The Carbonate and Sodium Environments in Precipitated and Biomimetic Calcium Hydroxy-Carbonate Apatite Contrasted with Bone Mineral: Structural Insights from Solid-State NMR

Abstract

Bone mineral consists of calcium hydroxy-carbonate apatite (HCA) that incorporates other minor cation substituents, primarily Na + (0.5−0.8 wt %). We examine the carbonate species in various HCA specimens with variable CO 3 2− contents (4−10 wt %), encompassing phases prepared by precipitation and a biomimetic specimen formed from a bioactive glass inside a simulated body fluid as well as bone tissue from beagle dog. Using magic-angle spinning (MAS) nuclear magnetic resonance (NMR) along with infrared spectroscopy experiments, we identified and quantified carbonate anions replacing either hydroxyl ("A-type" CO 3 2− ) or phosphate ("B-type" CO 3 2− ) anions in the HCA lattice, along with the carbonate species present in the amorphous surface layer present at all synthetic and biogenic nanocrystalline HCA particles. Advanced 13 C-based NMR experimentation enabled the selective detection of the minor CO 13 3 2− population of intact bone monoliths, whose 13 C NMR signals are otherwise swamped by those from collagen, unless chemically invasive deproteination procedures are invoked. The CO 3 2− species present in 4 week-and 8 month-old bone of the alveolar process from beagle dog revealed mainly B-type lattice sites and carbonates present in the amorphous surface layer. No tissue aging effects were observed in the local CO 3 2− environments. Likewise, NMR revealed very similar 23 Na + parameters in HCA, regardless of its synthetic or biogenic origin or degree of structural order. A combination of interatomic-distance-sensitive MAS NMR experiments allowed the identification of the local environments of the various carbonate, phosphate, hydroxyl, and water species present in both the interior and the surface layer of the synthetic HCA particles. We highlight the similarities/differences in the chemical speciation and the spatial distribution of CO 3 2− anions present in carbonate-bearing amorphous calcium phosphate (ACP) relative to the ACP-like surface layer of HCA and discuss the 13 C NMR peak assignments of the up to four coexisting CO 3 2− populations in the synthetic/ biogenic HCA phases.

Metadynamics Simulations of the pH-Dependent Adsorption of Phosphoserine and Citrate on Disordered Apatite Surfaces: What Interactions Govern the Molecular Binding?

“…Moreover, it is nowadays well known that biomolecules interacting with nanometer-sized apatite particles (such as bone mineral) bind at an amorphous surface devoid of OH moieties. 6,17,63,67 These features remain unaccounted for in nearly all modeling work to date. Our present study strongly suggested that OH groups at the HA surface perturb the modeled results significantly and must be removed in the surface preparation.…”

“…We conclude that surface hydroxyl groups should be removed altogether when simulating (bio)molecular adsorption, as in the disordered surface model of ref 52. Moreover, we recall that all apatite nanoparticles (e.g., bone mineral) are coated by an ACP-like layer, 3,6,17,62−69 which is completely, 17,63,96 or nearly, 67 devoid of HA-type OH groups.…”

“…A more fundamental problem with nearly all current DFT/AIMD/MD simulations, however, concerns the HA surface speciation of these models, where the prevailing approach is to cleave the stoichiometric HA crystal and preserve its periodicity, ,− ,,− which is tantamount to assuming that the simulated HA surface is present in a solution with pH > 14, i.e., far from physiological conditions. − Moreover, it is nowadays well established that all synthetic/biogenic nanometer-sized HA particles exhibit a core – shell organization, where an ordered core of “apatitic” Ca 2+ , PO 4 3– , and OH – ions is coated by a 1–2 nm thick surface layer of ACP, rich in acidic phosphate (HPO 4 2– ) moieties and water but essentially devoid of isolated (HA-type) hydroxyl groups, ,,− and often termed the “hydrated surface layer”. ,, Hence, biomolecules adsorbing at HA (“apatite”) nanoparticles interact with amorphous, rather than well-ordered, domains. As pointed out previously, ,, this property has strong bearings for a faithful computer modeling of biomolecule–HA interactions, as the adsorption de facto occurs at the surface layer of ACP, whose hydrated and disordered CaP environments are distinctly different from a perfect HA structure.…”

The Journal of Physical Chemistry C Virtual Special Issue on Advanced Characterization by Solid-State NMR and In Situ Technology and in Recognition of Michael Hunger’s 65th Birthday

“…The stereoselective hydrogenation of propyne to propene over Pd–Ag/Al 2 O 3 catalysts has been studied by Xu and coworkers using parahydrogen-induced polarization (PHIP) NMR techniques . Edén and coworkers revealed the local environments and interactions of various species in both the interior and the surface layer of bone minerals by 31 P­{ 1 H}, 13 C­{ 1 H}, and 31 P­{ 13 C} heteronuclear correlation (HETCOR) NMR . The Hermans group characterized silica-supported boron by double quantum–single quantum (DQ-SQ), HETCOR, refocused insensitive nuclei enhanced by polarization transfer (RINEPT), heteronuclear multiple-quantum correlation (HMQC) NMR to understand the surface sites and their structures for oxidative dehydrogenation .…”

“…6 Edeń and coworkers revealed the local environments and interactions of various species in both the interior and the surface layer of bone minerals by 31 P{ 1 H}, 13 C{ 1 H}, and 31 P{ 13 C} heteronuclear correlation (HETCOR) NMR. 7 The Hermans group characterized silica-supported boron by double quantum−single quantum (DQ-SQ), HETCOR, refocused insensitive nuclei enhanced by polarization transfer (RINEPT), heteronuclear multiple-quantum correlation (HMQC) NMR to understand the surface sites and their structures for oxidative dehydrogen-ation. 8 Solid-state NMR was used by the Sato group to characterize Cs-containing clay nanoparticles for carbon dioxide capture and storage.…”