Chiral Plasmonic Nanochains via the Self-Assembly of Gold Nanorods

Chiral Plasmonic Nanochains via the SelfAssembly of Gold Nanorods and Helical Glutathione Oligomers Facilitated by Cetyltrimethylammonium Bromide Micelles Jun Lu,† Yi-Xin Chang,† Ning-Ning Zhang,† Ying Wei,† Ai-Ju Li,† Jia Tai,† Yao Xue,† Zhao-Yi Wang,† Yang Yang,‡ Li Zhao,§ Zhong-Yuan Lu,†,∥ and Kun Liu*,† †

State Key Laboratory of Supramolecular Structure and Materials, College of Chemistry, Jilin University, Changchun 130012, P.R. China ‡ Department of Chemistry and Biochemistry and Department of Materials Science and Engineering, University of Maryland, College Park, Maryland 20742, United States § School of Life Sciences, Jilin University, Changchun 130012, P.R. China ∥ State Key Laboratory of Supramolecular Structure and Materials, Institute of Theoretical Chemistry, Jilin University, Changchun 130023, P.R. China S Supporting Information *

ABSTRACT: Gold nanorods are excellent anisotropic building blocks for plasmonic chiral nanostructures. The near-infrared plasmonic band of nanorods makes them highly desirable for biomedical applications such as chiral bioimaging and sensing, in which a strong circular dichroism (CD) signal is required. Chiral assemblies of gold nanorods induced by self-associating peptides are especially attractive for this purpose as they exhibit plasmonic-enhanced chiroptical activity. Here, we showed that the presence of cetyltrimethylammonium bromide (CTAB) micelles in a gold nanorod solution promoted the self-association of L-/D-glutathione (GSH) and significantly enhanced the chirality of the resulting plasmonic nanochains. Chiroptical signals for the ensemble in the presence of CTAB micelles were 20 times greater than those obtained below the critical micelle concentration of CTAB. The strong optical activity was attributed to the formation of helical GSH oligomers in the hydrophobic core of the CTAB micelles. The helical GSH oligomers led the nanorods to assemble in a chiral, end-to-end crossed fashion. The CD signal intensities were also proportional to the fraction of nanorods in the nanochains. In addition, finite-difference time-domain simulations agreed well with the experimental extinction and CD spectra. Our work demonstrated a substantial effect from the CTAB micelles on gold nanoparticle assemblies induced by biomolecules and showed the importance of size matching between the inorganic nanobuilding blocks and the chiral molecular templates (i.e., the GSH oligomers in the present case) in order to attain strong chiroptical activities. KEYWORDS: gold nanorods, cetyltrimethylammonium bromide, glutathione oligomer, chirality, plasmonic first involves top-down techniques such as electron beam lithography and focused-ion beam etching, which offers planar chiral patterns and relatively simple three-dimensional nanostructures with low throughput and resolution.7,8 By contrast, bottom-up approaches via the self-assembly of achiral inorganic

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lasmonic nanostructures with chiroptical properties hold promise in a wide range of applications involving chemical sensing,1 enantioselective separation,2 chiral catalysis,3 and optical materials,4−6 owing to a much stronger circular dichroism (CD) signal and broader spectral range compared with those in molecular systems. Rational design of chiroptical nanostructures has been of intense interest both experimentally and theoretically. Two general strategies have been considered for generating chiroptical nanostructures. The © 2017 American Chemical Society

Received: November 15, 2016 Accepted: March 15, 2017 Published: March 23, 2017 3463

DOI: 10.1021/acsnano.6b07697 ACS Nano 2017, 11, 3463−3475

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ACS Nano nanoparticles (NPs) in the presence of chiral organic molecules allow for large-scale, parallel productions of complex chiral nanostructures with nanoscale precision and remarkable tunability.9−15 An assembly of achiral NPs and chiral molecules can generate chiroptical activity mainly in two ways, namely, molecule dipole−plasmon chiral interaction between a NP and chiral molecules and NP−NP plasmon interaction between chirally arranged NPs.16,17 In the former case, plasmonic chiral activity arises from the Coulomb (dipole−dipole) coupling interaction between the oscillating electrons of a plasmonic nanoparticle and the chiral charge distribution of chiral molecules surrounding the nanoparticle.18−24 The effect from such coupling is expected to be rather weak, as strong chiroptical activity requires a high degree of chirality from the well-oriented, self-assembled monolayer of chiral molecules on the NP surface and considerable overlap between the plasmonic band of the metal NPs and the absorption band of the chiral molecules.10,25 In the latter case, relatively stronger chiroptical activity can be achieved by the collective chirality arising from the asymmetric spatial arrangement of achiral inorganic NP ensembles, typically formed using chiral molecular templates.26−32 The chiral nanostructure, distinguishable from its mirror image, exhibits enhanced chiroptical signals owing to much stronger dipolar Coulomb and electromagnetic interactions between the metal NPs. Among plasmonic nanoparticles studied, gold nanorods (Au NRs) have been extensively used for the assembly of chiral plasmonic nanostructures with strong chiroptical signals due to their excellent physical properties. Au NRs possess a longitudinal surface plasmon resonance (LSPR) in the visible to near-infrared region (650−1200 nm);33 in this special optical window, biological systems are known to be highly transparent due to low scattering and energy absorption from blood and soft tissues. As a result, Au NRs have shown promising potential in a wide range of biological applications such as bioimaging and thermo-chemotherapy.34,35 Another important characteristic of NRs for building chiral nanostructures is their shape anisotropy. Theoretical calculation has proven that chiral nanostructures need a minimum of two anisotropic NRs to form, compared to four isotropic nanospheres.36 In addition, the large electromagnetic field enhancement at the ends of NRs can greatly increase the chiroptical signal around their LSPR region. Prompted by these advantages, interests in utilizing Au NRs as building blocks to fabricate chiral nanostructures have grown quickly. Liz-Marzán and co-workers proposed the theoretical possibility of generating optical activities based on a pair of Au NRs.37 Kotov and co-workers were the first to observe the chiroptical activities of three-dimensional twisted Au NR dimers formed via self-assembly with DNA molecules.38 Wang and co-workers used DNA origami to arrange NRs in “X” and “T” shapes with tailored chirality.39 Liu and co-workers fabricated a dynamic plasmonic system, in which Au NRs walked directionally and progressively on DNA origami with tunable chirality.40 Ding and co-workers regulated and controlled the plasmonic chiroptical activity by manipulating the orientation of the NR dimers relative to the DNA axis and the inter-rod distance.41 Other chiral templates such as twisted supramolecular nanofibers, liquid crystals, and phospholipid films have also been utilized to fabricate chirally arranged NR assemblies.31,42,43

Chiral templates used to fabricate chiral nanostructures are mostly built via the self-association of biomacromolecules, whereas small biomolecules that largely exist as bioentities, such as amino acids and oligopeptides, are seldom used due to their size mismatch with nanoscale NRs.38 Although Tang and Liu separately employed cysteine and glutathione to end-to-end assemble Au NRs with distinctive chiroptical activity,19,44 the resulting chiral signals were relatively weak and attributed to molecule dipole−plasmon coupling (induced by the well oriented small biomolecules) rather than the formation of chirally arranged nanostructures. In addition, technical difficulties in characterizing the small biomolecule structures between NRs make it hard to investigate the assembly mechanism and the origin of chirality, which limits the advances in the use of small biomolecules as structure-directing agents. Achieving strong plasmonic chiral signals from assemblies of small biomolecules with Au NRs is still challenging. Au NRs are commonly synthesized with a cationic surfactant, cetyltrimethylammonium bromide (CTAB), which governs the anisotropic growth and colloidal stability of the NRs. Above its critical micelle concentration (cmc), CTAB forms a tightly packed bilayer on the NR surface through hydrophobic interactions of its alkyl chains. The ammonium cations of the outer bilayer are critical for the colloidal stability of the NRs in aqueous solution. It should be noted that above the cmc, CTAB micelles coexist with the CTAB-coated NRs in solution. In the CTAB bilayer or micelles, the alkyl chains of CTAB supply a nanoscale, hydrophobic confined space where hydrophobic molecules can easily diffuse into and accumulate to relatively high concentrations. For example, it has been shown that a variety of nanostructures can be generated via CTAB-assisted assembly of hydrophobic porphyrin molecules, including chiral NRs, with the morphology controlled by the CTAB concentrations used.45 The hydrophobic confinement effect provided by CTAB micelles could also be exploited for the selfassembly of NRs induced by biomolecules, especially for amphiphilic polypeptides and proteins.46 Hydrophobic confinement has been extensively studied in various systems, such as the lipid bilayer of cell membranes and micelles composed of sodium dodecyl sulfate, and it has been shown to significantly alter the driving forces of peptide folding and to facilitate the assembly of polypeptides.47−50 For example, neuronal cell membranes promoted the transformation of embedded amyloid β-peptides from random-coil unimers to folded oligomers that were stabilized by the hydrophobic environment.51 Similarly, the hydrophobic environment in CTAB micelles or bilayers on the surfaces of NRs could also expedite peptide folding and self-association processes. Therefore, it should be possible to use CTAB micelles to tune the chirality of nanostructures resulting from peptide-assisted assembly of CTAB-covered NPs, regardless of the NP geometry. Herein, we demonstrated that CTAB micelles promoted the self-association of L- or D-glutathione (GSH) and significantly enhanced the chiral assembly of NRs. Below the cmc of CTAB, the self-association of GSH only induced the end-to-end assembly of Au NRs, with negligible chiroptical signals arising from the nanostructures. By contrast, above the cmc, L- and DGSH accumulated in CTAB micelles or bilayers on the Au NR surface and formed helical oligomers in the confined hydrophobic space. Subsequently, these nanoscale helical oligomers induced the formation of chiral chains of Au NRs with strong chiroptical signals. Electron microscopy imaging studies 3464


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Figure 1. Effects of CTAB concentration on the self-assembly of Au NRs induced by L- or D-GSH, as monitored by extinction spectroscopy (a,c,e) and CD spectroscopy (b,d,f). Self-assembly conditions: (a,b) [CTAB] = 100 mM and [L-GSH] = 0.10 mM; (c,d) [CTAB] = 100 mM and [D-GSH] = 0.10 mM; (e,f) [CTAB] = 0.20 mM and [L-GSH] = 0.10 mM. Spectra were recorded at 1 h intervals for a−d and 5 min intervals for e and f. Arrows indicate the direction of spectral evolution.

Figure 2. Magnitude of plasmonic CD signals versus the fraction of Au NRs in nanochains assembled in the presence of (a) L-GSH and (b) DGSH.

revealed that Au NRs were connected by GSH oligomers to form end-to-end crossed junctions between adjacent NRs, resulting in three-dimensional chiral nanochains. The intensity of the plasmonic chiral signals was proportional to the concentration of Au NRs in the nanochains. Our experimental observations were also well-supported by finite-difference timedomain (FDTD) simulations of chirally arranged nanostructures.

We have studied the effect of CTAB micelles on the selfassembly process in the presence of GSH, above the cmc of CTAB in water. A CTAB concentration of 100 mM was used, which was similar to the assembly conditions reported previously by Wang and co-workers.56 The self-assembly process was monitored using extinction and CD spectroscopy and by transmission electron microscopy (TEM) (Figures 1−3). Figure 1a shows the temporal variation of extinction spectra for the assembly of Au NRs with 0.10 mM L-GSH. Before adding L-GSH, the extinction spectrum of the isolated NRs showed a LSPR band at 682 nm and a transverse surface plasmon resonance (TSPR) band at 517 nm. During the selfassembly process, the TSPR band remained constant but the LSPR band gradually decreased in intensity, with a concomitant formation of a new band at longer wavelengths (Figures 1a, S1a and S2a), indicating a typical end-to-end assembly of Au NRs.57,58 An examination by TEM revealed that the NRs had organized into 1D nanochains (Figure 3a). The number of NRs per chain and the number of chains gradually increased with the self-assembly time (Figures S3a and S4), consistent with previous studies of the self-assembly process.59,60 The self-assembly process was also monitored by CD spectroscopy. No CD signal was observed for discrete NRs. After triggering self-assembly with 0.10 mM L-GSH, distinct CD signals were immediately observed in the LSPR region of

RESULTS AND DISCUSSION Synthesis of Chiral Plasmonic Nanochains. The chiral plasmonic nanochains were prepared by the end-to-end assembly of Au NRs, facilitated by chiral GSH ligands. The as-synthesized NRs had a mean length of 46.89 ± 4.31 nm and width of 14.58 ± 1.80 nm and were stabilized by a bilayer of CTAB on the NR surface. The end-to-end assembly process was triggered by introducing L- (or D-) GSH to an aqueous solution of the NRs. Through the formation of strong Au−thiol bonds, GSH molecules selectively replaced CTAB at the ends of NRs; this is a consequence of the relatively weaker interaction between CTAB and the Au (111) end faces compared to the CTAB−Au interactions on the (100) and (110) side faces.52,53 Subsequently, the GSH ligands at adjacent NRs self-associated, resulting in the formation of 1D assemblies of NRs.54,55 3465


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Figure 3. Effects of CTAB concentration on the self-assembly of Au NRs induced by L- or D-GSH. Self-assembly conditions were as follows: (a−c) [CTAB] = 100 mM and [L-GSH] = 0.10 mM; (d−f) [CTAB] = 100 mM and [D-GSH] = 0.10 mM; and (g,h) [CTAB] = 0.20 mM and [LGSH] = 0.10 mM. Representative TEM images for nanochains (a,d,g) without and (b,e,h) with SiO2 shells and SEM images (c,f) for nanochains without SiO2 shells. Insets in parts a, d, and g represent the NR junctions for a LH EEX junction (green circle), a RH EEX junction (red circle), and a PEEJ (blue circle), respectively. (i) Percentages of LH EEX junctions (green), RH EEX junctions (red), and PEEJ (blue) in three kinds of nanochains. For each type of nanochain, the configuration of more than 150 junctions was analyzed.

NRs in the chains revealed that the intensity of the chiral signal of the plasmonic nanochains was indeed proportional to the amount of NRs assembled into chains (Figures 2a, S3a,b and S4). As D-GSH is the enantiomer of L-GSH, self-assembly of NRs induced by D-GSH should yield nanochains with the opposite chirality. Figure 1c,d shows the temporal variations of extinction spectra and CD spectra for the assembly of NRs with 0.10 mM D-GSH under otherwise identical conditions used for L-GSH. Although the extinction spectra for the D-GSH experiments showed a trend similar to those of L-GSH (Figures 1a,c, S1a,b and S2a,c), the direction of the bisignate CD signal was opposite to that of NR chains assembled with L-GSH

the spectrum (Figure 1b). A relatively weak positive CD signal appeared at ∼510 nm, which was attributed to the TSPR band of NRs. A more obvious feature was the appearance of a bisignate CD wave in the LSPR region of the spectrum, with a negative peak centered around 648 nm and a positive peak at 760 nm. During the assembly, the negative and positive peaks underwent continuous red shifts from 648 to 670 nm and 760 to 890 nm, respectively (Figure S2b). The intensity of CD signals also gradually increased with time, until the NR assemblies reached a steady state after 12 h (Figure S3b). The variation of CD signals was consistent with the tendency of the consumed and assembled NRs in the extinction spectra. Plots of the magnitude of the CD signal against the fraction of 3466


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Scheme 1. Illustrations of NR Dimers with (a) Planar End-to-End Junction (PEEJ) and (b) Right-Handed End-to-End Crossed (EEX) Junction with Their Mirror Imagesa

a

The PEEJ dimer can be superposed on its mirror image, whereas the EEX dimer has a pair of mirror-symmetric structures that cannot be superposed on each other.

Under otherwise identical conditions, the growth of nanochains with a high degree of chirality was only observed above the cmc of CTAB. Chiral Configuration of NR Junctions in Nanochains. It has been demonstrated theoretically and experimentally that plasmonic chiroptical activity can originate from chiral arrangements of plasmonic NPs.26,36 Interestingly, close inspection of the images of the nanochains (formed at 100 mM of CTAB) from both scanning electron microscopy (SEM) (Figure 3c,f) and cryogenic transmission electron microscopy (cryo-TEM) (Figure S7g−i) revealed that some of the junctions in the nanochains were not connected in a typical end-to-end fashion. Rather, an end-to-end crossed (EEX) structure with overlapping ends was observed between two adjacent NRs. To avoid structural deformation upon sample drying on flat TEM grids, SiO2 encapsulation was used to “freeze” the three-dimensional (3D) structures of the nanochains in solution during the self-assembly process.62 Both cryo-TEM images and TEM images of the SiO2encapsulated nanochains confirmed the existence of EEX junctions (Figures 3b,e and S7). Depending on the geometry of the NR junction, the overall structure may or may not be chiral. The illustrations in Scheme 1 show that a planar end-to-end junction (PEEJ) of two NRs results in an achiral dimer, whereas a chiral dimer is formed with an EEX junction. The EEX junction is a 3D structure with a pair of mirror-symmetric structures that are nonsuperposable (i.e., left-handed EEX and right-handed EEX junctions), analogous to S- and R-enantiomers for small molecules. For right-handed EEX (RH EEX) junctions, the NR unit rotates counterclockwise along the length of the nanochains (Figure 3a inset). Whereas for left-handed EEX (LH EEX) junctions, the NR unit rotates clockwise along the length of the nanochains (Figure 3d inset). The EEX structure of NRs is similar to those in chiral nanostructures of Au NRs reported previously. A junction of rods,63 3D plasmonic chiral tetramers of NPs,64 and NR-assembled “L” shape nanoarchitectures39 are all example structures that showed chiral bisignate signals in the LSPR region of their CD spectra. To understand the correlation between the chiral arrangements of EEX junctions and the chiroptical signals from the nanochains, we quantified the fraction of SiO2-encapsulated LH EEX and RH EEX junctions in nanochains prepared under different conditions. It should be emphasized that the CD

(Figures 1b,d and S2b,d). These results indicated the successful preparation of plasmonic nanochains with reverse chirality compared with plasmonic nanochains formed under L-GSH induction. TEM studies of the nanochains revealed that the number of NRs per chain and the number of chains gradually increased with self-assembly time (Figure 3d). In addition, plots of the magnitude of the CD signal against the NR fraction in the chains (Figures 2b and S3c,d) revealed that the chiral character of the D-type plasmonic nanochain also increases linearly with the fraction of NRs in the chains, consistent with the result for the L-type plasmonic nanochains. Synthesis of Achiral Plasmonic Nanochains below the cmc of CTAB. Controlling the CTAB concentration was critical to the self-assembly of NRs with GSH (Figure S5). Controlled experiments were performed with 0.20 mM of CTAB, which was below the cmc of CTAB (∼1.0 mM). It should be noted that the NRs were still colloidally stable, and no self-assembly was observed when GSH was absent (Figure S6). Figure 1e shows the variation in extinction spectra of the assembly induced with 0.10 mM of L-GSH and 0.20 mM of CTAB. The red shift of the LSPR band over time indicated that the NRs self-assembled in a typical end-to-end fashion, which was further confirmed by the presence of nanochains in the TEM images (Figure 3g). Figure 1f shows the temporal variation of CD spectra at different assembly times; compared to CD spectra obtained for the assembly using 100 mM of CTAB (Figure 1d), this assembly yielded CD signals that were approximately 20 times weaker (with a maximum of 3.95 mdeg at 702 nm) in the LSPR spectral region. Close inspection of TEM images of the assembly revealed that the average distance between two adjacent NRs was only 0.93 ± 0.13 nm (Figure 3g inset), significantly smaller than the corresponding distance (2.19 ± 0.75 nm) in nanochains formed using 100 mM of CTAB. The distance of 0.93 nm is close to the distance (1.24 nm) between neighboring sulfur atoms of two GSH molecules linked by their glutamyl (Glu) residues (inset of Figure 3g). As pH 3.0 is below the isoelectric point of GSH (5.93), a GSH molecule exists as a zwitterion with an anionic carboxyl group and a cationic amine group in the Glu residue;61 it is the electrostatic interaction between Glu residues in adjacent GSH molecules that drives the end-to-end assembly.55 In summary, although GSH can induce the end-to-end assembly of NRs both above and below the cmc of CTAB, the resulting nanochains possessed different degrees of chirality. 3467


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Figure 4. FDTD simulations of optical signals of the NR assembly. Simulated (a) extinction and (b) CD spectra of a dimer with a twist angle of −90 to +90° with 30° increments. The inset in (a) provides the top and front views of the dimer. The extinction spectra overlapped when the two NRs are arranged at same angle but in opposite directions. (c) Simulated CD spectra of meso-isomeric or diastereomeric nanochains. Different colored lines correspond to different handedness of the stereocenters in the nanochains. The same twist angle of 20° was used for both the RH EEX and LH EEX junctions. (d) Simulated CD spectra of right-handed helical nanochains with a constant gyration angle of 20° (dimer to heptamer). The inset represents a heptamer.

drastically different electromagnetic coupling efficiencies with right- and left-handed circularly polarized light (Figure 4a,b). As anticipated, simulated CD signals for the enantiomers (i.e., the LH EEX and RH EEX dimers) are bisignate curves with equal magnitudes that are mirror images of one another. The characteristic bisignate Cotton effect yielded two opposite peaks in the LSPR region. This is in agreement with experimental results in the present study and others involving similar systems.66,67 An increase in the absolute twist angle resulted in more intense simulated CD signals and blue shifts of the bisignate peaks and their zero-crossing points. For nanochains with more than two NRs, two or more stereocenters are present and could result in the formation of meso-isomers or diastereomers. Using FDTD simulations, we studied the effect of enantiomer excess on the overall chiroptical activity arising from the nanochains. Our results indicated that a trimer with two LH (or RH) EEX junctions displayed a stronger left-handed (or right-handed) bisignate CD signal compared to that of a left-handed dimer. For a trimer containing one LH EEX and one RH EEX junction, it appeared as a meso-superstructure and showed negligible optical activity due to internal compensation (Figure 4c). A tetramer containing two LH EEX junctions and one RH EEX junction showed a CD signal similar to that of a left-handed NR dimer, but with a red shift of the peak maximum; the same trend was observed for its LSPR peak (Figures 4c and S9a). These results demonstrate that the chiroptical property of the nanochain is driven by the type of EEX enantiomer present in excess in the nanochain, which is consistent with our experimental observations. As such, an enantiomerically pure nanochain should display the maximum chiroptical response. Figures 4d and S9b show the calculated extinction and CD spectra of nanochains with purely RH EEX junctions and a gyration angle of 20°, for a chain length of up to seven NRs. The intensity of the bisignate CD signal increased with the number of NRs in the nanochain, in good agreement with the

signals for the chiral NR chains after SiO2 encapsulation showed the same types of bisignate spectra compared to those of the nanochains before SiO2 encapsulation (Figure S8), although disassembly of the nanochains under the basic conditions required for SiO2 encapsulation (pH 8.5) led to a decrease in signal intensities. Therefore, we could only obtain a qualitative correlation between the chiral arrangements of EEX junctions and the chiroptical signals from the nanochains. Also, we only assigned the handedness of EEX junctions in which the 3D spatial arrangement can be unambiguously identified. For LGSH-induced chiral nanochains formed at 100 mM of CTAB, more RH EEX junctions (50.4%) than LH EEX junctions (34.3%) were observed. Therefore, the ensemble of nanochains showed overall right-handed chiroptical activity. When D-GSH was used to induce chiral assembly under these conditions, the percentages of RH EEX and LH EEX junctions were 40.7 and 50.0%, respectively, resulting in overall left-handed chiroptical signals for the nanochain ensemble. By contrast, 86.2% of the NR junctions in nanochains prepared with 0.20 mM of CTAB had a 2D planar structure, and the fractions of LH EEX and RH EEX junctions were almost identical (Figure 3i). Numerical Simulation of Chiroptical Properties of the Nanochains. Numerical simulation of optical properties can assist in understanding the contribution to chiroptical activity from the chiral spatial arrangements of plasmonic nanoparticles.36,65 We performed FDTD simulations to compare the extinction and chiroptical properties for nanochains with various spatial arrangements and chain lengths (Figure 4). Figure 4a,b shows the extinction and CD spectra for an EEX junction in a NR dimer with twist angles from −90 to +90° in 30° increments. When the twist angle is 0° (i.e., two parallel NRs), the assembled structure is achiral. As expected, results of the FDTD simulation for achiral dimers showed no distinguishable CD responses in the range of 300 to 900 nm. For nonzero twist angles, the EEX dimers appear to be chiral. Results from the FDTD simulations for the chiral EEX dimers show 3468


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Figure 5. Effects of CTAB concentration on the formation of GSH oligomers. L-GSH (0.10 mM) was incubated in varying concentrations of CTAB solutions at pH 3.0 and 45 °C for 24 h. (a) HPLC chromatograms of 0.10 mM L-GSH incubated with CTAB (concentrations indicated in the legend). ESI-MS spectra of GSH oligomers formed at varying concentrations of CTAB and retention time (tR); (b) [CTAB] = 0.20 mM and tR = 0.54 min, (c) [CTAB] = 1.0 mM and tR = 0.54 min, (d) [CTAB] = 10 mM and tR = 0.54 min, (e) [CTAB] = 10 mM and tR = 4.18 min, and (f) [CTAB] = 100 mM and tR = 3.75 min. The major mass spectral peaks are annotated with the lowest possible n/z, where n is the oligomer number and z is the charge. m/z on the x-axis of MS spectra stands for mass-to-charge ratio.

association of GSH molecules. Therefore, the effects of CTAB micelles on the self-association of GSH were studied in order to elucidate any potential influence on the self-assembly of NRs. We chose a method based on high-performance liquid chromatography/electrospray ionization mass spectrometry (HPLC-ESI-MS) to determine the self-association of L-GSH in the presence of varying concentrations of CTAB. L-GSH (0.10 mM) was incubated in CTAB (concentration range = 0.20−100 mM) at pH 3.0 and 45 °C for 24 h prior to analysis by HPLC and MS. Figure 5 shows the chromatographic and mass spectral data from these experiments. At pH 3.0, peaks with retention times (tR) between 0.20 and 0.92 min in the HPLC profiles were mainly attributed to L-GSH monomers and dimers, with a very small quantity of trimers present. Assignments of the HPLC peaks were done using MS data. For samples with CTAB concentrations above the cmc (i.e., 10 and 100 mM), the relatively larger peaks with tr between 3.50 and 5.63 min were found to be a mixture of CTA+ from the CTAB micelles and GSH oligomers (from dimer to nonamer). As shown in Figure 5d,e, the GSH peaks were much more intense in the mixture of CTAB micelles and GSH oligomers (tR = 4.18 min) than those in solution (tR = 0.54 min). These results suggest that at concentrations above the cmc, most of the zwitterionic GSH molecules preferred to associate with CTAB micelles. Considering that at pH 3.0 the GSH molecule has a zwitterionic Glu residue with the rest of the molecule being relatively more hydrophobic, it is reasonable to hypothesize that GSH molecules may behave like a zwitterionic surfactant and distribute into the walls of the CTAB micelles with the polar Glu residue facing out.68 In addition, we estimated the concentration of GSH in the CTAB micelles to be approximately 25 times higher than that outside the micelles (see Supporting Information for details). The accumulation of GSH molecules in the confined space should facilitate their selfassociation to form oligomers.

experimental results. The intensity of the normalized CD signals also increased linearly with the number of NRs in the chain (Figure S10). An analysis of the nanochains formed via LGSH induction gave an average aggregation number of approximately 4.5 at 12 h, which is in the range of the simulation study. The chiroptical response of the self-assembly was also confirmed using the asymmetry or anisotropy factor (g-factor) determined experimentally and numerically. This factor is defined as g=

Δε ε

where Δε and ε are the molar circular dichroism and molar extinction, respectively. Figure S11 shows the variation of the gfactor throughout the self-assembly process with 100 mM of CTAB and 0.1 mM of L-GSH (the same conditions as Figure 1a,b). A negative peak appeared near 634 nm, and its g-factor increased linearly with time, in agreement with the linear increase in the CD signal amplitude as the fraction of assembled NRs increased. A maximum g-factor of 0.005 was observed for the positive peak near 900 nm when the assembly achieved a steady state at 12 h. Figure S12 shows the simulated g-factor increasing with the length of oligomers; however, the calculated g-factor (0.60) is much larger than our experimental result (0.005). The difference suggests that the chirality of the synthesized nanochains is partly internally compensated, due to a mixture of LH EEX and RH EEX junctions and PEEJs in the nanochains. Effects of CTAB Micelles on the Formation of GSH Oligomers. Peptides show different assembly behaviors in cell cytoplasm or cell membranes, depending on the hydrophobicity of their environment. Similar to cell membranes, the hydrophobic core of CTAB micelles may provide an environment similar to that of the cell membranes and affect the self3469


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Figure 6. Formation of GSH oligomers in 10 mM GSH solutions at pH 3.0 and 45 °C without the use of CTAB. (a) ESI-MS spectrum of LGSH incubated for 24 h. CD spectra of (b) L-GSH and (c) D-GSH with increasing incubation times. (d) 1H NMR spectra of L-GSH for various incubation times, t. Different colored bands were used to indicate the positions of new resonances belonging to L-GSH oligomers. (e) Fingerprint region of a 2D NOESY spectrum of L-GSH incubated for 5 days. (f) Truncated GSH oligomeric structure showing a repeat unit with intermolecular hydrogen bonding between adjacent L-GSH molecules (left) and an illustration of a right-handed helical GSH oligomer based on results from NOESY and CD experiments (right).

junctions in NR chains induced by either L- or D-GSH (Figure 3i) also suggests the possibility of forming enantiomeric oligomers from only L- or D-GSH. The positive CD band observed at 210 nm and the negative band at 195 nm can be ascribed to peptide n−π* and π−π* transitions, respectively, which are characteristic peaks for an antiparallel β-sheet structure.72 Typically, the assembly of β-sheets with only Ltype residues forms left-handed supramolecular nanostructures.73 The formation of oligomers with the opposite chirality (i.e., right-handed helices) from L-GSH might have been caused by the hydrophobic confinement effect of CTAB micelles or the acidic condition used in self-assembly. The formation of right-handed helices from L-type residues has been observed previously for amyloid fibrils under acidic conditions.73 For DGSH, a bisignate signal with the opposite chirality to that of LGSH was observed, indicating the formation of mostly lefthanded helical structures. The bisignate peaks of the helical L-(D-) GSH oligomers have the same handedness as those from the NR chains linked by the corresponding GSH oligomers, suggesting that the molecule dipole−plasmon coupling effect from the interaction of GSH oligomers with NRs could also contribute to their plasmonic chiroptical activities. Nuclear magnetic resonance (NMR) spectroscopy was also used to monitor the self-association process of L-GSH and to study the interactions between GSH molecules in space. Figure 6d shows the 1H NMR spectra of L-GSH oligomers formed with various incubation times at pH 3.0 and 45 °C. CTAB was not used in these experiments. After 5 days, all of the resonances corresponding to L-GSH became relatively broad due to the self-association behavior. Area under the resonances

We also studied the effect of the concentration of GSH on GSH self-association in the absence of CTAB micelles under otherwise identical conditions. ESI-MS results showed that the formation of GSH oligomers is dependent on its concentration (see Figure S13). When the concentration of GSH was increased from 0.10 to 10 mM, oligomers with aggregation numbers up to nine were observed (Figure 6a), which is similar to the oligomers formed with 0.10 mM of GSH and 0.10 M of CTAB. It should be noted that the mass spectral peak of GSSG (MW = 612.8), corresponding to oxidized glutathione, was much smaller than that of GSH dimers (MW = 614.8) (Figure S13b). This result and the presence of trimers, pentamers, and heptamers suggest the building block for self-association was GSH unimer rather than GSSG, in contrast to previous reports where GSSG served as the building block of fibrils in nonpolar solvents.69,70 In addition to characterization with mass spectrometry, CD spectroscopy was employed to study the chiroptical property of the GSH oligomers. Figure 6b,c shows the temporal variation of CD spectra of L-GSH and D-GSH as a function of incubation time. A solution of freshly prepared L-GSH unimer exhibits two negative peaks at 195 and 222 nm, consistent with the CD spectrum reported in the literature.71 A new positive peak developed at 210 nm, and its intensity gradually increased with incubation time. For longer incubation times (up to 4 days), a characteristic right-handed bisignate peak with a negative peak at 195 nm and a positive peak at 210 nm gradually appeared. This suggests that the L-GSH oligomers formed have predominantly a right-handed helical structure, although the presence of left-handed helices in the oligomers cannot be excluded. The observation of both RH EEX and LH EEX 3470


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ACS Nano Table 1. 1H NMR Data of L-GSH Unimers and Oligomersa

a

* Denotes protons where the resonance shifted between unimers and oligomers.

mechanism of helix formation. The GSH amino resonance was not observed in a solution of freshly prepared L-GSH unimers due to chemical exchange with the solvent. However, with the formation of oligomers over time, the Glu amino resonance reappeared at 7.83 ppm. This is likely a result of the Glu amino group participating in hydrogen bonding, rendering it unavailable for chemical exchange. As shown in Table 1, the main difference between the 1H NMR spectra of GSSG and L-GSH was Cys βH, where two resonances were observed for GSSG. The remaining resonances showed negligible differences in chemical shifts between the oxidized and reduced forms of glutathione. After incubation for 5 days, the characteristic resonance of GSSG (3.28 ppm) was still not observed for the solution of oligomers. This again indicates the GSH unimer, rather than GSSG, is the building block for GSH oligomers, an observation supported by MS data presented earlier. In our investigations, L- and D-GSH adopt an antiparallel βsheet conformation and predominantly form right-handed and left-handed helical oligomers, respectively. The GSH oligomers are expected to have nanoscale dimensions that are more comparable to the diameter of NRs than GSH unimers, which are molecular entities. It is also plausible that oligomers attached to the ends of NRs are more oriented, whereas GSH unimers are more randomly dispersed in solution. We observed the formation of predominantly LH EEX NR junctions in the presence of left-handed helical oligomers, while the opposite was observed for right-handed helical oligomers (i.e., formation of mostly RH EEX NR junctions). It appeared that chirality of the oligomers attached to the NRs was transferred to the nanoscale chiral assemblies of NRs, leading to strong chiroptical activity from the ensemble in the visible−NIR range.

for the L-GSH unimer remained mostly unchanged during the course of the study, indicating that no L-GSH precipitated from the solution. As the self-association progressed, five new resonances appeared at 2.41, 3.10, 4.23, 7.83, and 8.66 ppm, and their intensities gradually increased with incubation time. Using data from 2D total correlation spectroscopy (Figure S14) and nuclear Overhauser enhancement spectroscopy (NOESY) (Figures 6e and S15), the five new resonances were assigned to glutamyl β-protons (Glu βH*), glutamyl γ-protons (Glu γH*), glutamyl α-protons (Glu αH*), glutamyl amide protons (Glu NH*), and glycine amide protons (Gly NH*). Table 1 lists the chemical shifts for these protons in L-GSH unimers and oligomers. The chemical shifts of these resonances for the LGSH oligomers are consistent with the presence of intermolecular interactions between oligomers. Resonances from cysteinyl amide protons (Cys NH), cysteinyl α-protons (Cys αH), and cysteinyl β-protons (Cys βH), as well as glycine α-protons (Gly αH) in the oligomers were observed at the same chemical shifts as the corresponding protons in L-GSH unimers, indicating that these protons existed in similar chemical environments in the unimers and the oligomers. Downfield shifts of the resonances for protons at both the Cand N-termini of L-GSH suggest that the oligomers were formed via an interaction between the C-terminal and Nterminal residues. For a better understanding of the aggregation mechanism, solutions of freshly prepared L-GSH unimers and oligomers obtained after incubated for 5 days were studied using NOESY. Figures 6e and S15 show the fingerprint region of the 2D NOESY spectra and peak assignments. Compared to freshly prepared L-GSH unimers, five new cross peaks (corresponding to correlations for Glu γH*-Gly NH*, Gly αH-Gly NH*, Glu αH*-Gly NH*, Cys βH-Cys NH, and Glu γH-Cys NH) appeared in the fingerprint region of the oligomers. The presence of Glu γH*-Gly NH* and Glu αH*-Gly NH* cross peaks indicates that these protons in the Glu and Gly residues are situated within 5 Å of one another, suggesting that hydrogen bonding occurs between the protonated amino side chain of Glu and the carbonyl group of Gly (Figure 6f). In this configuration, each GSH molecule forms two hydrogen bonds with neighboring GSH molecules via its Glu amino group and Gly carbonyl group. Taken together, these results suggest that L-GSH adopts an antiparallel β-sheet conformation via hydrogen bonding to form righthanded helical oligomers (Figure 6f). This observation provides further support to the right-handed helical structure deduced from CD data presented earlier (see Figure 6b). Finally, chemical exchange behavior of the Glu amino protons in GSH unimers and oligomers also provides insights into the

CONCLUSION In summary, CTAB micelles present in the Au NR solution facilitated the formation of helical GSH oligomers through hydrophobic confinement. The handedness of helical GSH oligomers was transferred to the NR chains, resulting in the creation of chiral EEX NR junctions. Remarkably, nanoscale GSH oligomers induced the self-assembly of Au NRs into nanochains with chiroptical signals that were 20 times greater than nanochains formed via GSH unimers. FDTD simulations of extinction and CD data were consistent with the experimental results, where a chiral nanostructure was observed with EEX junctions between two neighboring NRs in nanochains. Importantly, our work indicated that CTAB micelles or other types of micelles can significantly enhance 3471


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solution was approximately 0.20 mM. It should be noted that contributions from the CTAB bilayers covering the surfaces of the NRs to the final CTAB concentration should be negligible. It is reported that there are approximate 10 000 CTAB molecules in the CTAB bilayer around one Au NR.75 As the concentration of NRs in the solution was approximately 1 nM, the total concentration of CTAB in the bilayer was on the order of 0.01 mM. Finally, 0.10 mM of LGSH was added to the NR solution, and the pH was adjusted to 3.0 with 0.10 M of HCl. The assembly was kept in a 45 °C bath. SiO2 Encapsulation of Chiral Plasmonic Nanochains. The chiral plasmonic nanochains were fixed with SiO2 via TEOS hydrolysis. Briefly, 2.0 μL of TEOS was added in a stirred 1.0 mL solution of the assembled NR chains. The pH of the solution was adjusted to 5.5 with 0.10 M of NaOH, and the solution was incubated at 45 °C for 4−5 h. Then, another 2.0 μL of TEOS was added to the solution and the pH of the solution was adjusted to 8.5 with 0.10 M of NaOH. The solution was then kept at 45 °C overnight. FDTD Simulations. Electromagnetic simulations were performed using the commercial software package Lumerical FDTD Solutions with perfectly matched layer absorbing boundary conditions. Extinction spectra were simulated with a planar polarized wave source. Circular dichroism spectra were calculated as the difference between the extinction spectra of right-hand and left-hand circular polarization excitation that is equal to left-handed extinction spectra minus righthanded extinction spectra. The excitation wavelength was set in the range of 300 to 900 nm. Dielectric functions in the simulations were formulated using the Johnson and Christy data for Au. Water with a refractive index of 1.33 was used as surrounding environment for all the simulations. Mesh size for the simulations was set at 2 nm. Characterization. CD spectra were recorded with a Jasco J-810 circular dichroism spectrometer. A 2 mm quartz sample cell and a scan speed of 500 nm/min were used. Extinction spectra were measured with a PerkinElmer Lambda 950 UV−vis−NIR spectrometer with a data interval of 2 nm using the same quartz cell. TEM imaging was performed with a JEOL JEM-2100F transmission electron microscope operating at 200 kV on carbon-coated TEM grids. Cryo-TEM experiments were performed on a JEM-2100 high-resolution TEM with a 120 kV accelerating voltage. SEM images were obtained with a HITACHI SU8000 scanning electron microscope with an electron voltage of 20 kV. HPLC-ESI-MS was performed using an Agilent1290 liquid chromatograph interfaced with a Bruker microTOF Q II mass spectrometer operating in positive ionization mode. NMR spectra were recorded at 37 °C using a Bruker Avance 600 spectrometer equipped with a cryoprobe. The WATERGATE technique was used to suppress the resonance from water. Spectra were obtained in 1:9 D2O/ H2O with sodium 2,2-dimethyl-isotope-2-silapentane-5-sulfonate as an internal standard.

the biomolecule-induced chiral assembly of nanoparticles (e.g., amino acids, peptides, proteins, etc.) due to the hydrophobic confinement effect exerted by the micelles on the selfassociation of these biomolecules. In addition, the chiroptical activity of chirally arranged nanostructures can be accentuated by peptide oligomers, as the nanoscale dimensions of the peptides become comparable to those of the inorganic building blocks.76 In this regard, a promising extension of our current work could involve the use of polypeptides or proteins to direct the self-assembly of inorganic nanoparticles, allowing access to even stronger chiroptical signals and longer range chiral nanostructures.

MATERIALS AND METHODS Materials. Hexadecyltrimethylammonium bromide (CTAB, ≥99%), gold(III) chloride trihydrate (HAuCl4·3H2O, 99.99%), sodium borohydride (NaBH4, ≥98%), L-ascorbic acid (≥99.0%), Lglutathione (L-GSH, >98.0%), and silver nitrate (≥AgNO3, 99.0%) were purchased from Sigma-Aldrich. D-Glutathione (D-GSH) was purchased from GL Biochem. Ltd. (Shanghai, China) with a purity of >98.0%. Tetraethylorthosilane (TEOS) was purchased from Beijing Shiji (Beijing, China). All chemicals were used as received. Deionized water (18.2 MΩ) was used in all the experiments. Synthesis and Regrowth of NRs. The NRs were prepared by the seed-mediated growth method reported previously.74 Briefly, seed gold NPs were prepared by mixing HAuCl4 (0.12 mL, 15 mM) with CTAB (3.5 mL, 0.10 M) and a freshly prepared, ice-cold NaBH4 solution (0.50 mL, 10 mM) at 25.5 °C. The mixture was stirred for 2 min. The seeds could be used within 0.5−2 h when stored in a 25 °C bath. To prepare the growth solution, AgNO3 (0.40 mL, 4.0 mM) and HAuCl4 (0.50 mL, 15 mM) were added to a 1.0 mM solution of CTAB (0.3645 g in 8.86 mL of deionized water) and stirred. Following the addition of ascorbic acid (0.124 mL 0.788 M), the dark yellow solution turned colorless. Finally, 0.10 mL of the seed solution was added to the growth solution to initiate NR growth. The mixture was then incubated at 27.0 °C for more than 12 h before use. The as-synthesized NRs needed further regrowth because of the limited spectral range of the CD spectrometer. Aqueous solutions of AgNO3 (0.40 mL 4.0 mM), ascorbic acid (0.124 mL 0.788 M), and HAuCl4 (0.50 mL 15 mM) were added to a 10 mL NR solution. The resultant solution was incubated at 27 °C for about 4 h. The regrowth process was repeated three times in order to achieve a blue shift of the LSPR peak from 840 to 700 nm. The mean diameter and length of the NRs were 14.58 ± 1.80 and 46.89 ± 4.31 nm, respectively. At the end of the regrowth process, the NRs were purified by centrifugation at 7000 rpm for 15 min and redispersed in the same volume of 0.10 M of CTAB solution before use. Assembly of Chiral Plasmonic Nanochains. The assembly conditions were similar to the method reported previously by Wang and co-workers.56 Briefly, glutathione (0.10 mM) was added in the solution of NRs in 0.10 M of CTAB. The pH was immediately adjusted to 3.0 using 0.10 M of HCl, and the solution was kept in a 45 °C bath. We also performed the assembly with different concentrations of GSH. Increasing the concentration of GSH to 1.0 mM or higher decreased the positive charge of NRs, as determined by ζpotential measurements, mainly due to substitution of the positively charged CTA+ on the side-face of the NRs with zwitterionic GSH (Figure S16). In these cases, the assembled NR chains became less stable and easily precipitated from the solution (Figure S17). Decreasing the concentration of GSH to 0.020 mM or lower resulted in no assembly of the NRs under otherwise identical conditions. Synthesis of Achiral Plasmonic Nanochains. The NRs were centrifuged and redispersed in deionized water two times to decrease the CTAB concentration to ∼0.20 mM. For example, 1.0 mL of the NR solution was centrifuged at 7000 rpm for 15 min twice. The supernatant was removed each time. The volume of the concentrated NR solution was accurately set to 44.7 μL and then increased to 1.0 mL with deionized water. The final concentration of CTAB in the NR

ASSOCIATED CONTENT S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsnano.6b07697. Calculations and Figures S1−S17 (PDF)

AUTHOR INFORMATION Corresponding Author

*E-mail: [email protected]. ORCID

Kun Liu: 0000-0003-2940-9814 Notes

The authors declare no competing financial interest.

ACKNOWLEDGMENTS K.L. and Z.-Y.L. gratefully acknowledge financial support from the National Natural Science Foundation of China (21534004). K.L. thanks the National Natural Science Foundation of China 3472


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(21474040, 21674042) and China’s Thousand Talent Plan for financial support. Y.Y. acknowledges financial support from the International Postdoctoral Exchange Fellowship Program 2013 funded by the Office of China Postdoctoral Council (20130036) and the China Postdoctoral Science Foundation (2013M540249, 2014-T70281). L.Z. thanks the National Science Foundation of China (21403085) for financial support. We gratefully thank Prof. Myongsoo Lee, Mr. Bowen Shen, and Miss Xin Liu for the cryo-TEM measurements.

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