J. Phys. Chem. 1992, 96, 661-668
assumes that this difference would also pertain at the CCSD level, the TZ2P/DZP CCSD dipole moment may be estimated to be 3.81 - 0.17 = 3.64 D. The latter estimate is now is acceptable agreement with experiment, 3.51 f 0.02 D. Such agreement betwen theoretical and experimental dipole moments is consistent with our conclusion that the DZd CCSD equilibrium geometry is reliable. Concluding Remarks An earlier theoretical study1’of diketene and its isomers yielded poor agreement with experiment for the molecular structure of diketene, without being able to say whether theory or experiment was likely to be the more reliable. Here the level of theory has been raised significantly, and the case presented that the best theoretical structures are significantly superior to experiment. Much of our analysis has focused on the C 4 and C-O (adjacent to C=C) distances determined by X-ray crystallogra~ h y . ~A~ variety ’ of direct and indirect evidence is presented to show that these experimental bond distances are unrealistically long. There appear to be less serious problems associated with the molecular structure determined experimentally from electron diffraction! Most notably among the problems, the two C-O distances in the electron diffraction structure are both 1.41 A. At every level of theory the C-O distance adjacent to the C = C double bond is longer, by 0.031 A (DZd SCF and DZP SCF), 0.028 A (TZ2P/DZP SCF), 0.025 A (DZd CISD), and 0.023 A (DZd CCSD). We estimate that the true difference in C-O
661
equilibrium bond distances is -0.024 A. Similarly, the two C-C distances in the electron diffraction structure are both 1.52 k while theory gives the distance adjacent to C - 0 as longer by 0.012 A (DZd and DZP SCF), 0.014 A (TZ2P/DZP SCF), 0.015 A (DZd CISD), and 0.018 A (DZd CCSD). There certainly is a difference in the diketene C-C bond distances, and we estimate it as -0.017 A. Final estimates of the diketene bond distances may be made by observing that the DZd CISD and CCSD rotational constants tightly bracket the experimental microwaves results. We therefore propose the following: ro(C=C) adj C=€ adj C
--
1.326 A
ro(C-0)
4 ro(C-C)
adj C - C
ro(C-C)
adj C=O
ro(C-C)
ro(C=O)
-
-
1.410 A 1.386 A 1.515 A 1,531 A
1.190 A
Needless to say, new experimental studies of the molecular structure of diketene are called for.
Acknowledgment. This research was supported by the National Science Foundation, Grant CHE-87 18469.
US.
Registry NO. 1, 674-82-8.
Ab Initio Molecular Orbital Calculations of DNA Bases and Their Radical Ions in Various Protonation States: Evidence for Proton Transfer in GC Base Pair Radical Anions Amy-Wile Colson,t Brent Besler,*David M. Close,l and Michael D. Sevilla**+ Department of Chemistry, Oakland University, Rochester, Michigan 48309; Department of Chemistry, Wayne State University, Detroit, Michigan 48202; and Department of Physics, East Tennessee State University, Johnson City, Tennessee 37614 (Received: July 31, 1991)
Ab initio molecular orbital calculations of various protonation states of DNA base and DNA base radical ions were performed to aid our understanding of primary radiation processes in DNA. Each of the structures was optimized at the STO-3G and 3-21G levels of theory, and single point calculations were performed at the 6-31G*//3-21G and 6-31+G(d)//3-21G levels. Each of the protonation states important to proton-transfer reactions in base pair radical ions found in irradiated DNA was considered. Calculations for three protonation states for the cytosine r e d u d radical were performed and the most stable is found to be the N-3 ring-protonated species. Calculations for the vertical ionization energies of the individual DNA bases yielded the following order T > C > A > G with the same order found for the adiabatic electron affinities of the bases. The best fit to experiment was found with Koopmans’ theorem ionization potentials. The energy for proton transfer in the GC and AT base pair radical cation and radical anions were estimated froni the energies of the individual species. All proton transfers were found to be energetically unfavorable except for the GC anion radical which is favored by 13 kcal. INDO calculations for ions of stacked four base DNA model system AT/GC predict the site of electron trapping in DNA model system is thymine, and the hole is found on guanine as predicted from ab initio energies for the individual bases. Both ab initio and INDO results for the AT/GC anion predict the site of the anion shifts from thymine to cytosine on the transfer of a proton from rmanine to the cytosine anion. These results lead to a revised model for ion radical localization after irradiation
Lntroduction Considerable interest has arisen of late in the primary radicals formed in DNA as a result of several reports that the initial ion radical distribution may be dependent on proton-transfer reactions Oakland University. ‘Wayne State UniGnity. 1 East Tennessee State University.
0022-3654/92/2096-661$03.00/0
between base pairs.lT2 Steenken first suggested that protontransfer reactions may be important in the initial stabilization of DNA ion radicah2 Although thymine was long thought to be the favored site of electron addition?” recently it has become clear (1) Sevilla, M. D.; Becker, D.; Yan, M.; Summerfield, S. R. J . Phys. Chem. 1991, 95, 3410-3415. (2) (a) Steenken, S. Chem. Rev. 1989,89,503. (b) Steenken, S. Abstracts, 38th Meeting of the Radiat. Res. Soc., 1990; p 55.
0 1992 American Chemical Society
662 The Journal of Physical Chemistry, Vol. 96, No. 2, 1992
that the cytosine anion is predominant at low temperatures in irradiated hydrated double-strand DNA.1-7 From these reports, the following model has arisen.l The initial anion radical distribution is a function of the electron affinity whereas the cation radical distribution is initially a function of ionization potential of the bases. Subsequent proton-transfer reactions between base pairs can alter the relative stabilities of the radical sites.2 Previous experimental work has shown that the pyrimidines, thymine, and cytosine have greater electron affinities than the purines, adenine, and guanine and serve as the sites of initial localization of the electron. According to this model, proton transfer from G to 'Cgradually shifts the electron to cytosine which accounts for the dominance of the cytosine anion in the DNA spectrum. Such proton-transfer reactions are not at present thought to shift the site of the cation. In this work we have performed a number of high level ab initio molecular orbital calculations for DNA bases and their ion radicals in various protonation states. Although several ab initio calculations for the DNA bases in various protonation states have been reported,E-18no ab initio calculations of the ion radicals in various protonation stam have been reported. Our calculations of energies predict the most stable gas-phase protonation states, the electron affinities and ionization potentials, and base pair proton-transfer energies. These calculations along with INDO calculations for a stacked four-base system, AT/GC, provide support and allow for a further elaboration for the current model for radiation damage to DNA.
Method of Calculation Calculations were performed using GAUSSIAN 9oI9 and DISCO~O sets of programs. These programs search for the optimum geometry using the criteria of minimum energy. Checks were performed for several molecules to ensure that the results found for each program were identical. The input data consist of a set of bond distances, bond angles and dihedral angles arranged in a Z matrix. Calculations at the STO-3GZ1and 3-21GZ2levels
(3) (a) Grhlund, A.; Ehrenberg, A.; Rupprecht, A.; StrBm, G. Biochim. Biophys. Acta 1971,254, 172. (b) Grlslund, A.; Ehrenberg, A,; Rupprecht, A. Int. J . Radiat. Biol. 1977, 31, 145. (4) Hiittermann, J.; Voit, K.; Oloff, H.; Kohnlein, W.; Grlslund, A,; Rupprecht, A. Faraday Discuss. Chem. SOC.1984, No. 78, 135. (5) Gregoli, S.; Olast, M.; Bertinchamps, A . Radiat. Res. 1982, 89, 238. (6) Boon, P. J.; Cullis, P. M.; Symons, M. C. R. J . Chem. SOC.,Perkin Trans. 2 1984, 1393. (7) Bernhard, W. A. J . Phys. Chem. 1989, 93, 2187. (8) Kwiatkowski, J. S.;Person, W. B.; Szczepaniak, K.; Szczesniak, M.; Acta Biochim. Pol, 1987, 34, 165. (9) Cieplak, P.; Bash, P.; Singh, U. C.; Kollman, P. A . J. Am. Chem. Soc. 1987, 109, 6283. (IO) Scanlan, M. J.; Hillier, I. H. J . Chem. Soc., Chem. Commun. 1984, 1904. (1 1) Latajka, Z.; Person, W. B.; Morokuma, K. THEOCHEM 1986,135, 253. (12) Leszczyiiski, J. Chem. Phys. Lett. 1990, 174, 347. (13) Sabio, M.; Topiol, S.; Lumma, W. C., Jr. J . Phys. Chem. 1990, 94, 1366. (14) Kwiatkowski, J. S.; Leszczyiiski, J. THEOCHEM 1990, 208, 35. (15) Mezey, P. G.; Ladik, J. J. Theor. Chim. Acta (Berlin) 1979,52, 129. (16) Aida, M.; Yamane, K.; Nagata, C. Mutat. Res. 1986, 173, 49. (17) Gould, I. R.; Hillier, 1. H. Chem. Phys. Lett. 1989, 161, 185. (18) Scanlan, M. J.; Hillier, I. H. J . Am. Chem. SOC.1984, 106, 3737. (19) GAUSSIAN 90, Revision H; M. J. Frisch, M. Head-Gordon, G. W. Trucks, J. B. Foresman, H. B. Schlegel, K. Raghavachari, M. Robb, J. S. Binkley, C. Gonzalez, D. J. Defrees, D. J. Fox, R. A. Whiteside, R. Seeger, C. F. Melius, J. Baker, R. L. Martin, L. R. Kahn, J. J. P. Stewart, S. Topiol, J. A . Pople; Gaussian, Inc.: Pittsburgh, PA, 1990. (20) (a) Almlof, J.; Faegri, K. J. R.; Korsell, K. J . Comput. Chem. 1982, 3, 385. (b) Saebo, S.; Almlof, J. Chem. Phys. Lett. 1987, 154, 521. (21) Hehre, W. J.; Stewart, R. F.; Pople, J. A. J. Chem. Phys. 1969, 51, 2657. (22) Binkley, J. S.; Pople, J. A.; Hehre, W. J. J . Am. Chem. SOC.1980, 120, 939.
Colson et al. were carried out with geometry optimization. Criteria for geometry optimization and SCF convergence were 10-4 hartree/bohr and hartree, respectively. The starting geometries for the STO-3G calculations were based on the optimized STO-3G structures of neutral DNA bases.23 The STO-3G optimized parameters were generally employed as the initial starting geometries for 3-21G calculations. They were followed by single point calculations in the 6-31G*24and 6-31+G(d)2S bases sets using the optimized geometries obtained from the 3-21G basis set. In addition, base structures were assumed to be planar except for the methyl group of thymine. The optimal conformations of the methyl group of thymine and the protonated amino group of cytosine were optimized for all parameters, Le., bond distances, bond angles, and dihedral angles. Calculations were performed on Dec 5000/200, VAX-VMS 3540, and Cray XMP-14 computers. Spin unrestricted Hartree-Fock type (UHF) optimizations for DNA radical species were first achieved at STO-3G using the geometries of Del Bene23as starting geometries. After finding large contaminations from higher order spin states in our calculations ( ( S 2 )>> 0.75), spin-restricted open-shell Hartree-Fock (ROHF) optimizations26were performed for all calculations reported in this work.
Results and Discussion Ab initio molecular orbital calculations were performed for five classes of DNA species: (I) natural DNA bases; (11) anionic radical DNA bases; (111) cationic radical DNA bases; (IV) neutral DNA base radicals: protonated/deprotonated forms of I1 and 111; (V) nonradical DNA base ions: protonated/deprotonated forms of I. The numbering schemes for these structures are shown in Figure 1. Our purposes in calculations for classes I-V are several. First, we wish to obtain optimized geometries and energies of various species important to the understanding of radiation damage to DNA (groups I-V). From these values, we estimate the proton-transfer energies in base pair anions (I, 11) and cations (I, 111) as well as the effect of proton transfer on the site of localization in stacked double base pair (GC/AT) ion radicals (I-V), Second, the calculation of ionization potentials and electron affinities is also of interest (groups 1-111) as these play a role in the initial localization of charge on irradiated DNA. In our calculations, the zero-point vibrational energies were not taken into account as differences in zero-point vibrational energies for tautomeric species are quite small (
