doi.org/10.1021/acs.chemmater.3c01291
    3. Yi-Wei Chen, Muhammad Haseeb Iqbal, Florent Meyer, Vincent Ball, Fouzia Boulmedais. Physical Chemistry Study of Collagen-Based Multilayer Films. Gels 2023, 9 (3) , 192. https://doi.org/10.3390/gels9030192

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