Facet-Specific Mineralization Behavior of Nano-CaP on Anatase

Letter pubs.acs.org/journal/abseba

Facet-Specific Mineralization Behavior of Nano-CaP on Anatase Polyhedral Microcrystals Guohui Shou, Lingqing Dong, Zongguang Liu, Kui Cheng, and Wenjian Weng* School of Materials Science and Engineering, State Key Laboratory of Silicon Materials, Zhejiang University, Hangzhou 310027, China S Supporting Information *

ABSTRACT: Biomimetic mineralization of nanocalcium phosphate (CaP) on metal oxide surfaces has gained great interest because of their relevance to osseointegration performance of implant materials. However, precisely controlling the nucleation behavior of mineralized nano-CaP on metal oxide at selective sites still remains a challenge. Here, we demonstrate a phenomenon on facet-specific mineralization on anatase TiO2 polyhedral microcrystals organized by two facets of {101} and {001} in complete cell culture medium: nano-CaP covers up {101} facets, while there are a few on {001} facets. The comparative experimental results indicate that the preadsorbed fetal bovine serum (FBS) protein on {001} facets might play a barrier role in preventing sequential nucleation of nano-CaP. This work thus provides insight into the understanding of mineralization on metal oxides, and a way to control the mineralization. KEYWORDS: anatase, polyhedral microcrystals, mineralization behavior, complete cell culture medium, FBS, αMEM Ti6Al4V substrates were soaked in a MEM solution at 37 °C, and we observed that well-crystallized nano-CaP formed on the substrates.21−23 Titanium-oxide (TiO2) has been widely used as the bioactive materials to modify the implant surfaces.24,25 CaP nucleation occurs easily on TiO2 surfaces.26 The mineralization of nanoCaP from solutions onto TiO2 macroscopical single crystal samples has been studied.27 In all, we believe that the nucleation of nano-CaP on the TiO2 surface is dominated by the inherent surface feature of TiO2, such as hydrophilicity and chemistries, etc. Moreover, the shape-controlled TiO2 polyhedral crystals provide a new perspective to study the mineralization behavior on different TiO2 facets. We have recently reported the facet-specific assembly of proteins on polyhedral nanocrystals.28 However, these previous efforts have only reported the adsorption behaviors of pure protein on nanocrystals. The observations still show a lack of the effects of distinct protein adsorption behavior on sequent nucleation kinetic of nano-CaP. In this work, decahedron anatase TiO2 polyhedral microcrystals (AN-TPMCs) with {001} and {101} facets exposed were successfully synthesized, and the AN-TPMCs were sequently used as the model crystals to demonstrate the facet-specific mineralization behavior of nano-CaP in cell culture mediums. AN-TMCs with {001} and {101} facets exposed were obtained by a hydrothermal synthesis process. For a typical

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alcium phosphate (CaP) compounds have been considered as the ideal biomaterials for bone substitution and repair.1,2 CaP is the main inorganic compound of bones and teeth.3,4 Promoting and controlling the mineralization of CaP on implant materials surface plays a critical role to accelerate bone healing at early implantation times.5,6 For example, CaPs are always used as the modification materials on implant surfaces to promote bone formation.7,8 Moreover, nanoscaled CaP particles have reported to play an important role in biomineral formation both in vitro and in vivo.9−12 Therefore, design and control of the biomimetic mineralization of nanoCaP on the implant material surface should promote the osteointegration performance of implants in clinical applications. Generally, simulated body fluid (SBF) is used as a medium for the development of biomimetic CaP due to the similar inorganic ion composition to biological fluids.13 The presence of reactive facets on anatase favors the growth of amorphous CaP in SBF.14 However, it is well-known that the implant’s environment in vivo is much more complex because of the existence of abundant proteins in blood.15 The mineralization of nano-CaP in vivo might be different from the in vitro evaluation with classical SBF mineralization tests, leading to different biological activity outcomes.16,17 Alpha-minimum essential medium (αMEM) solutions with adding fetal bovine serum (FBS) protein are widely used in culturing cells in vitro, which has been considered to be more similar to the environment in vivo.18,19 For example, titanium was soaked in a MEM solution at 37 °C to study the mineralization of MEM on titanium. CaP nanoparticles could be found after 24 h.20 © XXXX American Chemical Society

Received: April 13, 2017 Accepted: May 4, 2017 Published: May 4, 2017 A

DOI: 10.1021/acsbiomaterials.7b00234 ACS Biomater. Sci. Eng. XXXX, XXX, XXX−XXX

Letter

ACS Biomaterials Science & Engineering

Figure 1. (a) XRD pattern of AN-TPMCs. (b) XPS spectrum of AN-TPMCs after heating at 520 °C for 60 min.

Figure 2. (a and b) SEM images of typical AN-TPMC, (c) TEM image of a single typical AN-TPMC, and (d) the schematic model of AN-TPMC exposed {001} and {101} facets.

experiment, 0.025 g of Ti powders, 250 μL of HF, and 7.50 mL of H2O2 were mixed with deionized water. Then, the solution was put into a dried Teflon-lined stainless steel autoclave, sealed, and heated at 180 °C for 10 h in an electric oven. All of the precipitates at the bottom were placed into a Muffle furnace for heat-treatment at 520 °C for 60 min in order to remove the fluorine element on AN-TMCs. The full details of the material synthesis and the approach of the experiments are provided in the Supporting Information. The X-ray diffraction (XRD) pattern as shown in Figure 1a revealed that all of the diffraction peaks agreed perfectly with those of the TiO2 anatase phase (JCPDS No. 21-1272) and without any impurity phase, suggesting the particles were welldeveloped and were pure TiO2 anatase phase. Moreover, the surface chemical composition was clearly demonstrated in the XPS spectrum (Figure 1b). The signals of Ti and O elements were detected. The slight quantity of F element on the ANTPMCs surface might be attributed to the use of HF during the synthesis process and could be easily removed after heating at 520 °C for 60 min in Figure 1b (binding energy at 684.5 eV), without changing the microcrystal structure and morphology. As shown in Figure 2a,b, scanning electron microscope (SEM) images of AN-TPMCs showed that the morphology

was decahedron. The top and bottom surfaces were square with a side length of 1 μm, and the width was 2 μm in the middle. The size and morphology of AN-TPMCs were also confirmed by the transmission electron microscopy (TEM) image in Figure 2c, and it could also reveal that AN-TPMCs were solid inside. According to the symmetry of anatase TiO2 crystals and studies in the past, the two flat and square surfaces at the top and bottom were {001} facets, and the eight trapezoid surfaces were {101} facets of the anatase crystal.29,30 Schematic illustration of AN-TPMC is shown in Figure 2d. SEM images of the mineralization of nano-CaP on ANTPMCs after soaking in the complete cell culture medium are shown in Figure 3. The nanodeposits were about 20 nm one particle, and AN-TPMC {101} facets were completely covered by a layer of the nanodeposits. This layer was compact by nanoparticles tightly aggregating one by one. We could not see {101} facets exposed at all in the SEM images but only nanodeposits, whereas only a few of the agglomerate nanoparticles were deposited and distributed sparsely on {001} facets. We could see that alarge proportion of the exposed area was the {001} facets. The schematic illustration of the nanodeposits on AN-TPMC is shown in Figure 3c. After soaking in the complete cell culture medium, Ca2p, P2s, and P2p B


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Figure 3. Low-magnification (a) and high-magnification (b) SEM images of the mineralization of nano-CaP on AN-TPMCs after soaking in the complete cell culture medium at 37 °C for 12 h, as well as the corresponding schematic illustration (c) and XPS spectrum (d).

Figure 4. Low-magnification (a) and high-magnification (b) SEM images of the mineralization of CaP on AN-TPMCs after soaking in FBS protein solution at 37 °C for 12 h, as well as the corresponding schematic illustration (c) and XPS spectrum (d).

shown in Figure 4a,b. The schematic illustration of the nanodeposits on AN-TPMC soaked in FBS protein solution is shown in Figure 4c. The XPS spectrum in Figure 4d also confirmed the nanodeposits were CaP. The distinct facetspecific mineralization behavior on AN-TPMCs occurred again. After AN-TPMCs was soaked in αMEM, both {001} and {101} facets were completely covered by the nanodeposits without obvious difference as shown in Figure 5a,b. The schematic illustration of the nanodeposits on AN-TPMC after soaking in αMEM culture medium is shown in Figure 5c. The XPS spectrum in Figure 5d confirmed the nanodeposits were CaP. The atomic ratio of P and Ca deposits in αMEM was about 1.1:1. It corresponded to the atomic ratio of CaHPO4,31 and the excrescent phosphorus element was from the amino acid.

peaks were obvious in the XPS spectrum (Figure 3d), which was not detected before soaking. It was evident that the complete cell culture medium gave rise to Ca and P core level signals (2s and 2p), suggesting that the deposited nanoparticles in SEM images were composed of CaP. Hence, a distinct facetspecific mineralization behavior on AN-TPMCs occurred in the complete cell culture medium. In order to understand what main factor is causing the mineralization difference between {101} and {001} facets, FBS protein solution and αMEM culture medium, which consist of the complete cell culture medium, were used to soak ANTPMCs separately. Surprisingly, after soaking in FBS protein solution, AN-TPMC {101} facets were completely covered by the nanodeposits, whereas there were none on {001} facets, as C


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Figure 5. Low-magnification (a) and high-magnification (b) SEM images of the mineralization of nano-CaP on AN-TPMCs after soaking in αMEM at 37 °C for 12 h, as well as the corresponding schematic illustration (c) and XPS spectrum (d).

Figure 6. Low-magnification (a) and high-magnification (b) SEM images of the mineralization of nano-CaP on AN-TPMCs after soaking in αMEM at 37 °C for 12 h after FBS preadsorbed at 37 °C for 6 h, as well as the corresponding schematic illustration (c) and XPS spectrum (d).

Figure 7. Low-magnification (a) and high-magnification (b) SEM images of the mineralization of nano-CaP on AN-TPMCs by UV illumination and then soaking in αMEM at 37 °C for 12 h after FBS was preadsorbed at 37 °C for 6 h. The red lines indicate boundaries of the crystal facets.

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Generally, protein adsorption on material surfaces occurs immediately once they come into contact with biological fluids40 when there are proteins in existence. Proteins can adsorb selectively on different crystal facets of one crystal particle28 because of water molecules of the solution and the surface hydroxyl groups. AN-TPMCs {001} and {101} facets are different in titanium saturability on the surfaces. Nondissociative water molecules adsorbed on the anatase {101} facets at both low and monolayer coverage,41,42 which could block the adsorption of FBS. On the anatase {001} facets, dissociative adsorption of water molecules was more stable,43,44 resulting in more surface hydroxyl groups, which could attract the adsorption of FBS. AN-TPMCs {001} were covered up by FBS, while only a few FBS were present on {101} facets. Ca2+ is in contact with interfacial FBS rather than {001} facets, and the number of Ca2+ sites available for nano-CaP mineralization decreases a lot due to the chelation with FBS. More FBS adsorbed on AN-TPMCs {001} facets result in FBS covering up the surfaces and chelating with Ca2+. This is why there are only a few nano-CaPs on {001} facets and sparse distribution with the existence of FBS. On the basis of the above analysis, mineralization of nano-CaP on {001} facets with the existence of FBS proteins is much downregulated due to the chelation between FBS and Ca2+. Nevertheless, mineralization on {101} facets is similar to that in αMEM due to the higher number of Ca2+ sites combining with HPO42− for nano-CaP mineralization when a few of the FBS on them chelated with Ca2+. On the other hand, when there is no FBS but only αMEM, the oxygen positions of the AN-TPMCs both facets match well with CaP;45 thus, no facet-specific mineralization behavior on ANTPMCs occurred in αMEM. When there is FBS present, more FBS adsorbed on AN-TPMCs {001} facets resulting in hindering the good matching between nano-CaP and {001} facets. Hence, a distinct facet-specific mineralization behavior on AN-TPMCs occurred in the presence of FBS. Interfacial FBS proteins have a strong negative influence on the mineralization of nano-CaP.46−48 FBS is extracted from the blood, and there is also a small amount of Ca2+ and HPO42− present in the FBS protein solution. This was why CaP formed in the FBS protein solution in Figure 4. It is well known that TiO2 with UV illumination leads to the improvement of hydrophilicity49 and that multilayer water molecules adsorb on the surfaces after UV illumination. The change in surface water molecules would greatly affect protein adsorption and usually prevent direct contact between protein and surfaces.50,51 Hence, UV illuminated AN-TPMCs could greatly reduce FBS adsorption on {001} facets, causing no distinction of the nano-CaP mineralization in αMEM with FBS between two facets (Figure 7). The fact proves again that the facet-specific mineralization of CaP on AN-TPMCs originated from the difference in protein adsorption between {001} and {101} facets. Although there are amino acids from αMEM detected to adsorb on the AN-TPMCs surface, it is unlikely to play a role in the mineralization behavior of nano-CaP (Figure 5). Therefore, we believe that the distinct facet-specific mineralization behavior on AN-TPMCs are dominant by the different adsorption behaviors of FBS on {001} and {101} facets. In summary, we demonstrated the facet-specific mineralization of nano-CaP on {101} facets of anatase TiO2 polyhedral, while there were only a few on {001} facets. The preadsorbed FBS proteins on {001} facets in complete cell culture medium might play a barrier role to effectively prevent sequent

No facet-specific mineralization behavior on AN-TPMCs occurred in αMEM culture medium. In order to further reveal the effects of FBS protein solution on the mineralization of nano-CaP, AN-TPMCs were soaked in FBS protein solution first at 37 °C for 6 h; then, they were soaked in αMEM for 12 h at 37 °C. When they were soaked in αMEM after FBS was preadsorbed, the nanodeposits on ANTPMCs were dramatically different on different crystal facets (Figure 6), similar to the results of those soaked in the complete cell culture medium. The distinct facet-specific mineralization behavior on AN-TPMCs occurred again. It indicated that the different AN-TPMCs facets with preadsorbed FBS eventually affect the mineralization behavior of nano-CaP. The new signal peak appearing at about 400 eV in XPS spectra could be attributed to the N 1s signal of protein nitrogen32 from the protein adsorbed on the surfaces. The Fourier transform infrared (FTIR) spectrum (Figure S1) also revealed that there were proteins adsorbed on AN-TPMCs after soaking in FBS. The spectrum showed the most characteristic features of the proteins.33 The broad band could be attributed to proteins, which all appeared in the FTIR spectrum. After irradiating under 254 nm ultraviolet light (UV) for 1 h, AN-TPMCs were soaked in FBS protein solution at 37 °C for 6 h; then, they were soaked in αMEM for 12 h at 37 °C. It indicated that facet-specific mineralization behavior on ANTPMCs disappeared after UV illumination (Figure 7). The EDS scanning is an effective method to detect CaP on the material.34 The EDS line scanning results (Figure S2c) also confirmed Ca and P signals of the nanodeposits on AN-TPMC, indicating the nanodeposits were CaP. The distinct facetspecific mineralization behavior on AN-TPMC was also confirmed by the TEM image (Figure S2a). The crystal structure of the particles we synthesized was anatase phase without any impurity phase (Figure 1a-b), and the microcrystals were decahedron exposed {001} facets and {101} facets (Figure 2). There was no facet-specific mineralization behavior on AN-TPMCs occurring when soaking in αMEM (Figure 5). Whereas the distinct facetspecific mineralization behavior on AN-TPMCs {001} and {101} facets occurred in the three other solutions in this work (Figures 3, 4, and 6), all with the existence of FBS, nano-CaP was completely covered on {101} facets, but a few of the agglomerate nano-CaPs were deposited and distributed sparsely on {001} facets. The nano-CaP layer on AN-TPMCs in FBS protein solution (Figure 4) was much thinner than that in the complete cell culture medium (Figure 3). It could be also confirmed from the peak intensity in XPS spectra. That was because the concentration of Ca2+ and HPO42− in FBS protein solution was much less than that in the complete cell culture medium. There are many factors that affect CaP nucleation and deposition on a material surface.35 The deposits in our work corresponded to CaHPO4, which was also confirmed at pH between 7 and 10.36 The electrostatic force for Ca2+ and HPO42− on the surface is the main factor.37 TiO2 surfaces are always negatively charged in an aqueous environment due to OH− groups; this could be advantageous to the adsorption of Ca2+ and HPO42−,38 which could induce mineralization of CaP.39 Thus, the mineralization occurs in both AN-TPMCs {001} and {101} facets in αMEM due to the attraction on Ca2+ and HPO42− when there is no protein but only αMEM. There is no facet-specific mineralization behavior on AN-TPMCs without protein. E


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(9) Dorozhkin, S. V. Nanosized and nanocrystalline calcium orthophosphates. Acta Biomater. 2010, 6 (3), 715−34. (10) Zhou, H.; Lee, J. Nanoscale hydroxyapatite particles for bone tissue engineering. Acta Biomater. 2011, 7 (7), 2769−81. (11) Tang, R. K.; Wang, L. J.; Orme, C. A.; Bonstein, T.; Bush, P. J.; Nancollas, G. H. Dissolution at the nanoscale: Self-preservation of biominerals. Angew. Chem., Int. Ed. 2004, 43 (20), 2697−2701. (12) Surmenev, R. A.; Surmeneva, M. A.; Ivanova, A. A. Significance of calcium phosphate coatings for the enhancement of new bone osteogenesis–a review. Acta Biomater. 2014, 10 (2), 557−79. (13) Kokubo, T.; Takadama, H. How useful is SBF in predicting in vivo bone bioactivity? Biomaterials 2006, 27 (15), 2907−15. (14) Ruso, J. M.; Verdinelli, V.; Hassan, N.; Pieroni, O.; Messina, P. V. Enhancing CaP Biomimetic Growth on TiO2 Cuboids Nanoparticles via Highly Reactive Facets. Langmuir 2013, 29 (7), 2350− 2358. (15) von Wilmowsky, C.; Moest, T.; Nkenke, E.; Stelzle, F.; Schlegel, K. A. Implants in bone: part II. Research on implant osseointegration: material testing, mechanical testing, imaging and histoanalytical methods. Oral Maxillofac Surg 2014, 18 (4), 355−72. (16) Barrere, F.; van Blitterswijk, C. A.; de Groot, K. Bone regeneration: molecular and cellular interactions with calcium phosphate ceramics. Int. J. Nanomedicine 2006, 1 (3), 317−32. (17) Alghamdi, H. S.; Bosco, R.; van den Beucken, J. J.; Walboomers, X. F.; Jansen, J. A. Osteogenicity of titanium implants coated with calcium phosphate or collagen type-I in osteoporotic rats. Biomaterials 2013, 34 (15), 3747−57. (18) Eagle, H. Nutrition needs of mammalian cells in tissue culture. Science 1955, 122 (3168), 501−14. (19) Eagle, H. Amino acid metabolism in mammalian cell cultures. Science 1959, 130 (3373), 432−7. (20) Tas, A. C. Grade-1 titanium soaked in a DMEM solution at 37 degrees C. Mater. Sci. Eng., C 2014, 36, 84−94. (21) Faure, J.; Balamurugan, A.; Benhayoune, H.; Torres, P.; Balossier, G.; Ferreira, J. M. F. Morphological and chemical characterisation of biomimetic bone like apatite formation on alkali treated Ti6Al4V titanium alloy. Mater. Sci. Eng., C 2009, 29 (4), 1252− 1257. (22) Dumelie, N.; Benhayoune, H.; Richard, D.; Laurent-Maquin, D.; Balossier, G. In vitro precipitation of electrodeposited calciumdeficient hydroxyapatite coatings on Ti6Al4V substrate. Mater. Charact. 2008, 59 (2), 129−133. (23) Drevet, R.; Velard, F.; Potiron, S.; Laurent-Maquin, D.; Benhayoune, H. In vitro dissolution and corrosion study of calcium phosphate coatings elaborated by pulsed electrodeposition current on Ti6Al4V substrate. J. Mater. Sci.: Mater. Med. 2011, 22 (4), 753−61. (24) Albrektsson, T.; Branemark, P. I.; Eriksson, A.; Lindstrom, J. The preformed autologous bone graft. An experimental study in the rabbit. Scand. J. Plast. Reconstr. Surg. 1978, 12 (3), 215−23. (25) Hazan, R.; Brener, R.; Oron, U. Bone-Growth to Metal Implants Is Regulated by Their Surface Chemical-Properties. Biomaterials 1993, 14 (8), 570−574. (26) Nooney, M. G.; Campbell, A.; Murrell, T. S.; Lin, X. F.; Hossner, L. R.; Chusuei, C. C.; Goodman, D. W. Nucleation and growth of phosphate on metal oxide thin films. Langmuir 1998, 14 (10), 2750−2755. (27) Murphy, M.; Walczak, M. S.; Hussain, H.; Acres, M. J.; Muryn, C. A.; Thomas, A. G.; Silikas, N.; Lindsay, R. An ex situ study of the adsorption of calcium phosphate from solution onto TiO2(110) and Al2O3(0001). Surf. Sci. 2016, 646, 146−153. (28) Dong, L.; Luo, Q.; Cheng, K.; Shi, H.; Wang, Q.; Weng, W.; Han, W. Q. Facet-specific assembly of proteins on SrTiO(3) polyhedral nanocrystals. Sci. Rep. 2015, 4, 5084. (29) Yang, H. G.; Sun, C. H.; Qiao, S. Z.; Zou, J.; Liu, G.; Smith, S. C.; Cheng, H. M.; Lu, G. Q. Anatase TiO2 single crystals with a large percentage of reactive facets. Nature 2008, 453 (7195), 638−41. (30) Liu, M.; Piao, L.; Zhao, L.; Ju, S.; Yan, Z.; He, T.; Zhou, C.; Wang, W. Anatase TiO(2) single crystals with exposed {001} and

nucleation of nano-CaP. Our results suggested that the mineralization of nano-CaP on metal oxide surface might be dependent on preadsorbed protein, which could be further attributed to the distinct surface atomic structures of facets. This work therefore demonstrated the central role of metal oxide distinct crystal facets in mediating the mineralization of nano-CaP. Nevertheless, this still needs to be further uncovered in the future, and with more understanding, it may help optimize the osteointegration of orthopedic and dental implants.

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ASSOCIATED CONTENT

* Supporting Information S

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsbiomaterials.7b00234. Detailed methods for preparing AN-TPMCs; experimental details; FTIR spectra; TEM; and EDS spectra (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. ORCID

Lingqing Dong: 0000-0002-2203-3212 Wenjian Weng: 0000-0002-9373-7284 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was financially supported by National Natural Science Foundation of China (51472216, 51372217, 31570962, and 51502262), Zhejiang Provincial Natural Science Foundation (LY15E020004), the 111 Project under Grant No. B16042, and the Fundamental Research Funds for the Central Universities (2017XZZX008-05).

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ABBREVIATIONS AN-TPMC, anatase TiO2 polyhedral microcrystals REFERENCES

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Facet-Specific Mineralization Behavior of Nano-CaP on Anatase

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