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Bioinspired Synthesis of Homogenous Cerium Oxide Nanoparticles and Two- or Three-Dimensional Nanoparticle Arrays Using Protein Supramolecules Mitsuhiro Okuda,† Yoko Suzumoto,‡ and Ichiro Yamashita*,†,§,|| †
Advanced Technology Research Laboratories, Panasonic Corporation, 3-4 Hikaridai, Seika, Kyoto 619-0237, Japan Panasonic Excel Staff Co., Ltd., 612 Suiginya, Shimogyo, Kyoto 600-8411, Japan § Graduate School of Material Science, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, Nara 630-0192, Japan CREST, JST, CREST, Japan Science and Technology Agency, 4-1-8 Honcho, Kawaguchi, Saitama 332-0012, Japan
)
‡
ABSTRACT: We developed an environmentally friendly method for the synthesis of cerium (Ce) oxide nanoparticles (NPs) and their two- and three-dimensional array formation using the cage shaped protein apoferritin. Apoferritin was used as a biotemplate for Ce oxide NP synthesis, and the cavity served as a restricted chemical reaction space where the trivalent Ce ions were oxidized and formed a Ce oxide NP through a process similar to iron oxide formation. The obtained Ce oxide NPs were characterized as CeO2, and their size was 5.0 ( 0.7 nm. Salt bridge formation between ferritins (apoferritins each containing a NP) by multivalent Ce ions was investigated. The best conditions of salt bridge formation produced a two-dimensional array of Ce oxide NP containing ferritin with a domain size of over 500 nm which has the potential to be used as an effective catalytic NP array. Three-dimensional arrays of Ce oxide NP containing ferritin with either an octahedral or prismlike morphology were also studied.
’ INTRODUCTION Nanoscale components, such as nanoparticles (NPs), nanorods (NRs), nanowires (NWs), and nanotubes (NTs) are indispensable to realize functional nanostructures, mesoscopic architecture with nanometric precision, and macroscopic organization of nanoblocks consorted with each another. NPs have been one of the most studied nanoscale components, and their versatility has been attracting researchers’ attention. An immense surface to volume ratio and the nanometric size of NPs realize their unprecedented properties, which cannot be accomplished using bulk materials. Therefore, a variety of NP fabrication methods—physical, chemical, and biological—have been developed.13 Recently, a biological method was proposed which synthesized NPs using bio-supramolecular templates, such as cage-shaped proteins,410 spherical viruses,1113 and tubeshaped proteins.14,15 Since the biological method uses no toxic reagents and is carried out in aqueous solution under ambient conditions at room temperature, the method is essentially environmentally friendly. This method is now attracting researchers’ attention and is very much satisfying the needs of ecotechnology and sustainable society. In this paper, we synthesized CeO2 NPs using the environmentally friendly biological method and made their independent two- and three-dimensional arrays, which have the potential to be applied in catalysis devices. Ce oxide (CeO2Ce2O3 is a well-known r 2011 American Chemical Society
multifunctional material used in a wide variety of applications, from a catalyst for three-way catalytic converters to administration as a neuroprotection agent for treating oxidative injury due to its nontoxic nature.1621 The catalytic CeO2 NP applications require homogeneous CeO2 NPs with high surface to volume ratio and also highly dense arrays of independent CeO2 NPs with surrounding space, ideally crystalline arrays. To address the demands, we employed the cage-shaped protein, apoferritin, and we synthesized and arrayed CeO2 NPs. Apoferritin is a ubiquitous iron storage protein that plays a pivotal role in the achievement of iron concentration homeostasis by storing iron atoms as nanoparticulate ferric hydroxide and supplying the iron ions when necessary.22 The protein shell has an outer diameter of 12 nm and an inner diameter of 7 nm, as defined by DNA information. The iron incorporation into apoferritin in vivo is achieved by the oxidation of divalent iron ions. Many kinds of homogeneous NPs have been artificially synthesized in vitro, such as Cr2O3, CoOOH, In2O3, CdSe, CdS, ZnSe, iron sulfide, Au/Pd, Eu(O)OH, Ti(O)OH, and Fe3xCoxO4.2331 The introduction of trivalent or tetravalent ions into the apoferritin has not been well-studied. Klem et al. Received: March 9, 2011 Revised: April 13, 2011 Published: April 18, 2011 2540
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Crystal Growth & Design reported photoinduced mineralization in apoferritin cavities using high-oxidation-state ions such as trivalent Eu ions and tetravalent Ti ions.30 However, mineralization via simple oxidation of high-oxidation-state metal (trivalent and tetravalent) in apoferritin has not been successful. To make apoferritin crystals, it was usual to add Cd ions to the solution. A pair of cadmium (Cd) binding sites at the 2-fold symmetry axes on the outer surface bind ferritin supramolecules via Cd ion salt bridges, and three-dimensional crystals were easily obtained.3240 Meanwhile, the fabrication methods of twodimensional apoferritin crystals, including ours, were developed for structural analysis and device application.4144 After protein elimination, the NPs were periodically arrayed with surrounding space and have been used as electric charge nodes. Even though Cd ion salt bridges are a very powerful way to form apoferritin crystals, Cd ions are toxic and from an environmental point of view should be replaced by some nontoxic ions. Here, we report the synthesis from trivalent ions of monodispersed CeO2 NPs in the cavities of apoferritin and a simple construction method for their two- and three-dimensional independent NPs arrays with surrounding space utilizing Ce salt bridges.
’ EXPERIMENTAL SECTION CeO2 NP Introduction into the Apoferritin Cavity. The reported experiments were conducted using recombinant horse liver L-chain ferritin without the first eight amino acid residues at the N terminal (apo-Fer8). Their overproduction and purification are described elsewhere.5,6 CeO2 NPs were synthesized in a solution composed of 0.4 mg/mL apo-Fer-8 (apoferritin), 2 mM CeCl3 3 7H2O (Kanto Chemical Co.), and 100 mM HEPES-NaOH (pH 7.7) (Dojindo) as final concentrations. None of the solutions were degassed. The buffer solution, apo-Fer-8 solution, and CeCl3 solution were added to pure water in a sequential manner. The temperature was regulated at 23 C using a thermostat bath, and the solution was incubated for 20 h. Henceforth, we call CeO2 containing ferritin as Ce-Fer8. Ce-Fer8 Purification. The 5 or 10 mL reaction solution was centrifuged (10000g 10 min) to discard the light-yellow bulk precipitates. The supernatant was retrieved and further filtered with a 220 nm filter. After concentration by a centrifugal filter (Millipore, Ultrafree-0.5, 50 kDa cutoff), the Ce-Fer8 solution was purified by sizeexclusion high-performance liquid chromatography (HPLC) (Tosoh Co., SW-4000 XL column) with 50 mM Tris-HCl (pH 8.0). There was one main peak corresponding to the size of Ce-Fer8, and fractions around this peak were collected and concentrated using a membrane (Ultrafree-0.5) with milli-Q water. Finally, the obtained solution was filtered through a 220 nm filter and used for the experiments. Confirmation of CeO2 NP Synthesis inside Apoferritin and Characterization of the Cerium Oxide NPs. The CeO2 NP formation inside the apoferritin was investigated by HPLC (Tosoh Co., SW-4000 XL column). After the HPLC column was equilibrated using Tris-HCl buffer (50 mM, pH 8.0), the purified Ce-Fer8 and apoFer8 solutions were applied. The retention volumes with the flow rate of 1 mL/min were measured by 280 and 350 nm light. 280 nm light detects protein and Ce oxide NPs, but 350 nm light detects only CeO2 NPs. The CeO2 NP structure was characterized using dried Ce-Fer8 by XRD with Cu KR radiation at 50 kV and 300 mA (Rigaku Corp., RINTTTR III). 300 mL of reaction solution was centrifuged to eliminate bulk precipitation (10000g 10 min), and the supernatant was condensed to 2 mL using a centrifugal filter (amicon, centriprep 30). The condensed supernatant was centrifuged at 15000g 1 min and filtered with a 220 nm filter again. A supernatant of the Ce-Fer8 solution was then
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purified by size-exclusion chromatography (SEC, GE Health care BioSciences, Sephacryl S-300 HR columns) with 50 mM Tris-HCl (pH 8.0) (Sigma). The fraction of Ce-Fer8 was condensed and centrifuged at 45000 rpm 4 h (Beckman, 50.2Ti rotor). The pellet of Ce-Fer8 was then dried out under nitrogen flow, and the dried sample was crushed into powder. The powder was used for XRD measurement. The CeO2 NPs and crystals of Ce-Fer8 were observed by transmission electron microscopy (TEM) at 200 kV (JEOL, JEM-2200FS) with and without aurothioglucose staining and at 400 kV (Topcon, EM002B) without staining for high resolution TEM (HR-TEM) observation. The diameters of 400 Ce oxide NPs were measured from the TEM image. Three-dimensional crystals of Ce-Fer8 were observed by scanning electron microscopy (SEM, JEOL, JSM-7400FS). SEM observation was conducted using samples on a carbon-coated TEM grid at an accelerating voltage of 5 kV.
Fabrication of Two- And Three-Dimensional Crystals of Ce-Fer8. All solutions except the Ce-Fer8 solution were degassed. For
fabrication of the two-dimensional crystal, 9.4 μL of Ce-Fer8 (0.85 mg/ mL) was mixed into 4 μL of CeCl3 3 7H2O (10 mM), 2 μL of MESNaOH (500 mM, pH 6.0), and 4.6 μL of Milli-Q water. This 20 μL solution was put on a hydrophobic flat plastic plate. After 5 min, a carbon coated TEM grid was placed on the solution surface to transfer the twodimensional crystal formed at the air/water interface. The excess solution was blotted and the grid was dried. Three-dimensional crystallization of Ce-Fer8 was carried out using the batch method. First, a solution of purified 18.9 μL of Ce-Fer8 (5.28 mg/mL), 20 μL of 500 mM MES pH 6.0, and 21.1 μL of Milli-Q water was mixed in a 200 μL tube. Then, a 40 μL solution of 100 mM CeCl3 3 7H2O was added and mixed carefully by pipet so as to make the solution uniform. The final concentration was 1 mg/mL Ce-Fer8, 100 mM MES pH 6.0, and 40 mM Ce ions. The tube was sealed as airtight and stored in a temperature controlled incubator at 23 C. Ce-Fer8 crystals appeared typically within 48 h. After 1 h, the embryonic crystal was retrieved and observed by TEM. After 48 h, matured crystals were picked up on a carbon coated TEM grid and observed by SEM.
’ RESULTS AND DISCUSSION Ce ions and apoferritin (apo-Fer8) were mixed to synthesize CeO2 NPs inside apoferritin following the protocol described above. After mixing, the solution color slowly changed from transparent to light yellow. A small amount of light yellow bulk precipitation started to form at some point during the incubation time. The precipitate was supposed to be CeO2 particles (Ce2O3 is purple). The reaction solution was incubated for 20 h to make sure that the reaction was completed. After incubation, the supernatant solution was carefully retrieved and a small aliquot of the purified sample was examined by TEM with and without aurothioglucose staining. Figure 1a showed the TEM image of the stained sample. There were homogeneous nanodots surrounded by thin white rings with an approximate diameter of 12 nm. Since it was proven that aurothioglucose cannot go through the apoferritin channels and cannot stain the cavity,5,6 the white thin rings should be the protein shells and homogeneous nanodots in the center should be CeO2 NPs formed in the cavity (Ce-Fer8). The stained purified solution was observed by TEM, and the core formation ratio was calculated by dividing the number of Ce-Fer8 by the number of all Fer8 (apo-Fer8 and Ce-Fer8).5,27 The TEM image data indicate that 97% of Fer8 had formed CeO2 NPs. The total yield, the ratio of Ce-Fer8 over initial Fer-8, was about 7%. Measurement of the NP size was carried out from the unstained TEM images (Figure 1b), which showed a clear image of the NPs because the contrast of the 2541
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Figure 1. TEM images of Ce-Fer8 with (a) and without (b) aurothioglucose staining. The stained sample shows NPs at the center of the protein shells. The unstained sample shows independent NPs which can be used for size measurement.
Figure 2. Size exclusion chromatography (HPLC) of apo-Fer8 without a NP (a) and Ce-Fer8 (b). Elution was monitored by light absorbance at 280 nm (protein, broken line) and at 350 nm (CeO2, solid line). The elution times of Ce-Fer8 and apo-Fer8 without a NP were the same (9.4 min).
Figure 3. XRD patterns of Ce-Fer8 (a). High-resolution TEM images of Ce-Fer8 (b and d), and their corresponding FFT filtered images (c and e).
protein shell was too low to be imaged. The particle size was determined using 400 Ce NPs to be 5.0 ( 0.7 nm. Furthermore, we carried out size exclusion chromatography (SEC) to eliminate the possibility that the NPs were just attached to the outside of the apoferritin. We subjected Ce-Fer8 and apoFer8 to SEC monitored by 280 and 350 nm optical absorbance. Since CeO2 particles absorb UV-light below 430 nm,41 CeO2 NPs can be detected by both 280 and 350 nm, whereas apoferritin can be detectable only by 280 nm. If CeO2 NPs are attached to the outside of apoferritin, the size of apo-Fer8 with NPs must be bigger than apo-Fer8 without and the 350 nm absorption peak would show a different retention volume from apo-Fer8 without NPs. Figure 2a shows the HPLC result of apoFer8. The retention volume detected by 280 nm was 9.4 mL, and the 350 nm absorption level was negligible. Figure 2b shows the HPLC result of Ce-Fer8. The retention volumes detected by 280 and 350 nm were the same, which were also the same as that with apo-Fer8 (Figure 2a). The results clearly indicated that the Ce-Fer8 was the same size as the apo-Fer8. Therefore, it was confirmed that the CeO2 NPs were formed inside apoferritin. Combining preceding knowledge,22,32,33 the result could be interpreted as follows. The electrostatic potential difference across the apoferritin shell produced by collectively negatively charged amino acid residues on the internal surface means that positively charged Ce ions are sucked into the cavity through the hydrophilic channels. Ce ions were further condensed at the collectives of negatively charged amino acid residues which worked as nucleus centers, and the CeO2 nuclei formed. Once nuclei formed, the surface worked as catalyst, and CeO2 NPs autocatalytically formed. This process led to the selective synthesis of CeO2 NPs inside apoferritins.
The structure of the CeO2 NPs was studied by XRD and HRTEM. The XRD pattern (Figure 3a) exhibits a set of typical peaks for the CeO2 structure (JCPDS Card No. 75-0120), and peaks from trivalent Ce-based phases (Ce2O3) were not identified. Five HR-TEM images analyzed with great care, however, showed two different sets of lattice distances. Four of the five HR-TEM images showed lattice distances of 2.7 and 3.0 Å (Figure 3b). Fast Fourier transform (FFT) analysis showed that the spots and angles corresponded with {111} and {111} or {111} and {200} of CeO2 (Figure 3c: JCPDS Card No. 75-0120). The results agreed with XRD. However, one of the five images was different from others, and the FFT analysis confirmed it as Ce2O3 (Figure 3d and e: JCPDS Card No. 23-1048). These data indicated that the obtained NPs were mainly CeO2 but there was a small amount of Ce2O3. It is plausible that trivalent Ce ions were oxidized to tetravalent Ce ions due to the presence of oxygen in the reaction solution. However, the presence of the Ce2O3 NPs suggested that all trivalent Ce ions were not oxidized during the time course of the NP formation period. Ce ion oxidization might take a long time, as some Ce ions remained as trivalent ions and were introduced into the cavity and formed the Ce2O3 NPs. This might explain the existence of Ce2O3 NPs. According to previous papers, apoferritin can be crystallized by salt bridges of cadmium (Cd).4143 Some literature reported that apoferritin denatured at the waterair interface to form an unfolded polypeptide film and that intact ferritin adsorbed beneath the denatured film and underwent self-arrangement to form a two-dimensional crystal through Cd salt bridges.4143 We investigated the same type of two-dimensional Ce-Fer8 crystal formation by multivalent Ce ions. Twenty microliters of Ce-Fer8 2542
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Figure 4. TEM image of a two-dimensional Ce-Fer8 crystal (a). Higher magnification TEM image of the two-dimensional Ce-Fer8 crystal showing a hexagonal closed packing array of CeO2 NPs (b). Schematic drawing of a two-dimensional crystal of Ce-Fer8 (c) (blue, Ce-Fer8s in the first layer; red, salt bridged Ce-Fer8s in the second layer; and yellow, partially salt bridged Ce-Fer8s in the second layer). Ce-Fer8s are depicted by circles and cubes for easy comprehension.
Figure 5. SEM images of three-dimensional Ce-Fer8 crystals. Octahedral morphology (a) and prismatic morphology (b) crystals were observed after 48 h. Parts c and d show TEM images of three-dimensional Ce-Fer8 crystals after 1 h of growth.
in the buffer solution including Ce ions was prepared as described above and put on a plastic film as a droplet. After 5 min of incubation, a TEM grid was placed on the surface of the droplet, and then the grid was removed from the droplet and the excessive solution was blotted with filter paper. The grid was observed by TEM (Figure 4). A regular array of CeO2 NPs with an area larger than 500 nm2 was observed. The two-dimensional Ce-Fer8 crystal shows regularity over a wide area. The result suggested that Ce ions could make salt bridges between Ce-Fer8, and the two-dimensional crystal was formed on the denatured film at the air/water interface. The result was the same with the twodimensional crystals of Cd-bridged apoferritin, known to have hexagonal close packing corresponding to the (111) crystal face of the fcc structure.44 In some parts, the two-dimensional regular array had additional Ce-Fer8s, which were supposed to adsorb on the first crystalline monolayer of Ce-Fer8. There were two types of position for the adsorbed Ce-Fer8 against the first hexagonal array. One is at the center of three Ce-Fer8s (red circle), and the other is a little off the center position of two Ce-Fer8s (yellow circle). These positions must be decided by the first hexagonal array. The supposed adsorption position against the first hexagonal array is depicted in Figure 4c, where Ce-Fer8 is represented as a cube which has the same 432 symmetry. When a CeFer8 adsorbed to the first layer, it is most plausible that it would be moored by three pairs of Ce salt bridges which were formed between the added Ce-Fer8 and three Ce-Fer8s in the first layer (Figure 4c, red cube). The result was that the CeO2 NP was added at the center of three CeO2 NPs. The NPs indicated by red circles showed the exact predicted position. The other possibility was that the additional Ce-Fer8 was moored by only one pair of
Ce salt bridges (Figure 4c, yellow cube), because two pairs of Ce salt bridges inevitably lead to three pairs of Ce salt bridges due to geometric restriction. The added Ce-Fer8 could move around the pair of Ce salt bridges, but the movement must not be free because there were restrictions from factors such as tertial hindrance or electrostatic interaction. The position a little off center of two Ce-Fer8s might be the favorable position for the Ce-Fer8 moored by one pair of salt bridges (yellow circle). The addition of Ce-Fer8 on the first layer, which seldom happens when using Cd ions, may indicate that the Ce salt bridge is stronger than the Cd salt bridge. However, it cannot be completely excluded that the Ce-Fer8 adsorbed on the twodimensional crystal surface during the removal of redundant solution on the TEM grid. The first layer of Ce-Fer8 easily forms a two-dimensional crystal due to a denatured film at the air/water interface which contains charged amino acids. The second layer is restricted by structural limitations and the electrostatic repulsion of apoferritin itself. Therefore, it is thought that crystallization of Ce-Fer8 is regulated. Since it has already been shown that the protein shell can be selectively eliminated by heat or UV/ Ozon treatment, the obtained dispersed Ce NPs with surrounding space could be used as an ideal catalyst plate.45,46 We further studied the Ce salt bridges via three-dimensional crystal formation. Figure 5a and b shows SEM images of the typical morphology of the three-dimensional Ce-Fer8 crystals obtained. These crystals have the octahedral or prism-like morphology which is observed with ferritin crystals produced by Cd salt bridges around the two-fold axes.39 Early stage Ce-Fer8 crystals, the sizes of which were about 300 nm after 1 hour of growth incubation, were also observed by TEM (Figure 5c). Crystals showed straight lines of CeO2 NPs in three directions 2543
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Crystal Growth & Design which precisely formed angles of 60 with each other (three lines in Figure 5c), which indicated that the CeO2 NP containing ferritin crystal has a face centered cubic (fcc) structure. The structure was, again, the same with ferritin crystals formed by Cd ions. Vekilov et al. reported that, after nucleation of an apoferritin crystal, the crystal growth dominantly progresses in the Æ110æ directions on the (111) plane of the apoferritin crystal through a quasi-planar nucleus structure using supersaturation solution conditions of Cd ions.36 The prism-like crystal was supposed to be derived from the crystal growth from two-dimensional crystal growth driven by Ce salt bridge formation; that is, a twodimensional crystal worked as a starting framework, and the crystal grew dominantly in the Æ110æ directions due to the formation of Ce salt bridges. These data supported that the ferritin crystals were formed by Ce ion salt bridges and the multivalent Ce ions essentially worked in the same way as in the crystallization with Cd ions.
’ CONCLUSION In summary, CeO2 NPs were synthesized and arrayed using a biological method. CeO2 NPs with a narrow size distribution were successfully prepared using apoferritin. The formation of CeO2 NPs in the apoferritin cavities was confirmed by TEM and HPLC. HR-TEM and XRD analysis showed that the NPs mainly consisted of CeO2 whereas there was a small amount of Ce2O3. A two-dimensional array of CeO2 NPs with surrounding space, which could serve as an ideal catalytic NP array, was realized by Ce-ferritin crystallization. Ce ions worked as salt bridges, which is the same process as when using Cd ions. The method developed here is simple and can be scaled up easily using larger troughs. This method will serve for a sustainable society through an essentially environmentally friendly process for CeO2 NP synthesis and arraying. ’ AUTHOR INFORMATION Corresponding Author
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[email protected]. Telephone: þ81774-98-2516. Fax: þ81-774-98-2515.
’ ACKNOWLEDGMENT The authors thank Dr. K. Iwahori (CREST) for valuable discussions and Dr. Y. Zenitani (Panasonic) for the XRD measurements. This work was partially supported by the Leading Project of the Ministry of Education, Culture, Sports, Science and Technology, Japan, and Human Frontier Science Program (RGP61/2007). English proofreading and modification by Dr. Sarah Ward Jones is also acknowledged. ’ REFERENCES (1) Sun, S. H.; Murray, C. B.; Weller, D.; Folks, L.; Moser, A. Science 2000, 287, 1989. (2) Zeng, H.; Li, J.; Liu, J. P.; Wang, Z. L.; Sun, S. H. Nature 2002, 420, 395. (3) Schnablegger, H.; Mann, S. Nature 1999, 402, 393. (4) Douglas, T.; Dickson, D. P. E.; Betteridge, S.; Charnock, J.; Garner, C. D.; Mann, S. Science 1995, 269, 54. (5) Okuda, M.; Iwahori, K.; Yamashita, I.; Yoshimura, H. Biotechnol. Bioeng. 2003, 84, 187. (6) Iwahori, K.; Yoshizawa, K.; Muraoka, M.; Yamashita, I. Inorg. Chem. 2005, 44, 6393.
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