J. Phys. Chem. 1995,99, 13033-13037
13033
Ab Initio Molecular Orbital Calculations of Radicals Formed by H and *OH Addition to the DNA Bases: Electron Affinities and Ionization Potentials Anny-Odile Colson and Michael D. Sevilla* Chemistry Department, Oakland University, Rochester, Michigan 48309 Received: April 27, 1995; In Final Form: June 19, 1 9 9 9
Ab initio molecular orbital calculations of the ionization potentials (IP's) and electron affinities (EA's) of DNA base radicals formed by addition of H' or OH' to DNA bases are presented in this work. IP's and EA's are obtained by calculating the energies of the LUMO and HOMO (Koopmans' values) of the cationic and anionic states, respectively. Scaling of the theoretical values to experimentally known ionization potentials and electron affinities of other small radical compounds leads to predicted trends in IP's and EA's of the DNA base adducts. These trends are shown to be in good agreement with experimental redox trends and aid our understanding of possible electron transfer processes. The present results indicate the OH' and H' adducts of the pyrimidines at C6 are most oxidizing, while the H' adduct of cytosine at N3 is most reducing. The calculated trend in electron affinities in conjunction with experimental observations results in the prediction that only a fraction of the base adducts will be reduced via electron transfer processes from thiols. All five sugar radicals have nearly equal electron affinities; however, their ionization potentials substantially differ. Delocalization effects which result in less electron repulsion in the anionic state are shown to account for differences in EA and IP scales. Conformational distortion of the purine bases upon adduct formation at the C4 and C5 sites is shown to be significant.
Introduction Among the radiation-induced DNA damages, the hydroxyl and hydrogen adduct DNA base radicals constitute an interesting subset of species, since they can result from both the direct and indirect effects. The direct effect which corresponds to ionization of the DNA itself leads to the formation of primary radical ions that can undergo rapid irreversible hydroxylation (cation radicals) or protonation (anion radicals). On the other hand, the indirect effect, which corresponds to energy deposition in the water phase surrounding the DNA, results in the formation of 'OH, H', and 'e-(aq). All three species can attack the neutral DNA bases and form the hydroxyl and hydrogen adducts of the bases. Over recent years, the base adducts resulting from both effects have been observed under various experimental conditions and the different sites of OH addition to the base moieties have been identified. Extensive reviews on these reactions have recently appeared.'-4 The site of OH radical addition to the DNA bases has been shown to strongly influence the redox properties of the resulting and it is believed that these properties are critical in determining the ability of the base hydroxyl radical adducts to abstract hydrogen atoms from the sugar moiety of the DNA backbone and subsequently induce strand breaks. Hydroxyl radicals react predominantly by addition to the C51 C6 double bond of cytosine and thymine, with a pronounced preference for C5,6,7giving rise to the formation of the 6-yl and 5-yl radicals. Characterization of the sites of OH' addition to guanine and adenine is less straightforward mostly due to the fact that the purine OH adducts undergo unimolecular transformations which make their identification more difficult. On the basis of charge density distribution in purines, the electron-rich C4 and C5 centers are likely sites for attack of the electrophilic OH radical. Steenken et al. have shown the major sites of OH addition in deoxyadenosine are C4 and C8; the C4 adduct subsequently undergoes dehydration. The C5 @
Abstract published in Advance ACS Abstracts, August 1, 1995.
0022-365419512099-13033$09.0010
adduct, although less abundant, has also been identified as a product of OH addition to N6,M-dimethyladenosine.* In its reaction with DNA, it has been shown that the H atom adds to the double bond of the bases in preference to abstraction of a hydrogen from the sugar m ~ i e t y . ~In . ' ~addition, because of the electrophilic character of the H atom, the preferences for attack on the DNA bases are very similar to those observed in the case of OH' attack. In this regard, the C5 and C6 hydrogen adducts of thymine have been observed in a 3:2 ratio in H atom addition reactions." It is well established that the electron adducts of the DNA bases resulting from the direct effect react further, typically by proton addition to the anion radical. Hence, direct (electron addition and protonation) and indirect (H atom addition) reduction of the neutral DNA bases can lead to the same radicals. In adenosine, protonation has been shown to occur at C2 and C8,'* and the radical anion of guanosine also results in the C8 adduct. Previous theoretical studies have focused on calculating hyperfine splitting constants and spin densities for several of these radicals,I3-l5 while recent FOCI calculations resulted in the electronic spectra of the H and OH adducts of uracil.I6 Our previous theoretical efforts have concentrated on the ionization potentials and electron affinities of the DNA component^.'^-^^ In this work, we employ ab initio molecular orbital theory combined with scaling to known experimental values to determine the electron affinities and ionization potentials of hydrogen and hydroxyl adducts of the DNA bases. Electron affinities predicted in this work do not include dipole bound states found in the gas phase for molecules with large dipole moments,24as only valence bound and virtual states are applicable to aqueous phase systems of interest to us.21*22 Further we note that OH- addition to DNA radical cations and H+ addition to DNA radical anions would result in many of the same base radical intermediates as OH' and H' addition.' In this work the relative values of electron affinities and ionization potentials are shown to relate to the relative redox properties of the various species. These results will aid our understanding 0 1995 American Chemical Society
Colson and Sevilla
13034 J. Phys. Chem., Vol. 99, No. 34, I995 of radioprotective and repair mechanisms of the radiationinduced DNA damaged bases through electron transfer reactions from thiols.
0
P
9
OH
Method of Calculation The ROHF/6-31G* polarization basis set25,27 is used to fully geometry optimize the OH and H neutral radical adducts of the bases presented in Figure 1 and to calculate their respective vertical electron affinities and ionization potentials. The Gaussian 9228 set of programs is employed on CrayC90 and IBM RS 6000 computers. The (x, y , z ) coordinates obtained at the ROHF/6-3lG* level for the geometry-optimized structures presented in Figure 1 are available in the supporting information.
Results and Discussion
1. Model Radicals. The electron affinities and ionization potentials of radicals are a measure of addition of one electron (EA) and removal of one electron (IP) from the same molecular orbital as illustrated below:
: t
- t t Although, in a recent work,22 we showed that accurate estimates of electron affinities of the DNA bases obtained at both the 6-31G* and levels could be calculated from scaled Koopmans’ values to experiment, Koopmans’ theorem does not apply to singly occupied states (radicals) and hence Koopmans’ values cannot be calculated for the radical adducts. However, the Koopmans’ ionization potentials (which are simply the energy of the HOMO) of the anionic states in the geometry of the neutral radical species are identical to the vertical electron affinities of the radicals. Likewise, the Koopmans’ estimates of the vertical ionization potentials of radicals can be calculated from the energy of the LUMO of the nonradical cations in the geometry of the radicals. These states are schematically represented below:
The electron affinity and ionization potential differ, since the electron repulsion between electrons in the anionic state (for electron affinities) is substantial and varies depending on the extent of electron delocalization in that state. For example, the difference (A) between the experimentally known ionization potentials and electron affinities of several model radicals (Table 1) varies between 6 and 11 eV. These values are a measure of the additional electron repulsion felt by the second electron over the first in the HOMO. As can be seen in Table 1, increased delocalization results in a smaller A. As previously shown,22scaling to known experimental values is needed to yield reliable estimates of gas phase electron affinities of the DNA bases. Eleven radical compounds (Table 1) for which experimental electron affinities are known were geometry optimized at the ROHF/6-31G* level ((x, y , z ) coordinates are available in the supporting information). Singlepoint calculations were performed at the ROHF/6-31G* and ROHF/D95v//6-31G* levels on the ionic states of the model
I
H .CISOH
H .C(5lOH
H sC(6IH
H .C(SIH
H eC13)H
Figure 1. Structures and nomenclature of DNA base radical intermediates resulting from OH’ and H’ attack. These structures are geometry optimized at the 6-31G*level in this work.
radicals. These compounds include di- and triatomic species which encompass a large range of electron affinities, as well as ring systems with and without heteroatoms which best resemble the DNA bases. The HOMO energies of these states are reported in Table 1. The experimental vs theoretical fits of HOMO energies calculated at the ROHF/6-31G* and ROHF/ D95v//6-31G* levels are in close agreement with near identical R2 values, as shown in Figure 2. Vertical ionization potentials of six of the model radical compounds employed above for which experimental ionization potentials are available (.C7H7, *C3H5,*C5H5,‘CH3, ‘NH2, ‘OH) are obtained by calculating the LUMO energy of the cation in the geometry of the radical parent. These calculated energies are fitted to the experimentally known ionization potentials and result in the relation IP(theory) = -4.885 (1.344)IP(expt), with R2 = 0.97. Our calculations sumarized in Table 1 show that the unscaled theoretical values, raw values, of A compare reasonably well with experimental values (0.8 eV average deviation). The A values calculated after scaling and presented in Table 1 show an improved fit, as expected (0.3 eV average deviation). The good fit found here after scaling for IP, EA, and A suggests that the EA and IP scales developed for DNA base radicals, see below, should also be reasonable estimates of experimental values. 2. DNA Bases. 2.1. Electron AfFnities. In this work, we have performed single-point calculations on the DNA base adducts in their anionic states to obtain the HOMO energies. These theoretical energies were then fitted to the 6-31G* relation, EA(theory) = -1.339 (1.395)EA(expt), and the resulting estimated electron affinities of the radicals (or ionization potentials of the anions) are shown in Figure 3, which presents estimates of energies for one-electron reduction of the DNA base intermediates in the gas phase. Single-point calculations performed at the ROHF/6-31G* level on the five ROHF/3-21G geometry-optimizeddeoxyribose radicals and their anionic states obtained in a short DNA fragment ( l’-amino-2’-deoxyribose 5’,3’-diphosphate) presented in an earlier work30 also lead to estimates of electron affinities of the sugar radical moiety. Among the radicals investigated, it is clear that the H’and OH’ adducts at C6 of the pyrimidines are the most oxidizing species. It is interesting to note that the electron affinities of the sugar radicals all lie within 0.1 eV toward the middle of the scale shown in Figure 3, which
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Radicals Formed by H' and *OH Addition to the DNA Bases
J. Phys. Chem., Vol. 99,No. 34, I995 13035
TABLE 1: Experimental Vertical Electron Amnities and Ionization Potentials and Calculated Energies of HOMO's and LUMO's of Test Radicals in their Anionic and Cationic States, Respectively (eV) ROHF16-3 1G* ROHF/D95v//6-31G* anion (-) HOMOb anion (-) HOMOb
expt EA"
- 1.57 -0.54 -0.16 0.02 1.47 1.03 0.76 1.01 1.57 1.09 3.72
0.08 f 0.03 0.362 f 0.019 0.771 k 0.005 0.912 f 0.006 1.570 f 0.022 1.70 f 0.03 1.804 f 0.007 1.8277 i 0.00002 1.861 f 0.004 2.39 f 0.13 3.3 & 0.2
'CH, 'C3H5g 'NH2 'C7H7h CH,O' CrjHsNH'' 'C5H5 'OH CH# C4H4Nll CH3COO'
-0.93 -0.16 0.25 0.99 1.67 1.32 1.21 1.58
expt I F
ROHF/6-3 1G* cation (-) LUMOb Adexpt Ae calc raw Afcalc scal
9.9 8.2 11.2 7.20 i 0.02" 8.6 12.90
7.70 6.03 9.95 5.27
9.8 7.8 10.4 6.3
9.3 6.6 10.1 5.3
9.5 7.6 10.2 6.6
6.75 12.95
6.8 11.1
6.0 11.9
7.2 11.6
1.69 4.1 1
Handbook of Chemistry and Physics, 74th ed.; Lide, D. R., Ed.; CRC Press: Boca Raton, FL, 1993-1994. The values listed are the negative of the calculated HOMO's and LUMO's. Chanon, M.; Rajzman, M.; Chanon, F. Tetrahedron 1990,46,6193. A(expt) is the difference between the experimental values of IP and EA of a radical. It gives a measure of the additional electron repulsion felt by the second electron (anionic state) over the first (neutral radical) in the HOMO. e A(ca1c raw) is simply the magnitude of the difference between the cation LUMO and anion HOMO. fA(ca1c scal) is the magnitude of the difference between the scaled values of the cation LUMO (IP) and anion HOMO (EA). See text. 8 Allyl radical. Benzyl radical. Anilinyl radical. Pyrrolyl radical. ROHFD95v
-L
I
0
1
3
2
4
Experimental Electron Affinities (eV)
Figure 2. Fit of the calculated electron affinities of the various radicals presented in Table 1 to the experimental electron affinities. The HOMO energies of the anionic state (Koopmans' EA) are calculated with ROHF/6-3 lG* and ROHFID95vN6-3lG* basis sets. Assuming the linear relationship EA(theory) = a b[EA(experiment)], the fit gives a = -1.339 and -0.781, b = 1.395 and 1.328, and R2 = 0.90 and 0.91 for the 2 basis sets used respectively.
+
therefore suggests all five radicals have roughly equal probability of being reduced and hence being healed via electron transfer. The trends presented here can also be used in predicting reduction of the damaged bases through electron transfer processes from thiols. Pulse radiolysis studies3' have shown RS- can reduce 'G(4)OH in dGMP and dG cation radicals via electron transfer reaction, while 'G(5)OH and 'G(8)OH do not react with RS-. In addition, recent ESR investigation^^^ performed on y-irradiated frozen solutions of TMP, dGMP, dAMP, and dCMP show cysteamine does not reduce either 'G(8)H or 'A(8)H, while, although not clearly observed, it likely reduces %(6)H. These results combined with the trend depicted in Figure 3 lead us to conjecture on the reduction capability of cysteamine toward the damaged bases investigatedin this work. Our results combined with the experimental observation suggest the critical range of electron affinities which will determine whether or not electron transfer from cysteamine can occur is in the 1.3-1.6 eV region. Hence, according to Figure 3, cysteamine will likely donate an electron to species whose electron affinities are larger than ca. 1.4 eV, that is 'C(6)OH, 'T(6)OH, 'C(6)H, T(6)H, 'A(4)OH, 'A(8)OH, and 'G(4)OH, the process involving the latter species having been experimentally
-0.5
-1
c
*C(3)H
L
Figure 3. Electron affinities and ionization potentials of the DNA base OH' and H' adduct radicals calculated by scaling Koopmans' EA's (anion HOMO's) and Koopmans' I P S (cation LUMO's) to experiment. These scales represent the estimated vertical EA's and IPS. Double headings on the IP scale correspond to species with equal ionization potentiais. Radicals with electron affinities above 1.4 eV are predicted to undergo reduction by thiols.
shownto while no electron transfer is predicted to occur with any of the species whose electron affinities lie below that of 'A(8)H. This prediction is confumed by experimental results in the case of 'A(8)H, 'G(8)OH, 'G(5)OH, and *G(8)H.31332 Figure 3 clearly shows 'C(3)H will not be reduced by cysteamine, while 'C(6)H most likely will. Since 5,6-dihydrocytosine has been experimentally observed33 and results from the pyrimidine protonated anion radical, our results as well as prior experiment^^^ suggest 'C(3)H converts to 'C(6)H before further reduction. As stated earlier, the experimentally observed preferred sites of 'OH attack on the pyrimidines are the C5 and C6 carbon
13036 J. Phys. Chem., Vol. 99, No. 34, I995 A
Localized
B
+e-
Delocalized
Figure 4. Electron repulsion effects accounting for differences in ranking in electron affinity and ionization potential scales. Localized radicals (A) have stronger electron repulsion than delocalized radicals (B) on addition of an extra electron.
atoms. In thymine, it has been shown that some abstraction could occur at the methyl group? resulting in the formation of UCH2' (Figure 1). This allyl like radical appears to be neither strongly reducing nor strongly oxidizing, as experimentally shown2and theoretically predicted (Figure 3). The present work suggests this damaged entity will not likely be repaired via electron transfer from thiols. 2.2. Ionization Potentials. Vertical ionization potentials of the DNA radical intermediates presented in Figure 1 are obtained by scaling calculated values of the LUMO energy of the cation in the geometry of the radical parent to experiment (IP(theory) = -4.885 (1.344)IP(expt)). The resulting estimates of the vertical ionization potentials of the DNA adducts obtained in their cationic states are shown in Figure 3. The scale of ionization potentials combined with that of electron affinities in Figure 3 can be employed in predicting possible electron transfer reactions which will subsequently heal the damaged base. Indeed, radicals with small ionization potentials such as 'C(3)H will easily reduce species such as 'C(6)OH, which has a high electron affinity. This observation might be of importance particularly for 'G(8)OH, whose oxidation by 'T(6)H or 'C(6)OH would likely result in the formation of 8-oxoguanine,while its reduction by 'C(3)H would lead to the ring-opened structure Fapy-G, for which formation rate constants have been ~ a l c u l a t e d .Furthermore, ~~ it appears that 'UCH2, whose electron affinity and ionization potential lie in the middle of the scales shown in Figure 3, may recombine. Recent ESR work performed in our laboratory suggests 'UCH2 will likely attack the thymine ring at C6 to form a dimer radical which can be repaired through H atom transfer reaction from thiols.32 An interesting feature of the properties of the radical intermediates presented in Figure 3 is that the overall trends in electron affinities and ionization potentials are similar (note the same species are at the high and low levels of the scales). However, there are some interesting differences that are best explained on the basis of electron delocalizationwhich reduces electron repulsion effects. For instance, all five sugar radicals have nearly identical electron affinities, while their ionization potentials differ by as much as ca. 1 eV. The C1' radical which has the lowest ionization potential among all five sugar radicals can delocalize its extra electron in the anionic state somewhat more than the other species. Delocalization results in less electron repulsion upon anion formation and therefore more substantially stabilizes the anionic states of the easily ionized species. In other words, the 'Cl' species, whose ionization potential lies ca. 1 eV below that of 'U', has an electron affinity similar to that of 'C5' most probably due to 'Cl's ability to delocalize the extra electron. This effect is schematically represented in Figure 4. A similar reasoning can apply to the
+
Colson and Sevilla base radical intermediates that shift positions in the two scales. For instance 'C(5)H and T(5)OH have their extra electron more localized than 'A(5)OH or 'A(8)H and therefore drop in electron affinity relative to the latter species. 3. Redox Potentials vs Electron Affinity and Ionization Potential. The redox properties of the radical intermediates have been experimentally measured against TNM (tetranitromethane), TMPD (N,N,N ',N '-tetramethyl-p-phenylenediamine), MV2+(methyl viologen), and Fe(CN)63-,8.'2'31,36,38 but a consistent scheme presenting the relative redox properties of all radical intermediates has yet to be produced. These properties can be related to the ionization potentials and electron affinities of the radical intermediates calculated here. In this regard, it is interesting to note that the trend in ionization potentials presented in Figure 3 is in good agreement with experimental results which have shown 'G(8)OH, 'G(5)OH, *C(5)OH,'A(5)OH, 'G(8)H, 'C(5)H and 'C(3)H have reducing capabilities mostly toward TNM, while the trend in electron affinities is in good agreement with experimental results which have shown 'C(6)OH, 'T(6)OH, 'C(6)H, 'T(6)H, 'A(4)OH and 'G(4)OH can oxidize TMPD.8712*31*36-38 To accurately relate redox potentials to electron affinities and ionization potentials, both molecular relaxation (adiabaticity) and solvation free energies must be accounted for. Molecular relaxation effects differ only slightly between DNA base structures, accounting for about 0.4-0.6 eV stabilization for DNA base ion radicals in our previous work.22 With regard to solvation, a recent study by Ruoff et al.39has shown that for anions of similar delocalization, including those of aromatic hydrocarbons, metalloporphyrins,and metal complexes, values of differential solvation free energies, AAG,,1, are quite constant and simply correct the EA by an additive constant; Le., E112 = EA - AAG,,, Eref.Values of A, Le., IP - EA, for individual radicals in Figure 3 range from 6 to 7 eV. Since A is a measure of delocalization, it indicates that differences in delocalization between these radicals are modest. Therefore, while aqueous solvation will stabilize the ions by ca. 3 eV each,20we expect only small effects on the relative orders in Figure 3. Finally we note that, for most of the possible radical-radical electron disproportionation reactions (R1' R2' R1+ R2**-) for species in Figure 3, the solvation effects must typically liberate 5-7 eV to overcome the difference between the gas phase ionization potential of R1' and the gas phase electron affinity of R2'. 4. Structural Features. In previous work,22we have fully geometry optimized the four DNA bases and their respective anion and cation radicals at the 6-31G* level and observed no significant degree of nonplanarity of the ring structures. A recent ab initio second-order Moller-Plesset study performed by Sponer et aL40 shows the nonplanarity mostly resides at the amino groups of cytosine, guanine, and adenine, whose deformability intervenes in the stabilization of base-base interactions. Stabilization of the species due to such pyramidalization is quite small (0.5-1.6 kcavmol). In the present work, the H and OH base radical adduct (Figure 1) geometry-optimized structures at the ROHF/6-3lG* level reveal a significant effect, particularly of the 'OH adduct radicals, on the planarity of the bases. Indeed, the hydroxyl adducts of the pyrimidines are slightly nonplanar, while the 4- and 5-OH adducts of the purines bend so as to take a pronounced "butterfly" shape, as shown in Figure 5. On the other hand, the hydrogen adducts and the 8-OH adducts of the purines remain mostly planar. This feature may be important not only in foreseeing potential geomeAdcal disruptions of the DNA helix upon formation of such radicals but also in conjecturing on the accessibility of radioprotective agents to the site of damage. Indeed, besides electron transfer
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Radicals Formed by H’and ‘OH Addition to the DNA Bases
J. Phys. Chem., Vol. 99, No. 34, 1995 13037 of this work. We thank the DOE National Energy Research SupercomputerCenter at Lawrence Livermore National Laboratory for generous grants of computer time.
Supporting Information Available: Coordinates (x, y , z) for species obtained at the ROHF/6-31G* level (12 pages). This material is contained in many libraries on microfiche, immediately follows this article in the microfilm version of the journal, can be ordered from the ACS, and can be downloaded from the Internet; see any current masthead page for ordering information and Internet access instructions. ‘G(5K)H
‘A(5)OH
Figure 5. C4 and C5 hydroxyl adducts of adenine and guanine taking on a very pronounced “butterfly” shape upon geometry optimization at the ROHF/6-3 1G* level.
reactions, such lesions could be healed via hydrogen atom transfer reactions from thiols (theoretical investigation of this process is in progress in our laboratory). The deformation of the DNA helix resulting from the significant nonplanarity of the base radical adduct could open the site for repair by thiols.
Summary The present results predict that of all the radical intermediates investigated in this study, the C6 position ‘OH and ‘H adducts of the pyrimidines are most oxidizing, while the N3 position ‘H adduct of cytosine is the most reducing species. The trends in electron affinities and ionization potentials calculated in this work lead to conjecture on potential electron transfer reactions among the various radical intermediates. For instance, reduction of ‘G(8)OH by ‘C(3)H or its oxidation by T(6)H’ should both readily occur, resulting in the formation of the ring-opened species Fapy-guanine or the oxidized species 8-oxoguanine, respectively. Deoxyribose radicals are predicted to have roughly equal oxidizing power, but ‘Cl’ clearly emerges as the most reducing sugar radical. Electron transfer processes involved in radioprotective mechanisms are also predicted from the calculated electron affinities presented in this work. These results show, in combination with experimental observation^,^' that thiols such as cysteamine will likely donate an electron to the species whose electron affinities lie near and above that of the deoxyribose radicals (1.6 eV). The present work shows that the overall trends in electron affinities and ionization potentials are similar, with the high and low ends of both scales being occupied by the same species. However, differences are noted within khe scales and explained on the basis of electron delocalization effects. Some easily ionized species are found to have delocalized structures which result in less electron repulsion upon formation of the anionic state. The trends in ionization potentials and electron affinities of the various DNA radical adducts obtained from scaling to experimental values of smaller model radical compounds are shown to be in excellent agreement with experimental redox trends. Upon formation of the hydroxyl adducts at the C4 and C5 positions of the purines, substantial conformational changes occur, resulting in “butterfly” shaped structures. v3*
Acknowledgment. We thank the National Cancer Institute of the National Institutes of Health (Grant ROlCA45424) and the Office of Health and Environmental Research of the Department of Energy (Grant DEFG0286ER60455)for support
References and Notes (1) Becker, D.; Sevilla, M. D. In Advances in Radiation Biology; Lett, J. T., Adler, H., Eds.; Academic Press: New York, 1993; p 121. (2) von Sonntag, C. The chemical basis of radiation biology 1; Taylor and‘Francis: London, 1987. (3) Steenken, S. Chem. Rev. 1989, 89, 503. (4) Sevilla, M. D.; Becker, D. R. SOC.Chem. Spec. Rev., Electron Spin Reson. 1994, 14, 130. ( 5 ) O’Neill, P.; Fielden, E. M. In Advances in Radiation Biology; Lett, J. T., Adler, H., Eds.; Academic Press: New York, 1993. Fujita, S.; Steenken, S. J. Am. Chem. SOC.1981, 103, 2540. Hazra, D. K.; Steenken, S. J. Am. Chem. SOC. 1983, 105, 4380. Vieira, A. J. S. C.; Steenken, S. J. Am. Chem. SOC.1987, 109,7441. Deeble, D. J.; von Sonntag, C. Int. J. Radiat. Biol. 1984, 49, 247. Scholes, G.; Simic, M. Biochim. Biophys. Acta 1968, 166, 255. Das, S.; Deeble, D. J.; von Sonntag, C. 2. Natur$orsch. 1985,40c, Candeias, L. P.; Steenken, S. J. Phys. Chem. 1992, 96, 937. Pullman, B.; Mantione, M. J. C. R. Acad. Sci. Paris 1965, t.261, Heiberg, A. B.; Jensen, H. H. Acta Chem. Scand. 1977, A31, 195. Westhof, E.; van Rooten, M. 2. Natur$orsch. 1976, 31c, 371. Krauss, M.; Osman, R. J. Phys. Chem. 1993, 97, 13515. Colson. A. 0.: Besler, B.; Close, D. M.; Sevilla, M. D. J. Phys. Chem.‘ 1992, 96, 661. (18) Colson, A. 0.;Besler, B.; Sevilla, M. D. J. Phys. Chem. 1992, 96, 9787. (19) Colson, A. 0.;Besler, B.; Sevilla, M. D. J. Phys. Chem. 1993, 97, 8092. (20) Colson, A. 0.;Besler, B.; Sevilla, M. D. J. Phys. Chem. 1993, 97, 13852. (21) Sevilla, M. D.; Besler, B.; Colson, A. 0. J. Phys. Chem. 1994,98, 2215. (22) Sevilla, M. D.; Besler, B.; Colson, A. 0. J. Phys. Chem. 1995, 99, 1060. (23) Colson, A. 0.; Sevilla, M. D. Int. J. Radiat. Biol. 1995, 67, 627. (24) Oyler, N. A.; Adamowicz, L. J. Phys. Chem. 1993, 97, 11122. (25) Hariharan, P. C.; Pople, J. A. Chem. Phys. Lett. 1972, 16, 217. (26) Binkley, J. S.; Pople, J. A.; Dobosh, P. A. Mol. Phys. 1974, 28, 1423. (27) Roothaan, C. C. J. Rev. Mod. Phys. 1960, 32, 179. (28) Frisch, M. J.; Trucks, G. W.; Head-Gordon, M.; Gill, P. M. W.; Wong, M. W.; Foresman, J. B.; Johnson, B. G.; Schlegel, H. B.; Robb, M. A.; Replogle, E. S.; Gomperts, R.; Andres, J. L.; Raghavachari, K.; Binkley, J. S.; Gonzalez, C.; Martin, R. L.; Fox, D. J.; DeFrees, D. J.; Baker, J.; Stewart, J. J. P.; Pople, J. A. GAUSSIAN 92, Revision B, C; Gaussian, Inc.: Pittsburgh, PA, 1992. (29) Dunning, T. H.; Hay, P. J. Modern Theoretical Chemistry I ; Plenum: New York, 1976. (30) Colson, A. 0.; Sevilla, M. D. J. Phys. Chem. 1995, 99, 3867. (31) O’Neill, P. Radiat. Res. 1983, 96, 198. (32) Wang, W.; Sevilla, M. D. Int. J. Radiat. Biol. 1994, 66, 683. (33) Swarts, S. G.; Becker, D.; Sevilla, M. D.; Wheeler, K. T. In preparation. (34) Wang, W.; Sevilla, M. D. Radiat. Res. 1994,138, 9. ( 3 5 ) Candeias, L. P.; Steenken, S. In The Early Effects of Radiation on DNA; Fielden, E. M., O’Neill, P., Eds.; Springer Verlag: Berlin, 1991; p 265. (36) Steenken, S. J. Chem. SOC.,Faraday Trans. 11987, 83, 113. (37) Steenken, S. Free Radical Res. Commun. 1992, 16, 349. (38) Deeble, D. J.; Das, S.; von Sonntag, C. J. Phys. Chem. 1985, 89, 5784. (39) Ruoff, R. S.; Kadish, K. M.; Boulas, P.; Chen, E. C. M. J. Phys. Chem. 1995, 99, 8843-8850. (40) Sponer, J.; Hobza, P. J. Phys. Chem. 1994, 98, 3161.
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