J. Phys. Chem. B 2008, 112, 7315–7319
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Interaction between Thymine Dimer and Flavin-Adenine Dinucleotide: A DFT and Direct Ab Initio Molecular Dynamics Study Hiroto Tachikawa*,† and Hiroshi Kawabata‡ DiVision of Materials Chemistry, Graduate School of Engineering, Hokkaido UniVersity, Sapporo 060-8628, Japan, and Department of Electronic Science and Engineering, Kyoto UniVersity, Nishikyo-ku, Kyoto 615-8510, Japan ReceiVed: January 10, 2008; ReVised Manuscript ReceiVed: March 25, 2008
The interaction between the fully reduced flavin-adenine dinucleotide (FADH-) and thymine dimer (T)2 has been investigated by means of density functional theory (DFT) calculations. The charges of FADH- and (T)2 were calculated to be -0.9 and -0.1, respectively, at the ground state. By photoirradiation, an electron transfer occurred from FADH- to (T)2 at the first excited state. Next, the reaction dynamics of electron capture of (T)2 have been investigated by means of the direct ab initio molecular dynamics (MD) method (HF/3-21G(d) and B3LYP/6-31G(d) levels) in order to elucidate the mechanism of the repair process of thymine dimer caused by the photoenzyme. The thymine dimer has two C-C single bonds between thymine rings (C5-C5′ and C6-C6′ bonds) at the neutral state, which is expressed by (T)2. After the electron capture of (T)2, the C5-C5′ bond was gradually elongated and then it was preferentially broken. The time scale of the C-C bond breaking and formation of the intermediate with a single bond (T)2- was estimated to be 100-150 fs. The present calculations confirmed that the repair reaction of thymine dimer takes place efficiently via an electrontransfer process from the FADH- enzyme. 1. Introduction The UV irradiation of DNA sometimes causes the formation of cyclobutane pyrimidine dimers (expressed by PyrPyr) between two adjacent thymine bases in DNA. Photolyase can cleave the cyclobutane ring of the PyrPyr by irradiation of near-UV light. Flavoprotein is one of the photolyases and contains two noncovalently bound chromophores. One chromophore is the fully reduced flavin-adenine dinucleotide (FADH-) and the catalytic cofactor that carries out the repair function upon excitation by either direct photon absorption or resonance energy transfer from the second chromophore, which is an antenna pigment that harvests sunlight and enhances repair efficiency.1–3 As a model for the catalytic reaction, it has been proposed that the excited flavin cofactor transfers an electron to the PyrPyr to generate a charge-separated radical pair (FADH radical + (PyrPyr)-).4,5 The anionic ring of the dimer is split by a [2 + 2] cycloreversion, and the excess electron returns to the flavin radical to restore the catalytically competent FADH-. Recently, Kao et al. observed directly thymine dimer repair in DNA by photolyase using femtosecond synchronization of the enzymatic dynamics with the repair function.6 They observed direct electron transfer from the excited (FADH-) to the thymine dimer (T)2 in 170 ps and back electron transfer from the repaired thymine in 560 ps. Pezeshk and co-workers measured electron spin resonance (ESR) spectra of thymine dimer radical anion formed at low temperature in the condensed phase.7 They suggest that the electron addition to the thymine dimer followed by ring opening occurs so fast that only the monomer radical anion was detectable at 77 K. Thus, it is well-known that one* Corresponding author. E-mail:
[email protected]. Fax: +81 11706-7897. † Hokkaido University. ‡ Kyoto University.
electron reduction strongly contributes to the thymine repair. Formation and repair reactions of thymine dimers have been investigated by several groups. Femtosecond time-resolved infrared spectroscopy showed that thymine dimer is fully formed around 1.0 ps after UV irradiation.8 This ultrafast photolesion rate points to an excited-state reaction that is nearly barrierless for bases that are properly oriented at the instant of light absorption. It was suggested that the low quantum yield of this photoreaction results from infrequent conformational states in the unexcited system. Several theoretical works have been carried out for thymine dimer to elucidate the dimerization mechanism. The formation of thymine dimers in DNA was investigated by means of the density functional theory (DFT) method.9 Although it is found that a thermally induced [2 + 2] cycloaddition reaction proceeds via a very high energy transition state (80-88 kcal/mol above the reactant complex), the energy barrier for UV light induced formation is only a few kilocalories per mole. Very recently, Boggio-Pasqua et al. have calculated potential energy curves (PECs) for the dimerization of thymine molecules.10 The groundstate PEC showed that the ground-state pathway has an activation barrier as high as 70 kcal/mol. At the excited state, photochemical [2 + 2] cycloaddition takes place through a converted mechanism. The barrierless process leads to a lowlying conical intersection S0/S1 states. Thus, the formation mechanism of thymine dimer from two monomers has been well-established from theoretical points of view. On the other hand, the DNA repair process of thymine dimer is not clearly understood. Experimental model studies have demonstrated that both the photodimer radical anion and cation undergo facile fragmentation reactions.11–13 Static ab initio calculations were carried out for the fragmentation reaction of thymine dimer radical anion and cation.14,15 The calculation showed that the unpaired electron of thymine dimer radical cation is localized on the lengthened C6-C6′ bond of thymine dimer and the fragmentation starts with the cleavage
10.1021/jp801564t CCC: $40.75 2008 American Chemical Society Published on Web 05/27/2008
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dQj ∂H ) dt ∂Pj dPj ∂H ∂U )) dt ∂Qj ∂Qj where j ) 1 - 3N, H is the classical Hamiltonian, Qj is the Cartesian coordinate of the jth mode, and Pj is the conjugated momentum. These equations were numerically solved by the Runge-Kutta method. No symmetry restriction was applied to the calculation of the energy gradients. The time step size was chosen as 0.10 fs, and a total of 10 000 or 20 000 steps were calculated for each dynamics calculation. The drift of the total energy is confirmed to be less than 10-3% throughout all steps in the trajectory. The momentum of the center of mass and the angular momentum were assumed to zero. More details of the direct ab initio MD calculations are described elsewhere.17–19
Figure 1. Chemical structures of flavin-adenine dinucleotide (FADH-), thymine dimer (T)2, and its complex FADH--(T)2.
of this bond. In the case of the radical anion, the C6-C6′ bond of thymine dimer is preferentially broken. The exact mechanism of the fragmentation, however, is not yet clearly understood for each of the dimer radicals. In the present study, the interaction between the fully reduced FADH- and (T)2 has been investigated by means of DFT calculation. Furthermore, the electron capture dynamics of (T)2 have been investigated by means of the direct ab initio molecular dynamics (MD) method in order to elucidate the mechanism of the repair process of thymine dimer caused by a photoenzyme.
3. Results 3.A. Structures of FADH--Thymine Dimer Complex. The optimized structure of the complex composed of FADHand (T)2 is illustrated in Figure 2. The complex is constructed of two hydrogen bonds, N-NH (r1) and CO-HN (r2). The bond distances, r1 and r2, are calculated to be 1.978 and 1.865 Å, respectively. To check the stability of these molecules, harmonic vibrational frequencies of FADH-, (T)2, and the complex are calculated at the B3LYP/6-31G(d,p) level. All frequencies are positive, indicating that these molecules are located on the local minima. The excitation energies of FADH--(T)2 are calculated at the TD-DFT(B3LYP)/6-31G(d,p) level. The results are listed in Table 1. The excitation energies from the ground state to the S1-S5 excited states are calculated to be 3.07, 3.50, 3.55, 3.89, and 4.45 eV, respectively. It is expected that weak and strong bands are appeared to be as S0 f S1 and S0 f S2 transitions, respectively.
2. Computational Methods Static DFT calculations were carried out using the Gaussian 03 program package.16 The structures and electronic states were calculated at the B3LYP/6-31G(d,p) level. The charges of atoms were estimated by means of the natural population analysis (NPA) method. As the damaged DNA system, FADH-, thymine dimer, and its complex composed of FADH- and thymine dimer were chosen. The chemical structures of these molecules are given in Figure 1. We assumed that the group of the FADH(denoted by R) is substituted by a hydrogen atom. To elucidate the mechanism of the repair reaction of thymine dimer, direct ab initio MD calculation was applied to the following reaction scheme:
(T)2 + e- f [(T)2]-* f [(T)2]relaxed The direct ab initio MD calculation was carried out at the B3LYP/6-31G(d) level of theory throughout. The neutral state of the thymine dimer was fully optimized by the energy gradient method. The trajectory for the anionic system was run on the assumption of vertical electron attachment. The electronic state of the system was monitored during the simulation. We confirmed carefully that the electronic state is kept during the reaction. The velocities of atoms at the starting point were set to zero (i.e., momentum vector of each atom is zero). The equations of motion for n atoms in a molecule are given by
Figure 2. Optimized structure of the FADH--(T)2 complex obtained at the B3LYP/6-311G(d) level of theory. Bond lengths are in angstroms.
Thymine Dimer and FADH- Interaction
J. Phys. Chem. B, Vol. 112, No. 24, 2008 7317
TABLE 1: Excitation Energies (Eex in eV), Oscillator Strengths (f in Arbitrary Units), and Configuration State Functions (CSFs) Calculated at the TD-DFT(B3LYP)/6-31G(d,p) Level state S1 S2 S3 S4 S5
CSFs and CI vectors 0.579φ 0.650φ 0.600φ 0.707φ 0.646φ
(HOMO (HOMO (HOMO (HOMO (HOMO
f f f f f
LUMO) - 0.342φ (HOMO f LUMO+1) LUMO+2) + 0.115φ (HOMO f LUMO+1) LUMO+1) + 0.368φ (HOMO f LUMO) LUMO+2) LUMO+3)
The shapes of molecular orbitals are illustrated in Figure 3. HOMO, LUMO+2, and LUMO+4 are composed of a localized orbital distributed on the FADH- molecule. On the other hand, LUMO and LUMO+1 are fully distributed on both (T)2 and FADH-. To elucidate the electronic structures of the excited states of FADH--(T)2, coefficients of configuration state functions (CSFs) are analyzed for each excited state. The results are listed in Table 1. The coefficients of CSFs of φ(HOMO f LUMO) and φ(HOMO f LUMO+1) are calculated to be 0.579 and -0.342 at the first excited state (S1), respectively. Here, φ(HOMO f LUMO) means a wave function (or CSF) whose one electron is excited from HOMO to LUMO. This result suggests that the first excited state is composed mainly by φ(HOMO f LUMO). Therefore, the first excitation band (S0 f S1) can be assigned to a charge-transfer (CT) band from FADH- to (T)2. The second and third excitation bands are attributed to the intramolecular π-π* transition and CT band, respectively. The FADH- and thymine dimer make a strong bound complex with a binding energy of 37.3 kcal/mol. At the ground state, the
Figure 3. Illustrations of molecular orbitals of the FADH--(T)2 complex obtained at the B3LYP/6-31G(d,p) level of theory.
Eex/eV
λmax/nm
f/10-3
3.07 3.50 3.55 3.89 4.45
404 355 350 319 279
1.8 109 0.3 0.0 179
charge of the electron is slightly transferred from FADH- to (T)2. The charge is fully separated by the photoirradiation, and the charge-transfer state expressed by (FADH)δ+-(T)2δ- efficiently takes place. To check the dependency of the computational method, the TD-DFT(BH&HLYP)/6-31G(d) calculation is carried out. The similar results are obtained as the excited states (see the Supporting Information). 3.B. Electron Capture Dynamics of Thymine Dimer. In the previous section, we showed that the electron of FADH- is transferred to thymine dimer by photoirradiation to the complex FADH--(T)2. In this section, the dynamics of the thymine dimer anion, following electron capture of neutral (T)2, is investigated by means of the direct ab initio MD method. Two levels of theory, HF/3-21G(d) and B3LYP/6-31G(d), are used in the dynamics calculations; both levels give the similar qualitative feature about the reaction dynamics (see the Supporting Information). Here, we discuss the reaction dynamics using the result from the B3LYP/6-31G(d) calculation.
Figure 4. Time propagations of (upper) potential energy and (lower) distances (R1 and R2) for the electron capture reaction of thymine dimer. Snapshots for the electron capture reaction of the thymine dimer calculated by direct ab initio MD calculation at the B3LYP/6-31G(d) level. Upper and lower thymine molecules are defined by Thy(I) and Thy(II), respectively.
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TABLE 2: Time Dependence of Bond Population, Spin Population, and Charges on Thymine Molecules (I and II) bond population
charge on Thy
bond spin population
pointa
time/fs
C(5-5′)
C(6-6′)
Thy(I)
Thy(II)
total charge
C(5-5′)
C(6-6′)
a b c d e f
-0.0 0.0 14.0 83.8 113.5 152.4 272.5
0.308 0.184 0.152 0.049 0.038 0.034 -0.020
0.264 0.247 0.267 0.274 0.305 0.298 0.209
0.023 -0.525 -0.546 -0.490 -0.495 -0.576 -0.509
-0.023 -0.475 -0.454 -0.510 -0.505 -0.424 -0.491
0 -1 -1 -1 -1 -1 -1
-0.145 -0.166 -0.230 -0.067 -0.041 0.021
-0.010 -0.011 -0.031 -0.029 -0.027 0.070
a
Points a-e correspond to those in Figure 4.
Figure 5. Reaction model for the repair processes of the electron capture of thymine dimer.
First, the structure of neutral thymine dimer is optimized at the B3LYP/6-31G(d) level. The C5-C5′ and C6-C6′ bond lengths (denoted by R1 and R2, respectively) are calculated to be R1 ) 1.593 Å and R2 ) 1.570 Å, respectively. The result of the direct ab initio MD calculation for the electron capture process of thymine dimer is given in Figure 4. The structure of thymine dimer at time ) 0.0 fs (point a) shows that two C-C bonds are connected to two thymine molecules. The bond distances are R1 ) 1.593 Å and R2 ) 1.570 Å at time zero (i.e., neutral structure). After the electron capture of the thymine dimer, the structure of (T)2- is drastically changed as a function of time, while the potential energy of the system gradually decreases, and it is minimized at 100-150 fs. At time ) 14.0 fs (point b), one of the C-C bonds is elongated: the C5-C5′ bond (R1) is elongated to 1.694 Å, which is 0.101 Å longer than that of time zero. The energy is -4.2 kcal/mol with respect to the zero level of time zero. In contrast, the C6-C6′ bond is not changed by the electron capture (R2 ) 1.582 Å at point b). The bond distance (R1) is elongated to 2.000 Å at time ) 83.8 fs (point c). The other C-C bond distance is still constant (R2 ) 1.594 Å), and the potential energy is -10.4 kcal/mol. At time ) 113.5 fs (point d), the energy is significantly lower than that of zero level (-18.7 kcal/mol), while the energy is
minimized around this region. The bond distances (R1 and R2) are calculated to be 2.674 and 1.599 Å, respectively. The intermediate is formed at this point. At 152.4 fs, the bond distance (R1) is further elongated up to 2.895 Å (point e). The intermediate with a single bond between the thymine rings is formed. At time ) 272.5 fs, the bonds (R1 and R2) are 3.116 and 1.582 Å. The energy rises (-13.3 kcal/mol) because the structure approaches gradually to the transition state (TS) for the C6-C6′ bond cleavage. However, the structure does not reach the transition state within this time scale. Longer simulation is needed to reach the transition state of the reaction, (T)2- f TS f T- + T. The increases of potential energy and R1 are caused by the increase of the torsion angle between the thymine rings. Time profiles of bond distances (R1 and R2) are given in Figure 4 (lower). Only the C5-C5′ bond is gradually elongated as a function of time, whereas the other bond remains up to the formation of the intermediate (time ) 100-150 fs). These results indicate that one of the C-C bonds is rapidly and preferentially broken after the electron capture of thymine dimer. In particular, the C5-C5′ bond is preferentially broken. To elucidate time dependence of the bonding nature between thymine molecules, the bond populations between C-C bonds are monitored as a function of time (Table 2). The calculation is carried out at the B3LYP/6-31G(d) level. Before the electron capture, the bond populations for the C5-C5′ and C6-C6′ bonds of (T)2 are 0.308 and 0.264, respectively, indicating that both C-C bonds are constructed of normal C-C bonds. After the electron capture of the thymine dimer, the bond population of C5-C5′ bond shows a smaller value (0.184), whereas that of the C6-C6′ bond is still constant (0.247), indicating that one of the C-C bonds (i.e., C5-C5′ bond) becomes weaker after the electron capture. The spin population in the C5-C5′ bond shows a negative value (-0.145), suggesting that the bonding nature of the C5-C5′ bond is changed to antibonding by electron capture. The bond population decreases suddenly after 14.0 fs. The C5-C5′ bond disappears at time ) 83.8 fs (bond population is close to zero). The excess electron is delocalized on both thymine rings at the final state of the reaction. These results suggest that the C-C bond cleaves and the intermediate is generated efficiently after the electron capture, while spin densities and charge are localized on one of the thymine rings. 4. Discussion 4.A. Model of the Repair Reaction of Thymine Dimer. The present calculations suggested that electron transfer occurs from FADH- to thymine dimer by photoirradiation to the complex. Once electron capture of thymine dimer takes place, one of the C-C bonds cleaves and an intermediate complex is formed. The C5-C5′ bond is preferentially broken in the initial stage of the reaction. On the basis of the present results, we propose here a model for the repair reaction of FADH--thymine dimer. The model is
Thymine Dimer and FADH- Interaction schematically illustrated in Figure 5. When the FADH--thymine dimer system is irradiated by UV light, the electron transfer occurs from FADH- to thymine dimer. The C-C bond of the thymine dimer anion is efficiently broken within 60-100 fs, and the intermediate is formed. After thermal activation, thymine dimer is fully separated to both neutral thymine and thymine anion radical. The excess electron is localized on one thymine molecule. The electron would be transferred from thymine anion to FADH radical by a tunneling mechanism. Finally, thymine dimer is converted to two normal thymine bases. 4.B. Comparison With Previous Studies. Kao et al. observed directly thymine dimer repair in DNA by photolyase using femtosecond synchronization of the enzymatic dynamics with the repair function.6 They observed direct electron transfer from the excited flavin cofactor to the thymine dimer and back electron transfer from the repaired thymine. The present calculation supports strongly their experimental finding. From the theoretical point of view, the structural changes of thymine dimer following hole or electron capture have been predicted by several groups.14,15,23 Aida et al. investigated structures and electronic states of thymine dimer radical cation and showed that the C6-C6′ bond is preferentially elongated and broken after the hole capture of thymine dimer. Durbeej and Eriksson investigated the radical anion of thymine dimer using DFT calculations. An electron attachment to thymine dimer preferentially cleaves the C6-C6′ bond. The present calculation strongly confirms their theoretical prediction. 4.C. Additional Comments. In the present study, several approximations were introduced in the calculation of the potential energy surface and the reaction dynamics. In particular, we assumed the B3LYP/6-31G(d) multidimensional potential energy surface in the dynamics calculations because a large number of steps needed to obtain the reaction dynamics. In previous papers, we investigated ionization and electron capture dynamics of benzene-H2O, formanilide-H2O, and (H2O)n using the HF/3-21G(d) and B3LYP/6-31G(d) levels of theory.20–22 The results obtained at these levels of theory would give a reasonable description of the ionization and electron capture dynamics of these complexes. Therefore, the level of theory used in the present calculation would be adequate to discuss qualitatively the electron capture process of the thymine dimer system. However, more accurate wave functions may provide deeper insight in the dynamics. Despite the several assumptions introduced here, the results enable us to obtain valuable information on the mechanism of the repair reaction of thymine dimer. Acknowledgment. The author (H.T.) is indebted to the Computer Center at the Institute for Molecular Science (IMS) for the use of the computing facilities. H.T. also acknowledge a partial support from a Grant-in-Aid for Scientific Research (C) from the Japan Society for the Promotion of Science (JSPS).
J. Phys. Chem. B, Vol. 112, No. 24, 2008 7319 Supporting Information Available: Excitation energies, harmonic vibrational frequencies, and result of dynamics calculation at the HF/3-21G(d) level. This material is available free of charge via the Internet at http://pubs.acs.org. References and Notes (1) Brueckner, F.; Hennecke, U.; Carell, T.; Cramer, P. Science 2007, 315, 859. (2) Crespo-Hernandez, C. E.; Cohen, B.; Kohler, B. Nature 2005, 436, 1141. (3) Mees, A.; Klar, T.; Gnau, P.; Hennecke, U.; Eker, A. P. M.; Carell, T.; Essen, L.-O. Science 2004, 306, 1789–1793. (4) Sancar, A. Chem. ReV. 2003, 103, 2203–2237. (5) Park, H. W.; Kim, S. T.; Sancar, A.; Deisenhofer, J. Science 1995, 268, 1866–1872. (6) Kao, Y.-T.; Saxena, C.; Wang, L.; Sancar, A.; Zhong, D. Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 16128. (7) (a) Pezeshk, A.; Podmore, I. D.; Heelis, P. F.; Symons, M. C. R. J. Phys. Chem. 1996, 100, 19714. (b) Podmore, I. D.; Heelis, P. F.; Symons, M. C. R.; Pezeshk, A. J. Chem. Soc., Chem. Commun. 1994, 1005. (8) Schreier, W. J.; Schrader, T. E.; Koller, F. O.; Gilch, P.; CrespoHernandez, C. E.; Swaminathan, V. N.; Carell, T.; Zinth, W.; Kohler, B. Science 2007, 315, 625. (9) Durbeej, B.; Eriksson, L. A. J. Photochem. Photobiol., A 2002, 152, 95. (10) Boggio-Pasqua, M.; Groenhof, G.; Schaefer, L. V.; Grubmuller, H.; Robb, M. A. J. Am. Chem. Soc. 2007, 129, 10996–10997. (11) Burdi, D.; Begley, T. P. J. Am. Chem. Soc. 1991, 113, 7768. (12) Diogo, H. P.; Dias, A. R.; Dhalla, A.; Minas da Piedade, M. E.; Begley, T. P. J. Org. Chem. 1991, 56, 7340. (13) Austin, R.; McMordie, S.; Begley, T. P. J. Am. Chem. Soc. 1992, 114, 1886. (14) (a) Aida, M.; Inoue, F.; Kaneko, M.; Dupuis, M. J. Am. Chem. Soc. 1997, 119, 12274. (b) Aida, M.; Kaneko, M.; Dupuis, M. Int. J. Quantum Chem. 1996, 57, 949. (15) Durbeej, B.; Eriksson, L. A. J. Am. Chem. Soc. 2000, 122, 10126. (16) Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Montgomery, J. A., Jr.; Vreven, T.; Kudin, K. N.; Burant, J. C.; Millam, J. M.; Iyengar, S. S.; Tomasi, J.; Barone, V.; Mennucci, B.; Cossi, M.; Scalmani, G.; Rega, N.; Petersson, G. A.; Nakatsuji, H.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Klene, M.; Li, X.; Knox, J. E.; Hratchian, H. P.; Cross, J. B.; Bakken, V.; Adamo, C.; Jaramillo, J.; Gomperts, R.; Stratmann, R. E.; Yazyev, O.; Austin, A. J.; Cammi, R.; Pomelli, C.; Ochterski, J. W.; Ayala, P. Y.; Morokuma, K.; Voth, G. A.; Salvador, P.; Dannenberg, J. J.; Zakrzewski, V. G.; Dapprich,S.; Daniels, A. D.; Strain, M. C.; Farkas, O.; Malick, D. K.; Rabuck, A. D.; Raghavachari, K.; Foresman, J. B.; Ortiz, J. V.; Cui, Q.; Baboul, A. G.; Clifford, S.; Cioslowski, J.; Stefanov, B. B.; Liu, G.; Liashenko, A.; Piskorz, P.; Komaromi, I.; Martin, R. L.; Fox, D. J.; Keith, T.; Al-Laham, M. A.; Peng, C. Y.; Nanayakkara, A.; Challacombe, M.; Gill, P. M. W.; Johnson, B.; Chen, W.; Wong, M. W.; Gonzalez, C.; Pople, J. A. Gaussian 03, revision B.04; Gaussian, Inc.: Pittsburgh, PA, 2003. (17) Tachikawa, H.; Abe, S. J. Chem. Phys. 2007, 126, 194310. (18) Tachikawa, H. J. Chem. Phys. 2006, 125, 144307. (19) Tachikawa, H. J. Chem. Phys. 2006, 125, 133119. (20) Tachikawa, H. J. Phys. Chem. A 2006, 110, 153. (21) Tachikawa, H. J. Phys. Chem. A 2004, 108, 7853. (22) Tachikawa, H.; Igarashi, M.; Ishibashi, T. J. Phys. Chem. A 2003, 107, 7505. (23) Borg, O. A.; Eriksson, L. A.; Durbeej, B. J. Phys. Chem. A 2007, 111, 2351.
JP801564T
