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Excess-Electron Transfer in DNA by a Fluctuation-Assisted Hopping Mechanism Shih-Hsun Lin, Mamoru Fujitsuka,* and Tetsuro Majima* The Institute of Scientific and Industrial Research (SANKEN), Osaka University, Mihogaoka 8-1, Ibaraki, Osaka 567-0047, Japan S Supporting Information *

ABSTRACT: The dynamics of excess-electron transfer in DNA has attracted the attention of scientists from all kinds of research fields because of its importance in biological processes. To date, several studies on excess-electron transfer in consecutive adenine (A):thymine (T) sequences in donor−DNA−acceptor systems have been published. However, the reported excess-electron transfer rate constants for consecutive T’s are in the range of 1010−1011 s−1 depending on the photosensitizing electron donor, which provides various driving forces for excess-electron injection into DNA. In this study, we employed a strongly electron-donating photosensitizer, a dimer of 3,4-ethylenedioxythiophene (2E), and an electron acceptor, diphenylacetylene (DPA), to synthesize a series of modified DNA oligomers (2-Tn, n = 3−6) in order to investigate the excess-electron transfer dynamics in these donor−DNA−acceptor systems using femtosecond laser flash photolysis. The relation between the free energy change for charge injection and the excess-electron transfer rate among consecutive T’s provided an intrinsic excess-electron hopping rate constant of (3.8 ± 1.5) × 1010 s−1 in the DNA, which is consistent with the fluctuation frequency of the DNA sugar backbone and bases (3.3 × 1010 s−1). Thus, we discuss the effect of structural fluctuations on the excess-electron hopping in DNA.

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mechanism, β has been determined to be 0.3−1.0 Å−1, and well-reported values in previous studies are in the range of 0.7− 0.8 Å−1.13,14,21 The variation in the reported values can be attributed to factors such as donor−acceptor energetics.22 However, in some cases of hole transfer in DNA, β values as small as 0.1 Å−1 have also been reported.7,9,23 Such small values indicate that the multistep hopping mechanism is operative.20,24,25 The hopping mechanism indicates the occurrence of multiple hole tunneling processes through DNA and realizes long-range hole transfer over several hundred angstroms.5,9 Thus, hole transfer in DNA via the hopping mechanism can be described by a single-step hopping rate. We have determined the single-step hole hopping rate constant through a consecutive A sequence as 2 × 1010 s−1 in a donor−DNA− acceptor system by means of nanosecond laser flash photolysis.26 Lewis and co-workers also reported G-to-G and A-to-A hole hopping rate constants of 4.3 × 109 and 1.2 × 109 s−1, respectively.27 Thus, single-step hole hopping takes several tens to hundreds of picoseconds. In contrast to hole transfer, the nature of excess-electron transfer in DNA by the hopping mechanism is relatively less understood. Several research groups have determined the β value for excess-electron transfer through T’s to be 0.1−0.3 Å−1, in accordance with the hopping mechanism.28−35 Our research group has studied a series of modified DNAs to estimate singlestep excess-electron hopping rates directly using femtosecond

INTRODUCTION Charge transfer in DNA with well-ordered nucleobases realizing continuous π−π stacking has attracted the attention of scientists for decades.1−4 From the mechanistic viewpoint, charge transfer in DNA can be classified as hole transfer via oxidation of a nucleobase by an adjacent radical cation or excess-electron transfer via reduction of a nucleobase by an adjacent radical anion. Numerous results from both theoretical and experimental studies suggest that electron-deficient intermediates generated by one-electron oxidation of DNA (i.e., the hole) can migrate among guanine (G) and adenine (A);5−11 on the other hand, excess-electron transfer in DNA can occur through cytosine (C) and thymine (T) because of their relatively high reduction potentials.12−14 Understanding of the mechanisms underlying oxidative and reductive charge transfers in DNA is critical to explain DNA damage/repair.15−18 From this viewpoint, several mechanisms based on various theoretical and experimental results have been proposed.3 To date, there have been several studies on hole transfer in DNA. These studies have employed systems such as donor− DNA−acceptor systems, and the results have revealed that both tunneling and hopping mechanisms are included in hole transfer in DNA. Usually, the rate of a single-step electron/hole transfer through spacers by the tunneling mechanism can be expressed as an exponential function of the donor−acceptor distance (RDA), as described by eq 1:5,19,20 kHT = k 0 exp( −βRDA )

(1)

Received: November 5, 2015 Revised: December 27, 2015 Published: January 7, 2016

where β is the damping factor and k0 is a temperaturedependent factor. For hole transfer by the tunneling © 2016 American Chemical Society

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DOI: 10.1021/acs.jpcb.5b10857 J. Phys. Chem. B 2016, 120, 660−666

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The Journal of Physical Chemistry B laser flash photolysis techniques. For this purpose, various donor−DNA−acceptor systems have been synthesized.36−40 As a photosensitizing electron donor, oligothiophenes (2T, 3T, 4T, 2E, and 3E) and an aminopyrene derivative (APy) were employed, while diphenylacetylene (DPA) was used as an electron acceptor (Figure 1).41−49 The redox and spectroscopic properties of the photosensitizing electron donors are summarized in Table 1.

Figure 2. DNA oligomers 1−6, 2-Tn (n = 3−6), 2-D, and 2-A. For 1, 2, 5, 6, and 2-Tn, the gap between the 5′ and 3′ indicates a missing phosphate linker between two nucleobases in the nicked-dumbbell structure.

Figure 1. Structures of the photosensitizing electron donors 2T, 3T, 4T, APy, 2E, and 3E and the electron acceptor DPA.

Table 1. Driving Forces for Electron Injection from the Singlet Excited Electron Donors to Thymine (ΔGCS) and DPA (ΔGET) and Absorption Peak Positions in the Singlet Excited (λS1) and Radical Cation (λ•+) States of APy, 2T, 3T, 4T, 2E, and 3E donor b

APy 2Tc 3Tc 4Td 2Ee 3Ec

−ΔGCSa (eV)

−ΔGETa (eV)

λS1 (nm)

λ•+ (nm)

0.24 0.16 −0.13 0.09 0.63 0.35

0.38 0.30 0.01 0.23 0.77 0.49

500−600 503 605 >700 530 620

509 445 585 675 445 540

(Table S1 in the Supporting Information). The DNA oligomers were purified on a JASCO HPLC with a reversed-phase C-18 column using an acetonitrile/50 mM ammonium formate gradient (Figure S1). Apparatus. All of the DNA oligomer samples were prepared in buffer solution (0.1 M NaCl and 10 mM sodium phosphate, pH 7.0 ± 0.1). Steady-state absorption, fluorescence, and circular dichroism (CD) spectra and melting temperature profiles were measured using a Shimadzu UV3100PC spectrophotometer, a Horiba FluoroMax-4P spectrofluorometer, a JASCO J-720 CD spectrophotometer, and a Shimadzu UV2700 spectrophotometer, respectively. The CD spectra of DNA oligomers were averages of 10 scans collected from 400 to 225 nm at a scan rate of 100 nm min−1. The time-resolved transient absorption spectra of the DNA oligomers were measured by the pump-and-probe method using a regeneratively amplified Ti:sapphire laser (Spectra Physics, Spitfire Pro F, 1 kHz) pumped by a Nd:YLF laser (Spectra Physics, Empower 15).53 The seed pulse was generated by a Ti:sapphire laser (Spectra Physics, MaiTai VFSJ-W). DNA oligomers were excited using the 350 nm laser pulse, which was generated by an optical parametric amplifier. The supercontinuum was generated by focusing the output of the amplifier on a sapphire plate. The chirp was corrected using a homemade program based on the optical Kerr effect crosscorrelation method.54 The time resolution of the present system is ∼300 fs.

a

The procedure for estimation of the driving force is provided in the Supporting Information. bFrom ref 46. cFrom ref 41. dFrom ref 43. e From ref 41 and this paper.

From a series of studies, the excess-electron hopping rate constant among consecutive T’s was determined to be on the order of 1010−1011 s−1.43−46 These results indicate that the photosensitizing electron donor affects not only the excesselectron injection rate41,49−51 but also the hopping rate, although the factor governing this phenomenon is not clear. In the present study, we synthesized DNA oligomers 2-Tn (n = 3−6) containing 2E as a photosensitizing electron donor and DPA as an electron acceptor (Figure 2) and examined them by femtosecond laser flash photolysis. 2E was chosen because it realizes the largest driving force for excess-electron injection into DNA and is expected to have a larger effect on the excesselectron hopping than other electron donors. This study was aimed at the clarification of the energetic aspects of the excesselectron transfer dynamics in donor−DNA−acceptor systems. The role of structural fluctuations in excess-electron transfer in DNA is also discussed.

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RESULTS AND DISCUSSION All of the DNA oligomers were synthesized as described in the Experimental Section, and the characterizations shown in Figure S1 supported their formation. In the steady-state absorption spectra shown in Figure 3, a clear peak at around 260 nm for all of the DNA oligomers is dominated by base-pair absorption. As the number of A:T base pairs increases, this peak increases in absorbance with a slightly blue shift for 2-Tn. At wavelengths longer than 300 nm, the absorption spectra of 2Tn are equivalent to the sum of those for DPA52 and 2E.41,55 From the absorption spectra of 2-D and 2-A, it is clear that only 2E absorbs photons at 340−360 nm. Thus, transient absorption measurements were performed using an excitation pulse at 350 nm to excite 2E without the interference of excited intermediates of DPA.

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EXPERIMENTAL SECTION DNA Synthesis. 2E and DPA were prepared and converted to their phosphoramidite derivatives by a procedure similar to that reported previously.41,52 All of the reagents were purchased from Glen Research (Sterling, VA, USA). All of the DNA oligomers were synthesized on an Applied Biosystems 3400 DNA synthesizer with standard solid-phase techniques and were characterized using MALDI-TOF mass spectrometry 661

DOI: 10.1021/acs.jpcb.5b10857 J. Phys. Chem. B 2016, 120, 660−666

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that of 2E regardless of the length of the DNA oligomer, which indicates that the fluorescence quenching is mainly due to excess-electron injection to the adjacent T and that the contribution of DPA is limited because of the distance between 2E and DPA. The dynamics of excess-electron transfer in the DNA oligomers was investigated by transient absorption measurements during femtosecond laser flash photolysis using a 350 nm laser pulse, which selectively excites 2E (Figures 6 and S3).

Figure 3. UV−vis absorption spectra of the DNA oligomers in buffer solution at 298 K.

In the CD spectra of all of the DNA oligomers (Figure 4), a positive band at around 280 nm and a negative band at around

Figure 4. Circular dichroism spectra of the DNA oligomers in buffer solution at 298 K. Figure 6. Transient absorption spectra during the laser flash photolysis of (a) 2-D and (b) 2-T3 upon excitation with a 350 nm femtosecond laser pulse at 295 K.

250 nm were observed, indicating that all of the DNA oligomers possess a B-form structure.43−47,56−58 Moreover, the thermal dissociation profiles of the synthetic DNA oligomers (Figure S2) indicate that as the number of base pairs in the DNA increases, the profile and Tm become clearer and higher, respectively. Thus, we can point out that the B-form structure is responsible for the transient phenomena found by the transient absorption measurements during femtosecond laser flash photolysis, which is consistent with previous reports.43−47 Fluorescence from 2E in the DNA oligomers was measured by selective excitation of 2E at 340 nm (Figure 5). It is clear that the fluorescence intensities of 2-Tn and 2-D are lower than

Immediately following excitation, the absorption band of 12E* was found at 530 nm for 2-D (Figure 6a).41 The decay of the 530 nm band and the rise of the 445 nm band attributable to the 2E radical cation (2E•+) occurred within 1−2 ps, indicating rapid excess-electron injection into the adjacent T (charge separation (CS)).41 On the other hand, 2-T3 showed an additional absorption band at around 510 nm after decay of 1 2E* (Figure 6b), suggesting the generation of DPA•− by excess-electron transfer (ET).43−49 Spectral changes after the generation of 2E•+ were analyzed by global fitting assuming two species (Figure 7). The speciesassociated spectrum for the faster component (τ1) is attributed to 2E•+−DNA•−−DPA, and that for the slower component (τ2) is attributed to 2E•+−DNA−DPA•−, as is evident from the absorption band around 510 nm. The analyzed kinetics traces of 2E•+ (445 nm) in 2-Tn are shown in Figure S4. As the number of base pairs increases, the absorption intensity of 2E •+−DNA−DPA •− decreases. From the ratio of the absorption intensities of 2E•+−DNA−DPA•− and 2E•+− DNA•−−DPA, the generation yield of 2E•+−DNA−DPA•− after excess-electron transfer was calculated. To the best of our knowledge, 2-T6 with six A:T base pairs is the longest DNA (23.8 Å) to show excess-electron transfer products by transient absorption measurements during femtosecond laser flash photolysis.

Figure 5. Fluorescence spectra of 2E41 in methanol and DNA oligomers in buffer solution at 298 K (λex = 340 nm). The peak indicated by an asterisk is the Raman scattering band of the solvent. 662

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Table 2. Values of the Rate Constants kCS, kET, kCR, and kBET in the DNA Oligomers DNA

kCSa (s−1)

kCRa (s−1)

2-D 2-T3 2-T4 2-T5 2-T6

× × × × ×

× × × × ×

1.6 1.6 1.6 1.6 1.6

12

10 1012 1012 1012 1012

1.3 5.0 4.0 7.7 6.3

11

10 1010 1010 1010 1010

kETa (s−1) − 5.3 2.7 1.9 1.9

c

× × × ×

10

10 1010 1010 1010

kBETb (s−1) −c 9.5 3.1 1.8 1.4

× × × ×

109 109 109 109

a c

Estimation error is less than 10%. bEstimation error is less than 5%. Not observed.

generation yield. The slow-decaying component in the DNA oligomers can be attributed to kBET. It is clear that the kCS values are similar to the reported value for the 2E−T dyad,41 which indicates that 12E* was quenched by CS to generate 2E•+ and T•−. The DPA•− generation yields in 2-T5 and 2-T6 were lower than that in 2-T3 because fast CR between 2E•+ and DNA•− cannot be ignored. Therefore, the CR process limits the efficiency of excess-electron transfer through T’s in DNA. In addition, the variation of kCR with the number of consecutive T’s probably indicates the slight stabilization of the negative charge on the stacking T’s.3,18 By application of eq 1 to kET of 2-Tn tentatively, β = 0.10 ± 0.031 Å−1 indicating a weak distance dependence was confirmed. Similar β values have been determined by photochemical product analysis of excess-electron transfer using flavinsensitized cleavage of the T−T cyclobutane dimer (0.11 Å−1, by Carell and co-workers28), flavin-sensitized cleavage of thymine oxetane (0.16 Å−1, by Stafforst and Diederichsen31), Ir(III)-sensitized loss of bromide from 5-bromouracil (0.12 Å−1, by Barton and co-workers32), and pyrene-derivative-sensitized loss of bromide from 5-bromouracil (0.22−0.26 Å−1, by Lewis et al.34,35). These smaller β values indicate that a multistep hopping mechanism, which shows a weak distance dependence, should be operative in 2-Tn. We concluded that excess-electron transfer in 2-Tn occurs by a multistep hopping mechanism consisting of photoinduced electron injection (kCS), stepwise electron hopping (khop), and electron trapping by DPA (ktrap). It should be noted that kET is expected to be lower than ktrap. Thus, excess-electron hopping is the rate-determining step, so khop can be estimated on the basis of the one-dimensional random walk model (eq 2):27,59

Figure 7. Species-associated spectra obtained by global fitting using a double-exponential function for (a) 2-T3, (b) 2-T4, (c) 2-T5, and (d) 2-T6 (orange, τ1; green, τ2; τ1 and τ2 correspond to (kCR + kET)−1 and kBET−1, respectively).

The rate constants for excess-electron injection into the adjacent T (kCS), initial charge recombination (CR) between the nucleobase radical anion and 2E•+ (kCR), and charge recombination between 2E•+ and DPA•− (kBET) indicated in Figure 8 were estimated as follows, and the results are

τ(N ) = (1/2k hop)N 2

(2)

where τ(N) is the time required for N hopping steps (i.e., kET−1) and khop is the rate constant for a single hop between neighboring nucleobases. The excess-electron hopping rate constant in 2-Tn is estimated to be (2.6 ± 0.5) × 1011 s−1. The estimated khop is larger than those reported previously.43−46 From a series of studies of excess-electron transfer in DNA using 2-Tn and 1−6, we found the khop values to be on the order of 1010−1011 s−1.43−46 Structural fluctuation of DNA has been pointed out as a factor contributing to the various hopping rates.33 For the CS process with larger ΔGCS, larger thermal energy is expected to be deposited in the DNA, resulting in larger structural fluctuations of the DNA. To verify this point, the ΔGCS dependence of ln khop was examined using estimated values (Figure 9). The linear nature of this plots indicates that ΔGCS is an essential parameter for khop. Notably, the intercept of the linear fit ((3.8 ± 1.5) × 1010 s−1) should correspond to the hopping rate for a non-energy-assisted (ΔGCS = 0) excess-electron transfer in DNA, i.e., the intrinsic

Figure 8. Schematic energy diagram for excess-electron transfer from 2E to DPA in 2-T6.

summarized in Table 2. The kCS and kCR values for 2-D were determined by global fitting assuming two species, i.e., 12E*− DNA and 2E•+−DNA•− (Figure S4). In the case of 2-Tn, the kCS value is considered equivalent to that of 2-D. After generation of 2E•+, the decay profiles can be analyzed by assuming two decay components. The rate of the fast-decaying component can be attributed to the sum of kCR and kET. The kCR and kET values were determined by considering the 663

DOI: 10.1021/acs.jpcb.5b10857 J. Phys. Chem. B 2016, 120, 660−666

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structural fluctuations is realized in this nicked-dumbbell donor−DNA−acceptor system. Moreover, the estimated intrinsic hopping rate agrees with theoretical results, indicating the effect of structural fluctuations on the excess-electron hopping in DNA. These results provide new insights into excess-electron transfer in DNA by the hopping mechanism.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpcb.5b10857. Calculation of driving forces, HPLC analysis, MALDITOF data, melting temperature profiles, transient absorption spectra, species-associated spectra, and kinetic traces (PDF)

Figure 9. Dependence of ln khop on −ΔGCS. A, B, and C are data for DNA oligomers 1 and 2,43 3 and 4,46 and 5 and 6,44,45 respectively.

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hopping rate. Interestingly, the intrinsic hopping rate agrees with the reported value for the DNA sugar backbone and base motions, which occur with periods as short as 30 ps at 303 K.60,61 This probably indicates that the excess-electron hopping is dominated by the structural dynamics of the DNA.62,63 It should be noted that the structural dynamics of DNA is also affected by environmental fluctuations such as reorganization of water molecules and/or counterions surrounding the DNA to stabilize a radical anion nucleobase.64,65 Both theoretical and experimental results have shown that the time scale of water molecule motions is about 10−30 ps.66−69 As they reorient to accommodate the DNA including the sugar backbone and the bases, the reported time scale is expected to be similar to the intrinsic hopping rate. Thus, we suppose that the thermally activated structural fluctuations induce motions of the backbone sugars and bases to propel the radical anion from one nucleobase to the next. This suggests that structural fluctuations are one important factor in the dynamics of excesselectron transfer in DNA and that the rate of excess-electron transfer will be enhanced by thermally activated structural fluctuations. In hole transfer in DNA, two mechanisms for hole hopping have been proposed, i.e., migration of a localized nucleobase radical cation and migration of a polaron, where a radical cation resides in a delocalized structure composed of nucleobases.3 The migration of a polaron in DNA was found to be influenced by the motion of the Na+ ions and the water molecules and was named the gating mechanism.70,71 On the other hand, some research groups, including ours, found that thermal fluctuations assist hole hopping on each nucleobase via continuous oxidative processes.72−74 Fiebig and colleagues found the time scale for this motion to be 10−100 ps.74 As mentioned above, we suggested that the excess-electron hopping is dominated by the structural dynamics of DNA with a similar time scale. Thus, a fluctuation-assisted hopping mechanism is a reasonable explanation for excess-electron transfer in DNA.

AUTHOR INFORMATION

Corresponding Authors

*M. Fujitsuka: E-mail: [email protected]. Phone: +816-6879-8496. Fax: +81-6-6879-8499. *T. Majima: E-mail: [email protected]. Phone: +81-6-6879-8495. Fax: +81-6-6879-8499. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was partly supported by Grants-in-Aid for Scientific Research (Projects 25220806, 25288035, and others) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of the Japanese Government.

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REFERENCES

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CONCLUSION To the best of our knowledge, this is the first study suggesting the role of a fluctuation-assisted hopping mechanism in excesselectron transfer in DNA. In the sequences we studied, the excess-electron hopping occurred between neighboring bases. We confirmed that excess-electron transfer in DNA is governed by the hopping mechanism and successfully observed that the rate of excess-electron transfer can be enhanced with an increase in the driving force for CS, which is equivalent to the thermal energy transferred to DNA, which causes structural fluctuations in these DNAs. Thus, fast charge hopping due to 664

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