Intermolecular channels direct crystal orientation in mineralized collagen
Xu, YiFei; Nudelman, Fabio; Eren, E Deniz; Wirix, Maarten J M; Cantaert, Bram; Nijhuis, Wouter H; Hermida-Merino, Daniel; Portale, Giuseppe; Bomans, Paul H H; Ottmann, Christian; Friedrich, Heiner; Bras, Wim; Akiva, Anat; Orgel, Joseph P R O; Meldrum, Fiona C; Sommerdijk, Nico
(2020) Nature Communications, volume 11, issue 1
(Article)
Abstract
The mineralized collagen fibril is the basic building block of bone, and is commonly pictured as a parallel array of ultrathin carbonated hydroxyapatite (HAp) platelets distributed throughout the collagen. This orientation is often attributed to an epitaxial relationship between the HAp and collagen molecules inside 2D voids within the fibril.
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Although recent studies have questioned this model, the structural relationship between the collagen matrix and HAp, and the mechanisms by which collagen directs mineralization remain unclear. Here, we use XRD to reveal that the voids in the collagen are in fact cylindrical pores with diameters of ~2 nm, while electron microscopy shows that the HAp crystals in bone are only uniaxially oriented with respect to the collagen. From in vitro mineralization studies with HAp, CaCO3 and γ-FeOOH we conclude that confinement within these pores, together with the anisotropic growth of HAp, dictates the orientation of HAp crystals within the collagen fibril.
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Keywords: General Chemistry, General Biochemistry,Genetics and Molecular Biology, General Physics and Astronomy
ISSN: 2041-1723
Publisher: Nature Publishing Group
Note: Funding Information: We thank Dr. Koen Pieterse (Institute for Complex Molecular Systems, Eindhoven University of Technology, the Netherlands (TU/e)) for his help with data analysis, Zaf Khalil (Department of Chemical Engineering and Chemistry, TU/e) for his help with bone sample preparation and Andreas J. Fijneman (Department of Chemical Engineering and Chemistry, TU/e) for helpful discussions. We thank Dr. Elena Macias (Radboud Institute for Molecular Life Sciences) for her critical review of the manuscript. This work was supported by the Netherlands Organization for Scientific Research (NWO) through VICI (F.N., M.J.M.W.) and Toppunt (Y.X.) grants to N.S. E.D.E. and N.S. were supported by the European Research Council (ERC) Advanced Investigator grant (H2020-ERC-2017-ADV-788982-COLMIN). Y.X. was supported by the Marie Curie Individual Fellowship (H2020-MSAC-IF-2019-885795-PolyTEM), and A.A. was supported by the Marie Curie Individual Fellowship (H2020-MSCA-IF-2017-794296-SUPERMIN). E.D.E. and A.A. were also partially supported by an NWO Echo Grant. W.B.’s contribution is partially based upon work supported by Oak Ridge National Laboratory, managed by UT-Battelle, LLC, for the U.S. Department of Energy. The work was further supported by an Engineering and Physical Sciences (EPSRC) Platform Grant to F.C.M. (EP/N002423/1), an EPSRC Program Grant (EP/R018820/1) which funds the Crystallization in the Real World Consortium (F.C.M.), and a Leverhulme research project grant (F.C.M., N.S., and Y.X.). NWO is also gratefully acknowledged for making access to the DUBBLE ESRF beamline possible. This project was also supported by grant 9 P41 GM103622 from the National Institute of General Medical Sciences of the National Institutes of Health. We also thank the University of Edinburgh for financial support. Publisher Copyright: © 2020, The Author(s). Copyright: Copyright 2020 Elsevier B.V., All rights reserved.
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