Large-Scale Automated Production of Highly Ordered Ultralong

Dec 6, 2016 - Practical applications of nanostructured materials have been largely limited by the difficulties in controllable and scaled-up synthesis...
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Large-Scale Automated Production of Highly Ordered Ultralong Hydroxyapatite Nanowires and Construction of Various Fire-Resistant Flexible Ordered Architectures Feng Chen and Ying-Jie Zhu* State Key Laboratory of High Performance Ceramics and Superfine Microstructure, Shanghai Institute of Ceramics, Chinese Academy of Sciences, Shanghai 200050, P. R. China S Supporting Information *

ABSTRACT: Practical applications of nanostructured materials have been largely limited by the difficulties in controllable and scaled-up synthesis, large-sized highly ordered self-assembly, and macroscopic processing of nanostructures. Hydroxyapatite (HAP), the major inorganic component of human bone and tooth, is an important biomaterial with high biocompatibility, bioactivity, and high thermal stability. Large-sized highly ordered HAP nanostructures are of great significance for applications in various fields and for understanding the formation mechanisms of bone and tooth. However, the synthesis of large-sized highly ordered HAP nanostructures remains a great challenge, especially for the preparation of large-sized highly ordered ultralong HAP nanowires because ultralong HAP nanowires are easily tangled and aggregated. Herein, we report our three main research findings: (1) the large-scale synthesis of highly flexible ultralong HAP nanowires with lengths up to >100 μm and aspect ratios up to >10000; (2) the demonstration of a strategy for the rapid automated production of highly flexible, fireresistant, large-sized, self-assembled highly ordered ultralong HAP nanowires (SHOUHNs) at room temperature; and (3) the successful construction of various flexible fire-resistant HAP ordered architectures using the SHOUHNs, such as high-strength highly flexible nanostructured ropes (nanoropes), highly flexible textiles, and 3-D printed well-defined highly ordered patterns. The SHOUHNs are successively formed from the nanoscale to the microscale then to the macroscale, and the ordering direction of the ordered HAP structure is controllable. These ordered HAP architectures made from the SHOUHNs, such as highly flexible textiles, may be engineered into advanced functional products for applications in various fields, for example, fireproof clothing. KEYWORDS: hydroxyapatite, nanowires, self-assembly, ordered structure, biomineralization, fire-resistant

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imposes major challenges in materials science. Among different morphologies of HAP, HAP nanowires are very promising for applications in various fields. Especially, ultralong HAP nanowires have enhanced properties and thus will widen and facilitate their applications in various fields such as bone tissue engineering, drug delivery, adsorbent for organic pollutants and heavy metal ions, and fire-resistant inorganic paper.3 Up to now, a variety of synthetic methods have been reported for the preparation of HAP nanowires, including the solvothermal/ hydrothermal method,3−6 microwave-assisted synthesis,7,8 hard template using porous anodic aluminum oxide,9 sol−gel process,10

ydroxyapatite (HAP) is the major inorganic component of human bone and tooth. HAP biomaterials have advantages such as high biocompatibility, bioactivity, and high thermal stability, thus, they are ideal functional materials for various biomedical applications such as bone repair/tissue engineering and drug delivery.1,2 Nanotechnology provides the possibilities for achieving the control over the structure, size, and morphology, and thus enhanced properties of HAP biomaterials. However, achieving ideal properties and applications of HAP nanostructured biomaterials remains a great challenge due to the difficulties in controllable and scaledup synthesis, fabrication of large-sized ordered nanostructures, and macroscopic processing of nanostructures. The facile synthesis of highly ordered HAP nanostructures with high flexibility, high strength and fabricability at the macroscopic level © 2016 American Chemical Society

Received: October 27, 2016 Accepted: November 30, 2016 Published: December 6, 2016 11483

DOI: 10.1021/acsnano.6b07239 ACS Nano 2016, 10, 11483−11495

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Figure 1. Characterization of highly flexible ultralong HAP nanowires obtained by the large-scale (5000 mL volume reaction system) calcium oleate precursor solvothermal method in the reaction system containing CaCl2, NaOH, NaH2PO4·2H2O, oleic acid, water, and methanol. (A) The stainless steel autoclave with a volume of 10000 mL used in the large-scale synthesis of ultralong HAP nanowires and the as-prepared solvothermal product slurry containing ultralong HAP nanowires. (B) Digital images of ultralong HAP nanowires which are separated from the solvothermal product slurry and dispersed in ethanol. (C−E) SEM micrographs of randomly distributed ultralong HAP nanowires. (F−H) TEM micrographs of randomly distributed ultralong HAP nanowires, and a high-resolution TEM (HRTEM) image of a single HAP nanowire is shown in (H), the inset of (H) shows an electron diffraction pattern.

and reverse micelles.11 Although some progress has been made, the facile large-scale synthesis of ultralong HAP nanowires with lengths up to >100 μm and their self-assembled highly ordered nanostructures is highly challengeable and has not been reported. Human bone and tooth have complex and highly ordered structures which are a unique nanocomposite of oriented apatite nanocrystals impregnated in the organic matrix.12 During the formation of mineralized tissues, oriented apatite nanocrystals are formed from the amorphous state under the direction of collagen molecules.13−15 The complex and oriented structures in bone and tooth can achieve a remarkable mechanical performance that combines the toughness of the inorganic material and flexibility of the organic matrix.16,17 However, the natural biomineralization growth of human bone and tooth is a very slow process that takes many years, which is not a practical method for the preparation of biomimetic materials for biomedical applications. It was reported that ordered HAP structures were synthesized using organic molecules,18,19 templates,9,20 substrates,21−23 collagen,24,25 silk,26 peptide-amphiphile,27 polymers,28,29 freezing,30,31 phase transformation,32 and hydrothermal strategy.33 However, the as-prepared ordered HAP structures are usually small in size with the order of several microns. Large-sized highly ordered HAP nanostructures, especially those with sizes larger than 100 μm, are very difficult to prepare. In addition, the removal of hard templates or substrates used in the synthesis

may cause damage to the ordered nanostructures. Although some progress has been made, the facile preparation of largesized highly ordered ultralong HAP nanowires with high flexibility, high strength and fabricability in the macroscopic scale remains a great challenge because ultralong HAP nanowires are easily tangled and aggregated. The scaled-up production of nanostructured materials is a universal challenge in nanotechnology and materials science, especially in dealing with highly ordered nanostructured materials. Only a few reports have been published in the literature, including the bioinspired process, plasma, flame, milling, and pyrolysis, for the scaled-up preparation of various kinds of nanostructured materials such as BaTiO3 nanoparticles, copper metal and oxide nanocrystals, and various monodisperse nanoparticles.34−36 To the best of our knowledge, the largescale synthesis of ultralong HAP nanowires with lengths up to >100 μm remains a great challenge and has not been reported. Herein, we report our three main research findings: (1) the realization of large-scale synthesis of highly flexible ultralong HAP nanowires with lengths up to >100 μm and aspect ratios up to >10000; (2) the demonstration of a strategy for the rapid automated production of highly flexible, fire-resistant, largesized, self-assembled highly ordered ultralong HAP nanowires (SHOUHNs) at room temperature; and (3) the successful construction of various flexible fire-resistant ordered HAP architectures using the SHOUHNs at room temperature, such as highly flexible high-strength nanostructured ropes (nanoropes), highly 11484

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ACS Nano flexible textiles, and 3-D printed well-defined highly ordered patterns, which may be engineered into functional highly ordered advanced products with promising applications in various fields.

RESULTS AND DISCUSSION Large-Scale Synthesis and Characterization of Highly Flexible Ultralong HAP Nanowires. The large-scale production of nanostructured materials is a key factor for the realization of their practical applications, but remains a great challenge. The laboratory synthesis of nanostructured materials is usually in a small scale of 100 μm and aspect ratios up to >10000 in the reaction system containing CaCl2, NaOH, NaH2PO4·2H2O, oleic acid, water, and methanol by the calcium oleate precursor solvothermal method (Figure 1A). The yield of HAP nanowires under the present experimental conditions is relatively high (∼93%). The solvothermal product slurry containing ultralong HAP nanowires can be obtained after the solvothermal treatment, which is highly stable and can preserve the homogeneous dispersion state for at least 6 months without precipitation. Figure 1B shows digital images of ultralong HAP nanowires which are separated from the solvothermal product slurry and dispersed in ethanol, exhibiting a filament-like morphology in a floccule-like state. The scanning electron microscopy (SEM) micrographs of the product are shown in Figure 1C−E, and transmission electron microscopy (TEM) images are shown in Figure 1F−H and Figure S1 in the Supporting Information. The product is composed of ultralong HAP nanowires with diameters of about 10 nm and lengths up to >100 μm and aspect ratios up to >10000. The as-prepared ultralong HAP nanowires tend to self-assemble to form nanowire bundles along the direction parallel to the c axis of single HAP nanowires (Figure 1E). Ultralong HAP nanowires are single crystalline in structure, and a high-resolution TEM (HRTEM) image of a single HAP nanowire reveals that the fringe spacings are 0.46 and 0.34 nm (Figure 1H), corresponding to the crystal planes of (110) and (002), respectively. The preferential growth direction of a single HAP nanowire is along the c-axis of HAP. The X-ray diffraction (XRD) pattern of ultralong HAP nanowires shows a single phase of hydroxyapatite (JCPDS no. 09-0432), as shown in Figure 2. In addition, we characterized two different natural minerals of apatite, and the powder XRD patterns of the yellow crystal and blue stone can be indexed to fluorapatite (JCPDS no. 70-0796). Both fluorapatite and hydroxyapatite belong to the minerals of apatite and have similar crystal structures. Although the as-prepared ultralong HAP nanowires have similar chemical and crystal structure to the natural apatite minerals, but their morphologies are obviously different. The as-prepared ultralong HAP nanowires are highly flexible, and they can bend naturally. In contrast, the natural minerals of apatite are fragile and brittle without flexibility. It is well-known that the flexibility of metals can be enhanced by reducing their diameters (Video S1 in the Supporting Information). However, it is difficult to achieve high flexibility of inorganic nonmetallic materials using the same strategy due to their high brittleness. The as-prepared ultralong HAP nanowires are highly flexible, and they can bend naturally at large angles (Figure 1C,D,F). The experimental results in this work demonstrate the feasibility of preparing highly flexible HAP materials using ultralong HAP nanowires as the building blocks.

Figure 2. XRD patterns and digital images of natural apatite minerals (fluorapatite) and ultralong HAP nanowires prepared by the large-scale calcium oleate precursor solvothermal method in the reaction system containing CaCl2, NaOH, NaH2PO4·2H2O, oleic acid, water, and methanol.

Formation Mechanism of Highly Flexible Ultralong HAP Nanowires. The large-scale production (5000 mL volume) of highly flexible ultralong HAP nanowires has been successfully realized by the scaled-up calcium oleate precursor solvothermal method in the reaction system containing CaCl2, NaOH, NaH2PO4·2H2O, oleic acid, water, and methanol. We propose a formation mechanism of ultralong HAP nanowires. In this work, ultralong HAP nanowires are synthesized based on a liquid−solid−solution mechanism.37,38 At the early stage of the synthetic process, calcium oleate forms before the solvothermal treatment through the chemical reaction between calcium ions and oleic acid in the reaction system containing CaCl2, NaOH, NaH2PO4·2H2O, oleic acid, water, and methanol. Calcium oleate plays an important role in the formation of ultralong HAP nanowires, acting as both the calcium source and the precursor.3 Calcium oleate can slowly and continuously provide Ca2+ ions for the formation of HAP, thus control the formation rate of HAP nuclei. HAP nuclei form via the chemical reactions between calcium oleate, OH−, and PO43− ions under the solvothermal conditions. Then, the newly formed HAP nuclei grow into ultralong HAP nanowires in a relatively long period of time under the solvothermal conditions at relatively high temperatures and high pressures. The molecules of oleic acid adsorbed on HAP nanowires may also play a role in the formation of ultralong HAP nanowires by directing the 1-D crystal growth of HAP. Finally, ultralong HAP nanowires are obtained and well dispersed in the reaction system, forming a viscous solvothermal product slurry (Figure 1A). The excellent dispersion property of ultralong HAP nanowires in the solvothermal product slurry is attributed to the unique reaction environment and the adsorption of oleic acid molecules on the surface of ultralong HAP nanowires. In this reaction system, there are abundant oleic acid molecules and sodium ions, which play a role as an anionic surfactant and can improve the dispersity of ultralong HAP nanowires. In addition, the dynamic environment under stirring during the solvothermal treatment is also propitious to the excellent dispersity of ultralong HAP nanowires in the reaction system. The unique reaction system results in high stability of the solvothermal product slurry, which can preserve the homogeneous dispersion state for at least 6 months without precipitation. 11485

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ACS Nano Rapid Automated Production of Highly Flexible, FireResistant, Large-Sized, Self-Assembled Highly Ordered Ultralong HAP Nanowires. We have developed a simple method for the rapid automated production at room temperature of highly flexible, fire-resistant, large-sized, self-assembled highly ordered ultralong HAP nanowires (SHOUHNs) using the as-prepared solvothermal product slurry containing ultralong HAP nanowires. The concentration of HAP nanowires in the as-prepared solvothermal product slurry for the preparation of the SHOUHNs is about 3.7 mg mL−1. Figure 3 and Video S2

product slurry in absolute ethanol and drying. The oriented direction of the SHOUHNs can be well controlled by simply adjusting the moving direction of the injecting needle. This simple prototype of the rapid automated production provides the possibility of realizing the scaled-up or even industrial production of large-sized SHOUHNs. Formation Mechanism of the Highly Flexible, FireResistant, Large-Sized SHOUHNs. The formation mechanism of the SHOUHNs is schematically illustrated in Figure 5, and will be discussed later. The Fourier transform infrared (FTIR) spectrum (Figure 6) indicates the interaction between carboxylic groups of oleic acid molecules and HAP nanowires. Two sharp bands at 2927 and 2856 cm−1 are attributed to the asymmetric and symmetric stretches of the CH2 groups in oleic acid molecules. The absorption bands at 1457, 1560, and 1620 cm−1 are attributed to the −COO− group.39 In addition, the bands corresponding to the PO43− group are observed at about 1027, 605, and 563 cm−1, while the peak at 3567 cm−1 can be assigned to the hydroxyl group of HAP.40 According to the literature, the absorption bands of oleic acid are located at about 1286, 1417, 1460, and 1710 cm−1 in the FTIR spectrum. For the as-prepared ultralong HAP nanowires in this work, the different absorption bands of the −COO− group appear, indicating the bridging coordination between oleic acid molecules and HAP nanowires.37,39,41 Furthermore, we propose that the SHOUHNs are formed by a surface-induced instant self-assembly process (Figure 5A,B). In the reaction system, oleic acid molecules can adsorb on the surface of ultralong HAP nanowires through the interaction between carboxylic groups of oleic acid molecules and calcium ions of HAP nanowires, and the alkyl chains expose to the mixed solvent. When the solvothermal product slurry containing ultralong HAP nanowires is injected into absolute ethanol, the constituents of water, methanol, and oleic acid in the solvothermal product slurry can diffuse into ethanol. Because the alkyl chains of oleic acid molecules are incompatible with the polar solvent (ethanol, methanol and water), ultralong HAP nanowires are separated out from the solution. In the process of solvent diffusion, oleic acid molecules adsorbed on the surface of ultralong HAP nanowires may modulate the self-assembly process of ultralong HAP nanowires by the “alcohol−oleic acid” interaction, expelling ultralong HAP nanowires to form aligned nanowire bundles. Since HAP nanowires have ultralong lengths, each ultralong HAP nanowire may present in different aligned nanowire bundles. Therefore, the ultralong HAP nanowires may be linked to each other by this connection, instantly forming the SHOUHNs, which are parallel to the moving direction of the injecting needle. We directly observed the formation process of the SHOUHNs by an optical microscope. The photographs (Figure 5C) are obtained under an optical microscope after in situ injecting the solvothermal product slurry containing ultralong HAP nanowires into absolute ethanol for different times of 2, 10, 20, 30, and more than 30 s. The formation of the SHOUHNs is a rapid process. The photographs on the edge and middle part of the SHOUHNs exhibit continuously aligned highly ordered structure of ultralong HAP nanowires. We clearly observed the change in the product with increasing time from 2 to 30 s, indicating the process of the solvent diffusion and the SHOUHNs formation. Furthermore, the strategy reported herein can be extended using different solvents (Figure S2 in the Supporting Information). The SEM micrographs show that the ordered structures of ultralong HAP nanowires can also be obtained

Figure 3. Rapid automated production of the SHOUHNs by simply injecting the solvothermal product slurry containing ultralong HAP nanowires into absolute ethanol at room temperature using the homemade automated equipment with round-end needles with an inner diameter of 1.69 mm. (A) A digital image showing the automated production of the SHOUHNs. (B, C) Digital images showing the as-prepared large-sized SHOUHNs.

(in the Supporting Information) demonstrate the automated preparation process of the SHOUHNs by simply injecting the solvothermal product slurry containing ultralong HAP nanowires into absolute ethanol at room temperature using our homemade automated equipment with round-end needles with an inner diameter of 1.69 mm. When the solvothermal product slurry containing ultralong HAP nanowires is injected through a syringe into absolute ethanol, the SHOUHNs are obtained instantly. The as-prepared SHOUHNs are smooth on the surface and highly flexible and are easy to be picked up and rolled up, as shown in Figure 4A,B. The SEM micrographs in Figure 4C−E show the highly ordered ultralong HAP nanowires in the SHOUHNs. The length of the SHOUHNs can be easily controlled by injecting a certain amount of the solvothermal product slurry containing ultralong HAP nanowires. The more the amount of the injected solvothermal product slurry, the longer the SHOUHNs. On the other hand, the diameter of the SHOUHNs can be easily controlled by the inner diameter of the needle used for injection, and the SHOUHNs with different diameters can be obtained by using needles with different inner diameters. It should be noted that the diameter of the SHOUHNs is smaller than the inner diameter of the injecting needle after the diffusion of the solvent from the solvothermal 11486

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Figure 4. Characterization of the SHOUHNs prepared by simply injecting the solvothermal product slurry containing ultralong HAP nanowires into absolute ethanol at room temperature. (A, B) Digital images showing the large-sized SHOUHNs. (C−E) SEM micrographs of the SHOUHNs.

nonwoven HAP textile made from the SHOUHNs is also prepared by moving the injecting needle along random directions (Figure 10C). The HAP textiles with different shapes can be easily fabricated according to the design. A complex well-designed flexible highly ordered pattern made from the SHOUHNs as the building material is also prepared by injecting the solvothermal product slurry into absolute ethanol along predetermined directions according to a designed pattern (Figure 10D). Furthermore, we have demonstrated the feasibility for the fabrication of the well-defined highly ordered 3-D HAP patterns which is constructed with the SHOUHNs using a commercial 3-D printer (Figure 10E,F and Video S3 in the Supporting Information). The Mechanical Properties of Highly Flexible FireResistant HAP Nanoropes. The HAP nanorope made from the SHOUHNs has a high flexibility and high strength. The combined HAP nanoropes obtained by twisting different numbers of single nanorope(s) were used for the investigation of the tensile stress−strain properties, as shown in Figure 11A, Figure S3 in the Supporting Information. The tensile strength significantly increases when the number of single nanoropes constituting a combined nanorope increases from 1 to 3. When the number of single nanorope(s) is 1, 2, 3, and 4, the maximum tensile strength of the combined HAP nanorope is 40.1, 65.8, 105.8, and 90.4 MPa, and the tensile strains of the combined HAP nanoropes range from 1.4 to 3.1%. A combined HAP nanorope by twisting 36 single nanoropes can even sling a weight of 500 g without breaking (Figure 11B). In addition, the high flexibility of the combined HAP nanorope can be maintained, which can be bent and tied into a knot (Figure 8A). Usually, the reported strengths of the compact bones are in the range of 78.8−151 MPa in a longitudinal direction (parallel to the long axis of the osteons) and 51−56 MPa in a transverse direction (perpendicular to the long axis of the osteons).42 The as-prepared flexible and fire-resistant HAP nanoropes exhibit not only compatible tensile strengths with natural bones but also high flexibility which can resist high compressive strength without fracture. The common HAP materials are usually fragile and ceramic-like, which can be easily crushed (Video S4 in the Supporting Information). Significantly different from the well-known HAP materials, the as-prepared HAP textiles made from the SHOUHNs display a high flexibility, which can be

in different alcohols, indicating the wide applicability of the method reported in this paper. The reported strategy herein is significant for developing flexible fire-resistant highly ordered inorganic (nonmetal/noncarbon) nanostructured materials. Construction of Various Flexible Fire-Resistant Highly Ordered HAP Architectures Using the SHOUHNs at Room Temperature. The as-prepared SHOUHNs are highly flexible, highly ordered, and fire-resistant and can be used as the building material for constructing various flexible and fireresistant ordered HAP architectures at room temperature, such as high-strength highly flexible nanoropes, highly flexible textiles, and 3-D printed highly ordered patterns with promising applications in various fields. The strategies for the preparation of the HAP nanorope and textile are illustrated in Figure 7. Several single nanoropes consisting of the SHOUHNs can be easily twisted together to obtain a combined HAP nanorope (Figure 8A). SEM micrographs (Figure 8B) indicate that the highly ordered structure of ultralong HAP nanowires can be well preserved on the surface of the combined HAP nanorope. SEM micrographs in Figure 8C exhibit the end of a bent combined HAP nanorope, indicating that the highly ordered structure of ultralong HAP nanowires is well preserved even at the bent end of the combined HAP nanorope. The SEM micrographs in Figure 8D show the cross section of a combined HAP nanorope which is cut off by a common scissors, exhibiting the highly ordered structure of ultralong HAP nanowires inside the nanorope. The highly flexible fire-resistant ordered HAP textiles constructed with the SHOUHNs as the highly ordered building blocks are successfully prepared by crisscross moving the injecting needles at room temperature (Figure 9). Figure 7B illustrates the strategy for the preparation of the gauze-like textile made from the SHOUHNs. The digital images of the as-prepared HAP textiles shown in Figure 9A−D exhibit a similar morphology to the common cotton gauze. The SEM micrographs (Figure 9E,F) show that the highly ordered structure of ultralong HAP nanowires are well preserved in the as-prepared textile. The flexible HAP textile made from the SHOUHNs with the subparallel (Figure 10A) orientation is prepared by moving the injecting needle along subparallel direction. The flexible HAP textile can be further rolled into a 3-D column which is flexible and can be easily folded (Figure 10B). Moreover, the 11487

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Figure 5. Formation mechanism of ultralong HAP nanowires and SHOUHNs. (A, B) Schematic illustration of the formation mechanism of ultralong HAP nanowires and ordering process of ultralong HAP nanowires. (C) Optical micrographs obtained under an optical microscope after in situ injecting the solvothermal product slurry containing ultralong HAP nanowires into absolute ethanol using a syringe with a needle with an inner diameter of 0.41 mm for different times of 2, 10, 20, 30, and more than 30 s.

Cytocompatibility and Cell Morphologies on the SHOUHNs. The cell proliferation curves in Figure 12A,B indicate a high biocompatibility of the as-prepared SHOUHNs. Compared with the blank control samples, the experimental samples (the SHOUHNs) do not show obvious effects on the viability of human bone mesenchymal stem cells (hBMSC) and osteoblast cells (hFOB 1.19) from 1 to 7 days. The SEM micrographs and fluorescent image of hBMSC cells cultured on the SHOUHNs exhibit a good growth state, which can grow along the SHOUHNs (Figure 12C−F). The high biocompatibility of the as-prepared SHOUHNs can be explained by the chemical properties of HAP, which is the major inorganic component of human bone and tooth. HAP-based biomaterials have high biocompatibility, thus, they are promising for applications in bone repair/tissue engineering.2 However, it is well-known that the reported HAP scaffolds and HAP ceramics are usually brittle, which limits their applications in various biomedical fields.43,44 Combining high biocompatibility, high flexibility,

Figure 6. FTIR spectrum of the as-prepared ultralong HAP nanowires.

repeatedly folded and thumped, just like common cotton textiles (Video S4 in the Supporting Information). 11488

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on a fire flame, while the cotton on the aluminum foil quickly burns on the fire flame. Figure 13C and Video S5 in the Supporting Information show a conventional cotton textile which is flammable, and the flower underneath the cotton textile is destroyed after the burning of a conventional paper above. In contrast, the HAP textile made from the SHOUHNs is nonflammable and fireproofing, and the flower underneath the HAP textile can be well protected after the burning of a conventional paper above. The excellent fire-resistant performance of the highly flexible HAP textile made from the SHOUHNs is promising for the application in fireproof clothing. The fire-resistant properties of the HAP textiles can be explained by their high thermal stability, excellent nonflammability, and low thermal diffusivity. Compared with the common cotton, the weight loss and endothermic/exothermic properties of the SHOUHNs used for the preparation of the HAP textiles are very small and stable from the room temperature to 1000 °C (Figure 13E). As shown by the TG curve in Figure 13E, the total weight loss of the SHOUHNs is ∼2.5% from 100 to 500 °C, which is approximate to the amount of oleic acid molecules adsorbed on the SHOUHNs. The thermal diffusivities of the SHOUHNs were measured to be as low as 7.2 × 10−4, 1.3 × 10−3, and 2.6 × 10−3 cm2 s−1 at 300, 900, and 1200 °C, respectively. Compared with the reported inorganic nonmetallic fibers/ wires, the as-prepared SHOUHNs and their derived ordered architectures such as HAP nanoropes and textiles display many advantages in terms of flexibility, thermal stability, and biosafety (Table S1 in the Supporting Information). The control over the synthesis, diameter, length, self-assembly, highly ordered

Figure 7. Schematic illustration of the strategies for the preparation of the high-strength highly flexible fire-resistant HAP nanorope (A) and the highly flexible fire-resistant cotton-like textile (B).

excellent mechanical properties, and fire-resistance, the highly ordered HAP architectures made of the SHOUHNs display promising applications in various fields. The Fire-Resistant Performance of the SHOUHNs and Their Derived Ordered Architectures. The SHOUHNs and their derived ordered architectures are biocompatible, flexible, and fireproofing (Figure 13), very different from the flammable conventional ropes used in daily life usually made from organic plant fibers such as hemp, flax, jute, and flammable cotton textiles. As shown in Figure 13A,B, the cotton can be well protected by the fire-resistant HAP textile (Figure 10C, thickness ∼0.3 mm) made from the SHOUHNs when the sample is put

Figure 8. Digital images (A) and SEM micrographs (B−D) of the as-prepared highly flexible, highly ordered, and fire-resistant HAP nanoropes made from the SHOUHNs. (A) Long and highly flexible combined HAP nanoropes. (B) SEM micrographs showing the highly ordered structure on the surface of a combined HAP nanorope. (C) SEM micrographs showing the highly ordered structure at the end of a combined HAP nanorope. (D) SEM micrographs showing the highly ordered structure of a cross section which is cut from a long combined HAP nanorope using a scissors. 11489

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Figure 9. Digital images (A−D) and SEM micrographs (E, F) of the as-prepared highly flexible fire-resistant HAP textiles made from the SHOUHNs. (A) A freshly prepared wet HAP textile which is obtained by injecting the solvothermal product slurry containing ultralong HAP nanowires into absolute ethanol along defined directions. (B−D) The dried gauze-like HAP textiles in a spreading, rolled or folded state. (E, F) SEM micrographs of a gauze-like HAP textile, exhibiting the highly ordered structure of ultralong HAP nanowires in the textile.

nanostructures, and even the orientation of the ordered nanostructures of the HAP materials has been realized in this work, and the strategy reported herein will provide a bright perspective for the future applications of HAP nanostructured materials in various fields.

room temperature. The SHOUHNs and their derived ordered architectures are biocompatible, environment friendly, highly flexible, high strength, and fireproof. More importantly, these flexible fire-resistant ordered HAP architectures made from the SHOUHNs such as nanoropes and textiles may be engineered into advanced functional products for applications in various fields, for example, fireproof clothing.

CONCLUSION In summary, large-sized highly ordered HAP nanostructures are of great significance for various applications such as hard tissue repair and for understanding the formation mechanisms of bone and tooth. However, the synthesis of large-sized highly ordered HAP nanostructures remains a great challenge, especially for the preparation of large-sized highly ordered ultralong HAP nanowires because ultralong HAP nanowires are easily tangled and aggregated. In this work, we have made three main research findings: (1) the large-scale production of highly flexible ultralong HAP nanowires has been realized with a good reproducibility; (2) we have succeeded in the rapid automated production of the SHOUHNs by simply injecting the as-prepared solvothermal product slurry containing ultralong HAP nanowires into absolute ethanol or other alcohols at room temperature; and (3) using the SHOUHNs as the highly ordered building blocks, highly flexible and high-strength nanoropes, highly flexible textiles, and 3-D printed well-defined highly ordered patterns have been successfully prepared at

EXPERIMENTAL SECTION Large-Scale Production of Highly Flexible Ultralong HAP Nanowires. The large-scale production (5000 mL volume) of ultralong HAP nanowires was realized by the scaled-up calcium oleate precursor solvothermal method in the reaction system containing CaCl2, NaOH, NaH2PO4·2H2O, oleic acid, water, and methanol. In a typical experiment, 1000 mL of CaCl2 (22.000 g) aqueous solution and 1000 mL of NaOH (70.000 g) aqueous solution were separately added into a mixture of water (900 mL), methanol (400 mL), and oleic acid (700 mL) with an addition rate of 20 mL/min under a mechanical agitation (300 r min−1). Then, 1000 mL of NaH2PO4·2H2O (28.800 g) aqueous solution was added into the above solution with an addition rate of 20 mL min−1 under continuing mechanical agitation (300 r min−1). The resulting mixture was transferred into a stainless steel autoclave with a volume of 10 L, sealed, and heated to 180 °C and maintained at that temperature for 40 h under continuing mechanical stirring (100 r min−1). Then, the solvothermal product slurry containing ultralong HAP nanowires was obtained after cooling down the reaction system to room temperature. All chemicals used in samples preparation were of analytical 11490

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Figure 10. Digital images of various flexible fire-resistant ordered HAP architectures prepared using the SHOUHNs as the highly ordered building blocks at room temperature. (A) A HAP textile made from the SHOUHNs which are prepared by injecting the solvothermal product slurry containing ultralong HAP nanowires into absolute ethanol along subparallel direction. (B) A HAP textile column made from a rolled HAP textile. (C) A HAP nonwoven textile made from the SHOUHNs prepared by injecting the solvothermal product slurry into absolute ethanol along random directions. (D) A complex well-designed pattern made from the SHOUHNs prepared by injecting the solvothermal product slurry into absolute ethanol along predetermined directions. (E, F) The 3-D printed well-defined highly ordered pattern made from the SHOUHNs.

Figure 11. Mechanical properties of the flexible fire-resistant HAP nanoropes. (A) The tensile stresses and strains of the HAP nanoropes obtained by using one single nanorope and by twisting 2, 3, and 4 single nanoropes. (B) A combined HAP nanorope obtained by twisting 36 single nanoropes exhibits a high load-bearing performance by withstanding a weight of 500 g. grade and purchased from Sinopharm Chemical Reagent Co. (Shanghai, China) and used as received without further purification. The dispersed ultralong HAP nanowires were prepared by dispersing the solvothermal product slurry into absolute ethanol. The ultralong HAP nanowires were separated, then washed with ethanol and deionized water three times, respectively, and dispersed in ethanol for further use. Rapid Automated Production of the SHOUHNs at Room Temperature. We have developed a strategy for the rapid automated production of highly flexible, fire-resistant, large-sized SHOUHNs using the as-prepared solvothermal product slurry containing ultralong HAP nanowires as the raw material at room temperature. The automated preparation of the SHOUHNs was carried out by simply injecting the solvothermal product slurry containing ultralong HAP nanowires into absolute ethanol at room temperature using our homemade automated equipment using round-end needles. When the

solvothermal product slurry containing ultralong HAP nanowires is injected through a syringe into absolute ethanol, the SHOUHNs are obtained instantly. The length of the SHOUHNs can be easily controlled by injecting a certain amount of the solvothermal product slurry. The more the amount of the injected solvothermal product slurry, the longer the SHOUHNs. On the other hand, the diameter of the SHOUHNs can be easily controlled by the inner diameter of the needle used for injection, and SHOUHNs with different diameters can be obtained by using needles with different inner diameters. Furthermore, the oriented direction of the SHOUHNs can be well controlled by simply adjusting the moving direction of the injecting needle. Construction of Various Flexible Fire-Resistant Ordered HAP Architectures Using the SHOUHNs as the Building Material. The HAP nanoropes were prepared by using the SHOUHNs as the building material, and the combined nanoropes were obtained by 11491

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Figure 12. Cytocompatibility and cell morphologies on the SHOUHNs. (A, B) The viabilities of hBMSC (A) and osteoblast cells (hFOB 1.19) (B) measured by the CCK8 assay. (C, D) SEM micrographs of hBMSC cells grown on the SHOUHNs. (E, F) The optical micrograph (E) and an image obtained by a fluorescence microscope (F) of hBMSC cells grown on the SHOUHNs. The F-actins and nuclei of hBMSC cells are stained with red and blue, respectively. twisting single HAP nanoropes together. The highly flexible HAP textiles constructed with the SHOUHNs as the building material were prepared by injecting the solvothermal product slurry containing ultralong HAP nanowires into absolute ethanol through crisscross moving of the injecting needles with an inner diameter of 0.6 mm. The flexible, fire-resistant, ordered HAP textiles made from subparallel SHOUHNs were prepared by injecting the solvothermal product slurry into absolute ethanol along subparallel directions. The HAP textiles made from randomly oriented SHOUHNs were prepared by injecting the solvothermal product slurry into absolute ethanol along random directions. Furthermore, the special pattern made from the SHOUHNs was prepared by injecting the solvothermal product slurry into absolute ethanol along well-designed directions. Cytocompatibility and Cell Morphologies on SHOUHNs. Human bone mesenchymal stem cells (hBMSCs) were purchased from ScienCell Research Laboratories (San Diego, U.S.A.). Osteoblast cells (hFOB 1.19) were obtained from American Type Culture Collection (ATCC, U.S.A.). The hBMSCs were cultured in mesenchymal stem cell medium (ScienCell Research Laboratories, San Diego, U.S.A.) in an incubator at 37 °C with 5% CO2. The hFOB 1.19 cells were cultured in DMEM-F12 medium (Gibco, U.S.A.) supplemented with G418 (0.3 mg mL−1), 10% fetal bovine serum (Gibco, U.S.A.) in an incubator at 34 °C with 5% CO2. For the cell proliferation assay, the hBMSCs and hFOB 1.19 cells were respectively seeded in 96-well plates at a density of 2 × 103 cells per well. The medium in the negative control group was the corresponding medium, while the medium in the experimental group was replaced by the leaching agent by the SHOUHNs (1 mg mL−1). And the cell viability was examined daily by the CCK8 assay following the manufacturer’s instructions from days 1 to 7. All the experiments were performed triply.

The morphologies of hBMSCs on the SHOUHNs were investigated by SEM and a fluorescence microscope. The hBMSCs were seeded in 24-well plates with the SHOUHNs at a density of 5 × 103 cells per well and cultured for 3 days. For the SEM imaging, the samples were rinsed with phosphate buffered saline (PBS) and fixed with 2.5% glutaraldehyde solution for 30 min. Then, the samples were dehydrated with ethanol aqueous solutions (30, 50, 75, 95, and 100 vol %) for 10 min and in absolute ethanol twice for final dehydration. Finally, the dehydrated samples were sputter coated with gold and observed with SEM. The fluorescence images of the cells cultured on the SHOUHNs were observed with a fluorescence microscope (DMi8, Leica Microsystems). The SHOUHNs used in fluorescence imaging were treated by heating at 600 °C for 3 h to reduce the autofluorescence of the samples. Then, the F-actins and nuclei of hBMSCs were separately stained by rhodamine phalloidin (BD Biosciences, U.S.A.) and 4′,6-diamidino-2-phenylindole (DAPI) (Thermo Scientific, U.S.A.) after culturing for 2 days. Characterization. The as-prepared samples were observed with a JEOL JEM-2100F field-emission transmission electron microscope (TEM) with an accelerating voltage of 200 keV and a field-emission scanning electron microscopy (SEM, SU8220, Hitachi, Japan). X-ray powder diffraction (XRD) patterns were obtained with a Rigaku D/max 2550 V X-ray diffractometer with a high-intensity Cu Kα radiation (λ = 1.54178 Å) and a graphite monochromator. Fourier transform infrared (FTIR) spectra were obtained on a FTIR spectrometer (FTIR-7600, Lambda Scientific, Australia). Mechanical measurements were carried out with a materials testing machine (H5K-S, Hounsfield, UK) at room temperature with an elongation rate of 2 mm min−1. The samples for thermal conductivity tests were compressed into round plates with a diameter of 10 mm at a pressure of 4 MPa and pretreated 11492

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Figure 13. Fireproof experiments of the HAP textile. (A, B) The performance of the aluminum foil (A) and the HAP textile covered aluminum foil (B) on the fire flame. (C, D) Fire-resistance experiments of a conventional cotton textile (C) and a textile made from the SHOUHNs (D). (E) TG and DSC curves of the common cotton and the SHOUHNs used for the preparation of the HAP textile. at 500 °C for 4 h. Then, the thermal diffusivity of samples was measured by the laser flash method. The thermogravimetric (TG) and differential scanning calorimetry (DSC) curves were measured on a STA 409/PC simultaneous thermal analyzer (Netzsch, Germany) with a heating rate of 10 °C min−1 in flowing air.

3D printing of ordered HAP architecture (AVI) Heavy weight falls down on HAP ceramics and the HAP textile (AVI) Fire-resistance of the common cloth and HAP textile and flexibility of the HAP textile after fire treatment (AVI)

ASSOCIATED CONTENT

AUTHOR INFORMATION

S Supporting Information *

Corresponding Author

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsnano.6b07239. TEM and SEM micrographs of the as-prepared ultralong HAP nanowires; digital images and SEM micrographs of the SHOUHNs obtained by injecting the solvothermal product slurry containing ultralong HAP nanowires into different solvents; mechanical properties of the HAP nanoropes made from the SHOUHNs; the comparison between HAP nanoropes/textiles and common inorganic (nonmetal) fibers/wires (PDF) Common method of improving flexibility of copper wires; the flexibility of the HAP textile (AVI) Automated fabrication process of SHOUHNs (AVI)

*E-mail: [email protected]. ORCID

Ying-Jie Zhu: 0000-0002-5044-5046 Notes

The authors declare no competing financial interest.

ACKNOWLEDGMENTS Financial support from the National Natural Science Foundation of China (51472259), the Science and Technology Commission of Shanghai Municipality (15JC1491001), and Youth Innovation Promotion Association of Chinese Academy of Sciences (2015203) is gratefully acknowledged. 11493

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