Laurencin, Danielle, Almora-Barrios, Neyvis, Leeuw, Nora H. de, Gervais, Christel, Bonhomme, Christian, Mauri, Francesco, Chrzanowski, Wojciech, Knowles, Jonathan C., Newport, Robert J., Wong, Alan, Gan, Zhehong and Smith, Mark E.. (2011) Magnesium incorporation into hydroxyapatite. Biomaterials, Vol.32 (No.7). pp. 1826-1837. ISSN 0142-9612

Preview

PDF WRAP_Smith_9774456-vcs_office-041211-mg_ha_v10.pdf - Accepted Version - Requires a PDF viewer such as GSview, Xpdf or Adobe Acrobat Reader Download (1620Kb)

Abstract

The incorporation of Mg in hydroxyapatite (HA) was investigated using multinuclear solid state NMR, X-ray absorption spectroscopy (XAS) and computational modeling. High magnetic field 43Ca solid state NMR and Ca K-edge XAS studies of a ∼10% Mg-substituted HA were performed, bringing direct evidence of the preferential substitution of Mg in the Ca(II) position. 1H and 31P solid state NMR show that the environment of the anions is disordered in this substituted apatite phase. Both Density Functional Theory (DFT) and interatomic potential computations of Mg-substituted HA structures are in agreement with these observations. Indeed, the incorporation of low levels of Mg in the Ca(II) site is found to be more favourable energetically, and the NMR parameters calculated from these optimized structures are consistent with the experimental data. Calculations provide direct insight in the structural modifications of the HA lattice, due to the strong contraction of the M⋯O distances around Mg. Finally, extensive interatomic potential calculations also suggest that a local clustering of Mg within the HA lattice is likely to occur. Such structural characterizations of Mg environments in apatites will favour a better understanding of the biological role of this cation.

Item Type:	Journal Article
Subjects:	Q Science > QC Physics
Divisions:	Administration > Vice Chancellor's Office Faculty of Science > Physics
Library of Congress Subject Headings (LCSH):	Magnesium, Hydroxyapatite, Nuclear magnetic resonance spectroscopy, X-ray spectroscopy
Journal or Publication Title:	Biomaterials
Publisher:	Elsevier Science BV
ISSN:	0142-9612
Date:	March 2011
Volume:	Vol.32
Number:	No.7
Page Range:	pp. 1826-1837
Identification Number:	10.1016/j.biomaterials.2010.11.017
Status:	Peer Reviewed
Publication Status:	Published
Access rights to Published version:	Restricted or Subscription Access
Funder:	Centre national de la recherche scientifique (France) (CNRS), Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC), Engineering and Physical Sciences Research Council (EPSRC), University of Warwick, University College London, Royal Society (Great Britain), Advantage West Midlands (AWM), European Regional Development Fund (ERDF), Sixth Framework Programme (European Commission) (FP6), Natural Sciences and Engineering Research Council of Canada (NSERC), National Research Foundation of Korea (NRF), Korea (South). Kyoyuk Kwahak Kisulbu, ELETTRA, European Union (EU), Birmingham Science City
Grant number:	EP/D504872 (EPSRC), R31-10069 (NRF), 091461 (CNRS), 2007512 (ELETTRA), RII3-CT-2004-506008-IA-SFS (EU)
References:	1. Elliott JC. Studies in Inorganic Chemistry Volume 18: Structure and Chemistry of the Apatites and Other Calcium Orthophosphates, 1994. 2. Dorozhkin SV. Calcium orthophosphates. Journal of Materials Science 2007;42(4):1061-1095. 3. Roberts NB, Walsh HPJ, Klenerman L, Kelly SA, Helliwell TR. Determination of elements in human femoral bone using inductively coupled plasma atomic emission spectrometry and inductively coupled plasma mass spectrometry. Journal of Analytical Atomic Spectrometry 1996;11(2):133-138. 4. Heaney RP. Role of dietary sodium in osteoporosis. Journal of the American College of Nutrition 2006;25(3, Suppl.):271S-276S. 5. Featherstone JDB. Prevention and reversal of dental caries: role of low level fluoride. Comm Dent Oral Epidemiol 1999;27(2):31. 6. Robinson C, Weatherell JA, Hallsworth AS. Distribution of magnesium in mature human enamel. Caries Research 1981;15(1):70-77. 7. Robinson C, Weatherell JA. Magnesium in bone and tooth. Metal Ions in Biological Systems 1990;26(Compend. Magnesium Its Role Biol., Nutr., Physiol.):489-504. 8. Landi E, Tampieri A, Mattioli-Belmonte M, Celotti G, Sandri M, Gigante A, et al. Biomimetic Mg- and MgCO3-substituted hydroxyapatites: synthesis characterization and in vitro behaviour. Journal of the European Ceramic Society 2006;26(13):2593-2601. 9. Rude RK, Gruber HE. Magnesium deficiency and osteoporosis: animal and human observations. Journal of Nutritional Biochemistry 2004;15(12):710-716. 10. Luoma H. The role of magnesium in the aetiology and prevention of caries: some new findings and implications. Magnesium research : official organ of the International Society for the Development of Research on Magnesium 1988;1(3-4):223-230. 11. Gomes S, Renaudin G, Jallot E, Nedelec JM. Structural Characterization and Biological Fluid Interaction of Sol-Gel-Derived Mg-Substituted Biphasic Calcium Phosphate Ceramics. ACS Applied Materials & Interfaces 2009;1(2):505-513. 12. Landi E, Logroscino G, Proietti L, Tampieri A, Sandri M, Sprio S. Biomimetic Mg-substituted hydroxyapatite: from synthesis to in vivo behavior. Journal of Materials Science: Materials in Medicine 2008;19(1):239-247. 13. Bigi A, Falini G, Foresti E, Gazzano M, Ripamonti A, Roveri N. Magnesium influence on hydroxyapatite crystallization. Journal of Inorganic Biochemistry 1993;49(1):69-78. 14. Suchanek WL, Byrappa K, Shuk P, Riman RE, Janas VF, TenHuisen KS. Preparation of magnesium-substituted hydroxyapatite powders by the mechanochemical-hydrothermal method. Biomaterials 2004;25(19):4647-4657. 15. Tampieri A, Celotti G, Landi E, Sandri M. Magnesium doped hydroxyapatite: synthesis and characterization. Key Eng Mater 2004;264-268(Pt. 3, Euro Ceramics VIII):2051-2054. 16. Mroz W, Bombalska A, Burdynska S, Jedynski M, Prokopiuk A, Budner B, et al. Structural studies of magnesium doped hydroxyapatite coatings after osteoblast culture. Journal of Molecular Structure;977(1-3):145-152. 17. Gibson IR, Bonfield W. Preparation and characterization of magnesium/carbonate co-substituted hydroxyapatites. Journal of Materials Science: Materials in Medicine 2002;13(7):685-693. 18. Bertinetti L, Drouet C, Combes C, Rey C, Tampieri A, Coluccia S, et al. Surface Characteristics of Nanocrystalline Apatites: Effect of Mg Surface Enrichment on Morphology, Surface Hydration Species, and Cationic Environments. Langmuir 2009;25(10):5647-5654. 19. Bertinetti L, Tampieri A, Landi E, Martra G, Coluccia S. Punctual investigation of surface sites of HA and magnesium-HA. Journal of the European Ceramic Society 2006;26(6):987-991. 20. Bigi A, Falini G, Foresti E, Gazzano M, Ripamonti A, Roveri N. Rietveld structure refinements of calcium hydroxylapatite containing magnesium. Acta Crystallogr, Sect B: Struct Sci 1996;B52(1):87-92. 21. Sprio S, Pezzotti G, Celotti G, Landi E, Tampieri A. Raman and cathodoluminescence spectroscopies of magnesium-substituted hydroxyapatite powders. Journal of Materials Research 2005;20(4):1009-1016. 22. Yasukawa A, Ouchi S, Kandori K, Ishikawa T. Preparation and characterization of magnesium-calcium hydroxyapatites. J Mater Chem 1996;6(8):1401-1405. 23. Bigi A, Boanini E, Capuccini C, Gazzano M. Strontium-substituted hydroxyapatite nanocrystals. Inorganica Chimica Acta 2007;360(3):1009-1016. 24. Bigi A, Foresti E, Marchetti F, Ripamonti A, Roveri N. Barium calcium hydroxyapatite solid solutions. Journal of the Chemical Society, Dalton Transactions: Inorganic Chemistry (1972-1999) 1984(6):1091-1093. 25. Tang Y, Chappell HF, Dove MT, Reeder RJ, Lee YJ. Zinc incorporation into hydroxylapatite. Biomaterials 2009;30(15):2864-2872. 26. Pizzala H, Caldarelli S, Eon J-G, Rossi AM, Laurencin D, Smith ME. A Solid-State NMR Study of Lead and Vanadium Substitution into Hydroxyapatite. J Am Chem Soc 2009;131(14):5145-5152. 27. Matsunaga K, Inamori H, Murata H. Theoretical trend of ion exchange ability with divalent cations in hydroxyapatite. Physical Review B: Condensed Matter and Materials Physics 2008;78(9):094101/094101-094101/094108. 28. Matsunaga K. First-principles study of substitutional magnesium and zinc in hydroxyapatite and octacalcium phosphate. Journal of Chemical Physics 2008;128(24):245101/245101-245101/245110. 29. Tamm T, Peld M. Computational study of cation substitutions in apatites. Journal of Solid State Chemistry 2006;179(5):1581-1587. 30. de Leeuw NH, Bowe JR, Rabone JAL. A computational investigation of stoichiometric and calcium-deficient oxy- and hydroxy-apatites. Faraday Discussions 2007;134:195-214. 31. Bertoni E, Bigi A, Cojazzi G, Gandolfi M, Panzavolta S, Roveri N. Nanocrystals of magnesium and fluoride substituted hydroxyapatite. Journal of Inorganic Biochemistry 1998;72(1,2):29-35. 32. Siegel R, Nakashima TT, Wasylishen RE. Sensitivity enhancement of NMR spectra of half-integer quadrupolar nuclei in the solid state via population transfer. Concepts in Magnetic Resonance, Part A 2005;26A(2):47-61. 33. Kwak H-T, Prasad S, Clark T, Grandinetti PJ. Enhancing sensitivity of quadrupolar nuclei in solid-state NMR with multiple rotor assisted population transfers. Solid State Nuclear Magnetic Resonance 2003;24(2 & 3):71-77. 34. Laurencin D, Wong A, Dupree R, Smith ME. Natural abundance 43Ca solid-state NMR characterization of hydroxyapatite: identification of the two calcium sites. Magnetic Resonance in Chemistry 2008;46(4):347-350. 35. Van Veenendaal E, Meier BH, Kentgens APM. Frequency stepped adiabatic passage excitation of half-integer quadrupolar spin systems. Molecular Physics 1998;93(2):195-213. 36. Lutz O, Schwenk A, Uhl A. Fourier transform nuclear magnetic resonance studies of magnesium-25 and calcium-43. Zeitschrift fuer Naturforschung, Teil A: Astrophysik, Physik und Physikalische Chemie 1975;30A(9):1122-1127. 37. Gervais C, Laurencin D, Wong A, Pourpoint F, Labram J, Woodward B, et al. New perspectives on calcium environments in inorganic materials containing calcium-oxygen bonds: A combined computational-experimental 43Ca NMR approach. Chemical Physics Letters 2008;464(1-3):42-48. 38. MacKenzie KJD, Smith ME. Multinuclear Solid-State Nuclear Magnetic Resonance of Inorganic Materials; Pergamon Press, Oxford, 2002. 39. Cahill LS, Hanna JV, Wong A, Freitas JCC, Yates JR, Harris RK, et al. Natural Abundance 25Mg Solid-State NMR of Mg Oxyanion Systems: A Combined Experimental and Computational Study. Chem--Eur J 2009;15(38):9785-9798, S9785/9781-S9785/9783. 40. Ravel B, Newville M. ATHENA, ARTEMIS, HEPHAESTUS: data analysis for x-ray absorption spectroscopy using IFEFFIT. Journal of Synchrotron Radiation 2005;12(4):537-541. 41. Klementev KV. Extraction of the fine structure from x-ray absorption spectra. Journal of Physics D: Applied Physics 2001;34(2):209-217. 42. Klementev KV. VIPER for Windows. freeware: wwwdesyde/~klmn/viperhtml. 43. Binsted N, Campbell JW, Gurman SJ, Stephenson PC. EXAFS Analysis programs. Warrington, UK: Daresbury Laboratory. 44. Sugiyama S, Minami T, Moriga T, Hayashi H, Koto K, Tanaka M, et al. Surface and bulk properties, catalytic activities and selectivities in methane oxidation on near-stoichiometric calcium hydroxyapatites. J Mater Chem 1996;6(3):459-464. 45. Skipper LJ, Sowrey FE, Pickup DM, Fitzgerald V, Rashid R, Drake KO, et al. Structural studies of bioactivity in sol-gel-derived glasses by X-ray spectroscopy. Journal of Biomedical Materials Research, Part A 2004;70A(2):354-360. 46. Laurencin D, Wong A, Chrzanowski W, Knowles JC, Qiu D, Pickup DM, et al. Probing the calcium and sodium local environment in bones and teeth using multinuclear solid state NMR and X-ray absorption spectroscopy. Physical Chemistry Chemical Physics 2010;12(5):1081-1091. 47. Rabone JAL, De Leeuw NH. Interatomic potential models for natural apatite crystals: Incorporating strontium and the lanthanides. Journal of Computational Chemistry 2006;27(2):253-266. 48. de Leeuw NH. Resisting the Onset of Hydroxyapatite Dissolution through the Incorporation of Fluoride. J Phys Chem B 2004;108(6):1809-1811. 49. Mostafa NY, Brown PW. Computer simulation of stoichiometric hydroxyapatite. Structure and substitutions. Journal of Physics and Chemistry of Solids 2007;68(3):431-437. 50. Ellis DE, Terra J, Warschkow O, Jiang M, Gonzalez GB, Okasinski JS, et al. A theoretical and experimental study of lead substitution in calcium hydroxyapatite. Physical Chemistry Chemical Physics 2006;8(8):967-976. 51. Ordejon P, Artacho E, Soler JM. Self-consistent order-N density-functional calculations for very large systems. Phys Rev B 1996 Apr 15;53(16):10441-10444. 52. Kohn W, Sham LJ. Self-Consistent Equations Including Exchange and Correlation Effects. Phys Rev 1965;140(4A):1133-&. 53. Perdew JP, Burke K, Ernzerhof M. Generalized gradient approximation made simple. Phys Rev Lett 1996 Oct 28;77(18):3865-3868. 54. Troullier N, Martins JL. Efficient Pseudopotentials for Plane-Wave Calculations .2. Operators for Fast Iterative Diagonalization. Phys Rev B 1991 Apr 15;43(11):8861-8869. 55. Anglada E, Soler JM, Junquera J, Artacho E. Systematic generation of finite-range atomic basis sets for linear-scaling calculations. Phys Rev B 2002 Nov 15;66(20):-. 56. Junquera J, Paz O, Sanchez-Portal D, Artacho E. Numerical atomic orbitals for linear-scaling calculations. Phys Rev B 2001 Dec 15;64(23):-. 57. Gale JD. GULP: A computer program for the symmetry-adapted simulation of solids. Journal of the Chemical Society-Faraday Transactions 1997;93(4):629-637. 58. Gale JD, Rohl AL. The General Utility Lattice Program (GULP). Molecular Simulation 2003;29(5):291-341. 59. Gale JD. GULP: Capabilities and prospects. Zeitschrift Fur Kristallographie 2005;220(5-6):552-554. 60. Born M, Huang K. Dynamical theory of crystal lattices. Oxford: Clarendon Press, 1954. 61. de Leeuw NH. A computer modelling study of the uptake and segregation of fluoride ions at the hydrated hydroxyapatite (0001) surface: introducing Ca-10(PO4)(6)(OH)(2) potential model. Phys Chem Chem Phys 2004 Apr 21;6(8):1860-1866. 62. Dick BG, Overhauser AW. Theory of the Dielectric Constants of Alkali Halide Crystals. Physical Review 1958;112(1):90-103. 63. Posner AS, Perloff A, Diorio AF. Refinement of the Hydroxyapatite Structure. Acta Crystallographica 1958;11(4):308-309. 64. Markovic M, Fowler BO, Tung MS. Preparation and comprehensive characterization of a calcium hydroxyapatite reference material. Journal of Research of the National Institute of Standards and Technology 2004;109(6):553-568. 65. Sudarsanan K, Young RA. Significant precision in crystal structural details: Holly Springs hydroxyapatite. Acta Crystallographica, Section B: Structural Crystallography and Crystal Chemistry 1969;25(Pt. 8):1534-1543. 66. de Leeuw NH. Local ordering of hydroxy groups in hydroxyapatite. Chem Commun (Cambridge, U K) 2001(17):1646-1647. 67. de Leeuw NH. Density functional theory calculations of local ordering of hydroxy groups and fluoride ions in hydroxyapatite. Physical Chemistry Chemical Physics 2002;4(15):3865-3871. 68. Stork L, Muller P, Dronskowski R, Ortlepp JR. Chemical analyses and X-ray diffraction investigations of human hydroxyapatite minerals from aortic valve stenoses. Zeitschrift Fur Kristallographie 2005;220(2-3):201-205. 69. Suetsugu Y, Tanaka J. Crystal growth and structure analysis of twin-free monoclinic hydroxyapatite. Journal of Materials Science: Materials in Medicine 2002;13(8):767-772. 70. Pickard CJ, Mauri F. All-electron magnetic response with pseudopotentials: NMR chemical shifts. Physical Review B: Condensed Matter and Materials Physics 2001;63(24):245101/245101-245101/245113. 71. PARATEC (PARAllel Total Energy Code) by Pfrommer B., Raczkowski D., Canning A., Louie S.G.; Lawrence Berkeley National Laboratory (with contributions from Mauri F., Cote M., Yoon Y., Pickard C. and Heynes P.). For more information see www.nersc.gov/projects/paratec <http://www.nersc.gov/projects/paratec>. 72. Troullier N, Martins JL. Efficient pseudopotentials for plane-wave calculations. Phys Rev B: Condens Matter 1991;43(3):1993-2006. 73. Kleinman L, Bylander DM. Efficacious form for model pseudopotentials. Physical Review Letters 1982;48(20):1425-1428. 74. Gervais C, Profeta M, Lafond V, Bonhomme C, Azais T, Mutin H, et al. Combined ab initio computational and experimental multinuclear solid-state magnetic resonance study of phenylphosphonic acid. Magnetic Resonance in Chemistry 2004;42(5):445-452. 75. Schimmel HG, Huot J, Chapon LC, Tichelaar FD, Mulder FM. Hydrogen Cycling of Niobium and Vanadium Catalyzed Nanostructured Magnesium. J Am Chem Soc 2005;127(41):14348-14354. 76. Pallister PJ, Moudrakovski IL, Ripmeester JA. Mg-25 ultra-high field solid state NMR spectroscopy and first principles calculations of magnesium compounds. Physical Chemistry Chemical Physics 2009;11(48):11487-11500. 77. Salager E, Day GM, Stein RS, Pickard CJ, Elena B, Emsley L. Powder Crystallography by Combined Crystal Structure Prediction and High-Resolution 1H Solid-State NMR Spectroscopy. J Am Chem Soc;132(8):2564-2566. 78. Bonhomme C, Gervais C, Coelho C, Pourpoint F, Azais T, Bonhomme-Coury L, et al. New perspectives in the PAW/GIPAW approach: J P-O-Si coupling constants, antisymmetric parts of shift tensors and NQR predictions. Magnetic Resonance in Chemistry 2010:doi:10.1002/mrc.2635. 79. Yesinowski JP, Eckert H. Hydrogen environments in calcium phosphates: proton MAS NMR at high spinning speeds. J Am Chem Soc 1987;109(21):6274-6282. 80. Isobe T, Nakamura S, Nemoto R, Senna M, Sfihi H. Solid-state double nuclear magnetic resonance study of the local structure of calcium phosphate nanoparticles synthesized by a wet-mechanochemical reaction. J Phys Chem B 2002;106(20):5169-5176. 81. Badraoui B, Bigi A, Debbabi M, Gazzano M, Roveri N, Thouvenot R. X-ray powder diffraction and solid-state NMR investigations in cadmium-lead hydroxyapatites. Eur J Inorg Chem 2001(5):1261-1267. 82. Badraoui B, Bigi A, Debbabi M, Gazzano M, Roveri N, Thouvenot R. Physicochemical properties and structural refinement of strontium-lead hydroxyapatites. Eur J Inorg Chem 2002(7):1864-1870. 83. Bryce DL. Calcium binding environments probed by 43Ca NMR spectroscopy. Dalton Trans 2010;39(37):8577-8836. 84. Bryce DL, Bultz EB, Aebi D. Calcium-43 Chemical Shift Tensors as Probes of Calcium Binding Environments. Insight into the Structure of the Vaterite CaCO3 Polymorph by 43Ca Solid-State NMR Spectroscopy. J Am Chem Soc 2008;130(29):9282-9292. 85. Dupree R, Howes AP, Kohn SC. Natural abundance solid state 43Ca NMR. Chemical Physics Letters 1997;276(5,6):399-404. 86. Cormier L, Neuville DR. Ca and Na environments in Na2O-CaO-Al2O3-SiO2 glasses: influence of cation mixing and cation-network interactions. Chemical Geology 2004;213(1-3):103-113. 87. Harries JE, Hukins DWL, Hasnain SS. Analysis of the EXAFS spectrum of hydroxyapatite. J Phys C: Solid State Phys 1986;19(34):6859-6872. 88. Lipton AS, Heck RW, Primak S, McNeill DR, Wilson DM, Ellis PD. Characterization of Mg2+ Binding to the DNA Repair Protein Apurinic/Apyrimidic Endonuclease 1 via Solid-State 25Mg NMR Spectroscopy. J Am Chem Soc 2008;130(29):9332-9341. 89. Perez-Huerta A, Cusack M, Janousch M, Finch AA. Influence of crystallographic orientation of biogenic calcite on in situ Mg XANES analyses. Journal of Synchrotron Radiation
URI:	http://wrap.warwick.ac.uk/id/eprint/40098

Data sourced from Thomson Reuters' Web of Knowledge

Request changes to a record

Actions (login required)

View Item