Mechanisms of Aggregation of Cysteine Functionalized Gold

Article pubs.acs.org/JPCC

Mechanisms of Aggregation of Cysteine Functionalized Gold Nanoparticles Robert G. Acres,*,† Vitaliy Feyer,‡ Nataliya Tsud,§ Elvio Carlino,∥ and Kevin C. Prince†,∥,⊥ †

Elettra-Sincrotrone Trieste S.C.p.A., in Area Science Park, Strada Statale 14, km 163.5, Basovizza (Trieste), 34149, Italy Peter Grünberg Institute (PGI-6) and JARA-FIT, Research Center Jülich, 52425 Jülich, Germany § Faculty of Mathematics and Physics, Department of Surface and Plasma Science, Charles University, V Holešovikách 2, 18000 Prague 8, Czech Republic ∥ CNR-IOM Laboratorio TASC, Basovizza (Trieste), I-34149, Italy ⊥ eChemistry Laboratory, Faculty of Life and Social Sciences, Swinburne University of Technology, Hawthorn, Melbourne, Victoria 3122, Australia ‡

S Supporting Information *

ABSTRACT: The interaction of gold nanoparticles (AuNPs) with cysteine and its derivatives is the basis of a number of bionanotechnologies, and for these, the most important process is aggregation (or antiaggregation), which enables an array of colorimetric detection methods. When AuNPs were functionalized with cysteine, its dimer cystine, or the cysteine-derived tripeptide, glutathione, three different mechanisms of aggregation were observed. Both cysteine and glutathione induced aggregation of AuNPs without further pH modification: the first by interparticle zwitterionic interaction and the second by interparticle hydrogen bonding. Cystine, however, did not induce aggregation, although it dissociated into two cysteinate moieties upon adsorption on the AuNPs, which appear to be chemically identical to cysteinate produced from cysteine adsorption. We show that the difference is due to the lower coverage of cysteinate from cystine and differences in charge states of the adsorbates. On modifying the pH to 1.5, the surface species become cationic (neutral COOH and protonated NH3+), and aggregation of cystine/AuNPs occurs immediately by interparticle hydrogen bonding. Thus, cysteine may induce aggregation by neutral hydrogen bonding or zwitterionic interaction between nanoparticles, but the mechanism depends sensitively on a number of parameters.

1. INTRODUCTION Gold nanoparticles (AuNPs) are important nanotechnological materials that have found application in a range of biosensing applications. Understanding how simple biomolecules such as amino acids, DNA bases, and simple peptides interact with AuNPs is critical to the design of systems composed of more complex molecules such as proteins and DNA strands, or in sensing devices.1−6 Cysteine (Cys) has a particularly high affinity for gold due to its sulfhydryl (thiol) side chain (Figure 1A), which enables bonding of Cys-containing peptides and proteins to metal surfaces.7−9 Cys has been used as a crosslinker for the attachment of proteins to gold substrates10,11 and is the basis for several biosensors, often in combination with AuNPs, because it still retains biofunctionality through the amine and carboxylic groups.11−17 Due to the biological importance of Cys there are also several sensors designed for its detection, again often involving AuNPs.18−21 AuNPs functionalized with Cys are known to self-assemble into aggregated networks.6,22,23 Cys-induced AuNP aggregation is usually attributed to the formation of zwitterionic networks involving head-to-head interaction of the deprotonated carboxylate (COO−) and protonated amine (NH3+) groups © 2014 American Chemical Society

of one AuNP-bound Cys with the opposite groups of Cys adsorbed on adjacent particles.6,19 Some guidance to the Cysgold surface chemistry of AuNPs can be obtained from studies of Cys adsorbed on bulk gold (single and polycrystalline), which have indicated that two forms of Cys are present on the surface (neutral and zwitterionic) when deposited from the gas phase or from solution.24−28 For Cys deposited on Au(110) at low coverage, the amounts of zwitterionic and neutral Cys were approximately equal, but with increasing coverage the neutral form saturated while the zwitterionic form continued to increase.26 Furthermore, as coverage increased, the adsorbed Cys formed paired zwitterionic rows along the [11̅0] direction, accounting for the increasing concentration of the zwitterionic species.29 Pairing has also been observed in a racemic mixture of L- and D-Cys on Au(110) by Kühnle et al.30 It has also been suggested by Ihs and Liedberg31 that Cys adsorbs as a fully protonated cation when deposited from unbuffered (pH ∼ 5.7) and acidic (pH 1.5) solution and as the fully deprotonated Received: March 10, 2014 Revised: April 17, 2014 Published: April 22, 2014 10481

dx.doi.org/10.1021/jp502401w | J. Phys. Chem. C 2014, 118, 10481−10487

The Journal of Physical Chemistry C

Article

beamline where this work was done,43−48 and this study is a natural extension of this work to AuNPs.

2. METHODS 2.1. AuNP Synthesis. AuNPs were produced by reduction of HAuCl4 by trisodium citrate in ultrapure water (18.2 MΩ· cm, Milli-Q) in a variation of the Turkevich49 and Frens50 methods, as detailed below. First a 4% (w/v) solution of HAuCl4 was produced by dissolution of AuCl3 (Alfa Aesar, 64.4% min purity) in 0.5% HCl (produced by dilution of 37% HCl from Carlo Erba Reagents). Second, a 1% (w/v) solution of trisodium citrate was produced by dissolution of solid trisodium citrate (Alfa Aesar, 99%) in ultrapure water. A total of 0.1 mL of 4% HAuCl4 was added to 40 mL of ultrapure water while stirring, resulting in a 0.01% (w/v) solution that was heated while 1 mL of the trisodium citrate solution was added dropwise. After 2−3 min the solution changed from its original light yellow to gray, then purple, and finally a ruby red color. After the color changed to red, the solution was boiled for a further 10 min. After cooling, the AuNP solution was filtered through a 0.22 μm syringe filter. The concentration of the AuNP solution was estimated to be 3.4 × 10−6 M, based on a first-principles calculation51 using the average AuNP dimension (17 nm), as determined from TEM (see below). Specifically, the number of Au atoms per nanoparticle (N) was calculated from eq 1, where ρ is the density of Au (fcc, 19.3 g/cm3), M is the atomic weight of Au (197 g/mol), and D is the AuNP diameter. Then the AuNP concentration, C, can be calculated from eq 2, where Ntotal is the total amount of Au atoms (determined from the mass of Au salt added), V is the solution volume, and NA is Avogadro’s number.

Figure 1. Structures of (A) cysteine (Cys), (B) cystine, and (C) glutathione (GSH).

anion in basic (pH 11.5) solution, but Shin et al.24 concluded that Cys deposited on Au(111) in vacuum was entirely zwitterionic. The dimer cystine consists of two Cys molecules joined via a disulfide bond (Figure 1B) and is also an important component in proteins. Zhang et al.10 observed that both Cys and cystine formed highly ordered self-assembled monolayers (SAMs) on Au(111), with 2D superstructures of adjacent molecules in both cases. In contrast, for electrochemical adsorption Hager and Brolo32 studied the desorption behavior of Cys and cystine on Au(111) under potential control in the presence of electrolytes and concluded that each species has a distinct adsorption and desorption potential, implying that the interactions of the two species with the surface were not equivalent. They further posited that SAMs of Cys have a higher density than those formed by cystine. Like Cys, glutathione (GSH, Figure 1C) has been shown to induce AuNP aggregation19,33−35 and is employed in several biosensors14,19,20,36−38 (both as the sensing target and as a component in the systems) and drug delivery applications.39,40 The mechanism of aggregation is controversial: Lim et al.33 found that the main aggregation method was via hydrogen bonding between the carboxylic groups of GSH adsorbed on adjacent particles, but Sudeep et al.19 and Zhang et al.,34 studying functionalized gold nanorods, concluded that zwitterionic interaction is the principle aggregation mechanism. Vallée et al.41,42 investigated GSH adsorbed on Au(111) via UHV evaporation and observed both neutral and zwitterionic states. When adsorbed from solution, the SAMs existed in the same ionic state on the surface as in solution: cationic at pH 1.1, zwitterionic at pH 6.3 and anionic at pH 12. In this study, soft X-ray photoelectron spectroscopy (SXPS) is used to investigate the adsorption from solution of Cys, cystine, and GSH on AuNPs, followed by drying. For comparison, Cys has been adsorbed on Au(110) from solution. SXPS is a useful technique for the study of biomolecules on metal surfaces, allowing the nature of the surface bonds and the chemical state of the functional groups to be determined. Several studies of biomolecules adsorbed on crystals of gold and other inorganic surfaces have been conducted at the

N=

π ρD 3 6 M

(1)

C=

Ntotal NVNA

(2)

Before reaction with biomolecules the AuNP solution was dialyzed in order to remove unreacted reagents and ions. Dialysis was conducted at room temperature in ultrapure water, using 10 kDa cellulose ester (CE) biotech dialysis membranes purchased from Spectra/Por. The dialysis period was 24 h with at least three water changes over this period. The AuNP/water ratio was approximately 10 mL/1 L or better, typically ∼20 mL in 3 L. The AuNP solution did not change color during dialysis and the dialyzed solution was analyzed using UV−vis spectroscopy from which a characteristic single peak at ∼520 nm was observed (Figure 2). 2.2. AuNP Functionalization. Solutions of biomolecules were prepared by dissolution of the corresponding solid in ultrapure water at concentrations of 1 × 10−2 M (Cys and GSH), while L-cystine was prepared as a saturated solution (∼1 × 10−3 M) due to its solubility limit.52 The reactions with AuNPs were carried out by mixing the biomolecule solution with AuNP solution in a 1:1 ratio and leaving the solution to react for 24 h, unstirred at room temperature. Following the 24 h reaction, the Cys/AuNP and cystine/AuNP samples were dialyzed to remove unreacted molecules, as described in the Supporting Information. When Cys was reacted with AuNPs there was a clear color change observed in the Cys/AuNP solution from the ruby red color of AuNPs to a dark purple (Figure 3) and UV−vis spectroscopy 10482



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nm (Figure 2), indicating a large degree of aggregation. As the reaction continued the AuNPs aggregated so much that they were visible to the naked eye and precipitated out of solution (resulting in a colorless solution). Due to the precipitation, it was not possible to subject this solution to dialysis. In order to remove the unreacted GSH, most of the solution was removed and the remaining AuNPs were diluted in ultrapure water. Rinsing was repeated three times after allowing the particles to settle. GSH-functionalized AuNPs were concentrated by gravity in the end of a Pasteur pipet for deposition onto the graphite substrate, resulting in a much denser patch than for the other molecules used in this study. The pH of the GSH/AuNP solution was 2.5 ± 0.1. While the cysteine and glutathione functionalized samples aggregated without pH modification, the cystine functionalized sample did not aggregate. The apparent color change with respect to the untreated AuNPs is due to dilution, and no shift in the UV/vis absorption peak was observed. On changing the pH of the cystine-treated sample to 1.5 by dropwise addition of HCl, the sample immediately aggregated, changing color initially to dark blue and forming black precipitated particles after several hours of incubation, similar to the aggregation of GSH/AuNPs. The ionic states of Cys, cystine, and GSH at various pH values, based on published pKa values6,42,54 are calculated in the Supporting Information and show that, at the unmodified pH values used in this study, Cys and cystine are zwitterionic in solution, while GSH is a mixture of cationic and zwitterionic states (Figures 2 and 3 of the Supporting Information). Cystine at the modified pH of 1.5 is mostly cationic, but some zwitterionic character remains. 2.3. TEM Characterization. Nanoparticle size, morphology, and structure were studied by diffraction contrast transmission electron microscopy (TEM) and high resolution TEM (HRTEM) experiments along with the relevant diffractograms by using a JEOL 2010F UHR TEM/STEM fieldemission gun electron microscope, operating at 200 kV with a measured objective lens spherical aberration coefficient Cs of 0.47 ± 0.01 mm and relevant spatial resolution at optimum defocus in HRTEM of 0.19 nm. The specimens for TEM analyses were prepared by depositing a droplet of dialyzed AuNP solution onto a carbon-coated copper grid and allowing the solution to evaporate, leaving AuNPs behind. The morphology of the dialyzed samples was analyzed by transmission electron microscopy (TEM), Figure 4. Assuming approximately ellipsoidal projected shapes and measuring the

Figure 2. UV−vis spectra of AuNP, Cys/AuNP, cystine/AuNP, and GSH/AuNP solutions. GSH/AuNP was analyzed immediately after reaction, while the other solutions were analyzed after dialysis. See text for explanation.

Figure 3. Photograph of AuNP, Cys/AuNP, cystine/AuNP, and GSH/AuNP solutions. GSH/AuNP was photographed immediately after reaction, while the other solutions were photographed after dialysis.

shows a broadening of the peak at 520 nm with new broad peak observed at ∼590 nm due to a bathochromic shift (Figure 2), indicating that aggregation has occurred6,19,33,53 while cystine/ AuNP only showed a lightening due to the dilution of the AuNP solution and showed no shift in the absorption peak position. The pH values of the resulting solutions were 5.8 ± 0.1 for Cys/AuNP and 6.3 ± 0.1 for cystine/AuNP. To analyses the Cys and cystine AuNP solutions with soft X-ray spectroscopy, they were drop cast onto freshly cleaved high purity graphite while being gently heated (∼60 °C) to accelerate evaporation. When the glutathione solution was added to the AuNP colloid there was an immediate color change to a dark blue (Figure 3) and a large bathochromic shift of the absorption peak to ∼650 nm, with only a small shoulder remaining at 520

Figure 4. TEM micrographs of dialyzed AuNPs: (A) Low magnification diffraction contrast image (scale 50 nm). (B) High resolution TEM (HRTEM) image of representative particles (scale 5 nm). (C) HRTEM image (scale 5 nm), close to the ⟨110⟩ zone axis, showing the different domains of the icosahedral particle and the relevant twinned regions whose orientation is shown in (D) diffractogram of the particle in (C), some of the reciprocal space vectors are marked in the diffractogram. Each sector of the particle is oriented around the ⟨110⟩ zone axis of the fcc Au lattice. 10483



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major and minor axis dimensions, most of the nanoparticles have a diameter of 14−17 nm and the particle size statistics are presented as a histogram in Figure 5 below. The majority of

3. RESULTS AND DISCUSSION Figure 6 shows the N 1s core level photoemission spectra of the AuNP samples, together with the spectrum of cysteine on

Figure 5. Histogram of particle dimensions assuming elliptical approximations of the particle’s projected shape in the TEM micrographs. Top: Minor ellipse axis; Bottom: Major ellipse axis.

Figure 6. N 1s spectra of (A) cysteine adsorbed on Au(110) from solution, (B) cysteine adsorbed on AuNPs, (C) cystine (dimer) adsorbed on AuNPs, (D) glutathione adsorbed on AuNPs. Photon energy 500 eV.

Au(110), and the binding energies and relative intensities of the peaks are summarized in Table 1. Two clear peaks are observed

particles exhibit an icosahedral shape but some particles also exhibit defect structures such as twinning planes and higher index facets, consistent with the truncated icosahedra described by Ascencio et al.55 2.4. Au(110) Functionalization. Before deposition, the Au(110) crystal (10 mm diameter disc, 2 mm thickness, supplied by MaTeck) was cleaned in UHV by repeated cycles of Ar+ sputtering (1 keV) and annealing at 673−773 K. After each cycle, the cleanliness was monitored by LEED and XPS. After cleaning, the levels of contaminants (C, N, O) were below detection limits. Deposition of L-cysteine onto Au(110) was carried out in a pure nitrogen atmosphere in a glovebag attached to the load lock of the end station. A droplet of saturated L-cysteine solution was placed onto the Au(110) surface for 2 min and then rinsed off with ultrapure water and dried under a stream of N2 (boil-off from liquid N2) and transferred back into UHV without leaving the glovebag. The sample was flashed to 350 K to desorb weakly bound overlayers and this resulted in a 3.5 Å thick layer (as determined from the attenuation of the Au 4f peak) and is taken as monolayer coverage here. 2.5. XPS Analysis. XPS analysis was conducted at the Materials Science Beamline (MSB), Elettra-Sincrotrone, Trieste, Italy.56 N 1s spectra for both the Au(110) and the AuNP samples were collected in normal emission (NE) geometry (60° incidence/0° emission) using photon energy hν = 500 eV with a combined resolution (beamline + analyzer) of 0.45 eV.

Table 1. Binding Energies, Assignments, and Relative Areas of the Two Fitted Peaks (N1 and N2) of AuNPs Functionalized with Cysteine, Cystine, and GSHa sample cysteine/ AuNPs cystine/ AuNPs GSH/AuNPs cysteine/ Au(110)

peak

binding energy (eV) ± 0.1

area (%)

ratio N 1s/ Au 4f (×100)

N1

399.7

56

3.06

N2 N1

401.5 399.8

44 75

2.39

N2 N1 N2 N1

401.4 400.1 401.5 399.5

25 82 18 26

N2

401.5

74

5.35 1.10

a

The data for cysteine adsorbed on Au(110) is also included. The ratio of N 1s to Au 4f intensity (by total area) is shown in the fifth column.

in the N 1s spectra of all samples: N1 located at about 399.7 eV and N2 at about 401.5 eV binding energy. The peak positions of N1 and N2 for Au(110) are consistent with results obtained by Gonella et al.26 for Cys deposited onto Au(110) in UHV, and by Cavalleri et al.27 for Cys adsorbed onto thin Au(111) films on Si substrates. N1 is assigned to the neutral form of the amino group (NH2) and N2 is assigned to zwitterionic/ 10484



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protonated amine (NH3+). The presence of two different ionic states (zwitterionic and neutral) is also consistent with studies conducted using IR spectroscopy and other techniques.24,31,57 We note that the ratio of N1 to N2 intensity is not the same for Cys adsorbed on Au(110) and AuNPs, and this may have two origins. First, the crystal surface is flat, facilitating intermolecular interaction, and with an absence of defects that may influence the chemical state of the adsorbates. Second, the AuNPs are aggregated so that at least part of the signal may come from molecules that are engaged in interparticle linkages, which may also influence the chemical state. The N 1s/Au 4f ratio is significantly lower for Au(110), but we do not believe this indicates a lower coverage. Instead we ascribe it to a simple geometrical effect: for the flat crystal surface all of the Au 4f electrons which are emitted normal to the surface have the minimum possible path length through the adsorbate. For the roughly spherical AuNPs, the Au 4f signal is emitted at a range of angles from normal to grazing angles, so the signal is considerably more attenuated. We conclude that the coverage is similar on both samples. For the continuous substrate of AuNPs considered by Caprile et al.58 the peak ratio was different, with the neutral peak dominating by 50−100% over the zwitterionic peak and this difference was attributed to less zwitterionic 2D network formation.58 Since the reaction with cysteine in the present study was conducted by mixing the AuNP colloid with cysteine solution in a 1:1 ratio (rather than by adding a droplet of cysteine to a continuous surface of AuNPs fixed on graphite), we propose that the mobility of AuNPs in solution (compared to immobilized particles on a substrate) allowed the formation of zwitterionic networks between AuNPs and resulted in the observed aggregation. As mentioned above, from the data in the literature it is expected that the adsorption of cysteine and cystine produce the same chemical species on the surface of gold, at least when adsorbed in vacuum.10 In addition, our S 2p spectra (see Supporting Information) demonstrate that the cystine does dissociate and adsorb as monomers, but adsorption of the first compound (Cys) in solution on AuNPs induces aggregation, while the second (cystine) does not. Furthermore, the surface coverage is lower for cystine adsorption than for cysteine, as implied by the ratio of N 1s to Au 4f intensity, consistent with the observations of Hager and Brolo32 that Cys produces a denser layer than cystine. This gives rise to fewer sites for interparticle zwitterionic interaction, but this is not the complete explanation for the lack of aggregation. The N 1s spectra show that the cysteinate in cystine/AuNPs has a higher proportion of neutral species (75%) than the Cys/AuNPs (56%). How can these results be rationalized? We explain the lower coverage by the necessity for a larger area site for the transition state between cystine in solution and the adsorbed state of two monomers. A small ensemble of a few Au atoms is likely to be sufficient for Cys to adsorb and lose H, with the amino and carboxylic acid groups pointing away from the surface. The S−S dimer bond may also need only a few Au atoms as a dissociation site, but it is likely that the group needs to be located nearly parallel to the surface, due to the steric requirements of the rest of the molecule. This implies that the relatively bulky amino and carboxylic groups will be sterically hindered by other cysteinate adsorbates. Calculations8,59 indicate that at lower adsorbate density, the amino nitrogen interacts with the surface, and this is consistent

with the studies of Cys on Au(110), where a higher population of neutral molecules is observed at lower coverage.29,30 This weak interaction evidently stabilizes the neutral species and explains why the lower coverage cystine/AuNPs system has a higher proportion of neutral nitrogen atoms. Thus, both the lower adsorbate density and different charge state contribute to preventing aggregation. Altering the pH, however, induced immediate aggregation by changing the charge state of the carboxylic groups, proving that the behavior is not simply a result of lower density.

4. CONCLUSIONS In conclusion, we have shown that cysteinate on AuNPs behaves differently depending on whether it is derived from Cys or cystine, and this influences the aggregation behavior through two mechanisms: first by absolute coverage, and second, an increase of amino nitrogen interaction with the surface, which stabilizes the neutral rather than the zwitterionic species. GSH might be expected to be similar since it causes aggregation, and given that adsorption occurs via the thiol of the cysteine residue, but in fact the mechanism of aggregation is quite different, and is based on hydrogen bonding, due to the ionic state of the molecules at the working pH. Previous studies of single crystal systems and our own data for Au(110) are useful for providing qualitative guidance to the adsorption mechanisms and charge states.

■

ASSOCIATED CONTENT

S Supporting Information *

Calculation of ionic state mole fractions, and S 2p spectra are presented. This material is available free of charge via the Internet at http://pubs.acs.org.

■

AUTHOR INFORMATION

Corresponding Author

*Tel.: +39 040 375 8458. E-mail: [email protected]. Notes

The authors declare no competing financial interest.

■ ■

ACKNOWLEDGMENTS We thank our colleagues at Elettra for providing high quality synchrotron light. REFERENCES

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Mechanisms of Aggregation of Cysteine Functionalized Gold

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