Gondwana Research 28 (2015) 858–868
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Phosphate-dependent morphological evolution of hydroxyapatite and implication for biomineralisation Shu-Dong Jiang a, Qi-Zhi Yao b, Yi-Fei Ma a, Gen-Tao Zhou a,⁎, Sheng-Quan Fu c a b c
CAS Key Laboratory of Crust-Mantle Materials and Environments, School of Earth and Space Sciences, University of Science and Technology of China, Hefei 230026, PR China School of Chemistry and Materials Science, University of Science and Technology of China, Hefei 230026, PR China Hefei National Laboratory for Physical Sciences at Microscale, University of Science and Technology of China, Hefei 230026, PR China
a r t i c l e
i n f o
Article history: Received 22 October 2013 Received in revised form 13 April 2014 Accepted 13 April 2014 Available online 2 May 2014 Handling Editor: R.D. Nance Keywords: Hydroxyapatite Phosphate Biomineral Biomimetic mineralisation Biomineralisation
a b s t r a c t Hydroxyapatite (HAP) with various morphologies was prepared, in the absence of biological or organic molecules, through an ammonia gas diffusion method at room temperature. Contrary to the common consensus that crystal morphology control of biominerals is generally achieved by biological or organic molecules, our may also play a crucial role in the special morphogenesis of hydroxyapatite. The results suggest that PO3− 4 morphology, structure and composition of the obtained products were characterised by X-ray diffraction (XRD), field emission scanning electron microscopy (FESEM), transmission electron microscopy (TEM), and high-resolution TEM (HRTEM). The FESEM and TEM analyses demonstrate that at a given concentration of Ca2+, increasing PO34 − concentration leads to the formation of hydroxyapatite with various morphologies ranging from porous flower-like spheres, hollow bur-like spheres to solid bur-like spheres. If the PO34 − concentration remains constant, however, the porous flower-like spheres are always obtained at different concentrations of Ca2 +. For all concentrations of PO34 −, a series of time-resolved experiments reveal that the initial precipitate is always unstable amorphous calcium phosphate (ACP), and that the generation of the different morphologies originates from the dissolution of amorphous calcium phosphate, followed by the crystallisation and self-assembly of hydroxyapatite. Possible mechanisms are proposed for the formation of HAP with the different shapes and architectures. The dependence of HAP morphology on phosphate concentration suggests that, in biomineralisation, biological genetic and physicochemical factors can cooperatively influence the formation of hydroxyapatite with unusual morphologies and hierarchical structures. © 2014 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved.
1. Introduction Calcium phosphates are of great significance in a wide range of fields including geology, chemistry, biology, medicine, and material sciences (Dorozhkin, 2007; Bengtsson et al., 2009; Dorozhkin, 2009, 2010). Geologically, the apatite minerals occur as accessory minerals in almost all igneous rocks, metamorphic rocks, veins and other ore deposits; and most commonly as fine-grained and often impure masses as the chief constituent of phosphate rock. The mineral apatite is one of the major reservoirs of phosphorous in the Earth's crust. As such, apatite plays a critical role in a number of geochemical processes. Apatite strongly influences the concentrations of P, Ca and F in surface, ground, and ocean water, and their rare earth element (REE) contents (Köhler et al., 2005; Goddéris et al., 2006; Harouiya et al., 2007). In biological systems, calcium phosphates occur as the principal inorganic constituent of normal (bones, teeth, fish enameloid, and some species of shells) and pathological (dental and urinary calculus and stones, atherosclerotic lesions) calcifications (LeGeros, 1991, 1994; Hesse and Heimbach, 1999; ⁎ Corresponding author. Tel./fax: +86 551 63600533. E-mail address:
[email protected] (G.-T. Zhou).
Dorozhkin and Epple, 2002). Structurally, they occur mainly in the form of poorly crystallised nonstoichiometric sodium-, magnesium-, and carbonate-containing hydroxyapatite (often called “biological apatite” or dahllite) (Dorozhkin and Epple, 2002; Dorozhkin, 2010). Amongst these compounds, hydroxyapatite, with the ideal chemistry Ca10(PO4)6(OH)2, has also gained considerable attention due to its many functional properties that allow for a wide range of applications such as hard tissue analogues, catalysts, liquid chromatographic columns, and chemical sensors (e.g., Sebti et al., 2002; Vallet-Regi and Gonzalez-Calbet, 2004; Cummings et al., 2009; Liu et al., 2009; Niu et al., 2012). Living organisms are capable of inducing the crystallisation and deposition of a wide variety of minerals (e.g., Lowenstam, 1981; Skinner and Jahren, 2004; Dorozhkin, 2010), but vertebrates mainly utilise the calcium phosphates in constructing their mineral phases both in normal circumstances in bone, dentin, and tooth enamel and in pathological ectopic mineral deposits. The predominant form of the mineral in all situations is biological apatite. However, the extent of mineralisation in a particular tissue or organ is quite variable, and the mineral crystal size and shape, as well as their packing and organisation may also be variable (Rohanizadeh and Legeros, 2007; George and Veis,
http://dx.doi.org/10.1016/j.gr.2014.04.005 1342-937X/© 2014 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved.
S.-D. Jiang et al. / Gondwana Research 28 (2015) 858–868
2008). For example, the basic nanoscale structure of bone consisting of mineralised collagen is usually plate-shaped and exceedingly small (2–4 nm thick and some tens of nanometres long and wide) (e.g., Weiner and Price, 1986; Hu et al., 2010), yet the basic building block of the mature enamel is an enamel rod — a dense array of needle-shaped apatite crystals, roughly 50 nm across and tens of microns long, with their crystalline c-axes aligned along the rods. Rohanizadeh and Legeros (2007) reported that Lingula adamsi shells consist of apatite crystals of varying size, shape, and orientation in different areas of the shell, and two different types of laminae were identified in L. adamsi shells under SEM analysis: compact and stratified laminae. A common consensus is that biological or organic molecules, such as proteins, induce the nucleation of a special polymorph and control the unique morphogenesis of biogenic mineral crystals (e.g., Belcher et al., 1996; Falini et al., 1996; Gower and Tirrell, 1998; Addadi et al., 2006; Politi et al., 2007; Gower, 2008; Mahamid et al., 2008; Tao et al., 2009; Deshpande et al., 2010; Xie and Nancollas, 2010; Yang et al., 2010; Zhou et al., 2010; Gómez-Morales et al., 2011). However, mineral formation in biological tissues always occurs in a fluid phase, which mediates the transport of lattice ions and regular moieties onto crystal surfaces. Some studies involving the various extracellular fluids, which are separated from the mineralising regions of the hard tissues, showed that electrolyte concentrations in a particular tissue or organ have a chemical composition different from that of the other tissues, organs or circulating blood (Howell et al., 1960, 1968; Wuthier, 1969, 1971; Lundgren and Linde, 1987; Larsson et al., 1988; Lundgren et al., 1992; Siqueira et al., 2012). These studies raise the question as to whether physicochemical factors in a particular tissue or organ, such as calcium and phosphate concentrations, ionic strength, solution pH, degree of supersaturation, and even temperature, also contribute to the unique morphogenesis of HAP besides biological or organic molecules. Here, we report on various hierarchical structures of HAP that were prepared through a simple gas diffusion process in an aqueous system without using any organic templates and/or additives at room temperature. The goal of this study is to examine the influence of phosphate on the development of hydroxyapatite morphology and to reveal the possible contribution of phosphate to hydroxyapatite biomineralisation. The study produced hydroxyapatite particles with various morphologies ranging from porous flower-like spheres, hollow bur-like spheres to solid bur-like spheres at different concentrations of PO3− 4 . Since no biological or organic molecules were added in our experiments, this excludes biological factors and highlights the influence of physicochemical factors on the fabrication of hierarchical structures of HAP. Contrary to the common consensus that crystal morphology control of biominerals is generally achieved by biological molecules, our results suggest that crystallite size, crystal shape, and packing and organisation of HAP in a particular tissue or organ may also be related to the local phosphate concentration. 2. Experimental section 2.1. Sample preparation All starting chemicals are of analytical grade and used without further purification; deionised water was used as solvent. CaCl2·2H2O was purchased from Silian Chemicals Ltd. Shanghai, China. (NH4)2HPO4 and NH3·H2O were from Sinopharm Chemical Reagent Co., Ltd. The experiments were carried out at room temperature (22 °C). In a typical procedure, 0.1472 g (1 mmol) of CaCl2·2H2O was dissolved in 20 mL of deionised water with vigorous stirring by a magnetic stirrer to form solution A. Then 0.0792 g (0.6 mmol) of (NH4)2HPO4 was dissolved in 20 mL of deionised water to produce solution B. Solution B was introduced into solution A with continuous stirring, and a white suspension was formed. In order to obtain a clear initial mineralization solution, a small amount of 0.1 M HCl was added dropwise into
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the white suspension while being stirred, and the pH of the initial mineralisation solution was adjusted to 5.0 by addition of 0.1 M HCl or diluted ammonia solution. 25 mL of the homogeneous solution was transferred into a 25-mL beaker with a piece of glass (1.8 cm × 1.8 cm) on the bottom for collecting the precipitate. Each beaker was covered with Parafilm with six punched needle holes and placed in a closed desiccator. 20 mL of diluted ammonia solution was put on the bottom of the desiccator as the source of NH3. A feature of this method is the ability to control the gas diffusion rate (NH3) by simply changing the concentration of the ammonia solution, which regulates the degree of supersaturation in the mineralisation system through the variation of pH. In this manner, confinement of the nucleation and growth of HAP can be achieved, mimicking to a large extent the deposition of HAP in vivo. A similar CO2 gas diffusion method has been extensively applied to the studies on biomimetic mineralisation of CaCO3 minerals (e.g., Albeck et al., 1996; Falini et al., 1996; Pokroy et al., 2006; Zhou et al., 2010). After different mineralisation durations, the beaker was removed from the desiccator, and the piece of glass with the mineralised crystals was separated from the solution, washed with deionised water several times, and allowed to dry at room temperature to obtain the final mineralised product. The dried precipitate was kept in a desiccator for further analysis and characterisation. For other samples, similar procedures were deployed except that the experimental parameters were varied. The detailed experimental parameters and mineralised products are listed in Table 1. 2.2. Mineral detection and characterisation Several analytical techniques were used to characterise the synthesised products. The powder X-ray diffraction (XRD) patterns of the synthesised samples were recorded with a Japan MapAHF X-ray diffractometer equipped with graphite-monochromatised Cu Kα irradiation (λ = 0.154056 nm), employing a scanning rate of 0.02°s−1 in the 2θ range of 3–60°. Infrared (IR) spectrum analyses were made on samples palletised with KBr powders in the range 4000–400 cm−1, using an infrared Fourier transform spectrophotometer (Nicolet, ZOSX). X-ray fluorescence (XRF) was performed on an XRF-1800 X-ray fluorescence spectrometer at room temperature. Microstructures of the products were observed by JEOL JSM-2010 field-emission scanning electron microscopy (FESEM). Selected area electron diffraction (SAED) patterns, high-resolution transmission electron microscopy (HRTEM) images, and transmission electron microscopy (TEM) images were obtained on a Hitachi model H-800 transmission electron microscope with an accelerating voltage of 200 kV. 3. Results and discussion 3.1. Results The phase composition and structure of the mineralised products were first identified by XRD. Fig. 1 shows the typical XRD patterns of the products mineralised for 24 h at phosphate concentrations of 0.015, 0.025 or 0.045 M (samples 1–3), maintaining calcium concentration at 0.025 M. The XRD results reveal that all of the products obtained at the three different concentrations of phosphate are the hexagonal HAP phase with the space group P63/m and lattice parameters a = 9.418 Å, c = 6.884 Å (JCPDS file, No. 09-0432), except that the (002) reflections in our samples are particularly strong and sharp. The stronger (002) reflection is most likely related to the preferential orientation of the HAP along the [001] direction. The broadened diffraction peaks from our products may imply that the mineralised products consist of nanocrystals and/or that slight distortions of the crystal lattice occur in the crystals. Corresponding FT-IR spectra of the products (samples 1–3) are presented in Fig. 2. The broad absorption peak between 2800 and 3800 cm−1 can be attributed to the O–H stretch of water and HAP. The characteristic band for H2O at 1640 cm−1 further indicates the presence of water in these mineralized products, which should
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Table 1 Experimental parameters and mineralized products.a Sample
[PO43+aq]ini (mol/L)
[Ca2+aq]ini (mol/L)
Initial ratio of Ca/P (aq)
Reaction Time (hours)
Product
Morphology
1 2 3 4 S1 S2 S3 5 6
0.015 0.025 0.045 0.045 0.015 0.025 0.045 0.015 0.015
0.025 0.025 0.025 0.025 0.025 0.025 0.025 0.050 0.075
1.667 1 0.556 0.556 1.667 1 0.556 3.333 5.000
24 24 24 120 10 min 10 min 10 min 24 24
HAP HAP HAP HAP ACP ACP ACP HAP HAP
Porous flower-like spheres Hollow bur-like spheres Rods, peanuts, dumbbells and quasi-spheres Solid bur-like spheres Spheroidal aggregates Spheroidal aggregates Spheroidal aggregates Porous flower-like spheres Porous flower-like spheres
a
For all samples, the initial pH of the mineralization solution is 5.0.
originate from the KBr pellet process. The peak around 1044 cm−1 is caused by the asymmetric stretching vibration in the PO34 − group. Two groups of bands in the range 490–630 cm−1 (565, 610 cm−1) are due to bending vibrations of the PO3− group. The peaks at 1387 and 4 869 cm−1 are from CO2− group, indicating incorporation of a trace of 3 CO23 − ions into the crystal structure of HAP, which may be from the mineralisation solution. Therefore, the mineralised products are close to biological apatite (e.g., Dorozhkin and Epple, 2002; Tadic et al., 2002). The composition of the products (samples 1–3) was further identified by XRF. The molar ratio of Ca to P in the three representative samples is 1.62, 1.63, and 1.63, respectively, indicating that their compositions are consistent within experimental error, and close to the Ca/P of 1.667 in ideal stoichiometric HAP (Ca10(PO4)6(OH)2). The morphology and size of the mineralised products were characterised by FESEM and TEM. Fig. 3 depicts the representative FESEM images of hydroxylapatite particles grown for 24 h at different concentrations of phosphate. At a phosphate concentration of 0.015 M (sample 1 in Table 1), all particles exhibit porous flower-like microspheres with an average size of 3.5 μm (Fig. 3A). Further magnification (e.g., Fig. 3B) shows that the microspheres are built with nanoplates that interconnect with each other to form 3 dimensional (3D) flowerlike structures. The thicknesses of the nanoplates determined from the SEM image are ca. 40–50 nm. The representative TEM image of a microsphere (Fig. 3C) further reveals that the nanoplates are almost transparent, although some intersecting black lines can be observed. The nearly transparent feature suggests that the nanoplates are very thin, whereas the intersecting black lines result from the standing projection of the interpenetrating nanoplates, in agreement with the SEM observations (e.g., Fig. 3B). The selected area electron diffraction (SAED) pattern of the product is shown in Fig. 3D. The diffraction rings can be clearly
assigned to the diffractions of the (002), (210), and (112) planes of HAP, further confirming that the microspheres are HAP. The HRTEM image (Fig. 3E) of a nanoplate at the edge of the HAP flower-like nanostructure (boxed in Fig. 3C) shows the continuous lattice fringes in the visible range, indicating its single crystalline nature. The clearly resolved fringes with a lattice spacing of 0.344 nm, which corresponds to the interplanar distance of the {0002} plane of the hexagonally structured apatite and corresponding fast Fourier transform (FFT) dots, demonstrate that the nanoplates are mainly dominated by the {0002} faces. When the phosphate concentration is increased to 0.025 M (sample 2 in Table 1), the panoramic FESEM image (Fig. 4A) shows that a high yield of HAP microspheres (almost 100%) can be harvested under these experimental conditions, with sizes in the range of 2–3 μm. Moreover, hollow structures are indicated by some broken spheres (indicated by arrows). Fig. 4B is the magnified image of a typical hollow microsphere. The more detailed information about the HAP hollow microsphere is shown in Fig. 4C, from which one can see that the hollow HAP particle is a hierarchical nanostructure, and that the entire architecture is constructed of nanoneedles. The TEM image of a random microsphere is shown in Fig. 4D. The distinct contrast between the black margin and light centre further reveals that the HAP sphere has a hollow interior chamber, and the diameter of the hollow chamber and the shell thickness can be determined as 800 and 900 nm, respectively. With the concentration of phosphate increased to 0.045 M (sample 3 in Table 1), a variety of aggregates with different shapes such as rods, peanuts, dumbbells and quasi-spheres can be seen (Fig. 5A–F). A higher magnification of the aggregates (Fig. 6A–D) shows that many small elongate HAP rod bundles are densely arranged in the HAP structures. Moreover, some imprints of tiny bundles can be found on the glass substrate,
Fig. 1. XRD patterns of the products mineralised at different concentrations of PO3− 4 (samples 1–3).
Fig. 2. FT-IR spectra of the products mineralised at different concentrations of PO3− 4 (samples 1–3).
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Fig. 3. SEM (A, B) and TEM images (C), SAED pattern (D), HRTEM image (E), and corresponding FFT pattern of the HRTEM image (inset) of the product mineralised at the PO3− 4 concentration of 0.015 M for 24 h (sample 1).
as shown in the boxed regions in Figs. 5B and 6A. However, after five days of growth (sample 4), microspheres are the dominant morphology, and other morphologies have almost vanished (Fig. 6E, F).
The TEM image of the sphere (Fig. 6G) reveals that it is solid rather than hollow. Fig. 7A shows a TEM image of the typical rod bundles. Fig. 7B and C show magnifications of the two boxed regions in Fig. 7A.
Fig. 4. SEM images (A, B, C) and TEM image (D) of the product mineralised at the PO3− concentration of 0.025 M for 24 h (sample 2). 4
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dumbbell–sphere growth, as described in the self-assembly of fluorapatite aggregates in gelatine gels or in the copolymer-mediated mineralization of metal carbonates (Kniep and Busch, 1996; Busch et al., 1999; Yu et al., 2002; Qu et al., 2011). This growth should start with the seed crystals of HAP, followed by elongation and self-similar branching at both ends of the seeds (Fig. 5B, C), continuing with the anisotropic dumbbell-shaped aggregates on the fractal faces (Fig. 5D), and finally ending up with the symmetrical spherical aggregates (Fig. 5 F). After 10 min of mineralization, spherical aggregates (e.g., Fig. 8A) are always obtained at all three concentrations of phosphate (samples S1– S3 in Table 1). The XRD patterns for samples S1–S3 show that the spherical nanoparticles are amorphous (Fig. 8B). Typical FT-IR spectra of samples S1–S3 are shown in Fig. 8C. The vibrational bands at 1050 cm−1 and 567 cm− 1 can be assigned to PO34 − ν3 and ν4 vibration modes (AlKattan et al., 2011), and the single broad peak at 567 cm− 1 is the most obvious characterisation of the ACP spectrum. The FT-IR spectra further confirm that the early precipitated phase is ACP rather than crystalline calcium phosphates (Li et al., 2007). However, when the phosphate concentration is 0.015 M and calcium concentration is increased from 0.025 to 0.075 M (samples 1, 5 and 6 in Table 1), porous flower-like microspheres with an average size of 3.5 μm are always observed (Figs. 3 and 9), indicating that changes in Ca2 + concentration have no perceptible effect on the morphology of hydroxyapatite under current conditions. 3.2. Discussion
Fig. 5. SEM images (A, B, C, D, E, F) of the product mineralised at the PO43− concentration of 0.045 M for 24 h (sample 3).
The magnified TEM images show that these sections are constructed of rod-like bundles with rugged surfaces and that the nanorods with very high density are radially arranged, generating a laminated structure, which is consistent with the SEM results (e.g., Fig. 6A and B). The lattice structure of the HAP nanorod in the boxed region in Fig. 7C and corresponding fast Fourier transform (FFT) dots are shown in Fig. 7D, from which an interplanar spacing of 0.344 nm for the {0002} of HAP was determined. Thus, the [001] crystallographic directions of the HAP block could be indexed. Interestingly, the broken ring pattern of electron diffraction (Fig. 7E) obtained from the boxed area (inset in Fig. 7E) exhibits 2-fold symmetry. That is to say, the diffraction rings of (002) and (004) are composed of two bright and two dark segments. This means that the crystallographic directions of the nanocrystals in the rod-like bundles are not random but are roughly arranged in the same orientation (Rohanizadeh and Legeros, 2007). In summary, all these results (e.g., Figs. 5, 6, and 7) suggest that the final morphologies of the particles obtained probably originate from a progressive stage of rod–peanut–
Up to now, two main mechanisms have been proposed to explain how crystals form: classical and non-classical crystallisation. In the classical mechanism, crystallisation is based on the addition of atoms/ molecules. After nucleation, further growth of the crystal occurs via an ion-by-ion attachment and unit cell replication, or well-established Ostwald ripening process, which involves the growth of larger crystals at the expense of smaller crystals. In contrast, non-classical crystallisation takes particles as intermediates, and crystal growth occurs through oriented attachment or mesocrystal formation (e.g., Penn and Banfield, 1999; Alivisatos, 2000; Banfield et al., 2000; Penn et al., 2001; Cölfen and Mann, 2003; Cölfen and Antonietti, 2005; Gebauer et al., 2008; Meldrum and Sear, 2008; Pouget et al., 2009; Zhou et al., 2009, 2010). The current findings (Figs. 3A, 4, and 5) show that increasing phosphate concentration is suitable for tailoring the morphology of hierarchical HAP structures, from porous flower-like microspheres through hollow microspheres to solid bur-like spheres. Therefore, it is reasonable to conclude that phosphate is one of the key factors affecting the morphology of final HAP during biomineralisation. Previous studies have indicated that inorganic ions, such as phosphate, magnesium, strontium, lithium, and sulphate, can modify calcium carbonate nucleation, growth, and facet stability (e.g., Reddy and Nancollas, 1976; Titiloye et al., 1991; Tracy et al., 1998; Raz et al., 2000). One assumption is that the inorganic ions selectively stabilise a set of faces of the calcium carbonate crystal through their preferential adsorption/anchoring to these faces, and thus influence the crystal growth. Moreover, the formation and polymorph evolution of calcium carbonate minerals are affected by the presence of phosphate or sulphate in solution, and salinity (e.g., Mucci, 1986; Mucci et al., 1989; Zhou et al., 2009). Addadi et al. (2003) noted that several groups of organisms produce amorphous calcium carbonate mineral phases, which can be stabilised by ions, including phosphate and magnesium, as well as polymers. Herein, for all concentrations of phosphate, the initial precipitates were always unstable ACP (Fig. 8), whereas extended mineralization time led to the formation of various morphological hydroxyapatite including porous flower-like spheres, hollow bur-like spheres and solid bur-like spheres (Figs. 3–7). This indicates that the generation of the various morphologies all experienced initial dissolution of ACP, followed by the crystallisation and self-assembly of hydroxyapatite. For the porous flower-like microspheres obtained at a phosphate concentration of
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Fig. 6. High magnification SEM images (A, B, C, D) of the product mineralised at the PO3− 4 concentration of 0.045 M for 24 h (sample 3) and SEM images (E, F) of the product mineralised at the PO3− concentration of 0.045 M for 120 h (sample 4). 4
0.015 M (sample 1), ACP nanoparticles first formed in solution, and then the crystallisation of HAP was based on these ACP nanoparticles. In solution and without boundaries, ACP nanoparticles will spontaneously aggregate into sphere-like agglomerates (e.g., Fig. 8A). However, the ACP nanoparticles become metastable with respect to the thermodynamically more stable HAP as the supersaturation falls over time in the surrounding solution. Therefore, the amorphous solid nanoparticles become coated with an ultrathin shell of a less-soluble crystalline phase until the system reaches equilibrium with respect to the surface layer. Unlike the external crystalline layer, however, the amorphous core remains out of equilibrium with the surrounding solution due to its higher solubility. Thus the core will dissolve spontaneously, whereas the ACP
solid nanoparticles can act as both the crystalline mineral phase precursor and the sacrificial template for the porous microspheres. Such phase transformation occurs first on the surface of the amorphous solid, followed by the growth and self-assembly of 2D nanoflakes. When the amount of the flakes grows sufficiently, the ACP nanoparticles disappear and an open successive porous structure forms. Therefore, the ACP nanoparticles play an important role as a template for the porous structure of HAP microspheres. When the phosphate concentration is increased to 0.025 M, the hollow bur-like spheres are formed. It has been reported that preferential dissolution of the interior with relatively high surface energy is also achieved by stabilisation of the surface with phosphate ions (Ozaki et al., 1984; Sugimoto et al., 1993; Ocana et al.,
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Fig. 7. TEM images of a typical peanut shape (A), and of the boxed region (B, C) in image A; HRTEM image of the boxed region (D) in image C, and fast Fourier transforms (FFTs) (insets) of the selected areas in image D; and the electron diffraction pattern (E) from the square of the inset.
1995; Jia et al., 2005). Since the external surface of the sphere-like agglomerates (e.g., Fig. 8A) formed by conglomeration of ACP particles is protected by adsorbed phosphate ions, the progressive dissolution and redistribution of matter from the interior to the exterior proceeds until formation of the hollow structure. In addition, the formation of the nanoneedle subunits is in accordance with the intrinsic crystal habit of hexagonal HAP (Markov, 2003; Rakovan, 2008; Peternell et al., 2009; Jiang et al., 2012). The entire structure (Fig. 4D) is constructed of a single layer of radially oriented nanoneedles, self-wrapping to form hollow interiors with the diameter of ca. 800 nm. In the case of the rod–peanut–dumbbell–sphere growth with 0.045 M phosphate (Fig. 5), it is generally recognised that intrinsic electrical forces resulting
from dipole crystals could drive the subunits' organisation into spherocrystals (Kniep and Busch, 1996; Busch et al., 1999). In the biomimetic formation of mesocrystal fluoroapatite (Busch et al., 1999), the basic viewpoint is the presence of intrinsic electric fields which take over control of the growth of the aggregates. This means that the individual “crystals” – the seeds as well as individuals of the following generations – contain a permanent dipole, an assumption which is consistent with observations on the biological significance of electric fields (pyro-, piezoelectricity) during apatite formation under in vivo or biomimetic conditions (Lang, 1966; Basett, 1968; Calvert and Mann, 1997). The polarity of collagen and the structural peculiarity of the apatite family, varying between centrosymmetric and acentric
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Fig. 8. Typical SEM image, XRD patterns and FT-IR spectra of ACP precipitated after 10 min (samples S1-S3).
distribution of the X-species {Ca5(PO4)3X, X = F, Cl, OH} (Bauer and Klee, 1993), support these ideas. Furthermore, Yamashita et al. (1996) showed that in the case of hydroxyapatite, polarizability is caused by a reorientation of the dipole moments of the OH− ions within the structural channels. Therefore, as one of the members of the apatite mineral family, the hydroxyapatite crystal would unavoidably control the growth of the aggregates by intrinsic electric fields. Moreover, compared with other possible candidates for the driving force (e.g. van der Waals forces), the electric dipolar interaction is stronger and can act over a longer range (Tang et al., 2002; Wang et al., 2005), and when the size of the subunits exceeds 10 nm, van der Waals forces would become negligible in driving the self-assembly of subunits (Wei, 2006;
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Zhou et al., 2009; Qu et al., 2011). Therefore, the intrinsic electrical forces between the crystallites are believed to be responsible for the aggregation of hydroxyapatite subunits. Consequently, once the ACP nanoparticles begin to dissolve and then HAP crystallises, under the control of intrinsic electric fields of the HAP crystallites, the individual HAP nanoparticles can attract each other to form the nanorod units. Subsequently, stacking of the subunits and a possible splitting growth lead to the formation of dumbbells and spheres. Biomineralisation widely occurs in a fluid phase under mild conditions such as almost neutral pH and ambient temperature, when the fluid medium can mediate the transport of lattice ions and regulatory moieties onto crystal surfaces. Therefore, all our experiments were carried out in aqueous solution at room temperature, and the NH3 diffusion technique was used to control the nucleation and growth of the minerals. Under current experimental conditions, all concentrations of phosphate always lead to the initial precipitation of unstable ACP (e.g., Fig. 8), and subsequently the ACP transforms into different morphological and organised hydroxyapatite (Figs. 3–5), indicating that a dissolution– recrystallisation process mediates the crystallisation transformation from precursor ACP to secondary HAP. It appears that water in the mineralization system also plays a key role in the formation of different morphological HAPs. In addition, it is well known that the apatite crystal has a primitive hexagonal structure with space group P63/m. In geologic apatites, particularly those that have grown from a melt or hydrothermal solution, the morphology is usually rather simple, such as short idiomorphic prismatic, sheet-like, granular and colloidal (Liu, 1990; Rakovan, 2008; Peternell et al., 2009). However, the morphologies and textures of apatite in bone and other hard tissues are extraordinarily complex, significantly departing from typical crystal habits of their geological counterparts. For example, in bone, a family of materials built up from mineralized collagen with highly complex intergrowths of apatite and organics, up to seven hierarchical levels of organisation have been identified (e.g., Boskey, 2007; Pasteris et al., 2008; Beniash et al., 2009; Dove, 2010). Crystal morphology in biominerals is key to their function, and is tightly controlled in many biomineralisation systems. A common consensus is that biological or organic molecules induce the nucleation of special polymorphs and control the unique morphogenesis of biogenic mineral crystals. For instance, the organic matrix that forms enamel is thought to regulate the shape and organisation of mineral particles (Fincham et al., 1999; Margolis et al., 2006), which consists of a number of proteins, with amelogenin, the major enamel protein, constituting more than 90 wt.% of the enamel matrix. On the other hand, biochemists have long recognised that the local solvation environment around biomolecules regulates the ability of calcium, and to some extent, magnesium to activate a variety of cellular functions (Dove, 2010), and there is recent evidence that the local solvation environment around biomolecules can also modulate mineralisation (Elhadj et al., 2006; Kowacz and Putnis, 2008; Stephenson et al., 2008; Dove, 2010). Moreover, physicochemical factors in a particular tissue or organ, such as calcium and phosphate concentrations, temperature, ionic strength, solution pH, and degree of supersaturation, are quite variable (Howell et al., 1960, 1968; Wuthier, 1969, 1971; Lundgren and Linde, 1987; Larsson et al., 1988; Lundgren et al., 1992; Siqueira et al., 2012). Hence, the physicochemical factors in the mineralisation surroundings may also influence and control the crystallisation and organisation of biominerals. Since no bio- or organic molecules were used in our experiments, and only phosphate or calcium concentration was changed, biological and/or macromolecule factors are excluded, highlighting the influence of the purely inorganic factors on the fabrication of hierarchical structures of HAP. Previous studies have showed that phosphate exerts a much more significant impact on the precipitation of apatite crystals than calcium in the normally mineralized tissues (Robison, 1923; Kay and Robison, 1924; Robison and Soames, 1924; Fell and Robison, 1934), which is attributed to the fact that apatite is structurally an inorganic phosphate crystal, and that calcium can be replaced in the apatite lattice by many
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Fig. 9. SEM images of the products obtained at the Ca2+ concentration of 0.025 M (A, sample 5) or 0.045 M (B, sample 6) while the PO3− concentration kept at 0.015 M. 4
other cations such as lead, barium and manganese. Recently, Schäck et al. (2013) reported that phosphate influences gene expression and quality of mineralisation. However, information on the effect of phosphate on the morphogenesis of HAP is less extensive. Intriguingly, in our experiments, increasing phosphate concentration from 0.015 to 0.045 M led to the formation of various morphologies changing from porous flower-like spheres, hollow bur-like spheres to solid bur-like spheres (Figs. 3–5). In addition, at a given concentration of phosphate, the porous flower-like spheres were always obtained at different concentrations of calcium (Fig. 9). It therefore appears that our results reveal a much stronger dependence of HAP morphology on phosphate concentration than on Ca2+ cations. Nevertheless, many reports have also shown that bio-/organic molecules, such as amino acids, gelatine collagen, polyaspartic acid and citric acid can affect the morphology of HAP crystallites (e.g., Kniep and Busch, 1996; López-Macipe et al., 1998; Busch et al., 1999; Spanos et al., 2001; Busch et al., 2003; Bigi et al., 2004; Gonzalez-McQuire et al., 2004; Tao et al., 2007; Martins et al., 2008; Diegmueller et al., 2009; Jiang et al., 2009, 2012). For example, Tao et al. (2007) reported that biomolecules such as Gly, Glu, and amelogenin are the effective regulators of the biological construction and control the reorganisation behaviours of HAP nanocrystals. Our results indicate that, in addition to bio- or organic molecules, phosphate concentrations should also affect the different morphogenesis and assembled structures of HAP. Moreover, it is well-known that electrolyte concentrations such as calcium and phosphate concentrations in a particular tissue or organ have a chemical composition different from that of the other tissues, organs or circulating blood. Combined with the results mentioned above, our results suggest that the concentration of phosphate may also contribute to the special morphogenesis of HAP in biomineralisation of a particular tissue or organ. These data serve to deepen our insight into biomineralisation. 4. Conclusions In this study, HAP with various morphologies was prepared via an ammonia gas diffusion method at room temperature and in the absence of bio- or organic molecules. The results show that at a given concentration of calcium, increasing phosphate concentration leads to the morphological evolution of HAP from porous flower-like microspheres, through hollow bur-like spheres to solid bur-like spheres. Furthermore, a series of time-resolved experiments show that the initial precipitate is an unstable ACP, and that the generation of the different morphologies of HAP all experience initial dissolution of ACP, and subsequent crystallisation and self-assembly of HAP. The complex morphogenesis and phosphate-dependence of HAP under experimental conditions indicates that, in addition to bio-/organic molecules, phosphate
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