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Research Article

Origin of transparency in scattering biomimetic collagen materials

View ORCID ProfileChrystelle Salameh, View ORCID ProfileFlore Salviat, Elora Bessot, Miléna Lama, Jean-Marie Chassot, Elodie Moulongui, Yan Wang, Marc Robin, Arnaud Bardouil, Mohamed Selmane, View ORCID ProfileFranck Artzner, View ORCID ProfileAlba Marcellan, View ORCID ProfileClément Sanchez, Marie-Madeleine Giraud-Guille, View ORCID ProfileMarco Faustini, View ORCID ProfileRémi Carminati, and View ORCID ProfileNadine Nassif
  1. aCollège de France, PSL University, 75231 Paris Cedex 05, France;
  2. bSorbonne Université, CNRS, Collège de France, Laboratoire Chimie de la Matière Condensée de Paris (LCMCP), F-75005 Paris, France;
  3. cCornea, External Disorders and Refractive Surgery, Fondation Ophtalmologique Rothschild, 75019 Paris, France;
  4. dSciences et Ingénierie de la Matière Molle, Ecole Supérieure de Physique et de Chimie Industrielles de la Ville de Paris (ESPCI) Paris, Paris Sciences et Lettres (PSL) University, CNRS, Sorbonne Université, 75005 Paris, France;
  5. eInstitut Langevin, ESPCI Paris, CNRS, PSL University, 75005 Paris, France;
  6. fCNRS, Institut de Physique de Rennes, UMR 6251, Université de Rennes, F-35000 Rennes, France;
  7. gInstitut des Matériaux de Paris Centre, Sorbonne Université, 75252 Paris Cedex 05, France

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PNAS June 2, 2020 117 (22) 11947-11953; first published May 18, 2020; https://doi.org/10.1073/pnas.2001178117
Chrystelle Salameh
aCollège de France, PSL University, 75231 Paris Cedex 05, France;
bSorbonne Université, CNRS, Collège de France, Laboratoire Chimie de la Matière Condensée de Paris (LCMCP), F-75005 Paris, France;
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  • ORCID record for Chrystelle Salameh
Flore Salviat
aCollège de France, PSL University, 75231 Paris Cedex 05, France;
bSorbonne Université, CNRS, Collège de France, Laboratoire Chimie de la Matière Condensée de Paris (LCMCP), F-75005 Paris, France;
cCornea, External Disorders and Refractive Surgery, Fondation Ophtalmologique Rothschild, 75019 Paris, France;
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  • ORCID record for Flore Salviat
Elora Bessot
bSorbonne Université, CNRS, Collège de France, Laboratoire Chimie de la Matière Condensée de Paris (LCMCP), F-75005 Paris, France;
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Miléna Lama
bSorbonne Université, CNRS, Collège de France, Laboratoire Chimie de la Matière Condensée de Paris (LCMCP), F-75005 Paris, France;
dSciences et Ingénierie de la Matière Molle, Ecole Supérieure de Physique et de Chimie Industrielles de la Ville de Paris (ESPCI) Paris, Paris Sciences et Lettres (PSL) University, CNRS, Sorbonne Université, 75005 Paris, France;
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Jean-Marie Chassot
eInstitut Langevin, ESPCI Paris, CNRS, PSL University, 75005 Paris, France;
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Elodie Moulongui
bSorbonne Université, CNRS, Collège de France, Laboratoire Chimie de la Matière Condensée de Paris (LCMCP), F-75005 Paris, France;
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Yan Wang
bSorbonne Université, CNRS, Collège de France, Laboratoire Chimie de la Matière Condensée de Paris (LCMCP), F-75005 Paris, France;
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Marc Robin
bSorbonne Université, CNRS, Collège de France, Laboratoire Chimie de la Matière Condensée de Paris (LCMCP), F-75005 Paris, France;
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Arnaud Bardouil
fCNRS, Institut de Physique de Rennes, UMR 6251, Université de Rennes, F-35000 Rennes, France;
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Mohamed Selmane
gInstitut des Matériaux de Paris Centre, Sorbonne Université, 75252 Paris Cedex 05, France
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Franck Artzner
fCNRS, Institut de Physique de Rennes, UMR 6251, Université de Rennes, F-35000 Rennes, France;
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Alba Marcellan
dSciences et Ingénierie de la Matière Molle, Ecole Supérieure de Physique et de Chimie Industrielles de la Ville de Paris (ESPCI) Paris, Paris Sciences et Lettres (PSL) University, CNRS, Sorbonne Université, 75005 Paris, France;
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Clément Sanchez
aCollège de France, PSL University, 75231 Paris Cedex 05, France;
bSorbonne Université, CNRS, Collège de France, Laboratoire Chimie de la Matière Condensée de Paris (LCMCP), F-75005 Paris, France;
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Marie-Madeleine Giraud-Guille
bSorbonne Université, CNRS, Collège de France, Laboratoire Chimie de la Matière Condensée de Paris (LCMCP), F-75005 Paris, France;
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Marco Faustini
bSorbonne Université, CNRS, Collège de France, Laboratoire Chimie de la Matière Condensée de Paris (LCMCP), F-75005 Paris, France;
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Rémi Carminati
eInstitut Langevin, ESPCI Paris, CNRS, PSL University, 75005 Paris, France;
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Nadine Nassif
aCollège de France, PSL University, 75231 Paris Cedex 05, France;
bSorbonne Université, CNRS, Collège de France, Laboratoire Chimie de la Matière Condensée de Paris (LCMCP), F-75005 Paris, France;
eInstitut Langevin, ESPCI Paris, CNRS, PSL University, 75005 Paris, France;
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  • ORCID record for Nadine Nassif
  • For correspondence: nadine.nassif@sorbonne-universite.fr
  1. Edited by Lia Addadi, Weizmann Institute of Science, Rehovot, Israel, and approved April 10, 2020 (received for review January 21, 2020)

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Significance

Disordered materials with heterogeneities at scales ranging from nano- to micrometers usually scatter visible light and become opaque beyond a certain thickness. However, transparent materials are found in nature. The physical origin of transparency in natural and artificial biopolymer materials is still not fully understood. Here, a gap of transparency is found in synthetic fibrillar collagen matrices within a very narrow range of concentration. The transparency results from structural partial order inhibiting light scattering, while preserving mechanical stability, stiffness, and nonlinearity. The potential to produce biomimetic hydrogels with such striking optical properties by self-assembly opens an interesting route in the study of photonic materials and provides new elements in the understanding of the appearance of transparency in natural materials.

Abstract

Living tissues, heterogeneous at the microscale, usually scatter light. Strong scattering is responsible for the whiteness of bones, teeth, and brain and is known to limit severely the performances of biomedical optical imaging. Transparency is also found within collagen-based extracellular tissues such as decalcified ivory, fish scales, or cornea. However, its physical origin is still poorly understood. Here, we unveil the presence of a gap of transparency in scattering fibrillar collagen matrices within a narrow range of concentration in the phase diagram. This precholesteric phase presents a three-dimensional (3D) orientational order biomimetic of that in natural tissues. By quantitatively studying the relation between the 3D fibrillar network and the optical and mechanical properties of the macroscopic matrices, we show that transparency results from structural partial order inhibiting light scattering, while preserving mechanical stability, stiffness, and nonlinearity. The striking similarities between synthetic and natural materials provide insights for better understanding the occurring transparency.

  • collagen
  • self-assembly
  • photonic materials
  • mechanical properties
  • transparency

Footnotes

  • ↵1C. Salameh and F.S. contributed equally to this work.

  • ↵2Present address: Institut Européen des Membranes (IEM), UMR 5635, Univ Montpellier, CNRS, Ecole Nationale Supérieure de Chimie de Montpellier (ENSCM), 34095 Montpellier, Cedex 5, France.

  • ↵3To whom correspondence may be addressed. Email: nadine.nassif{at}sorbonne-universite.fr.
  • Author contributions: N.N. designed research; C. Salameh, F.S., E.B., M.L., J.-M.C., E.M., Y.W., M.R., A.B., M.S., A.M., M.F., and N.N. performed research; C. Salameh, F.S., E.B., M.L., J.-M.C., F.A., A.M., C. Sanchez, M.-M.G.-G., M.F., R.C., and N.N. analyzed data; and C. Salameh, F.S., M.L., J.-M.C., F.A., A.M., R.C., and N.N. wrote the paper.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2001178117/-/DCSupplemental.

Published under the PNAS license.

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Origin of transparency in scattering biomimetic collagen materials
Chrystelle Salameh, Flore Salviat, Elora Bessot, Miléna Lama, Jean-Marie Chassot, Elodie Moulongui, Yan Wang, Marc Robin, Arnaud Bardouil, Mohamed Selmane, Franck Artzner, Alba Marcellan, Clément Sanchez, Marie-Madeleine Giraud-Guille, Marco Faustini, Rémi Carminati, Nadine Nassif
Proceedings of the National Academy of Sciences Jun 2020, 117 (22) 11947-11953; DOI: 10.1073/pnas.2001178117

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Origin of transparency in scattering biomimetic collagen materials
Chrystelle Salameh, Flore Salviat, Elora Bessot, Miléna Lama, Jean-Marie Chassot, Elodie Moulongui, Yan Wang, Marc Robin, Arnaud Bardouil, Mohamed Selmane, Franck Artzner, Alba Marcellan, Clément Sanchez, Marie-Madeleine Giraud-Guille, Marco Faustini, Rémi Carminati, Nadine Nassif
Proceedings of the National Academy of Sciences Jun 2020, 117 (22) 11947-11953; DOI: 10.1073/pnas.2001178117
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  • Article
    • Abstract
    • Collagen Concentration Gradient and Gap in Transparency
    • Ultrastucture of Transparent Collagen Matrices and Analogy with Cornea
    • Correlation Between Microstructure and Optical and Mechanical Properties
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    • Acknowledgments
    • Footnotes
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