Electron Interaction with Phosphate Cytidine Oligomer dCpdC: Base

Jan 7, 2014 - Electron Interaction with Phosphate Cytidine Oligomer dCpdC: Base-. Centered Radical Anions and Their Electronic Spectra. Jiande Gu,*. ,...
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Electron Interaction with Phosphate Cytidine Oligomer dCpdC: BaseCentered Radical Anions and Their Electronic Spectra Jiande Gu,*,† Jing Wang,‡ and Jerzy Leszczynski‡,* †

Drug Design & Discovery Center, State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai 201203 China ‡ Interdisciplinary Nanotoxicity Center, Department of Chemistry, Jackson State University, Jackson, Mississippi 39217, United States ABSTRACT: Computational chemistry approach was applied to explore the nature of electron attachment to cytosine-rich DNA single strands. An oligomer dinucleoside phosphate deoxycytidylyl-3′,5′-deoxycytidine (dCpdC) was selected as a model system for investigations by density functional theory. Electron distribution patterns for the radical anions of dCpdC in aqueous solution were explored. The excess electron may reside on the nucleobase at the 5′ position (dC•−pdC) or at the 3′ position (dCpdC•−). From comparison with electron attachment to the cytosine related DNA fragments, the electron affinity for the formation of the cytosine-centered radical anion in DNA is estimated to be around 2.2 eV. Electron attachment to cytosine sites in DNA single strands might cause perturbations of local structural characteristics. Visible absorption spectroscopy may be applied to validate computational results and determine experimentally the existence of the base-centered radical anion. The timedependent DFT study shows the absorption around 550−600 nm for the cytosine-centered radical anions of DNA oligomers. This indicates that if such species are detected experimentally they would be characterized by a distinctive color.

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deoxycytidine (dGpdC),13 and the cytosine-centered trinucleoside phosphate (dGpdCpdG)14 have been investigated recently using the reliable DFT approaches. Both experiments and theoretical studies have confirmed that the nucleobases in DNA can capture excessive electrons, forming the base-centered radical anions.15−17 Although the electron capture ability of the bare nucleobases is low, with electron affinity close to zero, the effects of the surroundings increase their electron affinity greatly.16,17 Moreover, the existence of a polarizable medium may even alter the nature of electron attachment to DNA and its subunits.10,15,17−21 Experimental studies on uracil have confirmed that the influence of the microsolvated water molecules is able to transform gas-phase dipole-bound anions (in which an electron is loosely bound to the molecule through its dipole-moment) into the tightly bound valence state.15,19−21 Theoretical studies suggest that the delocalized unpaired electron density of the radical anions of the purine nucleotides in the gas phase turns out to be well-localized, due to the influence of the polarizable continuum medium.10,17,18 This effect may lead to the existence of different locations of the excess electron in DNA segments as shown in the studies of the electron attachment to the dinucleoside phosphate deoxyguanylyl-3′,5′-deoxyguanosine (dGpdG) in the presence of a polarizable medium.22

INTRODUCTION DNA has been speculated as the medium for electron transport soon after its structure has been solved for the first time.1−3 Apparently, π-stacked assemblies of the nucleobases in DNA adopt a variety of local conformations depending upon sequence context. Obviously, these conformations could affect the coupling, the energetic properties, and the steps involved in the electron migration process in DNA.4 It is well recognized that owing to their relatively large electron affinity thymine (T) and cytosine (C) are expected to be the main step stones for the excess electron during the electron transfer process in DNA.5 The experimental study by Ray et al. in 2005 suggested that the number of C bases might affect the electron capture ability of the single strand of DNA in monolayer.6 Importantly, the electron capture by layers made of double-strand DNA is less efficient than capturing by layers made of single-strand CTrich oligomers. Therefore, a detailed description of the local structure of the cytosine centered single-strand DNA segments is crucial for understanding and predicting the elementary mechanisms of electron transfer through the cytosine-rich DNA oligomers. Electron attachment to the cytosine-rich DNA fragments has been explored systematically: ranging from consideration of models consist of nucleobase, nucleoside, and to nucleotides.7−12 As crucial steps to achieve the realistic description of electron interacting with the single-strand nucleotide oligomers, the dinucleoside phosphate deoxycytidylyl-3′,5′-deoxyguanosine (dCpdG), dinucleoside phosphate deoxyguanylyl-3′,5′© 2014 American Chemical Society

Received: September 16, 2013 Revised: January 6, 2014 Published: January 7, 2014 915

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and p-type polarization functions for H, namely 6-31+G(d,p),28 were used in the calculations. Geometries of the nucleotide dimer dCpdC and the corresponding radical anions were optimized using the M06-2X/6-31+G(d,p) approach. The Barone-Tomasi polarizable continuum model (PCM)29 with the standard dielectric constant of water (ε = 78.39) was used to simulate the solvated environment of an aqueous solution. The adiabatic electron affinity was computed as the difference between the absolute energies of the appropriate neutral and anion species at their respective optimized geometries, AEA = Eneut − Eanion The time-dependent density functional theory (TDDFT) approach has become widely applied in studying electronic transitions because of its remarkably low computational cost and its high reliability as compared to other sophisticated quantum chemical methods for the valenceexcited states.30−32 In the present study, TDDFT approach (M06-2X functionals along with the valence triple-ζ basis set 6311+G(d,p))28 was employed to calculate the electronic transition energies of the electron attached species. Circular dichroism (CD) spectra are derived based on the TDDFT calculations. The GAUSSIAN 09 system of DFT programs33 was used for all computations.

In order to explore the mechanism of electron capture and electron transfer mechanisms involving cytosine-rich DNA oligomers, it is necessary to examine the interaction of an excess electron with oligomers of the nucleotides. In DNA oligomers, the excess electron may reside on different locations, forming various radical anions. The studies of these local minimum structures of the radical anions are expected to reveal the favored positions of an attached excess electron in DNA oligomers. This information is also important for understanding the details of electron migration along the DNA strands. Here we report theoretical investigations of electron attachment to the cytosine-rich DNA single strand segment dinucleoside phosphate deoxycytidylyl-3′,5′-deoxycytidine (dCpdC: Scheme 1) in the presence of a polarizable medium. This model Scheme 1. Model of a Cytosine-Rich DNA Single Strand: Dinucleoside Phosphate Deoxycytidylyl-3′,5′-Deoxycytidine (dCpdC)

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RESULTS AND DISCUSSION A. Neutral dCpdC. The initial structure of the neutral dCpdC is constructed based on our previous studies of the Bform DNA trimer dGpdCpdG by replacing one dG with dC and removing another dG fragment in the trimer. Two initial structures of dCpdC were obtained by the replacing-removing procedures. Geometric optimizations without constrains of both initial structures lead to the same optimized geometry. The optimized geometry of dCpdC in the neutral form in aqueous solution (modeled by the PCM) is depicted in Figure 1 and the base−base stacking pattern parameters are reported

represents the minimal unit of cytosine-rich single-strand DNA oligomers. Investigations of the different structures of the radical sites of this system provide the information on how local structures influence the electron affinity of cytosine, an important electron acceptor in DNA strands. Moreover, the investigations of the electron excitations in these systems might eventually lead to future experimental determinations of the corresponding radical anions. Theoretical Methods. The density functionals M062X,23−25 which well describe stacking interactions, is one of the best computational tool for the systems in which base−base stacking dominates the structural characteristics. Previous studies of the stacked bases have demonstrated that the geometric parameters (that characterize the stacking patterns) predicted by the M06-2X method with double-ζ basis sets augmented with polarized and diffused functions are very close to those predicted by the MP2 method with triple-ζ basis set with polarized functions (base−base distances less than 0.02 Å and base−base angles less than 1°).26 The stacking energy differences between the M06-2X and MP2 methods are less than 1 kcal/mol.26 The functional M06-2X has been successfully applied in the study of radical anions of nucleobases. The electron affinities of the five nucleobases evaluated by the M06-2X approach are close to those predicted by the G4 method.17 Moreover, a recent benchmark exploration of the performance of time-dependent DFT methods reveals that M06-2X is the best overall performing GH-mGGA functional among the 24 tested functionals.27 In the present study the M06-2X functional and the valence double-ζ basis set, augmented with d-type polarization functions as well as the diffuse functions for heavy elements

Figure 1. Optimized geometries of dCpdC in aqueous solution (PCM model). Here O1 and O2 are the geometric centers of atoms N3, N1, and C5 of dC1 and of dC2, respectively. v1 and v2 are the plane vectors defined by the atoms N3, N1, and C5 of dC1 and of dC2, respectively. t1 and t2 are the vectors of the bases pointing from O1 to the atoms N4 of dC1 and from O2 to the atoms N4 of dC2, respectively. O1′ is the projection of O1 on the base-plane of C2. For base−base stacking pattern parameters see Table 1. Color conventions: gray: carbon; blue: nitrogen; red: oxygen; orange: phosphorus. Bond lengths in Å.

in Table 1. Of course, this structure is only one of possible local minima on the potential energy surface. However, it presents the biologically important B-form of single-strands DNA with well-stacked bases in aqueous solutions. The base-center of dC1 (O1, defined as the geometric center of N3, N1, and C5 of dG1) is 3.276 Å away from the base-plane of dC2 (C2: defined by N3, N1, and C5 of dC2). The longer distance (3.991 Å) between the base-centers, R(O1, O2), 916

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Table 1. Geometric Parameters of the Base−Base Stacking Pattern of the Optimized Structures of the Neutral and the Radical Anions of dCpdC (Distances in Å and Angles in deg) species

R(O1, O2)a

R(O1, C2)b

R(O2, O1′)c

ϕ(v1, v2)d

ϕ(t1, t2)e

dCpdC dC•−pdC dCpdC•−

3.991 4.148 4.127

3.276 2.575 3.127

2.279 3.252 2.693

8.6 29.6 11.5

37.8 42.7 38.1

a

R(O1, O2): distance between the base-centers O1 and O2, see Figure 1. bR(O1, C2): distance between the base-center and the base-plane of C2. R(O2, O1′): distance between the base-center O2 and the projected base-center O1 (projected on the base-plane of C2), defined as (R(O1, O2)2 − R(O1, C2)2)1/2 dϕ(v1, v2): angle between the base-plane vectors. eϕ(t1, t2): angle between the base-direction vectors lying on the base-plane. c

nucleobase C1 is the principle host of the unpaired electron. As illustrated by the singly occupied molecular orbital (SOMO) depicted in Figure 2, the excess electron reside on the first π antibonding orbital of C1. The Natural Population Analysis (NPA) reveals that over 0.88 negative charge is located on the C1 fragment in dC•−pdC (see Table 2). Analogously, the

indicates that the bases slide away along the base-planes significantly (R(O2, O1′) is 2.279 Å for the projected base−base center distance). The two base planes are found to be not far away from parallel configuration. The angle between the baseplane vectors (ϕ(v1, v2), v1 and v2, defined by N3, N1, and C5 of dC1 and that of dC2, respectively) is predicted to be 8.6°. In addition, the rotation of the bases around helix (ϕ(t1, t2), t1 and t2, are the vectors defined by N4 and the base center of dC1 and that of dC2, respectively) is measured to be 37.8°. These parameters are close to the typical values observed in B-DNA.34 B. Base-Centered Radical Anions of dCpdC. The excess electron is found to reside on the nucleobase of either dC1 (dC•−pdC, Figure 2) or dC2 (dCpdC•−, Figure 3). The

Table 2. Natural Population Analysis of Charge Distributions of dCpdC and the Corresponding Radical Anions (in au)a species

C1

C2

S1

S2

P

dCpdC dC•−pdC dCpdC•−

−0.27 −1.15 −0.27

−0.27 −0.30 −1.17

0.62 0.54 0.61

0.64 0.64 0.56

−0.72 −0.73 −0.73

a

C1 and C2 are the nucleobases of dC1 and dC2, S1 and S2 are the corresponding sugar moieties, and P is the phosphate group of dCpdC.

geometric feature and the SOMO of dCpdC•− (see Figure 3) imply that excess electron locates on C2 moiety. The corresponding NPA charge indicates that over 0.90 negative charge is distributed on C2 fragment (Table 2) in the radical anion dCpdC•−. C. Base−Base Stacking Pattern. Electron attachment to the bases of the cytidine oligomer alters the cytosine−cytosine base-stacking pattern. The base planes are significantly away from parallel configuration. The base-planes tilt by 11.5° in dCpdC•− and by 29.6° in dC•−pdC. The large plane−plane angle in dC•−pdC is the due to center of the negative charge of C1 that attracts the positively charged H on C5 and N4 of dC2, causing the rotation of the base C2 around the glycosidic bond. Moreover, excess electron on the base increases the base−base sliding distance significantly. The projected base−base center amounts to 2.693 Å in dCpdC•− and 3.252 Å in dC•−pdC. For comparison, this distance is 2.279 Å in the neutral oligomer. The base−base stacking pattern in dCpdC is disrupted by the electron attachment. This is consistent with the previous studies of the guanine-rich olegomers (dGpdG and dGpdCpdG) and the GC oligomers.14,22 This phenomenon implies that the base−base stacking structure does not favor accepting of an excess electron. It is important to note that the base rotation does not encounter crucial changes due to electron attachment. Although ϕ(t1, t2) of dC•−pdC is 5° greater than that in neutral oligomer, the effective base rotation value experiences smaller increase because this rise in angle value also includes the effects of the large base-planes tilt angle in dC•−pdC. Therefore, electron attachment to cytosine sites in DNA single strands might lead to local structural disturbances only. D. Electron Affinities. The predicted stability (from an energetic point of view) of the radical anions follows the order: dC•−pdC > dCpdC•−. The AEA is predicted to be 2.08 eV for

Figure 2. Optimized structure of dC•−pdC and the corresponding SOMO in aqueous solution. Bond lengths in Å. For color conventions, see Figure 1

Figure 3. Optimized structure of dCpdC•− and the corresponding SOMO in aqueous solution. Bond lengths in Å. For color conventions see Figure 1

optimized structure of dC•−pdC reveals that the structure of the nucleobase in dC1 (C1) is significantly different from that in the neutral species due to electron attachment. The elongated bond lengths for C2O2 (1.25 Å vs 1.23 Å), N3C4 (1.37 Å vs 1.32 Å), C4N4 (1.41 Å vs 1.34 Å), C5C6 (1.40 Å vs 1.35 Å), and C6N1 (1.42 Å vs 1.36 Å) are found in C1 of dC•−pdC. Meanwhile, the geometric parameters of nucleobase C2 are literally the same as those in the neutral form. The geometric feature of dC•−pdC strongly indicates that the 917

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formation of dC•−pdC and 1.98 eV for formation of dCpdC•− anion. The AEA of dC•−pdC is about the same as that of pdC•−p (2.09 eV with M06-2X/6-31+G(d,p), see Table 3). On

formation of the phosphate-centered radical anion in DNA is between 0.6 to 1.6 eV, more likely around 0.6 eV, in aqueous solution.22 Moreover, the phosphate-centered radical anions in general have large structural distortions in the phosphate group. In this case, electron attachment to the phosphate group of dCpdC is less viable. The cytosine-centered radical anions of dCpdC are found to be electronically stable. The vertical electron detachment energy (VDE) is predicted to be 2.59 eV for dC•−pdC and 2.40 eV for dCpdC•−, respectively. Detachment of the excess electron from the radical anions is difficult through the thermal motion. E. Electronic Spectra. The neutral cytindine nucleotide oligomer is colorless. Its first excitation energy is predicted to be 4.9 eV (252 nm, about 13 nm less than the experimental value 265 nm37) in the present study. However, the radical anions of dCpdC are expected to have lower excitation states due to the excess electron that locates on the π* antibonding orbital of the nucleobase. The predictions of the first ten excited states of dCpdC•− and dC•−pdC were performed within the TDDFT formalism. Since the VDE of dCpdC•− is 2.40 eV and that of dCpdC•− is 2.59 eV, only the first three observable transitions will be presented and discussed below. The computed electronic transition energies of dCpdC•− and dC•−pdC (Table 4) reveal that the first transition energy is very low, 1.55 eV (801 nm) for dCpdC•− and 1.70 eV (727 nm) for dC•−pdC, respectively. Molecular orbital analysis indicates that this first excitation corresponds to the transition of the unpaired electron from the nucleobase C2 to C1 in dCpdC•− (Figure 5) and from C1 to C2 in dC•−pdC, respectively (Figure 6). Therefore, this excitation can be viewed as the electron migration along DNA. π → π transition of the excess electron is observed on dC1 moiety in dC•−pdC with excitation energy of 2.12 eV or 583 nm (the second excitation), and on dC2 moiety in dCpdC•− with 2.15 eV or 577 nm (the third excitation). As comparison, this π → π transition is predicted to be the first excitation in the cytosine-centered radical anion of cytidine diphosphates, pdCp. The corresponding excitation energy amounts to 2.16 eV or 574 nm. The third excitation state of dC•−pdC and the second excitation state of dCpdC•− are found to have the feature of the molecular Rydberg state. The excess electron is primarily dipole-bounded to the stacked bases. The corresponding excitation energy is 2.24 eV (554 nm) for dC•−pdC and 2.03 eV (612 nm) for dCpdC•−, respectively. Similar molecular Rydberg state can also be identified for the radical anion pdC•−p as the second excited state with excitation energy of 2.22 eV (558 nm). The visible absorption spectra of the radical anions of dCpdC (ranging from 400 to 700 nm) are depicted in Figure 7. Thus, the cytosine-centered radical anions are expected to reveal their color in aqueous solutions. Circular dichroism (CD) spectroscopy represents a useful tool in the structure determination of DNA in aqueous solutions.36 The calculated visible CD spectra presented in Figure 8 indicate that the second and the third transitions of the cytosine at the 5′-position and that at the 3′-position have different phases. Therefore, if it is detectable, visible CD spectroscopy could be applied to identify the location of the radical center in the electron attached cytosine-rich oligomers.

Table 3. Theoretical Predictions for the AEAs of Cytosine Containing Nucleoside, Nucleotides, and Oligonucleotides in Aqueous Solution (in eV) (Numbers in Parentheses Are Zero-Point Corrected Energies) process

AEA

VEAa

VDEb

dCpdC → dCpdC•− dCpdC → dC•−pdC dGpdCp → dGpdC•−p pdCpdG → pdC•−pdG 3′,5′-dCDP → 3′,5′-dC•−DP 5′-dCMP → 5′-dC•−MP 3′-dCMP → 3′-dC•−MP dC → dC•− C → C•−

1.89 (1.98) 1.98 (2.08) 1.96c 2.07c 1.99,d 2.00 (2.09)e 1.89f 2.18f 1.81g 1.89h

1.32 1.32

2.40 2.59

1.39e

2.57e

a VEA = E(neutral) − E(anion); the energies are evaluated using the optimized neutral structures. bVDE = E(neutral) − E(anion); the energies are evaluated using the optimized anion structures. cReference 14; M05-2X/DZP++, PCM single point based on the gas-phase optimized structures. dReference 10, B3LYP/DZP++. ePresent research, M06-2X/6-31+G(d,p). fReferences 9 and 11, B3LYP/DZP ++. gReference 34, B3LYP/6-31+G(d). hReference17, B3LYP/DZP+ +.

the other hand, the AEA of dCpdC•− is about 0.1 eV smaller than that for dC•−pdC. Since the bases in dC•−pdC are less stacked, one might attribute this 0.1 eV difference to the stacking interaction between the bases. Namely, stacking slightly reduces the electron affinity of cytosine in DNA single-strands. This effect of stacking interaction seems to be independent of the neighboring bases. The GC stacked oligomers possess literally the same AEA values (1.96−2.07 eV).14,17 To determine the potential ability to capture an excess electron to the cytidine oligomers, the vertical attachment energy (VEA) and the corresponding electron state of dCpdC have been examined. The VEA value is calculated to be 1.32 eV in the PCM approximation to simulate the surroundings. The molecular orbital analysis reveals that the excess electron resides on the π antibonding orbitals of both cytosine bases, as shown in Figure 4. That seems to suggest that the excess electron might be captured between the stacked bases in the nascent stage of electron attachment. Subsequent geometric rearrangements lead to the more stable one-base-centered radical anions. Previous study concludes that the AEA for the

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CONCLUSIONS Electron distribution patterns for the radical anions of dCpdC in aqueous solution have been explored. The excess electron may reside on the nucleobase at the 5′ position (dC•−pdC) or

Figure 4. SOMO of the dCpdC vertically attached an electron in aqueous solutions. 918

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Table 4. Transition Energies (ΔE) and Oscillator Strengths ( f) of the First Three Transitions of dCpdC•−, dC•−pdC, and pdC•−pa dC•−pdC

a

dCpdC•−

pdC•−p

state

ΔE (eV)

f

ΔE (eV)

f

ΔE (eV)

f

S1 S2 S3

1.705 (727 nm) 2.123 (584 nm) 2.240 (554 nm)

0.005 0.006 0.003

1.549 (801 nm) 2.027 (612 nm) 2.147 (577 nm)

0.004 0.003 0.009

2.158 (574 nm) 2.224 (558 nm) 2.530 (490 nm)

0.005 0.007 0.001

TDDFT(M06-2X) calculations with basis set 6-311+G(d,p) based on the M06-2X/6-31+G(d,p) optimized structures.

Figure 8. CD spectra of dC•−pdC and dCpdC•−.

•−

Figure 5. MOs of the excited states of dCpdC .

to the base-centered anions, for electron attachment to cytidine-rich oligomers. From comparison with electron attachment to the cytosine related DNA fragments: pdCpdG, dGpdCp, pdCp, dCp, pdC, dC, and C, the electron affinity for the formation of the cytosine-centered radical anion in DNA is estimated to be around 2.2 eV. Base−base stacking patterns in DNA single strands seem to be affected by electron attachment to the bases. However, electron attachment to cytosine sites in DNA single strands might lead only to local structural disorder. This information should be vital in exploring the cytosinecytosine electron migration mechanism. Detection the existence of the base-centered radical anion is crucial for experimental studies of DNA. Visible absorption spectroscopy may provide a feasible approach to facilitate such investigations. An analysis of absorption visible spectra reveals the absorption bands around 550 to 600 nm for the cytosine-centered radical anions of DNA oligomers. We suggest that the electron attachment to cytidine oligomers might result in adding color to DNA single-strands.

Figure 6. MOs of the excited states of dC•−pdC.

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: (J.G.) [email protected]. *E-mail: (J.L.) [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS Work in the USA was supported by the NSF CREST Grant (HRD-0833178). We would like to thank the Mississippi Center for Supercomputing Research for a generous allotment of computer time.

Figure 7. Absorption spectra of dC•−pdC and dCpdC•−.

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at the 3′ position (dCpdC•−). These two radical anions are expected to be electronically viable species, stabilized by the influence of the polarizable medium. dC•−pdC is expected to be more stable than the dCpdC•− anion. We concluded that the phosphate-centered radical anion is less viable, as compared

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