Photoinduced Electron Transfer in DNA - American Chemical Society

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Photoinduced Electron Transfer in DNA: Charge Shift Dynamics Between 8-Oxo-Guanine Anion and Adenine Yuyuan Zhang, Jordan Dood, Ashley Beckstead, Xibo Li, Khiem Van Nguyen, Cynthia J. Burrows, Roberto Improta, and Bern Kohler J. Phys. Chem. B, Just Accepted Manuscript • Publication Date (Web): 08 Feb 2015 Downloaded from http://pubs.acs.org on February 9, 2015

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The Journal of Physical Chemistry

Photoinduced Electron Transfer in DNA: Charge Shift Dynamics Between 8-Oxo-Guanine Anion and Adenine Yuyuan Zhang,a Jordan Dood,a,† Ashley A. Beckstead,a Xi-Bo Li,b Khiem V. Nguyen,b Cynthia J. Burrows,b,* Roberto Improta,c,* and Bern Kohler a,* a

Department of Chemistry and Biochemistry, Montana State University, Bozeman, Montana 59717, USA b

Department of Chemistry, University of Utah, 315 S. 1400 East, Salt Lake City, Utah 84112, USA c

CNR-Consiglio Nazionale delle Ricerche Istituto di Biostrutture e Bioimmagini (IBB-CNR), Via Mezzocannone 16, 80136, Napoli, Italy

Figures: 6 Tables: 4

†

Current address: School of Medicine and Biomedical Sciences, The University at Buffalo, SUNY, Buffalo, NY 14214

* Corresponding Authors: Bern Kohler: [email protected], Tel: +1 406-994-7931, Fax: +1 406-994-5407 Roberto Improta: [email protected], Tel: +39 081 2536614 Cynthia J. Burrows: [email protected], +1 801-585-7290

1 ACS Paragon Plus Environment


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Abstract Femtosecond time-resolved IR spectroscopy is used to investigate the excited-state dynamics of a dinucleotide containing an 8-oxoguanine anion at the 5’-end and neutral adenine at the 3’-end. UV excitation of the dinucleotide transfers an electron from deprotonated 8-oxoguanine to its πstacked neighbor adenine in less than 1 ps, generating a neutral 8-oxoguanine radical and an adenine radical anion. These species are identified by the excellent agreement between the experimental and calculated IR difference spectra. The quantum efficiency of this ultrafast charge shift reaction approaches unity. Back electron transfer from the adenine radical anion to the 8-oxguanine neutral radical occurs in 9 ps, or approximately 6 times faster than between the adenine radical anion and the 8-oxoguanine radical cation (Y. Zhang et al. Proc. Nat. Acad. Sci. USA 2014, 111, 11612-11617). The large asymmetry in forward and back electron transfer rates is fully rationalized by semiclassical nonadiabatic electron transfer theory. Forward electron transfer is ultrafast because the driving force is nearly equal to the reorganization energy, which is estimated to lie between 1 and 2 eV. Back electron transfer is highly exergonic and takes place much more slowly in the Marcus inverted region.

Keywords DNA base radicals, charge shift dynamics, photorepair, time-resolved vibrational spectroscopy, Marcus theory


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Introduction Oxidative damage of guanine produces 8-oxo-7,8-dihydroguanine (8-oxo-G), a redox-active nucleobase that can repair the cyclobutane pyrimidine dimer (CPD) photoproduct formed in DNA by UV light.1,2 8-Oxo-G has similar redox characteristics as flavin adenine dinucleotide (FAD),3,4 the cofactor used by the DNA repair enzyme photolyase.5-7 UV-B irradiation of 8-oxoG is proposed to transfer an electron to the nearby CPD, ultimately breaking the covalent linkage between the two pyrimidine bases.1,2 8-Oxo-G’s presence in a DNA or RNA strand can position it near a CPD without the need for the protein scaffold used by photolyase to bring FAD and the CPD into proximity. These features suggest that 8-oxo-G may have provided photoredox activity analogous to modern day flavins before the emergence of sophisticated repair enzymes.2 Very recently, we investigated the excited-state dynamics of the d(OA) dinucleotide containing 8-oxo-G at the 5’-end (O) and adenine (A) at the 3’-end, a crude FAD mimic, in D2O solution at neutral pH.8 The time-resolved IR spectra (TRIR) monitoring the double-bond stretching region revealed distinctive positive bands that arise from a charge-transfer (CT) state formed by electron transfer (ET) from 8-oxo-G to adenine, unambiguously demonstrating the ability of 8-oxo-G to participate in photoinduced ET.8 At alkaline pH, 8-oxo-G deprotonates (pKa = 8.6)9 to yield an anion with the structure shown in Fig. 1. It was reported previously that steady-state UV-B irradiation of aqueous solutions containing thymine-thymine and uracil-uracil CPDs and the nucleoside of 8-oxo-G (8-oxo-dGuo) results in enhanced CPD repair at pH 9 compared to pH 7.10 Notably, the flavin heterocycle in FADH2 bound to photolyase is also in a deprotonated anionic state.11,12 Although 8-oxo-G is not present in an oligonucleotide context in the experiments reported in ref. 10, the results suggest that the protonation state of the 8-oxopurine base could affect photorepair perhaps due to differences in excited-state lifetimes and ET quantum yields. Indeed, femtosecond transient absorption (fs-TA) experiments monitoring 3 ACS Paragon Plus Environment


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excited-state absorption revealed that the 8-oxo-G anion has a much longer excited-state lifetime compared to its neutral form (43 ps vs. 0.9 ps).13 Here, we study the photophysics of the d(OA) dinucleotide in alkaline aqueous solution (denoted d(O–A), where O– is the deprotonated form of 8-oxo-G in basic conditions) in order to learn how O– differs from O as an excited-state electron donor. Miller and co-workers first experimentally verified the presence of the Marcus inverted region,14,15 in which ET rates slow down even as the reaction exergonicity increases. A key was the study of intramolecular ET reactions that circumvent the maximum rate imposed by the diffusional encounter of the donor and acceptor (~2 × 1010 M-1 s-1). In their pioneering work on distance-dependent ET, Miller et al.16 suggested that the maximum rate of intramolecular ET exceeds 1013 s-1 when donor and acceptor are in contact. In DNA, neighboring nucleobases are in van der Waals contact, and UV excitation has been shown to yield a pair of oppositely charged radicals on a subpicosecond time scale.8,17,18 Yet, fs-TA experiments have also shown that the radicals persist for tens to hundreds of picoseconds.19-21 The dramatic asymmetry between forward and back ET rates suggests that back ET in DNA takes place in the Marcus-inverted region. In this paper, the ET dynamics of the 8-oxo-G anion are presented. Using a semiclassical formalism for nonadiabatic ET, a detailed comparison is made between rates for anionic vs. neutral 8-oxo-G that provides insight into the factors governing photoinduced ET between πstacked nucleobases.


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Methods 1. Experimental The TRIR laser system for conducting UV-pump/broadband-mid-IR-probe experiments has been discussed elsewhere.22 Briefly, the laser fundamental at 800 nm (80 fs, 3.5 mJ/pulse, 1 kHz) was produced by a Ti:Sapphire regenerative amplifier using chirped pulse amplification (Libra HE, Coherent). Approximately 1 W of the fundamental was used to pump a white-light seeded, twostage optical parametric amplifier (OPerA Solo, Coherent) that generated intense UV pump pulses at 265 and 295 nm. The 265 nm pump pulse energy was attenuated to 3.2 µJ and the beam size was 450 µm (fwhm) at the sample; these parameters for the 295 nm pump experiments were 1.8 µJ and 370 µm. The corresponding pump fluences were thus 1.7 – 2.0 mJ cm-2. A mechanical chopper set to 500 Hz let through every other pump pulse, allowing the change in absorbance (∆A) to be calculated as described in ref. 22. Approximately 800 mW of the laser fundamental was used to pump an optical parametric amplifier (TOPAS-C, Light Conversion) producing signal and idler pulses, which were mixed non-collinearly in a GaSe crystal for difference frequency generation (NDFG, Light Conversion). This produced approximately 10 mW of mid-IR probe pulses at the double-bond stretching region with 200 cm-1 of bandwidth. These probe pulses were split into “signal” and “reference” beams, where the reference beam was used to reduce the pulse-to-pulse noise. Both signal and reference beams were attenuated to approximately 200 µW at the sample. The composite TRIR spectra were obtained in two scans: 1550 – 1720 cm-1 was measured using λprobe = 6150 nm (1626 cm-1), whereas the region from 1475 – 1550 cm-1 was acquired with λprobe = 6450 nm (1550 cm-1).



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The relative polarization between the pump and probe pulse was set to the magic angle (54.7˚) to eliminate kinetics due to molecular reorientation. A motorized translation stage (Newport) controlled the optical delay of the pump and probe pulses at the sample, giving 4 ns of total delay with 8 fs resolution. Both the signal and reference probe beams were passed through the sample and focused into a spectrograph (Triax, Horiba). A 100 lines/mm grating blazed for 6000 nm projected the signals onto a liquid nitrogen-cooled, dual-row, 64-element MercuryCadmium-Telluride array (Infrared Systems Development). Kinetics traces were fit to one or two exponentials with the Igor Pro version 6.34 program (WaveMetrics), and the uncertainties reported here are twice the standard deviation (2σ). Two milliliters of sample were recirculated through a flow cell (Harrick) with a 100 µm path length. The synthesis and characterization of the d(OA) dinucleotide were based on ref. 23; the complete procedure is described in ref. 8. A 5.0 mM d(OA) solution was prepared in 50 mM phosphate buffer and 100 mM NaCl in D2O (to minimize IR absorption by H2O), and the pH was adjusted by adding concentrated NaOD solution (40 wt% in D2O, 99.5 atom % D, SigmaAldrich). The pD value (= −log10[D3O+]) was computed using the standard formula pD = pH + 0.4, where pH is the nominal reading made with a calibrated pH electrode. Because the extinction coefficient of the neutral form of O is 2× larger than that of the basic form at 295 nm, the pD was adjusted to 10.4 in order to minimize the amount of the neutral form present. UV−visible and FTIR spectra were taken after laser exposure and compared to those recorded for the fresh solution. No signs of photodegradation were observed. HPLC was also used to check for laser-induced oxidation. The elution time was consistent with fresh sample; the known oxidation products, which elute faster, were not observed.


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2. DFT Calculations Geometry optimizations, vibrational frequencies and intensities for monomeric molecules and radicals in their ground states were obtained by density functional theory (DFT) using the PBE0 functional24,25 and 6-31+G(d,p) basis set. A previous study of GMP and its cation in D2O showed that inclusion of the 2’-deoxyribose group and explicit D2O molecules (H-bonded to the exchangeable deuterons of the nucleobases) dramatically improves the agreement with experiment for the ring in-plane vibration and carbonyl stretching modes, respectively.26 In light of these findings, calculations were performed on the 2’-deoxyribonucleosides with five explicit D2O molecules. In the calculations, all labile protons were replaced by deuterons. The structures for the radicals of 8-oxo-7,8-dihydro-2’-deoxyguanosine (8-oxo-dGuo) and 2’-deoxyadenosine (dAdo) used in the calculations and the arrangement of explicit D2O molecules are shown in Fig. S1. The same arrangement of explicit solvent molecules was used to model both the radical and closed-shell version of each nucleobase. Only a dedicated study based on extensive molecular dynamics (MD) simulations (outside the scope of the present paper) could assess the structure of the first solvation shell around the nucleobases and its effect on the electronic state (see ref. 27 for an example). For 8oxo-dGuo and its anion, the number of water molecules around the C6=O or C6−O− group could depend on the charge, potentially affecting the computed IR frequencies. In order to explore this effect, test geometry optimizations were performed on both 8-oxo-dGuo and its anion solvated by six water molecules arranged as shown in Fig. S1c. In this case, the additional water molecule coordinated perpendicularly to the C6=O or C6−O− group leads to a further increase of the distance between the oxygen and carbon atoms of the carbonyl moiety by ∼0.01 Å, and thus a red shift of the calculated vibrational frequencies. In any case, in the absence of the outer



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solvation shells, calculations on small clusters likely overestimate the solute-solvent interaction energy, leading to unphysical effects in the calculation of the IR spectra. As a consequence, we chose a conservative approach that employs a cluster containing a minimum number (5) of explicit water molecules, a strategy that has previously yielded accurate IR spectra.8,26 The excited state of d(O−A) was explored by PCM/TD-M052X calculations (see SI). Note that the M052X functional is able to accurately treat the dispersion interaction between the two bases, and thus does not suffer from overestimating the CT state stability.28 These calculations were performed on the entire dinucleotide with the two bases in stacked conformation. Explicit water molecules were not included due to computational costs. Statespecific PCM/TD-DFT calculations29,30 were used to compute the solvent contribution to the reorganization energy. A polarizable continuum model (PCM) was used to account for the bulk solvent effect.31 The calculated vibrational frequencies were multiplied by a factor of 0.97 and broadened by a Gaussian function of 20 cm-1 fwhm. The calculated intensities were scaled to match the experimental extinction coefficients (ε).

Results 1. Experimental Results At pD = 10.4, the O moiety forms a stable enolate at the C6 position (O¯),9 whereas A is unchanged due to its lack of an acidic proton (see structure in Fig. 1). O¯ can be selectively excited at 295 nm, whereas 265 nm excites both O¯ and A (Fig. 1a). The excited-state dynamics are probed by broadband mid-IR pulses, which monitor the ring in-plane vibration and carbonyl stretching modes (Fig. 1b).


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Figure 1. UV–visible (a) and FTIR spectra (b) for d(O¯A) at pD = 10.4. The spectra for 8-oxo-dGuo (O¯) and AMP monomers at these conditions (dash lines) are also shown for comparison. The excitation wavelengths used in the pump-probe experiments are indicated by gray arrows. Vibrational mode assignments from ab initio calculations are included for convenience (see text).

Fig. 2a displays TRIR spectra for the O¯ monomer upon 265 nm excitation over an extended probing window where the spectral signature of the O neutral radical is expected (see calculation below). The IR spectrum at each delay time shown in Fig. 2 was an average of 5,000 spectra (10 s accumulation). The negative signals originate from ground state bleaching (GSB), which recovers biexponentially (τ1 = 3.0 ± 0.8 ps, τ2 = 48 ± 1 ps, see Fig. 3a). The expected GSB at 1680 cm-1 is masked by a strong positive signal at all delay times, hinting that the decay of the excited-state absorption (ESA) signal happens simultaneously with the GSB recovery. The excited-state dynamics of the O¯ monomer were described in detail in ref. 13.



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Figure 2. TRIR spectra following 265 nm excitation at the indicated pump-probe delay times for the O¯ monomer at pD = 10.4 (a) and the d(O¯A) dinucleotide at pD = 10.4 (b). The spectra following 295 nm excitation for d(O¯A) are shown in panel (c). Red arrows point to the positive features assigned to the CT state (see text). Curved black arrows point to the frequency (1589 cm-1) of the kinetic trace presented in Figure 3.

For d(O–A), the positive signal near 1680 cm-1 is absent, and the center frequencies and relative intensities of the negative signals in the TRIR spectra agree well with the inverted FTIR spectrum, as shown in Fig. 2b. Additionally, a new positive band at 1537 cm-1, indicated by a red arrow, can be clearly identified even at the earliest delay times. Decay of this strong feature and recovery of the GSB signal at 1589 cm-1 proceed in unison on a time scale of 9.3 ± 0.6 ps (compare Fig. 3, panels a and b. Table 1 summarizes the fitting parameters). By t ≈ 50 ps, all positive and negative signals have decayed completely to a featureless negative offset caused by D2O heating,32 indicating that virtually all d(O–A) excited states have returned to the thermally equilibrated ground state.


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Figure 3. Kinetic traces of O (νpyri) at 1589 cm-1 (a) and the positive feature at 1537 cm-1 (b) following 265 nm excitation of d(O¯A) at pD = 10.4. The kinetics trace for the monomeric 8-oxo-7,8-dihydro-2’deoxyguanosine (8-oxo-dGuo) at the same pD is included for comparison.

Table 1. Single-frequency fit parameters for the d(O¯A) mid-IR GSB and ESA signals. fast slow A1 a τ1 (ps) A2 a τ2 (ps) b 295 nm GSB 0.85 ± 0.08 9 ± 1 0.15 ± 0.03 50 ± 20 ESAc 1.0 ± 0.1 9±1 ― ― b 265 nm GSB 1.0 ± 0.1 9.3 ± 0.6 ― ― ESAc 1.0 ± 0.1 9.3 ± 0.6 ― ― a

Traces were fit to / / , and amplitudes were normalized, ∑ 1. Offset (A3) due to solvent heating not shown. Identical values indicate globally linked parameters. The uncertainties reported are 2σ values from the fitting program unless otherwise noted. b O (νpyri) at 1589 cm-1. The uncertainty of A1 for 265 nm excitation was estimated from the ratio of the noise floor (∆A = 2 × 10-5) to the maximum GSB signal (∆A = 3 × 10-4). c Monitored at 1537 cm-1. The uncertainty of A1 was estimated from the ratio of the noise floor (∆A = 2 × 10-5) and the maximum ESA signal (∆A = 2 × 10-4).

The distinct feature at 1537 cm-1 is also observed when the O– residue is selectively excited with a 295 nm pump pulse (Fig. 2c), and it decays with a time constant of 9 ± 1 ps (Table1), which is identical to that observed at 265 nm excitation within experimental error. However, the GSB at 1680 cm-1 is not nearly as pronounced. This suggests the existence of a positive signal in close proximity to 1680 cm-1, which is reminiscent of the strong ESA band 11 ACS Paragon Plus Environment


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implicated in the TRIR spectra of the monomeric O¯ (compare Fig. 2, panels a and c). Furthermore, a single-frequency fit to the GSB kinetics at 1589 cm-1 reveals a biexponential recovery. The majority of the GSB amplitude (85 ± 8%) decays on a time scale of 9 ± 1 ps, but a minor component (15 ± 3%) with a lifetime of 50 ± 20 ps is also required to fit the kinetics (Table 1). The latter is similar to the slow-decaying component observed for the O¯ monomer. It is important to note that although the GSB at 1589 cm-1 recovers biexponentially upon 295 nm excitation, the positive feature at 1537 cm-1 decays monoexponentially for both excitation wavelengths (Table 1).

2. Computational Results The calculated vibrational spectra for the 8-oxo-G anion (8-oxo-dGuo¯·5D2O in the calculation, denoted O¯ for simplicity) and A (dAdo·5D2O in the calculation) in the double bond stretching region are shown in Fig. 4a (see Fig. S2 for the entire spectra). Assignments based on the dominant character of each normal mode are indicated. The band centered at 1690 cm-1 (experimental and theoretical values are compared in Table 2) reflects predominantly C8=O stretching (νC8=O). The mode at 1624 cm-1 is mainly due to collective ring in-plane vibrations (νrings). The most intense band observed at 1590 cm-1 originates from a ring in-plane vibration localized on the pyrimidine ring (νpyri). Another intense feature at 1460 cm-1 receives significant contribution from the C2–ND2 group (νamino). The C6−O bond distance is significantly elongated in 8-oxo-dGuo¯·5D2O (1.28 Å, compared to the C8=O bond length of 1.24 Å), indicating singlebond character. Furthermore, the C6−O stretch is significantly coupled to the pyrimidine ring vibration. Our calculations predict that the νamino mode at 1460 cm-1 and the weak feature at ~1520 cm-1 are asymmetrically and symmetrically coupled with the C6−O stretching, respectively. For A, the ring in-plane vibration is predicted to lie in close proximity to νrings of O¯ 12 ACS Paragon Plus Environment

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in agreement with the FTIR spectrum (Fig. 1b). The relative positions and intensities of these vibrational modes are well reproduced by the calculations.

Figure 4. Calculated vibrational spectra for (a) the ground state 8-oxo-dGuo¯·5D2O, (b) 8-oxodGuo(N7D)•·5D2O neutral radical, and (c) 8-oxo-dGuo(N1D)•·5D2O neutral radical. The calculations for dAdo·5D2O and dAdo•¯·5D2O (dashed curves) from ref. 8 are included for comparison. (d) Difference spectra obtained from the above monomeric species. Molecular structures and mode assignments are included for convenience. All transition frequencies were multiplied by a factor of 0.97 and broadened by a Gaussian function with 20 cm-1 fwhm. The intensities were scaled to match the experimental ones.



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ET from O− to A creates an O neutral radical and an A radical anion. The vibrational spectra of the two tautomers of the neutral radical produced by one-electron oxidation of O− are predicted to be quite distinct in the double bond stretching region (compare panels b and c of Fig. 4). The N7-deuterated tautomer (8-oxo-dGuo(N7D)•·5D2O in the calculation, denoted O(N7D)• for simplicity) exhibits a prominent feature at 1745 cm-1. This mode is assigned to the stretching of the C8=O bond, which is particularly short (1.218 Å). Importantly, for O(N7D)• a prominent vibrational band is predicted at 1539 cm-1, which is assigned to νamino (strongly coupled with pyrimidine ring stretching). The N1-deuterated tautomer (8-oxo-dGuo(N1D)•·5D2O in the calculation, denoted O(N1D)•) lacks vibrational activity in this region. In this tautomer the deuteron at N1 decreases the partial double-bond character of the N1−C2 and N1−C6 bonds, while increasing the double-bond character of the C6−O (mainly responsible for the peak at 1655 cm-1) and C2−ND2 (related to the peak at 1587 cm-1) bonds. These changes are responsible for the large blue-shift of the νamino frequency upon going from O(N7D)• to O(N1D)•. The complete spectra are shown in Fig. S3.

Table 2. Experimental and theoretical (PCM/PBE0/6-31+G(d,p) and harmonic approximation) vibrational frequencies in cm-1 for the ground states of 8-oxo-dGuo¯·5D2O and two tautomers of its one-electron oxidation product 8-oxo-dGuo•·5D2O. All transition frequencies were scaled by a factor of 0.97. νamino νpyri νrings νC6=O νC8=O 8-oxo-dGuo¯·5D2O Expt. ― 1589 1612 ― 1685 Calc. 1460 1590 1623 ― 1690 • 8-oxo-dGuo(N7D) ·5D2O Expt. 1537 ― 1640 ― ― Calc. 1539 1600 1649 ― 1745 8-oxo-dGuo(N1D)•·5D2O Expt. ― ― ― ― ― Calc. 1587 ― 1616 1655 1693


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Discussion 1. New Deactivation Channel in the π-Stacked Dinucleotide Although the O¯ monomer has a lifetime of 50 ps in aqueous solution (Fig. 3a, green trace), much faster relaxation with a time constant of 9 ps (Fig. 3a, red trace) is observed when O¯ is πstacked with A. The ESA band of the O¯ monomer at 1680 cm-1 decays in 50 ps upon excitation at either 265 nm (Fig. 2a) or 295 nm.13 Pronounced differences in the TRIR spectra of the O¯ monomer compared to d(O¯A) (Fig. 2) provide evidence of a new deactivation channel in the dinucleotide. In order to assign the 1537 cm-1 band that only appears in the TRIR spectrum of the dinucleotide (Fig. 2, compare panels a and b), we use global target analysis to decompose the 2D data into a set of species-associated difference spectra (SADS), each of which is assumed to arise from a single transient species that decays monoexponentially.33-36

2. Kinetic Modeling A global fit to the time- and frequency-dependent signals measured with 265 and 295 nm excitation reveals two decay components that are in excellent agreement with the lifetimes obtained by fitting the single-probe-wavelength signals presented in Table 1 and Fig. 3. The fitting yielded a 9 ps time constant for both excitation wavelengths, and an additional 50 ps component with only 15% amplitude in the case of 295 nm excitation. A rise time of ~2 ps is also needed to reproduce the early-time kinetics. This slow signal increase, which is not seen in the kinetics of the monomers (e.g., compare red and green traces in Fig. 3a), is difficult to interpret. One possibility is that forward ET occurs relatively slowly due to dynamic stacking within the excited-state lifetime. However, 2 ps may be too fast for the large scale backbone motions required to move the bases to a more parallel conformation.37 Another possibility is that



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the blue shift of the absorption bands due to vibrational cooling (VC) could generate the rising signal.26 Indeed, careful analysis shows that the 1537 cm-1 feature exhibits a subtle blue shift at early times (see Fig. S4). The best kinetic model obtained from target analysis consists of two parallel decay channels—the photoexcited d(O¯A) dinucleotide branches to two states, which have lifetimes determined by global analysis. This kinetic scheme is summarized in Fig. 5. The 9 ps SADS obtained from global analysis is displayed in Fig. 6.

Figure 5. Kinetic scheme for d(O¯A) excited-state dynamics. The population of each channel and lifetime determined by global fitting are indicated (also see Table 1). The initial steps, indicated in gray, occur too quickly to be resolved in these experiments.


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Figure 6. Comparison of experimental SADS and the calculated difference spectrum for d(O¯A). (a) 9 ps SADS at 295 nm (short-dashed line) and 265 nm (long-dashed line) excitation obtained from global fitting, compared with the difference spectra obtained for 8-oxo-dGuo(N7D)• (solid line) calculated at the PCM/PBE0/6-31+G(d,p) level and harmonic approximation with explicit D2O molecules included; (b) the difference spectra obtained for 8-oxo-dGuo(N1D)• (gray) calculated at the same level of theory; (c) comparison of the experimental spectrum of 8-oxo-dGuo(N7D)• obtained from two-photon detachment of 8-oxo-dGuo− (orange dashed-dotted line) and the theoretical spectrum (orange solid line). The calculated frequencies have been multiplied by 0.97 and broadened by a Gaussian function of 20 cm-1 fwhm.

For 265 nm excitation, the shape of the 9 ps SADS (long-dashed line in Fig. 6a) closely matches the shape of the TRIR spectra at t ≥ 1 ps because there is only one contributing component on this time scale as is evident from the monoexponential decay of the GSB and ESA signals (Table 1 and Fig. 3). In this case, the spectral shape of the 9 ps component is insensitive to the exact kinetic model used in the target analysis. The 9 ps SADS obtained for 295 nm excitation (short-dashed line in Fig. 6a) is nearly identical in shape to that seen for 265 nm



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excitation. Although two transient species contribute to the TRIR spectra following 295 nm excitation, the large separation in time scales (9 and 50 ps) means that there is only one absorbing species at t > 50 ps, which in turn ensures clean extraction of the two SADS. The shape of the 50 ps SADS (see Fig. S5) closely resembles that of the monomer O−, suggesting that this component originates from unstacked conformations. In previous experiments, monomerlike decays have been observed in unstacked base systems.17,20,38 It is apparent from Fig. 6a that the common 9 ps SADS seen at both excitation wavelengths consists of three negative bands which correspond to the ground state bands of O and A (see assignments shown in Figs. 2 and 4), and a strong positive feature corresponding to absorption by a transient species.

Table 3. Standard reduction potentials (V vs. SHE) for the redox couples of interest. Electron Donors E°(O /O) or E°(O•/O–) 1.18a 0.67b •+

Electron Acceptors E°(A/A•– ) E°(TT/TT•–) −2.45c −1.96d

a

Value from ref. 39. Calculated as described in the SI. c Value measured in dimethylformamide from ref. 40. d The reduction potential of thymine dimer (TT) was obtained from Rehm-Weller fits to the fluorescence quenching of a series of electron donors by thymine dimer (ref. 41). The reduction potential vs. saturated calomel electrode (SCE) was converted to SHE by adding 0.24 V (ref. 42). b

3. Photoinduced Charge Shift in π-Stacked Bases ET has recently been shown to be an important decay channel for excited states of π-stacked nucleobases.8,17,18 Our calculations predict that ET from O− to A in d(O−A) is energetically feasible. In particular, the CT state of d(O−A) is calculated to be lower in energy than the lowest optically bright 1ππ* state localized on the O moiety (see SI). We discuss next the evidence that UV excitation of d(O−A) triggers interbase ET. ET in d(O−A) from O− to A is a charge shift reaction that generates a neutral 8-oxoguanine radical (O•) and an adenine radical anion (A•−). In 18 ACS Paragon Plus Environment

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contrast, excitation of d(OA) at neutral pH triggers charge separation, creating the oppositely charged radical ions O•+ and A•−.8 To estimate ∆G° for forward ET (FET) from O¯ to A, we use the following equation,43 ∆G°FET = e[E°(O•/O¯) − E°(A/A•¯) + w] – E00,

(1)

where e is the elementary charge, w is the work term arising from the electrostatic interaction of the products, E00 is the relaxed singlet energy, and the E° values are standard reduction potentials for the indicated couples. Experimental reduction potentials used in this study are summarized in Table 3. Because there is no evidence that ET takes place slower than 2 ps, the use of Ephoton instead of E00 may be more appropriate as suggested for ET reactions that take place on an ultrafast time scale. With this modification and because the work term for a charge shift reaction is zero, eq. 1 becomes, ∆G°FET = e[E°(O•/O–) − E°(A/A•–)] – Ephoton.

(2)

∆G°FET is calculated to be −1.56 eV at 265 nm and −1.08 eV at 295 nm using the reduction potentials in Table 3. The driving force (−∆G°FET) for the charge shift reaction is about 0.5 eV higher than for the charge separation reaction in d(OA) (see Table 4). Because forward ET is thermodynamically favorable at both excitation wavelengths the difference spectra calculated for the redox pairs O•/O¯ and A/A•¯ were compared with the experimental 9 ps SADS (Fig. 6a). For ground state d(O−A), the negative charge is localized on the oxygen atom in the C6 enolate group (see structure in Figs. 1 and 4) because the N7deuterated tautomer is thermodynamically more stable than the N1-deuterated form.9 For the neutral radical O•, the one-electron oxidized product of O−, the situation is reversed—consistent with ref. 44, our PBE0/6-31+G(d,p) calculation predicts that the N1-deuterated radical (O(N1D)•) is more stable than the N7-deuterated one (O(N7D)•) by 0.23 eV (see structures in Fig. 4).44



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Clearly, the calculated difference spectrum obtained from the less stable O(N7D)• provides a far better match to the 9 ps SADS than the one obtained with O(N1D)• (Fig. 6a and b). In a separate experiment, an electron was photodetached from the O¯ monomer to the water solvent by two-photon excitation at 265 nm. The resulting TRIR spectrum recorded approximately 4 ns after excitation is shown in Fig. 6c and compared with the theoretical spectrum. A distinct peak at ~1540 cm-1 matches well the theoretical frequency of the νamino mode of O(N7D)•. Therefore, the strong and distinct absorption band at 1537 cm-1 seen in photoexcited d(O¯A) is unambiguously assigned to νamino of O(N7D)• generated from a photoinduced charge shift reaction. The excellent match between the experimental and theoretical spectra indicates that the O(N7D)• radical decays back to O¯ on a time scale of 9 ps via back ET before tautomerization to the thermodynamically more stable O(N1D)• radical can take place. Considering that the neutral radical is a very weak acid (pKa = 6.6, see discussion of this value in the SI),44 the deprotonation required for tautomer interconversion is expected to take place too slowly to compete with the high rate of back ET. Unfortunately, the vibrational marker bands of A•− are predicted to be weak (Fig. 4b). The strongest band in our spectral window, a mode at 1610 cm-1, is hidden in the d(O–A) TRIR spectra by the strong νpyri mode of O– and the νamino mode of O(–DN1)•. This raises the question of whether O(N7D)• is created by transferring an electron to A, or by ejecting an electron to the solvent. Compelling evidence against the latter possibility comes from the 9 ps SADS determined for 295 nm excitation. The A moiety cannot be directly excited to a significant extent by a 295 nm photon, yet the long-lived SADS reveals a negative feature centered at 1623 cm-1, which is a marker band for ground state adenine. The bleaching of vibrations in the electronic ground state of A would not be seen if excitation were to remain fully localized on O at all times.


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Instead, the bleaching of A vibrations is consistent with an initial excited state on O that transfers an electron to A. The same conclusion is reached by considering the 9 ps SADS for 265 nm excitation. The GSB recovery of O– and A would proceed differently if water were the electron acceptor, and not A. The electron ejected to the solvent and its geminate partner O• would likely be separated by several solvent shells, and the geminate recombination would extend to the nanosecond time scale as commonly seen in photodetachment experiments.45,46 In the case of d(OA−), however, the dynamics cease roughly 50 ps after excitation at 265 nm. Evidence therefore suggests that the electron initially localized on the C6–O– enolate group of O– is transferred to A, creating O(N7D)• and an A•– radical, even though the latter is not observed spectroscopically.

4. Comparison to d(OA) photophysics at neutral pH The ∆G°FET for forward ET from O to A at neutral conditions, generating a pair of oppositely charged radical ions, O•+ and A•–, is −1.05 eV and −0.57 eV at 265 nm and 295 nm excitation, respectively (Table 4). Forward ET takes place in this case faster than the instrumental response time (< 1 ps). The quantum yield of charge separation depends markedly on the excitation wavelength and is equal to 0.4 at 265 nm (UV-C), but decreases to only 0.1 at 295 nm (UV-B).8 In contrast, the charge shift quantum yield for d(O–A) approaches unity at 265 nm as indicated by the absence of a monomer-like 50 ps decay. At 295 nm, the efficiency decreases slightly to 0.85 and the remaining population decays via the monomer-like pathway (Table 1 and Fig. 5). The higher quantum yield of forward ET for d(O–A) than for d(OA) may be because the rate of forward ET in the former is significantly faster than the rate of other nonradiative decay channels. Although the driving force for forward ET in d(O–A) is larger than for d(OA), we



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cannot use this relationship to determine which reaction is faster as the reorganization energy is expected to differ for charge shift and charge separation reactions (see below).47 However, the competing S1(1ππ*) S0 nonradiative transition proceeds on a time scale of 50 ps for O–, which is much slower than the photoinduced charge shift reaction that takes place in less than 2 ps. In comparison, charge separation and nonradiative decay by O in d(OA) both occur on the subpicosecond time scale. This suggests that the higher quantum yield for forward ET from O– to A may be due to the slower rate of nonradiative decay by the anion. At both pD conditions, the transient radicals decay via back ET. At neutral pD, the back ET between O•+ and A•– radical ions, or charge recombination, takes place with a time constant of 60 ps.8 Decay of the 1537 cm-1 vibrational mode of the neutral radical O• indicates that back ET occurs with a time constant of just 9 ps for d(O–A). ∆G° for the two back ET reactions O• + A•– → O– + A and O•+ + A•– → O + A can be estimated by the following equations: ∆G°BET = e[E°(A/A•–) − E°(O•/O–) – w]

(3a)

∆G°BET = e[E°(A/A•–) − E°(O•+/O) – w]

(3b)

As mentioned previously, w is zero for the charge shift reaction 3a, but nonzero for the charge recombination reaction 3b. Estimating w requires a model for the heterogeneous dielectric environment experienced by stacked bases in DNA.48 Regions near the minor groove of DNA are estimated to have an effective dielectric constant of 20.49 Recent electrostatic force microscopy experiments suggest that the dielectric constant of double-stranded DNA is approximately 8.50 Using effective dielectric constants of 20 and 8, the work term amounts to −0.2 and −0.5 eV, respectively. These large values can significantly reduce the driving force for back ET calculated with equations 3a and b. However, we expect the work term to be smaller than these


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estimates in a dinucleotide like d(OA) or d(O–A) because the bases are more effectively hydrated than stacked bases in the core of double helical DNA. In this case, the dielectric constant appropriate for a dinucleotide may approach that of water (εr = 80). Combining this higher value with a separation of 3.4 Å predicts a value of w on the order of −0.05 eV. This value is small enough compared to the overall driving force to be neglected as was done in a study of the photophysics of FAD in aqueous solution.3 Rates of forward and back ET in d(OA) at neutral and basic conditions were analyzed using a nonadiabatic ET formalism (Table 4). In particular, ET reaction rates ( kET ) were estimated using the semiclassical Hopfield expression for nonadiabatic ET derived from conventional Marcus theory,51-53 ,

(4)

where VR is the electronic coupling between the reactant and the product, ∆G° is the free energy of the ET reaction, λ is the total reorganization energy, and

, and ℏ is the

energy of the characteristic vibrational mode coupled to ET. The total reorganization energy includes contributions from the solvent and from vibrational modes of the donor and acceptor that are strongly coupled to charge transfer. In Table 4, the driving force (−∆G°BET) for each back ET reaction was computed using eqs. 3a and 3b. The time constants of the reactions (τBET) in column 5 of Table 4 are those determined from the TRIR experiments (Table 1 and ref. 8). A value of ℏ = 0.33 eV (2700 cm-1) was assumed for the vibrational mode in equation 4, corresponding roughly to an OD or ND stretch. These modes were chosen because the observed back ET rate is faster in H2O than in D2O (see Fig. S6), suggesting that the O–H(D) stretch and/or the bending overtone are important 23 ACS Paragon Plus Environment


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accepting modes. Then, using values of VR of 100 cm-1 and 1000 cm-1, values that are assumed to bracket the actual couplings, the total reorganization energy (λ, column 2 in Table 4) was calculated for the back ET reactions using equation 4.

Table 4. Reorganization energies (λ) and time constants for forward ET (τFET) calculated from eq. 4 as described in the text. BET Reaction O• + A•¯ → O¯ + A O•+ + A•¯ →O+A a

b

λ (eV) 1.0 1.65 1.11 1.60

VR (cm-1) 1000 100 1000 100

∆G°BET a (eV) −3.12 −3.12 −3.63 −3.63

τBETb (ps) 9 9 60 60

∆G°FET c (eV) −1.56 (−1.08) −1.56 (−1.08) −1.05 (−0.57) −1.05 (−0.57)

τFET d (ps) 0.02 (0.01) 1 (2) 0.01 (0.015) 1.6 (3.4)

Calculated from equations 3a and b using values in Table 3.

Experimental values from this study and ref. 8.

c

∆GFET values were calculated from equation 2 using Ephoton = 4.68 eV (265 nm) and, in parentheses, 4.20 eV (295 nm). d Calculated for 265 nm excitation using equation 4 and ET parameters in the same row. Values in parentheses are for 295 nm excitation.

The actual electronic coupling may fall toward the lower end of this range based on comparisons with related donor-acceptor complexes. For example, Kao et al.54 obtained a coupling constant of ~150 cm-1 (18.6 meV) for ET in a covalently linked, π-stacked donoracceptor complex containing N-acetyl-tryptophan methylester and thymine. A similarly small coupling value of ~100 cm-1 was determined by Heitele et al.55 for porphyrin-quinone cyclophanes that adopt a π-stacked geometry like the nucleobases. Lewis et al.56 estimated couplings of 200 to 350 cm-1 for hole transfer from an aromatic linker to a π-stacked adenine. On the other hand, much larger couplings of ~1000 cm-1 were reported for contact radical ion pairs such as those formed between alkyl-substituted benzene donors and a tetracyanoanthracene acceptor.57 If VR is as large as 1000 cm-1, then the ET reaction becomes adiabatic and equation 4 should no longer apply. However, Gould et al.57 suggested that the 24 ACS Paragon Plus Environment

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expression for nonadiabatic ET still satisfactorily predicts adiabatic ET rates when the driving force is sufficiently large compared to the reorganization energy. Table 4 shows that even with an electronic coupling as large as 1000 cm-1 the predicted ET parameters are mostly reasonable. As is often the case with fits to a nonadiabatic rate expression like equation 4, the ET rates are sensitive to the choice of parameters. For example, the ET rate is proportional to the square of the electronic coupling constant VR. As we used likely upper and lower limits of VR to compute λ, it is not easy to estimate the errors in the computed values. Nevertheless, the estimated reorganization energies range from 1 to 2 eV, and are in good accord with reported values for similar donor-acceptor systems. Newton, Rösch, and co-workers calculated λ for ET between two adjacent π-stacked nucleobases embedded in a DNA duplex by dividing the DNAwater system into five different dielectric regions: the donor-acceptor pair, other nucleobases in the DNA duplex, the sugar-phosphate backbone, water bound to the DNA, and bulk water. The values obtained ranged from 1.1 to 1.9 eV.58 Gould et al. estimated λ to be approximately 0.7 eV for alkyl-substituted benzene donor and tetracyanoanthracene acceptor.57 A much larger λ value of 2.1 eV was reported for N-acetyl-tryptophan methylester as donor and thymine as acceptor.54 In both cases, the distance between the aromatic donor and acceptor is 3.5 to 4.0 Å, similar to the spacing between the nucleobases in DNA. It is generally accepted that λ is 0.9 – 1.2 eV for the hole-injection and electron-hole recombination steps between the hole donor and its nearest πstacked nucleobase in stilbene-capped DNA hairpins.56 Several theoretical studies of hole transport along DNA duplexes also predicted similar λ values.59-61 The reasonable λ values obtained from equation 4 indicate that the semiclassical, nonadiabatic formalism can satisfactorily account for the observed rates of back ET in photoexcited d(OA) and d(O−A). In each case, the estimated value of λ is smaller than the



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driving force, confirming Marcus inverted behavior. The λ values estimated in Table 4 are somewhat smaller than values of 2.15 eV and 2.32 eV for the charge shift and charge separation cases, respectively, calculated using quantum chemistry methods (see SI). The prediction that λ is greater for charge separation than for charge shift is consistent with the expectation that shifting an electron from one base to another requires less solvent reorganization than when two oppositely charged radical ions recombine to yield neutral molecules.47 The reorganization energies are more similar in Table 4, but this may be due to the crude model used and uncertainty about the appropriate value of the electronic coupling. For both d(OA) and d(O−A), there is a large asymmetry in the forward and back ET rates. Back ET takes place on a time scale of 60 and 9 ps for d(OA) and d(O−A), respectively, while the forward ET, albeit not experimentally resolvable, takes places in less than 1 or 2 ps. To accurately describe the ultrafast forward ET, nonequilibrium solvent and solute effects must be taken into account. For example, coherent vibrational effects of the solute results in oscillatory pattern of the ET rates, and the full reorganization energy of the solvent may not be available to facilitate the ultrafast ET reaction.62 Of course, the inertial and diffusional solvation of water occur on time scales of < 50 fs and ~500 fs, respectively, which are fast enough to promote ultrafast ET reactions.63 With the caveat that nonequilibrium effects may be important, and assuming that λ, VR, and ℏ take on identical values as for the back ET reaction, the semiclassical nonadiabatic formalism (equation 4) predicts forward ET rates that range from 10 fs to 3 ps (last column in Table 4). It has been reported that λ and VR may differ for forward and back ET reactions,54-56,64 because different electronic states are involved. For example, the Coulombic interaction between the oppositely charged porphyrin and quinone radical ions in cyclophanes leads to a smaller


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donor-acceptor distance for charge recombination in comparison to charge separation and thus a larger VR.55 Even if we use λ and VR values 25% smaller than those used for back ET (similar to the trend observed in the cyclophane systems),55 the slowest forward ET reaction takes place with a 3 ps time constant. It is apparent that the fast rates observed experimentally stem from the small driving force of the forward ET reactions. In spite of its simplicity, the model succeeds in predicting the ultrafast rates of forward ET and the much slower rates of back ET in both dinucleotides.

5. Comparisons to DNA Charge Transport The O− anion can deliver an electron more efficiently to its π-stacked A neighbor than neutral O. However, the O•/A•− radical pair generated in the charge shift reaction is energetically more stable than the O•+/A•− radical pair produced at neutral pH. As both radical pairs are in the Marcus inverted region, back ET for the former proceeds faster than for the latter (Table 4). This is similar to the hole injection and hole-electron recombination observed in the synthetic hairpins investigated by Lewis65 and Majima66 and their co-workers. For example, the hole injection from diphenylacetylene-4,4’-dicarboxamide (DPA) to its nearest guanine is energetically more favorable and thus faster than injection to adenine on account of the low oxidation potential of guanine.56 However, the low-energy exciplex generated in the former process results in rapid charge recombination and thus low hole-transport quantum efficiency.56,65 Similarly, the quantum efficiency of excess electron transfer (as opposed to hole transfer) along a DNA strand also suffers from rapid back ET. Although the electron injection from stilbene diether to a nearby pyrimidine base takes place in less than several picoseconds, charge recombination between the radical ions proceeds on a time scale of tens of picoseconds.67 This



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time scale is similar to what we have observed for the d(OA) dinucleotide and orders-ofmagnitude faster than for electron and hole hopping in DNA.65 Evidence suggests that virtually all exciplexes generated in UV-irradiated DNA strands such as d(OA) and other di- and oligonucleotides decay via efficient charge recombination.8,38 The lack of follow-on reactions contributes to the photostability of the genetic material. On the other hand, in synthetic DNA hairpins containing an electron- or hole-donating aromatic linker, the exciplex generated by hole or electron injection initiates charge transport along the DNA strand via either superexchange or a hopping mechanism. The former is responsible for shortrange hole transport over 1 to 3 base pairs in DNA hairpins, whereas the latter is responsible for long-range transport over 10 Å via several charge ‘hopping’ steps.68 Charge transport is only possible because superexchange or charge hopping occurs faster than the charge recombination within the initial exciplex. Charge recombination between DPA and a guanine radical ion proceeds on a time scale of approximately 1.2 ns.56 This is orders of magnitude slower than the observed rate for O•+ + A•¯→ O + A, even though the driving force for charge recombination is nearly the same (3.67 eV vs. 3.63 eV). Using the parameters from ref. 56 in eq. 4 predicts a rate constant on the order of 108 s-1 in qualitative agreement with Lewis et al. This comparison shows that the predicted ET rates depend sensitively on the choice of λ and ℏ, which control the width of the free energy parabola (see equation 4). Charge recombination following UV-induced charge separation in natural DNA and synthetic hairpins is highly exergonic. This is in stark contrast to the thermoneutral hole- or electron-hopping that is usually of interest in DNA (e.g., 5’-G•+G-3’ ⟶ 5’-GG•+-3’). Theoretical studies suggest that the reorganization energy for charge hopping also falls in the 1.0 – 1.5 eV 28 ACS Paragon Plus Environment

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range,60,69 while the donor-acceptor coupling can be as large as 1000 cm-1. In this case, the nonadiabatic formalism predicts a much faster rate than is seen experimentally (~109 s-1) and an adiabatic formalism has to be invoked.60

6. Implications for CPD photorepair The high quantum yield for forward ET seen in d(O–A) may indicate that O– can deliver an electron more efficiently to a thymine CPD (TT) than neutral O. This could explain why both thymine and uracil dimers underwent ring-opening reversion in the presence of the 8-oxo-G nucleoside in 10-fold higher yield at pH 9 compared to pH 7.10 However, as was discussed above for charge transport along DNA strands, the quantum yield of photoinduced ET is not the sole factor controlling the CPD repair yield. For example, if the back ET reaction is fast, it may compete with the breaking of the C5–C5’ and C6–C6’ σ-bonds of the one-electron reduced CPD, decreasing the efficiency of photorepair.7 Indeed, when the pH-dependence of the repair yield was studied by steady-state methods in oligonucleotides (see Fig. S7 in the SI), no enhancement of yield was observed up to pH 9, suggesting that faster back ET in the DNA duplex might counteract the nominal advantage that O– is a slightly better electron donor. Due to the high cost of synthesis, ET rates for systems containing both O and CPD by TRIR spectroscopy have yet to be directly measured. Nevertheless, these rates can be estimated from the driving forces calculated by equation 3. The computed ∆GBET values for the two reactions involving thymine dimer are displayed in Table 5. The large driving forces once again place the reactions in the Marcus-inverted region (see discussion above). However, both reactions are ~0.5 eV less exothermic than when adenine is the electron acceptor. This reduction in driving force and the concomitant decrease in τBET (Table 5) suggest that rapid back ET could 29 ACS Paragon Plus Environment


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compete with scission of the C6–C6’ linkage of the CPD, which is reported to occur with a time constant of 90 ps in photolyase7 and 435 ps in flavin-CPD model experiments.4 There is a delicate balance between forward ET yield and the back ET rate—for alkaline conditions, the quantum efficiency for the forward ET is higher, but the back ET that competes with photorepair is faster; at neutral conditions, on the other hand, the forward ET is not nearly as efficient, but back ET proceeds slower. Similar considerations determine the efficiency of CPD repair by photolyase.6,7,70,71 Table 5. Predicted back ET rates for the TT radical anion with O• and O•+ compared with rates for A•¯. τBET Reaction ∆G°BET a (eV) (ps) O• + TT•¯ → O¯ + TT −2.63 0.6b – 3c O•+ + TT•¯ → O + TT −3.14 3d – 11e • •¯ ¯ O +A →O +A −3.12 9 O•+ + A•¯ → O + A −3.63 60 a

Calculated using values shown in Table 3. Computed by equation 4 with λ = 1.0 eV, VR = 1000 cm-1, T = 298 K and ℏ = 2700 cm-1. c Computed by equation 4 with λ = 1.65 eV, VR = 100 cm-1, T = 298 K and ℏ = 2700 cm-1. d Computed by equation 4 with λ = 1.1 eV, VR = 1000 cm-1, T = 298 K and ℏ = 2700 cm-1. e Computed by equation 4 with λ = 1.6 eV, VR = 100 cm-1, T = 298 K and ℏ = 2700 cm-1. b

Conclusions We have demonstrated that a photoinitiated charge shift reaction takes place on an ultrafast time scale and with virtually 100% quantum efficiency in the case of d(O–A), generating an O• neutral radical and the A•– radical anion. The ET yield is unity at 265 nm (UVC) excitation and decreases to 0.85 at 295 nm (UVB). Although highly reactive radical ions are generated, their


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parent molecules are reformed on a time scale of 9 ps, making this one of the fastest back ET reactions in DNA di- and oligonucleotides.38 Extremely fast ET prevents follow-on reactions such as tautomerization and (de)protonation from taking place, thereby inhibiting DNA photodamage. Back ET between O• and A•– and between O•+ and A•– is highly exergonic and both reactions take place in the Marcus inverted region. On the other hand, the forward ET reactions for both photoexcited d(OA) and d(O–A) occur in a region where –∆G is comparable in size to λ, allowing the rates of forward ET to occur at close to the maximal possible values (> 1013 s-1). The high quantum yield for ET in d(O–A) suggests that an electron could be transferred rapidly and efficiently from O to a neighboring CPD. However, this advantage may be offset by the high rate of back ET predicted from the Marcus theoretical analysis presented in this study. Further work is required to understand the competition between forward and back ET important for CPD cleavage. Although the modeling is crude at this point, the reasonable agreement between the predictions of semiclassical non-adiabatic Marcus theory and experiment is an encouraging first step. In particular, the analysis presented here is the first to offer an explanation for the strong asymmetry in forward and back ET rates. With further refinement and realistic estimates of the electronic coupling, it should be possible to understand ET rates resulting from UV excitation of DNA in a quantitative way that goes beyond the qualitative correlation between driving force and charge recombination rates noted previously.38



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Associated Content Supporting Information Details about excited state calculations and the calculation of the reorganization energy are included. A brief discussion of reduction potentials of 8-oxo-G radicals is given together with supplementary figures. This material is available free of charge via the Internet at http://pubs.acs.org.

Acknowledgement Work at Montana State University was supported by NSF (CHE-1112560) and NASA (NNX12AG77G). The TRIR apparatus was constructed with funding from the M. J. Murdock Charitable Trust. Work at University of Utah was supported by NSF (CHE-1152533). R. I. was supported by the Italian Ministero dell’Istruzione, dell’Università e della Ricerca (MIUR Grants PRIN-2010ERFKXL and FIRB-RBFR08DUX6-003), and French Agency for Research Grant ANR-12-BS08-0001-01.


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TOC Graphic


Photoinduced Electron Transfer in DNA - American Chemical Society

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