Theoretical Determination of One-Electron Redox Potentials for DNA

ARTICLE pubs.acs.org/JPCA

Theoretical Determination of One-Electron Redox Potentials for DNA Bases, Base Pairs, and Stacks Y. Paukku and G. Hill* Interdisciplinary Center for Nanotoxicity, Department of Chemistry, Jackson State University, 1400 J. R. Lynch Street, P.O. Box 17910, Jackson, Mississippi, United States

bS Supporting Information ABSTRACT: Electron affinities, ionization potentials, and redox potentials for DNA bases, base pairs, and N-methylated derivatives are computed at the DFT/M06-2X/6-31þþG(d,p) level of theory. Redox properties of a guanine
guanine stack model are explored as well. Reduction and oxidation potentials are in good agreement with the experimental ones. Electron affinities of base pairs were found to be negative. Methylation of canonical bases affects the ionization potentials the most. Base pair formation and base stacking lower ionization potentials by 0.3 eV. Pairing of guanine with the 5-methylcytosine does not seem to influence the redox properties of this base pair much.

’ INTRODUCTION Redox properties of nucleic acid bases are important characteristics of DNA and are one of the key factors in the storage and transfer mechanism of the genetic information. Correct determination of the redox potentials, electron affinities (EAs), and ionization potentials (IPs) is of great interest for the understanding of thermodynamic and kinetic properties of DNA, possible radiation damage and repair, and oxidation reactions as well as excess electron transfer through DNA. DNA interaction with drugs and intercalating agents depends on the electrondonating abilities of bases. It is known that base alterations and single-strand breaks are mediated by the one-electron deficient DNA base radicals. Therefore, there is a need to understand the chemical and physical mechanism of DNA oxidation. Unfortunately, limited experimental information is available for the redox potentials, EAs, and IPs of DNA bases and base pairs.1
4 Only recently, the experimental oxidation potential of the guanine-cytosine base pair was obtained.47 Futhermore, experimentally provided values are diverse; therefore, correct theoretical determination of highly accurate redox properties of DNA is important. Several theoretical works devoted to the calculation of EAs, IPs, and redox potentials have been done recently. First, computational studies were reported by Colson,5 Sevilla,6 and Hutter.7 Wetmore et al.8 investigated IPs and EAs of the DNA and RNA nucleotide bases using the DFT/B3LYP theory level. This work r 2011 American Chemical Society

provided evidence of the existence of stable radical-anion species of thymine and uracil. Positive values of adiabatic electron affinities (AEAs) were obtained for these bases. However, the AEAs of cytosine, guanine, and adenine were calculated to be negative. Russo9 studied the IPs and EAs of nucleotide bases using several DFT functionals and basis sets. Obtained IP values were consistent with the experimental data. As for AEAs, the study has shown that the positive or negative sign of the AEA values for cytosine and guanine strongly depended on the level of theory used. Li et al10 investigated the influence of basis set size on the EA values for nucleic acid bases. This work has shown that modest basis set sizes can produce relatively good results for the EA. However, inclusion of diffuse functions in the basis set can result in contamination of the valence-bound state with the dipole-bound state, especially in the case of purine bases and guanine in particular. Also, EAs and IPs have been reported for base pairs.11 Ab initio propagator calculations in the partial thirdorder approximation have been used for the prediction of IPs by Dolgounitcheva et al.12 Crespo-Hernandez et al. computed ionization energies13 and redox potentials14 for DNA nucleosides, DNA bases, and base pairs. The values were determined from an experimentally calibrated set of equations that correlate the Received: February 8, 2011 Revised: March 23, 2011 Published: April 18, 2011 4804

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The Journal of Physical Chemistry A vertical ionization (EA) energy of 20 organic molecules with their experimental reversible redox potentials. The study showed that base pairing and covalent, as well as noncovalent, interactions modulate the redox potentials of DNA bases. Calculation of the IPs in an aqueous medium was reported by Close15 in 2004. High-level quantum chemical ab initio coupled-cluster and multiconfigurational perturbation methods were used to calculate VEA and AEA of DNA and RNA in the study of Roca-Sanjuan.18 Recently, a number of density functional methods and basis sets were explored for EA and one-electron reduction potential calculations of nitrobenzenes by Zubatyuk et al.19 The results demonstrated the dependence of calculated EAs on the basis set. Basis sets augmented by diffuse functions performed much better in comparison with basis sets that do not contain diffuse functions at all. Also, it was shown that local and most of the hybrid generalized gradient approximation (GGA) functionals give very high errors in EA values, in contrast to meta-GGA functionals, which perform much better. There are some theoretical16 and experimental17 works that studied the effect of methylation on ionization and oxidation potentials of DNA bases. DNA methylation49 is a normal part of every organismal development and is an essential process for genomic imprinting, X-chromosome inactivation, suppression of repetitive elements, and so on. In humans, DNA methylation occurs mostly in the cytosine of the CpG dinucleotides. However, alterations in DNA methylation patterns have been linked with cancer development.50 Therefore, the effect of methylation on redox properties of nucleic acid bases is of particular importance. Thus, this work is devoted to the theoretical investigation of EAs, IPs, as well as one-electron reduction (Ered) and oxidation (Eox) potentials for DNA bases, their N-methylated derivatives, guanine-cytosine, adenine-thymine, and guanine-5-methylcytosine base pairs, and a guanine
guanine stack model.

’ COMPUTATIONAL DETAILS In order to find the most suitable and computationally affordable level of theory for the calculation of redox potentials, Møller
Plesset perturbation theory (MP2)20,21 and density functional theory (DFT)22 computations were performed. A number of density functionals were tested. New-generation DFT functionals have been shown to provide good results for EAs and IPs.23
26 Therefore, hybrid meta functionals MPWB1K, M05, M05-2X, M06, and M06-2X were evaluated (see Table S1, Supporting Information). All results reported in this study are based on the DFT M06-2X/6-31þþG(d,p) level of theory calculations.27
31 Because the solvation model directly affects final values of the redox potentials, several solvent models (PCM,32,33 CPCM,34,35 IEFPCM,36 SMD37) were applied toward the calculations (Table S2, Supporting Information). The structures of the target molecules were fully optimized without any geometric constraint. Local minima were verified on the potential energy surface by frequency calculations. Consequently, free energies of solvation were evaluated with the polarizable continuum model (PCM) using scaled Bondi’s atomic radii by full optimization of the gas-phase geometries.38 AEAs as well as adiabatic ionization potentials (AIPs) are computed as the energy difference between fully optimized neutral and corresponding radical-anion or radical-cation forms in the gas phase. Vertical ionization potentials (VIPs) were obtained from the difference in total energies between a fully optimized neutral molecule and its radical-cation evaluated at the geometry

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Table 1. AEAs for the DNA Bases, Base Pairs, and N-Methylated Derivatives Calculated at M06-2X/6-31þþG(d,p) EA, eV

EAzpe, eV

Ade

0.72

0.59

Gua

0.34

0.28

Cyt

0.24

0.13

Thy

0.09


0.03

1-MeC 3-MeC

0.25 0.23

0.14 0.10

5-MeC

0.25

0.14

1-MeG

0.42

0.37

7-MeG

0.46

0.39

1-MeA


0.08


0.18

3-MeA


0.02


0.13

7-MeA

0.37

0.24

G-C A-T


0.35
0.03


0.48
0.18

G-5-MeC


0.31


0.45

EAexp, eV41

EAexp, eV42

0.012 0.23

0.13

0.069

0.12

of the neutral molecule. All calculations were performed with the Gaussian 09 program package.39 Molecular orbital and electrostatic potential visualization were obtained with the MaSK Molecular Modeling and Simulation Kit, version 1.2.2.40

’ RESULTS AND DISCUSSION Electron Affinities. Table 1 lists AEAs and ZPE-corrected values for AEAs obtained at the M06-2X/6-31þþG(d,p) level of theory. Determination of accurate EAs for such systems as DNA bases is problematic due to the possibility of the formation of dipole-bound or valence-bound negatively charged species. Also, there is a problem with experimental data. Available experimental values are quite divergent, and there are no direct experimental values for guanine and for methylated derivatives of nucleobases. The order of AEAs for DNA bases obtained in this study is T < C < G < A. The ZPE-corrected EA for thymine is slightly negative, and the ZPE-corrected value for adenine is overestimated by 0.58 eV compared to available experimental data. Positive values of AEAs for adenine, guanine, and cytosine suggest the existence of stable anion-radical species of these bases. Because 5-methylcytosine is biologically relevant, its redox properties are of great interest. However, no significant difference in EAs is found for 5-methylcytosine and ordinary cytosine. In contrast to cytosine, there is a serious change in EA values for adenine and its 1-methylated and 3-methylated derivatives. AEAs for all base pairs were found to be negative. This is in agreement with previous work of Al-Jihad et al.54 for the A-T base pair and in contradiction with the study of Li et al.,11 where AEAs for A-T and G-C were determined to be positive (0.30 and 0.49 eV, respectively). Corresponding results are probably the best estimate for the given level of theory. Because EA is basisset-dependent, the results could be improved with a more extended basis set. Ionization Potentials. AIPs and VIPs for DNA bases, base pairs, and methylated derivatives are presented in Table 2. Obtained results are in good agreement with available experimental values. Only the AIP of cytosine is overestimated by 0.1 eV. There is a slight decrease in both the AIP and VIP values for methylated 4805

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Table 2. AIPs and VIPs for the DNA Bases and Base Pairs and N-Methylated Derivatives Calculated at M06-2X/6-31þþG(d,p)

Ade Gua Cyt Thy 1MeC 3MeC 5MeC 1MeG 7MeG 1MeA 3MeA 7MeA G-C A-T G-5MeC

AIP, eV

AIPzpe, eV

AIPexp, eV51

VIP, eV

VIPzpe, eV

VIPexp, eV52,53

8.26 7.83 8.83 8.93 8.53

8.26 7.82 8.78 8.90 8.50

8.26 7.77 8.68 8.87

8.51 8.24 8.95 9.23 8.69

8.49 8.22 8.85 9.18 8.62

8.44 8.24 8.80 ∼9.1 8.65

8.20

8.19

8.42

8.40

8.48

8.44

8.64

8.57

8.78

7.70

7.69

7.66

8.06

8.04

7.74

7.73

8.20

8.18

7.97

7.93

8.41

8.31

7.98

7.98

8.26

8.21

8.27

8.24

8.67

8.63

7.06 7.90 7.02

7.05 7.85 7.01

7.50 8.30 7.47

7.50 8.27 7.46

bases, which is especially noticeable for 3- and 5-MeC. The general sequence of AIP and VIP values is the following G < A < C < T, where guanine has the lowest IP and, therefore, is the most easily oxidizable. Present observations are in accord with previous experimental and theoretical findings.8,9,15 Ionization potentials for guanine-cytosine, guanine-5-methylcytosine, and adenine-thymine base pairs are significantly lower than those of single bases. Despite the visible change in the IP value between cytosine and 5-methylcytosine, no significant difference in IP values has been found for G-C and G-5-MeC base pairs. These results are consistent with previous findings of Kanvah and Schuster,17 who concluded that substitution of C for 5-MeC has no significant effect on the oxidation reaction rate and is not a general cause of oxidative damage in DNA. Reduction and Oxidation Potentials. The electrode reduction/oxidation potential is related to the free-energy change ΔG0 by the Nernst equation E0 ¼


ΔG0 þ EH nF

where n is the number of electrons transferred, F is Faraday’s constant (the negative of the charge on 1 mol of electrons), and EH is the absolute potential of the normal hydrogen electrode (
4.36 V). Therefore, the one-electron reduction/oxidation potential can be calculated using the thermodynamic cycle represented in Scheme 1. The upper part of the cycle represents the gas-phase process, and the lower part corresponds to the solvent phase. According to the cycle, the free energy of reduction in solution can be calculated as EA solv ðR
Þ
ΔGsolv ðOÞ ΔGred sol ðOÞ ¼ ΔGgas þ ΔG

Scheme 1. Thermodynamic Cycle for the Calculation of One-Electron Reduction/Oxidation Potentials in Solution

Table 3. One-Electron Reduction Potentials for DNA Bases, Base Pairs, and N-Methylated Derivatives Calculated at M062X/6-31þþG(d,p) Ered, V

Eredexp, V1

Δ

%Δ

Ade


2.77


2.52

0.25

9.03

Gua Cyt


2.97
2.36

36°, and the tilt is >1°). The geometry of this model was fully optimized at the M06-2X/6-31þþG(d,p) theory level with the PCM (Bondi) solvent model. Figure 2 represents the optimized structure of the GG stacked model. The obtained optimized geometry shows a ∼118° twist between two guanines and a vertical distance of ∼3.2
3.4 Å between them. Figure 3 shows the molecular electrostatic potential (MEP) of stacked guanine
guanine bases. The MEP plot indicates a positive electrostatic potential (shown in blue and green), corresponding to regions of amino groups and hydrogens. Regions of 4807

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Table 5. EAs, IPs, and Reduction and Oxidation Potentials for Stacked Guanine−Guanine Bases

GG G

AEA, eV

AEAzpe, eV

Ered, V

AIP, eV

AIPzpe, eV

VIP, eV

VIPzpe, eV

Eox, V

−0.11 0.34

−0.17 0.28

−2.94 −2.97

7.54 7.83

7.52 7.82

7.97 8.24

7.90 8.22

1.38 1.41

Figure 2. Optimized structure of the stacked GG model.

Figure 4. HOMO of the stacked GG model, side and top views.

Figure 3. Map of the electrostatic potential of the stacked GG bases, calculated at the M06-2X/6-31þþG(d,p) level.

negative electrostatic potential (shown in red) are noticeable around oxygen and N7 atoms, with the strongest negative potential on the oxygen in the C6dO moiety. Biological activity depends on the orientation as well as the depth of the MEP surface of GG base stacks. This electrostatic model helps predict

the influence of different sequences and geometries on the reactivity of DNA. Table 5 lists AEAs, AIPs, VIPs, and reduction and oxidation potential values for the stacked GG model and ordinary guanine. As can be seen, stacking changes the EA and IP values significantly. The AEA of stacked GG is negative. AIP and VIP values are lower by 0.3 eV. It was pointed out previously that GG stacks can act as thermodynamic sinks for the hole migrations, caused by oxidizing agents.45,46 Our results are consistent with these observations. Figure 4 shows HOMOs of stacked GG bases. In the neutral species, the HOMO is localized equally on both guanine bases. Although HOMO localization depends on the conformations and the distance between bases, the IP is not governed directly by the geometric changes45 of stacked GG. However, it was shown that conformational changes slightly affect the value of the IP. Because stacked GG bases are more easily oxidized, the electrophilic attacks on stacked GG are more favored. Although stacking has not been found to affect oxidation and reduction potential values significantly, there is a 4808

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The Journal of Physical Chemistry A slight decrease in the oxidation potential and increase in the reduction potential values.

’ CONCLUSIONS The M06-2X DFT functional was found to be suitable for the calculation of one-electron reduction and oxidation and IPs for DNA bases and base pairs, especially in the case of a stacked model, because this level of theory allows one to obtain reasonable results in a relatively short computational time. EAs are predicted less successfully due to dipole-bound contamination and diffuse functions of basis sets. Improved basis sets would solve this problem. No significant difference in EAs for nonmethylated and methylated DNA bases was found. Positive values of EA provide evidence for the existence of stable radicalanion species of some DNA bases and methylated analogues. Calculated values of IPs, Ered, and Eox are in good agreement with the experimental ones. In general, methylation of DNA bases lowers the IPs and Eox by 0.3
0.6 eV (V), depending on the position of the methyl group in the molecule. Ionization and oxidation potentials decrease upon base pair formation. No change in IP and Eox is observed when guanine is paired with 5-methylcytosine, which leads to the conclusion that 5-methylcytosine is not a general cause of oxidative damage in DNA. Reduction potential computations can be affected by the possible contamination of the valence-bound state with the dipole-bound state. Nevertheless, a good correlation of theoretical and experimental data is obtained with the following value order for DNA bases: G < A < C < T. On the basis of the general trend in the Ered values, methylation affects the Ered of cytosine and adenine more significantly as compared to that of guanine. Stacking affects the ionization and oxidation potentials and significantly lowers the values of the IP in the GG stack model, suggesting that the GG sequence is the most easily oxidized site in DNA. ’ ASSOCIATED CONTENT

bS

Supporting Information. Tables with EA and reduction potential values for adenine and cytosine obtained at different levels of theory as well as reduction and oxidation potential values for adenine, obtained at the M06-2X/6-31þþG(d,p) level of theory with different solvent models in water. This material is available free of charge via the Internet at http://pubs.acs.org.

’ AUTHOR INFORMATION Corresponding Author

*E-mail: [email protected]. Phone: (601)-979-1699. Fax: (601)-979-7823.

’ ACKNOWLEDGMENT This research was supported in part by the National Science Foundation through TeraGrid resources provided by NCSA under NSF-CREST (Grant No. HRD-0833178) and EPSCoR(Grant No. 362492-190200-01\NSFEPS-0903787) grants. The authors thank the Mississippi Center for Supercomputing Research (Oxford, MS) for a generous allotment of computer time. ’ REFERENCES (1) Seidel, C. A. M.; Schulz, A.; Sauer, M. H. M. J. Phys. Chem. 1996, 100, 5541–5553.

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