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The Mineral–Collagen Interface in Bone

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Abstract

The interface between collagen and the mineral reinforcement phase, carbonated hydroxyapatite (cAp), is essential for bone’s remarkable functionality as a biological composite material. The very small dimensions of the cAp phase and the disparate natures of the reinforcement and matrix are essential to the material’s performance but also complicate study of this interface. This article summarizes what is known about the cAp-collagen interface in bone and begins with descriptions of the matrix and reinforcement roles in composites, of the phases bounding the interface, of growth of cAp growing within the collagen matrix, and of the effect of intra- and extrafibrilar mineral on determinations of interfacial properties. Different observed interfacial interactions with cAp (collagen, water, non-collagenous proteins) are reviewed; experimental results on interface interactions during loading are reported as are their influence on macroscopic mechanical properties; conclusions of numerical modeling of interfacial interactions are also presented. The data suggest interfacial interlocking (bending of collagen molecules around cAp nanoplatelets) and water-mediated bonding between collagen and cAp are essential to load transfer. The review concludes with descriptions of areas where new research is needed to improve understanding of how the interface functions.

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Notes

  1. For these ballpark estimates, values from [2] are used for human osteocytes (6 × 104 osteocytes per mm3 and radii of 8, 3 and 3 μm for an ellipsoid of volume equivalent to those measured experimentally) and from [3] for human canaliculi (50-nm canaliculi radius, 40-μm mean canaliculi length and 40 canaliculi per osteocyte).

  2. For purposes of this estimate, nanoplatelet dimensions of 40 nm × 20 nm × 4 nm and 0.4 volume fraction of mineral were assumed.

  3. Zeolites are a group of nanoporous aluminosilicate materials typified by surface area of ~900 m2/g and density of ~0.8 g [5].

  4. The crystal’s unit cell is the parallelepiped defined by the lattice vectors (c, a 1 and a 2 in the hexagonal axial system) and thus is the building block of the crystal lattice.

  5. Dislocations are linear defects in the ordered lattice of crystals, and their motion and multiplication produce the ductility typical of many metals. As such, dislocations and their characterization are a significant topic in materials science. It is with great difficulty that crystals such as Si for semiconductor wafers can be grown dislocation-free. Dislocations are surrounded by strain fields extending micrometers or more from their axes. In crystals as small as those in bone, the physical meaning of crystal defects such as dislocations is difficult to imagine. However, one growth dislocation per nanoplatelet would correspond to a dislocation density as high as in heavily worked metals and could produce the measured broadening.

  6. The papers by Garnero in this issue [41, 42] cover fibrillar collagen in much more detail.

  7. The c-axis of the cAp crystal lattice is along the longest nanoplatelet dimension and the collagen molecule axes. The a-axes (there are two of them in the hexagonal crystal system) are along the shorter nanoplatelet edges.

  8. The original report attributed the change to replacement of formalin with phosphate-buffered saline via diffusion.

  9. That is, the lattice plane perpendicular to the cAp c-axis. (100) is the lattice plane normal to the a-axis.

  10. Crystalline solids scatter x-rays over specific, very narrow angular ranges because of their long range order and sharp periodicities. Amorphous materials do not have such tightly defined periodicities but do possess some short range order at the level of a very few atomic diameters. This very limited ordering suffices to produce broad but relatively weak maxima in scattered intensity, which, when intercepted by an x-ray area detector, appear to be diffuse halos (as opposed to relatively sharp diffraction rings).

  11. In continuum mechanics, the classic Eshelby inclusion problem involves an ellipsoidal linear elastic inclusion embedded in an infinite linear elastic body. The original formulation was for an inclusion that has undergone a transformation and whose size and shape are constrained by the surrounding material. The resulting strain fields are inhomogeneous, and fields neighboring inclusions could influence other particles’ growth.

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Acknowledgments

The author is very grateful to Prof. Arthur Veis for countless helpful discussions (and debates) on bone and other mineralized tissues, particularly on the proteins involved with these tissues. Support is gratefully acknowledged from NIDCR grant DE001374, and NIDCR and its staff had no input into this paper. Further, the author has no potential conflict of interest to report.

Conflict of Interest

S. R. Stock has no conflict of interest to disclose.

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This article does not contain any studies with human or animal subjects performed by the author.

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  1. Department of Cell and Molecular Biology, Feinberg School of Medicine, Northwestern University, 303 E. Chicago Ave., Chicago, IL, 60611-3008, USA

    S. R. Stock

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Stock, S.R. The Mineral–Collagen Interface in Bone. Calcif Tissue Int 97, 262–280 (2015). https://doi.org/10.1007/s00223-015-9984-6

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