Selective Suspension of Single-Walled Carbon Nanotubes Using β

Feb 20, 2014 - Article Options. ACS ActiveView PDF .... ACS Editors' Choice: Using Data Analysis to Evaluate and Compare Chemical Syntheses. This week...
0 downloads 0 Views 2MB Size
Download PDF
Article pubs.acs.org/JPCC

Selective Suspension of Single-Walled Carbon Nanotubes Using β‑Sheet Polypeptides Nicole M. B. Cogan,† Charles J. Bowerman,† Lisa J. Nogaj,† Bradley L. Nilsson,† and Todd D. Krauss*,†,‡ †

Department of Chemistry, University of Rochester, Rochester, New York 14627, United States Institute of Optics, University of Rochester, Rochester, New York 14627, United States

‡

S Supporting Information *

ABSTRACT: Individual single-walled carbon nanotubes (SWNTs) were suspended in water using amphipathic β-sheet peptides of the general sequence Ac-(XKXE)2-NH2. By substituting natural and nonnatural amino acids of varying aromatic and hydrophobic character in the X position, the interactions between the peptide and the nanotube sidewall could be systematically varied. Surprisingly, enhancing the degree of favorable π−π and hydrophobic interactions, which strongly influence the self-assembly properties of these peptides, did not correlate with an improvement in nanotube dispersion efficiency. We found that substituents in the X-position of the peptides play a significant role in SWNT interaction and contributes to (n,m) structure specificity.

yields more efficient SWNT dispersion due to π−π interactions with the nanotube sidewall.12,13,18,22−30 In addition, peptides have the ability to self-assemble into higher-order structures, and this property has been shown to play a role in SWNT solubilization by, for example, yielding qualitatively brighter nanotubes.17,28,31−33 Several custom-designed peptides have been developed to suspend SWNTs and to understand the favorable interactions that occur between the SWNTs and the peptide.17,23,25,26,31−34 Despite one recent study that probed the importance of the amino acid tryptophan in peptide−nanotube interaction,26 most studies that investigate the effect of amino acid aromaticity on nanotube dispersion use only natural amino acids in their sequence.23,24,30,31 Although efficient dispersion is achieved, the limited number of natural amino acids restricts the structural possibilities of the peptide and thus the range of achievable properties for peptide−SWNT interaction. Nonnatural amino acids possess a wider range of properties, including hydrophobic character, aromatic surface area, and secondary structure propensity, and therefore provide a unique perspective when studying favorable nanotube interactions. For example, there is a direct relationship between the aromatic content of a peptide and its ability to self-assemble.35 A more thorough understanding of how peptides interact with and disperse SWNTs is necessary for the development of efficient surfactants that optimize the unique optical properties of SWNTs. Exploiting nonnatural amino acids in the context of peptides will facilitate acquisition of this needed insight.

1. INTRODUCTION Single-walled carbon nanotubes (SWNTs) possess many unique optical properties, including size-tunable near-infrared (NIR) emission,1,2 high photostability,3 and a lack of fluorescence intermittency at room temperature.3,4 The electronic and optical properties are strongly dependent on the nanotube diameter and chiral angle, defined by the chiral indices (n,m).1 Although these properties make SWNTs excellent candidates as biological labels and in fluorescencebased biosensors, they are also a highly hydrophobic material, and due to strong van der Waals interactions between sp2hybridized carbons, they aggregate in nearly all solvents. Bundling results in quenching of SWNT fluorescence due to nonradiative energy transfer from the semiconducting to the nonemissive metallic nanotubes.2 This unfortunate tendency for SWNTs to aggregate and bundle inhibited early optical studies of SWNTs until O’Connell et al. developed a method to disperse individual nanotubes in water through noncovalent interactions with surfactants.2 Subsequently, various types of surfactants have emerged as nanotube dispersants including ionic molecules,2,5 bile salts,6 polymers,7,8 and biological molecules such as single-stranded DNA (ssDNA)9,10 and peptides.11−21 Suspending and isolating individual SWNTs allows the spectroscopic features of the various (n,m) structures to be resolved. The biocompatibility and structural diversity of amino acids give polypeptides a unique platform as SWNT dispersing agents. In order to design peptides that efficiently suspend SWNTs with high fluorescence quantum yield (QY), it is necessary to understand the favorable interactions occurring between the peptide and the nanotube sidewall. For example, it has been observed that increased aromatic content on peptides © 2014 American Chemical Society

Received: November 5, 2013 Revised: February 18, 2014 Published: February 20, 2014 5935

dx.doi.org/10.1021/jp410870y | J. Phys. Chem. C 2014, 118, 5935−5944

The Journal of Physical Chemistry C

Article

In this study, β-sheet peptides of the short sequence motif Ac-(XKXE)2-NH2 were used to suspend SWNTs. Amino acid X was systematically substituted with various natural and nonnatural amino acids, changing both the physicochemical and self-assembly properties of the peptide.36−38 The effect of the peptide properties on SWNT dispersion was studied by utilizing the absorption and photoluminescence (PL) properties of dispersed SWNTs. Critical to this work was the usage of nonnatural amino acids in addition to natural amino acids, which enables a broader assessment of how the peptide interacts with nanotubes. Through the global change of hydrophobic amino acids in the peptide sequence, we show that an increase in the aromaticity and/or hydrophobic character of the amino acid surprisingly does not correlate with more efficient SWNT dispersion by these peptides. Instead, varying amino acid X in Ac-(XKXE)2-NH2 has a significant effect on the fluorescence QY of the dispersion and (n,m) structure specificity; enhanced dispersion of different (n,m) structures is observed for different peptide sequences.

K1NalE)2-NH2 (MALDI-TOF-MS) m/z 1362.71 (1362.66 calcd for [MH+]), 1384.77 (1384.64 calcd for [MNa+]), 1400.76 (1400.61 calcd for [MK+]). Ac-(2NalK2NalE)2-NH2 (MALDI-TOF-MS) m/z 1362.55 (1362.66 calcd for [MH+]), 1384.57 (1384.64 calcd for [MNa+]), 1400.54 (1400.61 calcd for [MK+]). Circular Dichroism (CD) Spectroscopy. Peptides were dissolved in unbuffered, filtered water (Barnstead, NANOpure 0.2 μm filter, 18 Ω) by the addition of water to the lyophilized powder followed by 3 cycles of 1 min of vortexing and 5 min of sonication to obtain optically clear, homogeneous solutions. Precise peptide concentrations were determined for stock solutions in correlation to HPLC standard curves (monitoring at 215 nm) using the method of O’Nuallian et al.39 Standard concentration curves were constructed as described,39 and absolute concentrations for each curve were determined by amino acid analysis of three independent dilutions for each curve. Once the sample stock concentration was determined, aliquots of the desired amount of peptides were prepared, frozen, and lyophilized; samples were then dissolved in the appropriate volume of water. Stock concentrations for the Trp, 1Nal, and 2Nal peptide variants were determined by UV absorbance as previously described.39 The secondary structure of the self-assembled peptide was characterized through CD spectroscopy using an AVIV 202 CD spectrometer. Spectra were obtained from 260 to 190 nm with a 1.0 nm step, 1.0 nm bandwidth, and 1 s integration time at 25 °C in a 0.1 mm path length quartz cuvette (Hellma). Background subtraction, conversion to molar ellipticity, and data smoothing with a least-squares fit were achieved using the AVIV software. Fourier Transform Infrared (FTIR) Spectroscopy. Peptide solutions were analyzed after dissolution in D2O, as described previously. FT-IR was performed using a Shimadzu 8400 FT-IR spectrophotometer. Spectra were obtained from 1750 to 1550 cm−1 with a 4 cm−1 resolution, Happ-Ganzel apodization, and 512 scans in a 0.2 mm path length CaF2 salt plate cell. Background spectra were collected and subtracted. Transmission Electron Microscopy (TEM). Samples (10 μL) were spotted directly onto either 200 mesh carbon coated copper grids for self-assembled peptides alone, or 300 mesh lacey carbon coated copper grids for peptide-dispersed SWNTs, and allowed to stand for 2 min. Excess solvent was carefully removed by capillary action using filter paper, and the grid was allowed to dry for an additional 2 min. Grids were then stained with 20 μL of uranyl acetate for 2 min, followed by removal of excess stain and 10−15 min of drying. Images were taken with a Hitachi 7650 TEM with an accelerating voltage of 80 kV for self-assembled peptide samples and with a FEI Tecnai F-20 field emission electron microscope with an accelerating voltage of 200 kV for peptide-dispersed SWNTs. Preparation of Peptide/SWNT Suspensions. Samples were prepared using methods adapted from O’Connell et al.2 and Zheng et al.9,10 Purified SWNTs manufactured by either the CoMoCAT (SouthWest Nanotechnologies, Inc.) or HiPco (Unidym, Inc.) methods were added to 1 mM peptide in D2O at a concentration of ∼0.5 mg/mL. The sample was shear homogenized (Ultra Turrax T8 homogenizer) for 1 h at a speed of 13 000 rpm and then probe sonicated using a Branson 450 Sonifier for 1 h at a power of 25 W. An ice bath was used during the sonication process to prevent excessive heating of the sample. Samples were ultracentrifuged using a TLA-55 rotor on a Beckman TL-100 Ultracentrifuge at 25 000 rpm (28000g) for 1 h. The upper portion of the supernatant was

2. EXPERIMENTAL METHODS Peptide Synthesis and Characterization. Ac-(XKXE)2NH2 peptides where X = Val, Ile, Leu, Phe, Trp, 1Nal, 2Nal, Cha, and F5-Phe were synthesized with a microwave-equipped Liberty Peptide Synthesizer (CEM). The Val, Ile, and Leu peptides were also purchased from United Biochemical Research, Inc., and then purified. Rink amide resin (Advanced ChemTech) was utilized and loaded using standard methods HBTU/HOBt activation. Peptide synthesis was carried out using standard Fmoc methods. After completion of the chain assembly, the peptide was cleaved manually using trifluoroacetic acid (TFA), triisopropylsilane (TIS), and water (95:2.5:2.5). High-performance liquid chromatography (HPLC) purification of the cleaved peptides was performed with a Shimadzu LC-AD HPLC system equipped with a variable wavelength absorbance detector using a reverse phase C18 column (Waters, BEH300 10 μm, 19 × 250 mm). A binary gradient of water (0.1% TFA) and acetonitrile (0.1% TFA) at 10 mL min−1 was used, and the column eluents were monitored by UV absorbance at 215 and 254 nm. Fractions were collected and lyophilized after their purity was confirmed by analytical HPLC performed using an RP-C18 column (Waters, BEH300 10 μm, 4.6 × 250 mm). Peptide identity was verified using matrix-assisted laser desorption ionization time-of-flight mass spectroscopy (MALDI-TOF MS). Ac-(VKVE)2-NH2 (MALDI-TOF-MS) m/z 970.57 (970.59 calcd for [MH+]), 992.57 (992.58 calcd for [MNa+]), 1008.55 (1008.55 calcd for [MK+]). Ac-(IKIE)2NH2 (MALDI-TOF-MS) m/z 1026.72 (1026.66 calcd for [MH+]), 1048.72 (1048.64 calcd for [MNa+]), 1064.61 (1064.70 calcd for [MK+]). Ac-(LKLE)2-NH2 (MALDI-TOFMS) m/z 1026.88 (1026.66 calcd for [MH+]), 1048.87 (1048.64 calcd for [MNa+]), 1064.85 (1064.61 calcd for [MK+]). Ac-(ChaKChaE)2-NH2 (MALDI-TOF-MS) m/z 1186.88 (1186.78 calcd for [MH+]), 1208.76 (1208.76 calcd for [MNa+]), 1224.85 (1224.74 calcd for [MK+]). Ac-(FKFE)2NH2 (MALDI-TOF-MS) m/z 1162.81 (1162.59 calcd for [MH+]), 1184.80 (1184.58 calcd for [MNa+]), 1200.77 (1200.55 calcd for [MK+]). Ac-(F5FKF5FE)2-NH2 (MALDITOF-MS) m/z 1522.10 (1522.40 calcd for [MH+]), 1544.05 (1544.39 calcd for [MNa+]), 1560.02 (1560.36 calcd for [MK+]). Ac-(WKWE)2-NH2 (MALDI-TOF-MS) m/z 1318.52 (1318.64 calcd for [MH+]), 1340.56 (1340.62 calcd for [MNa+]), 1356.53 (1356.59 calcd for [MK+]). Ac-(1Nal5936

dx.doi.org/10.1021/jp410870y | J. Phys. Chem. C 2014, 118, 5935−5944

The Journal of Physical Chemistry C

Article

Figure 1. (a) Structure of the Ac-(XKXE)2-NH2 sequence motif and the nonnatural amino acids (b) 1Nal, (c) 2Nal, (d) Cha, and (e) F5-Phe used in this study.

Table 1. Dispersion Efficiency of SWNTs Suspended in Ac-(XKXE)2-NH2 Peptides and the Corresponding Amino Acid Propertiesa amino acid X

aromatic

HPLC retention time Rt (min)

amino acid hydrophobicityb

β-sheet propensityc

Val (V) Ile (I) Leu (L) Phe (F) Trp (W) 1Nal 2Nal Cha F5-Phe

no no no yes yes yes yes no yes

10.3 11.1 11.3 11.8 11.95 12.7 13.2 13.2 13.4

1.22 1.80 1.70 1.79 2.25 3.36 3.36 2.72 2.12

1.86 1.71 1.1 1.43 1.3

CoMoCAT QYd (%) 0.066 0.108 0.103 0.116

± ± ± ±

0.056 0.030 0.048 0.025

0.040 ± 0.011 0.090 ± 0.012

HiPco QYd (%) 0.056 0.050 0.068 0.037 0.035

± ± ± ± ±

0.025 0.037 0.041 0.023 0.013

0.025 ± 0.019

a

Peptides are listed in increasing order of peptide hydrophobicity, from top to bottom, as determined by HPLC retention times. bAmino acid hydrophobicity based on water−octanol partition coefficients relative to glycine.44 cPropensity to occur in β-sheet secondary structures from the PDB select data set.41 dQY values calculated using IR-125 in DMSO as a reference dye with 632.98 nm excitation.

spectra were corrected for the power of the excitation source as well as the efficiency of the emission monochromator and detector. Each PLE map was normalized to the peak of maximum intensity.

carefully removed as to not disturb the sedimented nanotubes. For comparison, sodium dodecylbenzenesulfonate (SDBS), sodium dodecyl sulfate (SDS), and ssDNA were also used to suspend SWNTs using preparation methods similar to those above (see Supporting Information for details). Optical Characterization. All optical measurements were obtained using a 1 cm path length quartz cuvette. Absorption spectra were acquired using a PerkinElmer Lambda 950 UV− vis−NIR spectrometer. Fluorescence spectra were acquired using a home-built fluorometer system with a 632.8 nm HeNe excitation source and a SpectraPro 300i monochromator equipped with a liquid-N2 cooled germanium detector for emission detection. Using methods previously reported,40 QY measurements were performed with IR-125 (Exciton, Inc.) in DMSO as a reference dye and 632.8 nm excitation. Photoluminescence Excitation (PLE) Spectroscopy. PLE maps for each sample were obtained using a 1 cm path length quartz cuvette and the home-built fluorometer described above. A 450 W xenon arc lamp source coupled to a SpectraPro 150 monochromator system was used for excitation with wavelengths ranging from 500 to 800 nm for CoMoCAT samples (450 to 800 nm for HiPco samples) and a 5 nm excitation step. SWNT emission was measured from 900 to 1300 nm for CoMoCAT samples (900 to 1600 nm for HiPco samples) every 2 nm with an integration time of 500 ms. All

3. RESULTS AND DISCUSSION The natural amino acids valine (Val), isoleucine (Ile), leucine (Leu), phenylalanine (Phe), and tryptophan (Trp) and the nonnatural amino acids 1-naphthylalanine (1Nal), 2-naphthylalanine (2Nal), cyclohexylalanine (Cha), and pentafluorophenylalanine (F5-Phe) were substituted into the peptide sequence Ac-(XKXE)2-NH2 at position X (Figure 1).36 The hydrophobic amino acids substituted into position X creates an amphipathic structure that can interact with SWNTs and suspend them in water. By tailoring the properties of amino acid X in the peptide sequence, specific properties of the peptide can be related to the efficiency and quality of nanotube solubilization. All peptide variants exhibited a β-sheet structure upon dissolution in water (no SWNTs present). Analysis of these peptide solutions by FT-IR confirmed the formation of β-sheet structure by the presence of an amide I stretch at 1620 cm−1. Analysis was performed using 1 mM peptide in D2O without the presence of SWNTs (Figure S1 in the Supporting Information).36 Further analysis of the peptide solutions by CD spectroscopy exhibited 5937

dx.doi.org/10.1021/jp410870y | J. Phys. Chem. C 2014, 118, 5935−5944

The Journal of Physical Chemistry C

Article

minima at 218 nm, indicative of β-sheet formation (Figure S2 in the Supporting Information).36 The presence of a second peak at 210 nm in the CD spectra of the Trp, 1Nal, and 2Nal peptides is not typical of β-sheet structures; this transition has been observed in aromatic amino acids due to the UV absorbance of the hydrophobic aromatics causing a π−π* transition. While this spectral feature is not observed for classic β-sheet structures, the FT-IR spectra of the aromatic substituted peptides confirm the secondary structure as βsheet.36 Table 1 summarizes the various peptides used in this study, their chemical properties, and the efficiency with which they disperse CoMoCAT and HiPco SWNTs. Note that the hydrophobic partition coefficient of each amino acid listed in Table 1 does not necessarily correlate directly to the relative comparative hydrophobic character of the peptides, which are sometimes found to fall outside the relative hydrophobic trends predicted by hydrophobicity of the constituent amino acids.41 However, relative peptide hydrophobicity can be characterized by the corresponding HPLC retention time. The Ac-(XKXE)2NH2 peptide retention times followed the trend Val < Ile < Leu < Phe < Trp < 1Nal < 2Nal < Cha < F5-Phe; the peptides listed in Table 1 are thus listed in order of increasing peptide hydrophobicity. The fluorescence QY of the samples was used as a measure of SWNT dispersion efficiency by comparing the QY to those of standard dispersing agents SDBS, SDS, and ssDNA of the sequence (GT)30. As shown in Table 2, SDBS

dispersed SWNTs yielded the brightest samples with a QY of ∼0.2%, while the peptide−nanotube samples have QY values ranging from ∼0.02 to ∼0.1% (Table 1). Error bars were calculated by repeating the experiments three times. The QY was measured using 632.98 nm excitation; due to the narrow range of λ22 wavelengths for CoMoCAT SWNTs structures,42 this QY value is a more accurate measure of the fluorescence efficiency in comparison to the HiPco QY, which has a wider range of λ22 wavelengths due to the variety of structures.43 The HiPco value was included for comparison to those samples that only dispersed HiPco nanotubes. The PL QY for SWNT solutions dispersed with peptides is of comparable fluorescence efficiency as those dispersed with ssDNA and SDS (∼0.07% to ∼0.1%) but in an absolute sense is quite low.45 The low QY may be due to a lack of appreciable nanotube surface coverage by the peptides or the presence of nanotube bundles caused by inefficient dispersion. To investigate the possibility of reduced surface coverage, the reducing agent dithiothreitol (DTT) was added to the peptidedispersed SWNTs to see whether an increase in the fluorescence QY occurred.46 The motivation for adding DTT was that fluorescence enhancement was previously observed in solutions of ssDNA-wrapped SWNTs through the addition of reducing agents such as DTT, Trolox, and β-mercaptoethanol;46 in contrast, SWNTs dispersed with SDBS exhibited little to no fluorescence enhancement upon the addition of these reducing agents. Since ssDNA has poor SWNT surface coverage, the brightening effect is believed to be due to passivation of defect sites along the exposed SWNT sidewall. Interestingly, the peptide-dispersed SWNTs did not exhibit any fluorescence enhancement through the addition of DTT, suggesting that the SWNTs do not have significant exposure to solvent. It is therefore unlikely that the peptides have insufficient surface coverage, and the low QY is more likely due to the presence of nanotube bundles arising from the inability to disperse SWNTs well in water.

Table 2. Dispersion Efficiency of SWNTs Suspended in Standard Surfactants surfactant

CoMoCAT QYa (%)

HiPco QYa (%)

SDBS SDS ssDNA (GT)30

0.264 ± 0.044 0.099 ± 0.040 0.120 ± 0.042

0.229 ± 0.052 0.078 ± 0.007 0.085 ± 0.027

a

QY values calculated using IR-125 in DMSO as a reference dye with 632.98 nm excitation.

Figure 2. Absorption spectra of (a) CoMoCAT and (b) HiPco SWNTs dispersed by the various Ac-(XKXE)2-NH2 peptide variants and the standard surfactants SDBS, SDS, and ssDNA. Each spectrum is normalized to the E11 peak of maximum intensity ((6,5) and (9,4) for CoMoCAT and HiPco, respectively) and offset for clarity. 5938

dx.doi.org/10.1021/jp410870y | J. Phys. Chem. C 2014, 118, 5935−5944

The Journal of Physical Chemistry C

Article

Figure 3. Normalized fluorescence intensities of each SWNT chirality in a CoMoCAT sample solubilized by the various surfactants and peptides used in this study. The intensities are taken from the corresponding PLE map normalized to the (6,5) peak. Only SWNT structures that could be spectrally resolved by at least one dispersing agent are displayed.

Figure 4. PLE maps of CoMoCAT SWNTs suspended by (a) SDBS, (b) Ac-(IKIE)2-NH2, and (c) Ac-(FKFE)2-NH2 and HiPco SWNTs suspended by (d) SDBS, (e) Ac-(IKIE)2-NH2, and (f) Ac-(FKFE)2-NH2. Each map is normalized to the peak of maximum intensity.

The quality of the peptide−nanotube dispersion can also be assessed by the combination of absorption and PLE spectroscopies. Figure 2 shows the absorption spectra of CoMoCAT (Figure 2a) and HiPco (Figure 2b) SWNTs dispersed by all peptides and standard surfactants. Well-resolved SWNT absorption peaks such as those observed with SDBS and SDS

dispersed SWNTs is indicative of efficient dispersion of individual SWNTs, compared to broad peaks which is indicative of SWNT bundles. From Figure 2, it is evident that the absorption peaks of SWNTs dispersed by Ile, Leu, and Phe peptide variants are comparable to those of SDBS, SDS, and ssDNA; this similarity indicates that the peptide−nanotube 5939

dx.doi.org/10.1021/jp410870y | J. Phys. Chem. C 2014, 118, 5935−5944

The Journal of Physical Chemistry C

Article

(FKFE)2 and (WKWE)2. The PLE maps of the aromatic Phe peptide variant (Figure 4c,f) shows that the peptide disperses both CoMoCAT and HiPco SWNTs efficiently. The aromatic Trp variant only disperses HiPco SWNTs and does so with low efficiency (QY = 0.035 ± 0.013%). Broad absorption peaks are observed in Figure 2b, indicative of nanotube bundles; while fluorescence from the SWNTs was able to be detected, the fluorescence intensity was insufficient for PLE analysis. When comparing the (FKFE)2 HiPco PLE map in Figure 4 to those of (IKIE)2 and the standard SDBS dispersed SWNTs, it is clear that there is an enhancement of the small diameter (8,3) and (6,5) structures. The enhancement of these nanotube structures is not observed with any other peptide variant (see Figures S3−S6 in the Supporting Information for HiPco chirality distribution and all PLE maps). (1NalK1NalE)2 and (2NalK2NalE)2. The 1Nal and 2Nal peptide variants (Figure 1b,c) are both highly aromatic and hydrophobic. While the 2Nal peptide variant dispersed SWNTs with low efficiency (as indicated by the low fluorescence QY), it was interesting to discover the inability of the 1Nal variant to disperse either nanotube type. The low dispersion efficiency suggests the importance of sterics and ring location on SWNT interaction in comparison to aromatic and hydrophobic character. (FKFE)2 and (ChaKChaE)2. The aromatic Phe variant efficiently dispersed both CoMoCAT and HiPco SWNTs, while the nonaromatic yet highly hydrophobic Cha variant only dispersed CoMoCAT. We hypothesized that either the Cha variant would exhibit enhanced dispersing ability due to favorable hydrophobic interactions or the Cha variant would not interact with SWNTs due to the lack of aromatic π−π interactions. However, while (ChaKChaE)2 was slightly less efficient at solubilizing SWNTs, both peptides dispersed SWNTs with comparable QYs, and thus neither anticipated result was observed. Thus, we conclude that the different electronic properties do not have a strong impact on the peptides ability to interact with the nanotube sidewall. (FKFE)2 and (F5FKF5FE)2. Pentafluorophenylalanine was used to study the effects of increased amino acid electronegativity on nanotube dispersion. Calculations have shown that the interactions between hexafluorobenzene and benzene (−5.38 kcal/mol) is about twice as favorable as the interactions between a benzene dimer (−2.48 kcal/mol).47 Because of this enhanced interaction of monomers, it was surprising to find that the fluorinated Ac-(F5FKF5FE)2-NH2 did not interact with the sp2 carbon sidewall and disperse SWNTs while Ac(FKFE)2-NH2 did. It should be noted that these calculations were performed with a benzene dimer and not with a nanotube sidewall, which introduces a curvature into the sp2 carbon structure. This interaction may not be favorable and may be the cause of the F5-Phe variant’s inability to disperse SWNTs. In addition, previous studies have observed an increase in nanotube dispersion as the electron-donating character on a phenyl ring is enhanced.22,25 The fluorine groups on the phenyl ring of F5-Phe are electron-withdrawing, which may explain the inability of the Ac-(F5FKF5FE)2-NH2 to disperse SWNTs. Additionally, in the context of peptides, the ideal geometry for optimal quadrupolar interactions between the F5-Phe side chain and the SWNT sidewall may not be accessible. Aromaticity. Increased aromatic content on peptides was reported to result in more efficient SWNT solubilization due to favorable π−π interactions with the nanotube sidewall.23,24 However, when comparing the fluorescence QY and PLE

dispersions are of comparable quality to SWNTs dispersed by the standard surfactants. However, SWNTs dispersed by Val, Trp, 2Nal, and Cha peptide variants show broad, less resolved absorption features, an indication of nanotube bundling, and overall lower quality dispersions. Photoluminescence excitation spectroscopy is an invaluable tool for characterizing SWNT dispersions because it allows for the direct observation of the nanotube structures that were dispersed in the sample, making it evident whether certain chiralities are favored with specific peptide sequences.1 In addition, by normalizing to the peak of maximum intensity, the relative abundance of each structure in a particular sample can be determined. PLE spectroscopy was performed on the peptide dispersed samples and the respective 2D contour maps of the various nanotube fluorescence peaks are summarized in Figure 3. These contour maps show the normalized fluorescence intensity for every SWNT structure in a CoMoCAT sample that could be spectrally resolved by at least one dispersing agent. It is evident that all the peptides disperse SWNTs comparable to ionic surfactants and ssDNA and in fact solubilize some chiralities more efficiently. For example, an enhancement of the PLE peaks for the (8,3) and (7,5) structures is observed for SWNTs suspended using the Ile and Cha peptide variants compared to SDBS, SDS, and ssDNA. However, the limited chirality distribution of CoMoCAT SWNTs makes it difficult to truly recognize chirality specificity between the various peptides. Since HiPco SWNTs have a wide distribution of chiralities within a narrow range of emission wavelengths, dispersion of some SWNT (n,m) structures over others is easily recognizable (Figure S3 in the Supporting Information). (VKVE)2, (IKIE)2, and (LKLE)2. The nonaromatic and least hydrophobic peptide variants dispersed SWNTs more efficiently than most of the aromatic-substituted peptides. In particular, the Ile and Leu variants yielded samples of relatively high QY (0.108 ± 0.030% and 0.103 ± 0.048% for CoMoCAT nanotubes, respectively) and well-resolved PLE maps with minimal energy transfer (see Figure 4 for Ile and Figure S5 in the Supporting Information for Leu). The relatively high QY implies efficient peptide interaction with the nanotube sidewall, resulting in the dispersion of individual SWNTs rather than bundles. In addition, the HiPco PLE map of the Ile variant shows that the peptide variant preferentially solubilizes (9,4) SWNTs relative to other chiral species. Other nanotube structures that are enhanced with the standard surfactant SDBS (Figure 4a,d) such as (7,6) and (8,6) are not nearly as abundant in the (IKIE)2 dispersed nanotubes (Figure 4b,e). The Leu peptide variant does not show this same structural specificity and has relative SWNT structure abundances comparable to those of SDBS. The Val variant dispersed SWNTs in a different manner compared to the Ile and Leu substituted peptides. The PLE map shows broad peaks with energy transfer between SWNT structures, which could be explained by the presence of bundles. This can also be observed in Figure 2, as the absorption peaks for the Val peptide variant is broader than those of the Ile and Leu peptide variants. This would also explain the lower fluorescence QY observed with (VKVE)2, with a value of 0.066 ± 0.056% for CoMoCAT SWNTs. The PLE map of HiPco SWNTs dispersed using the Val variant shows an enhancement in the relative abundances of (7,5) and (7,6) SWNTs compared to SDBS, indicating preferential interaction with those chiral species. 5940

dx.doi.org/10.1021/jp410870y | J. Phys. Chem. C 2014, 118, 5935−5944

The Journal of Physical Chemistry C

Article

fluorescence intensities of the various peptides used in this study, it was surprising to find that aromaticity did not correlate with either increased QY or narrowed PLE absorption peaks, both of which indicate higher quality SWNT dispersions. In fact, some nonaromatic amino acids were found to solubilize SWNTs better than aromatic amino acids, and some aromatic amino acids were not successful at dispersing SWNTs at all (see Table 1). For example, the Phe variant efficiently dispersed SWNTs, while the more aromatic Trp-substituted peptide dispersed only HiPco SWNTs and not CoMoCAT, although the QY of the suspension was low, indicating poor quality dispersion. The aromatic nonnatural amino acid variants F5-Phe and 1Nal were not successful at solubilizing SWNTs. Interestingly, while the 1Nal variant did not disperse SWNTs, the 2Nal variant dispersed both CoMoCAT and HiPco SWNTs, albeit with low QY. These results were surprising not only because the aromatic residues did not enhance the peptide’s interaction with SWNTs, but because the two naphthylalanine derivatives, which possess the same electronic properties, yielded distinctly different solubilization efficiencies for the two SWNT types. On the other hand, all nonaromatic amino acid substituted peptides, (IKIE)2, (LKLE)2, (VKVE)2, and (ChaKChaE)2, efficiently dispersed SWNTs. In particular, the Ile and Leu variants dispersed SWNTs very well and yielded well-resolved PLE maps (see Figures S4−S6 in the Supporting Information). It is possible that sterics prevent efficient interaction between the aromatic amino acids and the nanotube sidewall, rendering small aliphatic amino acid peptides more efficient at dispersing SWNTs. These results indicate that π−π interactions with the nanotube sidewall are not the main determinant for peptide interaction with SWNTs, suggesting that other peptide properties must be considered. Hydrophobicity. The results of peptides with enhanced hydrophobic character mimic those of aromaticity; highly hydrophobic peptide variants did not solubilize SWNTs efficiently. Surprisingly, in comparison to the highly hydrophobic variants such as 2Nal, the relatively less hydrophobic (although still hydrophobic relative to all the natural amino acids) Ile, Leu, and Phe peptide variants resulted in SWNT dispersions with higher QYs. In addition, Ile, Leu, and Phe yielded well-dispersed SWNTs as displayed in the highly resolved PLE maps (Figure 4 and Figures S4−S6 in the Supporting Information). Interestingly, although the Phe and Trp variants possess aromatic character, the Phe variant dispersed SWNTs more efficiently than the moderately more hydrophobic Trp variant. For naturally occurring amino acids, normally it is very difficult to separate the effect of aromatic character versus hydrophobic character on the optical properties of the SWNT dispersion. However, by utilizing the wide range of properties available with nonnatural amino acids, a highly hydrophobic structure that lacks aromaticity can be substituted into Ac(XKXE)2-NH2 in order to directly probe the role of hydrophobic character in SWNT dispersion. The nonnatural amino acid Cha has similar spatial structure as Phe (Figure 1a) and retains significant hydrophobic character, yet it is not aromatic. The steric profiles of Phe and Cha are distinctly different, however. Comparing the Phe and Cha peptide variants gives insight into the role of aromatic vs hydrophobic interactions in SWNT solubilization. Interestingly, (FKFE)2 efficiently suspended both CoMoCAT and HiPco SWNTs, while (ChaKChaE)2 only suspended CoMoCAT. For CoMo-

CAT samples, (FKFE)2 has a QY of 0.116 ± 0.025% and (ChaKChaE)2 has comparable QY of 0.090 ± 0.012%, indicating similar dispersion efficiencies for the two peptides. It was surprising to find that lack of aromaticity did not eliminate nanotube interaction, and increasing the hydrophobic character did not markedly enhance the interaction either. These findings suggest that sterics and the manner in which the ring binds to the peptide backbone have an important role in nanotube interaction. These results along with those of the natural amino acids indicate that aromaticity and high hydrophobicity are not essential for effective nanotube solubilization by β-sheet peptides. Qualitative Assessment of the Peptides Self-Assembled Structure. In order to fully understand how the peptide variants interact with SWNTs in the suspension, other peptide properties must be taken into consideration. It is widely known that amphipathic β-sheet peptides with alternating hydrophobic and hydrophilic residues undergo self-assembly into amyloid-like nanoribbons.38,48 The Ac-(FKFE)2-NH2 peptide in particular has been extensively studied as a selfassembling peptide that forms soluble β-sheet structures when in water.36,49−51 The properties of self-assembled materials derived from Ac-(XKXE)2-NH2 β-sheet peptides is dramatically influenced by the properties of the amino acids in the X position.36 The hydrophobicity, aromaticity, and β-sheet propensity of amino acids in position X can affect both selfassembly propensity and the morphology of the self-assembled materials. Thus, it is possible that nanotube dispersion by these peptides is also influenced by the self-assembly properties of these materials; perhaps nanotubes are dispersed not by the monomeric β-sheet peptides, but by assembled forms of these peptides.52−54 For example, the ability of β-sheet peptides to self-assemble into nanofibers has been shown to increase the amount of SWNTs dispersed due to the nanotube surface acting as a template for self-assembly.17 Conversely, selfassembled nanofibrils may be unable to efficiently disperse SWNTs. In this case, dispersion would only be possible with the small percentage of monomeric peptide that remains unincorporated into assembled peptide nanoribbons. The peptide self-assembled structures in absence of the SWNTs were characterized using FT-IR spectroscopy, CD spectroscopy, and TEM (Figure S7 in the Supporting Information). FT-IR and CD spectroscopy were used to confirm the secondary structure of all peptides: a maximum at 1620 cm−1 in the FT-IR spectra (Figure S1 and Table S1 in the Supporting Information) and a minimum at 218 nm in the CD spectra (Figure S2 and Table S1 in the Supporting Information) are known signatures of a β-sheet structure. All peptides also formed fibrils in the absence of SWNTs (Figure S7 and Table S2 in the Supporting Information); however, the question remains whether the peptides form β-sheet structures and/or fibrils during or after processing with the SWNTs and exactly what form of the peptide interacts with and disperses the SWNTs (see Figures S8 and S9 in the Supporting Information for representative TEM images of peptidedispersed SWNTs). To better understand the secondary structure after SWNT solubilization, the CD spectra of the peptides acting as dispersing agents in the presence of CoMoCAT and HiPco SWNTs were collected (Figure S2 in the Supporting Information). CD is an average of the peptide’s secondary structure, making it difficult to deduce quantitative conclusions on the peptide structure. However, qualitative observations of 5941

dx.doi.org/10.1021/jp410870y | J. Phys. Chem. C 2014, 118, 5935−5944

The Journal of Physical Chemistry C

Article

images of the two peptides, where the 1Nal variant forms rigid fibrils of 3.38 ± 0.33 nm widths and the 2Nal variant forms flat tape fibrils of 8.07 ± 1.01 nm widths (Figures S7f and S7g in the Supporting Information, respectively). Although (1NalK1NalE)2 did not disperse either CoMoCAT or HiPco SWNTs, CD measurements of the supernatant of the sonicated peptide−nanotube samples indicated that it contained some of the (1NalK1NalE)2 peptide; this indicates that the 1Nal variant did not interact well with the SWNTs. Indeed, (1NalK1NalE)2 was unable to solubilize SWNTs. Further, a decrease in the CD β-sheet signal of the peptide in the presence of SWNTs implies that there is less β-sheet structure present in the peptide−SWNT dispersions compared to the peptide alone. In stark contrast, the 2Nal variant exhibits enhanced βsheet structure formation in the presence of SWNTs and likewise was able to disperse CoMoCAT SWNTs, although not especially well. The PLE map of (ChaKChaE)2 dispersed CoMoCAT SWNTs indicates that the peptide does not exhibit a preference for solubilizing any SWNT chirality. Out of all tested peptides and standards, the Cha variant dispersed the highest abundance of (8,3), (7,5), (8,4), and (7,6) SWNTs, but there is evidence in the PLE map of energy transfer between SWNT structures. The presence of significant energy transfer is an indication of interaction between nanotubes which may be due to inefficient peptide coverage of the nanotube sidewall and/or the solubilization of bundles. Similar to the Trp variant, no CD signal was detected for the sonicated peptide−HiPco nanotube supernatant. These results are again consistent with the dispersion of SWNT bundles rather than individual nanotubes. Finally, similar to the Trp variant, no peptide was detected in the CD spectrum of the sonicated F5-Phe peptide−nanotube supernatant for either CoMoCAT or HiPco SWNTs. This indicates that after ultracentrifugation no peptide remained in the supernatant, perhaps due to the peptide fibrils interacting with SWNT bundles rather than individual nanotubes that are ultimately centrifuged out of solution during sample preparation, but this can also be attributed to efficient self-assembly of the F5-Phe peptide into nanofibrils.

how the peptide structure changes in the presence of SWNTs can be accurately deduced through changes in CD signal intensity, indicating whether or not an increase in β-sheet, αhelical, or random coil structure occurs. We found the Ile variant likely adopts β-sheet orientations both alone and in the presence of SWNTs. While the Leu variant shows a strong β-sheet CD signal in the absence of SWNTs, a decrease in β-sheet signature in addition to some random coil signal was observed in the presence of SWNTs. The Val variant shows a significant decrease in β-sheet CD signal in the presence of SWNTs compared to the peptide alone. Since the highest quality SWNT suspensions for CoMoCAT SWNTs occurred with the (IKIE)2 and (LKLE)2 peptides, which exhibit a highly ordered, strong β-sheet structure, it is possible that CoMoCAT SWNTs are better dispersed by peptides that are more β-sheet in character. Supporting this argument, the (VKVE)2 peptide has significantly decreased β-sheet structure along with a very rigid selfassembled structure and also does not suspend CoMoCAT SWNTs as well as the Ile or Leu variants. The Trp and Phe peptide variants are interesting to compare because both are highly hydrophobic and aromatic. With regards to CoMoCAT SWNTs, Trp did not result in efficient SWNT solubilization, while the Phe variant efficiently interacted with and dispersed SWNTs. Thus, comparing the self-assembly properties of the Phe and Trp peptide variants provides interesting insight into how the peptides interact with nanotubes. In the absence of SWNTs, the Ac-(FKFE)2-NH2 peptide is known to display polymorphism, assembling into long flat tapes with a width of 7.51 ± 0.73 nm in addition to long helical tapes of 7.46 ± 0.83 nm width and a periodicity of 18.03 ± 0.96 nm (Figure S7d in the Supporting Information). This helical structure is unique to the Phe variant. It is possible that this secondary self-assembled structure of the Phe variant assembles analogous to the helical ssDNA10 around the SWNT circumference and allows for the enhanced dispersion of smaller diameter SWNTs. However, further experiments beyond the scope of this study would need to be performed in order to confirm this speculation. The unique helical self-assembled structure of the Phe peptide variant is vastly different from the rigid tapes formed by the Trp variant. The CD spectrum of the Trp peptide variant in the presence of HiPco SWNTs shows a decrease in β-sheet signal compared to the peptide alone. Interestingly, even though the Trp peptide variant did not disperse CoMoCAT SWNTs, no signal was detected in the CD spectrum of the sonicated peptide−nanotube supernatant, suggesting that no peptide remained in the supernatant after ultracentrifugation. One explanation is that self-assembled nanofibrils derived from these types of amphipathic peptides (Figure S7e in the Supporting Information) sediment upon ultracentrifugation.55 On the other hand, it is also possible that the self-assembled peptide fibrils interact with SWNT bundles rather than individual nanotubes. Since bundles pellet during ultracentrifugation, peptide would not be detected in the supernatant. This would also explain the low fluorescence intensities observed with HiPco SWNTs dispersed with the Trp variant. A comparison of (1NalK1NalE)2 and (2NalK2NalE)2 selfassembled structure is also interesting since 1Nal and 2Nal have identical electronic properties. It is evident from the FT-IR spectra of the 1Nal and 2Nal variants alone that while both peptides exhibit β-sheet structures, the self-assembled structures are distinctly different. This can be observed in the TEM

4. CONCLUSIONS Through both natural and nonnatural amino acid substitution, the properties of the peptide Ac-(XKXE)2-NH2 have been varied to study the interactions with SWNTs. We have shown that the most efficient dispersing peptides were (IKIE)2, (LKLE)2, and (FKFE)2 and that surprisingly no correlation exists between dispersion efficiency and aromaticity and/or hydrophobicity. However, the unique molecular interactions of a given peptide with nanotubes results in the preferential dispersion of varying SWNT chiralities. SWNTs are excellent candidates for many biological applications, but their low QY is a major disadvantage to their integration. Higher fluorescence efficiency is necessary in order to incorporate nanotubes into these applications, and this can be achieved through enhanced interaction between the dispersing agent and the nanotube sidewall. Although the peptides used in this study do not show significant improvement on the poor QY exhibited by most surfactant suspended SWNTs, these findings help us better understand the interactions between peptides and nanotubes and will aid in the development of more efficient biocompatible dispersing agents. 5942

dx.doi.org/10.1021/jp410870y | J. Phys. Chem. C 2014, 118, 5935−5944

The Journal of Physical Chemistry C

■

Article

(11) Nicolosi, V.; Cathcart, H.; Dalton, A. R.; Aherne, D.; Dieckmann, G. R.; Coleman, J. N. Spontaneous Exfoliation of Single-Walled Carbon Nanotubes Dispersed Using a Designed Amphiphilic Peptide. Biomacromolecules 2008, 9, 598−602. (12) Wang, S.; Humphreys, E. S.; Chung, S.-Y.; Delduco, D. F.; Lustig, S. R.; Wang, H.; Parker, K. N.; Rizzo, N. W.; Subramoney, S.; Chiang, Y.-M.; et al. Peptides with Selective Affinity for Carbon Nanotubes. Nat. Mater. 2003, 2, 196−200. (13) Zorbas, V.; Ortiz-Acevedo, A.; Dalton, A. B.; Yoshida, M. M.; Dieckmann, G. R.; Draper, R. K.; Baughman, R. H.; Jose-Yacaman, M.; Musselman, I. H. Preparation and Characterization of Individual Peptide-Wrapped Single-Walled Carbon Nanotubes. J. Am. Chem. Soc. 2004, 126, 7222−7227. (14) Xie, H.; Ortiz-Acevedo, A.; Zorbas, V.; Baughman, R. H.; Draper, R. K.; Musselman, I. H.; Dalton, A. B.; Dieckmann, G. R. Peptide Cross-Linking Modulated Stability and Assembly of PeptideWrapped Single-Walled Carbon Nanotubes. J. Mater. Chem. 2005, 15, 1734−1741. (15) Arnold, M. S.; Guler, M. O.; Hersam, M. C.; Stupp, S. I. Encapsulation of Carbon Nanotubes by Self-Assembling Peptide Amphiphiles. Langmuir 2005, 21, 4705−4709. (16) Witus, L. S.; Rocha, J.-D. R.; Yuwono, V. M.; Paramonov, S. E.; Weisman, R. B.; Hartgerink, J. D. Peptides that Non-Covalently Functionalize Single-Walled Carbon Nanotubes to give Controlled Solubility Characteristics. J. Mater. Chem. 2007, 17, 1909−1915. (17) Tsyboulski, D. A.; Bakota, E. L.; Witus, L. S.; Rocha, J.-D. R.; Hartgerink, J. D.; Weisman, R. B. Self-Assembling Peptide Coatings Designed for Highly Luminescent Suspension of Single-Walled Carbon Nanotubes. J. Am. Chem. Soc. 2008, 130, 17134−17140. (18) Dieckmann, G. R.; Dalton, A. B.; Johnson, P. A.; Razal, J.; Chen, J.; Giordano, G. M.; Muñoz, E.; Musselman, I. H.; Baughman, R. H.; Draper, R. K. Controlled Assembly of Carbon Nanotubes by Designed Amphiphilic Peptide Helices. J. Am. Chem. Soc. 2003, 125, 1770−1777. (19) Pender, M. J.; Sowards, L. A.; Hartgerink, J. D.; Stone, M. O.; Naik, R. R. Peptide-Mediated Formation of Single-Wall Carbon Nanotube Composites. Nano Lett. 2005, 6, 40−44. (20) Su, Z.; Leung, T.; Honek, J. F. Conformational Selectivity of Peptides for Single-Walled Carbon Nanotubes. J. Phys. Chem. B 2006, 110, 23623−23627. (21) Ortiz-Acevedo, A.; Xie, H.; Zorbas, V.; Sampson, W. M.; Dalton, A. B.; Baughman, R. H.; Draper, R. K.; Musselman, I. H.; Dieckmann, G. R. Diameter-Selective Solubilization of Single-Walled Carbon Nanotubes by Reversible Cyclic Peptides. J. Am. Chem. Soc. 2005, 127, 9512−9517. (22) Samarajeewa, D. R.; Dieckmann, G. R.; Nielsen, S. O.; Musselman, I. H. Doping Single-Walled Carbon Nanotubes with Surfactant Peptides Containing Electron-Donor Substituents and Nitrogen Heterocycles. Carbon 2013, 57, 88−98. (23) Zorbas, V.; Smith, A. L.; Xie, H.; Ortiz-Acevedo, A.; Dalton, A. B.; Dieckmann, G. R.; Draper, R. K.; Baughman, R. H.; Musselman, I. H. Importance of Aromatic Content for Peptide/Single-Walled Carbon Nanotube Interactions. J. Am. Chem. Soc. 2005, 127, 12323−12328. (24) Xie, H.; Becraft, E. J.; Baughman, R. H.; Dalton, A. B.; Dieckmann, G. R. Ranking the Affinity of Aromatic Residues for Carbon Nanotubes by Using Designed Surfactant Peptides. J. Pept. Sci. 2008, 14, 139−151. (25) Poenitzsch, V. Z.; Winters, D. C.; Xie, H.; Dieckmann, G. R.; Dalton, A. B.; Musselman, I. H. Effect of Electron-Donating and Electron-Withdrawing Groups on Peptide/Single-Walled Carbon Nanotube Interactions. J. Am. Chem. Soc. 2007, 129, 14724−14732. (26) Su, Z.; Mui, K.; Daub, E.; Leung, T.; Honek, J. Single-Walled Carbon Nanotube Binding Peptides: Probing Tryptophan’s Importance by Unnatural Amino Acid Substitution. J. Phys. Chem. B 2007, 111, 14411−14417. (27) Deshpande, M. S.; Mazumdar, S. Sequence Specific Association of Tryptic Peptides with Multiwalled Carbon Nanotubes: Effect of Localization of Hydrophobic Residues. Biomacromolecules 2012, 13, 1410−1419.

ASSOCIATED CONTENT

S Supporting Information *

FT-IR and CD characterization of peptides; chirality distribution for HiPco SWNTs; PLE maps for all peptides; TEM analysis of peptides; representative TEM images of peptidedispersed SWNTs; HPLC and MALDI-TOF-MS traces for peptide characterization; sample preparation methods for the various surfactants used for comparison. This material is available free of charge via the Internet at http://pubs.acs.org.

■

AUTHOR INFORMATION

Corresponding Author

*E-mail [email protected]; Ph (585) 275-5093 (T.D.K.). Present Addresses

C.J.B.: Department of Chemistry, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599. L.J.N.: Department of Chemistry, Gannon University, Erie, PA 16541. Notes

The authors declare no competing financial interest.

■

ACKNOWLEDGMENTS The authors thank Prof. Oleg Prezhdo and Dr. Vitaly Chaban for their assistance with molecular modeling. The authors gratefully acknowledge the Division of Chemical Sciences, Geosciences, and Biosciences, Office of Basic Energy Sciences of the U.S. Department of Energy through Grant DE-FG0206ER15821 for financial support.

■

REFERENCES

(1) Bachilo, S. M.; Strano, M. S.; Kittrell, C.; Hauge, R. H.; Smalley, R. E.; Weisman, R. B. Structure-Assigned Optical Spectra of SingleWalled Carbon Nanotubes. Science 2002, 298, 2361−2366. (2) O’Connell, M. J.; Bachilo, S. M.; Huffman, C. B.; Moore, V. C.; Strano, M. S.; Haroz, E. H.; Rialon, K. L.; Boul, P. J.; Noon, W. H.; Kittrell, C.; et al. Band Gap Fluorescence from Individual SingleWalled Carbon Nanotubes. Science 2002, 297, 593−596. (3) Hartschuh, A.; Pedrosa, H. N.; Novotny, L.; Krauss, T. D. Simultaneous Fluorescence and Raman Scattering from Single Carbon Nanotubes. Science 2003, 301, 1354−1356. (4) Carlson, L. J.; Krauss, T. D. Photophysics of Individual SingleWalled Carbon Nanotubes. Acc. Chem. Res. 2008, 41, 235−243. (5) Matarredona, O.; Rhoads, H.; Li, Z.; Harwell, J. H.; Balzano, L.; Resasco, D. E. Dispersion of Single-Walled Carbon Nanotubes in Aqueous Solutions of the Anionic Surfactant NaDDBS. J. Phys. Chem. B 2003, 107, 13357−13367. (6) Wenseleers, W.; Vlasov, I. I.; Goovaerts, E.; Obraztsova, E. D.; Lobach, A. S.; Bouwen, A. Efficient Isolation and Solubilization of Pristine Single-Walled Nanotubes in Bile Salt Micelles. Adv. Funct. Mater. 2004, 14, 1105−1112. (7) O’Connell, M. J.; Boul, P.; Ericson, L. M.; Huffman, C.; Wang, Y.; Haroz, E.; Kuper, C.; Tour, J.; Ausman, K. D.; Smalley, R. E. Reversible Water-Solubilization of Single-Walled Carbon Nanotubes by Polymer Wrapping. Chem. Phys. Lett. 2001, 342, 265−271. (8) Nish, A.; Hwang, J.-Y.; Doig, J.; Nicholas, R. J. Highly Selective Dispersion of Single-Walled Carbon Nanotubes Using Aromatic Polymers. Nat. Nanotechnol. 2007, 2, 640−646. (9) Zheng, M.; Jagota, A.; Semke, E. D.; Diner, B. A.; McLean, R. S.; Lustig, S. R.; Richardson, R. E.; Tassi, N. G. DNA-Assisted Dispersion and Separation of Carbon Nanotubes. Nat. Mater. 2003, 2, 338−342. (10) Tu, X.; Manohar, S.; Jagota, A.; Zheng, M. DNA Sequence Motifs for Structure-Specific Recognition and Separation of Carbon Nanotubes. Nature 2009, 460, 250−253. 5943

dx.doi.org/10.1021/jp410870y | J. Phys. Chem. C 2014, 118, 5935−5944

The Journal of Physical Chemistry C

Article

(28) Hashida, Y.; Umeyama, T.; Mihara, J.; Imahori, H.; Tsujimoto, M.; Isoda, S.; Takano, M.; Hashida, M. Development of a Novel Composite Material with Carbon Nanotubes Assisted by SelfAssembled Peptides Designed in Conjunction with β-Sheet Formation. J. Pharm. Sci. 2012, 101, 3398−3412. (29) Samarajeewa, D. R.; Dieckmann, G. R.; Nielsen, S. O.; Musselman, I. H. Modifying the Electronic Properties of SingleWalled Carbon Nanotubes Using Designed Surfactant Peptides. Nanoscale 2012, 4, 4544−4554. (30) Salzmann, C. G.; Ward, M. A. H.; Jacobs, R. M. J.; Tobias, G.; Green, M. L. H. Interaction of Tyrosine-, Tryptophan-, and LysineContaining Polypeptides with Single-Wall Carbon Nanotubes and Its Relevance for the Rational Design of Dispersing Agents. J. Phys. Chem. C 2007, 111, 18520−18524. (31) Jeong, W.-j.; Lim, Y.-b. Combination Self-Assembly of β-Sheet Peptides and Carbon Nanotubes: Functionalizing Carbon Nanotubes with Bioactive β-Sheet Block Copolypeptides. Macromol. Biosci. 2012, 12, 49−54. (32) Sheikholeslam, M.; Pritzker, M.; Chen, P. Dispersion of Multiwalled Carbon Nanotubes in Water Using Ionic-Complementary Peptides. Langmuir 2012, 28, 12550−12556. (33) Muñoz, E.; Sreelatha, A.; Garriga, R.; Baughman, R. H.; Goux, W. J. Amyloidogenic Peptide/Single-Walled Carbon Nanotube Composites Based on Tau-Protein-Related Peptides Derived from AcPHF6: Preparation and Dispersive Properties. J. Phys. Chem. B 2013, 117, 7593−7604. (34) Jeong, W.-j.; Choi, S.-j.; Choi, J. S.; Lim, Y.-b. Chameleon-like Self-Assembling Peptides for Adaptable Biorecognition Nanohybrids. ACS Nano 2013, 7, 6850−6857. (35) Gazit, E. A Possible Role for π-Stacking in the Self-Assembly of Amyloid Fibrils. FASEB J. 2002, 16, 77−83. (36) Bowerman, C. J.; Ryan, D. M.; Nissan, D. A.; Nilsson, B. L. The Effect of Increasing Hydrophobicity on the Self-Assembly of Amphipathic β-Sheet Peptides. Mol. BioSyst. 2009, 5, 1058−1069. (37) Bowerman, C. J.; Liyanage, W.; Federation, A. J.; Nilsson, B. L. Tuning β-Sheet Peptide Self-Assembly and Hydrogelation Behavior by Modification of Sequence Hydrophobicity and Aromaticity. Biomacromolecules 2011, 12, 2735−2745. (38) Bowerman, C. J.; Nilsson, B. L. Review Self-Assembly of Amphipathic β-Sheet Peptides: Insights and Applications. Pept. Sci. 2012, 98, 169−184. (39) O’Nuallain, B.; Thakur, A. K.; Williams, A. D.; Bhattacharyya, A. M.; Chen, S.; Thiagarajan, G.; Wetzel, R.; Indu, K.; Ronald, W. Kinetics and Thermodynamics of Amyloid Assembly Using a HighPerformance Liquid Chromatography-Based Sedimentation Assay. In Methods in Enzymology; Academic Press: New York, 2006; Vol. 413, pp 34−74. (40) Lakowicz, J. R. Principles of Fluorescence Spectroscopy, 3rd ed.; Springer: New York, 2006. (41) Costantini, S.; Colonna, G.; Facchiano, A. M. Amino Acid Propensities for Secondary Structures are Influenced by the Protein Structural Class. Biochem. Biophys. Res. Commun. 2006, 342, 441−451. (42) Bachilo, S. M.; Balzano, L.; Herrera, J. E.; Pompeo, F.; Resasco, D. E.; Weisman, R. B. Narrow (n,m)-Distribution of Single-Walled Carbon Nanotubes Grown Using a Solid Supported Catalyst. J. Am. Chem. Soc. 2003, 125, 11186−11187. (43) Nikolaev, P.; Bronikowski, M. J.; Bradley, R. K.; Rohmund, F.; Colbert, D. T.; Smith, K. A.; Smalley, R. E. Gas-Phase Catalytic Growth of Single-Walled Carbon Nanotubes from Carbon Monoxide. Chem. Phys. Lett. 1999, 313, 91−97. (44) Fauchere, J.-L.; Charton, M.; Kier, L. B.; Verloop, A.; Pliska, V. Amino Acid Side Chain Parameters for Correlation Studies in Biology and Pharmacology. Int. J. Pept. Protein Res. 1988, 32, 269−278. (45) Carlson, L. J.; Maccagnano, S. E.; Zheng, M.; Silcox, J.; Krauss, T. D. Fluorescence Efficiency of Individual Carbon Nanotubes. Nano Lett. 2007, 7, 3698−3703. (46) Lee, A. J.; Wang, X.; Carlson, L. J.; Smyder, J. A.; Loesch, B.; Tu, X.; Zheng, M.; Krauss, T. D. Bright Fluorescence from Individual Single-Walled Carbon Nanotubes. Nano Lett. 2011, 11, 1636−1640.

(47) Tsuzuki, S.; Uchimaru, T.; Mikami, M. Intermolecular Interaction between Hexafluorobenzene and Benzene: Ab Initio Calculations Including CCSD(T) Level Electron Correlation Correction. J. Phys. Chem. A 2006, 110, 2027−2033. (48) Hamley, I. W. Peptide Fibrillization. Angew. Chem., Int. Ed. 2007, 46, 8128−8147. (49) Marini, D. M.; Hwang, W.; Lauffenburger, D. A.; Zhang, S.; Kamm, R. D. Left-Handed Helical Ribbon Intermediates in the SelfAssembly of a β-Sheet Peptide. Nano Lett. 2002, 2, 295−299. (50) Fishwick, C. W. G.; Beevers, A. J.; Carrick, L. M.; Whitehouse, C. D.; Aggeli, A.; Boden, N. Structures of Helical β-Tapes and Twisted Ribbons: The Role of Side-Chain Interactions on Twist and Bend Behavior. Nano Lett. 2003, 3, 1475−1479. (51) Hwang, W. M.; Marini, D. M.; Kamm, R. D.; Zhang, S. Q. Supramolecular Structure of Helical Ribbons Self-Assembled from a βSheet Peptide. J. Chem. Phys. 2003, 118, 389−397. (52) Senguen, F. T.; Lee, N. R.; Gu, X.; Ryan, D. M.; Doran, T. M.; Anderson, E. A.; Nilsson, B. L. Probing Aromatic, Hydrophobic, and Steric Effects on the Self-Assembly of an Amyloid-β Fragment Peptide. Mol. BioSyst. 2011, 7, 486−496. (53) Senguen, F. T.; Doran, T. M.; Anderson, E. A.; Nilsson, B. L. Clarifying the Influence of Core Amino Acid Hydrophobicity, Secondary Structure Propensity, and Molecular Volume on Amyloidβ 16−22 Self-Assembly. Mol. BioSyst. 2011, 7, 497−510. (54) Doran, T. M.; Kamens, A. J.; Byrnes, N. K.; Nilsson, B. L. Role of Amino Acid Hydrophobicity, Aromaticity, and Molecular Volume on IAPP(20−29) Amyloid Self-Assembly. Proteins: Struct., Funct., Bioinf. 2012, 80, 1053−1065. (55) Lee, N. R.; Bowerman, C. J.; Nilsson, B. L. Sequence Length Determinants for Self-Assembly of Amphipathic β-Sheet Peptides. Pept. Sci. 2013, 100, 738−750.

5944

dx.doi.org/10.1021/jp410870y | J. Phys. Chem. C 2014, 118, 5935−5944