Carbon Nanotubes Facilitate Oxidation of Cysteine Residues of

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Carbon Nanotubes Facilitate Oxidation of Cysteine Residues of Proteins Atsushi Hirano, Tomoshi Kameda, Momoyo Wada, Takeshi Tanaka, and Hiromichi Kataura J. Phys. Chem. Lett., Just Accepted Manuscript • DOI: 10.1021/acs.jpclett.7b02157 • Publication Date (Web): 04 Oct 2017 Downloaded from http://pubs.acs.org on October 5, 2017

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The Journal of Physical Chemistry Letters

Carbon Nanotubes Facilitate Oxidation of Cysteine Residues of Proteins Atsushi Hirano,*,† Tomoshi Kameda,‡ Momoyo Wada,† Takeshi Tanaka,† Hiromichi Kataura† †

Nanomaterials Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Ibaraki 305-8565, Japan

‡

Artificial Intelligence Research Center, National Institute of Advanced Industrial Science and Technology (AIST), Koto, Tokyo 135-0064, Japan

AUTHOR INFORMATION Corresponding Author *E-mail: [email protected]

ACS Paragon Plus Environment

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ABSTRACT. The adsorption of proteins onto nanoparticles such as carbon nanotubes (CNTs) governs the early stages of nanoparticle uptake into biological systems. Previous studies regarding these adsorption processes have primarily focused on the physical interactions between proteins and nanoparticles. In this study, using reduced lysozyme and intact human serum albumin in aqueous solutions, we demonstrated that CNTs interact chemically with proteins. The CNTs induce the oxidation of cysteine residues of the proteins, which is accounted for by charge transfer from the sulfhydryl groups of the cysteine residues to the CNTs. The redox reaction simultaneously suppresses the intermolecular association of proteins via disulfide bonds. These results suggest that CNTs can affect the folding and oxidation degree of proteins in biological systems such as blood and cytosol.

TOC GRAPHICS


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Nanomaterials undergo protein adsorption in the early stages of their uptake into biological systems. The protein layers formed around them are called the “protein corona”.1 There is an urgent need to determine and predict the components of the protein corona, recently termed the “protein coronome”,2 since they are associated with biological effects, including cellular internalization and long-term fate, which differ from those of pristine nanomaterials.3 Approaches to achieve this goal include proteomics and interactomics, which provide a comprehensive understanding of the protein components and protein–protein interactions.4 Although these approaches are useful to identify the protein coronas for certain targets, they rarely predict results under other conditions. To predict the components and conformation of the protein corona, it is necessary to elucidate the fundamental mechanism of the interactions between proteins and nanomaterial surfaces. Carbon nanotubes are among the most intensively explored nanomaterials and are of interest in various applications, such as electronic and optical devices, biosensors and drug carriers. However, there are increasing concerns regarding their biological effects. Although previous studies have addressed the physical interactions between proteins and nanomaterials to clarify the mechanism of formation of the protein corona,5-8 little work has addressed their chemical reactions, including intermolecular electron transfer. Since the oxidation potential (Eox) of generally available CNTs is less than approximately 1 V (vs. normal hydrogen electrode (NHE)),9 CNTs undergo redox reactions that are governed by the O2,H+/H2O couple and depend on the pH values in aqueous solutions as follows:10,11 4(e−h+)CNT + O2 + 4H+ ⇌ 4(h+)CNT + 2H2O (1) where h+ and e− represent a hole and an electron in a CNT, respectively. CNTs with a relatively small diameter, typically ca. 1 nm, are oxidized at acidic to neutral pH values.12 In fact, our previous study demonstrated that CNTs oxidized by the O2,H+/H2O couple receive


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electrons from thiols, such as cysteine, dithiothreitol (DTT) and glutathione, thereby leading to disulfide bond formation, i.e., oxidation of the sulfhydryl groups.13 It remains unclear whether such a redox reaction is possible for proteins with free cysteine residues. The oxidation of cysteine residues in proteins, such as serum albumin, can affect the homeostasis of biological systems.14 In this study, we tested the redox reaction of sulfhydryl groups of protein cysteine residues with CNTs. Specifically, we predicted that the free cysteine residues would be oxidized by the CNTs. We used hen egg white lysozyme as our first model protein because it has eight cysteine residues. We prepared “reduced lysozyme” and “S-alkylated lysozyme” as a reactive sample and a negative control sample, respectively, to examine the reactivity of the cysteine residues (Scheme 1). The reduced lysozyme was produced by the addition of DTT to a native lysozyme solution, which in principle should result in the production of eight free cysteine residues (Scheme 1). DTT was sufficiently removed by dialysis (Figure S1). The S-alkylation of the reduced lysozyme was performed using N-ethylmaleimide (NEM). NEM itself has no effect on the redox chemistry of the CNTs (Figure S2). The CNTs used in this study were single-wall CNTs of ca. 1-nm diameter including metallic and semiconducting species, which were synthesized using the high-pressure catalytic CO (HiPco) decomposition method.15 The CNTs were purified in advance by dispersion, centrifugation and subsequent washing processes to remove catalytic metal particles and soluble impurities. The native, reduced and S-alkylated lysozyme solutions were mixed with the CNT dispersions to examine the chemical reactions between the proteins and the CNTs. Notably, the remaining urea and SDS affected the secondary structure of lysozyme (Figure S3).


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Scheme 1. Preparation of reduced and S-alkylated lysozyme.a

a

The structure of native lysozyme was obtained from the Protein Data Bank (PDB 1HEL). The blue curved line indicates the peptide backbone of lysozyme. The numerals on the peptide backbone indicate the positions of cysteine (Cys) residues. The reaction in the bracket describes the alkylation of cysteine residues of the reduced lysozyme using NEM, leading to inactivation of the residues.

The mixtures of each protein with CNTs were analyzed by absorption spectroscopy. The absorption spectra of the CNTs showed typical peaks assigned to the first and second optical transitions of metallic and semiconducting CNTs (Figure S4). The addition of the proteins to the CNT dispersions resulted in spectral changes in the wavelength region of 900–1300 nm, which corresponds to the first optical transition band of the semiconducting CNTs (S11 band). The semiconducting CNTs in the sample included (6,5), (8,3), (7,5), (8,4), (10,2), (7,6), (9,4), (10,3), (8,6), (9,5), (8,7) and (10,5) CNTs, as confirmed by photoluminescence excitation spectra (Figure S5). The native lysozyme was found to show slightly attenuated spectral intensities in the


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S11 band with increasing protein concentration (Figure 1A). Notably, the reduced lysozyme showed increased spectral intensities with increasing protein concentration up to ca. 0.5 µM, whereas S-alkylated lysozyme showed approximately constant spectral intensities (Figure 1B,C). For all samples, the spectral peak positions were redshifted by the addition of the proteins (Figure 1D), which can be attributed to environmental effects, such as the surrounding dielectric


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Figure 1. (A-C) Absorption spectra of the CNTs in the first optical transition band of the semiconducting CNTs in the presence of various concentrations of native lysozyme (A), reduced lysozyme (B), and S-alkylated lysozyme (C). Insets show the main peak intensities near 1250 nm, which correspond to (10,3), (9,5), (8,7) and (10,5) CNTs (Figure S5), as functions of the lysozyme concentration. (D) The absorption spectra of the CNTs in the presence and absence of


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1.0 µM native lysozyme, reduced lysozyme and S-alkylated lysozyme. The gray vertical lines show representative peak positions of the absorption spectrum in the absence of the protein.

constant,16 of the CNTs modulated by the adsorption of the proteins.17 The restoration of the spectral intensities induced by the reduced lysozyme unambiguously indicates reduction of the CNTs caused by charge transfer, i.e., electron doping, from the protein. Larger-diameter CNTs, which basically correspond to peaks at longer wavelengths in the S11 band, showed greater restoration of the intensities, which is consistent with the theoretical understanding of the redox chemistry. Specifically, the larger-diameter CNTs tend to have narrower band gaps and hence lower oxidation potential (Eox),12 which can be more easily oxidized by the O2,H+/H2O couple as follows:18,19 O2 + 4H+ + 4e− ⇌ 2H2O (1.23 V vs NHE)

(2)

The larger-diameter CNTs receive more electrons from the coexisting reductants at higher energy levels,13 which was further supported by the fractional intensities of each spectral peak (Figure S6). The spectral restoration by the addition of the proteins was more evident at an acidic pH (Figure S7). The reduction of the metallic CNTs contained in the sample was further confirmed by the Raman spectra in the region of 200–320 cm-1, which corresponds to the radial breathing mode (RBM) of the CNTs. The S-alkylated lysozyme restored the Raman spectral intensities despite a lack of free cysteine residues (Figure 2A), which can be explained by alteration of the resonance energy20 or by the desorption of dissolved oxygen molecules in the vicinity of the CNTs,21 which


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is caused by the protein adsorption. In any case, the reduced lysozyme caused greater restoration of the spectral intensities than the S-alkylated lysozyme did (Figure 2A). The Raman spectra can be decomposed into seven components using Lorentzian curves (Figure 2). According to the spectral decomposition, the CNT sample was found to contain metallic (10,1), (9,3), (10,4), (9,6) and (8,8) CNTs and semiconducting (10,0) and (9,2) CNTs. Figure 2C shows the peak intensities of each chiral CNT in the presence and absence of 2 µM reduced or S-alkylated lysozyme. The spectral intensities of the metallic CNTs, i.e., (9,3), (10,4) and (9,6) CNTs, were higher in the presence of the reduced lysozyme than in the presence of the S-alkylated one, which is typical of the reduction of CNTs, as mentioned above.12,21 The insignificant effect for the (10,1) CNTs seems to be ascribable to their wider bandgap, specifically their higher oxidation potential (Eox), compared with those of the other metallic CNTs. The marginal effect of the reduced lysozyme on the reduction of the semiconducting species, i.e., (10,0) and (9,2) CNTs, was also concordant with the theoretical understanding of the redox chemistry of CNTs;12 briefly, metallic species have no bandgap and hence unoccupied states to which electrons can transfer in aqueous solutions. The reduction, i.e., electron doping, of the CNTs was further confirmed by measuring the Raman spectra in the G-band region of the CNTs. Metallic CNTs, except for armchair species, have a typical broad G– peak at approximately 1400–1550 cm-1 (Figure 2D), which is believed to be attributable to a frequency-softened and broadened longitudinal optical phonon feature.22 The spectral intensity of the G– peak has been reported to increase with the increasing reduction of the CNTs.12 Here, the spectral intensity of the G– peak was restored by the addition of either reduced or S-alkylated lysozyme (Figure 2D). The effect of the former was more pronounced than that of the latter, which is consistent with the results for the RBM region


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(Figure 2A), demonstrating the reduction of the metallic CNTs by electron transfer from the protein to the CNTs.

Figure 2. (A) RBM Raman spectra of the CNTs in the presence and absence of 2 µM reduced lysozyme or S-alkylated lysozyme. (B) A representative fitting analysis of the RBM Raman spectrum in the presence of 2 µM reduced lysozyme. The black line and the red line in the


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middle graph depict raw data and the fit using Lorentzian curves, respectively; the broken blue line depicts the baseline. The top and bottom graphs show the residuals of the fitting and the decomposed spectra, respectively. The assignment of the CNTs was based on the literature.12 (C) Spectral intensities of each chiral CNTs obtained from the fitting analyses. Error bars represent the standard error from three independent experiments. (D) G-band Raman spectra of the CNTs in the presence and absence of 2 µM reduced lysozyme or S-alkylated lysozyme.

Our previous study addressing the redox chemistry of thiols in combination with CNTs showed that the CNTs induce disulfide bond formation of thiols such as cysteine, DTT and glutathione according to the following equation:13 2(h+)CNT + 2RSH ⇌ 2(e−h+)CNT + RSSR + 2H+

(3)

where RSH and RSSR depict the reduced and oxidized forms of the thiols, respectively. Thus, the electron transfer from the reduced lysozyme to the CNTs was anticipated to be accompanied by disulfide bond formation of the protein. We utilized PEG-PC-Mal to determine the number of remaining free cysteine residues; this material has the ability to confer the polyethylene glycol (PEG) moiety on cysteine residues (Figure 3A), leading to PEGylation of the sulfhydryl groups. Because the molecular weight of the PEG moiety is ca. 5,000 Da, the molecular weight of the protein molecule increases by 5,000 Da per free cysteine residue, which is readily detectable via sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) under non-reducing conditions.23 The CNTs were reacted with the proteins via an ultrasonication process, which exposed reactive CNT surfaces to the proteins. The reduced lysozyme sample without CNT addition and ultrasonication, used as a control sample, had a molecular weight of 14.3 kDa


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before PEGylation (Figure 3B, lane 1); note that there was a small amount of a dimeric form of the lysozyme (28.6 kDa), which may be ascribable to partial oxidation of the protein. The dimeric form was difficult to remove in the preparation process, as similar bands were also observed for S-alkylated lysozyme irrespective of the addition of the CNTs (Figure 3B, lanes 5 and 6). The control sample with PEGylation exhibited multiple bands that could be assigned to the oxidized lysozyme with different numbers of free cysteine residues (Figure 3B, lane 4). Some bands were somewhat broad, which can be attributed to the diversity of the oxidized form; for example, the lysozyme with two free cysteine residues can in principle have 28 isomers because lysozyme has eight cysteine residues. The main components of the PEGylated control sample were partially oxidized lysozyme molecules with 1–4 free cysteine residues. We could not assign the PEGylated control lysozyme with higher numbers (more than four) of free cysteine residues. Importantly, the addition of CNT and subsequent ultrasonication of the reduced lysozyme eliminated the bands corresponding to the lysozyme with free cysteine residues and caused the appearance of a distinct band at approximately 15 kDa (Figure 3A, lane 2). These results suggest that the CNTs facilitate intramolecular oxidation, i.e., disulfide bond formation, of the lysozyme. The pale band at approximately 35 kDa was unidentified at this time. In contrast, in the absence of CNTs, there was a band for the lysozyme with a free cysteine residue as well as one for lysozyme without free cysteine residues (Figure 3B, lane 3). More importantly, a broad band at 40–200 kDa was found under the condition, which clearly indicates that intermolecular disulfide bond formation was preferentially induced during the processes in the absence of the CNTs.


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Figure 3. (A) PEGylation of free cysteine residues. The molecular weight of the PEG moiety is ca. 5,000 Da. PC is a photocleavable linker. (B) SDS-PAGE under non-reducing conditions. PEGylation of the reduced lysozyme shows multiple bands (lane 4), indicating lysozyme with different numbers of free cysteine residues (-SH).

A similar procedure was applied to human serum albumin (HSA), the native form of which has a free cysteine residue (Cys34) on the surface (Figure 4A). This residue undergoes oxidation depending on the oxidative stress in the blood. In addition to native HSA, we prepared Salkylated HSA by the S-alkylation of Cys34 of native HSA. Both native HSA and S-alkylated HSA shifted the absorption peaks, an indication of adsorption of the HSA molecules onto the CNTs. The difference in the spectral intensities of the CNTs between native HSA and Salkylated HSA was small but still significant (Figure 4B). The restoration of the spectral


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intensities by the addition of the S-alkylated HSA is attributable to the removal of the dissolved oxygen in a similar manner to that which occurs in lysozyme. The small difference in the spectra may be associated with the preferential binding of the extended hydrophobic region of HSA to the CNT surfaces, which decreases the reactivity of the single free cysteine of HSA. SDS-PAGE of the HSA clearly indicates the oxidation of the cysteine residue.14 The native HSA has a single band corresponding to a molecular weight of 66.5 kDa, whereas the PEGylated HSA without CNT addition or ultrasonication has a sub-band corresponding to the HSA with a free cysteine (Figure 4C, rightmost lane). There are at least two possible reasons that not all HSA was PEGylated: most of the native HSA had already been oxidized, or the reactivity of the free cysteine residue was too low to be PEGylated due to steric hindrance by the surrounding residues (Figure 4A). Notably, HSA processed by CNT addition and subsequent ultrasonication lacked this sub-band, whereas HSA without the addition of CNTs retained the original band. Despite the elimination of the free cysteine residue in the presence of CNT, the production of a dimeric form of HSA was not observed (data not shown). Thus, the oxidation of a cysteine residue was proposed to occur in HSA, although the resulting oxidation products remain unidentified.


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Figure 4. (A) The structure of HSA (PDB 1AO6) in the vicinity of Cys34 (represented by sticks). (B) Absorption spectra of the CNTs in the presence of 1 µM HSA. Gray vertical lines depict representative peak positions of the absorption spectrum in the absence of the protein. (C) SDSPAGE under non-reducing conditions.

The results shown above suggest that the CNTs preferentially facilitate the intramolecular oxidation of the cysteine residues. This preferential oxidation can be explained by the suppression of lateral interactions between adsorbed proteins by the CNT surface curvature.24 In addition, molecular dynamics (MD) simulation indicated that the reduced lysozyme has a structured conformation even on the CNT sidewall, which can facilitate intramolecular disulfide bond formation (Figure S8 and S9). HSA has a native-like conformation on the CNT sidewall (Figure S10). Because the redox reaction is governed by electron transfer from the cysteine residues to the valence bands of the CNTs, the reactivity should depend on the bandgap of the CNTs. We believe that future studies could use separated metallic and semiconducting CNTs or chiral CNTs to more fully characterize the CNT dependency of this redox reaction. In conclusion, we investigated the oxidation of cysteine residues in proteins using absorption and Raman spectroscopy of the CNTs and SDS-PAGE of the PEGylated proteins. We demonstrated that the CNTs facilitate the intramolecular oxidation of cysteine residues in proteins through the redox reaction between the sulfhydryl groups and the CNTs. The intramolecular oxidation of the proteins simultaneously suppressed their intermolecular association. The CNTs were thus found to affect protein folding and function. We anticipate that the ability of CNTs to oxidize cysteine residues will be reflected in the components and


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conformation of the protein corona that forms around CNTs in the early stages of their uptake into biological systems and, further, in their in vivo dynamics and toxicity.

ASSOCIATED CONTENT Supporting Information The Supporting Information is available free of charge on the ACS Publications website. Experimental details and additional figure (PDF) AUTHOR INFORMATION Corresponding Author *E-mail: [email protected] (A.H.). ORCID Atsushi Hirano: 0000-0002-4138-0308 Notes The authors declare no competing financial interests. ACKNOWLEDGMENT This work was supported by JSPS KAKENHI Grant No. 25220602. REFERENCES (1) Cedervall, T.; Lynch, I.; Lindman, S.; Berggard, T.; Thulin, E.; Nilsson, H.; Dawson, K. A.; Linse, S. Understanding the Nanoparticle-Protein Corona Using Methods to Quantify Exchange


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Rates and Affinities of Proteins for Nanoparticles. Proc. Natl. Acad. Sci. USA 2007, 104, 20502055. (2) Rihn, B. H.; Joubert, O. Comment on "Protein Corona Fingerprinting Predicts the Cellular Interaction of Gold and Silver Nanoparticles". ACS Nano 2015, 9, 5634-5635. (3) Docter, D.; Westmeier, D.; Markiewicz, M.; Stolte, S.; Knauer, S. K.; Stauber, R. H. The Nanoparticle Biomolecule Corona: Lessons Learned-Challenge Accepted? Chem. Soc. Rev. 2015, 44, 6094-6121. (4) Pisani, C.; Gaillard, J. C.; Odorico, M.; Nyalosaso, J. L.; Charnay, C.; Guari, Y.; Chopineau, J.; Devoisselle, J. M.; Armengaud, J.; Prat, O. The Timeline of Corona Formation around Silica Nanocarriers Highlights the Role of the Protein Interactome. Nanoscale 2017, 9, 1840-1851. (5) Antonucci, A.; Kupis-Rozmyslowicz, J.; Boghossian, A. A. Noncovalent Protein and Peptide Functionalization of Single-Walled Carbon Nanotubes for Biodelivery and Optical Sensing Applications. ACS Appl. Mater. Interfaces, 2017, 9, 11321-11331. (6) Calvaresi, M.; Zerbetto, F. The Devil and Holy Water: Protein and Carbon Nanotube Hybrids. Acc. Chem. Res. 2013, 46, 2454-2463. (7) Yang, S. T.; Liu, Y.; Wang, Y. W.; Cao, A. Biosafety and Bioapplication of Nanomaterials by Designing Protein-Nanoparticle Interactions. Small 2013, 9, 1635-1653. (8) Zuo, G.; Kang, S. G.; Xiu, P.; Zhao, Y.; Zhou, R. Interactions between Proteins and CarbonBased Nanoparticles: Exploring the Origin of Nanotoxicity at the Molecular Level. Small 2013, 9, 1546-1556.


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(9) Hirana, Y.; Juhasz, G.; Miyauchi, Y.; Mouri, S.; Matsuda, K.; Nakashima, N. Empirical Prediction of Electronic Potentials of Single-Walled Carbon Nanotubes With a Specific Chirality (n,m). Sci. Rep. 2013, 3, 2959. (10) Zheng, M.; Diner, B. A. Solution Redox Chemistry of Carbon Nanotubes. J. Am. Chem. Soc. 2004, 126, 15490-15494. (11) O'Connell, M. J.; Eibergen, E. E.; Doorn, S. K. Chiral Selectivity in the Charge-Transfer Bleaching of Single-Walled Carbon-Nanotube Spectra. Nat. Mater. 2005, 4, 412-418. (12) Strano, M. S.; Huffman, C. B.; Moore, V. C.; O'Connell, M. J.; Haroz, E. H.; Hubbard, J.; Miller, M.; Rialon, K.; Kittrell, C.; Ramesh, S. et al. Reversible, Band-Gap-Selective Protonation of Single-Walled Carbon Nanotubes in Solution. J. Phys. Chem. B 2003, 107, 6979-6985. (13) Hirano, A.; Kameda, T.; Sakuraba, S.; Wada, M.; Tanaka, T.; Kataura, H. Disulfide Bond Formation of Thiols by Using Carbon Nanotubes. Nanoscale 2017, 9, 5389-5393. (14) Anraku, M.; Chuang, V. T.; Maruyama, T.; Otagiri, M. Redox Properties of Serum Albumin. Biochim. Biophys. Acta 2013, 1830, 5465-5472. (15) 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. (16) Choi, J. H.; Strano, M. S. Solvatochromism in Single-Walled Carbon Nanotubes. Appl. Phys. Lett. 2007, 90, 223114. (17) Hirano, A.; Tanaka, T.; Kataura, H.; Kameda, T. Arginine Side Chains as a Dispersant for Individual Single-Wall Carbon Nanotubes. Chem. Eur. J. 2014, 20, 4922-4930.


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(18) Knorr, F. J.; Hung, W. C.; Wai, C. M. Aromatic Electron Acceptors Change the Chirality Dependence of Single-Walled Carbon Nanotube Oxidation. Langmuir 2009, 25, 10417-10421. (19) Nish, A.; Nicholas, R. J. Temperature Induced Restoration of Fluorescence from Oxidised Single-Walled Carbon Nanotubes in Aqueous Sodium Dodecylsulfate Solution. Phys. Chem. Chem. Phys. 2006, 8, 3547-3551. (20) Strano, M. S.; Moore, V. C.; Miller, M. K.; Allen, M. J.; Haroz, E. H.; Kittrell, C.; Hauge, R. H.; Smalley, R. E. The Role of Surfactant Adsorption during Ultrasonication in the Dispersion of Single-Walled Carbon Nanotubes. J. Nanosci. Nanotechnol. 2003, 3, 81-86. (21) Blanch, A. J.; Shapter, J. G. Surfactant Concentration Dependent Spectral Effects of Oxygen and Depletion Interactions in Sodium Dodecyl Sulfate Dispersions of Carbon Nanotubes. J. Phys. Chem. B 2014, 118, 6288-6296. (22) Haroz, E. H.; Duque, J. G.; Tu, X.; Zheng, M.; Hight, Walker A. R.; Hauge, R. H.; Doorn, S. K.; Kono, J. Fundamental Optical Processes in Armchair Carbon Nanotubes. Nanoscale 2013, 5, 1411-1439. (23) Makmura, L.; Hamann, M.; Areopagita, A.; Furuta, S.; Munoz, A.; Momand, J. Development of a Sensitive Assay to Detect Reversibly Oxidized Protein Cysteine Sulfhydryl Groups. Antioxid. Redox Signal. 2001, 3, 1105-1118. (24) Asuri, P.; Karajanagi, S. S.; Yang, H.; Yim, T. J.; Kane, R. S.; Dordick, J. S. Increasing Protein Stability through Control of the Nanoscale Environment. Langmuir 2006, 22, 5833-5836.


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Carbon Nanotubes Facilitate Oxidation of Cysteine Residues of

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