Titania Hybrid Nanoparticles through

28 Jul 2014 - In this study, a facile approach is proposed to prepare dopamine/titania hybrid nanoparticles (DTHNPs), which are synthesized via direct...
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Preparation of Dopamine/Titania Hybrid Nanoparticles through Biomimetic Mineralization and Titanium(IV)−Catecholate Coordination for Enzyme Immobilization Chen Yang,† Hong Wu,†,‡,∥ Jiafu Shi,§,‡ Xiaoli Wang,† Jingjing Xie,† and Zhongyi Jiang*,†,‡,∥ †

Key Laboratory for Green Chemical Technology of Ministry of Education, School of Chemical Engineering and Technology, Tianjin University, Tianjin 300072, China ‡ Collaborative Innovation Center of Chemical Science and Engineering (Tianjin), Tianjin 300072, China § School of Environment Science and Engineering, Tianjin University, Tianjin 300072, China ∥ National Key Laboratory of Biochemical Engineering, Institute of Process Engineering, Chinese Academy of Sciences, Beijing 100190, China S Supporting Information *

ABSTRACT: In this study, a facile approach is proposed to prepare dopamine/titania hybrid nanoparticles (DTHNPs), which are synthesized via directly blending titanium(IV) bis(ammonium lactato) dihydroxide (Ti-BALDH) and dopamine aqueous solution. The amino group in dopamine is mainly in charge of inducing the hydrolysis and condensation of titanium precursor to form titania, and the catechol group in dopamine acts as an organic ligand to form titanium(IV)−catecholate coordination. These DTHNPs were characterized by tranmission electron miscroscopy (TEM), scanning electron microscopy (SEM), X-ray diffraction (XRD), and X-ray photoelectron spectroscopy (XPS). The morphology of DTHNPs is changed from slightly cottonshaped aggregates to monodisperse nanoparticles with the increase of dopamine concentration. As a model enzyme, catalase (CAT) is entrapped in the DTHNPs during the nanoparticle preparation process. Surprisingly, the entrapment efficiency of CAT can be high up to nearly 100%, and no enzyme leakage could be detected. Moreover, immobilized CAT possesses 90% the catalytic activity of free enzyme.

1. INTRODUCTION

Compared with biomacromolecule inducers, small molecule inducers sometimes are more convenient for the large scale biomimetic production of titania. Spermidine and spermine, the first reported small molecule inducers, have demonstrated that at least three amine functionalities were required for rapid reaction.12 Similarly, Jiang and co-workers tried different kinds of basic amino acids to induce mineralization.15 However, the hydrolysis and condensation of Ti-BALDH only occurred in the presence of arginine, possessing a high pI value and four amino functionalities, which was in good agreement with previous studies. The dopamine molecule with a catechol group shows its capability to adhere versatile substances even in the most inhospitable regions (under very harsh and wet conditions).16,17 Meanwhile, the catechol group has a high affinity to plenty of metal ions through coordination. The coordination of organic ligands with specific metal species plays a significant role in a broad range of biological functions because of their various properties, which include stimuli responsiveness endowed by the dynamic nature of molecular coordination bonds, and the combination of physical and chemical properties from both inorganic and organic materials.18 For catechol ligands, growing evidence supports that metal-catechol

Nature possesses an exceptional ability to assemble inorganic matters into hierarchical minerals through the mediation of specific biomolecules. This process is called biomineralization, which is triggered at near neutral pH in aqueous solution and room temperature. Biomineralization is ubiquitous in living organisms, such as skeletons, shells, teeth, etc.1 It is amazing to witness that a high level of temporal and spatial control can be realized in the biomineralization process.2And to the best of our knowledge, most natural biominerals are composed of silica or calcium salts. Recently, inspired by silica-based biomineralization processes, the biomimetic strategy has been extended to the preparation of other oxides, such as titania, zirconia, and gallium oxide.3,4 Compared with silica, titania has remarkable antimicrobial properties, superior mechanical strength, and pH corrosion resistance.5 In 2003, Morse and co-workers first used silicatein to fabricate titania materials.6 Since then, researchers have utilized proteins and peptides (lysozyme, viral capsids, (leucine-lysine)8-PEG70),7−10 polyamines (poly(2-(dimethylamino) ethyl methacrylate)),11 or other small molecules (just arginine, spermidine, and spermine)12,13 to induce the hydrolysis and condensation of titanium precursor to form amorphous/nanocrystalline titania. For efficient mediation of biomineralization, these biomolecule inducers usually contain a nucleophilic group, such as −OH and a hydrogen-bonding acceptor group, such as primary or substituted amine amino groups.14 © 2014 American Chemical Society

Received: Revised: Accepted: Published: 12665

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min−1 measured the circular dichroism (CD) spectra of CAT, dopamine, and the mixture of CAT and dopamine at 25 °C. 2.4. Assay of Immobilized Enzyme. 2.4.1. Entrapment efficiency. The amount of immobilized CAT was measured according to Bradford’s method.19 Specifically, the absorbance at 595 nm was measured after mixing Coomassie Brilliant Blue reagent with supernatant solution from centrifugation and washing. The entrapment efficiency was acquired according to eq 1:

coordination has substantial contribution to the formation process of biological materials including adhesion, tenacity, and intensity. In theory, the hydroxyl and amino group in the dopamine molecule will endow it the capacity to induce the formation of titania; however, rare reports can be found relevant to this issue.14 Herein, dopamine was designed as an inducer for the mineralization of titanium. Meanwhile, dopamine coordinates with titanium(IV), which in turn facilitates the biomimetic mineralization process. The morphology, crystallinity, and surface properties of the dopamine/titania hybrid nanoparticles (DTHNPs) were characterized. A one-pot precipitation procedure was further used to entrap catalase (CAT) to explore the performance of DTHNPs as enzyme supporters. The catalytic activity and stabilities of the entrapped CAT and free CAT were further studied.

entrapment efficiency (%) =

m − (C1V1 + C2V2) × 100% m (1)

where m (mg) represented the initial weight of CAT; C1 (mg mL−1), V1 (mL) and C2 (mg mL−1), V2 (mL) stood for the concentration and volume of the reactor supernatant and the washing solution, respectively. 2.4.2. Determination of CAT activity. The free or entrapped enzyme activity was determined by measuring the decrease concentration of H2O2 absorbance at 240 nm using UV−vis (Hitachi U-3010) spectrophotometer. The H2O2 reaction solution (19.6 mM) was prepared in the Tris-HCl buffer solution (50 mM, pH 7.0). A constant amount of the DTHNPs with 0.05 mg immobilized CAT were added into 20 mL reaction solution followed by stirring 3 min. A certain amount of DTHNPs with 0.05 mg bound CAT were added into 20 mL reaction solution at 25 °C followed by stirring 3 min, and filtered the solution to remove DTHNPs before absorbance measurement. By comparison, the same amount (0.05 mg) of free enzyme was used in the reaction system. The relative activity (%) was calculated according to eq 2:

2. EXPERIMENTAL SECTION 2.1. Materials. Catalase (hydrogen peroxide oxidoreductase; 1178 U; 250 kDa; EC.1.11.1.6), titanium(IV) bis(ammonium lactato) dihydroxide (Ti-BALDH, 50 wt % aqueous solution), and tris(hydroxymethyl) amiomethane (Tris) were obtained from Sigma Chemical Company. Dopamine hydrochloride was purchased from Yuancheng Technology Development (Wuhan, China). The water used in all experiments was purified by a three-stage Millipore MilliQ Plus system with a resistivity higher than 18.2 MΩ cm. All the reagents were of analytical grade and used without further purification. 2.2. Methods. 2.2.1. Preparation of DTHNPs. In a typical titania precipitation, dopamine solution (final concentration of 5 mg mL−1, dispersed in deionized water) was mixed with the Ti-BALDH precursor solution (final concentration of 50 mM). After adding Ti-BALDH to dopamine solution, the solution instantly became orange and turbid within a few seconds. The mixture was agitated for 3 min at room temperature. The resultant composites were removed by centrifugation for 4500 r min−1 and then washed three times with deionized water. 2.2.2. Entrapment of CAT in DTHNPs. CAT was dispersed into a Tris-HCl buffer (50 mM, pH 7). Then, dopamine was added to CAT solution. The precipitates reaction was initiated by adding Ti-BALDH solution. The mixture consisted of dopamine (final concentration of 5 mg mL−1), Ti-BALDH (final concentration of 50 mM), and CAT (final concentration of 1 mg mL−1). In control experiments, phosphate buffers with various concentrations replaced the Tris-HCl buffer at pH 7. 2.3. Characterizations. The morphology of the DTHNPs was examined by scanning electron microscopy (SEM, Philips XL30 ESEM) with an accelerating voltage of 20 kV and transmission electron microscopy (TEM, JEM-100CX II). The element analysis was observed by energy-dispersive spectroscopy (EDS) attached to the SEM. The crystallinity of the DTHNPs was acquired by SAED attached to the TEM. The crystallite size of the DTHNPs was measured by the X-ray powder diffraction (XRD) (Philips X_Pertpro diffractometer) using Co−Kα radiation with an accelerating voltage of 40 kV and current of 40 mA. The X-ray photoelectron spectroscopy (XPS) was adopted to characterize the surface properties of the DTHNPs by PerkinElmer PHI 1600 ESCA system with a monochromatic Mg−Kα resource and a charge neutralizer. The Perkin−Elmer Pyris analyzer was used to collect the thermogravimetric analysis (TGA) data. The Jasco J-810 spectropolarimeter (Tokyo, Japan) with a scan rate of 50 nm

relative activity (%) immobilized enzyme activity = × 100% free enzyme activity

(2)

2.4.3. Determination of Kinetic Parameters. The Michaelis−Menten constant (Km) and the maximum reaction rate (Vmax) of the free or immobilized CAT were confirmed by using different concentrations H2O2 reaction solution ranging from 2 to 45 mM. The same amount (0.05 mg) of free or immobilized CAT was introduced to the reaction system followed by stirring 1 min. Km and Vmax were acquired from the slope and intercept of the curve according Lineweaver−Burk plots as eq 3: K 1 1 1 = m + V Vmax [S] Vmax

(3)

where V (mM min−1) and [S] (mM) were the initial reaction rate and substrate concentration, respectively. Vmax (mM min−1) was the maximum reaction rate under infinite initial substrate concentration. 2.4.4. Stability. For pH stability, the free and immobilized enzyme activity were measured under various pH values in the buffers ranging from 4.0 to 9.0 (Tris-HCl buffer pH 9.0−7.0; PBS buffer pH 6.0; sodium acetate buffer pH 5.0−4.0;) at 25 °C for 3 h. When exploring the temperature stability, the free or immobilized enzyme was incubated under different temperature range from 30 to 70 °C in pH 7.0 Tris-HCl buffer for 3 h. The relative activity (%) was calculated at each specific pH (or temperature) according to eq 4: 12666

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Figure 1. One structure characterization of DTHNPs: (a) SEM image (bar 1 μm), (b) TEM image (bar 0.2 μm), (c) EDS spectra of DTHNPs, (d) HRTEM (bar 5 nm), (e) XRD images of DTHNPs without calcination.

defined as the ratio of the enzyme activity in each reaction cycle to enzyme activity in the first cycle according to eq 5:

relative activity (%) enzyme activity at the specific condition = × 100% enzyme activity at 30 °C, pH 7.0

recycling activity (%) enzyme activity in the n th cycle = × 100% enzyme activity in the 1st cycle

(4)

2.4.5. Recycling Stability and Storage Stability. The DTHNPs containing CAT were collected after each reaction batch (20 °C, 19.58 mM H2O2, reaction time 3 min), and the same amount of reaction solution was added to fulfill the next reaction cycle. The recycling efficiency of entrapped CAT was

(5)

The free and entrapped CATs were stored at 4 °C in the Tris-HCl buffer for a certain period of time. The storage stability was evaluated by comparing the enzyme activity after storage to its highest activity according to eq 6: 12667

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Figure 2. (a) XPS spectra of DTHNPs. High-resolution spectra (b) C 1s, (c) N 1s, (d) O 1s, and (e) Ti 2p XPS spectra of DTHNPs.

storage activity (%) enzyme activity after storage = × 100% the highest enzyme activity

The images indicated the DTHNPs comprised of interconnected polyhedra with sizes on the range of 30−80 nm. Similar structures were observed in silica nanoparticles induced by polydopamine.23 The size was smaller than those formed with spermidine12 or arginine15 at neutral pH (an average size were 1000 nm, 150 nm, respectively). Energy dispersive spectroscopy (EDS) (Figure 1c) indicated that the DTHNPs were enriched in titanium, carbon, oxygen. In addition, the nitrogen element peak verified the existence of dopamine. High resolution transmission electron microscopy (HRTEM) (Figure 1d) and selected-area electron diffraction (SAED) (inset of Figure 1b) were used to observe whether the freshly as-prepared sample was crystalline. Interestingly, lattice fringes could be observed in the image, implying the generation of partially crystallized phases. Furthermore, X-ray diffraction (XRD) (Figure 1e) demonstrated that the crystal phase was anatase. However, it was reported that the titanium minerals induced by biomacromolecules from a Ti-BALDH solution were usually of amorphous structure.6,24 The surface element composition of the DTHNPs was characterized by using X-ray photoelectron spectroscopy (XPS). As illustrated in Figure 2a, there were C 1s, O 1s, N 1s, and Ti 2p peaks in the XPS spectrum. Quantitative analysis

(6)

3. RESULTS AND DISCUSSION 3.1. Preparation of DTHNPs and the Formation Mechanism. Dopamine (5 mg mL−1) induced the watersoluble precursor titanium(IV) bis (ammonium lactato) dihydroxide (Ti-BALDH, 50 mM) at pH 7.0 and 25 °C to rapidly form orange precipitations. The stirring time (30 s or 12 h) had no influence on the color or the resulting particles (data not shown). Meanwhile, this change in color implied the formation of the titanium(IV)−catecholate coordination.20 Specifically, catechol group was an excellent metal chelator and could coordinate with titanium atom with a wide pH (1− 12).21 Neutral pH led to the generation of titanium(IV) triscatechol, in which three catechol ligands bounded with one titanium atom.20,22 Both scanning electron microscopy (SEM) and transmission electron microscopy (TEM) were used to observe the morphology and size distribution of the dopamine/titania hybrid nanoparticles (DTHNPs) as shown in Figure 1a and b. 12668

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The thermogravimetric analysis (TGA) experiment of the three DTHNPs samples prepared from different dopamine concentrations was operated to determine the content of inorganic and organic moieties in the DTHNPs. As shown in Figure 4, a mass loss below 300 °C for all three kinds of

of the DTHNPs displayed the existence of 51.42% carbon, 33.32% oxygen, 12.75% titanium, 2.51% nitrogen, verifying the coexistence of dopamine and titania. High-resolution XPS spectra for the DTHNPs were illustrated in Figure 2b−e. The binding energies of Ti 2p3/2 and Ti 2p1/2 were centered at 458.5 and 464.2 eV, respectively, clearly revealing that the Ti element was in an oxidation state of +4. The O 1s XPS spectrum exhibited three peaks at 529.9, 531.0, and 532.8 eV, which could be assigned to Ti−O*−Ti, Ti−O*H, and C−O* bond,23 where the oxygen bonds were marked by asterisk, respectively. Moreover, the two peaks of N 1s could be corresponded to N*−C (BE = 399.5)25 from dopamine and N*H4+ (BE = 401.5). The C 1s XPS spectrum consisted of three bonds at 284.7, 286.2, and 288.3 eV. These peaks could be attributed to the dopamine catechol ring,6 C*−OH, and C*−N, respectively. Moreover, the dopamine concentration had a conspicuous effect on the morphology of the DTHNPs as shown in Figure 3. When adding a low concentration of dopamine (1 mg

Figure 4. TGA curve of DTHNPs with various dopamine concentrations.

samples could be due to the evaporation of physically adsorbed water and bound water, and partly decomposition of organic moiety.15 It could be inferred that the DTHNPs were hydrophilic, and this property benefited enzymes in preserving their activity. Once heating continuously to 600 °C, the weight got lost through the oxygenolysis of carbon and nitrogen. In this stage, the organic moiety in the DTHNPs was completely decomposed. Thus, the remaining mass represented the amount of titania originally distributed in the DTHNPs. With the increase of dopamine concentration, more organic moieties was included in DTHNPs. The postulated mechanism about the role of dopamine was tentatively presented based on two reactions, as depicted in Scheme 1. In one reaction, the metal coordination induced by the catechol group brought titanium atoms in close proximity, which would facilitate the condensation process.12 In another reaction, the amino group in dopamine attacked the hydrogen in Ti-BALDH, and a pair of electrons on the dopamine nitrogen accepted the hydrogen.26 The hydrolysis and condensation process were induced by the nucleophilic substitution of another adjacent Ti-BALDH molecule.27 3.2. Enzyme Immobilization in/on NTHNPs. To exploit the potential application, CAT was used as model enzyme entrapped in the dopamine/titania hybrid nanoparticles (DTHNPs). The entrapment efficiency as a function of enzyme concentration was investigated. Specifically, the entrapment efficiency declined monotonically with the increase of the enzyme concentration from 0.1 to 4.0 mg mL−1 (Flocculent structure will be obviously observed with a higher CAT concentration) as shown in Table 1. Notably, at low enzyme concentration, the entrapment efficiency was nearly 100%. When the concentration was up to 4.0 mg mL−1, the entrapment efficiency still kept over 90%. Moreover, enzyme molecule could not be detected in aqueous solution after incubating the immobilized enzyme for 24 h. The high immobilization efficiency of the DTHNPs was ascribed to the covalent binding of enzymes with the catechol groups. Specifically, the highly active quinone, oxidized from catechol in aqueous media, further reacted with nucleophiles, just as

Figure 3. TEM image (right) and SEM image (left) at different dopamine concentrations: (a, d) 1, (b, e) 10, (c, f) 100 mg mL−1.

mL−1), it was obviously that the solution changed into orange without precipitation. After a long time stirring (12 h), slightly cotton-shaped precipitations were obtained by centrifugation (Figure 3a and b). With the increase of the content of dopamine, bigger nanoparticles were generated. When the fabrication conditions were conducted at higher temperature or a wider pH range (2−10), the morphology of the DTHNPs did not show much difference (date not shown) 12669

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Scheme 1. Proposed Mechanism of DTHNP Formation Induced by Dopamine

Table 1. Entrapment Efficiency of CAT within Hybrid NPs CAT concentration (mM) entrapment efficiency (%)

sample 1

sample 2

sample 3

sample 4

sample 5

sample 6

0.1 100

0.2 100

0.5 100

1 100

2 97.99

4 94.31

Activity assays were conducted to assess the effect of operation parameters (such as temperature and pH) on the CAT activity. The similar pH stabilities for free and entrapped CAT, incubated at different pH (from 4 to 9) and room temperature for 3 h, were obtained as shown in Figure 5a. This was because a large number of enzyme molecules would exist on the surface of DTHNPs formed from low concentration of dopamine. This guaranteed the high activity of immobilized enzyme, but impaired the protection of carrier to enzyme molecule. For high temperature, the decline in activities of CAT immobilized in the DTHNPs was caused by denaturation of enzyme molecules and increase of mass transfer resistance. For free enzyme, the activity at 30 °C was only marginally higher than that at 40 °C, and subsequently substantial decrease happened, until lost all activity at 60 °C (Figure 5b). However, the immobilized enzyme showed an enhanced tolerance to thermal stress. The optimal temperature moved from 30 to 40 °C, and the slope of curve was smaller than that of free enzyme. Particularly, even at 70 °C the enzyme still preserved 20% of its catalytic activity. This could be explained from the following two aspects: (1) CAT was covalently attached to dopamine according to Schiff base reaction or Michael addition, and the interaction prevented the inactivation of CAT. (2) The steric constraints of the DTHNPs effectively prevented enzyme from denaturation. Due to the rigidity of the cage in the titania

amino group in enzyme through Michael addition or Schiff base reaction.28,29 The apparent kinetic parameters (Km, Vmax) of the reaction were measured among the entrapped and free enzyme as shown in Table 2. The higher value (74.46 mM) of Km could be Table 2. Kinetic Parameters of Free and Immobilized Enzymes free enzyme enzyme-entrapped DTHNPs

Vmax (mM min−1)

Km (mM)

42.44 31.24

69.44 74.46

observed for the immobilized enzyme in comparison to that for the free enzyme (69.44 mM), implying a lower affinity between enzymes and substrates. Simultaneously, it was obvious that, after entrapped in the DTHNPs, the maximal reaction rate (Vmax) decreased, exhibiting a lower Vmax of 31.24 mM min−1 in contrast with 42.44 mM min−1 for the free enzyme. Considering the enzyme entrapment process was under neutral pH, room temperature, and aqueous solution, and the DTHNPs consisting of biocompatible dopamine and TiBALDH, the decline in catalytic rate could be described to the diffusion limitation of substrate/product rather than the denaturation of enzyme. 12670

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Figure 5. (a) pH, (b) thermal, (c) storage, and (d) recycling stability of immobilized CAT in DTHNPs.

■

matrix, CAT molecules were suppressed to undergo the thermal denaturation of unfolding-refolding motions. The storage stability of entrapped CAT in buffer solution retained 90% of its initial activity, while free CAT lost nearly 70% activity after 55 days stored (Figure 5c). It could be implied that the DTHNPs provided a suitable microenvironment for enzyme. As reported in previous literature,30 the decrease in enzyme activity might be ascribed to proteindegradation microbial. Hence, the high activity retention might be connected with the antibiotic function of titania. The reuse capability of the CAT entrapped DTHNPs was evaluated. At first, no appreciable decrease of activity was observed. And more than 50% of its initial activity was retained after 6 cycles (Figure 5d). The confinement effect of the biomimetic titania toward enzymes might be responsible for the high recycling stability. The breakage of the DTHNPs after continuous stirring might cause the decrease in CAT activity.31

ASSOCIATED CONTENT

S Supporting Information *

CD spectroscopy (Figure S1); PBS influence for entrapment efficiency (Figure S2); dopamine concentration’s influence for enzyme activity (Figure S3). This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*Tel.: +86-22-27406646. Fax: +86-22-23500086. E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The authors thank the National Science Fund for Distinguished Young Scholars (21125627), the Program of Introducing Talents of Discipline to Universities (B06006), Specialized Research Fund for the Doctoral Program of Higher Education (No. 20130032110023), and Program for New Century Excellent Talents in University (No. NCET-10-0623) for financial support.

4. CONCLUSIONS In summary, an approach of combining biomimetic mineralization and titanium(IV)−catecholate coordination is developed to synthesize dopamine/titania hybrid nanoparticles (DTHNPs) through simply mixing Ti-BALDH and dopamine under mild conditions. The amino group in dopamine induces the mineralization and the catechol group in dopamine coordinates with titanium, both of which make contributions to the formation of DTHNPs. The size and shape of DTHNPs can be tailored by changing the dopamine concentration. Owing to the integration of the physicochemical prosperities of both dopamine (reaction with the amino group in enzyme molecule) and titania (antibiotic function), the DTHNPs can be considered as excellent supporters for enzyme immobilization. As a model enzyme, CAT is entrapped through coprecipitation during the formation of DTHNPs. The resultant immobilized enzyme possesses high enzyme entrapment efficiency without any enzyme leakage. Meanwhile, the immobilized enzyme retains 90% catalytic activity of the free enzyme.

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