Amorphous Calcium Carbonate Stabilized by a Flexible Biomimetic

Article pubs.acs.org/crystal

Amorphous Calcium Carbonate Stabilized by a Flexible Biomimetic Polymer Inspired by Marine Mussels Sha-Sha Wang and An-Wu Xu* Division of Nanomaterials and Chemistry, Hefei National Laboratory for Physical Sciences at Microscale, Department of Chemistry, University of Science and Technology of China, Hefei 230026, China S Supporting Information *

ABSTRACT: Organisms make use of amorphous materials as a certain precursor to form insoluble complex biominerals in the presence of various organic matrices. In this article, we demonstrate that amorphous calcium carbonate (ACC) nanoparticles can be highly stabilized by a polymerized dopamine (DA), a biomimetic molecule inspired by adhesive proteins in mussels. The cross-linking polydopamine (PDA, a mussel mimicking polymer) flexible chains are adhesively associated with the ACC particles to form ACC@PDA core− shell spheres. We are able to modulate the thickness of PDA shells in the range of a few to several tens of nanometers by adjusting the additive DA amount. The thickness of this mussel mimicking PDA shell significantly influences the stability of ACC nanoparticles; the thicker the PDA shell is, the more stable the ACC core is. The obtained ACC−PDA hybrid particles have high stability, partly because the complexing interaction of Ca2+ ions with PDA and encapsulating PDA networks inhibit ACC dissolution and retard subsequent Ostwald ripening, and partly because the PDA coating builds isolated confinement spaces for ACC that prevents contacting and merging of ACC particles which further restrains possible solid-phase transformation. Notably, the protecting effects of PDA endow the obtained ACC−PDA composite powder with enough stability to exist for at least one year in the solid state. Our resulting hybrid ACC−PDA nanoparticles with tunable size and high stability could serve as a model system for multistep biomineralization, limited space crystallization, and potential biomedical applications as well.

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INTRODUCTION In nature, living organisms make use of functional minerals to fabricate their hard parts with exquisite morphologies and hierarchical structures.1 Calcium carbonate (CaCO3) is one of the most abundant biominerals for a variety of functions, including sea urchin teeth,2 photosensory organs in brittlestars,3 piranha otoliths,4 and so on. These organic−inorganic hybrid materials with exceptional properties far beyond those artificial materials with the same components are attributed to their crystal alignments and hierarchical microstructures.5 Consequently, the crystallization strategies during the biomineralization process have been extensively investigated to understand the growth pathway toward desired architectures. In recent years, an increasing number of reports have revealed that as a transient precursor, amorphous calcium carbonate (ACC) plays an important role in the formation of more stable CaCO3 polymorphs (e.g., vaterite, aragonite, and calcite) with sophisticated shapes both in bio- or biomimetic mineralization.6 The instability and relatively high solubility of ACC allow it to transform into biominerals with complex morphologies as amorphous precursors could be molded into any shape while avoiding a high ionic strength and the related osmotic pressure.7 For instance, ACC is widely used by crustaceans for their cyclic molt of the exoskeleton.8 During this process, ACC is biologically stabilized by magnesium ions © 2013 American Chemical Society

and initially deposits in the cuticle, then subsequently transforms into calcite. The L-aspartic acid-rich proteins were found to switch on the transformation of the magnesiumstabilized amorphous phase to the newly calcified tissue. As a mostly utilized depot for temporarily storing calcium and carbonate species, ACC must be prevented from the spontaneous crystallization unless the hard parts of organisms need wound-healing. In other words, the stabilization of the intrinsically unstable ACC is of great significance as well as a great challenge for biomimetic researchers. Generally, ACC is a thermodynamically unstable phase and transforms easily into crystalline CaCO3 polymorphs without stabilizing additives.9 Aizenberg et al. found that macromolecules extracted from ACC-comprising ascidian skeletons10 and sponge spicules11 are glycoproteins rich in glutamic acid and hydroxyamino acid, which could restrain the phase transformation of ACC in vitro. Moreover, by mimicking the functional groups of biomacromolecules, synthetic polymers such as poly(aspartic acid),12 poly(acrylic acid),13 and poly(propyleneimine) dendrimers14 were used to modify the ACC particles with relatively high stability. Besides this, phytic acid,15 Received: November 30, 2012 Revised: March 21, 2013 Published: April 4, 2013 1937

dx.doi.org/10.1021/cg301759t | Cryst. Growth Des. 2013, 13, 1937−1942

Crystal Growth & Design

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magnesium ions,16 and ethanol solvent17 were also proven to be able to retard the crystallization of ACC. Recently, several confined systems were designed elaborately to investigate the influence of such localized volumes on crystallization.18,22 These studies demonstrate that the restricted environment has a significant effect on the stabilization of ACC. Herein, we describe a facile and effective approach to synthesize stable ACC nanoparticles via a polymerization of dopamine (DA). Dopamine, a biomimetic molecule inspired by mussel adhesive proteins that contains catechol and amine functional groups, can self-polymerize in an alkaline environment, and the polydopamine (PDA) layers spontaneously deposit onto a variety of surfaces under a wet condition (Scheme 1).19 ACC-containing components with intimately

and high stability could serve as an ideal model to study the kinetic transformation stages of biomineralization. Furthermore, as PDA is nontoxic and biocompatible, so potential biomedical applications could be anticipated as well. In this work, we prepared ACC−PDA nanocomposites at room temperature by using a CaCl2 aqueous solution with dimethyl carbonate (DMC) and different amounts of DA. The reaction started when adding a certain amount of NaOH into the reaction solution under stirring. DA molecules polymerized instantly as the colorless solution became brown. At the same time, the hydrolysis of DMC took place and released carbonate ions homogeneously in the reaction solution. After being stirred for 1.5 min, the transparent solution turned turbid, indicating the formation of ACC. The reaction temperature plays a crucial role in the generation of ACC: a higher temperature will lead to smaller ACC particles and vice versa. When the reaction temperature is lower than 10 °C, ACC particles cannot form.

Scheme 1. Proposed Formation Processes of PDA by the Spontaneous Oxidative Polymerization of DA Molecules under an Alkaline Condition

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EXPERIMENTAL SECTION

Preparation. All chemicals, calcium chloride (CaCl2), dimethyl carbonate (DMC) and sodium hydroxide (NaOH) (Shanghai Chemical Reagents Co.), dopamine hydrochloride (DA) (SigmaAldrich) were analytical grade and were used without further purification. All glassware was cleaned and sonicated in ethanol for 5 min and after rinsed with distilled water and further soaked with a H2O-HNO3 (65%)-H2O2 (1:1:1,V/V/V) solution, then rinsed with deionized water, and finally dried in air with acetone. In a typical run, 90 mg of DMC and different amounts of DA (5−70 mg) were dissolved into 16 mL of CaCl2 (12.5 mM) aqueous solution

associated organic matrix exist widely in nature; thus our asprepared hybrid ACC−PDA nanoparticles with tunable size

Figure 1. (a) XRD pattern of the sample obtained in the presence of DA (35 mg) after reaction for 2.5 min, showing no diffraction of crystalline CaCO3. (b) FTIR spectra of free DA molecules, reference PDA particles polymerized for 12 h, and ACC−PDA particles in the presence of DA (35 mg) after 2.5 min growth, respectively. (c) TEM micrograph of pure ACC spheres prepared in the absence of DA after 2.5 min reaction. (d) TEM micrograph of ACC−PDA composites prepared in the presence of DA (35 mg) after 2.5 min growth. 1938



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at room temperature. The reaction was started by adding 4 mL of NaOH (0.5 M) aqueous solution to the former solution under stirring. After 2.5 min the resulting precipitates were extracted from the reaction solution by centrifugation and washed thoroughly with acetone and then dried at 40 °C in an oven. Reference PDA particles were obtained from a polymerization solution prepared as above without adding CaCl2 and DMC, which was stirred at room temperature overnight (12 h). Particles were collected by centrifugation and washed thoroughly with deionized water and then dried at 40 °C in an oven. Selective dissolution of the ACC cores from ACC−PDA hybrid nanoparticles was performed by adding the dried ACC−PDA sample in 0.01 M hydrochloric acid and standing for 2 days. The remaining precipitate was washed thoroughly with water and dried at 40 °C in an oven. Characterization. Scanning electron microscopic (SEM) images were obtained with a JEOL JSM-6700F operated at 15 kV. The X-ray powder diffraction (XRD) patterns of the samples were obtained on a Rigaku X-ray diffractometer with CuKα radiation (λ = 1.54178 Å), and the operation voltage and current were maintained at 30 kV and 140 mA, respectively. Fourier transform infrared spectroscopy (FTIR) spectra were recorded on a MAGNA-IR 750 FTIR spectrometer. Transmission electron microscopic (TEM) images, selected area electron diffraction (SAED) patterns, and micro-EDX analysis were performed on a JEOL-2010 microscope with an accelerating voltage of 200 kV. Sample grids were prepared by sonicating powdered samples in ethanol for 20 min and evaporating one drop of the suspension onto a carbon-coated, holey film supported on a copper grid for TEM measurements.

a network of particle junctions. Compared to the pure ACC spheres with a smooth surface grown in the absence of DA (Figure 1c), the surface of ACC-PDA spheres is rough due to flexible PDA coating; moreover, the size of ACC−PDA nanoparticles decreases by 37%. There is an obvious trend that when other conditions are kept constant, the more DA molecules are added, the smaller ACC nanoparticles are observed (Figures S2 and 3). This is because PDA flexible chains are not only incorporated into ACC primary nanoparticles but also coated on the ACC surface, which stabilize ACC and further prevent ACC nanoparticles from growing bigger. Furthermore, PDA chains should also affect the surface tension of the nucleating nanoparticles, further demonstrating the relationship between ACC particle size and the PDA concentration in the growth solution. It is worth noting that severe aggregation of spherical grains is observed for ACC− PDA samples due to the strong adhesion from PDA flexible chains. Overall, we demonstrate the as-prepared ACC-PDA hybrid nanoparticles are amorphous in nature. The microstructures and compositions of obtained ACCPDA nanospheres were further characterized by highmagnification transmission electron microscope (TEM) and energy dispersive X-ray (EDX) measurements. From Figure 2,

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RESULTS AND DISCUSSION The precipitate collected after 2.5 min reaction was identified by X-ray diffraction (XRD) analysis and Fourier transform infrared spectroscopy (FTIR). Figure 1a shows the XRD pattern of the sample obtained in the presence of 35 mg of DA, indicating that the as-synthesized product is amorphous phase. The FTIR spectrum of this sample shows the characteristic absorption of ACC (Figure 1b). Absorption bands appearing at 1491/1410 cm−1 (asymmetric stretching), 1072 cm−1 (symmetric stretching), and 866 cm−1 (out-of-plane bending) can be assigned to the vibrations of the carbonate group in ACC. The split peak at 1410/1491 cm−1 identifies the short-range atomic structure in ACC, which provides the transformation sites for further crystallization.20 The broad and weak absorption at about 710 cm−1 proves the absence of crystalline polymorphs (calcite or aragonite). FTIR spectra of free DA molecules and reference PDA particles (see the preparation method in Experimental Section) are also displayed in Figure 1b. It can be observed that the spectrum of DA molecules shows many narrow peaks in the fingerprint region, which have disappeared in the spectrum of PDA because the polymerization restricts bending and stretching vibration of free DA molecules. The peaks at 1615 cm−1 and 3420 cm−1 appearing in the IR spectrum of PDA are attributed to the aromatic rings and catechol groups.21 The IR spectrum of the obtained ACC− PDA samples shows the characteristic absorption peak at 1615 cm−1, indicating the existence of PDA in the ACC−PDA composite particles (Figures 1b and S1b−f in the Supporting Information (SI)). From Figure S1 it can be clearly seen that the absorption intensity at 1615 cm−1 increases with an increase in the content of PDA component in the ACC−PDA composites. A typical transmission electron microscopy (TEM) image of the as-synthesized ACC-PDA hybrid nanoparticles produced in the presence of 35 mg of DA is shown in Figure 1d. Spherical particles with an average diameter of 220 nm are observed, and the particles adhere to each other to form

Figure 2. TEM images of the ACC-PDA core−shell spheres obtained in the presence of (a) 5 mg and (b) 35 mg of DA after 2.5 min reaction. The average thickness of the shells is determined to be 2.7 and 12.6 nm, respectively.

it can be clearly seen that an obvious contrast between the pale shell and the dark core indicates the formation of a core (ACC)-shell (PDA) structure of the hybrid particles. When adding 5 mg of DA molecules into solution, the resulting ACC−PDA hybrid nanospheres display a thin shell with a thickness of about 2.7 nm (Figure 2a). Some voids can be directly visualized in the inner region of the spheres when the electron beam passed through, which is a trait for CaCO3.22 Figure 2b reveals that a measured thickness of the shell is about 12.6 nm when 35 mg of DA was introduced in solution. It is found that the thickness of PDA shell increases with an increase in the amount of additive DA molecules, and this can be easily explained by more DA molecules polymerization and wrapping ACC particles. To shed light on detail compositions of the 1939



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Figure 3. TEM images of (a) temporarily PDA-stabilized ACC nanoparticles with 10 mg of DA aging in mother solution for 5 h; (b) the obtained hollow PDA skins by treating the precipitates (in the presence of 60 mg of DA after 2.5 min reaction) with dilute hydrochloric acid. (c) EDX spectrum taken from the white circle area in (b) demonstrating the absence of the Ca element.

hydrochloric acid); therefore the faster diffusion rate of Ca2+ and CO32− ions passing through PDA shells leads to the formation of the bigger PDA capsules and some broken shells. It is commonly accepted that pure ACC is thermodynamically unstable so that crystalline products will spontaneously nucleate and grow from it. Without addition of DA molecules, ACC was detected to transform into calcite within 2 h. PDA coating on ACC particles essentially results in the stabilization of amorphous particles and remarkable inhibition of ACC transformation into thermodynamically favored phases. The relative delay of crystallization leads to a kinetically driven crystal growth route, which is a rather different mechanism than a single-step pathway. According to the Ostwald step rule, crystallization is often a sequential phase-transformation process in which the least stable and least dense phase is formed first and transforms into the denser phase later.23 In our case, ACC does not recrystallize to form the most stable calcite phase directly but through a less stable vaterite phase. Figure 4a reveals that vaterite crystals nucleate from the precipitated ACC−PDA colloids (25 mg of DA) aging in mother solution for 1 day. The corresponding XRD (Figure 4c) and SAED pattern (the inset in Figure 4a) recorded from the [001] zone axis verifies the vaterite phase. The remaining networks of hollow PDA spheres associated with the large vaterite crystals indicate that the crystalline phase grew at the expense of ACC precursor particles (dissolution of ACC) by diffusion through the PDA shells. After aging for 3 days, calcite with characteristic rhombohedral morphology appeared and the vaterite hexagonal crystals disappeared (Figure 4b). The whole phase transformation walks along an amorphous precursor−metastable intermediate−most stable product process, which clearly follows the kinetically controlled multistage crystallization. The XRD results of ACC−PDA precipitates with 25 mg of DA aging in mother solution for different time periods also support the above conclusion (Figure 4c). After aging for 7 h, ACC was still the only phase, while inconspicuous crystalline peaks detected after 14 h indicate the onset of crystallization. With aging time elongated, diffraction peaks of vaterite phase appeared within 1 day and weak calcite signals were also found. With proceeding crystal growth, the intensity of the calcite peaks increased and no other crystalline diffraction peaks were observed after 3 days. As such, multistep crystallization via amorphous precursors, metastable vaterite intermediates, and final most stable calcite was completed (Figure 4c). On the basis of the above results, we propose a rational mechanism to explain the formation and stabilization of ACC− PDA hybrid nanoparticles. As illustrated in Scheme 2, rapid

ACC−PDA core−shell hybrid particles, EDX analyses of the inner core and the outer shell marked by white circles in Figure 2b were displayed in Figure S4, panels a and b, respectively. It is found that Ca signals fall sharply and the O/Ca atomic ratio increases significantly when the X-ray beam scanned from the inner core to the shell of the spheres, further confirming the core is ACC and the shell is PDA. TEM and EDX results demonstrate the formation of the core−shell structure of ACC−PDA hybrid nanospheres. We are able to modulate the thickness of PDA shells in the range of a few to several tens of nanometers by adjusting the additive DA amount (Figure S5). The thickness of this mussel mimicking PDA shell significantly influences the stability of ACC nanoparticles; the thicker the PDA shell is, the more stable the ACC core is. The ACC−PDA nanoparticles can be stabilized temporarily because of the PDA protection. PDA skins with different thickness exhibit varying degrees of porosity and therefore inhibit the dissolution of ACC to different extents. PDAstabilized ACC particles kept in mother solution for 5 h were separated and observed using TEM. After maintaining the original core−shell structure for a certain time, some amorphous cores were dissolved, and the hollow PDA capsules were left. Figure 3a shows a typical TEM image of a temporary coexistence of ACC−PDA nanoparticles and PDA hollow spheres in the system. The former has an average diameter of 265 nm and the measured thickness of the shell is around 3.5 nm. With gradual dissolution of the ACC core, the flexible PDA shells shrunk inward due to the loss of support with ACC dissolving. Finally Ca2+ and CO32− species passed through the polymer shells and dissolved into the solution for subsequent crystallization to more stable crystalline phases. The ultimate PDA hollow spheres remained the original spherical morphology of ACC−PDA composites with an average diameter down to 170 nm and a thickness up to 30 nm. Excellent shrinkage performance confirms the remarkable flexibility of polymer chains. On the other hand, we used dilute hydrochloric acid to selectively dissolve the ACC core, leaving hollow PDA skins as revealed in Figure 3b. The estimated thickness of the PDA shells is about 20 nm, which is much thinner than the one in Figure 3a, and the average diameter of the PDA capsules is bigger than that in Figure 3a. Some of the PDA remnants were broken during acid etching and collapsed into small pieces. The absence of Ca signal shown in EDX spectrum (Figure 3c) confirms that ACC was totally removed by dilute hydrochloric acid etching from ACC−PDA hybrid nanoparticles. With dilute hydrochloric acid etching, the dissolution rate of ACC cores is much faster than aging in mother solution (without dilute 1940



Article

polymerized DA is ready to attach to all kinds of surfaces (Scheme 2, stage 2). At the same time, hydrolysis of DMC catalyzed by NaOH happens and releases carbon dioxide homogeneously in the solution to provide a carbonate source for ACC formation. After being stirred for 1.5 min, the transparent solution becomes turbid, indicating the nucleation of ACC. With stirring for another minute, the size and morphology of the precipitate particles tend to be stable (Scheme 2, stage 3). According to previous work,24 Ca2+ ions have a close affinity to the catechol groups, so we anticipate that a strong adhesive interaction between PDA and ACC takes place during the whole mineralization process, from the prenucleation stage to the final stage. As a result, adhesive PDA networks not only encapsulate the ACC nanoparticles outside but also stay inside, which stabilize the ACC phase, as illustrated in stage 4. Two modes have been proposed for ACC transformation into crystalline CaCO3: dissolution−recrystallization and solidstate conversion.25 The resulting ACC−PDA hybrid particles have high stability, partly because the complexing interaction of Ca2+ ions with PDA and encapsulating PDA networks inhibit ACC dissolution and retard subsequent Ostwald ripening and partly because the PDA coating builds isolated confinement spaces for ACC that prevent contacting and merging of ACC particles which further restrains possible solid-phase transformation.22 Notably, the protecting effects of PDA endow the obtained ACC−PDA composite powder with enough stability to exist for at least one year in the solid state (Figure S6).

Figure 4. (a) TEM image of crystalline vaterite grown from PDAstabilized ACC particle networks after 1 day aging in mother solution. Inset is the corresponding SAED pattern taken from vaterite. (b) TEM image of rhombohedral calcite crystals after 3 days aging in mother solution. (c) XRD patterns of precipitates (25 mg of DA) isolated from mother solution after different time intervals. The label “c” represents the diffraction peaks from calcite (JCPDS card no. 471743), and the label “v” points to the diffraction peaks from vaterite (JCPDS card no. 33-0268).

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CONCLUSIONS Generation of amorphous precursors with a matrix composed of macromolecules or lipid membranes is a common strategy employed by organisms to form complex biominerals. Take sea urchin as an example: ACC-containing vesicles are delivered to the crystal deposition sites and transform into calcific larval spicules.26 In the present work, similar ACC-containing capsules with a biomimetic matrix have been successfully synthesized using a mussel-mimicking polymer with a strong adhesive property. The inherent unstable amorphous phase can exist in the solid state for at least one year, displaying superior persistence and stability. We anticipate that the encapsulating ACC precursors could provide fundamental understandings of multistep transformation, confined environment crystallization in biomineralization process, and so on. The obtained biocompatible ACC−PDA hybrid nanoparticles with effective permeability and nontoxicity are also expected to fabricate novel inorganic−organic hybrid materials applied in drug delivery and filters. Further study of detailed description of its confined crystallization and potential applications will be provided in a forthcoming publication.

Scheme 2. Schematic Illustration of the Formation Procedures and Stabilization of ACC−PDA Core−Shell Hybrid Spheres

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ASSOCIATED CONTENT

S Supporting Information *

IR spectra, SEM images, TEM images and SAED, EDS spectra, photographs and XRD pattern. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

mixing of NaOH solution and CaCl2 solution containing DA and DMC molecules affords an alkaline reaction environment. Under vigorous stirring, the self-polymerization of DA takes place immediately as the solution color turns to brown and

*E-mail: [email protected]. Notes

The authors declare no competing financial interest. 1941



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ACKNOWLEDGMENTS Support from the National Basic Research Program of China (2010CB934700, 2011CB933700) and the National Natural Science Foundation of China (21271165).

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Amorphous Calcium Carbonate Stabilized by a Flexible Biomimetic

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