Letter pubs.acs.org/JPCL
Electron Transfer Mechanism in Helical Peptides Himadri Shekhar Mandal* and Heinz-Bernhard Kraatz Department of Chemistry, University of Saskatchewan, 110 Science Place, Saskatoon, SK S7N 5C9, Canada S Supporting Information *
ABSTRACT: Electrochemical studies of a set of ferrocene-labeled helical peptides of increasing length were carried out by forming self-assembled monolayers (SAMs) on gold electrodes. Electron transfer (ET) rates showed a very weakly distance dependent nature that has been interpreted as a result of a dynamically controlled tunneling mechanism. Specifically, the slow equilibrium between the α- and the 310 helical conformers in a SAM has been invoked, and the rate of formation of the more conductive 310 conformer has been proposed to be related to the ET rates observed.
SECTION: Electron Transport, Optical and Electronic Devices, Hard Matter
T
he helix is a frequently observed secondary structure in proteins.1 Specifically, the photosynthetic reaction center is rich in helical content,2 and electron transfer (ET) studies of synthetic helical model peptides may help to elucidate the mechanism of complex biological ET processes. Additionally, there are reports3,4 in which the natural photosystem was mimicked by synthetic helices functionalized with lightharvesting chromophores, making such studies relevant to the development of artificial solar energy converters, and exploiting helices as part of nanoscaled photovoltaic devices. At present, the discussion over ET in helices is, however, highly controversial. Reports excluding the possibility for helical peptides as charge mediators were published,5 although several groups6,7 claimed the helical backbone as an excellent ET medium. The mechanistic discussion is even more debated and involves ET by tunneling following (a) the “distance model”, which considers proteins as “generic organic matrices”8 and ET depends simply on the donor−acceptor (D−A) distance;9 (b) the “pathway model”,10 in which ET depends on the peptide backbone as well as the intramolecular H-bonding network,11 and (c) the highly efficient “H-bond shortcuts”.12,13 Apart from these, hopping of electrons7,14−16 or holes14,17,18 through the peptide backbone, a “conformationally gated mechanism”19,20 have also been proposed. In this context, we have investigated ET in a set of Leu-based helical peptides of increasing length. The peptides possess the redox-active ferrocene (Fc) at the Nterminal and the thiol-functionalized cysteine residue at the Cterminal: Fc-KTALnNPC-NH2, where n = 10 (Fc10L), 14 (Fc14L), and 18 (Fc18L). For preparing redox-diluted selfassembled monolayers (SAMs), suitable for electrochemical studies, acetyl (Ac)-analogues were also synthesized (Figure 1a). We used Leu for several reasons: (i) high helix-forming propensity and (ii) high probability of forming well-packed and ordered SAMs because of the van der Waals interactions and interdigitations among the hydrophobic side chains and, most importantly, because it is less accessible to the solvent (which is © 2012 American Chemical Society
Figure 1. (a) Chemical structures of the Fc/Ac peptides. (b) A schematic diagram of the redox-diluted peptide SAM.
water during the electrochemical measurements) to avoid any solvent-mediated long-range ET.21,22 Lysine was introduced at the N-terminal because it extends away from the helical backbone and creates a polar and water-accessible environment around the pendent Fc to reduce its reorganization energy to Fc+ upon oxidation. Details of the peptide design can be found elsewhere.23 Received: January 3, 2012 Accepted: February 22, 2012 Published: February 22, 2012 709
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For ET studies, mixed SAMs were prepared on gold microelectrodes from trifluoroethanolic (TFE) solutions of each Fc-peptide and the corresponding Ac-peptide (5:95), and cyclic voltammograms (CVs) were recorded in 2 M NaClO4 aqueous solutions (Figure S8, Supporting Information (SI)). More than 5% of the Fc-peptides was avoided to exclude the repulsions among the neighboring Fc units upon oxidation. Also, an aqueous solution of high ionic strength (2 M NaClO4) was used to screen any electrostatic effect of the helix dipoles on the Fc units. To check whether the structural integrity, i.e., the helicity of the peptides in the SAMs is retained in such high ionic environment, peptide modified gold substrates were soaked in 2 M NaClO4 D2O solutions for 2 h and Fourier transform-reflection absorption infrared (FT-RAIR) spectra were taken. The spectra were essentially identical to those obtained before soaking (data not shown). The absence of any absorption band at ∼1456 cm−1 for the amide II′ of the deuterium-exchanged peptide group24 indicated the resistance of the peptides to unfold and undergo any H−D exchange. The formal potentials (E0′) were similar (∼450 ± 15 mV) for all the peptide SAMs, suggesting a comparable environment around the redox active Fc moiety. The standard ET rate constants (keto) were calculated from the CVs, and a sluggish decrease of the ET rates with the increase of the peptide length was revealed (Figure 2a), consistent with the electrochemical impedance spectroscopic (EIS) measurements (SI). Figure 2a shows a compilation of the ET rates from this work together with those of other shorter Fc-peptides (with similar thiol linker) studied on gold surfaces by electrochemical measurements,25 as a function of the peptide spacer length (d). Two distinct ET regimes are clearly evident. For the shorter peptides (23 Å), keto shows a distinct pattern of very weak distance dependence (β = 0.04 Å−1). Similar observations were reported elsewhere from ET studies of oligoprolines,30 DNA,31 and PNA (peptide nucleic acid),32 and rationalized as a transition from tunneling to the hopping mechanism following several theoretical predictions.33,34 In hopping, the electron is suggested to populate the lowest unoccupied molecular orbital (LUMO) of the bridge first (reduction) and then transfer to the acceptor.34 This mechanism has been recommended to be unlikely to occur in ET over short distances due to the huge energetic barrier to transfer an electron onto the LUMO of the bridge, but is probable when the D−A distance is large.30−34 Interestingly, no Faradic response due to the reduction (electron hopping) or oxidation (hole hopping) of the peptide bridge was detected when CVs of the Ac-peptides were recorded (Figure 2b) and thereby rules out the involvement of hopping in our peptides. In addition, the current−voltage (I−V) profile of a SAM of peptide Ac18L (Figure 2c) clearly shows an exponential increase of the current with the bias voltage, which is similar to the behavior observed for alkanethiolates, proteins35,36 that exhibit ET by tunneling. At this point, we would like to emphasize that the distance dependence of ET (the value of β) simply signifies the conductive nature of the bridge. Extensively studied alkane chains where the ET mechanism is tunneling, show β = 1.0 Ǻ −1,37 whereas the highly conductive oligophenylenevinylene (OPV) derivatives for which the ET mechanism is also tunneling, have β = 0.06 Ǻ −1.38 So a change of the β value
Figure 2. (a) ET rate constant versus the D−A distance for several Fclabeled peptides (□)25 and the series of peptides Fc10L, Fc14L, and Fc18L (○). The distances for our peptides were obtained from molecular mechanics force field (MMFF) optimized structures (SI). (b) CVs of Fc10L (solid) and Ac10L (dashed) using glassy carbon electrode in 50 mM TBAP in TFE at a scan rate of 5 mV/s at 22 ± 1 °C.27 (c) Current−voltage (I−V) response of the Ac18L SAM; the black and red curves represent experimental data and fit to the Simmons model for electron tunneling,28,29 respectively.
should not be regarded as an indication of a switch in the ET mechanism. Considering the redox-inactive behavior of the peptide backbone, it can be proposed that the apparent transition in ET rates is most likely related to the structural change (from random to stable helices) with the increase in the length of the peptides.39−41 Also, following the literature where the H-bond is considered as a very efficient tunneling medium,42,43 the low β value could be related to the presence of the extensive intramolecular H-bond network in the helical peptides, as suggested by Maran and co-workers.13 The above justification is, however, unable to explain the different β value and the orders of magnitude lower ET rates in our case compared to those studied44 in solutions (β = 0.5−1.3 Ǻ −1)11,41,44,45 Recently, we reported19 that ET in helical peptide SAMs is governed by the degree of molecular dynamics (MD): the more restricted the peptide MD, the slower the ET rate. We also suggested that ET may involve certain ET active conformers, and the frequency of formation of these conformers might control the overall ET rate. Here, we point out that short peptide helices exist as equilibrium mixtures of α and 310 helices because of their low energetic barrier.46 Circular dichroism (CD) studies of the peptides studied here also indicate the presence of this equilibrium and a comparable population of both conformers in TFE solutions (Figure S2, Table S1, SI). The time-scale (τ) for this equilibrium in 710
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solutions is in the range of nanoseconds,47 but recent studies of a helical peptide showed an increase of τ by orders of magnitude (∼50s) when the peptide was assembled in a SAM.48 This time-scale correlates well with our observed ET rates. Since infrared studies specify that the equilibrium shifts exclusively to the α-helical conformation in solid state (Figures S3 and S6, Table S2, SI), and the 310-helix is known to be more conductive than the α-helix (because of the increased number, i → i + 3 versus i → i + 4, respectively, and shorter, thereby stronger intramolecular H-bonds),46 it can be suggested that the 310 conformation may be a potential candidate for the ET active conformer, and the rate of formation of this particular conformation (which is sluggish in close-packed SAMs compared to that in solutions) controls the overall ET rate in helical peptide SAMs. Combining our previous results with the present work, the ET mechanism could be fluctuationcontrolled tunneling as proposed by Balabin and co-workers.49 It is also evident that the ET rates obtained for the helical peptides in SAMs are not intrinsic, and the value of β might be related to the decrease of rates as a result of more limited MD due to larger van der Waals interactions in the longer helical peptide SAMs.
supporting electrolyte was 2.0 M NaClO4, and the working, counter, and reference electrodes were peptide-modified gold microelectrodes, Pt wire, and Ag/AgCl/3.0 M KCl (BAS), respectively. For current−voltage (I−V) measurements, scanning tunneling microscopic (STM) images were taken using a U-SPM system (Quesant Instrument Corporation) at room temperature. A Pt−Ir tip (mechanically cut) was used, and constant current mode was employed. The built-in scanning tunneling spectroscopic (STS) module was engaged to collect I−V data at different points. The data presented in this work is an average of 100 data points and fitted in MS Office Excel.
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ASSOCIATED CONTENT
S Supporting Information *
MMFF-optimized structures of the Fc peptides, synthesis protocol, CD spectra, FT-IR spectra, CVs, XPS, FT-RAIR spectra, ellipsometric thickness, and EIS spectra. This material is available free of charge via the Internet http://pubs.acs.org.
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AUTHOR INFORMATION
Corresponding Author
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*Address: Department of Chemistry, University of Pittsburgh, Chevron Science Center, 219 Parkman Avenue, Pittsburgh, PA 15260, USA. Phone: 412-624-8431. E-mail:
[email protected].
EXPERIMENTAL SECTION Peptides were synthesized using a semiautomated solid phase synthesizer following standard solid phase synthesis protocol. Fluorenylmethyloxycarbonyl (Fmoc)-protected L-α-amino acids, 1-hydroxy benzotriazole (HOBt) were purchased from SynPep (Dublin, CA). 5-(4-Fmocaminomethyl-3,5dimethoxyphenoxy)valericacid-MBHA (PAL) resin and (1Hbenzotriazol-1-yloxy)tris-(dimethylamino) phosphoniumhexafluorophosphate (BOP) were from Advanced ChemTech (Louisville, KY). All other reagents and solvents, including Nmethyl-2-pyrrolidinone (NMP), 1,8-diazabicyclo[5.4.0]undec7-ene (DBU) and diisopropylethyl-amine (DIPEA) were obtained from Sigma-Aldrich Canada Ltd. and used as received. CD spectra were taken with an Applied Photophysics π*-180 instrument at 22 ± 1 °C. Ellipticity is reported as the mean residue ellipticity (θ, in deg·cm2·dmol−1) and calculated as θ = θobs(MRW/10lc), where θobs is the ellipticity measured in millidegrees, MRW is the mean residue molecular weight of the polypeptide, c is the concentration of the sample in mg/mL, and l is the optical path length of the cell in centimeters (0.01). A Bio-Rad FTS-40 system was used to record the Fourier transform infrared (FT-IR; KBr) spectra at a resolution of 0.5 cm−1. For surface characterization by X-ray photoelectron spectroscopy (XPS) and FT-RAIRS, we prepared SAMs of the peptides on gold substrates (Platypus Technologies, Inc.) by incubating in 0.1 mM TFE solutions for 5 days. The XPS spectra were recorded in an Axis-165 X-ray photoelectron spectrometer (Kratos Analytical). The film thickness was measured using a LSE Stokes ellipsometer with a fixed angle of 70° and a fixed wavelength of 632.8 nm. Ellipsometry constants were refractive index Ns = 0.133 and absorption index Kf = 3.462 for the Au substrate, and monolayer refractive index = 1.44.50−52 For ET rate measurements, gold microelectrodes (diameter of 50 μm) were immersed in 0.1 mM solutions of the Fc and Ac peptides (5:95) in TFE, and self-assembly was allowed for 5 days; they were then washed thoroughly with TFE and dried under a stream of N2. For cleaning and activating the gold electrodes and the other gold surfaces, published procedures were followed.50 Electrochemical measurements were carried out on a CHI 660B potentiostat. The
Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS We thank the Natural Science and Engineering Research Council of Canada for funding.
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REFERENCES
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(50) Kraatz, H.-B.; Bediako-Amoa, I.; Gyepi-Garbrah, S. H.; Sutherland, T. C. Electron Transfer through H-bonded Peptide Assemblies. J. Phys. Chem. B 2004, 108, 20164−20172. (51) Irene, B.-A.; Sutherland, T. C.; Li, C.-Z.; Silerova, R.; Kraatz, H.B. Electrochemical and Surface Study of Ferrocenoyl Oligopeptides. J. Phys. Chem. B 2004, 108, 704−714. (52) Dey, S. K.; Long, Y. T.; Chowdhury, S.; Sutherland, T. C.; Mandal, H. S.; Kraatz, H.-B. Study of Electron Transfer in FerroceneLabeled Collagen-like Peptides. Langmuir 2007, 23 (12), 6475−6477.
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