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New Insights into the Ultrastructure of Bioapatite After Partial Dissolution: Based on Whale Rostrum, the Densest Bone

Published online by Cambridge University Press:  10 October 2019

Lingyi Tang ,
Li Zhang ,
Michael Yue ,
Da Tian ,
Mu Su  and
Zhen Li Open the ORCID record for Zhen Li [Opens in a new window]
Lingyi Tang
Affiliation:
College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China
Li Zhang
Affiliation:
College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China
Michael Yue
Affiliation:
University of Maryland School of Medicine, Baltimore, MD 21201, USA
Da Tian
Affiliation:
College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China
Mu Su
Affiliation:
College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China
Zhen Li*
Affiliation:
College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China State Key Laboratory for Mineral Deposits Research, Nanjing University, Nanjing, Jiangsu 210046, China
*
*Author for correspondence: Zhen Li, E-mail: [email protected]
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Abstract

Mineral particles in bone are interlaced with collagen fibrils, hindering the investigation of bioapatite crystallites (BAp). This study utilized a special whale rostrum (the most highly mineralized bone ever recorded) to measure the crystallites of bone BAp via long-term dissolution in water. The BAp in the rostrum has a low solubility (6.7 ppm Ca and 3.8 ppm P after 150 days dissolution) as well as in normal bones, which leads to its Ksp value of ~10−53. Atomic force microscopy results show tightly compacted mineral crystallites and confirm the low amount of collagen in the rostrum. Additionally, the mineral crystallites demonstrate irregular plate-like shapes with variable sizes. The small crystallites (~11 × 24 nm) are easily detached from BAp prisms, compared with the large crystallites (~50 nm). Moreover, various orientations of crystallites are observed on the edge of the prisms, which suggest a random direction of mineral growth. Furthermore, these plate-like crystallites prefer to be stacked layer by layer under weak regulation from collagen. The morphology of rostrum after dissolution provides new insights into the actual morphology of BAp crystallites.

Keywords

bioapatitedissolutionHRTEMmorphologyrostrum
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 25 , Issue 6 , December 2019 , pp. 1323 - 1330
Copyright
Copyright © Microscopy Society of America 2019 

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References

Alexander, B, Daulton, TL, Genin, GM, Lipner, J, Pasteris, JD, Wopenka, B & Thomopoulos, S (2012). The nanometre-scale physiology of bone: Steric modelling and scanning transmission electron microscopy of collagen-mineral structure. J R Soc Interface 9(73), 1774–1786.Google Scholar
Anderson, HC, Garimella, R & Tague, SE (2005). The role of matrix vesicles in growth plate development and biomineralization. Front Biosci 10, 822–837.Google Scholar
Baig, AA, Fox, JL, Wang, Z, Higuchi, WI, Miller, SC, Barry, AM & Otsuka, R (1999). Metastable equilibrium solubility behavior of bone mineral. Calcif Tissue Int 64(4), 329–339.Google Scholar
Barry, AB, Baig, AA, Miller, SC & Higuchi, WI (2002). Effect of age on rat bone solubility and crystallinity. Calcif Tissue Int 71(2), 167–171.Google Scholar
Bocciarelli, DS (1970). Morphology of crystallites in bone. Calcif Tissue Res 5(3), 261–269.Google Scholar
Brzezinska-Miecznik, J, Haberko, K, Sitarz, M, Bucko, MM & Macherzynska, B (2015). Hydroxyapatite from animal bones - Extraction and properties. Ceram Int 41(3), 4841–4846.Google Scholar
Burger, C, Zhou, HW, Wang, H, Sics, I, Hsiao, BS, Chu, B, Graham, L & Glimcher, MJ (2008). Lateral packing of mineral crystals in bone collagen fibrils. Biophys J 95(4), 1985–1992.Google Scholar
Cazalbou, S, Combes, C, Eichert, D & Rey, C (2004). Adaptative physico-chemistry of bio-related calcium phosphates. J Mater Chem 14(14), 2148–2153.Google Scholar
Chen, W, Wang, Q, Meng, S, Yang, P, Jiang, L, Zou, X, Li, Z & Hu, S (2017). Temperature-related changes of Ca and P release in synthesized hydroxylapatite, geological fluorapatite, and bone bioapatite. Chem Geol 451, 183–188.Google Scholar
Cho, GY, Wu, YT & Ackerman, JL (2003). Detection of hydroxyl ions in bone mineral by solid-state NMR spectroscopy. Science 300(5622), 1123–1127.Google Scholar
Currey, JD (2002). Bones: Structure and Mechanics. Princeton, New Jersey, USA: Princeton University Press.Google Scholar
Daculsi, G, Bouler, JM & Legeros, RZ (1997). Adaptive crystal formation in normal and pathological calcifications in synthetic calcium phosphate and related biomaterials. In International Review of Cytology - A Survey of Cell Biology, vol. 172, Jeon, KW (Ed.), pp. 129–191. San Diego: Elsevier Academic Press Inc.Google Scholar
Deymier, AC, Nair, AK, Depalle, B, Qin, Z, Arcot, K, Drouet, C, Yoder, CH, Buehler, MJ, Thomopoulos, S, Genin, GM & Pasteris, JD (2017). Protein-free formation of bone-like apatite: New insights into the key role of carbonation. Biomaterials 127, 75–88.Google Scholar
Dorozhkin, SV (2002). A review on the dissolution models of calcium apatites. Prog Cryst Growth Charact Mater 44(1), 45–61.Google Scholar
Elliott, JC (2002). Calcium phosphate biominerals. In Phosphates: Geochemical, Geobiological, and Materials Importance, Kohn, MJ, Rakovan, J & Hughes, JM (Eds.), pp. 427–453. Washington, DC: Mineralogical Society of America.Google Scholar
Eppell, SJ, Tong, WD, Katz, JL, Kuhn, L & Glimcher, MJ (2001). Shape and size of isolated bone mineralites measured using atomic force microscopy. J Orth Res 19(6), 1027–1034.Google Scholar
Fernandez-Moran, H & Engstrom, A (1957). Electron microscopy and x-ray diffraction of bone. Biochim Biophys Acta 23(2), 260–264.Google Scholar
Finean, JB & Engstrom, A (1957). Apatite crystallites in bone. Biochim Biophys Acta 23(1), 202–202.Google Scholar
Francis, MD (1965). Solubility behavior of dental enamel and other calcium phosphates. Ann N Y Acad Sci 131(2), 694–712.Google Scholar
Fulmer, MT, Ison, IC, Hankermayer, CR, Constantz, BR & Ross, J (2002). Measurements of the solubilities and dissolution rates of several hydroxyapatites. Biomaterials 23(3), 751–755.Google Scholar
Glimcher, M (1959). Molecular biology of mineralized tissues with particular reference to bone. Rev Modern Phys 31(2), 359–393.Google Scholar
Glimcher, MJ (2006). Bone: Nature of the calcium phosphate crystals and cellular, structural, and physical chemical mechanisms in their formation. In Medical Mineraology and Geochemistry, Sahai, N & Schoonen, MAA (Eds.), pp. 223–282. Chantilly: The Mineralogical Society of America & Geochemical Society.Google Scholar
Hughes, JM, Cameron, M & Crowley, KD (1989). Structural variations in natural F, OH, and CL apatites. Am Mineral 74(7–8), 870–876.Google Scholar
Karampas, IA, Orkoula, MG & Kontoyannis, CG (2012). Effect of hydrazine based deproteination protocol on bone mineral crystal structure. J Mater Sci Mater Med 23(5), 1139–1148.Google Scholar
Kim, HM, Rey, C & Glimcher, MJ (1995). Isolation of calcium-phosphate crystals of bone by nonaqueous methods at low-temperature. J Bone Miner Res 10(10), 1589–1601.Google Scholar
Landis, WJ, Hodgens, KJ, Song, MJ, Arena, J, Kiyonaga, S, Marko, M, Owen, C & Mcewen, BF (1996). Mineralization of collagen may occur on fibril surfaces: Evidence from conventional and high-voltage electron microscopy and three-dimensional imaging. J Struct Biol 117(1), 24–35.Google Scholar
Legeros, RZ (1981). Apatites in biological systems. Progr Cryst Growth Charact 4(1), 1–45.Google Scholar
Li, Z & Pasteris, JD (2014). Chemistry of bone mineral, based on the hypermineralized rostrum of the beaked whale Mesoplodon densirostris. Am Mineral 99(4), 645–653.Google Scholar
Li, Z, Pasteris, JD & Novack, D (2013). Hypermineralized whale rostrum as the exemplar for bone mineral. Connect Tissue Res 54(3), 167–175.Google Scholar
Luttge, A (2006). Crystal dissolution kinetics and Gibbs free energy. J Electron Spectrosc Relat Phenom 150(2-3), 248–259.Google Scholar
Nudelman, F, Pieterse, K, George, A, Bomans, PHH, Friedrich, H, Brylka, LJ, Hilbers, P, De With, G & Sommerdijk, N (2010). The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors. Nat Mater 9(12), 1004–1009.Google Scholar
Ren, F, Leng, Y, Ding, Y & Wang, K (2013). Hydrothermal growth of biomimetic carbonated apatite nanoparticles with tunable size, morphology and ultrastructure. CrystEngComm 15(11), 2137.Google Scholar
Rey, C, Collins, B, Goehl, T, Dickson, IR & Glimcher, MJ (1989). The carbonate environment in bone-mineral - A resolution-enhanced fourier-transform infrared-spectroscopy study. Calcif Tissue Int 45(3), 157–164.Google Scholar
Rey, C, Combes, C, Drouet, C, Lebugle, A, Sfihi, H & Barroug, A (2007). Nanocrystalline apatites in biological systems: Characterisation, structure and properties. Materialwiss Werkstofftech 38(12), 996–1002.Google Scholar
Rho, JY, Kuhn-Spearing, L & Zioupos, P (1998). Mechanical properties and the hierarchical structure of bone. Med Eng Phys 20(2), 92–102.Google Scholar
Rogers, KD & Zioupos, P (1999). The bone tissue of the rostrum of a Mesoplodon densirostris whale: A mammalian biomineral demonstrating extreme texture. J Mater Sci Lett 18(8), 651–654.Google Scholar
Rootare, HM, Deitz, VR & Carpenter, FG (1962). Solubility product phenomena in hydroxyapatite-water systems. J Colloid Sci 17(3), 179–206.Google Scholar
Schwarcz, HP, Abueidda, D & Jasiuk, I (2017). The ultrastructure of bone and its relevance to mechanical properties. Front Phys 5, 39. doi: 10.3389/fphy.2017.00039.Google Scholar
Snoeck, C & Pellegrini, M (2015). Comparing bioapatite carbonate pre-treatments for isotopic measurements: Part 1-Impact on structure and chemical composition. Chem Geol 417, 394–403.Google Scholar
Suvorova, EI & Madsen, HEL (1999). Observation by HRTEM the hydroxyapatite–octacalcium phosphate interface in crystals grown from aqueous solutions. J Cryst Growth 198(3), 677–681.Google Scholar
Tomazic, BB, Brown, WE & Eanes, ED (1993). A critical-evaluation of the purification of biominerals by hypochlorite treatment. J Biomed Mater Res 27(2), 217–225.Google Scholar
Tong, W, Glimcher, MJ, Katz, JL, Kuhn, L & Eppell, SJ (2003). Size and shape of mineralites in young bovine bone measured by atomic force microscopy. Calcif Tissue Int 72(5), 592–598.Google Scholar
Traub, W, Arad, T & Weiner, S (1989). 3-Dimensional ordered distribution of crystals in turkey tendon collagen-fibers. Proc Natl Acad Sci USA 86(24), 9822–9826.Google Scholar
Wachtel, E & Weiner, S (1994). Small-angle X-ray-scattering study of dispersed crystals from bone and tendon. J Bone Miner Res 9(10), 1651–1655.Google Scholar
Wang, LJ & Nancollas, GH (2008). Calcium orthophosphates: Crystallization and dissolution. Chem Rev 108(11), 4628–4669.Google Scholar
Wang, LJ, Nancollas, GH, Henneman, ZJ, Klein, E & Weiner, S (2006). Nanosized particles in bone and dissolution insensitivity of bone mineral. Biointerphases 1(3), 106–111.Google Scholar
Wang, Y, Azais, T, Robin, M, Vallee, A, Catania, C, Legriel, P, Pehau-Arnaudet, G, Babonneau, F, Giraud-Guille, MM & Nassif, N (2012). The predominant role of collagen in the nucleation, growth, structure and orientation of bone apatite. Nat Mater 11(8), 724–733.Google Scholar
Weiner, S (2008). Biomineralization: A structural perspective. J Struct Biol 163(3), 229–234.Google Scholar
Weiner, S & Price, PA (1986). Disaggregation of bone into crystals. Calcif Tissue Int 39(6), 365–375.Google Scholar
Zhu, YN, Zhang, XH, Chen, YD, Xie, QL, Lan, JK, Qian, MF & He, N (2009). A comparative study on the dissolution and solubility of hydroxylapatite and fluorapatite at 25 °C and 45 °C. Chem Geol 268(1–2), 89–96.Google Scholar
Zylberberg, L, Traub, W, De Buffrenil, V, Allizard, F, Arad, T & Weiner, S (1998). Rostrum of a toothed whale: Ultrastructural study of a very dense bone. Bone 23(3), 241–247.Google Scholar