Driving Force Dependence of Charge Separation and Recombination

Sep 29, 2014 - Charge transfer in DNA has attracted great attention of scientists because of its importance in biological processes. However, our know...
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Driving Force Dependence of Charge Separation and Recombination Processes in Dyads of Nucleotides and Strongly Electron-Donating Oligothiophenes Shih-Hsun Lin, Mamoru Fujitsuka,* Mayuka Ishikawa, 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: Charge transfer in DNA has attracted great attention of scientists because of its importance in biological processes. However, our knowledge on excess-electron transfer in DNA still remains limited in comparison to numerous studies of hole transfer in DNA. To clarify the dynamics of excess-electron transfer in DNA by photochemical techniques, new electron-donating photosensitizers should be developed. Herein, a terthiophene and two 3,4-ethylenedioxythiophene oligomers were used as photosensitizers in dyads including natural nucleobases as electron acceptors. The charge separation and recombination processes in the dyads were investigated by femtosecond laser flash photolysis, and the driving force dependence of these rate constants was discussed on the basis of the Marcus theory. From this study, the conformation effect on charge recombination process was found. We expect that 3,4-ethylenedioxythiophene oligomers are useful in investigation of excess-electron-transfer dynamics in DNA.

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INTRODUCTION Charge transfer (CT) in DNA by hopping and tunneling processes through the nucleobases with well-ordered continuously π−π stacking has attracted attention of scientists for decades. From the mechanistic viewpoint, CT in DNA can be classified to hole transfer (HT) as oxidation of a nucleobase by an adjacent radical cation and excess-electron transfer (EET) as reduction of a nucleobase by an adjacent radical anion. In the HT in DNA, it has been well established that guanine (G) and adenine (A), which exhibit relatively low oxidation potentials, act as hole carriers; in contrast, in the EET in DNA, thymine (T) and cytosine (C) are expected to be the excess electron carriers due to their high reduction potentials.1−3 One of the key steps in the study of EET in DNA by photochemical techniques is an excess electron injection to DNA from a photosensitizing electron donor, which possesses sufficiently low oxidation potential in the excited state (EOXS1) to reduce a nucleobase. Various photosensitizers, such as stilbene diether,4,5 pyrene and its derivatives,6−9 and phenothiazine,10 have been used to investigate the electron injection to DNA by femtosecond laser flash photolysis. In the previous reports, we used dimer and tetramer of thiophene (2T and 4T) as the photosensitizing electron donors because of their high electron donating ability and well-known photochemical properties.11,12 In these studies, it was confirmed that singlet excited 2T and 4T can donate an electron to both T and C. Furthermore, the excess electron injection from 2T to A was confirmed, indicating that EET through consecutive As could be examined.12 For the study of the EET in DNA with various sequence, a new donor with an electron donor ability higher than 2T and 4T should be employed. © 2014 American Chemical Society

In the present study, as a photosensitizing electron donor, we used the dimer and trimer (2E and 3E, respectively) of 3,4ethylenedioxythiophene (EDOT)13 and terthiophene (3T) as a reference (Figure 1). Because of the strongly electron donating nature of the ether substituent, EDOT-based oligomers are expected to reduce various nucleobases efficiently. The redox and spectroscopic properties of EDOT-based oligothiophenes are compared with those of oligothiophenes in Table 1. To

Figure 1. Structures of (a) 2E, 3T, and 3E and (b) dyads 1−15. Received: September 24, 2014 Published: September 29, 2014 12186

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tion), and the 1H NMR spectrum was the same as in the literature.17 DNA Synthesis. The sensitizers, 2E, 3T, and 3E, were converted to corresponding phosphoramidite derivatives by procedures similar to those previously reported.17,18 All reagents were purchased from Glen Research (USA). All dyad molecules were synthesized on an Applied Biosystems 3400 DNA synthesizer with standard solid-phase techniques and purified on a JASCO HPLC with a reversed-phase C-18 column with an acetonitrile/ammonium formate (50 mm) gradient (Figure S1−S3, Supporting Information). The dyad compounds were characterized by MALDI-TOF mass spectroscopy (Table S1, Supporting Information). Apparatus. Steady-state absorption and fluorescence spectra were measured using a Shimadzu UV-3100PC and Horiba FluoroMax-4P, respectively. The subpicosecond transient absorption spectra 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). The seed pulse was generated by the Ti:sapphire laser (Spectra Physics, MaiTai VFSJ-W). Samples were excited using a 345, 370, or 400 nm laser pulse. The 345 and 370 nm laser pulses were generated by an optical parametric amplifier,19 whereas the 400 nm laser pulse was the second harmonic generation of output of the amplifier. A white continuum pulse, which was generated by focusing the residual of the fundamental light to a sapphire plate after a computer controlled optical delay, was divided into two parts and used as the probe and the reference lights, of which the latter was used to compensate the laser fluctuation. Both the probe and reference lights were directed to a rotating sample cell with 1.0 mm of optical path and were detected with a charge-coupled device detector equipped with a polychromator (Solar, MS3504). Details of pulse radiolysis are indicated in the Supporting Information.

Table 1. Oxidation Potentials in the Ground (EOX) and Singlet Excited State (EOXS1), Singlet Excitation Energy (ES1), and Absorption Peak Positions in the Singlet Excited State (λS1) and Radical Cation State (λ•+) of Oligothiophenes 2T and 3T and oligo(EDOT)s 2E and 3E 2T 2E 3T 3E

d

EOXa (V)

ES1b (eV)

EOXS1a,c (V)

λS1 (nm)

λ•+ (nm)

1.28 0.65e 1.19e 0.41e

3.53 3.54 3.08 3.02

−2.25 −2.89 −1.89 −2.61

503 530f 605f 620f

445 440f 585f 536f

a

Units: V versus NHE. bEstimated from the cross-point of the absorption and fluorescence spectra. cEOXS1 = EOX − ES1. dFrom ref 12 and 14. eFrom ref 13. fThis study.

clarify dynamics of excess electron injection process, the dyad molecules of oligothiophene and nucleotide (Figure 1) were examined by femtosecond laser flash photolysis in this study. In all dyads, oligothiophenes were tethered to the 3′-position of nucleobases. The present study revealed that the charge separation (CS) and charge recombination (CR) processes in these dyads can be analyzed by the Marcus theory and conformation of the dyad structure has an important role in the ET dynamics.

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EXPERIMENTAL SECTION Synthesis of 2E. 2E was synthesized according to the procedure in the reference paper13 using BisEDOT15 and BrOTBS16 as starting materials (Scheme S1 in the Supporting Information). Yield of the two-step reaction was 40%. Due to the very poor solubility of 2E, the corresponding 13C NMR spectrum was not determined: mp 184−186 °C; 1H NMR (400 MHz, CDCl3) δ 1.85 (m, 4H), 2.77 (t, J = 7.2 Hz, 4H), 3.66 (q, J = 5.6 Hz, 4H), 4.31−4.22 (m, 8H) ppm; FAB-HRMS calcd for C18H22O6S2 398.0858, found 398.0849. Synthesis of EDOT-OTBS. The synthesis of EDOT-OTBS was similar to that for 2E-OTBS (Scheme S2 in the Supporting Information): yield, 15%; colorless oil; 1H NMR (400 MHz, CDCl3) δ 0.05 (m, 6H), 0.90 (s, 9H), 1.84 (m, 4H), 2.71 (t, J = 7.2 Hz, 2H), 3.65 (t, J = 5.2 Hz, 2H), 4.17 (m, 4H), 6.11 (s, 1H) ppm; 13C NMR (100 MHz, CDCl3) δ −5.33, 18.30, 22.25, 25.92, 33.26, 62.16, 64.49, 64.65, 95.14, 117.62, 137.55, 141.45 ppm; FAB-HRMS calcd for C15H26O3SSi 314.1372, found 315.1477 ([M + H+]). Synthesis of 3E-OTBS. 3E-OTBS was synthesized according to the reported procedure (Scheme S2 in the Supporting Information):13 yield, 35%; mp 238−240 °C; 1H NMR (400 MHz, CDCl3) δ 0.05 (m, 12H), 0.90 (s, 18H), 1.84 (m, 4H), 2.71 (t, J = 7.2 Hz, 4H), 3.66 (t, J = 6.4 Hz, 4H), 4.36−4.20 (m, 12H). 13C NMR (100 MHz, CDCl3) δ −5.27, 18.35, 22.20, 25.98, 33.32, 62.28, 64.51, 64.94, 65.13, 106.06, 107.81, 115.65, 136.00, 136.59, 137.24; FAB-HRMS calcd for C36H54O8S3Si2 766.2519, found 766.2524. Synthesis of 3E. The synthetic procedure of 3E was the same as the one for 2E (Scheme S2 in the Supporting Information). Yield: 90%. Due to the very poor solubility of 2E, the corresponding 13C NMR spectrum was not determined: mp 192−194 °C; 1H NMR (400 MHz, CDCl3) δ 1.85 (m, 4H), 2.77 (t, J = 7.2 Hz, 4H), 3.66 (m, 4H), 4.31−4.22 (m, 12H); FAB-HRMS calcd for C24H26O8S3 538.0790, found 538.0780. Synthesis of 3T. 3T was synthesized according to the reported procedure (Scheme S3 in the Supporting Informa-

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RESULTS AND DISCUSSION Steady-state absorption spectra of 1−15 are shown in Figures 2 and S4 (Supporting Information). Absorption bands due to 2E,

Figure 2. Normalized absorption (dashed lines) and fluorescence (solid lines) spectra of 2E (yellow) and 1 (black), 2 (red), 3 (green), 4 (blue), and 5 (orange).

3T, and 3E appeared in the wavelength region longer than 300 nm for all dyads, whereas absorption bands around 275 nm are attributable to nucleobases. Fluorescence from the oligothiophene of the dyads was observed by selective excitation of oligothiophene as shown in Figures 2 and S4 (Supporting Information). It is clear that fluorescence intensity largely 12187

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depends on the nucleobase, whereas the peak position depends on oligothiophenes. To understand variations in the fluorescence intensity, driving forces for CS and CR (ΔGCS and ΔGCR, respectively) were calculated using eqs 1 and 2,3,20 ΔGCS = EOXS1 − E RED + C

(1)

ΔGCR = E RED − EOX + C

(2)

where ERED and EOX are the reduction potential of the nucleobases and oxidation potential of oligothiophenes (Table 1) reported in the literature.3 C is the Coulombic term, which was estimated to be −0.1 eV.20 From Table 2, it was confirmed Table 2. Driving Forces (ΔGCS and ΔGCR) and Rate Constants (kCS and kCR) of CS and CR in Dyads 1−15 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15

−ΔGCSa (eV)

kCSb (s−1)

−ΔGCRa (eV)

0.01 0.32 0.54 0.63 0.73 −0.75 −0.44 −0.22 −0.13 −0.03 −0.27 0.04 0.26 0.35 0.45

× × × × ×

3.63 3.32 3.10 3.01 2.91 3.93 3.62 3.40 3.31 3.21 3.39 3.08 2.86 2.77 2.67

6.4 1.0 7.7 1.0 2.5 d d 3.5 5.8 8.7 d 1.1 1.1 1.8 2.0

11

10 1012 1011 1012 1012

× 1010 × 1010 × 1010 × × × ×

1011 1012 1012 1012

kCRc (s−1) 1.1 6.7 2.9 3.8 3.4 d d 6.5 6.5 7.3 d 8.3 2.8 3.7 3.7

× × × × ×

1011 1010 1011 1011 1011

Figure 3. (a) Transient absorption spectra of 12 during laser flash photolysis using 400 nm femtosecond laser pulse as the excitation pulse. (b) Kinetic trace of ΔOD at 536 nm of 12 (red square) and fitted curve (green line).

× 109 × 109 × 109 × × × ×

3E•+, indicating the electron injection from 13E* to A in accordance with the negative ΔGCS value. The CS states were deactivated by CR to generate the ground state mainly. Spectra observed at longer delay time (longer than hundreds picoseconds) can be attributed to the solvated electron, which did not participate in reduction of the nucleobase. Figure 3b shows its kinetic trace and a fitted curve assuming 1.1 × 1011 s−1 of a rising component as well as a decay discussed later. Similar CS processes were confirmed with all dyads except for 6, 7, and 11, which exhibited only absorption band of the singlet excited state of photosensitizing electron donors, indicating the absence of CS due to highly positive ΔGCS values. The rate constants of CS (kCS) of all dyads were obtained by applying a single exponential function to the rising kinetic profile of oligothiophene radical cation and by applying a single exponential function to the decaying kinetic profile of singlet excited oligothiophene. The rate constants for CR (kCR) were obtained by applying a single exponential function to the decaying kinetic profile of the oligothiophene radical cation. For dyads 12−15, a dual exponential function has to be applied to realize an adequate fit. The estimated rate constants are summarized in Table 2 along with the driving force (ΔG) values. Notably, CS was confirmed even when G was used as the electron acceptor, despite G being known as a hole carrier in DNA.1,2 In addition, the CS process in dyad with A as the electron acceptor was accelerated by using stronger electron donating photosensitizer (2E and 3E) compared to our previous report.12 Thus, these results indicate that all natural nucleobases act as an acceptor of an excess electron by using EDOT oligomers as electron donors. As indicated in the above section, 12−15 decayed according to the dual exponential function (Table 3). Like dinucleobase dyads, the donor−acceptor dyads are expected to exist in various conformations in solution, which can be classified as stacked and unstacked forms, as shown in Figure 4. The

1010 e 1011 e 1011 e 1011 e

ΔGCS and ΔGCR were calculated using eqs 1 and 2, respectively. Estimated error is less than 20%. cEstimated error is less than 10%. d Not observed. eRate constant of the fast component. a b

that the extent of fluorescence quenching increased as an increase in the −ΔGCS value, indicating contribution of photoinduced CS in deactivation pathway of the singlet excited oligothiophenes. Notably, dyad 1 also showed fluorescence with reduced intensity, indicating a possibility that G acts as an electron acceptor by using 2E as a donor. Similar fluorescence quenching was observed with dyads with 3E and 3T except for the cases of 6, 7, and 11, as expected from the highly positive ΔGCS values, supporting the CS from the excited 3E and 3T. Because of the delay fluorescence, which is caused by the CR process, quantitative correlation between fluorescence intensity and the CS rate constant was not discussed. CS dynamics of the oligothiophene−nucleotide dyads were investigated by transient absorption measurements. The femtosecond laser flash photolysis studies were carried out by selective excitation of photosensitizers, 2E, 3T, and 3E. The transient absorption spectra of 2E and 1−15 are shown in Figures S5, S6, and S7 (Supporting Information). As a representative case, the transient absorption spectra and a kinetic trace of ΔOD of 12 are shown in Figure 3a,b, respectively. In Figure 3a, 12 showed an absorption band at 620 nm immediately after the excitation, which is attributed to 13E* generated by the laser pulse. With the decay of the absorption band at 620 nm within 10 ps approximately, an absorption band at 536 nm appeared concomitantly. Because the 536 nm band is similar to the absorption band of 3T•+ (Figure S8, Supporting Information) in position, this band is attributed to 12188

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Table 3. Rate Constants (kCR and kCR′) and Pre-exponential Factors (A and A′) of CR in dyad 12−15 12 13 14 15

kCRa (1010 s−1)

103Aa

kCR′a (1010 s−1)

103A′ a

Fs b

8.3 28 37 37

34 2.7 2.1 3.4

1.1 0.47 1.1 0.81

5.8 1.6 1.4 1.8

0.85 0.63 0.60 0.65

a

Estimated error is less than 10%. bFs = A/(A + A′), which was estimated as the fraction of stacked form of dyads in solution.

Figure 5. ΔG (ΔGCS and ΔGCR) dependence of kET (kCS, ●; kCR, ○). Numbers close to the marks indicate compounds. The solid and hollow black squares are the 2T dyads.12 The solid and hollow red circles are dyads 1−5. The solid and hollow green circles correspond to dyads 8−10. The solid and hollow orange circles correspond to dyads 12−15. The solid blue line was calculated by eqs 3 and 4 using λS, λV, V, and ℏ⟨ω⟩ of 0.20, 1.10, 0.050, and 0.19 eV, respectively.12 The solid pink line was calculated using λS, λV, V, and ℏ⟨ω⟩ of 0.23, 0.99, 0.043, and 0.19 eV, respectively.37

Figure 4. Proposed schematic energy diagram of CS and CR of 3E dyads (12−15). RU and RS are the distance between 3E and nucleobase (A, C, T, and U) in the stacked30−33 and unstacked forms,30,34 respectively. kCR and kCR′ are the CR rate constants in the stacked and unstacked forms, respectively.

kET =

⎛ ⎛ S m ⎞⎞ π |V |2 ∑ ⎜e−S⎜ ⎟⎟ ⎝ m ! ⎠⎠ ℏ λSkBT m ⎝ 2

⎛ (λ + ΔG + mℏ⟨ω⟩)2 ⎞ ⎟ × exp⎜ − S 4λSkBT ⎝ ⎠

conformational changes have large effects on various kinetics in dinucleobase dyads and donor−acceptor dyads, as indicated by both experimental21−29 and theoretical studies.26,30−32 We assumed that the fast and slow rate constants are due to the stacked and the unstacked forms, respectively, because faster CS and CR will be possible with shorter donor−acceptor distance in the stacked form (Figure 4). Because the time scale for the stacking/unstacking conformational change is reported to be on the order of 10 ns,32 conformational change will not compete with the CS and CR processes. If we assume identical extinction coefficients for oligothiophene radical cations in the stacked and unstacked forms, the ratio of the pre-exponential factor, Fs, will represent the ratio of the stacked and unstacked forms. From this assumption, it is indicated that 15−40% of dyads are in the unstacked form, whereas 60−85% are in the stacked form (Table 3). Notably, major contribution of the stacked form was also indicated by the theoretical calculation for ground state of dinucleobase dyads and dimers.31,32 In the case of CS processes of 12−15, contributions of the stacked and unstacked forms are also expected, but they are hard to distinguish because of fast kinetics. From the Fs values in Table 3 and results of theoretical works, the stacked form is expected to contribute to the kinetics mainly. For dyads except for 12− 15, stacked forms can be taken into account. It is evident from the estimated rate constants, the kCS value became larger with an increase in the −ΔGCS value and the kCR value became smaller with an increase in the −ΔGCR value, thereby indicating that both CS and CR processes in 1−15 comply with the Marcus theory.35,36 This relationship became clear when the observed rate constants were plotted against the ΔG (ΔGCS and ΔGCR) values (Figure 5). It is noted that for 12−15, only kCR values of the stacked form were included in Figure 5. According to the Marcus theory, the electron-transfer rate (kET) can be expressed using eq 3.36

S=

λV ℏ⟨ω⟩

(3)

(4)

In eq 3, λS is the solvent reorganization energy, V is the electronic coupling, S is the electron-vibration coupling constant given by eq 4, and ⟨ω⟩ is the averaged angular frequency. In eq 4, λV is the internal reorganization energy. Along with our previous report,12 the rate constants of CS and CR processes were well-reproduced by the Marcus theory with the parameters similar to the ones of hole injection and recombination processes.37 For CS and CR processes in photosensitizer-nucleotide dyads, this result yields valuable insights that the dynamics of oxidation and reduction of nucleobases by photosensitizers show driving force dependence similar to each other at room temperature. Slightly larger electronic coupling for electron injection (0.050 eV) than for hole injection (0.043 eV) is also interesting because it suggests a slightly larger interaction between LUMOs of donor and acceptors.

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CONCLUSION By use of strongly electron-donating oligothiophenes as electron donors, a panoramic survey of CS and CR processes in dyads with all natural nucleobases as electron acceptors was accomplished on the basis of the Marcus theory. In addition, the conformation effect on CR was found. The investigation of EET dynamics in DNA with 2E and 3E is in progress.

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ASSOCIATED CONTENT

S Supporting Information *

Synthesis schemes, characterization data, HPLC analysis, steady-state absorption and fluorescence spectra, and transient absorption spectra. This material is available free of charge via the Internet at http://pubs.acs.org. 12189

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AUTHOR INFORMATION

Corresponding Authors

*M. Fujitsuka. E-mail: [email protected]. *T. Majima. E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS

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REFERENCES

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

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