Article pubs.acs.org/Langmuir
Histidine Adsorption on TiO2 Nanoparticles: An Integrated Spectroscopic, Thermodynamic, and Molecular-Based Approach toward Understanding Nano−Bio Interactions Imali A. Mudunkotuwa and Vicki H. Grassian* Department of Chemistry, University of Iowa, Iowa City, Iowa 52242, United States S Supporting Information *
ABSTRACT: Nanoparticles in biological media form dynamic entities as a result of competitive adsorption of proteins on nanoparticle surfaces called protein coronas. The protein affinity toward nanoparticle surfaces potentially depends on the constituent amino acid side chains which are on the protein exterior and thus exposed to the solution and available for interaction. Therefore, studying the adsorption of individual amino acids on nanoparticle surfaces can provide valuable insights into the overall evolution of nanoparticles in solution and the protein corona that forms. In the current study, the surface adsorption of L-histidine on TiO2 nanoparticles with a diameter of 5 nm at pH 7.4 (physiological pH) is studied from both macroscopic and molecular perspectives. Quantitative adsorption measurements of L-histidine on 5 nm TiO2 particles yield maximum adsorption coverage of 6.2 ± 0.3 × 1013 molecules cm−2 at 293 K and pH 7.4. These quantitative adsorption measurements also yield values for the equilibrium constant and free energy of adsorption of K = 4.3 ± 0.5 × 102 L mol−1 and ΔG = −14.8 ± 0.3 kJ mol−1, respectively. Detailed analysis of the adsorption between histidine and 5 nm TiO2 nanoparticle surfaces with attenuated total reflectance Fourier transform infrared (ATR-FTIR) spectroscopy indicates both the imidazole side chain and the amine group interacting with the nanoparticle surface and the adsorption to be reversible. The adsorption results in no change in surface charge and therefore does not change nanoparticle−nanoparticle interactions and thus aggregation behavior of these 5 nm TiO2 nanoparticles in aqueous solution.
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INTRODUCTION The field of nanoscience and nanotechnology continues to grow with superior materials being fabricated for a broad range of applications in industry, energy and health.1−4 The inherent size-dependent chemical, mechanical, optical, electrical, magnetic, electro-optical, and magneto-optical properties, that differ from their bulk counterparts, render these materials to be of great interest from many scientific and application-based perspectives.5 The unique behavior arises in part from the large contribution of the surface free energy to the total free energy as a result of the high surface-to-volume ratio of the constituent atoms in nanomaterials.6 From a medical and diagnostic perspective, these materials are attractive candidates in reaching inaccessible targets (e.g., the brain) and interacting with cellular machinery.7 Therefore, with increased usage both intentional and unintentional exposure to nanomaterials is inevitable.8 Consequently, it is of vital importance that design of safe nanomaterials and safety assessment of existing materials are conducted in parallel to the development of applications.9 Understanding the interactions at the nano−bio interface plays a key role in this process and in the sustainable development of nanoscience and nanotechnology.10−12 The formation of a “protein corona” is well established in the literature for nanoparticles in biological media which result from the competitive adsorption of proteins on nanoparticle surfaces.13,14 This can cause changes in nanoparticle interfacial © 2014 American Chemical Society
properties and aggregation state while altering the biological identity of the nanoparticles that affect their fate within cells and tissues.15,16 The protein corona is a dynamic entity where at the initial stage high abundance low affinity proteins bind to the primary nanoparticle surface which exchange over time with lower abundant high affinity proteins.15,17,18 Both thermodynamic and kinetics play a role in protein adsorption and determining the final constituents of the corona. Therefore, irrespective of the several thousand proteins present in biological fluid, the protein corona is enriched with a significantly lower number, about 10−50 proteins, with the highest affinity proteins binding to nanoparticles at equilibrium.15,19,20 To follow the evolution of the protein corona and to better understand the final state reached at equilibrium, an important focus that needs further attention is the interaction of individual amino acids at the nanoparticle surface. Protein affinities toward nanomaterials are dependent on the number of domains present that have attractive interactions with the nanoparticle surface.21 These “domains” are specific portions of the protein that are rich in particular amino acids. For example, high molecular weight kininogen adsorbs onto iron oxide nanoReceived: March 24, 2014 Revised: June 29, 2014 Published: June 30, 2014 8751
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the impact of histidine adsorption on particle mobility. The findings of the current study are expected to contribute toward bridging the gap between protein corona evolution and interactions at the molecule−surface interface in aqueous matrices. Furthermore, this information is also useful in biocompatible nanomaterial synthesis where amino acids are used to control size and morphology as well as stabilizing agents and in understanding surface adsorption of proteins in cell media.40−44
particles via domain 5 which is rich in histidine. Another aspect of importance is the hydrophobicity/hydrophilicity of the nanoparticle surface which is determined by the presence of polar functional groups (e.g., surface hydroxyl groups on oxide surfaces).10,22 Based on this, surface interactions with biomolecules can vary significantly. Shrivastava et al. has explicitly shown with the use of NMR spectroscopy and a combined proteomics−mass spectrometry approach that acylphosphatase (AcP) enzyme has a preferential binding domain and orientation on silica nanoparticle surfaces. The surface interactions were found to occur via predominantly hydrophobic and basic amino acids from the two α-helices of the enzyme protein.23 Furthermore, amino acid side chains are responsible for stabilizing higher order secondary structures of proteins.10 When specific domains interact with nanoparticles with high curvature, this can cause an unfolding or distortion of the protein secondary structure.14,24,25 This can lead to new catalytic sites that become exposed and/or the deformation of existing catalytic sites that may trigger undesirable biological responses. Since conformational changes in the proteins are typically irreversible even under conditions where the adsorption may be a reversible process, protein adsorption can affect physiological function of the protein even once it is desorbed or displaced back into solution.26,27 Therefore, to better understand the adsorption of proteins and the impact that surface adsorption can have on protein structure, a comprehensive understanding of amino acid−nanoparticle interactions is required.28,29 Histidine is an essential amino acid with a side chain pKa close to physiological pH, with pKa2 6.04. This enables ready exchange of protons with respect to small changes in the medium pH that affect the charged state of the side chain. Additionally, the neutral imidazole ring of histidine can undergo tautomerization with ring flips (rotamerization) to interconvert between protonated and deprotonated forms with negligible changes in the space occupied by the ring which is generally important for protein function.30 Furthermore, Lhistidine is known to complex effectively with transition metal ions in the solution. These structural and chemical properties of histidine are utilized by biological systems, and as a result it is found in a large number of metalloproteins, ion channels, and enzyme active sites. It is also a precursor of histamine, a biogenic amine that triggers local immune responses.31−33 Since TiO2 nanoparticles are used heavily in cosmetics, construction materials, medical applications, and energy storage devices, and in the year 2010 the nanoscale TiO2 production was estimated to be 5000 tons (and expected to increase), there is the potential for histidine−TiO2 nanoparticle interactions to occur.3,34−36 Although a large number of toxicological studies have been conducted to assess the safety of TiO2 nanoparticles, fundamental information on how nanoscale TiO2 interacts with biological molecules remains sparse especially under aqueous conditions.37−39 This knowledge is necessary to understand structure−function relationships, which aid in improving their applications and potentially safe design. Therefore, to obtain a comprehensive understanding of the adsorption processes at the molecule−surface interface, spectroscopic analysis was conducted using attenuated total reflection Fourier transform infrared (ATR-FTIR) spectroscopy along with quantitative adsorption measurements to obtain the thermodynamic parameters on the histidine−TiO2 nanoparticle model system. Nanoparticle aggregation was also measured using dynamic light scattering techniques to analyze
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EXPERIMENTAL METHODS
Attenuated Total Reflectance Fourier Transform Infrared (ATR-FTIR) Spectroscopic Analysis of Solution Phase Adsorption. Molecular level insights of L-histidine adsorption on TiO2 nanoparticles were investigated using ATR-FTIR spectroscopy. The following protocol was used to carry out the experiments. A suspension of TiO2 NPs (1 mL of 1.5 mg/mL) was directly deposited on the horizontal AMTIR crystal and dried overnight. Once dried, the surface was covered with a flow cell (1 mL) connected to a peristaltic pump and flushed with water (pH 7.4, ∼1 mL/min) to eliminate loosely bound particles, and then the background spectrum was collected. A solution of histidine (0.5 mM at pH 7.4) was then introduced in the flow system, and single beam ATR-FTIR spectra were collected as a function of time at 4 cm−1 resolution for 30 h. Each single beam spectrum was referenced to the background water spectrum to obtain the absorbance spectrum. This process then removes contributions from the water bending mode [δ(H2O)] around 1640 cm−1. In preliminary studies, solution phase spectra were collected in the absence of TiO2 nanoparticle film at 5, 10, 50, 100, and 250 mM concentrations where peaks were observed only when histidine concentrations were above 10 mM. Thus, there is no solution phase contribution toward the spectral intensity for the adsorbed species when concentration below 10 mM is used. In this study, 0.5 mM histidine concentration is therefore well below that value. The side chain contributions of histidine in solution phase are identified by comparing with the spectra of glycine. To distinguish between the structural changes taking place upon protonation−deprotonation of the histidine functional groups, solution phase spectra were collected as a function of pH. Furthermore, to identify possible formation of peptide bonds, adsorption of his-gly peptide on TiO2 NPs was investigated as well. The extent of reversible adsorption was investigated by introducing pure water (pH 7.4) for 1 h after the adsorption experiments. All experiments were conducted in triplicate. HPLC Analysis of Solution Phase Adsorption. Quantitative adsorption studies of histidine on TiO2 nanoparticles were conducted according to previous studies but with slight modification.45 Briefly, TiO2 nanoparticles (2 g/L) were added to a series of histidine solutions (0.01−8.0 mM) and mixed for 24 h to achieve the adsorption equilibrium. From the supernatant, aliquots (1 mL) were withdrawn, filtered (Xpertec, 2 μm pore), centrifuged at 22 000 rpm for 30 min to remove any unfiltered particles, and analyzed for remaining histidine using HPLC (Dionex Ultimate 3000) equipped with a UV−vis detector (λ = 210 nm). The mobile phase consisted of 40 mM Na2SO4 (pH 2.65 adjusted with methanesulfonic acid). The adsorbed histidine was calculated by determining the difference between the initial and final solution phase concentrations. Experiments were conducted as a function of temperature (293, 298, 303, 310, and 320 (±0.5) K) to get additional thermodynamic data. To investigate the role of ionic strength, quantitative histidine adsorption measurements were also conducted as a function of ionic strength at 1 mM histidine. All experiments were conducted in triplicate. Dynamic Light Scattering (DLS) Aggregation Measurements. The aggregation behavior of TiO2 nanoparticles in the presence of histidine was investigated using a Beckman Coulter Delsa Nano Submicron particle analyzer. The hydrodynamic diameter and the zeta potential of TiO2 NPs (0.01 g/L) at pH 7.4 were measured in the presence of increasing concentrations of histidine (0, 0.01, 0.1, 1.0, and 5.0 mM). TiO2 NPs stock solution (1 g/L) was sonicated (40% amplitude, 30 sec) to form uniform suspensions, and aliquots (50 μL) 8752
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Figure 1. Characterization of TiO2 nanoparticles. (a) XRD pattern and (b) TEM image. The single particle diameter average and standard deviation was obtained by determining the diameter for over 100 particles. The BET surface area given is an average of three replicate measurements. (c) ATR-FTIR characterization of the TiO2 nanoparticle films on the AMTIR crystal after drying overnight. Besides lattice vibrations at 830 and 920 cm−1, there are bands associated with O−H groups and adsorbed water on the surface (broad O−H stretch at 3200 cm−1 and O−H bending mode for adsorbed water at 1640 cm−1).
Figure 2. Solution phase speciation of histidine as a function of pH. (a) Molecular structures of histidine as a function of histidine deprotonation; where pKa1 = 1.70, pKa2 = 6.04, and pKa3 = 9.09. (b) Quantitative calculation of histidine speciation using the Henderson−Hasselbalch equation. (c) ATR-FTIR spectra of aqueous solutions of histidine (250 mM) as a function of pH: acidic (pH 1.6), neutral (pH 7.4), and basic (pH 10.0). ment shows a relatively narrow size distribution with a hydrodynamic diameter of 417 ± 52 nm. Sources of Nanomaterials and Chemicals. All experiments conducted herein used TiO2 nanoparticles purchased from Nanostructured and Amorphous Materials Inc. (Houston, TX). These
were added to the histidine solutions (5 mL) and allowed to equilibrate for 24 h under dark conditions. The ultrasonication of TiO2 nanoparticle stock suspension is used to break up any of the agglomerates so as to form a uniform suspension. DLS measurement is then taken immediately after the sonication process. This measure8753
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[νs(CC) + νs(CN)]ring + [δas(NH3+)] maximum originally at 1627 cm−1 shifts to 1600 cm−1 as the asymmetric carboxylate [νas(COO−)] stretch vibration grows in. Thus, according to literature assignments at pH 7.4, the peak corresponds to overlap of three vibrational modes, [νs(CC) + νs(CN)]ring + δas(NH3+) + νas(COO−).47,48 Furthermore, the broad band in the region extending from 1485 to 1550 cm−1 results from the overlap of the ring breathing mode; νs(CN) + δ(CH)]ring and the amine group symmetric bending mode; δs(NH3+).47,48 Changing the pH from pH 1.6 to pH 7.4 causes the peak maxima to shift from 1530 to 1512 cm−1, corresponding to the deprotonation of the imidazole group. Thus, according to literature assignments at pH 7.4, the peak corresponds to overlap of three vibrational modes, [νs(CC) + νs(CN)]ring + δas(NH3+) + νas(COO−).47,48 The IR spectra changes are seen under basic conditions as well. At pH 10.0, the broad peak near 1600 cm−1 split into three main components. With the change in pH 7.4 to pH 10.0, the only structural change that occurs is the deprotonation of the amine group. According to earlier studies, the deprotonated amine group has a scissor mode, δ(NH2), in the region between 1590 and 1650 cm−1.48 Additionally, the shoulder at 1497 cm−1 at pH 10 as a result of the deprotonation of the amine group can be attributed to the [νs(CC) + νs(CN)]ring vibration. Therefore, the band maximum appearing at 1562 cm−1 at the higher pH is assigned to the overlap between deprotonated amine group vibration and the imidazole ring vibration, whereas the peak at 1627 cm−1 observed in the spectrum collected at pH 1.6 is identified with the [νs(CC) + νs(CN)]ring vibration. Additional bands at 1441 and 1408 cm−1 correspond to δ(CH2) and νs(COO−), respectively, and the broad bands near 1343 and 1260 cm−1 result from the overlap of vibrational modes associated with the side chain CH2 groups, the imidazole ring, and the carboxylic/ carboxylate groups. Figure 3 illustrates the curve fits for the pH 7.4 solution phase according to the above discussion. The peak components
nanoparticles were characterized extensively with transmission electron microscopy (TEM), X-ray diffraction (XRD), and Brunauer−Emmett−Teller (BET) measurements. L-Histidine (SigmaAldrich 99.5% certified ACS plus) solutions were prepared using Optima water (Fisher Scientific). The pH was adjusted using NaOH (0.08 M, Fisher Scientific ACS plus) solution. The ionic strength studies were conducted in NaCl solutions (Sigma-Aldrich 99.5% certified ACS plus).
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RESULTS AND DISCUSSIONS Nanomaterial Characterization. TiO2 nanoparticles were extensively characterized with respect to size, shape, surface area, and crystalline phase present. The XRD pattern, TEM image, and ATR-FTIR spectra for these TiO2 nanoparticles are presented in Figure 1. According to Figure 1a, the crystalline phase is entirely anatase. TEM images show uniform particles with nearly spherical shape and an average diameter of 5 ± 1 nm as determined by the analysis of over 100 particles (Figure 1b). These images were obtained by sonicating (1 min) a dilute suspension of TiO2 nanoparticles (∼10 mg/L) and drying a droplet onto a TEM grid followed by imaging. As can be observed, the particles appear highly aggregated. This is to be expected, as these particles have high surface energies and undergo aggregation in order to minimize their energy. Particle diameters were determined considering particles near the edges of the aggregates, as they can be more clearly delineated as separate particles. The surface area of the particles as measured by BET N2 adsorption is 248 ± 4 m2/g. Analysis of Solution Phase Histidine ATR-FTIR Spectra under Physiological pH. Histidine consists of an imidazole ring (C3H4N2), an amine (NH2), and a carboxylic group (COOH). As shown in Figure 2a, these three functional groups can be protonated, and therefore, the speciation is sensitive to solution pH (Figure 2b). Structural changes of histidine as the protonation state changes as a function of pH can easily be observed in the ATR-FTIR spectra collected (Figure 2c). Because histidine has increased structural complexity with its imidazole side chain when compared to simple amino acids such as glycine, it is useful to compare the spectra of glycine to histidine. ATR-FTIR spectra of solution phase amino acids glycine and histidine at pH 7.4, provided in Supporting Information Figure S1, illustrate this fact. For glycine, peaks at 1600, 1510, 1441, 1408, and 1328 cm−1 correspond to [νas(COO−) + δas(NH3+)], δs(NH3+), δsc(CH2), νs(COO−), and γ(CH2) vibrations, respectively.46,47 Thus, this comparison allows for the identification of the broad bands in the histidine spectrum around 1600, 1512, 1346, and 1275 cm−1 to be associated with the side chain CH2 group and imidazole vibrations. According to Figure 2b, approximately 57% of the histidine molecules at pH 1.6 are completely protonated (H3-his) while in the remaining histidine (43%) the carboxylate group is deprotonated (H2-his). Therefore, the prominent peak at 1737 cm−1 results from the carbonyl stretch [νs(CO)] while the peak at 1627 cm−1 corresponds to the ring breathing mode; [νs(CC) + νs(CN)]ring and asymmetric bending mode of protonated amine group; [δas(NH3+)].47−49 Additionally, some contribution from the asymmetric carboxylate [νas(COO−)] stretch vibration can be observed by a shoulder at 1600 cm−1. As the pH increases to pH 7.4, approximately 93% of the histidine molecules are in the H1-his form where no protonated carboxylic functionality exists (Figure 2b). Correspondingly, νs(CO) at 1737 cm−1 diminishes in intensity and the
Figure 3. ATR-FTIR spectrum of aqueous solutions of histidine (250 mM) at pH 7.4. The spectrum has been curve fitted using a Gaussian− Lorentzian (GL30) line shape for each peak.
consist of Gaussian/Lorentzian line shape product with 70% Gaussian and 30% Lorentzian character (GL30). These vibrational mode assignments are summarized in Table 1. At pH 7.4, the overlapping bands around 1600 and 1512 cm−1 cannot be fully resolved. However, according to the literature and the pH dependent study, the peak component at 1637 cm−1 can potentially be attributed to the imidazole ring 8754
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Table 1. ATR-FTIR Spectroscopic Data for Solution Phase and Adsorbed Histidine at pH 7.4 vibrational frequency (cm−1) experimental values mode of vibration
a
νs(CO) [νs(CC) + νs(CN)]ring + νas(COO−) + δas(NH3+) [νs(CN) +δ(CH)]ring+ δs(NH3) δs(NH2) δ(CH2) νs(COO−) δ(C−OH) [νs(CN) + νs(C−N)]ring + δ(CH) [νs(C−N) + νs(C−C)]ring + γ(CH2) ν(C−N)ring + δ(C−H) a
solution 1600, 1637 1461,1512 1441 1408 1346 1265, 1290 1194, 1231
adsorbed
literature values for solution phase (refs 48−50)
1725 1588, 1617, 1642 1512 1552 1441 1388 1418 1338 1276 1230
1720−1740 1575−1640 1439−1550 1590−1650 1425−1475 1390−1425 1400−1420 1343−1345 1268−1270 1010−1265
νs/as, symmetric/asymmetric stretching vibration; δs/as, symmetric/asymmetric deformation/bending; γ, twisting vibration; δ, bending vibration.
Figure 4. ATR-FTIR spectra of (a) adsorbed histidine at a solution phase concentration of 0.5 mM and a pH of 7.4 as a function of time. Spectra are shown for t = 3, 30 min, 1, 6, 10, 15, and 30 h. (b) Curve fitted spectra using Gaussian−Lorentzian (GL30) line shape are shown for several selected times.
vibrations and while the 1600 cm−1 peak component may comprise of both δas(NH3+) and νas(COO−) vibrations thus appearing as a single, broad peak. Curve fitting of the solution phase spectrum was conducted mainly to compare with that of the adsorbed phase spectra which are much broader. Therefore, insights from the analysis of solution phase histidine can aid in the analysis of adsorbed histidine as discussed in below. ATR-FTIR Spectroscopy of Histidine Adsorption on TiO2 Nanoparticle Surfaces. ATR-FTIR spectra of TiO2 nanoparticles following histidine adsorption at a solution phase concentration of 0.5 mM and as a function of time are shown in Figure 4. The adsorbed phase spectra were collected over 30 h time period. In Figure 4, the spectral region from 1200 to 1800 cm−1 is shown. This is the region of the infrared where adsorbed histidine vibrations can be analyzed in detail with respect to the different moieties present as discussed above for the pH dependent solution phase data. The full infrared region from 800 to 3800 cm−1 for each of these spectra is shown in Supporting Information Figure S2. As already noted, at the low concentration used, that is, 0.5 mM, there is no significant
contribution of solution phase species to the adsorbate vibrational spectrum. Additionally, histidine adsorption showed to be reversible as the peaks diminished when water was flowed following the adsorption experiments. There are several significant differences between the solution phase (Figure 3) and adsorbate spectra (Figure 4a). For example, the relative intensity between νas(COO−) and the other vibrational modes show a significant reduction in intensity with the most prominent being that of the band at 1512 cm−1. This suggests there is a change in the absorption coefficient which can result due to interactions of the functional group with the surface which results in charge redistribution, changes in bond angles, bond distances, and symmetry upon adsorption. As already noted, vibrations associated with the imidazole ring and δ(NH3+) contribute toward bands observed within this spectral range. Temporal variations are also observed; peaks with initial maxima at 1611−1598 cm−1 shift and broaden over time and a new peak appearing at 1725 cm−1 is observed at higher coverage. Furthermore, there is a shoulder 8755
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observed at 1418 cm−1 on the broad peak centered at 1384 cm−1 after 6 h. To resolve the overlapping bands in the adsorbed phase and temporal variations, spectra collected over a period of time, at 3 min, 6, 15, and 30 h, are curve fit using a process similar to that for solution phase spectra, that is, using a Gaussian−Lorentzian (GL30) line shape. These data are shown in Figure 4b, and the corresponding peak assignments are summarized in Table 1. The broad band at 1611 cm−1 shifts to 1598 cm−1 over time. This band consists of possibly up to three vibrational components including a surface coordinated asymmetric (NH3+) stretch (1642 cm−1), the imidazole ring vibration (1617 cm−1), and the asymmetric stretch of carboxylate groups νas(COO−) at 1588 cm−1. Correspondingly, the νs(COO−) shows a broad peak at 1384 cm−1 with a shoulder at 1418 cm−1. According to the analysis of the solution phase spectra (see Figure 2c), the imidazole and amine group have vibrations with wavenumbers in the 1485−1550 cm−1 spectral region. Therefore, the components at 1512 and 1552 cm−1 , respectively, which have shifted, are due to surface complexation involving the amine and imidazole groups. Additionally, a new peak near 1725 cm−1 appears after 6 h and is observed even after 24 h. This is the wavenumber expected for the stretching mode of the carbonyl group. Since no carbonyl groups should exist at pH 7.4, the origin of this peak needs further consideration. One possibility is there is amide bond formation between the adsorbed histidine molecules. Furthermore, the reduction in the relative intensity of the band at 1512 cm−1 also suggests the possibility of the NH2 group undergoing reaction. Although amide bond formation between a carboxylic acid and an amine is an unfavorable process which requires activating the carboxylic group, the surface has the potential to provide a lower energy pathway. If peptide bond formation is occurring on the surface of these nanoparticles, it can have important biological implications. In this case, the peak observed at 1725 and 1552 cm−1 may result from the amide I and amide II vibrational modes. Thus, adsorption of his-gly peptide on TiO2 NPs was studied under the same conditions for comparison and the spectra for this dipeptide are shown in Supporting Information Figure S3. The reason for selecting this peptide was to have less complexity in the spectra so as to more readily and easily identify bonds associated with amide formation. Figure S3 shows the spectra for solution phase and the adsorbed phase peptide. There is no solution phase contribution at 0.5 mM, and no difference is observed between solution phase and adsorbed phase. In general, amide I and amide II peaks are observed at 1650 and 1545 cm−1, respectively, in proteins. However, in this dipeptide, the overlap of the νas(COO−) of the terminal carboxylate group with the amide II peak has resulted in a single broad band centered around 1574 cm−1 which does resemble the broad peak at 1598 cm−1 in adsorbed histidine. But the amide I peak for his-gly is at 1685 cm−1 which is significantly different from that for adsorbed histidine and thus confirms that the peak at 1725 cm−1 is not likely due to amide bond formation. Furthermore, the amide III region was not observed in the adsorbed histidine spectra. It is then concluded the peaks at 1552 and 1512 cm−1 are a result of surface complexed amine and imidazole group and this complexation causes a change in the relative intensities in the adsorbed phase spectra. Additionally, the new peak at 1725 cm−1 can be attributed to the concerted protonation and deprotonation of the carboxylate and amine groups, respec-
tively, for some of the adsorbed histidine molecules. This process can be facilitated by the surface hydroxyl groups as illustrated in Figure 5. The illustration shows the protonated
Figure 5. Cartoon representation of proposed adsorption modes of histidine on TiO2 nanoparticle surfaces. Amine groups H-bond to the surface which enables intramolecular proton transfer to the carboxylate group in some of the adsorbed histidine. Furthermore, the imidazole ring can interact with the surface Ti atoms via the π-orbitals and the amine group can form H-bonds with the surface O atoms (not shown).
amine group H-bonding with the surface oxygen which can then promote proton transfer to the carboxylate group resulting in a shoulder at 1418 cm−1 corresponding to δ(C−OH).48 The trend in peak maxima shift from 1611 to 1598 cm−1 is consistent with deprotonation of the amine group that resulted in the peak maxima shift from 1600 to 1562 cm−1 in the solution phase study (Figure 2c). In the curve fitting procedure, the δ(CH2) mode at 1441 cm−1 becomes more clearly identified and shows no significant peak shift. However, there are changes in the region 1150 to 1380 cm−1 corresponding to the imidazole ring breathing modes. In a study by Tsud et al., histidine adsorption on CeO2 was investigated by synchrotron radiation photoemission, resonant photoemission, and NEXAFS; histidine binding to the ceria surface was deduced to be via the anionic carboxylate and all three nitrogen atoms with the imidazole ring parallel to the surface.50 The N atom of the imidazole ring was found to interact strongly via the π-orbitals, while the amine N atom interacts with the oxide via its H atoms. Therefore, in addition to the possible H-bonding illustrated in Figure 5, this π-orbital interaction can also occur in for the histidine−TiO2 surface complex and with additional interaction with the amine (NH2) group. Adsorption Isotherms and Binding Affinity (K) for Histidine on 5 nm TiO2 Particles. Although the molecular details as analyzed above are complex, the quantitative adsorption studies of histidine on TiO2 at pH 7.4 show a Langmuir-like behavior with the initial uptake being linearly proportional to concentration and then leveling off at higher concentrations (Figure 6). Although there may be multiple binding sites and interactions between adsorbates, these structures may be similar in energy, and thus, Langmuir behavior is observed. Therefore, assuming monolayer adsorption of histidine on the TiO2 nanoparticle surface at pH 7.4 and it being reversible at 24 h, the experimental data can be fit using the Langmuir model, according to eq 1. Cads =
max KCads [Ceq ]
1 + K[Ceq ]
(1)
where Cads is adsorbed [histidine], Ceq is unbound [histidine] at the equilibrium, Cmax ads is saturation of [histidine], and K is the 8756
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which are H-bonded or coordinated with the surface. Therefore, it can be concluded that interactions between histidine and the surface are not only electrostatic in nature but in fact also occur through H-bonding or coordination as presented. Aggregation Behavior of TiO2 NPs in the Presence of Histidine. Aggregation plays a key role in determining the mobility, uptake, and dissolution behavior of nanoparticles.51,52 Therefore, the current study investigated any changes that may occur in the aggregation behavior of TiO2 nanoparticles upon adsorption of histidine. In the absence of histidine, TiO2 nanoparticles which were at 417 ± 52 nm immediately after sonication aggregated into particles with a hydrodynamic diameter of nearly half-micrometer in size, 434 ± 33 nm, after 24 h which is not unusual for nanoparticles as a result of their high surface energy. However, adsorption of ligand molecules can change the aggregation state and thus can impact the mobility.45 Ligand molecules can potentially diffuse into interparticle spaces of the aggregates, and in the case where there is higher affinity to the ligand, adsorption takes place. This can enhance, inhibit, or reverse the aggregation process by changing surface charge as well as steric interactions. Furthermore, sonication prior to the addition of ligand is considered to weaken the aggregate structure to facilitate diffusion of ligand molecules.45 However, in this case, in contrast to previous studies with citric acid as a ligand, aggregate size did not change significantly upon addition of histidine (Table 3). The zeta potential values for each of these
Figure 6. Adsorption isotherm for histidine on 4 nm TiO 2 nanoparticles at pH 7.4 and at a temperature of 293 K. These data have been fit according to the Langmuir adsorption model with Kads = 4.2 ± 0.5 × 102 L mol−1 and Cmax = 6.2 ± 0.3 × 1013 molecules cm−2.
equilibrium binding constant. From this analysis, the saturation concentration (Cmax ads ) and the equilibrium binding constant (K) of histidine were calculated to be 6.2 ± 0.3 × 1013 molecules cm−2 and 4.2 ± 0.5 × 102 L mol−1, respectively. Additionally, the free energy (ΔG) of histidine adsorption on 5 nm TiO2 particles can be calculated by (2)
ΔG = −RT ln K
Table 3. Hydrodynamic Diameter and Zeta Potential Measurements As a Function of Histidine Concentration Using DLS after 24 h
−1
to be −14.7 ± 0.3 kJ mol at 293 K. This value of the free energy is in accordance with a physisorption process. Therefore, it can be concluded that, in solution at pH 7.4, histidine is physisorbed on the TiO2 NPs. Also these thermodynamic parameters obtained from the quantitative adsorption studies suggest that the interaction between histidine and TiO2 nanoparticles to be H-bonding, dipole− dipole, and/or electrostatic interactions. Adsorption of histidine was further conducted at different temperatures, (293, 298, 303, 310, and 320 K) to obtain the enthalpy and the entropy changes associated with the adsorption process. The respective equilibrium constants and calculated free energies are given in Table 2. The thermodynamic parameters calculated from this
[histidine] mM 0 0.01 0.1 1 5
293 298 303 310 320
Kads (L mol−1) 4.2 3.3 3.0 1.9 1.9
± ± ± ± ±
0.5 0.5 0.5 0.2 0.5
× × × × ×
2
10 102 102 102 102
ΔG = −RT ln Kads (kJ mol−1) −14.7 −14.4 −14.4 −13.5 −13.9
± ± ± ± ±
± ± ± ± ±
33 82 34 54 36
zeta potential (mV) −36.0 −33.0 −30.7 −31.7 −32.6
± ± ± ± ±
2.6 3.7 2.4 2.9 2.6
solutions varied slightly but stayed within a small range of −36.0 ± 2.6 mV (0 mM histidine) to −30.7 ± 2.4 mV (0.1 mM histidine), indicating that no significant changes in the surface charge with histidine adsorption which is consistent with the lack of the change in aggregation behavior observed. The aggregation is controlled by the net interactive forces between particle surfaces, which depend on surface charge and steric repulsions.52−54 At pH 7.4, histidine is in its neutral from and therefore does not change the surface charge upon adsorption. Furthermore, the saturation coverage of histidine (6.2 ± 0.3 × 1013 molecules cm−2) indicates only a single layer of histidine is on the NPs surface. Therefore, the steric repulsions do not increase significantly upon histidine binding as well. The overall effect is to have no change in aggregation state upon adsorption of histidine.
Table 2. Temperature Dependent Adsorption Studies of Histidine at pH 7.4 T (K)
Dh (nm) 434 568 501 500 584
0.3 0.4 0.4 0.3 0.6
data showed an exothermic adsorption with ΔH = −24.5 ± 5.2 kJ mol−1 and ΔS = −0.03 ± 0.02 kJ mol−1 K−1. These values agree well with a typical physisorption process. Experiments conducted under different ionic strength conditions gave decreasing surface adsorption with increasing ionic strength initially and approached a constant value at the highest salt concentrations investigated (see Figure S4 in the Supporting Information). Histidine that adsorbs at high ionic strength is not bound electrostatically but consists of those
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CONCLUSIONS AND IMPLICATIONS The current study gives a detailed analysis of the adsorption of histidine on 5 nm TiO2 NPs in physiological pH aqueous solutions. The findings of this study are as follows: (1) The adsorption was observed to be reversible. Analysis using the Langmuir model gave an equilibrium binding constant and maximum adsorption for histidine on TiO2 NPs 8757
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of 4.2 ± 0.5 × 102 L mol−1 and 6.2 ± 0.3 × 1013 molecules cm−2, respectively, at pH 7.4 at a temperature of 293 K. (2) The free energy change associated with the adsorption was −14.7 ± 0.3 kJ mol−1 at 293 K. (3) Temperature dependent studies over the range of 293− 320 K gave enthalpy (ΔH) and entropy changes (ΔS) of −24.5 ± 5.2 and −0.03 ± 0.02 kJ mol−1 K−1, respectively. (4) From the spectroscopic data, it is proposed that the adsorption is somewhat more complex than a single configuration and that there are different modes of adsorption for histidine on the nanoparticle surface. Interactions occur between the imidazole side chain, the amine group via Hbonding, π-orbital interactions with the surface. (5) Bulk adsorption studies and surface charge measurements also indicate electrostatic interactions between the protonated amine group and the negatively charged surface occur but are not the only interactions. (6) Some of the adsorbed histidine has protonated carboxylic groups at higher pH values than expected when compared to protonated species in solution phase. This is a result of surface induced deprotonation of the amine group and proton transfer to the carboxylate group potentially mediated by surface hydroxyl groups. (7) The aggregation behavior as measured by DLS is shown to be unaffected by L-histidine adsorption as the surface charge did not change upon adsorption. This is in contrast to the studies of citric acid on TiO2 nanoparticles. A detailed understanding of amino acid residues allows for insights into understanding the complexity and challenges of dynamic changes and complex interactions with proteins at the nano−bio interface. An investigation of lysozyme adsorption on silica nanoparticles by Vertegel et al. clearly highlights the dependence of adsorption patterns, protein structure, and function on particle size.55 The changes in protein function were attributed to the decrease in α-helix content. In a more recent study using small-angle neutron scattering (SANS) and UV−vis spectroscopy, it was further shown the impact of pH and size on protein-mediated aggregation.56 Physiologically relevant tripeptide glutathione (GSH) was investigated in the presence of α-alumina nanoparticles which suggested exclusive electrostatic interactions via the carboxylate groups with the alumina surface.57 These studies can greatly benefit from individual amino acid−nanoparticle studies as the molecular level information provides greater potential toward designing biocompatible nanomaterial in a more controlled fashion.11 Furthermore, these single amino acid component and small peptide studies can be used in prediction models for more complex systems. Xia et al. has developed a biological surface adsorption index (BSAI) to characterize these interactions under biologically relevant aqueous conditions.58,59 In these studies, the adsorption coefficients are correlated to a set of solute descriptors (R, π, α, β, V) by log K i = c + rR i + pπi + aαi + bβi + vVi
amino acids on nanoparticle surfaces and specifically histidine. Koppen et al. have studied the adsorption configurations of cysteine, lysine, glutamic acid, and histidine on anatase (101) and (001) and rutile (110) and (100) using Carr−Parrinello simulations of aqueous solutions.60 The calculated adsorption energies of glutamic acid and lysine using these configurations are given as 160 and 110 kJ mol−1 for the rutile surface, while on the anatase surface it was reported to be largely dependent on the surface orientation. Feyer et al. used XPS and NEXAFS to study the adsorption of L-histidine from the gas phase on clean and oxygen coated Cu(110) surfaces at submonolayer, monolayer, and multilayer coverage.32 The spectra obtained have shown that at low coverage histidine interacts only via the carboxylate group and the imidazole N atoms, and as the coverage increases the molecules were randomly oriented. This study was followed by investigating the adsorption of histidine and histidine containing peptides on Au(111) that has shown chemisorption via the imidazole ring and carboxylate group. Furthermore, differences were observed between the gly-his-gly and gly-gly-his peptide spectra highlighting the influence of amino acid sequence on the bonding geometry.31 All of the experimental studies noted above are conducted under highly controlled, gas phase conditions which give insightful information on the amino acid−surface interactions. However, in terms of nanotoxicology, which deals with much more complex matrices and in aqueous environments, the applicability of gas-phase investigations in the absence of solvent effects become questionable especially for charged molecules.61 Therefore, the current study focuses on an experimental approach to understand the adsorption of histidine on TiO2 nanoparticle surfaces in aqueous solutions at physiological pH 7.4.
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ASSOCIATED CONTENT
S Supporting Information *
ATR-FTIR spectra of solution phase glycine, histidine, and hisgly peptide, full spectral range of adsorbed histidine, adsorbed his-gly peptide, and ionic strength dependence of histidine adsorption on TiO2. This material is available free of charge via the Internet at http://pubs.acs.org/.
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AUTHOR INFORMATION
Notes
Any opinions, findings and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation. The authors declare no competing financial interest. The authors declare no competing financial interest.
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ACKNOWLEDGMENTS This material is based on the work supported by the National Science Foundation under Grant CBET-1424502.
(3)
With known adsorption coefficients and regression analysis, the coefficients [r, p, b, v] can be derived which correspond to the hydrophobic, H-bond acidity/basicity, dipolarity/polarizability, and lone-pair interactions, respectively. The constant c is the electrostatic interactions which can be measured by the zeta potential. Therefore, bulk measurements along with microscopic analysis can allow for the validation of such models. Furthermore, several simulation and experimental studies have been conducted to understand the adsorption process of
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