Photoinduced Electron Transfer on β-Sheet Cyclic Peptides - The

of charge transfer in helical peptides: from hopping to superexchange. Jingxian Yu , John R. Horsley , Andrew D. Abell. RSC Adv. 2017 7 (67), 4237...
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J. Phys. Chem. B 2001, 105, 10416-10423

Photoinduced Electron Transfer on β-Sheet Cyclic Peptides Hiroshi Sasaki,† Maki Makino,† Masahiko Sisido,*,† Trevor A. Smith,‡ and Kenneth P. Ghiggino‡ Department of Bioscience and Biotechnology, Faculty of Engineering, Okayama UniVersity, 3-1-1 Tsushimanaka, Okayama 700-8530, Japan, and School of Chemistry, UniVersity of Melbourne, Victoria 3010, Australia ReceiVed: March 28, 2001

Gramicidin S analogues that contain a single pyrenyl group and a single p-nitrophenyl group at different positions were synthesized. Photoinduced electron transfer (ET) from an excited pyrenyl group located at the fourth position to a nitrophenyl group located at five different positions was investigated on the β-sheet chains of the cyclic peptides. The observed ET rate constants displayed a complex dependence on the number of spacer units or on the edge-to-edge distance between the two aromatic groups. The ET rate constants, however, showed a reasonable linear relationship with the equivalent σ-distances calculated from the BeratanOnuchic tunneling pathway model, if through-hydrogen-bond ET was taken into account. The results support the applicability of the tunneling pathway model on both helix and β-sheet model peptides.

Photoinduced electron transfer (ET) on peptides and proteins has been studied by a number of researchers, and the ET mechanism on these systems has been discussed widely.1,2 A simple and practical model for predicting the ET rates on peptides and other molecular systems has been presented by Beratan and Onuchic.3 It is the tunneling pathway model that has been successfully applied to several protein systems.4,5 However, the validity of the model itself and the parameters used in it have not been thoroughly examined on simple model peptides, such as single R-helix polypeptides6-8 and isolated β-sheet peptides.9,10 In the previous work,8 we prepared model R-helical polypeptides that contain a single pyrenyl group and a single pnitrophenyl group as the donor-acceptor pair and measured the ET rates as a function of the number of spacer units or of the edge-to-edge distances. The ET rates were found to decrease with the edge-to-edge distance according to an approximate relation, kET ) 1.4 × 109 exp[-0.66(ree - 3)] (s-1, ree in Å). The application of the tunneling pathway model to the R-helix showed that the ET rates may be reasonably interpreted when through-hydrogen-bond (HB) electron jumps were taken into consideration. As for the β-sheet conformation, however, a similar model study is not easy to do because there is no isolated β-sheet peptide. Very often, β-sheet conformations are found as a part of protein structure or a part of large peptide assemblies. Some cyclic peptides are exceptional cases in which two β-sheet chains are folded and stabilized with interstrand hydrogen bonds. A typical example is gramicidin S (GS).11 GS is a well-known C2-symmetric cyclic decapeptide of the following amino acid sequence: 5′

Pro-1Val-2Orn-3Leu-4D-Phe

|

4′

|

3′

2′

1′

5

D-Phe- Leu- Orn- Val- Pro

* Corresponding author. Tel: +81-86-251-8218. Fax: +81-86-251-8219. E-mail: [email protected]. † Okayama University. ‡ University of Melbourne.

The cyclic peptide has antiparallel β-sheet strands that are linked by the β-turns at the 4D-Phe-5Pro sequences. The two β-sheet strands are stabilized by four hydrogen bonds, (1Val)NsHs OdC(3′Leu), (1Val)CdOsHsN(3′Leu), (3Leu)NsHsOdC(1′Val), and (3Leu)CdOsHsN(1′Val). The hydrophobic side groups of 1Val and 3Leu are oriented to one side of the cyclic structure, and the hydrophilic side groups of 2Orn are positioned on the other side. The unique amphiphilic structure may be related to the antibiotic activity of this cyclic peptide. The unique and rigid structure of GS has been employed as the framework for pyrenyl excimers. 12 In this study, the 4D-Phe unit was replaced by a D-1pyrenylalanine (D-pyrAla) unit and one of the four hydrophobic amino acids, or the 4′D-Phe was replaced by a L- or D-pnitrophenylalanine (ntrPhe) unit, respectively. The GS analogues are named as P4Tm (m ) 1, 3, 1′, 3′, and 4′), where m indicates the position of the ntrPhe unit. A GS analogue that contains an isolated pyrenyl group at the fourth position was also synthesized and named as P4. As has been described in our previous study,7,8 the pyrenyl group acts as the donor and the nitrophenyl group works as an electron acceptor. Since the fluorescence lifetime of the pyrenyl group is very long (242 ns at -58°), the relatively slow ET process that occurs across the edge-to-edge distance of up to about 18 Å can be followed on the β-sheet framework. Experimental Section Synthesis of the GS Analogues that Contain a D-pyrAla Unit at the Fourth Position and a ntrPhe Unit at the 1, 3, 1′, 3′, or 4′ Position. A linear peptide, Fmoc-4′D-Ph--5′Pro1Val-2Orn(Boc)-3Leu-4D-pyrAla-5Pro-1′Val-2′Orn(Boc)3′Leu-OH and its analogues that contain a single ntrPhe unit at the 1, 3, 1′, 3′, or 4′ position were synthesized by the solidphase method on a Fmoc/PyBOP protocol. The Fmoc protecting group of the linear peptides was removed, and the free peptides were cyclized with HATU in DMF. The crude cyclic peptides were purified first by gel chromatography and then by HPLC (C4 column/0.1% aqueous TFA + acetonitrile). The purified cyclic peptides were characterized by TOF mass spectroscopy (PE Biosystems Voyager DE Pro). The wild-type GS peptide with Boc-protected Orn units [GS(Boc)2] was prepared by the Boc protection of the commercial GS peptide. Detailed proce-

10.1021/jp011181+ CCC: $20.00 © 2001 American Chemical Society Published on Web 10/03/2001

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Figure 1. CD spectra of the GS analogues in the amide absorption region (left) and pyrenyl absorption region (right). TMP solution, [peptide] ) 10-4 M, at 25 °C.

dures for the peptide synthesis and the spectroscopic data are described in the Supporting Information. Spectroscopic Measurements. Absorption and CD spectra were recorded on a Jasco U-best 560 instrument and a Jasco J720WI instrument, respectively, in DMF and in trimethyl phosphate (TMP). Fluorescence spectra were recorded on a Jasco FP777 instrument in argon-saturated DMF solution. The concentration of the peptide was adjusted to be 2.4 × 10-6 M. Fluorescence decay curves were measured on a time-correlated single-photon counting instrument (Horiba NAES550), equipped with a hydrogen discharge lamp (pulse width ) about 2.5 ns) in argon-saturated DMF. For the P4T3 and P4T1′ peptides, a picosecond photon counting system at the University of Melbourne was used.8 The observed decay curves (λex ) 345 nm, λem ) 375 nm) were analyzed using multicomponent exponential functions by using a iterative reconvolution program. The fluorescence decay curves were measured at -58°, -30°, 0°, and +30 °C, by using an Oxford DN1704 or an Oxford Optistat liquid-nitrogen cryostat. Results and Discussion CD Spectra and Conformational Analysis of the GS Analogues. CD spectra of GS(Boc)2 and the GS analogues in TMP are shown in Figure 1. The CD profiles of the GS analogues in the amide absorption region are very similar to each other, indicating that the skeletal conformations of the analogues and GS(Boc)2 are essentially the same. The small negative peak at 243 nm observed in the analogues is assigned to the Ba absorption band of the pyrenyl group. Relatively large CD signals are induced at the Bb (260-280 nm) and La (320350 nm) absorption bands of the pyrenyl group, indicating that the orientation of the pyrenyl group is constrained with respect to the cyclic skeleton. At the La band where contribution of the nitrophenyl absorption can be neglected, the signs and the magnitudes of the CD signals are virtually the same for all GS analogues except the P4T3 analogue. The similarity of the CD profile suggests that the side-chain orientations of the pyrenyl groups are also the same for all GS analogues. The different CD profile in the P4T3 analogue may be explained in terms of a strong exciton-type interaction between the neighboring pyrenyl-nitrophenyl pair. The broad positive peak around 260-290 nm is assigned to the contribution of the L-ntrPhe unit. In the P4T4′ analogue that contains a 4′D-ntrPhe unit, a broad negative peak is

Figure 2. Side-chain energy contour map of the P4 analogue. The side-chain rotational angles of D-1-pyrenylalanine, χ1(CR-Cβ) and χ2(Cβ-Cγ) were varied. Ten contour lines were drawn at the interval of 1 kcal mol-1 from the minimum point, (χ1,χ2) ) (175°,280°).

overlapped at this wavelength region, whereas no broad peak is observed for the P4 analogue that contains no ntrPhe unit. These CD results indicate that the CD signs of ntrPhe units are primarily determined by the chirality of the ntrPhe unit. CD spectra were measured also in DMF solution down to 265 nm. The CD profiles were very similar to those in TMP solution, indicating that the skeletal and the side chain conformations of the GS analogues are virtually the same in the two solvents. The orientation of pyrenyl group in the 4D-pyrAla-5Pro sequence that takes a β-turn was predicted from molecular mechanics calculations under vacuum.13 The skeletal conformation and the side-chain orientations except for the orientation of pyrenyl group were taken from the X-ray crystallographic data of GS.11 The energy contour maps for the side-chain rotations [χ1(CR-Cβ),χ2(Cβ-Cγ)] of the 4D-pyrAla unit of all the GS analogues were virtually the same. As an example, Figure 2 shows the energy contour map of the P4T1 analogue. The map shows two major energy minima at (χ1,χ2) ) (175°,

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Figure 3. Side-chain energy contour maps of the P4T1 (left), P4T3 (center), and P4T4′ (right) analogues. The side-chain rotational angles of L-p-nitrophenylalanine (P4T1 and P4T3) or D-p-nitrophenylalanine (P4T4′) were varied. Ten contour lines were drawn at the interval of 1 kcal mol-1 from the minimum point, (χ1,χ2) ) (185°,65°) for P4T1, (175°,70°) for P4T3, and (180°,95°) for P4T4′.

280°; PI orientation) and (50°,75°; PII orientation). Although the PI orientation has lower energy by about 1 kcal mol-1 and a wider area of the allowed region than the PII orientation, the latter cannot be neglected in the interpretation of the ET rates. The side-chain energy contour maps of ntrPhe units were also calculated. The maps for the P4T1, P4T3, and P4T4′ analogues are compared in Figure 3. The maps for the P4T1′ and P4T3′ were very similar to the those for the P4T1 and P4T3, respectively. In the case of the P4T1 analogue (left), the angles between 80° and 170° are disallowed for χ1, due to a collision between the aromatic ring of 1ntrPhe and the isobutyl group of 3Leu. Since the p-nitrophenyl group has a C symmetry around 2 χ2, the contour map suggests only two possible orientations: (χ1,χ2) ) (185°,65°) and (300°,130°). The former has a lower energy by about 2 kcal mol-1 and a much wider area of the allowed region. In the case of the P4T3 analogue (center), the

map suggests that only a single energy minimum is allowed at (175°,70°). The two contour maps, therefore, suggest that the p-nitrophenyl side groups of the P4T1, P4T3, P4T1′, and P4T3′ analogues reside in a single orientation around (χ1,χ2) ) (180°, 70°) at low temperatures. In the case of the P4T4′ analogue (right), the map shows two energy minima that may be almost equally populated: (180°, 95°; TI orientation) and (60°,65°; TII orientation). Since the side group of 4′D-ntrPhe at the β-turn can rotate without collision with other side groups, this rotational freedom must be taken into consideration. To summarize the results of the conformational calculations, two different orientations (PI and PII) are allowed for each pyrenyl group in all GS analogues, and two orientations (TI and TII) are allowed for a nitrophenyl group in the P4T4′ analogue. The variations of the rotational angles and, as a

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TABLE 1: Edge-to-Edge Distances, ET Rate Constants in DMF at Different Temperatures, Thermodynamic Parameters, and the Equivalent σ-Distances According to the Tunneling Pathway Model on the GS Analogs kET (s-1) -58 °C

-30 °C

0 °C

30 °C

∆Hqa

∆Sqb

σL (Å)

P4T1 (ree ) 9.8 Å for PI orientation, 7.1 Å for PII orientation) 2.2 × 106 3.1 × 106 5.2 × 106 8.8 × 106 1.6 -22 17.7 P4T3 (ree ) 4.9 Å for PI orientation, 4.1 Å for PII orientation) 4.7 × 108 5.5 × 108 6.0 × 108 8.2 × 108 0. -18 9.8 P4T1′ (ree ) 9.2 Å for PI orientation, 9.3 Å for PII orientation) 5.3 × 108 4.9 × 108 5.5 × 108 6.3 × 108 0.0 -18 12.4 P4T3′ (ree ) 12.8 Å for PI orientation, 12.2 Å for PII orientation) 6.8 × 106 1.5 × 107 2.1 × 107 2.3 × 107 1.4 -20 18.4 P4T4′ (ree ) 17.8Å for (PI,TI) orientation, 16.8 Å for (PII,TI) orientation, 17.1 Å for (PI,TII) orientation, 16.4 Å for (PII,TII) orientation) 5.8 × 105 6.8 × 105 7.2 × 105 7.6 × 105 0.1 -31 20.7 a

In kcal mol-1. b In cal mol-1 deg-1.

Figure 5. Fluorescence spectra of the GS analogues in argon-saturated DMF at -58 °C. λex ) 345 nm, [peptide] ) 2.4 × 10-6 M. The inset shows the spectra of the P4T1′ and P4 analogues that are normalized at 376 nm. The difference between the two spectra is also shown.

Figure 4. Computer-predicted conformations of the GS analogues. The side-chain orientations of pyrenylalanine were set to the PI orientation (χ1,χ2) ) (175°,280°). Those of p-nitrophenylalanine were set to each minimum-energy orientation. Those in the P4T4′ analogue were the TI orientation, (χ1,χ2) ) (180°,95°). The pyrenyl-nitrophenyl edge-to-edge distances are indicated.

consequence, the distribution of the edge-to-edge distances must be taken into consideration in interpreting the ET data. The edgeto-edge distances between the pyrenyl and nitrophenyl groups for all possible combinations of the side-chain orientations were calculated and are listed in Table 1. Conformations of the GS analogues with the minimum-energy side-chain orientations are illustrated in Figure 4. The pyrenyl groups are set to the PI orientation and the nitrophenyl group in the P4T4′ analogue is set to the TI orientation. Steady-State Fluorescence Spectra. Fluorescence spectra of the GS analogues measured at -58 °C are shown in Figure 5. The pyrenyl fluorescence is quenched by the introduction of the nitrophenyl group and the extent of the quenching strongly depends on the positions of the nitrophenyl group. For example, the pyrenyl fluorescence is markedly quenched for the P4T3 analogue, in which the pyrenyl-nitrophenyl edge-to-edge distance may be 4.1-4.9 Å. In contrast, very small quenching is observed for the P4T4′ analogue, for which the edge-to-edge distance is predicted to be 16.4-17.8 Å. The distance dependence of the fluorescence intensity may be interpreted in terms of the distance dependence of intramolecular ET across the cyclic peptide. No intermolecular quenching may be expected under the present range of concentrations. The spectral profiles were compared in the normalized fluorescence spectra. The profiles of the P4T1, P4T3′, and P4T4′ analogues were exactly the same as that of the P4 peptide, indicating that no species other than the excited pyrenyl group is present in these analogues. The spectrum of the P4T1′ analogue, however, showed an additional very weak broad band at the long wavelength region, as shown in the inset of Figure 5. A similar broad band was observed also for the P4T3 analogue with smaller intensity. The broad bands, although very small, suggest that an exciplex-type species is formed in the P4T1′ and the P4T3 analogues. Incidentally, similar exciplextype fluorescence has been observed in the pyrenyl-nitrophenyl pair on a pyrAla-Glu(OChx)3-ntrPhe sequence that was built into an R-helical polypeptide [Glu(OChx) ) γ-cyclohexyl-Lglutamate]. Similar spectral profiles were observed at other temperatures up to +30 °C.

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Figure 8. Eyring plot of the ET rate constants at -58°, -30°, 0°, and +30 °C in DMF.

Figure 6. Fluorescence decay curves of the GS analogues in argonsaturated DMF at -58 °C. λex ) 345 nm, [peptide] ) 2.4 × 10-6 M.

exponential decay has been observed for the P4 analogue at all temperatures, the multicomponent decay may be explained either by the conformational distributions as discussed above or by the multiplicity of the ET processes. As found in the steadystate spectra (Figure 5), the P4T1′ and P4T3 analogues showed a very weak broad band at long wavelengths that may be attributed to an exciplex-type species. This additional excitedstate process may add complexity to the decay curves, although the contribution of the exciplex-type emission is very small. For the P4T3, P4T1′, and P4T3′ analogues that showed multicomponent decay curves, the average decay times were used for evaluating the ET rate constants. Although this treatment leaves some uncertainty, the trend of the distance dependence is not altered because the ET rate constants vary over three-orders of magnitude (see Figure 7). The ET rate constants (kET) were calculated from the decay times of the GS analogues in the absence (P4′, t0) and presence (P4′Tm, τ) of the ntrPhe unit

kET ) 1/τ0 - 1/τ

Figure 7. Dependence of the ET rate constants on the pyrenylnitrophenyl edge-to-edge distances. The bold solid lines are for the GS analogues, and the open circles are for the R-helical polypeptides (ref 8).

Fluorescence Decay Curves. The ET rates on the cyclic peptides can be evaluated directly from the fluorescence decay curves. The decay curves were measured in DMF at -58, -30, 0, and +30 °C. Those measured at -58 °C are shown in Figure 6. The P4 analogue that contains no nitrophenyl group showed a single-exponential decay with the lifetime of 242 ns at -58 °C. The introduction of the p-nitrophenyl group accelerated the fluorescence decay, and the extent of the acceleration markedly depended on the positions of the nitrophenyl group. The decay profiles of the P4T4′ and P4T1 analogues were essentially single-exponential, indicating that the distributions of the pyrenyl-nitrophenyl distances in these peptides cause little effect on the ET rates. In the case of P4T3′, the decay curve was fitted by two-component exponential functions. However, since the contribution of the slow-decaying component was 83%, the ET rates may be mainly governed by the conformation that gives the longer pyrenyl-nitrophenyl distance. In the case of the P4T1′ and P4T3 analogues, much faster decays were observed than decays of the other analogues, as shown in the inset of Figure 6. The decay curves were fitted to two- or three-component exponential functions at all temperatures. Since a single-

(1)

The rate constants measured at -58°, -30°, 0°, and +30 °C are listed in Table 1. Distance Dependence of the ET Rate Constants. The logarithms of the ET rate constants at -58 °C are plotted against the possible ranges of the edge-to-edge distances in Figure 7 (bold solid lines). The plot shows a complex dependence on the edge-to-edge distance. Particularly, the edge-to-edge distance of the P4T1 analogue is predicted to be shorter than that of the P4T1′ analogue, but the observed ET rate constant is much higher in the latter peptide. The complex distance dependence suggests that there exists a factor other than the edge-to-edge distance in determining the ET rate constant. In the same figure, the ET rate constants for the pyrenylnitrophenyl pairs on the R-helical polypeptides in DMF at -58 °C are also plotted.8 The ET rate constants measured on different polypeptide structures show approximately similar distance dependences. Temperature Dependence of the ET Rate Constants. The temperature dependence of the ET rate constants are shown in the form of an Eyring plot in Figure 8. The temperature dependence is very small as compared with that of other intramolecular ET systems, indicating that the skeletal structure of the GS analogues is a rigid framework and the ET process is mostly governed by a pure electron tunneling with small solvent reorganization. The small temperature dependence has been observed also in the R-helical polypeptides.8 The activation enthalpies and entropies were calculated from the slopes and intercepts of the Eyring plot and are listed in Table 1. Theoretical Prediction of the ET Rates on the Basis of the Tunneling Pathway Model. The distance dependences of

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Figure 9. Optimum ET pathways on the GS analogues calculated according to the tunneling pathway model with Beratan’s parameters.

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Sasaki et al. Å), the tunneling pathway model predicts that the ET rate constants must follow the following equation:

kET ) 1013 exp[-0.73(σL - 3)] (s-1, σL in Å)

(2)

The predicted relation is indicated by a solid line in Figure 10. The experimental data show a similar slope to that predicted, but the absolute values seem to be a little smaller than the predicted values. The ET rate constants measured on the R-helical polypeptides are also plotted in Figure 10 as open circles. The two types of experimental data on different peptide conformations are in good agreement with each other indicating a general applicability of the tunneling pathway model. Figure 10. ET rate constants of the GS analogues in DMF at -58 °C plotted against the equivalent σ-distances calculated according to the tunneling pathway model with Beratan’s parameters.

the ET rates of proteins and model peptides have been analyzed on the basis of the tunneling pathway model with Beratan’s parameters. The detail of the model and the parameters have been described before.3-5,8 The model was applied to the GS analogues by using the atomic coordinates predicted from the molecular mechanics calculations (Figure 4). The product (ΠCiHBjTSk) of the decaying factors for a jump across a covalent bond C, for a jump across a hydrogen bond (O‚‚‚HN) HB, and for a jump across vacant space TS was calculated along all possible ET pathways that connect one of the aromatic carbons of the pyrenyl group to one of the aromatic carbons of the nitrophenyl group. The optimum ET pathway that gave the largest product was searched for each GS analogue. The optimum pathways of all analogues are illustrated in Figure 9. In the cases of P4T3′ and P4T4′, two equivalent ET pathways were found, in which an electron jump takes place across the antiparallel β-strands through one of the two hydrogen bondings. In these cases, the product was evaluated as a sum of the two products for the equivalent pathways. The product of the decaying factors was converted to a nonintegral number of σ bonds nσ, that gives the same value as the product for the optimum pathway (ΠCiHBjTSk ) Cnσ). The equivalent number of σ bonds was then converted to the equivalent σ distance (σL ) 1.4nσ).3 The experimental ET rate constants must be multiplied by a correction factor to give a maximum rate constant that is optimized for the nuclear factor. As described before,8 we assume the correction factor to be 9, and each observed ET rate constant was multiplied by that factor to yield the maximum ET rate constant kET(max). The logarithms of the maximum ET rate constants are plotted against the equivalent σ distances in Figure 10. The plot shows a reasonable linear correlation between the two quantities. In particular, the large deviations of the P4T1 and P4T1′ analogues in Figure 7 are markedly improved in Figure 10, indicating that the ET rate is not simply determined by the edge-to-edge distance but depends on the ET pathways including jumps through hydrogen bonds. In the case of the P4T1 analogue, for example, the electron must mediate along the peptide main chain, whereas in the case of P4T3′ and P4T4′ the inter-strand hydrogen bonds may work as the shortcut for the electron mediation. As we have already stressed in the case of the R-helical polypeptides, hydrogen bonds play an important role in the electron mediation in peptides and proteins. If we assume that the ET rate constant approaches 1013 (s-1) when the donor and the acceptor are in the closest contact (3

Conclusion The ET rate constants on β-sheet cyclic peptides showed complex dependence on the edge-to-edge distance. However they exhibited reasonable correlation with the equivalent σ distances calculated on the basis of the tunneling pathway model. The applicability of the tunneling pathway model to both R-helix and β-sheet peptides was demonstrated, provided that the through-hydrogen bond jumps were taken into consideration. Acknowledgment. This work has been supported by a Grand-in-Aid for Specially Promoted Research from the Ministry of Education, Science, Sports and Culture, Japan (No.11102003). Supporting Information Available: Full description of the synthesis of the cyclic peptides. This material is available free of charge via the Internet at http://pubs.acs.org. References and Notes (1) For recent reviews, see: (a) Langen, R.; Colon, J. L.; Casimiro, D. R.; Karpishin, T. B.; Winkler, J. R.; Gray, H. B. JBIC 1996, 1, 221. (b) Gray, H. B.; Winkler, J. R. Annu. ReV. Biochem. 1996, 65, 537. (c) Kakitani, T. Photons, Substances, Life, and Reactions from Physical and Chemical Point of View (in Japanese); Maruzen: Tokyo, 1998. (2) Isied, S. S.; Ogawa, M. Y.; Wishart, J. F. Chem. ReV. 1992, 92, 381. (3) (a) Beratan, D. N.; Onuchic, J. N.; Hopfield, J. J. J. Chem. Phys. 1987, 86, 4488. (b) Onuchic, J. N.; Beratan, D. N. J. Chem. Phys. 1990, 92, 722. (c) Beratan, D. N.; Betts, J. N. Onuchic, J. N. Science 1991, 252, 1285. (d) Beratan, D. N.; Betts, J. N.; Onuchic, J. N. J. Phys. Chem. 1992, 96, 2852. (4) (a) Wuttke, D. S.; Bjerrum, M. J.; Winkler, J. R.; Gray, H. B. Science 1992, 256, 1007. (b) Beratan, D. N.; Onuchic, J. N.; Winkler, J. R.; Gray, H. B. Science 1992, 258, 1740. (c) Wuttke, D. S.; Bjerrum, M. J.; Chang, I.-J.; Winkler, J. R.; Gray, H. B. Biochim. Biophys. Acta 1992, 1101, 168. (d) Casimiro, D. R.; Richards, J. H.; Winkler, J. R.; Gray, H. B. J. Phys. Chem. 1993, 97, 13073. (e) Casimiro, D. R.; Wong, L.-L.; Colon, J. L.; Zewert, T. E.; Richards, J. H.; Chang, I.-J.; Winkler, J. R.; Gray, H. B. J. Am. Chem. Soc. 1993, 115, 1485. (5) Murakami, H.; Hohsaka, T.; Ashizuka, Y.; Sisido, M. J. Am. Chem. Soc. 1998, 120, 7520. (6) (a) Galoppini, E.; Fox, M. A. J. Am. Chem. Soc. 1996, 118, 2299 (b) Fox, M. A.; Galoppini, E. J. Am. Chem. Soc. 1997, 119, 5278. (7) (a) Sisido, M.; Tanaka, R.; Inai, Y.; Imanishi, Y. J. Am. Chem. Soc. 1989, 111, 6790. (b) Inai, Y.; Sisido, M.; Imanishi, Y. J. Phys. Chem. 1991, 95, 3847. (c) Sisido, M. AdV. Photochem. 1997, 22, 197. (8) Sisido, M.; Hoshino, S.; Kusano, H.; Kuragaki, M.; Makino, M. Sasaki, H.; Smith, T. A.; Ghiggino, K. J. Phys. Chem., submitted for publication. (9) (a) Gretchikhine, A. B.; Ogawa, M. Y. J. Am. Chem. Soc. 1996, 118, 1543. (b) Fernando, S. R. I.; Kozhov, V.; Ogawa, M. Y. Inorg. Chem. 1998, 37, 1900. (10) Langen, R.; Chang, I.-Jy; Germanas, J. P.; Richards, J. H.; Winkler, J. R.; Gray, H. B. Science 1995, 268, 1733.

Electron Transfer on β-Sheet Peptides (11) (a) Hull, S. E.; Karlsson, R.; Main, P.; Woolfson, M. M.; Dodson, E. J. Nature, 1978, 275, 206. (b) Liquori, A.; De Santis, P.; Int. J. Biol. Macromol. 1980, 2, 112. (12) Mihara, H.; Hayashida, J.; Hasegawa, H.; Ogawa H. I.; Fujimoto, T.; Nishino, N. J. Chem. Soc., Perkin Trans. 2 1997, 517.

J. Phys. Chem. B, Vol. 105, No. 42, 2001 10423 (13) The program PEPCON with the ECEPP force field was used for the molecular mechanics calculation. (a) Sisido, M. Peptide Chemistry 1991, 1992, 29, 105. (b) Beppu, Y. Comput. Chem. 1989, 13, 101. (c) Momany, F. A.; McGuire, R. F.; Burgess, A. W.; Scheraga, H. A. J. Phys. Chem. 1975, 79, 2361.