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Mechanistic Insights into Hyaluronic Acid Induced Peptide Nanofiber Organization in Supramolecular Hydrogels

  • Alexis Bigo−Simon
    Alexis Bigo−Simon
    Université de Strasbourg, CNRS, Institut Charles Sadron (UPR22), 23 rue du Loess, 67034 Strasbourg Cedex 2, BP 84047, France
    Université de Strasbourg, Faculté de Chimie, UMR7140, 1 rue Blaise Pascal, 67008 Strasbourg Cedex, France
  • Jennifer Rodon Fores
    Jennifer Rodon Fores
    Université de Strasbourg, CNRS, Institut Charles Sadron (UPR22), 23 rue du Loess, 67034 Strasbourg Cedex 2, BP 84047, France
    Institut National de la Santé et de la Recherche Médicale, INSERM Unité 1121, CRBS, 1 rue Eugène Boeckel, 67000 Strasbourg, France
    Université de Strasbourg, Faculté de Chirurgie Dentaire, 8 rue Sainte Elisabeth, 67000 Strasbourg, France
  • Miryam Criado-Gonzalez
    Miryam Criado-Gonzalez
    Université de Strasbourg, CNRS, Institut Charles Sadron (UPR22), 23 rue du Loess, 67034 Strasbourg Cedex 2, BP 84047, France
    Institut National de la Santé et de la Recherche Médicale, INSERM Unité 1121, CRBS, 1 rue Eugène Boeckel, 67000 Strasbourg, France
    Université de Strasbourg, Faculté de Chirurgie Dentaire, 8 rue Sainte Elisabeth, 67000 Strasbourg, France
  • Lucille Blandin
    Lucille Blandin
    Université de Strasbourg, CNRS, Institut Charles Sadron (UPR22), 23 rue du Loess, 67034 Strasbourg Cedex 2, BP 84047, France
  • Jean-Yves Runser
    Jean-Yves Runser
    Université de Strasbourg, CNRS, Institut Charles Sadron (UPR22), 23 rue du Loess, 67034 Strasbourg Cedex 2, BP 84047, France
    Institut National de la Santé et de la Recherche Médicale, INSERM Unité 1121, CRBS, 1 rue Eugène Boeckel, 67000 Strasbourg, France
    Université de Strasbourg, Faculté de Chirurgie Dentaire, 8 rue Sainte Elisabeth, 67000 Strasbourg, France
  • Bernard Senger
    Bernard Senger
    Institut National de la Santé et de la Recherche Médicale, INSERM Unité 1121, CRBS, 1 rue Eugène Boeckel, 67000 Strasbourg, France
    Université de Strasbourg, Faculté de Chirurgie Dentaire, 8 rue Sainte Elisabeth, 67000 Strasbourg, France
  • Guillaume Fleith
    Guillaume Fleith
    Université de Strasbourg, CNRS, Institut Charles Sadron (UPR22), 23 rue du Loess, 67034 Strasbourg Cedex 2, BP 84047, France
  • Marc Schmutz
    Marc Schmutz
    Université de Strasbourg, CNRS, Institut Charles Sadron (UPR22), 23 rue du Loess, 67034 Strasbourg Cedex 2, BP 84047, France
    More by Marc Schmutz
  • Rachel Schurhammer
    Rachel Schurhammer
    Université de Strasbourg, Faculté de Chimie, UMR7140, 1 rue Blaise Pascal, 67008 Strasbourg Cedex, France
  • Alain Chaumont
    Alain Chaumont
    Université de Strasbourg, Faculté de Chimie, UMR7140, 1 rue Blaise Pascal, 67008 Strasbourg Cedex, France
  • Pierre Schaaf*
    Pierre Schaaf
    Université de Strasbourg, 23 rue du Loess, 67034 Strasbourg Cedex 2, BP 84047, France
    Institut National de la Santé et de la Recherche Médicale, INSERM Unité 1121, CRBS, 1 rue Eugène Boeckel, 67000 Strasbourg, France
    Université de Strasbourg, Faculté de Chirurgie Dentaire, 8 rue Sainte Elisabeth, 67000 Strasbourg, France
    Université de Strasbourg, CNRS, Institut Charles Sadron (UPR22), 23 rue du Loess, 67034 Strasbourg Cedex 2, BP 84047, France
    *E-mail: [email protected]
  • Jérôme Combet*
    Jérôme Combet
    Université de Strasbourg, CNRS, Institut Charles Sadron (UPR22), 23 rue du Loess, 67034 Strasbourg Cedex 2, BP 84047, France
    *E-mail: [email protected]
  • , and 
  • Loïc Jierry*
    Loïc Jierry
    Université de Strasbourg, CNRS, Institut Charles Sadron (UPR22), 23 rue du Loess, 67034 Strasbourg Cedex 2, BP 84047, France
    *E-mail: [email protected]
    More by Loïc Jierry
Cite this: Biomacromolecules 2023, 24, 8, 3794–3805
Publication Date (Web):August 3, 2023
https://doi.org/10.1021/acs.biomac.3c00445
Copyright © 2023 American Chemical Society

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    Abstract

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    Composite hydrogels composed of low-molecular-weight peptide self-assemblies and polysaccharides are gaining great interest as new types of biomaterials. Interactions between polysaccharides and peptide self-assemblies are well reported, but a molecular picture of their impact on the resulting material is still missing. Using the phosphorylated tripeptide precursor Fmoc-FFpY (Fmoc, fluorenylmethyloxycarbonyl; F, phenylalanine; Y, tyrosine; p, phosphate group), we investigated how hyaluronic acid (HA) influences the enzyme-assisted self-assembly of Fmoc-FFY generated in situ in the presence of alkaline phosphatase (AP). In the absence of HA, Fmoc-FFY peptides are known to self-assemble in nanometer thick and micrometer long fibers. The presence of HA leads to the spontaneous formation of bundles of several micrometers thickness. Using fluorescence recovery after photobleaching (FRAP), we find that in the bundles both (i) HA colocalizes with the peptide self-assemblies and (ii) its presence in the bundles is highly dynamic. The attractive interaction between negatively charged peptide fibers and negatively charged HA chains is explained through molecular dynamic simulations that show the existence of hydrogen bonds. Whereas the Fmoc-FFY peptide self-assembly itself is not affected by the presence of HA, this polysaccharide organizes the peptide nanofibers in a nematic phase visible by small-angle X-ray scattering (SAXS). The mean distance d between the nanofibers decreases by increasing the HA concentration c, but remains always larger than the diameter of the peptide nanofibers, indicating that they do not interact directly with each other. At a high enough HA concentration, the nematic organization transforms into an ordered 2D hexagonal columnar phase with a nanofiber distance d of 117 Å. Depletion interaction generated by the polysaccharides can explain the experimental power law variation dc1/4 and is responsible for the bundle formation and organization. Such behavior is thus suggested for the first time on nano-objects using polymers partially adsorbing on self-assembled peptide nanofibers.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.biomac.3c00445.

    • Figures S1–S17; Additional SAXS-WAXS investigations are described in Section 1; Experimental setup of HPLC analysis is provided in Figure S2 (PDF)

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