Gold Nanoparticle-Stabilized, Tyrosine-Rich Peptide Self-Assemblies

Article Cite This: Biomacromolecules XXXX, XXX, XXX−XXX

pubs.acs.org/Biomac

Gold Nanoparticle-Stabilized, Tyrosine-Rich Peptide Self-Assemblies and Their Catalytic Activities in the Reduction of 4‑Nitrophenol Namhun Lee,†,‡ Dae-Won Lee,*,‡ and Sang-Myung Lee*,‡ †

Downloaded via UNIV OF WINNIPEG on December 2, 2018 at 18:18:12 (UTC). See https://pubs.acs.org/sharingguidelines for options on how to legitimately share published articles.

Super Ultra Low Energy and Emission Vehicle (SULEEV) Center, Korea University, Anam-ro 145, Seongbuk-gu, Seoul 02841, Republic of Korea ‡ Department of Chemical Engineering, Division of Chemical and Biological Engineering, Kangwon National University, Gangwon-Do 24341, Republic of Korea S Supporting Information *

ABSTRACT: Peptides are suitable candidates for templates in the fabrication of various metal nanoparticles (NPs) because of their metal-binding ability and templating effect, which impart physicochemical properties to the produced nanoparticles. Peptide-binding gold nanoparticles (AuNPs) show high catalytic activity that permits their application in oxidation or reduction reactions. Herein, we prepared morphology-controllable AuNPs stabilized by self-assembled tyrosinerich peptides (YC7) by varying the pH and YC7 peptide/Au3+ concentration ratio in 2-(N-morpholino)ethanesulfonic acid (MES) buffer solution. The catalytic activities of the YC7 peptide-stabilized AuNPs (YC7@AuNPs) were tested for 4nitrophenol (4-NP) reduction, and kinetic analysis was performed to calculate the apparent rate constants and activation energies. The relatively low activation energy of the YC7@AuNPs could be explained by the hypothesis that the tyrosinemoiety of YC7 enriches the electron density of Au metal.

■

heterogeneous states, for the Suzuki cross-coupling reaction.6 Because of their high catalytic activities, peptide-templated AuNPs have been applied to oxidation and reduction reactions in various biosensor applications. Typically, AuNPs are utilized as peroxidase-mimetic nanocatalysts for biomimetic oxidation with a substrate such as 3,5,3′,5′-tetramethylbenzidine (TMB), luminol, 10-acetyl-3,7-dihydroxyphenoxazine (Amplex Red), or 2,2′-azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) (ABTS).20−27 To the best of our knowledge, the use of YC7 peptide as a template in the synthesis of AuNPs and the redox activity of AuNPs stabilized by self-assembled YC7 peptide have not been reported. The reduction of 4-nitrophenol (4NP) to 4-aminophenol (4-AP), which is an important pharmaceutical precursor, is a probe reaction worthy of analysis for evaluating the redox activity of AuNP catalysts28 and for amplifying the detection signal of biomarker proteins.29 Here, we introduce a robust method for the synthesis of morphology-controllable AuNPs stabilized by self-assembled YC7 peptide and report their high catalytic activity for 4nitrophenol reduction. Novel YC7-templated AuNPs (YC7@ AuNPs) were prepared via a robust one-pot reaction in 2-(Nmorpholino)ethanesulfonic acid (MES) buffer, which is one of common biological buffers, at the phase transition temperature of YC7 (around 60 °C) within 5 min. Under these fabrication conditions, two processes occur simultaneously: self-assembly

INTRODUCTION Bioinspired or biomimetic strategies for the fabrication of various types of nanoparticles (NPs) have recently gained interest as they impart unique morphologies and properties to the NPs under mild conditions.1,2 Most biomolecules, including biopolymers, DNA, viruses, and peptides, have been demonstrated to be robust surface stabilizers or templates for NPs.3−11 In particular, peptides are used as effective templates for the synthesis of nobel metal NPs (Au, Pt, and Pd), and the resulting peptide-templated NPs are widely employed as catalysts, sensing probes, and so forth.12−14 The diverse choice of peptide sequences for the synthesis of customized NPs with specific physicochemical properties and the need for mild synthesis conditions are highly advantageous in this regard.15,16 Knecht and co-workers developed various types of Pd and Au nanocatalysts specifically controlled by metal-binding peptides and elucidated the synthesis mechanism and catalytic properties by empirical and theoretical approaches.17−19 A tyrosine-rich peptide (YYACAYY: abbreviated as YC7 or TRP), one of the well-known self-assembling peptide building blocks, shows unique and interesting properties when used as a metal ion-coordinating template in NP synthesis. Our group introduced a TRP-based method for fabricating flower-like PdNPs, which were successfully applied to a copper-free Sonogashira coupling reaction.9 We also developed a sphereto-bridge-shaped Pd ion-chelated TRP nanocatalyst (YC7@ Pd2+), which showed a unique feature, that is, reversible thermal-phase transition between the homogeneous and © XXXX American Chemical Society

Received: August 12, 2018 Revised: November 6, 2018

A

DOI: 10.1021/acs.biomac.8b01221 Biomacromolecules XXXX, XXX, XXX−XXX

Article

Biomacromolecules

Figure 1. Schematic diagram for the robust synthesis of two types of tyrosine rich peptide-stabilized AuNPs (YC7@AuNPPhed and YC7@ AuNPBump). Tris, MES, or PBS; stock solution concentration = 10 or 50 mM; pH = 5.0, 7.0, or 9.0) at 90 °C in a thermomixer (Eppendorf Thermomixer Comfort, Eppendorf, Germany). Subsequently, an aliquot of the desired YC7 solution (500 μL) was added to a 1 mM aqueous solution of HAuCl4 (50 μL) at 60 °C, and the mixture was stirred (1000 rpm) at this temperature for 30 min. The resulting nanoparticles (YC7@AuNPs) were collected and washed 3 times with distilled water. Characterization of YC7@AuNPs. The morphologies of the synthesized YC7@AuNPs were observed by TEM (LEO 912AB Omega, Zeiss, Germany). Zeta potential measurements and analysis by DLS were performed using a zeta potential and particle size analyzer (ELSZ-2000, Otsuka, Japan). X-ray photoelectron spectroscopy (XPS) was performed on a K Alpha+ instrument (Thermo Scientific, U.K.) under ultrahigh vacuum conditions (5 × 10−8 mbar), and the spectra were calibrated by fixing the C 1s peak position at 284.5 eV. X-ray diffraction (XRD) measurements were carried out using an X’pert-Pro MPD diffractometer (Bruker, Netherlands) equipped with a Cu Kα radiation source (λ = 0.1542 nm) operated at 30 mA and 40 kV. Evaluation of the Catalytic Activity. A 100 μM aqueous solution of 4-NP (1.5 mL) was added to a cubic quartz cell (7.03 cm3) containing 10−200 mM of aqueous NaBH4 solution (0.75 mL) and the desired solution of YC7@AuNPs (0.75 mL, Au concentration = 10, 25, 50, or 100 μM, as determined by inductively coupled plasma (ICP) analysis). The concentration of 4-NP was measured continuously by UV−vis spectrometry (Optizen Alpha, Mecasys, South Korea) over 20 min. The catalytic reactions were performed at five different temperatures (i.e., 25, 35, 45, 55, and 65 °C), and the corresponding kapp and Ea were determined using a pseudo-first-order plot and the Arrhenius correlation, respectively (eqs 1 and 2). Each reaction was repeated five times, and average values were calculated.

of the YC7 molecules and reduction of the Au precursor ions (AuCl4−) to Au metal seeds, followed by the growth of YC7stabilized NPs with a specific morphology. The influence of the synthesis conditions, such as pH, buffer type, buffer concentration, and [AuCl4−]/[YC7] ratio, on the structure and morphology of the YC7@AuNPs was investigated. The YC7@AuNPs was characterized in detail by transmission electron microscopy (TEM), UV−vis spectroscopy, X-ray diffraction (XRD), X-ray photoelectron spectroscopy (XPS), dynamic light scattering (DLS), and so on. The nanoscale morphology of AuNPs with sizes of 40−50 nm changed from polyhedral to bumpy depending on the molar ratio of YC7 and Au precursor ions (AuCl4−). The catalytic activity of the YC7@ AuNPs was examined for the reduction of 4-NP to 4-AP with NaBH4. Kinetic parameters such as the apparent rate constant (kapp) and activation energy (Ea) were determined by pseudofirst-order kinetic analyses of the 4-NP reduction results. The relatively low Ea of the YC7@AuNPs could be explained based on the hypothesis that the tyrosine-mediated electron transfer enriches the electron density of the Au metal.

■

MATERIALS AND METHODS

Materials. Gold(III) chloride trihydrate (HAuCl4·3H2O, ≥98%), sodium borohydride (≥96%), tris(hydroxymethyl)aminomethane (Tris, ≥99.9%), sodium bicarbonate (SBC, ≥99.5%), 2-(Nmorpholino)ethanesulfonic acid (MES, ≥99%), sodium chloride (NaCl, ≥99%), and potassium chloride (KCl, ≥99%) were purchased from Sigma-Aldrich (U.S.A.). Sodium phosphate dibasic anhydrous (Na2HPO4, ≥99%), potassium phosphate monobasic (KH2PO4, ≥99%), and 4-nitrophenol (≥98%) were purchased from Daejung Chemicals & Metals Co. Ltd. (South Korea). The YC7 peptide (+H3N-YYACAYY-COO−; mw. 916.02; ≥95%) was purchased from GL Biochem (China). All materials were used without further purification. Synthesis of YC7@AuNPs. The YC7 peptide (0.1, 0.2, 0.33, or 0.66 mM) was dissolved in the desired buffer solution (1 mL, SBC,

kapp =

Ea = B

ln(I /I0) t

ln k T −1

(1)

(2) DOI: 10.1021/acs.biomac.8b01221 Biomacromolecules XXXX, XXX, XXX−XXX

Article

Biomacromolecules

Figure 2. TEM images of YC7 peptide/Au ion-derived nanostructures prepared by the indicated buffers and their pH values. (Other conditions: [HAuCl4] = 1 mM; [YC7] = 0.033 mM; [Buffer] = 50 mM) (Insert TEM image in f,h,i = 20× magnified image of selected area).

■

RESULTS AND DISCUSSIONS YC7 assembly templated AuNPs (YC 7 @AuNPs) were prepared by a simple one-pot reaction within a short time of 5 min, as mentioned in the experimental session. The proposed reaction mechanism is depicted in Figure 1. Upon mixing the YC7 molecules and Au ions at 60 °C, the tyrosine moieties of the YC7 molecules chelate with the Au ions, and then two events occur simultaneously: (i) the reduction of Au ions by the buffer solution and (ii) the self-assembly of YC7 peptide molecules by the temperature change (90 → 60 °C). Then, the YC7 or YC7 assembly stabilized Au seeds nucleate and grow into stable and well-dispersed AuNPs with specific morphologies depending on the molar ratio of the added Au ions and YC7 peptide. Most biomimetic NPs are obtained by using reducing agents such as ascorbic acid, citrate, NaBH4, or hydrazine in water. However, we synthesized AuNPs by using the buffer solution as the reductant of the Au precursor ions instead of employing these reductants, which is attractive from the perspective of green chemistry. Thus, we examined the effects of buffer conditions (buffer salt type, buffer concentration, and pH) on the YC7@AuNP nanostructure. Figure 2 shows the TEM images of YC7@AuNP prepared using three different buffers adjusted to specific pH values. The use of Tris, PBS, and MES buffers adjusted to pH 5.0 resulted in the nanomaterials with

different sizes: 500−570 nm in the Tris buffer and 50−188 nm in PBS and MES buffers (Figure 2a−c). The product formation mechanism is thought to be closely related to the balance between the intermolecular attraction among the YC7 peptides, which triggers the peptide association, and the reducing power of the buffer for Au3+ ions. Under low-pH conditions (pH 5.0), which corresponds to low reducing power, Au is mostly present in ionic form. Meanwhile, the YC7 peptide (isoelectric point: 6.1) is largely protonated, so that the π−π interactions among the tyrosine residues are strengthened as a result of the weakened ionic repulsion among them.30 Thus, the solution became a self-assembly favorable environment that allows the formation of an “Au ion”-chelated YC7 self-assembled nanostructure, similar to inter−bridged spheres (Figure 2a−c). XPS analysis confirmed that the chelated Au was not reduced but remained in the ionic state (Figure S1a−c). In the case of the Tris and PBS buffers adjusted to pH 7.0, Au is predominantly present in the ionic state, while deprotonation of the phenol groups causes strong electrostatic repulsion among the YC7 peptides. Given the formation of the interbridged spherical nanostructures (Figure 2d,e), similar to those formed at pH 5.0, the π−π interactions among peptides are thought to exist, although they are weakened by the repulsive forces between the phenolate anions.30 Unlike the result obtained at pH 5.0, AuNPs were C

DOI: 10.1021/acs.biomac.8b01221 Biomacromolecules XXXX, XXX, XXX−XXX

Article

Biomacromolecules

Figure 3. TEM images of YC7@AuNPs prepared in different Au ion precursor-to-peptide concentration ratio ([HAuCl4]/[YC7]); (a,e) 100, (b,f) 50, (c,g) 30 and (d,h) 15 ([MES] = 50 mM, pH 9.0).

lowered from 50 to 10 mM. As shown in Figures S2a,b, even after the pH was adjusted to 7.0 and 9.0, metallic AuNPs were not formed, and a disordered (Au ion-chelated) YC7 selfassembly chain was obtained. This result indicated that Au ions cannot be reduced to metallic form with 10 mM MES solution, confirming that the MES concentration is a primary factor in determining the formation of metal NPs. Next, the effect of the molar ratio of Au ions and YC7 peptide on the nanoscale morphology of YC7@AuNPs was examined with fixing the buffer conditions to [MES] = 50 mM and pH = 9.0 (Figure 3). When the molar ratio of AuCl4− and YC7 ([HAuCl4]/[YC7]) was 100 (Figure 3a,e, Type 1), AuNPs with a polyhedral morphology of AuNP were obtained. The NP size was confirmed to be 40−60 nm by DLS analyses, and the thickness of the peptide layer was measured to be 0.8− 0.9 nm. These observations implied that the YC7 peptide (or its self-assembly) acts as a molecular template for the formation of polyhedral AuNPs with a uniform morphology and size. With a gradual increase in the molar concentration of YC7 (relative to that of AuCl4−), the templating effect of YC7 peptide got became more pronounced. As shown in Figure 3b,f, AuNPs with a quasi-polyhedral or triangular morphology were more predominant than those with a uniform polyhedral morphology ([HAuCl4]/[YC7] = 50, Type 2). AuNPs with a distinctive “bumpy” morphology were observed when the [HAuCl4]/[YC7] molar ratio was 30 (Figures 3c,g, Type 3). When the [HAuCl4]/[YC7] molar ratio was further decreased to 15 (Figure 3d, Type 4), a large background tissue of the YC7 peptide self-assembly was observed, which might be caused by the excess concentration of YC7 molecules. It was supported by UV/vis and TEM-EDS mapping analysis results which are given as supplementary data (Figure S3 in Supporting Information). XPS and XRD analyses were performed to confirm the metallic nature of the fabricated YC7@AuNPs. As shown in Figure S4, diffraction peaks corresponding to Au metal were observed at 2θ = 38.3°, 44.1°, 64.8°, 77.7°, and 82.3° ([110], [200], [220], [311], and [222], respectively). X-

formed at pH 7.0 (tiny black dots in Figure 2d,e), albeit in small number. The strong repulsive forces between the peptide molecules promoted chelation of the Au3+ ion to the peptide, and a large number of these ions were not reduced to the metallic state. The size of the nanospheres seems to change with the type of buffer salt used. On the other hand, the number of “metallic” AuNPs increased greatly in the PBS and MES buffers adjusted to pH 9.0 (Figure 2h,i). The metallic state of Au was confirmed by XPS analysis (Figure S1h,i). Tiny inter−bridged AuNPs (18.8−25.1 nm) were found in the PBS buffer (Figure 2h), while fully separated AuNPs with bumpy or polyhedral morphologies (25.6−39.0 nm) were formed in the MES buffer (Figure 2i). These results suggested that these buffer solutions adjusted to pH 9.0 created a highly reductive environment in which intermolecular repulsion among the YC7 peptides was very strong. The YC7 peptides containing abundant deprotonated phenol groups play the role of a template as well as a stabilizer for the AuNP formation. Unlike the case of pH 5.0 and 7.0, no separate peptide self-assembly structure was observed at pH 9.0, implying that the YC7 peptide molecules are utilized for AuNP formation rather than for their self-assembly. Conversely, in the Tris buffer increasing the pH to 9.0 did not promote the formation of AuNPs; rather, a shapeless cloud−like Au ion-chelated peptide assembly was formed (Figure 2g). The ionic state of Au was confirmed in Figure S1g. This result implied that the Tris buffer was ineffective for the creation of a reductive environment. Meanwhile, fully separated “metallic” AuNPs were also formed in the MES buffer adjusted to pH 7.0, as shown in Figure 2f, and the metallic state of Au was confirmed from Figure S1f. The NPs were slightly smaller in size than those generated at pH 9.0 (36.3−39.0 nm, Figure 2i). Because MES is well-known for its reducing power comparable to that of 4-(2hydroxyethyl)-1-piperazineethanesulfonic acid (HEPES),13,14,31 the reduction of Au ions was thought to be effective even at pH 7.0. In order to examine the effect of the MES buffer on AuNP formation, the buffer concentration was D

DOI: 10.1021/acs.biomac.8b01221 Biomacromolecules XXXX, XXX, XXX−XXX

Article

Biomacromolecules

Figure 4. Illustration of the reduction mechanism of 4-NP by NaBH4 occurred on the surface of AuNPs.

Figure 5. Absorbance changes at 400 nm for different NaBH4 concentrations as a function of time; (a) YC7@AuNPPhed and (b) YC7@AuNPBump.

also because the kinetic analyses of their activities would be more straightforward than those of Types 2 and 4. Figure 4 illustrates the mechanism of 4-NP reduction on the Au surface. First, 4-NP and BH4− as reducing agents diffuse to the nearby the Au surface (Step 1). Then, the 4-NP molecules are reduced by the electrons transferred from the coadsorbed BH4− on the Au surface (Step 2, Langmuir−Hinshelwood mechanism).28,32,33 Finally, the catalytic reaction is terminated by the desorption of 4-AP from the Au surface (Step 3). Figure 5 depicts the reaction results, that is, the UV absorbance of 4-NP (λ = 400 nm) for different concentrations of NaBH4 as a function of reaction time. When the NaBH4 concentration was 10 mM (100 times the 4-NP concentration), the 4-NP concentration declined very slowly over time when using YC7@AuNPBump or YC7@AuNPPhed as the catalyst. With increasing NaBH4 concentration from 50 to 200 mM, both catalysts showed noticeable improvements in the rate of 4-NP conversion. The higher the NaBH4 concentration,

ray photoelectron spectra also indicated that Au existed in the metallic state (Au0 4f5/2 ≈ 87.8 eV; Au0 4f7/2 ≈ 83.9 eV) in both YC7@AuNPPhed and YC7@AuNPBump. The HR-TEM and FFT diffraction analyses also supported the formation of metallic gold particles (Figure S5 in Supporting Information). Meanwhile, FT-IR analysis demonstrated the existence of YC7 peptide in AuNPs, because both of YC7@AuNP has the CO double bond stretching of amide I groups at 1650 cm−1, which directly features peptide bond moiety of YC7 peptide (Figure S6 in Supporting Information). For the reaction test (reduction of 4-NP), we employed Type 1 (YC7@AuNPPhed, Figure 3a,e) and Type 3 (YC7@ AuNPBump, Figure 3c,g) as the catalyst. This was because the former has a more uniform morphology close to polyhedral than does Type 2, and the latter does not involve the unnecessary peptide background tissue see in Type 4. The choice of Type 1 and Type 3 was reasonable, not only because they represented two morphologically different groups, but E

DOI: 10.1021/acs.biomac.8b01221 Biomacromolecules XXXX, XXX, XXX−XXX

Article

Biomacromolecules

Figure 6. Kinetic analysis of catalytic reduction of p-nitrophenol using two types of YC7@AuNP: (a) absorbance changes at 400 nm as a function of reaction time; (b) linear plots used to determine pseudo-first-order kinetics taken from step 2 of (a); (c) pseudo-first-order rate constants (k) versus temperature obtained from two catalysts; and (d) Arrhenius plots to calculate activation energies (Ea).

Table 1. Kinetic Parameters of Various AuNP Catalysts for Reduction of 4-Nitrophenol AuNP catalyst

K (10−3 s‑1)

Ea (kJ/mol)

ref

YC7@AuNPBump YC7@AuNPPhed WALRRSIRRQSY@AuNP TSNAVHPTLRHL@AuNP AYSSGAPPMPPF@AuNP TGIFKSARAMRN@AuNP SSKKSGSYSGSKGSKRRIL@AuNP CTAB@AuNP DMF@AuNP hollow porous AuNP nanocages AuNP nanoboxes AuNP partially hollow boxes AuNP

3.5 4.2

18.0 ± 1.3 18.7 ± 3.4 26.2 ± 0.9 18.1 ± 2.3 20.0 ± 1.0 25.8 ± 3.1 29.0 ± 1.4 50.3 ± 2.3 31.0 33.6 28.04 ± 1.43 44.25 ± 2.63 55.44 ± 3.15

this work this work 18 18 19 19 34 37 38 39 40 40 40

11.2 6 3 7.42 47.2 18.70 9.83

Next, kinetic analysis was performed to determine the apparent rate constant (kapp) and the activation energy (Ea) for the two types of YC7@AuNP catalysts. The absorbance plots at 25 °C for YC7@AuNPBump and YC7@AuNPPhed are compared in Figure 6a. With the termination of step 1, step 2 begins, where 4-NP is reduced by BH4− coadsorbed on the Au surface. In step 2, the absorbance of 4-NP sharply decreases in both catalytic systems. In Figure 6b, the plots of the logarithmic value of relative UV absorbance (the relative 4-NP concentration) during step 2 as a function of time were linear, implying that the reaction rate has pseudo-first-order dependence on 4-NP concentration. Because the initial concentration of NaBH4 was almost 100 times higher than that of 4-NP, the concentration could be regarded as unchanged and the BH4− concentration term can be dumped into rate constant, resulting

the shorter is the time taken for step 1. The length of step 1 might be associated with the diffusion of BH4− ions onto the Au surface.18,19,34 Interestingly, step 1 was much longer in the case of YC7@AuNPPhed than for YC7@AuNPBump. Diffusion resistance might be caused by the severe charge repulsion between the BH4− ions and the crammed phenolates in the peptide self-assembly layer of YC7@AuNPs, and the degree of resistance should be strongly dependent on the thickness of the self-assembly layer of YC7@AuNPs. The thicker the selfassembly layer, the stronger is its diffusion resistance, which would prolong step 1. As shown in Figure 3e,g, the YC7 peptide assembly layer of YC7@AuNPPhed (average layer thickness = 0.89 nm) is thicker than that of YC7@AuNPBump (average layer thickness = 0.81 nm), thus supporting our hypothesis. F

DOI: 10.1021/acs.biomac.8b01221 Biomacromolecules XXXX, XXX, XXX−XXX

Biomacromolecules

■

in the pseudo-first-order dependence of the rate law on the 4NP concentration. By linear regression, the kapp values of YC7@AuNPBump and YC7@AuNPPhed were determined to be 3.1 × 10−3 and 5.0 × 10−3 s−1, respectively (Table 1). To determine Ea, the rate constants were calculated by changing the reaction temperature from 25 to 65 °C (Figure 6c). The Arrhenius plots were regressed to straight lines (Figure 6d), whose slopes corresponded to Ea, 18.0 ± 1.3 kJ/mol (YC7@ AuNPBump) and 18.7 ± 3.4 kJ/mol (YC7@AuNPPhed). Both the catalysts showed perfect Arrhenius behavior even at an elevated temperature of 65 °C, clearly demonstrating that the YC7 peptide is a good biomolecular stabilizer that preserves the inherent catalytic activity of the AuNPs in a thermostable manner. Finally, the Ea of the two catalysts was smaller than those of other peptide-stabilized AuNPs in the literature (Table 1). Thus, the role of the YC7 peptide or its assembly in the 4-NP reduction activity should be explained. The 4-NP reduction is thought to occur on YC7@AuNPs via two routes: (i) the conventional Langmuir−Hinshelwood mechanism on an uncoordinated Au surface; and (ii) the tyrosine-mediated Langmuir−Hinshelwood mechanism on the YC7-coordinated Au surface. Route (ii) indicates that the tyrosine moiety of YC7 participates in the catalytic process as a redox mediator. The abundant phenoxide anions of YC7 at pH 9.0 increase the electron density in the π−π* transition of the tyrosine residues, thereby promoting electron transfer from tyrosine to the Au metal coordinated to tyrosine residues.35,36 Consequently, the Au metal coordinated to YC7 is enriched in electron density, so that the reaction is accelerated more actively than that in the case of the uncoordinated Au metal. This additional tyrosinemediated route would be reflected on the improved activation energies of YC7@AuNPs.

■

Article

ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.biomac.8b01221.

■

XPS analysis of YC7 peptide/Au ion-derived nanostructures prepared by the indicated buffers and their pH values (Figure S1), TEM images of YC7@AuNPs prepared in MES buffers adjusted to different pH values and concentrations (Figure S2), UV/vis spectra of pure YC7 peptide and YC7@AuNPBump and TEM-EDS mapping images (Figure S3), XRD and XPS analysis of YC7@AuNPs (Figure S4), HR-TEM and FFT diffraction patterns of YC7@AuNPs (Figure S5), and FT-IR spectra of YC7 peptide and YC7@AuNPs (Figure S6) (PDF)

AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. *E-mail: [email protected]. ORCID

Dae-Won Lee: 0000-0003-4614-5013 Notes

The authors declare no competing financial interest.

■

ACKNOWLEDGMENTS This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science & ICT(MSIT) (NRF-2016R1A5A1009592).

■

CONCLUSION

REFERENCES

(1) Gröschel, A. H.; Müller, A. H. E. Self-assembly concepts for multicompartment nanostructures. Nanoscale 2015, 7 (28), 11841− 118476. (2) Bai, Y.; Luo, Q.; Liu, J. Protein self-assembly via supramolecular strategies. Chem. Soc. Rev. 2016, 45 (10), 2756−2767. (3) Wang, T.; Zhang, Z.; Gao, D.; Li, F.; Wei, H.; Liang, X.; Cui, Z.; Zhang, X. E. Encapsulation of gold nanoparticles by simian virus 40 capsids. Nanoscale 2011, 3 (10), 4275−4282. (4) Peelle, B. R.; Krauland, E. M.; Wittrup, K. D.; Belcher, A. M. Design Criteria for Engineering Inorganic Material-Specific Peptides. Langmuir 2005, 21, 6929−6933. (5) Hnilova, M.; Oren, E. E.; Seker, U. O. S.; Wilson, B. R.; Collino, S.; Evans, J. S.; Tamerler, C.; Sarikaya, M. Effect of Molecular Conformations on the Adsorption Behavior of Gold-Binding Peptides. Langmuir 2008, 24, 12440−12445. (6) Kim, S.; Cho, H.-J.; Lee, N.; Lee, Y.-S.; Shin, D.-S.; Lee, S.-M. A phase-reversible Pd containing sphere-to-bridge-shaped peptide nanostructure for cross-coupling reactions. RSC Adv. 2017, 7 (53), 33162−33165. (7) Slocik, J. M.; Stone, M. O.; Naik, R. R. Synthesis of gold nanoparticles using multifunctional peptides. Small 2005, 1 (11), 1048−52. (8) Bhattacharjee, R. R.; Das, A. K.; Haldar, D.; Si, S.; Banerjee, A.; Mandal, T. K. Peptide-Assisted Synthesis of Gold Nanoparticles and Their Self-Assembly. J. Nanosci. Nanotechnol. 2005, 5 (7), 1141− 1147. (9) Kim, Y.-O.; Jang, H.-S.; Kim, Y.-h.; You, J. M.; Park, Y.-S.; Jin, K.; Kang, O.; Nam, K. T.; Kim, J. W.; Lee, S.-M.; Lee, Y.-S. A tyrosine-rich peptide induced flower-like palladium nanostructure and its catalytic activity. RSC Adv. 2015, 5 (95), 78026−78029.

In conclusion, AuNPs stabilized by self-assembled YC7 peptide were synthesized by utilizing a buffer salt as the reductant for the Au precursor ions. The use of MES buffer at pH 9.0 resulted in the formation of polyhedral and bumpy YC7@ AuNPs depending on the [HAuCl4−]/[YC7] ratio. The formation mechanism of YC7@AuNPs is supposed to involve deprotonation of the tyrosine residues, followed by coordination of the Au3+ cations, and subsequent reduction of the Au ions by MES, growth of AuNPs, and self-assembly of the YC7 peptide via π−π stacking between the tyrosine residues. YC7@ AuNPs was then tested as a catalyst for the reduction of 4-NP. The reaction predominantly followed pseudo-first-order kinetics, that is, the Langmuir−Hinshelwood mechanism, on the Au metal surface. The tyrosine moiety of the YC7 peptide was thought to promote the catalytic activity of the Au metal at pH 9.0 by making the Au metal electron-rich via electron donation. The apparent rate constant and activation energy of the YC7@AuNPs were ∼4.0 × 10−3 s−1 and 18.0 ± 2.1 kJ/mol, respectively, and the latter was presumed to be due to the tyrosine-mediated activity enhancement. On the basis of these results, it is anticipated that these unique morphologycontrollable AuNPs stabilized by the tyrosine-rich peptide assembly can be widely utilized as active components in biomimetic catalysis, sensing, diagnostics, and so forth. G

DOI: 10.1021/acs.biomac.8b01221 Biomacromolecules XXXX, XXX, XXX−XXX

Article

Biomacromolecules

other transition metal nanoparticles. Coord. Chem. Rev. 2015, 287, 114−136. (29) Das, M. A. A. j.; Yang, H.; et al. A Nanocatalyst-Based Assay for Proteins: DNA-Free Ultrasensitive Electrochemical Detection Using Catalytic Reduction of p-Nitrophenol by Gold-Nanoparticle Labels. J. Am. Chem. Soc. 2006, 128, 16022−16023. (30) Lee, N.; Jang, H.-S.; Lee, M.; Kim, Y.-O.; Cho, H. J.; Jeong, D. H.; Shin, D.-S.; Lee, Y.-S.; Lee, D.-W.; Lee, S.-M. Au ion-mediated self-assembled tyrosine-rich peptide nanostructure embedded with gold nanoparticle satellites. J. Ind. Eng. Chem. 2018, 64, 461−466. (31) Ferreira, C. M. H.; Pinto, I. S. S.; Soares, E. V.; Soares, H. M. V. M. (Un)suitability of the use of pH buffers in biological, biochemical and environmental studies and their interaction with metal ions − a review. RSC Adv. 2015, 5 (39), 30989−31003. (32) Hervés, P.; Pérez-Lorenzo, M.; Liz-Marzán, L. M.; Dzubiella, J.; Lu, Y.; Ballauff, M. Catalysis by metallic nanoparticles in aqueous solution: model reactions. Chem. Soc. Rev. 2012, 41 (17), 5577−5587. (33) Ciganda, R.; Li, N.; Deraedt, C.; Gatard, S.; Zhao, P.; Salmon, L.; Hernández, R.; Ruiz, J.; Astruc, D. Gold nanoparticles as electron reservoir redox catalysts for 4-nitrophenol reduction: a strong stereoelectronic ligand influence. Chem. Commun. 2014, 50 (70), 10126−10129. (34) Bhandari, R.; Knecht, M. R. Synthesis, characterization, and catalytic application of networked Au nanostructures fabricated using peptide templates. Catal. Sci. Technol. 2012, 2 (7), 1360−1366. (35) Slocik, J. M.; Naik, R. R.; Stone, M. O.; Wright, D. W. Viral templates for gold nanoparticle synthesis. J. Mater. Chem. 2005, 15 (7), 749−753. (36) Zhou, Y.; Chen, W.; Itoh, H.; Naka, K.; Ni, Q.; Yamane, H.; Chujo, Y. Preparation of a novel core−shell nanostructured gold colloid−silk fibroin bioconjugate by the protein in situ redox technique at room temperature. Chem. Commun. 2001, No. 23, 2518−2519. (37) Fenger, R.; Fertitta, E.; Kirmse, H.; Thunemann, A. F.; Rademann, K. Size dependent catalysis with CTAB-stabilized gold nanoparticles. Phys. Chem. Chem. Phys. 2012, 14 (26), 9343−9349. (38) Yamamoto, H.; Yano, H.; Kouchi, H.; Obora, Y.; Arakawa, R.; Kawasaki, H. N. N-Dimethylformamide-stabilized gold nanoclusters as a catalyst for the reduction of 4-nitrophenol. Nanoscale 2012, 4 (14), 4148−4154. (39) Guo, M.; He, J.; Li, Y.; Ma, S.; Sun, X. One-step synthesis of hollow porous gold nanoparticles with tunable particle size for the reduction of 4-nitrophenol. J. Hazard. Mater. 2016, 310, 89−97. (40) Zeng, J.; Zhang, Q.; Chen, J.; Xia, Y. A comparison study of the catalytic properties of Au-based nanocages, nanoboxes, and nanoparticles. Nano Lett. 2010, 10 (1), 30−35.

(10) Si, S.; Mandal, T. K. pH-Controlled Reversible Assembly of Peptide-Functionalized Gold Nanoparticles. Langmuir 2007, 23, 190−195. (11) Si, S.; Bhattacharjee, R. R.; Banerjee, A.; Mandal, T. K. A mechanistic and kinetic study of the formation of metal nanoparticles by using synthetic tyrosine-based oligopeptides. Chem. - Eur. J. 2006, 12 (4), 1256−65. (12) Ferreira, C. M. H.; Pinto, I. S. S.; Soares, E. V.; Soares, H. M. V. M. (Un)suitability of the use of pH buffers in biological, biochemical and environmental studies and their interaction with metal ions − a review. RSC Adv. 2015, 5 (39), 30989−31003. (13) Ahmed, S. R.; Oh, S.; Baba, R.; Zhou, H.; Hwang, S.; Lee, J.; Park, E. Y. Synthesis of Gold Nanoparticles with Buffer-Dependent Variations of Size and Morphology in Biological Buffers. Nanoscale Res. Lett. 2016, 11 (1), 65−76. (14) Habib, A.; Tabata, M.; Wu, Y. G. Formation of Gold Nanoparticles by Good’s Buffers. Bull. Chem. Soc. Jpn. 2005, 78 (2), 262−269. (15) Chen, C. L.; Rosi, N. L. Peptide-based methods for the preparation of nanostructured inorganic materials. Angew. Chem., Int. Ed. 2010, 49 (11), 1924−1942. (16) Ulijn, R. V.; Smith, A. M. Designing peptide based nanomaterials. Chem. Soc. Rev. 2008, 37 (4), 664−75. (17) Bhandari, R.; Knecht, M. R. Effects of the Material Structure on the Catalytic Activity of Peptide-Templated Pd Nanomaterials. ACS Catal. 2011, 1 (2), 89−98. (18) Briggs, B. D.; Li, Y.; Swihart, M. T.; Knecht, M. R. Reductant and sequence effects on the morphology and catalytic activity of peptide-capped Au nanoparticles. ACS Appl. Mater. Interfaces 2015, 7 (16), 8843−8851. (19) Li, Y.; Tang, Z.; Prasad, P. N.; Knecht, M. R.; Swihart, M. T. Peptide-mediated synthesis of gold nanoparticles: effects of peptide sequence and nature of binding on physicochemical properties. Nanoscale 2014, 6 (6), 3165−3172. (20) Zhang, Y.; Xu, C.; Li, B.; Li, Y. In situ growth of positivelycharged gold nanoparticles on single-walled carbon nanotubes as a highly active peroxidase mimetic and its application in biosensing. Biosens. Bioelectron. 2013, 43, 205−210. (21) Gao, Z.; Xu, M.; Lu, M.; Chen, G.; Tang, D. Urchin-like (gold core)@(platinum shell) nanohybrids: A highly efficient peroxidasemimetic system for in situ amplified colorimetric immunoassay. Biosens. Bioelectron. 2015, 70, 194−201. (22) Jv, Y.; Li, B.; Cao, R. Positively-charged gold nanoparticles as peroxidase mimic and their application in hydrogen peroxide and glucose detection. Chem. Commun. (Cambridge, U. K.) 2010, 46 (42), 8017−8019. (23) Long, Y. J.; Li, Y. F.; Liu, Y.; Zheng, J. J.; Tang, J.; Huang, C. Z. Visual observation of the mercury-stimulated peroxidase mimetic activity of gold nanoparticles. Chem. Commun. (Cambridge, U. K.) 2011, 47 (43), 11939−41. (24) Ponlakhet, K.; Amatatongchai, M.; Sroysee, W.; Jarujamrus, P.; Chairam, S. Development of sensitive and selective glucose colorimetric assay using glucose oxidase immobilized on magnetite−gold−folate nanoparticles. Anal. Methods 2016, 8 (47), 8288− 8298. (25) Liu, D.; Yang, J.; Wang, H. F.; Wang, Z.; Huang, X.; Wang, Z.; Niu, G.; Hight Walker, A. R.; Chen, X. Glucose oxidase-catalyzed growth of gold nanoparticles enables quantitative detection of attomolar cancer biomarkers. Anal. Chem. 2014, 86 (12), 5800−6. (26) Wang, C.; Liu, C.; Luo, J.; Tian, Y.; Zhou, N. Direct electrochemical detection of kanamycin based on peroxidase-like activity of gold nanoparticles. Anal. Chim. Acta 2016, 936, 75−82. (27) Lien, C. W.; Huang, C. C.; Chang, H. T. Peroxidase-mimic bismuth-gold nanoparticles for determining the activity of thrombin and drug screening. Chem. Commun. (Cambridge, U. K.) 2012, 48 (64), 7952−7954. (28) Zhao, P.; Feng, X.; Huang, D.; Yang, G.; Astruc, D. Basic concepts and recent advances in nitrophenol reduction by gold- and H

DOI: 10.1021/acs.biomac.8b01221 Biomacromolecules XXXX, XXX, XXX−XXX