Bone Mineral: Update on Chemical Composition and Structure

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Bone Mineral: Update on Chemical Composition and Structure View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Open Archive Toulouse Archive Ouverte Open Archive Toulouse Archive Ouverte (OATAO) OATAO is an open access repository that collects the work of Toulouse researchers and makes it freely available over the web where possible. This is an author-deposited version published in: http://oatao.univ-toulouse.fr/ Eprints ID: 3715 To link to this article: DOI:10.1016/j.corsci.2005.05.031 URL: http://dx.doi.org/10.1007/s00198-009-1063-2 To cite this version: Rey, Christian and Combes, Christèle and Drouet, Christophe and Glimcher, Melvin J. ( 2009) Bone mineral: update on chemical composition and structure. Osteoporosis International, vol. 20 (n° 6). pp. 1013-1021. ISSN 0937-941X Any correspondence concerning this service should be sent to the repository administrator: [email protected] Osteoporos Int (2009) 20:1013–1021 DOI 10.1007/s00198-009-0860-y Bone mineral: update on chemical composition and structure C. Rey & C. Combes & C. Drouet & M. J. Glimcher History many of the synthetic apatite crystals, compared with the extremely small particle size of bone mineral. The structure of the Ca–P solid phase in bone was first Further studies were directed in roughly three avenues: identified by deJong in 1926 as a crystalline calcium continued more careful and complete analytical composi- phosphate similar to geological apatite by chemical analyses tional data of bone mineral, from which it was clearly and, most importantly, by X-ray diffraction [1]. The X-ray established that the chemical composition of bone crystals in diffraction data was confirmed a few years later [2]. many ways did not correspond to the chemical compositions These findings initiated a flurry of research on a more of stoichiometric hydroxyapatite. Indeed, the bone crystals detailed chemical composition and crystal structure of both were found to contain significant and varying amounts of geological and synthetic apatites and of bone mineral, initially carbonate and HPO4 ions. Much later, it was discovered by a carried out principally by geologists, crystallographers, and variety of techniques, including solid-state NMR [3], Raman chemists, but later by biochemists and physiologists because spectroscopy [4], and inelastic neutron scattering [5], that of the clear potential of this new information to shed light on the biological bone apatites contain only a very small the biological and physiological functions of bone mineral and percentage of the total number of hydroxyl groups present in as indicators of disorders of the skeletal system. highly purified synthetic calcium hydroxyapatites. It soon became clear that there were significant structural Other studies clearly pointed out that a substantial and chemical compositional differences between the many fraction of the phosphate ions are situated on the surfaces different geological hydroxyapatites, synthetic hydroxyapa- of the bone mineral crystals which are mainly protonated tites, and the apatite crystals found in bone and related skeletal and in a disordered environment [6], in contrast to the tissues in addition to the very large size of the geological and phosphate ions in lattice positions, which are unprotonated. Also, other uniquely protonated phosphate ions were identified in bone mineral by phosphorus 31 NMR Data presented at the Third Meeting on Bone Quality, France, 24–25 spectroscopy, which are not present in synthetic calcium June 2008: Bone Ultrastructure. phosphate apatites [7]. C. Rey : C. Combes : C. Drouet Structural studies were first carried out to determine University of Toulouse, crystal size by measuring the extent of X-ray diffraction CIRIMAT, ENSIACET, peak broadening [8], which yielded crystal sizes varying 118 Route de Narbonne 31077, from 31 to 290Å. More detailed structural data were Toulouse Cedex 04, France obtained by the then recently introduced field of electron M. J. Glimcher (*) microscopy and electron diffraction [9–11], which revealed Laboratory for the Study of Skeletal Disorders and Rehabilitation, that the bone crystals were thin plates, approximately 500Å Department of Orthopaedic Surgery, ’ long, 250Å wide, and 100Å thick. However, calculations Harvard Medical School and Children s Hospital, – 300 Longwood Ave, from low-angle X-ray diffraction scattering studies [12 14] Boston, MA 02115, USA were more consistent with the conclusions that the bone e-mail: [email protected] crystals were very much smaller than those observed by rods [16–18]. This was further confirmed by atomic force microscopy [19, 20]. Further TEM compositional studies of the bone crystals from a wide variety of species as a function of “crystal age” (vide infra) revealed that the initial Ca–P solid phase deposited consisted of irregular, roughly round electron dense particles, some as small as ~10Å [21]. These data focused attention on the important physiological implications of the enormous surface area of the bone nanocrystals, especially during the early stages of new bone formation and calcification, and its role in ion homeostasis of the extracellular fluids. These data demonstrate another important structural and physical chemical characteristic of the bone crystals as a function of crystal age (vide infra), further complicating the problem of quantitatively describing the bone crystals in a particular sample of bone substance. Great strides have been made in utilizing in vitro calcification experiments using purified native collagen fibrils and metastable solutions of Ca and P to gain information on the composition and structure of the initial Ca–P solid phase formed during heterogeneous nucleation. These have demonstrated that purified natively 3D-packed collagen molecules in collagen fibrils with an axial period of approximately 670Å are capable of heterogeneously nucle- ating apatite crystals in vitro [22–24]. It was hoped that this information on the potential chemistry and structure of the initial nucleation sites within the collagen fibril responsible for initiating crystallization might be obtained from the in vitro nucleation experiments. The chemical and X-ray diffraction data identifying the Fig. 1 X-ray diffractometer patterns obtained from bone fractions with nanocrystals nucleated in vitro by collagen fibrils, including intensity as the ordinate and diffraction angle (2θ) as the abscissa. a the specific location of the nanocrystals in an orderly Seventeen-day-old chick embryo periosteal bone. b Five-week post- – 3 repeating pattern within the collagen fibrils [25 27], was hatch chick, 2.1-2.2 g/cm density fraction. c Two-year-old chick, 2.2- later confirmed by wide- and low-angle X-ray diffraction 2.3 g/cm3 density fraction. d Highly crystalline synthetic hydroxyap- atite. Patterns derived from rate meter charts obtained with a studies [28]. Much more quantitative in vitro nucleation continuously scanning diffractometer equipped with a diffracted-beam experiments were carried out by Katz [29], who quantita- monochromator, using CuKα radiation. (From Bonar et al. [70]) tively measured the kinetics of in vitro calcification of native collagen fibrils and established the size of the apatite nuclei found in his in vitro nucleation studies (~ 20 ions Robinson et al. by TEM which were rods 250Å long and under the specific conditions of his experiments). Various 50Å thick and not platelets. Crystal perfection, another schema and experiments were devised from these in vitro structural property of the individual bone nanocrystals, is studies of nucleation of the likely composition of the nuclei also a function of the extent of mineralization, as (first solid phase Ca–P formed during in vitro calcification) demonstrated by the changes in their wide-angle X-ray and the potential role of the phosphoryl groups and glutamic diffraction patterns [15] (Fig. 1). acid side chains of a particular noncollagenous matrix More accurate evaluations of the size and shape of the protein in bone (bone sialoprotein-BSP) [27, 29, 30, 32]. bone crystals were later obtained by the development of Very importantly, solid-state 31P NMR analysis of the techniques, which removed essentially all of the organic youngest sample of native bone available at that time matrix constituents of the bone samples prior to TEM identified for the first time the presence of a seryl without altering the bone crystals, thus permitting their phosphate-calcium bond, presumably directly linking a examination by high-resolution TEM and electron diffrac- prominent protein in the organic matrix of bone (BSP) tion as well as 3D stereoscopic TEM, which firmly with the mineral phase [33]. established that the bone apatite crystals were indeed A number of other experiments were also devised and nanosized, very thin, long platelets (nanocrystals), and not carried out to surmount the problems of how to isolate the very youngest bone mineral crystals in specimens of bone The earliest such experiments were carried out on the without introducing any contact of the specimens with very outermost layers of bone of the midshaft of the long water, which not only very rapidly dissolves the crystals but bones of embryonic chick (and other species) using only also introduces physical and chemical compositional non-aqueous solvents. The bone samples were powdered changes in the crystals which remain in the bone sample. and density-separated in non-aqueous solvents. The very While the chemical composition and crystal structure, lowest density
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