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Ultrafast bone-like apatite formation on bioactive tricalcium silicate cement using mussel-inspired polydopamine
Ceramics International 45 (2019) 3033–3043
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Ceramics International journal homepage: www.elsevier.com/locate/ceramint
Ultrafast bone-like apatite formation on bioactive tricalcium silicate cement using mussel-inspired polydopamine
T
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Meng Wu, Tao Wang , Yangyang Wang, Hui Wang College of Material Science and Technology, Nanjing University of Aeronautics and Astronautics, Nanjing 210016, China
A R T I C LE I N FO
A B S T R A C T
Keywords: Tricalcium silicate Polydopamine Bone-like apatite Biomaterials Attachment mechanism Carbonated hydroxyapatite
The growing bone-like apatite layer at the tissue-implant interface is the essential condition for materials to bond robustly to surrounding bone and may provide a favorable environment for living bone formation. Inspired by versatility of mussel adhesive proteins, we developed an ultrafast and accessible route to accelerate effectively the formation of amorphous calcium phosphate (ACP), the precursor phase of bone-like apatite, on the surface of polydopamine (PDA)-coated tricalcium silicate (TCS) within 5 min in simulated body fluid (SBF). The key of the method lies in successful preparation of PDA coating on the surface of hydrated TCS by simple dip-coating of hydrated TCS in an aqueous solution of dopamine. A strong adsorption between PDA coating and surface of hydrated TCS could be formed via bidentate hydrogen and electrostatic bonds. After 7 d of soaking in SBF, the bone-like apatite layer on the surface of PDA-coated TCS disk, about 91.1 µm in height was thicker than that on the surface of pristine TCS disk, determining about 49.5 µm. The results indicate that PDA coating can facilitate the kinetic deposition of bone-like apatite on its surface. The abundant Ca2+ ions and the lower interface energy of ACP at the interface between ACP and surfaces of PDA-coated TCS disks are responsible for the ultrafast precipitation of ACP and formation of bone-like apatite layer which is carbonated hydroxyapatite (HA) confirmed by different analytical tools. The route can open avenues for development of PDA-coated TCS biomaterials for hard tissue repair and substitution.
1. Introduction Materials science dedicated to use of a large variety of materials to biomedical applications is of prime importance to tissue engineering, a multidisciplinary field of research that utilizes strategies of engineering sciences, biology, and chemistry to repair tissue of living tissues [1]. In the last few decades, considerable efforts have been made to develop many different types of biomaterials including polymers, ceramics, metals and composites for diverse clinical applications in tissue replacement and regeneration [2]. Notably, tricalcium silicate (TCS), a Sicontaining third generation biomaterial that can stimulate specific cellular responses and regeneration of living tissues, has recently been an intensive biomaterial of research for bone and tooth defect repair and substitution owing to its sufficient physicochemical properties and excellent bone bioactivity [3,4]. The bone-bonding bioactivity is the capability to chemically bond with the surrounding tissues through the formation of bone-like apatite layer, a c-axis-oriented hydroxyapatite (HA) crystals, at the tissue-biomaterial interface when in contact with physiological fluids [5]. Interestingly, this growth behavior of bone-like apatite resembles that found in natural bone mineral to form
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sophisticated hierarchical structures with collagen fibrils resulting in fascinating physicochemical properties, where the c-axes of carbonated HA crystals are spatially aligned with the long axes of the collagen fibrils [6–10]. It has been generally accepted that the rate of apatite formation can indicate the degree of in vivo bone bioactivity of the material. Typically, the bone-bonding ability of TCS can be determined by monitoring bone-like apatite layer formation on its surface in a simulated body fluid (SBF) with ion concentrations similar to those of human blood plasma [11]. Most studies on bioactive TCS focus on the enhancement of the physicomechanical properties (a shorter setting time, good injectability, improved mechanical strength and enhanced washout resistance) by blending a myriad of additives [12–15] and the extension of scope for applications such as using as injectable biomaterials, bioceramics and scaffolds [16–18]. Nevertheless, there are a smaller amount of literatures on accelerating the kinetic deposition process of biologically active apatite that not only increases cell adhesion and improves the mitotic activity of the cells [19], but also plays a key role in the enhancement of bone-bonding ability and bone growth [20]. Therefore, it is greatly meaningful to devote efforts to promoting
Corresponding author. E-mail address: [email protected] (T. Wang).
https://doi.org/10.1016/j.ceramint.2018.10.149 Received 12 September 2018; Received in revised form 17 October 2018; Accepted 17 October 2018 Available online 18 October 2018 0272-8842/ © 2018 Elsevier Ltd and Techna Group S.r.l. All rights reserved.
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2.3. Determination of the rate of apatite formation
ultrafast apatite formation on bioactive TCS in terms of its applications in hard tissue engineering. Inspired by versatility of mussel adhesive proteins, polydopamine (PDA) coatings that can attach to a broad variety of surfaces have achieved widespread success for a multitude of biomedical applications [21]. More recently, a route of PDA-assisted HA formation that can effectively induce and accelerate the deposition of HA on non-bioactive interfaces, including noble metals, semiconductors, ceramics and polymers has been verified [22–24]. Moreover, a study has demonstrated that PDA coatings remarkably promoted demineralized dentin remineralization, and all dentin tubules were occluded by densely packed HA crystals [25]. Despite some publications on non-bioactive interfaces, the surface of hydrated TCS has not been investigated yet. In addition, there has been a limitation of understanding of adhesion mechanism between PDA and the surface of hydrated TCS, and the mechanism of bone-like apatite formation on PDA-coated TCS was not proposed either. Herein, we report an ultrafast and accessible route to accelerate effectively the formation of amorphous calcium phosphate (ACP), which is a crucial intermediate that undergoes subsequently the transformation into biological apatite in osteogenesis [26], on the surface of PDA-coated TCS within several minutes under physiological conditions. The key of the method lies in successful preparation of PDA coating on the surface of hydrated TCS by simple dip-coating of hydrated TCS in an aqueous solution of dopamine. The abundant catecholamine moieties in PDA concentrate Ca2+ ions at the interface and thus facilitate the nucleation of ACP. Additionally, the lower interface energy of ACP at the interface between ACP and the surface of PDAcoated TCS is also advantageous to the precipitation of ACP. The attachment mechanism between PDA coating and surface of hydrated TCS and the mechanism of bone-like apatite formation on PDA-coated TCS were also investigated in detail.
To evaluate the rate of apatite formation on the TCS disks and PDAcoated TCS disks, they were immersed in the SBF at 37 °C for a predetermined time period, and the ratio of the surface area of disk to volume of the SBF was 10 cm−1. The SBF was prepared in the light of the method described by Kokubo [11] and its ion concentrations were as follows: 142.0 mM Na+, 5.0 mM K+, 1.5 mM Mg2+, 2.5 mM Ca2+, 147.8 mM Cl−, 4.2 mM HCO3−, 1.0 mM HPO42−, 0.5 mM SO42−. The SBF was refreshed every 3 days. After soaking for the desired time, the disks were extensively rinsed with deionized water followed by drying at 60 °C in a vacuum oven. 2.4. Characterizations The PDA coating on the surface of TCS disk was characterized using X-Ray photoelectron spectroscopy (XPS; Omicron, Taunusstein, Germany) with Al Kα (1486.8 eV) 300 W X-ray source. Fourier transform infrared (FTIR; Nicolet Co., USA) analyses with a resolution of 4 cm−1 in the spectral range of 4000–400 cm−1 were performed to determine the surface chemical functionality of the PDA-coated TCS disk and bone-like apatite layer. The surface topography of PDA-coated TCS disk was analyzed by atomic force microscopy (AFM; Seiko Instruments, Japan). The morphological changes of apatite mineralization on the surfaces of different disks were investigated with a field-emission scanning electron microscope (FESEM; Hitachi High Technologies Co., Japan). Phase composition analysis was carried out on bone-like apatite using X-ray diffraction (XRD; Rigaku Co., Japan) with Cu Ka radiation at 40 mA and 45 kV. The surface morphologies and microstructures of the bone-like apatite were analyzed using transmission electron microscope (TEM, JEOL, Co., Japan). The concentrations of Calcium (Ca) and phosphorus (P) in the SBF after soaking for pre-selected time period were measured using inductively coupled plasma atomic emission spectroscopy (ICP-AES; Varian Co., USA). In addition, pH values of the storage solution were determined using an electrolyte-type pH meter (SX-620, Sanxin Instruments Co., Shanghai, China).
2. Experimental section 2.1. Materials
3. Results and discussion
TCS powders were prepared by the wet-chemical method as previously reported [27]. Briefly, 0.2 mol Si(OC2H5)4 (TEOS) was added into a mixture of 80 ml deionized water and 1 mol anhydrous ethanol. Then, the solution was adjusted by nitric acid and pH was 1–2 under continuous stirring at room temperature. After mixing uniformly, 0.6 mol CaC2O4 was put into the solution and the mixture was stirred by a magnetic stirrer at 60 °C for 2 h, followed by drying at 120 °C. The sample was sintered at 1450 °C for 6 h and ground using ball milling for 3 h at the speed of 350 r/min. Hereafter, the resulting powders were sieved to 300-mesh for further experiments. Dopamine hydrochloride was purchased from Sigma-Aldrich and other chemical reagents used in the experiments were of analytical grade.
It is well accepted that the hydraulic property of TCS, which can react with water to form Ca(OH)2 and calcium silicate hydrate (CSH), is responsible for a wide array of applications. Fig. 1 (A) shows the FTIR spectra of TCS disk, PDA and PDA-coated TCS disk. In the FTIR spectrum of TCS disk, a narrow and sharp peak at 3644 cm−1 corresponded to the stretching vibration of hydroxyl group indicating the presence of Ca(OH)2. In addition, the intensive peak at 966 cm−1 was assigned to Si-O stretching vibration implying the presence of CSH [28]. The PDA peak at 1600 cm−1 was due to the overlap of the C˭C resonance vibrations in the aromatic ring and the N–H bending vibrations of the amide group. The peak at 1502 cm−1 was attributed to the N–H shearing vibrations of the amide group [29–31]. After PDA modification, the peak at 3644 cm−1 was disappeared and intensity of the peak at 966 cm−1 weakened. Moreover, the characteristic peaks of PDA were also appeared in corresponding region in the FTIR spectrum of PDAcoated TCS disk, which verified the existence of PDA coating on TCS disk. The chemical constituents of TCS disk after soaking in dopamine solution were further investigated. XPS wide spectra of TCS disk before and after PDA modification are shown in Fig. 1(B). The significant differences between two XPS spectra were the absence of silicon peaks (Si 2p and Si 2s) and the presence of nitrogen peak (N 1s) in the XPS spectrum of the PDA-coated TCS disk. High resolution XPS of Si 2p and N 1s peaks for TCS disk and PDA-coated TCS disk were more apparent (Fig. 1(C) and (D)). Furthermore, the intensity of O 1s, Ca 2s and Ca 2p peaks of original TCS disk decreased following the surface modification of PDA, indicating the formation of PDA layer on the surfaces of TCS
2.2. Preparation of TCS disks and PDA-coated TCS disks The 1-day-set TCS disks with a height of 2 mm and a diameter of 10 mm were prepared. Firstly, TCS powders were mixed with deionized water at a liquid/solid of 0.5. Then, freshly mixed cement pastes were cast in stainless steel molds and stored in a 37 °C, 100% humidity water bath for 1 d. To prepare PDA-coated TCS disks, TCS disks were immersed in PDA solution formed by an oxidative polymerization of dopamine-hydrochloride (2 mg/ml in 10 mM Tris, pH 8.5) for 24 h at 37 °C. Simultaneously, the 1-day-set TCS disks were soaked in Tris (pH 8.5) for 24 h at 37 °C to keep similar degree of hydration for different TCS disks. After soaking, as-prepared TCS disks with and without PDA coatings were rinsed with deionized water and dried at 60 °C in a vacuum oven. 3034
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Fig. 1. (A) FTIR spectra of TCS disks, PDA and PDA-coated TCS disks. (B) XPS wide spectra of TCS disks before and after PDA modification, high resolution XPS of (C) nitrogen peak (N 1s) and (D) silicon peak (Si 2p) for TCS disks and PDA-coated TCS disks.
disks. The AFM topographies and the surface roughness of TCS disks before and after PDA modification are presented in Fig. 2. It was obvious that the surface morphologies were significantly changed and the average surface roughness values increased from 22.34 nm to 37.48 nm in comparison with that of the pristine TCS disk, which suggested the formation of PDA coating on TCS disks. The results of the FTIR, XPS and AFM analyses reveal that the PDA coating could deposit on TCS disks via a dip-coating process of the disks in an aqueous solution of dopamine. It is known that catechol in PDA or other catecholic derivatives plays a crucial role in attaching to virtually any type of materials through forming strong covalent or noncovalent interactions with substrates [32,33]. In essence, the specific attachment mechanism depends mainly on the relationship between substrates and catecholic groups. As mentioned above, when TCS particles are in contact with water, an amorphous nanostructured hydration product namely CSH is deposited on the surface of original TCS, while Ca(OH)2 crystals nucleate and grow in the available capillary pore space resulting in a highly alkaline environment. CSH is a porous, non-stoichiometric and tobermorite-like structural silicate chain layer possessing silanol (SiOH) functions [34–36]. The Si-OH groups on the surface of CSH are attacked by OH− ions to form SiO− groups (Fig. 3(A1)), and therefore produce negatively charged surface surrounded by Ca2+ ions via electrostatic interactions [37–40]. Due to continuous release of Ca2+ and OH−, the surfaces reveal an inversion of the zeta potential in the solutions of pH > 11.6 [41]. Fig. 3(B1) shows the proposed binding mechanism of PDA to the negatively charged CSH surface. Although the exact adhesion mechanism is unconfirmed now, previous studies [42–44] have verified that OH
Fig. 2. AFM topographies and the surface roughness of (A) TCS disk and (B) PDA-coated TCS disk. Sa: average surface roughness; Sq: root mean square.
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Fig. 3. Digital images of (A) TCS disk and (B) PDA-coated TCS disk, (A1) schematic illustration for the surface of hydrated TCS disk. CSH is negatively charged at alkaline pH, surrounded by Ca2+ ions (not shown for clarity). (B1) proposed binding mechanism of PDA to the CSH surface.
Fig. 4. SEM micrographs of (A-D) TCS disks and (A1-D1) PDA-coated TCS disks after soaking in SBF for (A-A1) 5, (B-B1) 10, (C-C1) 20 and (D-D1) 30 min. The scale bar represents 3 µm.
Fig. 5. SEM micrographs of (A-D) TCS disks and (A1-D1) PDA-coated TCS disks after soaking in SBF for (A-A1) 60, (B-B1) 120, (C-C1)180 and (D-D1) 360 min. The scale bar represents 3 µm.
of PDA make it potentially ampholytic or zwitterionic. It is negatively charged because of partial ionization of OH groups in PDA at alkaline pH [45]. The partially ionized OH groups of PDA interact via electrostatic interactions with the Ca2+ ions which are adsorbed on the negatively charged CSH surface. The combination of these sorts of interactions leads then to a strong attachment between PDA film and CSH
groups of 3,4-dihydroxyphenylalanine (DOPA) can form bidentate hydrogen bonding interaction with mica, a silicate mineral containing silicate chains. Consequently, it is speculated reasonably that the PDACSH surface interaction may be attributed to bidentate hydrogen bonding between the OH groups of catechol and the O atoms of silicate tetrahedra in CSH. Additionally, amine groups and dihydroxyl groups 3036
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Fig. 6. SEM micrographs of (A-D) TCS disks and (A1-D1) PDA-coated TCS disks after soaking in SBF for (A-A1) 1, (B-B1) 3, (C-C1) 7 and (D-D1) 14 d. Inserts are the higher magnification images of apatite spherulites displaying the different morphological changes.
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Fig. 7. SEM images of the variations in thickness of apatite layer on the surfaces of (A, B) TCS disks and (A1, B1) PDA-coated TCS disks after soaking in SBF for (A, A1) 1 and (B-B1) 7 d.
layer were observed grown assembling and developing the clusters and aggregates of precipitates (Fig. 6(B1), blue arrows), implying that the formation of biomimetic apatite on hydrated TCS surface follows the layer-by-layer growth mode [46]. After 7–14 d of soaking in SBF, the surface became more homogeneous and dense, and the apatite precipitates grew continuously abiding by the layer-by-layer growth mode. Inserts are the higher magnification images of apatite spherulites showing the progressively morphological evolution. At high magnifications, the layer displayed mainly an interlocked plate-like morphology, which is a typical form for bone-like apatite crystals. Interestingly, it was found that the apatite spherulites possessing a plate-like structure developed step by step, and eventually turn into a solid rounded-globular (Fig. 6(D1)). Although there have been efforts to investigate the in vitro bioactivity of experimental or different commercially available TCS, most of the studies were qualitative in nature. It should be emphasized that it is a great challenge to quantify precisely the percentage of the TCS surface covered by bone-like apatite or the variations in thickness of the carbonated apatite layer over time because of the indistinguishable amount of apatite on TCS surface and the multiple chemical reactions including the hydration of substrate and the precipitation of apatite. Here, we attempted to perform semi-quantitative analysis on apatite layer formed on TCS surface by SEM images of the cross sections of the samples. The SEM micrographs of the variations in thickness of apatite layer on the surfaces of TCS disks and PDA-coated TCS disks over time are shown in Fig. 7. After 1 d of exposure to SBF, the apatite layer on the surface of PDA-coated TCS disk, about 33.2 µm in height was thicker than that on the surface of TCS disk, determining about 12.5 µm. Thereafter with increasing soaking time to 7 d, the height of apatite layer on the surface of TCS disk increased to 49.5 µm. However, the height of apatite layer on the surface of PDA-coated TCS disk, about 91.1 µm in thick, revealed more significantly elevated trend, suggesting that PDA coating may promote the kinetic deposition process of bone-
substrate. In order to gain insight into the contribution of PDA coating on the process and kinetics of apatite deposited on hydrated TCS substrate, the surface structural alterations of different TCS disks as a function of soaking time were comprehensively and systematically examined. Fig. 4 shows the SEM micrographs of TCS disks and PDA-coated TCS disks after a short-term soaking in SBF. After 5 min of storage in SBF, the surface of PDA-coated TCS disk exhibited the spheroidal precipitates characteristic of ACP (Fig. 4(A1)), which is a key intermediate that transforms subsequently into bone-like apatite in osteogenesis [26]. By contrast, free from obvious ACP spherulites were observed on the surfaces of TCS disks, which show the cubic and polygonal crystals until 20 min of incubation in SBF (Fig. 4(A), (B) and (C)). Additionally, some of the smaller spherules are deposited within the net-like CSH (Fig. 4(D)). As soaking time increased, numerous ACP spherulites dispersed on the surfaces of different TCS disks were compacted and packed to form clusters of spheroidal bodies full of the surface of hydrated TCS. In particular, the spherule clusters on the surfaces of PDAcoated TCS disks were more and bigger in comparison with those on the surface of pristine TCS disks (Fig. 5), indicating that the PDA layer provided the benefits of accelerating ACP formation on the surface of hydrated TCS. Fig. 6 shows the SEM micrographs of TCS disks and PDA-coated TCS disks after a medium-term immersion in SBF. After immersion in SBF for 1 d, the surface of TCS disk revealed the microtopography of aggregated spherulites containing a number of voids (Fig. 6(A), pink arrows), while the surface of PDA-coated TCS disk was covered by a dense granular layer in absence of a porous structure; and some small apatite spherulites were occasionally distributed on the newly formed apatite layer (Fig. 6(A1), green ellipses). After 3 d of immersion in SBF, the surface of TCS disk displayed the similar structure to that of TCS disk soaked in SBF for 1d (Fig. 6(B), yellow polygons). For PDA-coated TCS disk, however, diffuse apatite spherulites on the freshly formed apatite 3038
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Fig. 8. Structure and morphology of bone-like apatite layer precipitated on the surface of hydrated TCS after soaking in SBF for 7 d. (A) TEM image, (B) HRTEM image, (C) SAED pattern, (D) XRD pattern and (E) FTIR spectrum.
agrees well with the SEM results presented in Fig. 6. In the high resolution transmission electron microscope (HRTEM) image, 0.172 nm is consistent with the spacing (004) plane of HA (Fig. 8(B)). The selected area electron diffraction (SAED) exhibited broad ring patterns around the dim dot patterns that are typical of HA aggregates with poor crystallinity. The resolvable rings were ascribed to (211), (112) and (300) planes of HA, and the dotted line pattern was assigned to (002) plane of HA, implying preferred development of the HA crystals in [002] direction. In addition, the dot patterns that might be not discerned corresponded to (213) plane of HA. The structure of the bone-like apatite was further confirmed by XRD investigation. It can be seen that the characteristic peaks at 2θ = 25.9°, 31.8°, 32.2° and 32.9° correspond to a poorly crystallized HA (PDF: 09-0432), along with several other small peaks (Fig. 8(D)). Additionally, compared to standard diffraction pattern, the stronger intensity ratio between the (002) and (211) diffraction (Fig. 9) implies the preferential growth of bone-like apatite along the c-axis [47]. FTIR analysis was carried out to further determine chemical composition of the bone-like apatite. The results in Fig. 8(E) indicate that bands at 473, 564, 602, 962 and 1039 cm−1 are attributed to vibrations of PO43-. The bands at 564 and 602 cm−1 are due to triply degenerated bending mode (v4) of the O-P-O bonds of PO43-. Moreover, the absorption band at 1039 cm−1, triply degenerated asymmetric stretching mode (v3) of the P-O bond of PO43-, is characteristic of HA. The bands at 1483 and 1427 cm−1 are due to the asymmetric stretching of CO32-, and the band at 874 cm−1 is assigned to the bending vibrations of CO32-. In particular, carbonate ions may substitute for phosphate ions to form biologically active carbonated HA when they are in aqueous media. The bands detected at 1483, 1427 and 874 cm−1 were assigned to the CO32- group of B-type carbonated HA, where PO43- is
Fig. 9. XRD pattern of bone-like apatite layer precipitated on the surface of hydrated TCS after soaking in SBF for 7 d. The intensity ratio between the (002) and (211) diffraction peaks is determined to be 0.55, while the ratio obtained from the standard PDF card is 0.40, suggesting preferential development of the HA crystals in c-axis direction. ID: the intensity ratio via determination of XRD pattern, IPDF: the intensity ratio from the standard PDF card.
like apatite on its surface. Various analytical tools were used to characterize the structure of the precipitated apatite on the surface of hydrated TCS after soaking in SBF for 7 d. The observation under TEM revealed the bone-like apatite contained nanocrystals of the plate-like morphology (Fig. 8(A)), which 3039
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Fig. 10. (A) Ca, (B) P concentration and (C) pH values of the SBF after immersion of TCS disks and PDA-coated TCS disks for different time intervals.
substituted by CO32-. This is in accordance to a previous report that CO32- groups could substitute PO43- groups in bone-like apatite [5]. Taken together, TEM, HRTEM, SAED, XRD and FTIR analyses unambiguously verified that the bone-like apatite formed on the surface of hydrated TCS is carbonated HA. To further explore how PDA coating promotes the formation of bone-like apatite on the surface of TCS disk, the changes in concentrations of Ca and P as well as pH values of the SBF after immersion of TCS disks and PDA-coated TCS disks for different time intervals were determined. As shown in Fig. 10, with the increase in soaking time, it is obvious that Ca concentration in SBF increased gradually, accompanied with a progressive decrease in the P concentration whether it was for the pristine TCS disks or the PDA-coated TCS disks. The enhancement of Ca and the drop of P may be due to the dissolution of Ca2+ from hydrated TCS to the SBF solution and the precipitation of ACP. Similarly, pH values of the SBF revealed a significant increase, which could be attributed to the continuous release of Ca(OH)2 from the surface of hydrated TCS into the SBF solution. However, the pH values, Ca and P concentration of the SBF after immersion of PDA-coated TCS disks showed more visible increase or decrease, suggesting that the existence of PDA coating on hydrated TCS surface promoted the dissolution of Ca2+ and OH− ions from the surface of hydrated TCS into the SBF solution and the formation of ACP. A fundamental understanding of the mechanism of bone-like apatite formation on PDA-coated TCS is essential for developing new kinds of PDA-coated TCS biomaterials. The mechanism of apatite formation on bioglass and wollastonite coating, which resembles the composition of the hydrated TCS has been proposed [48,49]. Recently, the mechanism of apatite formation on hydraulic calcium silicate cements has also been discussed [50]. A parallel series of stages will be utilized in this discussion to clarify the contribution of PDA coating on the process and
kinetics of bone-like apatite formed on hydrated TCS substrate. Fig. 11 illustrates schematically the mechanism of bone-like apatite formation on the surfaces of hydrated TCS disks without (left column) and with (right column) PDA modification. Stage 1: Hydration and PDA modification. As discussed above, the Si-OH groups on the surface of CSH that is formed on the surface of original TCS following their progressive hydration are attacked by OH− ions to form SiO− groups, and therefore produce negatively charged surface.
≡Si – OH + OH− = ≡SiO− + H2 O
(1)
In contrast, a layer of PDA having abundant catechol functional groups and partially ionized OH groups forms on the surface of hydrated TCS owing to the cross-linking of DOPA and lysine amino acids in a manner reminiscent of melanin formation and its spontaneous attachment through bidentate hydrogen bonding as well as electrostatic interactions. Stage 2: Binding of Ca2+. The negatively charged surface attracts electrostatically Ca2+ from the solution to decrease the total energy of the system, thus resulting in an increase of Ca2+ at the interface. This region, consisting of a charged surface and an equal but opposite charge in the solution, is called an electric double layer on which new products may form under suitable conditions. [51] (2)
≡SiO− + Ca2 + = SiO−⋯Ca2 + 2+
ions are adsorbed at the inFor PDA-coated TCS disk, some Ca terface between a negatively charged surface and the PDA coating. On the other hand, plentiful Ca2+ ions are concentrated on the surface of PDA coating due to the high affinitive interaction between Ca2+ ions and catechol moieties in PDA [22,52]. Therefore, there are more Ca2+ ions in the electric double layer near the surface of 3040
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Fig. 11. Schematic illustration of the mechanism of bone-like apatite formation on hydrated TCS substrate without (left column) and with (right column) PDA coating.
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PDA-coated TCS disk, which was verified by the analyses of Ca and P concentration as well as pH values of the SBF. Stage 3: Soaking in SBF. After the hydrated TCS soaking in SBF, the hydrolyzed HPO42− ions in solution interact electrostatically with Ca2+ ions in the electric double layer. Stage 4: Formation of ACP. The ACP spherulites precipitate on the surface of the hydrated TCS when the SBF solution at the interface supersaturates with respect to ACP as a result of continuous release of Ca2+ ions from the hydrated TCS into the SBF solution. The rate of the ACP nucleation on the surface of PDA-coated TCS disk is much higher than that of the original TCS disk (as shown in Fig. 4). The higher ionic activity product (IP) and lower interface energy of ACP at the interface between ACP and surface of PDA-coated TCS disk are responsible for the higher rate of the ACP nucleation on their surfaces. According to the experimental results above, the more enrichment of Ca2+ and HPO42− ions in the electric double layer near the surface of PDA-coated TCS disk lead to the more elevated IP of the ACP in SBF in comparison with that on the surface of original TCS disk. Moreover, the larger roughness of PDA-coated TCS disk could decrease interface energy between the ACP and the substrate, indicating that it may provide a specific surface with lower interface energy against the ACP. Once the ACP nuclei are formed, they can grow spontaneously by consuming the Ca and P ions from the SBF solution. Stage 5: Growing by layer-layer mode. The evolution of ACP to calcium phosphate occurs because it is unstable [53,54]. In general, the most thermodynamically stable bone-like apatite, namely carbonated HA, evolves from the ACP phase under physiological conditions. Hereafter, the carbonated HA nucleates and undergoes further growth via layer-layer mode rather than island or layer-plusisland growth mode [46].
[8] [9] [10] [11] [12]
[13] [14]
[15]
[16] [17] [18]
[19]
[20] [21] [22]
[23]
[24]
4. Conclusions [25]
In summary, we developed an ultrafast and accessible route to promote the kinetic deposition process of ACP on the surface of PDAcoated TCS within 5 min in SBF. The bidentate hydrogen bonds and electrostatic interactions create a strong attachment between PDA coating and the surface of hydrated TCS. Our findings show that PDA coating can accelerate effectively the formation of bone-like apatite on its surface. In addition, the mechanism of bone-like apatite formation on PDA-coated TCS was also proposed. The higher rate of the ACP nucleation is attributed to the higher IP and lower interface energy of ACP at the interface between ACP and surface of PDA-coated TCS disk due to the existence of PDA coating. Hereafter, the ACP transforms into carbonated HA and undergoes further growth via layer-layer mode rather than island or layer-plus-island growth mode.
[26] [27] [28]
[29]
[30]
[31]
[32]
Acknowledgements
[33] [34]
This research was funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions.
[35] [36]
References
[37] [1] S. Pina, J.M. Oliveira, R.L. Reis, Natural-based nanocomposites for bone tissue engineering and regenerative medicine: a review, Adv. Mater. 27 (2015) 1143–1169. [2] K.J.L. Burg, S. Porter, J.F. Kellam, Biomaterial developments for bone tissue engineering, Biomaterials 21 (2000) 2347–2359. [3] C. Wu, J. Chang, A review of bioactive silicate ceramics, Biomed. Mater. 8 (2013) 032001. [4] L.L. Hench, J.M. Polak, Third-generation biomedical materials, Science 295 (2002) 1014–1017. [5] F.A. Müller, L. Müller, D. Caillard, E. Conforto, Preferred growth orientation of biomimetic apatite crystals, J. Cryst. Growth 304 (2007) 464–471. [6] E.D. Spoerke, S.G. Anthony, S.I. Stupp, Enzyme directed templating of artificial bone mineral, Adv. Mater. 21 (2009) 425–430. [7] S.W. White, D.J. Hulmes, A. Miller, P.A. Timmins, Collagen-mineral axial
[38]
[39]
[40]
[41] [42]
3042
relationship in calcified turkey leg tendon by X-ray and neutron diffraction, Nature 266 (1977) 421–425. S. Weiner, W. Traub, H.D. Wagner, Lamellar bone: structure-function relations, J. Struct. Biol. 126 (1999) 241–255. T.A. Taton, Nanotechnology: boning up on biology, Nature 412 (2001) 491–492. A.K. Nair, A. Gautieri, S.W. Chang, M.J. Buehler, Molecular mechanics of mineralized collagen fibrils in bone, Nat. Commun. 4 (2013) 1724. T. Kokubo, H. Takadama, How useful is SBF in predicting in vivo bone bioactivity? Biomaterials 27 (2006) 2907–2915. R.J. Chung, A.N. Wang, K.H. Lin, Y.C. Su, Study of a novel hybrid bone cement composed of γ-polyglutamic acid and tricalcium silicate, Ceram. Int. 43 (2017) S814–S822. X. Wang, H. Sun, J. Chang, Characterization of Ca3SiO5/CaCl2 composite cement for dental application, Dent. Mater. 24 (2008) 74–82. Z. Huan, J. Chang, Self-setting properties and in vitro bioactivity of calcium sulfate hemihydrate-tricalcium silicate composite bone cements, Acta Biomater. 3 (2007) 952–960. W. Liu, D. Zhai, Z. Huan, C. Wu, J. Chang, Novel tricalcium silicate/magnesium phosphate composite bone cement having high compressive strength, in vitro bioactivity and cytocompatibility, Acta Biomater. 21 (2015) 217–227. W. Zhao, J. Wang, W. Zhai, Z. Wang, J. Chang, The self-setting properties and in vitro bioactivity of tricalcium silicate, Biomaterials 26 (2005) 6113–6121. W. Zhao, J. Chang, Preparation and characterization of novel tricalcium silicate bioceramics, J. Biomed. Mater. Res. A 73 (2005) 86–89. P. Pei, X. Qi, X. Du, M. Zhu, S. Zhao, Y. Zhu, Three-dimensional printing of tricalcium silicate/mesoporous bioactive glass cement scaffolds for bone regeneration, J. Mater. Chem. B 4 (2016) 7452–7463. N. Olmo, A.I. Martı́n, A.J. Salinas, J. Turnay, M. Vallet-Regı́, M.A. Lizarbe, Bioactive sol-gel glasses with and without a hydroxycarbonate apatite layer as substrates for osteoblast cell adhesion and proliferation, Biomaterials 24 (2003) 3383–3393. W. Xue, X. Liu, X. Zheng, C. Ding, In vivo evaluation of plasma-sprayed wollastonite coating, Biomaterials 26 (2005) 3455–3460. M.E. Lynge, R. van der Westen, A. Postma, B. Städler, Polydopamine-a nature-inspired polymer coating for biomedical science, Nanoscale 3 (2011) 4916–4928. J. Ryu, S.H. Ku, H. Lee, C.B. Park, Mussel-inspired polydopamine coating as a universal route to hydroxyapatite crystallization, Adv. Funct. Mater. 20 (2010) 2132–2139. M. Lee, S.H. Ku, J. Ryu, B.P. Chan, Mussel-inspired functionalization of carbon nanotubes for hydroxyapatite mineralization, J. Mater. Chem. 20 (2010) 8848–8853. M. Wu, T. Wang, J. Zhang, H. Qian, R. Miao, X. Yang, PDA/CPP bilayer prepared via two-step immersion for accelerating the formation of a crack-free biomimetic hydroxyapatite coating on titanium substrates, Mater. Lett. 206 (2017) 56–59. Y. Zhou, Y. Cao, W. Liu, C. Chu, Q. Li, Polydopamine-induced tooth remineralization, ACS Appl. Mater. Interfaces 4 (2012) 6901–6910. E.D. Eanes, Amorphous calcium phosphate, Monogr. Oral. Sci. 18 (2001) 130–147. M. Wu, T. Wang, Y. Wang, F. Li, M. Zhou, X. Wu, A novel and facile route for synthesis of fine tricalcium silicate powders, Mater. Lett. 227 (2018) 187–190. L. Grech, B. Mallia, J. Camilleri, Characterization of set intermediate restorative material, biodentine, bioaggregate and a prototype calcium silicate cement for use as root-end filling materials, Int. Endod. J. 46 (2013) 632–641. W. Liu, Y. Li, X. Meng, G. Liu, S. Hu, F. Pan, H. Wu, Z. Jiang, B. Wang, Z. Li, X. Cao, Embedding dopamine nanoaggregates into a poly(dimethylsiloxane) membrane to confer controlled interactions and free volume for enhanced separation performance, J. Mater. Chem. A 1 (2013) 3713–3723. J. Jiang, L. Zhu, L. Zhu, B. Zhu, Y. Xu, Surface characteristics of a self-polymerized dopamine coating deposited on hydrophobic polymer films, Langmuir 27 (2011) 14180–14187. Z. Xi, Y. Xu, L. Zhu, Y. Wang, B. Zhu, A facile method of surface modification for hydrophobic polymer membranes based on the adhesive behavior of poly(DOPA) and poly(dopamine), J. Membr. Sci. 327 (2009) 244–253. H. Lee, S.M. Dellatore, W.M. Miller, P.B. Messersmith, Mussel-inspired surface chemistry for multifunctional coatings, Science 318 (2007) 426–430. Q. Ye, F. Zhou, W. Liu, Bioinspired catecholic chemistry for surface modification, Chem. Soc. Rev. 40 (2011) 4244–4258. I.G. Richardson, The nature of the hydration products in hardened cement pastes, Cem. Concr. Compos. 22 (2000) 97–113. I.G. Richardson, The calcium silicate hydrates, Cem. Concr. Res. 38 (2008) 137–158. B. Lothenbach, A. Nonat, Calcium silicate hydrates: solid and liquid phase composition, Cem. Concr. Res. 78 (2015) 57–70. C. Labbez, B. Jönsson, I. Pochard, A. Nonat, B. Cabane, Surface charge density and electrokinetic potential of highly charged minerals: experiments and monte carlo simulations on calcium silicate hydrate, J. Phys. Chem. B 110 (2006) 9219–9230. C. Labbez, A. Nonat, I. Pochard, B. Jönsson, Experimental and theoretical evidence of overcharging of calcium silicate hydrate, J. Colloid Interface Sci. 309 (2007) 303–307. A. Picker, L. Nicoleau, A. Nonat, C. Labbez, H. Cölfen, Identification of binding peptides on calcium silicate hydrate: a novel view on cement additives, Adv. Mater. 26 (2014) 1135–1140. C. Plassard, E. Lesniewska, I. Pochard, A. Nonat, Nanoscale experimental investigation of particle interactions at the origin of the cohesion of cement, Langmuir 21 (2005) 7263–7270. B. Jönsson, H. Wennerström, A. Nonat, B. Cabane, Onset of cohesion in cement paste, Langmuir 20 (2004) 6702–6709. S. Das, N.R. Martinez Rodriguez, W. Wei, J. Herbert Waite, J.N. Israelachvili,
Ceramics International 45 (2019) 3033–3043
M. Wu et al.
[43]
[44]
[45]
[46] [47]
(2006) 1038–1042. [48] C. Ohtsuki, T. Kokubo, T. Yamamuro, Mechanism of apatite formation on CaOSiO2-P2O5 glasses in a simulated body fluid, J. Non-Cryst. Solid 143 (1992) 84–92. [49] X. Liu, C. Ding, P.K. Chu, Mechanism of apatite formation on wollastonite coatings in simulated body fluids, Biomaterials 25 (2004) 1755–1761. [50] L. Niu, K. Jiao, T. Wang, W. Zhang, J. Camilleri, B.E. Bergeron, H. Feng, J. Mao, J. Chen, D.H. Pashley, F.R. Tay, A review of the bioactivity of hydraulic calcium silicate cements, J. Dent. 42 (2014) 517–533. [51] P. Li, F. Zhang, The electrochemistry of a glass surface and its application to bioactive glass in solution, J. Non-Cryst. Solids 119 (1990) 112–118. [52] N. Holten-Andersen, T.E. Mates, M.S. Toprak, G.D. Stucky, F.W. Zok, J.H. Waite, Metals and the integrity of a biological coating: the cuticle of mussel byssus, Langmuir 25 (2009) 3323–3326. [53] H. Pan, X. Liu, R. Tang, H. Xu, Mystery of the transformation from amorphous calcium phosphate to hydroxyapatite, Chem. Commun. 46 (2010) 7415–7417. [54] L. Wang, G.H. Nancollas, Calcium orthophosphates: crystallization and dissolution, Chem. Rev. 108 (2008) 4628–4669.
Peptide length and dopa determine iron-mediated cohesion of mussel foot proteins, Adv. Funct. Mater. 25 (2015) 5840–5847. J. Yu, Y. Kan, M. Rapp, E. Danner, W. Wei, S. Das, D.R. Miller, Y.F. Chen, J.H. Waite, J.N. Israelachvili, Adaptive hydrophobic and hydrophilic interactions of mussel foot proteins with organic thin films, Proc. Natl. Acad. Sci. USA 110 (2013) 15680–15685. B.K. Ahn, S. Das, R. Linstadt, Y. Kaufman, N.R. Martinez Rodriguez, R. Mirshafian, E. Kesselman, Y. Talmon, B.H. Lipshutz, J.N. Israelachvili, J. Herbert Waite, Highperformance mussel-inspired adhesives of reduced complexity, Nat. Commun. 6 (2015) 8663. B. Yu, J. Liu, S. Liu, F. Zhou, Pdop layer exhibiting zwitterionicity: a simple electrochemical interface for governing ion permeability, Chem. Commun. 46 (2010) 5900–5902. M. Ohring, Materials Science of Thin Films: Deposition & Structure, 2nd ed., Academic Press, San Diego, CA, 2002 (Ch. 7). Q. Shi, J. Wang, J. Zhang, J. Fan, G.D. Stucky, Rapid-setting, mesoporous, bioactive glass cements that induce accelerated in vitro apatite formation, Adv. Mater. 18
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Ceramics International journal homepage: www.elsevier.com/locate/ceramint
Ultrafast bone-like apatite formation on bioactive tricalcium silicate cement using mussel-inspired polydopamine
T
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Meng Wu, Tao Wang , Yangyang Wang, Hui Wang College of Material Science and Technology, Nanjing University of Aeronautics and Astronautics, Nanjing 210016, China
A R T I C LE I N FO
A B S T R A C T
Keywords: Tricalcium silicate Polydopamine Bone-like apatite Biomaterials Attachment mechanism Carbonated hydroxyapatite
The growing bone-like apatite layer at the tissue-implant interface is the essential condition for materials to bond robustly to surrounding bone and may provide a favorable environment for living bone formation. Inspired by versatility of mussel adhesive proteins, we developed an ultrafast and accessible route to accelerate effectively the formation of amorphous calcium phosphate (ACP), the precursor phase of bone-like apatite, on the surface of polydopamine (PDA)-coated tricalcium silicate (TCS) within 5 min in simulated body fluid (SBF). The key of the method lies in successful preparation of PDA coating on the surface of hydrated TCS by simple dip-coating of hydrated TCS in an aqueous solution of dopamine. A strong adsorption between PDA coating and surface of hydrated TCS could be formed via bidentate hydrogen and electrostatic bonds. After 7 d of soaking in SBF, the bone-like apatite layer on the surface of PDA-coated TCS disk, about 91.1 µm in height was thicker than that on the surface of pristine TCS disk, determining about 49.5 µm. The results indicate that PDA coating can facilitate the kinetic deposition of bone-like apatite on its surface. The abundant Ca2+ ions and the lower interface energy of ACP at the interface between ACP and surfaces of PDA-coated TCS disks are responsible for the ultrafast precipitation of ACP and formation of bone-like apatite layer which is carbonated hydroxyapatite (HA) confirmed by different analytical tools. The route can open avenues for development of PDA-coated TCS biomaterials for hard tissue repair and substitution.
1. Introduction Materials science dedicated to use of a large variety of materials to biomedical applications is of prime importance to tissue engineering, a multidisciplinary field of research that utilizes strategies of engineering sciences, biology, and chemistry to repair tissue of living tissues [1]. In the last few decades, considerable efforts have been made to develop many different types of biomaterials including polymers, ceramics, metals and composites for diverse clinical applications in tissue replacement and regeneration [2]. Notably, tricalcium silicate (TCS), a Sicontaining third generation biomaterial that can stimulate specific cellular responses and regeneration of living tissues, has recently been an intensive biomaterial of research for bone and tooth defect repair and substitution owing to its sufficient physicochemical properties and excellent bone bioactivity [3,4]. The bone-bonding bioactivity is the capability to chemically bond with the surrounding tissues through the formation of bone-like apatite layer, a c-axis-oriented hydroxyapatite (HA) crystals, at the tissue-biomaterial interface when in contact with physiological fluids [5]. Interestingly, this growth behavior of bone-like apatite resembles that found in natural bone mineral to form
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sophisticated hierarchical structures with collagen fibrils resulting in fascinating physicochemical properties, where the c-axes of carbonated HA crystals are spatially aligned with the long axes of the collagen fibrils [6–10]. It has been generally accepted that the rate of apatite formation can indicate the degree of in vivo bone bioactivity of the material. Typically, the bone-bonding ability of TCS can be determined by monitoring bone-like apatite layer formation on its surface in a simulated body fluid (SBF) with ion concentrations similar to those of human blood plasma [11]. Most studies on bioactive TCS focus on the enhancement of the physicomechanical properties (a shorter setting time, good injectability, improved mechanical strength and enhanced washout resistance) by blending a myriad of additives [12–15] and the extension of scope for applications such as using as injectable biomaterials, bioceramics and scaffolds [16–18]. Nevertheless, there are a smaller amount of literatures on accelerating the kinetic deposition process of biologically active apatite that not only increases cell adhesion and improves the mitotic activity of the cells [19], but also plays a key role in the enhancement of bone-bonding ability and bone growth [20]. Therefore, it is greatly meaningful to devote efforts to promoting
Corresponding author. E-mail address: [email protected] (T. Wang).
https://doi.org/10.1016/j.ceramint.2018.10.149 Received 12 September 2018; Received in revised form 17 October 2018; Accepted 17 October 2018 Available online 18 October 2018 0272-8842/ © 2018 Elsevier Ltd and Techna Group S.r.l. All rights reserved.
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2.3. Determination of the rate of apatite formation
ultrafast apatite formation on bioactive TCS in terms of its applications in hard tissue engineering. Inspired by versatility of mussel adhesive proteins, polydopamine (PDA) coatings that can attach to a broad variety of surfaces have achieved widespread success for a multitude of biomedical applications [21]. More recently, a route of PDA-assisted HA formation that can effectively induce and accelerate the deposition of HA on non-bioactive interfaces, including noble metals, semiconductors, ceramics and polymers has been verified [22–24]. Moreover, a study has demonstrated that PDA coatings remarkably promoted demineralized dentin remineralization, and all dentin tubules were occluded by densely packed HA crystals [25]. Despite some publications on non-bioactive interfaces, the surface of hydrated TCS has not been investigated yet. In addition, there has been a limitation of understanding of adhesion mechanism between PDA and the surface of hydrated TCS, and the mechanism of bone-like apatite formation on PDA-coated TCS was not proposed either. Herein, we report an ultrafast and accessible route to accelerate effectively the formation of amorphous calcium phosphate (ACP), which is a crucial intermediate that undergoes subsequently the transformation into biological apatite in osteogenesis [26], on the surface of PDA-coated TCS within several minutes under physiological conditions. The key of the method lies in successful preparation of PDA coating on the surface of hydrated TCS by simple dip-coating of hydrated TCS in an aqueous solution of dopamine. The abundant catecholamine moieties in PDA concentrate Ca2+ ions at the interface and thus facilitate the nucleation of ACP. Additionally, the lower interface energy of ACP at the interface between ACP and the surface of PDAcoated TCS is also advantageous to the precipitation of ACP. The attachment mechanism between PDA coating and surface of hydrated TCS and the mechanism of bone-like apatite formation on PDA-coated TCS were also investigated in detail.
To evaluate the rate of apatite formation on the TCS disks and PDAcoated TCS disks, they were immersed in the SBF at 37 °C for a predetermined time period, and the ratio of the surface area of disk to volume of the SBF was 10 cm−1. The SBF was prepared in the light of the method described by Kokubo [11] and its ion concentrations were as follows: 142.0 mM Na+, 5.0 mM K+, 1.5 mM Mg2+, 2.5 mM Ca2+, 147.8 mM Cl−, 4.2 mM HCO3−, 1.0 mM HPO42−, 0.5 mM SO42−. The SBF was refreshed every 3 days. After soaking for the desired time, the disks were extensively rinsed with deionized water followed by drying at 60 °C in a vacuum oven. 2.4. Characterizations The PDA coating on the surface of TCS disk was characterized using X-Ray photoelectron spectroscopy (XPS; Omicron, Taunusstein, Germany) with Al Kα (1486.8 eV) 300 W X-ray source. Fourier transform infrared (FTIR; Nicolet Co., USA) analyses with a resolution of 4 cm−1 in the spectral range of 4000–400 cm−1 were performed to determine the surface chemical functionality of the PDA-coated TCS disk and bone-like apatite layer. The surface topography of PDA-coated TCS disk was analyzed by atomic force microscopy (AFM; Seiko Instruments, Japan). The morphological changes of apatite mineralization on the surfaces of different disks were investigated with a field-emission scanning electron microscope (FESEM; Hitachi High Technologies Co., Japan). Phase composition analysis was carried out on bone-like apatite using X-ray diffraction (XRD; Rigaku Co., Japan) with Cu Ka radiation at 40 mA and 45 kV. The surface morphologies and microstructures of the bone-like apatite were analyzed using transmission electron microscope (TEM, JEOL, Co., Japan). The concentrations of Calcium (Ca) and phosphorus (P) in the SBF after soaking for pre-selected time period were measured using inductively coupled plasma atomic emission spectroscopy (ICP-AES; Varian Co., USA). In addition, pH values of the storage solution were determined using an electrolyte-type pH meter (SX-620, Sanxin Instruments Co., Shanghai, China).
2. Experimental section 2.1. Materials
3. Results and discussion
TCS powders were prepared by the wet-chemical method as previously reported [27]. Briefly, 0.2 mol Si(OC2H5)4 (TEOS) was added into a mixture of 80 ml deionized water and 1 mol anhydrous ethanol. Then, the solution was adjusted by nitric acid and pH was 1–2 under continuous stirring at room temperature. After mixing uniformly, 0.6 mol CaC2O4 was put into the solution and the mixture was stirred by a magnetic stirrer at 60 °C for 2 h, followed by drying at 120 °C. The sample was sintered at 1450 °C for 6 h and ground using ball milling for 3 h at the speed of 350 r/min. Hereafter, the resulting powders were sieved to 300-mesh for further experiments. Dopamine hydrochloride was purchased from Sigma-Aldrich and other chemical reagents used in the experiments were of analytical grade.
It is well accepted that the hydraulic property of TCS, which can react with water to form Ca(OH)2 and calcium silicate hydrate (CSH), is responsible for a wide array of applications. Fig. 1 (A) shows the FTIR spectra of TCS disk, PDA and PDA-coated TCS disk. In the FTIR spectrum of TCS disk, a narrow and sharp peak at 3644 cm−1 corresponded to the stretching vibration of hydroxyl group indicating the presence of Ca(OH)2. In addition, the intensive peak at 966 cm−1 was assigned to Si-O stretching vibration implying the presence of CSH [28]. The PDA peak at 1600 cm−1 was due to the overlap of the C˭C resonance vibrations in the aromatic ring and the N–H bending vibrations of the amide group. The peak at 1502 cm−1 was attributed to the N–H shearing vibrations of the amide group [29–31]. After PDA modification, the peak at 3644 cm−1 was disappeared and intensity of the peak at 966 cm−1 weakened. Moreover, the characteristic peaks of PDA were also appeared in corresponding region in the FTIR spectrum of PDAcoated TCS disk, which verified the existence of PDA coating on TCS disk. The chemical constituents of TCS disk after soaking in dopamine solution were further investigated. XPS wide spectra of TCS disk before and after PDA modification are shown in Fig. 1(B). The significant differences between two XPS spectra were the absence of silicon peaks (Si 2p and Si 2s) and the presence of nitrogen peak (N 1s) in the XPS spectrum of the PDA-coated TCS disk. High resolution XPS of Si 2p and N 1s peaks for TCS disk and PDA-coated TCS disk were more apparent (Fig. 1(C) and (D)). Furthermore, the intensity of O 1s, Ca 2s and Ca 2p peaks of original TCS disk decreased following the surface modification of PDA, indicating the formation of PDA layer on the surfaces of TCS
2.2. Preparation of TCS disks and PDA-coated TCS disks The 1-day-set TCS disks with a height of 2 mm and a diameter of 10 mm were prepared. Firstly, TCS powders were mixed with deionized water at a liquid/solid of 0.5. Then, freshly mixed cement pastes were cast in stainless steel molds and stored in a 37 °C, 100% humidity water bath for 1 d. To prepare PDA-coated TCS disks, TCS disks were immersed in PDA solution formed by an oxidative polymerization of dopamine-hydrochloride (2 mg/ml in 10 mM Tris, pH 8.5) for 24 h at 37 °C. Simultaneously, the 1-day-set TCS disks were soaked in Tris (pH 8.5) for 24 h at 37 °C to keep similar degree of hydration for different TCS disks. After soaking, as-prepared TCS disks with and without PDA coatings were rinsed with deionized water and dried at 60 °C in a vacuum oven. 3034
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Fig. 1. (A) FTIR spectra of TCS disks, PDA and PDA-coated TCS disks. (B) XPS wide spectra of TCS disks before and after PDA modification, high resolution XPS of (C) nitrogen peak (N 1s) and (D) silicon peak (Si 2p) for TCS disks and PDA-coated TCS disks.
disks. The AFM topographies and the surface roughness of TCS disks before and after PDA modification are presented in Fig. 2. It was obvious that the surface morphologies were significantly changed and the average surface roughness values increased from 22.34 nm to 37.48 nm in comparison with that of the pristine TCS disk, which suggested the formation of PDA coating on TCS disks. The results of the FTIR, XPS and AFM analyses reveal that the PDA coating could deposit on TCS disks via a dip-coating process of the disks in an aqueous solution of dopamine. It is known that catechol in PDA or other catecholic derivatives plays a crucial role in attaching to virtually any type of materials through forming strong covalent or noncovalent interactions with substrates [32,33]. In essence, the specific attachment mechanism depends mainly on the relationship between substrates and catecholic groups. As mentioned above, when TCS particles are in contact with water, an amorphous nanostructured hydration product namely CSH is deposited on the surface of original TCS, while Ca(OH)2 crystals nucleate and grow in the available capillary pore space resulting in a highly alkaline environment. CSH is a porous, non-stoichiometric and tobermorite-like structural silicate chain layer possessing silanol (SiOH) functions [34–36]. The Si-OH groups on the surface of CSH are attacked by OH− ions to form SiO− groups (Fig. 3(A1)), and therefore produce negatively charged surface surrounded by Ca2+ ions via electrostatic interactions [37–40]. Due to continuous release of Ca2+ and OH−, the surfaces reveal an inversion of the zeta potential in the solutions of pH > 11.6 [41]. Fig. 3(B1) shows the proposed binding mechanism of PDA to the negatively charged CSH surface. Although the exact adhesion mechanism is unconfirmed now, previous studies [42–44] have verified that OH
Fig. 2. AFM topographies and the surface roughness of (A) TCS disk and (B) PDA-coated TCS disk. Sa: average surface roughness; Sq: root mean square.
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Fig. 3. Digital images of (A) TCS disk and (B) PDA-coated TCS disk, (A1) schematic illustration for the surface of hydrated TCS disk. CSH is negatively charged at alkaline pH, surrounded by Ca2+ ions (not shown for clarity). (B1) proposed binding mechanism of PDA to the CSH surface.
Fig. 4. SEM micrographs of (A-D) TCS disks and (A1-D1) PDA-coated TCS disks after soaking in SBF for (A-A1) 5, (B-B1) 10, (C-C1) 20 and (D-D1) 30 min. The scale bar represents 3 µm.
Fig. 5. SEM micrographs of (A-D) TCS disks and (A1-D1) PDA-coated TCS disks after soaking in SBF for (A-A1) 60, (B-B1) 120, (C-C1)180 and (D-D1) 360 min. The scale bar represents 3 µm.
of PDA make it potentially ampholytic or zwitterionic. It is negatively charged because of partial ionization of OH groups in PDA at alkaline pH [45]. The partially ionized OH groups of PDA interact via electrostatic interactions with the Ca2+ ions which are adsorbed on the negatively charged CSH surface. The combination of these sorts of interactions leads then to a strong attachment between PDA film and CSH
groups of 3,4-dihydroxyphenylalanine (DOPA) can form bidentate hydrogen bonding interaction with mica, a silicate mineral containing silicate chains. Consequently, it is speculated reasonably that the PDACSH surface interaction may be attributed to bidentate hydrogen bonding between the OH groups of catechol and the O atoms of silicate tetrahedra in CSH. Additionally, amine groups and dihydroxyl groups 3036
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Fig. 6. SEM micrographs of (A-D) TCS disks and (A1-D1) PDA-coated TCS disks after soaking in SBF for (A-A1) 1, (B-B1) 3, (C-C1) 7 and (D-D1) 14 d. Inserts are the higher magnification images of apatite spherulites displaying the different morphological changes.
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Fig. 7. SEM images of the variations in thickness of apatite layer on the surfaces of (A, B) TCS disks and (A1, B1) PDA-coated TCS disks after soaking in SBF for (A, A1) 1 and (B-B1) 7 d.
layer were observed grown assembling and developing the clusters and aggregates of precipitates (Fig. 6(B1), blue arrows), implying that the formation of biomimetic apatite on hydrated TCS surface follows the layer-by-layer growth mode [46]. After 7–14 d of soaking in SBF, the surface became more homogeneous and dense, and the apatite precipitates grew continuously abiding by the layer-by-layer growth mode. Inserts are the higher magnification images of apatite spherulites showing the progressively morphological evolution. At high magnifications, the layer displayed mainly an interlocked plate-like morphology, which is a typical form for bone-like apatite crystals. Interestingly, it was found that the apatite spherulites possessing a plate-like structure developed step by step, and eventually turn into a solid rounded-globular (Fig. 6(D1)). Although there have been efforts to investigate the in vitro bioactivity of experimental or different commercially available TCS, most of the studies were qualitative in nature. It should be emphasized that it is a great challenge to quantify precisely the percentage of the TCS surface covered by bone-like apatite or the variations in thickness of the carbonated apatite layer over time because of the indistinguishable amount of apatite on TCS surface and the multiple chemical reactions including the hydration of substrate and the precipitation of apatite. Here, we attempted to perform semi-quantitative analysis on apatite layer formed on TCS surface by SEM images of the cross sections of the samples. The SEM micrographs of the variations in thickness of apatite layer on the surfaces of TCS disks and PDA-coated TCS disks over time are shown in Fig. 7. After 1 d of exposure to SBF, the apatite layer on the surface of PDA-coated TCS disk, about 33.2 µm in height was thicker than that on the surface of TCS disk, determining about 12.5 µm. Thereafter with increasing soaking time to 7 d, the height of apatite layer on the surface of TCS disk increased to 49.5 µm. However, the height of apatite layer on the surface of PDA-coated TCS disk, about 91.1 µm in thick, revealed more significantly elevated trend, suggesting that PDA coating may promote the kinetic deposition process of bone-
substrate. In order to gain insight into the contribution of PDA coating on the process and kinetics of apatite deposited on hydrated TCS substrate, the surface structural alterations of different TCS disks as a function of soaking time were comprehensively and systematically examined. Fig. 4 shows the SEM micrographs of TCS disks and PDA-coated TCS disks after a short-term soaking in SBF. After 5 min of storage in SBF, the surface of PDA-coated TCS disk exhibited the spheroidal precipitates characteristic of ACP (Fig. 4(A1)), which is a key intermediate that transforms subsequently into bone-like apatite in osteogenesis [26]. By contrast, free from obvious ACP spherulites were observed on the surfaces of TCS disks, which show the cubic and polygonal crystals until 20 min of incubation in SBF (Fig. 4(A), (B) and (C)). Additionally, some of the smaller spherules are deposited within the net-like CSH (Fig. 4(D)). As soaking time increased, numerous ACP spherulites dispersed on the surfaces of different TCS disks were compacted and packed to form clusters of spheroidal bodies full of the surface of hydrated TCS. In particular, the spherule clusters on the surfaces of PDAcoated TCS disks were more and bigger in comparison with those on the surface of pristine TCS disks (Fig. 5), indicating that the PDA layer provided the benefits of accelerating ACP formation on the surface of hydrated TCS. Fig. 6 shows the SEM micrographs of TCS disks and PDA-coated TCS disks after a medium-term immersion in SBF. After immersion in SBF for 1 d, the surface of TCS disk revealed the microtopography of aggregated spherulites containing a number of voids (Fig. 6(A), pink arrows), while the surface of PDA-coated TCS disk was covered by a dense granular layer in absence of a porous structure; and some small apatite spherulites were occasionally distributed on the newly formed apatite layer (Fig. 6(A1), green ellipses). After 3 d of immersion in SBF, the surface of TCS disk displayed the similar structure to that of TCS disk soaked in SBF for 1d (Fig. 6(B), yellow polygons). For PDA-coated TCS disk, however, diffuse apatite spherulites on the freshly formed apatite 3038
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Fig. 8. Structure and morphology of bone-like apatite layer precipitated on the surface of hydrated TCS after soaking in SBF for 7 d. (A) TEM image, (B) HRTEM image, (C) SAED pattern, (D) XRD pattern and (E) FTIR spectrum.
agrees well with the SEM results presented in Fig. 6. In the high resolution transmission electron microscope (HRTEM) image, 0.172 nm is consistent with the spacing (004) plane of HA (Fig. 8(B)). The selected area electron diffraction (SAED) exhibited broad ring patterns around the dim dot patterns that are typical of HA aggregates with poor crystallinity. The resolvable rings were ascribed to (211), (112) and (300) planes of HA, and the dotted line pattern was assigned to (002) plane of HA, implying preferred development of the HA crystals in [002] direction. In addition, the dot patterns that might be not discerned corresponded to (213) plane of HA. The structure of the bone-like apatite was further confirmed by XRD investigation. It can be seen that the characteristic peaks at 2θ = 25.9°, 31.8°, 32.2° and 32.9° correspond to a poorly crystallized HA (PDF: 09-0432), along with several other small peaks (Fig. 8(D)). Additionally, compared to standard diffraction pattern, the stronger intensity ratio between the (002) and (211) diffraction (Fig. 9) implies the preferential growth of bone-like apatite along the c-axis [47]. FTIR analysis was carried out to further determine chemical composition of the bone-like apatite. The results in Fig. 8(E) indicate that bands at 473, 564, 602, 962 and 1039 cm−1 are attributed to vibrations of PO43-. The bands at 564 and 602 cm−1 are due to triply degenerated bending mode (v4) of the O-P-O bonds of PO43-. Moreover, the absorption band at 1039 cm−1, triply degenerated asymmetric stretching mode (v3) of the P-O bond of PO43-, is characteristic of HA. The bands at 1483 and 1427 cm−1 are due to the asymmetric stretching of CO32-, and the band at 874 cm−1 is assigned to the bending vibrations of CO32-. In particular, carbonate ions may substitute for phosphate ions to form biologically active carbonated HA when they are in aqueous media. The bands detected at 1483, 1427 and 874 cm−1 were assigned to the CO32- group of B-type carbonated HA, where PO43- is
Fig. 9. XRD pattern of bone-like apatite layer precipitated on the surface of hydrated TCS after soaking in SBF for 7 d. The intensity ratio between the (002) and (211) diffraction peaks is determined to be 0.55, while the ratio obtained from the standard PDF card is 0.40, suggesting preferential development of the HA crystals in c-axis direction. ID: the intensity ratio via determination of XRD pattern, IPDF: the intensity ratio from the standard PDF card.
like apatite on its surface. Various analytical tools were used to characterize the structure of the precipitated apatite on the surface of hydrated TCS after soaking in SBF for 7 d. The observation under TEM revealed the bone-like apatite contained nanocrystals of the plate-like morphology (Fig. 8(A)), which 3039
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Fig. 10. (A) Ca, (B) P concentration and (C) pH values of the SBF after immersion of TCS disks and PDA-coated TCS disks for different time intervals.
substituted by CO32-. This is in accordance to a previous report that CO32- groups could substitute PO43- groups in bone-like apatite [5]. Taken together, TEM, HRTEM, SAED, XRD and FTIR analyses unambiguously verified that the bone-like apatite formed on the surface of hydrated TCS is carbonated HA. To further explore how PDA coating promotes the formation of bone-like apatite on the surface of TCS disk, the changes in concentrations of Ca and P as well as pH values of the SBF after immersion of TCS disks and PDA-coated TCS disks for different time intervals were determined. As shown in Fig. 10, with the increase in soaking time, it is obvious that Ca concentration in SBF increased gradually, accompanied with a progressive decrease in the P concentration whether it was for the pristine TCS disks or the PDA-coated TCS disks. The enhancement of Ca and the drop of P may be due to the dissolution of Ca2+ from hydrated TCS to the SBF solution and the precipitation of ACP. Similarly, pH values of the SBF revealed a significant increase, which could be attributed to the continuous release of Ca(OH)2 from the surface of hydrated TCS into the SBF solution. However, the pH values, Ca and P concentration of the SBF after immersion of PDA-coated TCS disks showed more visible increase or decrease, suggesting that the existence of PDA coating on hydrated TCS surface promoted the dissolution of Ca2+ and OH− ions from the surface of hydrated TCS into the SBF solution and the formation of ACP. A fundamental understanding of the mechanism of bone-like apatite formation on PDA-coated TCS is essential for developing new kinds of PDA-coated TCS biomaterials. The mechanism of apatite formation on bioglass and wollastonite coating, which resembles the composition of the hydrated TCS has been proposed [48,49]. Recently, the mechanism of apatite formation on hydraulic calcium silicate cements has also been discussed [50]. A parallel series of stages will be utilized in this discussion to clarify the contribution of PDA coating on the process and
kinetics of bone-like apatite formed on hydrated TCS substrate. Fig. 11 illustrates schematically the mechanism of bone-like apatite formation on the surfaces of hydrated TCS disks without (left column) and with (right column) PDA modification. Stage 1: Hydration and PDA modification. As discussed above, the Si-OH groups on the surface of CSH that is formed on the surface of original TCS following their progressive hydration are attacked by OH− ions to form SiO− groups, and therefore produce negatively charged surface.
≡Si – OH + OH− = ≡SiO− + H2 O
(1)
In contrast, a layer of PDA having abundant catechol functional groups and partially ionized OH groups forms on the surface of hydrated TCS owing to the cross-linking of DOPA and lysine amino acids in a manner reminiscent of melanin formation and its spontaneous attachment through bidentate hydrogen bonding as well as electrostatic interactions. Stage 2: Binding of Ca2+. The negatively charged surface attracts electrostatically Ca2+ from the solution to decrease the total energy of the system, thus resulting in an increase of Ca2+ at the interface. This region, consisting of a charged surface and an equal but opposite charge in the solution, is called an electric double layer on which new products may form under suitable conditions. [51] (2)
≡SiO− + Ca2 + = SiO−⋯Ca2 + 2+
ions are adsorbed at the inFor PDA-coated TCS disk, some Ca terface between a negatively charged surface and the PDA coating. On the other hand, plentiful Ca2+ ions are concentrated on the surface of PDA coating due to the high affinitive interaction between Ca2+ ions and catechol moieties in PDA [22,52]. Therefore, there are more Ca2+ ions in the electric double layer near the surface of 3040
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Fig. 11. Schematic illustration of the mechanism of bone-like apatite formation on hydrated TCS substrate without (left column) and with (right column) PDA coating.
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PDA-coated TCS disk, which was verified by the analyses of Ca and P concentration as well as pH values of the SBF. Stage 3: Soaking in SBF. After the hydrated TCS soaking in SBF, the hydrolyzed HPO42− ions in solution interact electrostatically with Ca2+ ions in the electric double layer. Stage 4: Formation of ACP. The ACP spherulites precipitate on the surface of the hydrated TCS when the SBF solution at the interface supersaturates with respect to ACP as a result of continuous release of Ca2+ ions from the hydrated TCS into the SBF solution. The rate of the ACP nucleation on the surface of PDA-coated TCS disk is much higher than that of the original TCS disk (as shown in Fig. 4). The higher ionic activity product (IP) and lower interface energy of ACP at the interface between ACP and surface of PDA-coated TCS disk are responsible for the higher rate of the ACP nucleation on their surfaces. According to the experimental results above, the more enrichment of Ca2+ and HPO42− ions in the electric double layer near the surface of PDA-coated TCS disk lead to the more elevated IP of the ACP in SBF in comparison with that on the surface of original TCS disk. Moreover, the larger roughness of PDA-coated TCS disk could decrease interface energy between the ACP and the substrate, indicating that it may provide a specific surface with lower interface energy against the ACP. Once the ACP nuclei are formed, they can grow spontaneously by consuming the Ca and P ions from the SBF solution. Stage 5: Growing by layer-layer mode. The evolution of ACP to calcium phosphate occurs because it is unstable [53,54]. In general, the most thermodynamically stable bone-like apatite, namely carbonated HA, evolves from the ACP phase under physiological conditions. Hereafter, the carbonated HA nucleates and undergoes further growth via layer-layer mode rather than island or layer-plusisland growth mode [46].
[8] [9] [10] [11] [12]
[13] [14]
[15]
[16] [17] [18]
[19]
[20] [21] [22]
[23]
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4. Conclusions [25]
In summary, we developed an ultrafast and accessible route to promote the kinetic deposition process of ACP on the surface of PDAcoated TCS within 5 min in SBF. The bidentate hydrogen bonds and electrostatic interactions create a strong attachment between PDA coating and the surface of hydrated TCS. Our findings show that PDA coating can accelerate effectively the formation of bone-like apatite on its surface. In addition, the mechanism of bone-like apatite formation on PDA-coated TCS was also proposed. The higher rate of the ACP nucleation is attributed to the higher IP and lower interface energy of ACP at the interface between ACP and surface of PDA-coated TCS disk due to the existence of PDA coating. Hereafter, the ACP transforms into carbonated HA and undergoes further growth via layer-layer mode rather than island or layer-plus-island growth mode.
[26] [27] [28]
[29]
[30]
[31]
[32]
Acknowledgements
[33] [34]
This research was funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions.
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References
[37] [1] S. Pina, J.M. Oliveira, R.L. Reis, Natural-based nanocomposites for bone tissue engineering and regenerative medicine: a review, Adv. Mater. 27 (2015) 1143–1169. [2] K.J.L. Burg, S. Porter, J.F. Kellam, Biomaterial developments for bone tissue engineering, Biomaterials 21 (2000) 2347–2359. [3] C. Wu, J. Chang, A review of bioactive silicate ceramics, Biomed. Mater. 8 (2013) 032001. [4] L.L. Hench, J.M. Polak, Third-generation biomedical materials, Science 295 (2002) 1014–1017. [5] F.A. Müller, L. Müller, D. Caillard, E. Conforto, Preferred growth orientation of biomimetic apatite crystals, J. Cryst. Growth 304 (2007) 464–471. [6] E.D. Spoerke, S.G. Anthony, S.I. Stupp, Enzyme directed templating of artificial bone mineral, Adv. Mater. 21 (2009) 425–430. [7] S.W. White, D.J. Hulmes, A. Miller, P.A. Timmins, Collagen-mineral axial
[38]
[39]
[40]
[41] [42]
3042
relationship in calcified turkey leg tendon by X-ray and neutron diffraction, Nature 266 (1977) 421–425. S. Weiner, W. Traub, H.D. Wagner, Lamellar bone: structure-function relations, J. Struct. Biol. 126 (1999) 241–255. T.A. Taton, Nanotechnology: boning up on biology, Nature 412 (2001) 491–492. A.K. Nair, A. Gautieri, S.W. Chang, M.J. Buehler, Molecular mechanics of mineralized collagen fibrils in bone, Nat. Commun. 4 (2013) 1724. T. Kokubo, H. Takadama, How useful is SBF in predicting in vivo bone bioactivity? Biomaterials 27 (2006) 2907–2915. R.J. Chung, A.N. Wang, K.H. Lin, Y.C. Su, Study of a novel hybrid bone cement composed of γ-polyglutamic acid and tricalcium silicate, Ceram. Int. 43 (2017) S814–S822. X. Wang, H. Sun, J. Chang, Characterization of Ca3SiO5/CaCl2 composite cement for dental application, Dent. Mater. 24 (2008) 74–82. Z. Huan, J. Chang, Self-setting properties and in vitro bioactivity of calcium sulfate hemihydrate-tricalcium silicate composite bone cements, Acta Biomater. 3 (2007) 952–960. W. Liu, D. Zhai, Z. Huan, C. Wu, J. Chang, Novel tricalcium silicate/magnesium phosphate composite bone cement having high compressive strength, in vitro bioactivity and cytocompatibility, Acta Biomater. 21 (2015) 217–227. W. Zhao, J. Wang, W. Zhai, Z. Wang, J. Chang, The self-setting properties and in vitro bioactivity of tricalcium silicate, Biomaterials 26 (2005) 6113–6121. W. Zhao, J. Chang, Preparation and characterization of novel tricalcium silicate bioceramics, J. Biomed. Mater. Res. A 73 (2005) 86–89. P. Pei, X. Qi, X. Du, M. Zhu, S. Zhao, Y. Zhu, Three-dimensional printing of tricalcium silicate/mesoporous bioactive glass cement scaffolds for bone regeneration, J. Mater. Chem. B 4 (2016) 7452–7463. N. Olmo, A.I. Martı́n, A.J. Salinas, J. Turnay, M. Vallet-Regı́, M.A. Lizarbe, Bioactive sol-gel glasses with and without a hydroxycarbonate apatite layer as substrates for osteoblast cell adhesion and proliferation, Biomaterials 24 (2003) 3383–3393. W. Xue, X. Liu, X. Zheng, C. Ding, In vivo evaluation of plasma-sprayed wollastonite coating, Biomaterials 26 (2005) 3455–3460. M.E. Lynge, R. van der Westen, A. Postma, B. Städler, Polydopamine-a nature-inspired polymer coating for biomedical science, Nanoscale 3 (2011) 4916–4928. J. Ryu, S.H. Ku, H. Lee, C.B. Park, Mussel-inspired polydopamine coating as a universal route to hydroxyapatite crystallization, Adv. Funct. Mater. 20 (2010) 2132–2139. M. Lee, S.H. Ku, J. Ryu, B.P. Chan, Mussel-inspired functionalization of carbon nanotubes for hydroxyapatite mineralization, J. Mater. Chem. 20 (2010) 8848–8853. M. Wu, T. Wang, J. Zhang, H. Qian, R. Miao, X. Yang, PDA/CPP bilayer prepared via two-step immersion for accelerating the formation of a crack-free biomimetic hydroxyapatite coating on titanium substrates, Mater. Lett. 206 (2017) 56–59. Y. Zhou, Y. Cao, W. Liu, C. Chu, Q. Li, Polydopamine-induced tooth remineralization, ACS Appl. Mater. Interfaces 4 (2012) 6901–6910. E.D. Eanes, Amorphous calcium phosphate, Monogr. Oral. Sci. 18 (2001) 130–147. M. Wu, T. Wang, Y. Wang, F. Li, M. Zhou, X. Wu, A novel and facile route for synthesis of fine tricalcium silicate powders, Mater. Lett. 227 (2018) 187–190. L. Grech, B. Mallia, J. Camilleri, Characterization of set intermediate restorative material, biodentine, bioaggregate and a prototype calcium silicate cement for use as root-end filling materials, Int. Endod. J. 46 (2013) 632–641. W. Liu, Y. Li, X. Meng, G. Liu, S. Hu, F. Pan, H. Wu, Z. Jiang, B. Wang, Z. Li, X. Cao, Embedding dopamine nanoaggregates into a poly(dimethylsiloxane) membrane to confer controlled interactions and free volume for enhanced separation performance, J. Mater. Chem. A 1 (2013) 3713–3723. J. Jiang, L. Zhu, L. Zhu, B. Zhu, Y. Xu, Surface characteristics of a self-polymerized dopamine coating deposited on hydrophobic polymer films, Langmuir 27 (2011) 14180–14187. Z. Xi, Y. Xu, L. Zhu, Y. Wang, B. Zhu, A facile method of surface modification for hydrophobic polymer membranes based on the adhesive behavior of poly(DOPA) and poly(dopamine), J. Membr. Sci. 327 (2009) 244–253. H. Lee, S.M. Dellatore, W.M. Miller, P.B. Messersmith, Mussel-inspired surface chemistry for multifunctional coatings, Science 318 (2007) 426–430. Q. Ye, F. Zhou, W. Liu, Bioinspired catecholic chemistry for surface modification, Chem. Soc. Rev. 40 (2011) 4244–4258. I.G. Richardson, The nature of the hydration products in hardened cement pastes, Cem. Concr. Compos. 22 (2000) 97–113. I.G. Richardson, The calcium silicate hydrates, Cem. Concr. Res. 38 (2008) 137–158. B. Lothenbach, A. Nonat, Calcium silicate hydrates: solid and liquid phase composition, Cem. Concr. Res. 78 (2015) 57–70. C. Labbez, B. Jönsson, I. Pochard, A. Nonat, B. Cabane, Surface charge density and electrokinetic potential of highly charged minerals: experiments and monte carlo simulations on calcium silicate hydrate, J. Phys. Chem. B 110 (2006) 9219–9230. C. Labbez, A. Nonat, I. Pochard, B. Jönsson, Experimental and theoretical evidence of overcharging of calcium silicate hydrate, J. Colloid Interface Sci. 309 (2007) 303–307. A. Picker, L. Nicoleau, A. Nonat, C. Labbez, H. Cölfen, Identification of binding peptides on calcium silicate hydrate: a novel view on cement additives, Adv. Mater. 26 (2014) 1135–1140. C. Plassard, E. Lesniewska, I. Pochard, A. Nonat, Nanoscale experimental investigation of particle interactions at the origin of the cohesion of cement, Langmuir 21 (2005) 7263–7270. B. Jönsson, H. Wennerström, A. Nonat, B. Cabane, Onset of cohesion in cement paste, Langmuir 20 (2004) 6702–6709. S. Das, N.R. Martinez Rodriguez, W. Wei, J. Herbert Waite, J.N. Israelachvili,
Ceramics International 45 (2019) 3033–3043
M. Wu et al.
[43]
[44]
[45]
[46] [47]
(2006) 1038–1042. [48] C. Ohtsuki, T. Kokubo, T. Yamamuro, Mechanism of apatite formation on CaOSiO2-P2O5 glasses in a simulated body fluid, J. Non-Cryst. Solid 143 (1992) 84–92. [49] X. Liu, C. Ding, P.K. Chu, Mechanism of apatite formation on wollastonite coatings in simulated body fluids, Biomaterials 25 (2004) 1755–1761. [50] L. Niu, K. Jiao, T. Wang, W. Zhang, J. Camilleri, B.E. Bergeron, H. Feng, J. Mao, J. Chen, D.H. Pashley, F.R. Tay, A review of the bioactivity of hydraulic calcium silicate cements, J. Dent. 42 (2014) 517–533. [51] P. Li, F. Zhang, The electrochemistry of a glass surface and its application to bioactive glass in solution, J. Non-Cryst. Solids 119 (1990) 112–118. [52] N. Holten-Andersen, T.E. Mates, M.S. Toprak, G.D. Stucky, F.W. Zok, J.H. Waite, Metals and the integrity of a biological coating: the cuticle of mussel byssus, Langmuir 25 (2009) 3323–3326. [53] H. Pan, X. Liu, R. Tang, H. Xu, Mystery of the transformation from amorphous calcium phosphate to hydroxyapatite, Chem. Commun. 46 (2010) 7415–7417. [54] L. Wang, G.H. Nancollas, Calcium orthophosphates: crystallization and dissolution, Chem. Rev. 108 (2008) 4628–4669.
Peptide length and dopa determine iron-mediated cohesion of mussel foot proteins, Adv. Funct. Mater. 25 (2015) 5840–5847. J. Yu, Y. Kan, M. Rapp, E. Danner, W. Wei, S. Das, D.R. Miller, Y.F. Chen, J.H. Waite, J.N. Israelachvili, Adaptive hydrophobic and hydrophilic interactions of mussel foot proteins with organic thin films, Proc. Natl. Acad. Sci. USA 110 (2013) 15680–15685. B.K. Ahn, S. Das, R. Linstadt, Y. Kaufman, N.R. Martinez Rodriguez, R. Mirshafian, E. Kesselman, Y. Talmon, B.H. Lipshutz, J.N. Israelachvili, J. Herbert Waite, Highperformance mussel-inspired adhesives of reduced complexity, Nat. Commun. 6 (2015) 8663. B. Yu, J. Liu, S. Liu, F. Zhou, Pdop layer exhibiting zwitterionicity: a simple electrochemical interface for governing ion permeability, Chem. Commun. 46 (2010) 5900–5902. M. Ohring, Materials Science of Thin Films: Deposition & Structure, 2nd ed., Academic Press, San Diego, CA, 2002 (Ch. 7). Q. Shi, J. Wang, J. Zhang, J. Fan, G.D. Stucky, Rapid-setting, mesoporous, bioactive glass cements that induce accelerated in vitro apatite formation, Adv. Mater. 18
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