Article pubs.acs.org/JPCB
Photoinduced Electron Detachment and Proton Transfer: The Proposal for Alternative Path of Formation of Triplet States of Guanine (G) and Cytosine (C) Pair 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: A viable pathway is proposed for the formation of the triplet state of the GC Watson−Crick base pair. It includes the following steps: (a) a low-energy electron is captured by cytosine in the GC pair, forming the cytosine base-centered radical anion GC−•; and (b) photoradiation with energy around 5 eV initiates the electron detachment from either cytosine (in the gas phase) or guanine (in aqueous solutions). This triggers interbase proton transfer from G to C, creating the triplet state of the GC pair. Double proton transfer involving the triplet state of GC pair leads to the formation of less stable tautomer G(N2−H)•C(O2H)•. Tautomerization is accomplished through a double proton transfer process in which one proton at the N3 of C(H)• migrates to the N1 of G(−H)•; meanwhile, the proton at the N2 of G transfers to the O2 of C. This process is energetically viable; the corresponding activation energy is around 12−13 kcal/mol. The base-pairing energy of the triplet is found to be ∼3−5 kcal/mol smaller than that of the singlet state. Thus, the formation of the triplet state GC pair in DNA double strand only slightly weakens its stability. The obtained highly reactive radicals are expected to cause serious damage in the DNA involved in biochemical processes, such as DNA replication where radicals are exposed in the single strands.
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INTRODUCTION The triplet states of DNA base pairs represent reactive species because they might form diradical complexes. The formation of the triplet state of DNA bases is unlikely the direct result of the photoinduced excitation of the bases in their ground state. It is believed that the DNA bases in the excited electronic states have short lifetime (in ps), and instead of crossing to the more reactive triplet states directly, they quickly convert to the electronic ground state.1−9 This characteristic of the DNA bases was of particular importance in the protection of these bases against photochemical damages under the conditions of early stage of the earth, where biological species were exposed to the strong UV radiation.1 Other than direct ionization of the components of DNA, two important events are involved in the radioactive interactions of the DNA related biological systems: (1) the formation of the excited states of the DNA bases, and (2) the production of the secondary free electrons with low kinetic energy.10−18 Numerous investigations suggest that the DNA bases of pyrimidine type (thymine T and cytosine C) are readily capture an electron with low kinetic energy and are able to form relatively stable radical anions.19−28 The stability of these radical anions is further improved greatly when they are Hbonded with the corresponding DNA bases of the purine type (adenine A and guanine G).29−37 Depending on the wavelength, the photochemistry or radiation-induced electron © 2014 American Chemical Society
detachments of these anionic radical systems are expected to produce the paired DNA bases either in triplet states or in singlet states. The tautomerizations of the triplet state of GC pair have been explored at the different levels of theory, ranging from CASSCF, CAS-PT2, and the density functional theory (DFT).38,39 In these studies, direct singlet−triplet excitation from GC pair has been suggested as the possible pathway leading to the formation of the triplet state of the GC pair. In the present investigation, we study other previously unexplored, nevertheless possible, pathways of the formation of the reactive triplet state of GC pair in Watson−Crick (WC) canonical form. Experiments suggested that the stable radical anion does exist in the water molecule solvated photoelectron study of uracil, thymine, and cytosine, and nucleosides.40,41 In the GC pair, the strong H-bonding between G and C greatly improves the stability of the radical anion of cytosine as revealed in the previous studies.30,31 Therefore, it is reasonable to explore a possible pathway of the formation of the triplet state of GC pair Special Issue: Photoinduced Proton Transfer in Chemistry and Biology Symposium Received: July 23, 2014 Revised: October 14, 2014 Published: October 23, 2014 2454
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through the formation of the radical anion of GC pair (doublet) and then by detachment of a free electron from this radical anion through photoexcitation that leads to formation of the triplet state of GC pair. To mimic the GC pair in DNA, in models of the base pairs considered here, the N1 atom of cytosine and the N9 atom of guanine are methylated. This allows for elucidation of the characteristics of electronic structures of the triplet state of the WC paired GC complex that enriches our understanding of the radiation related DNA damage and repair mechanisms.38,39 Interestingly, the results of the present study also suggest that it is possible to control the yields of the GC pairs with different spin states through electron-photoexcitation experiments.
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Table 1. Electron Affinities of GC Pair (in eV) and the Electron Detachment Energies of the Radical Anions of GC Paira process GC + e → GC−• GC + e → G(−H)−C(H)• GC + e → GC−• GC + e → G(−H)−C(H)•
AEAb
process
Gas Phase 0.28; 0.44;e,f GC−• → GC + e g 0.36 0.40; 0.57;e G(−H)−C(H)• → GC + e 0.50g Aqueous Phase 1.91; 1.86h GC−• → GC + e 2.10 G(−H)−C(H)• → GC + e
VDEc
tVDEd
1.03; 1.16g 1.84; 2.09g
4.29
2.49 3.04
5.86 5.49
3.83
a
Energy values in the table are not corrected using the zero-point vibrational energy. bAEA = E(neutral, optimized) − E(anion, optimized). cVDE = [E(neutral, singlet) − E(anion)] based on the optimized anion structure. dtVDE = [E(neutral, triplet) − E(anion)] based on the optimized anion structure. eSee ref 48. fSee ref 36. gSee ref 37. hSee ref 49.
THEORETICAL METHODS
The recently developed Minnesota density functional M062X42−44 provides a computational approach suitable for the study of excited state species and radicals. The electron affinities of the five nucleobases evaluated by the M06-2X approach are close to those predicted by the G4 method.19 A recent benchmark exploration of the performance of timedependent DFT methods reveals that M06-2X is the best overall performing GH-mGGA functional among the 24 tested functionals.45 In the present study, the M06-2X functional and the valence double-ζ basis set, aug-cc-pVDZ, were used in the calculations. The Barone−Tomasi polarizable continuum model (PCM)46 with the standard dielectric constant of water (ε = 78.39) was applied 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, (adiabatic electron affinity) AEA = Eneut − Eanion at their respective optimized geometries. The Gaussian 09 system of DFT programs47 were used for all computations.
It is important to state that the electron vertical detachment energy (VDE) for the formation of singlet state of GC pair is computed to be 1.03 eV in the gas phase and 2.49 eV in aqueous solutions, respectively. On the other hand, the electron vertical detachment energy for the creation of the triplet state of GC pair (tVDE) is predicted to be significantly large: 4.29 eV in the gas phase and 5.86 eV in aqueous solutions, respectively. These large tVDE values indicate that the establishment of the triplet state of GC pair is viable when the system is exposed to the high-energy radiations. Moreover, the substantial differences between the VDE and tVDE suggest that in experiments, it is possible to control the formation of the triplet state of GC pair by adjusting the photo energy during the electron detachment procedures. As expected, relatively larger VDEs have been predicted in the present computational study for the distonic radical anion G(−H)−C(H)• pair, as compared with the normal radical GC anion (1.84 eV vs 1.03 eV in the gas phase and 3.03 eV vs 2.49 eV in aqueous solutions). However, the tVDE value of G(−H)−C(H)• pair is lower than that of GC−• pair in the gas phase (3.83 vs 4.29 eV) and in aqueous solutions (5.49 vs 5.86 eV). The triplet state seems to favor the G(−H)C(H) tautomeric form of the GC pair. Figure 1 summarizes the predicted relative energies of complexes along the pathway of the formation of the triplet state of GC pair. Photoinduced Electron Detachment. Upon recalling that the ionization potential of the guanine base is determined
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RESULTS AND DISCUSSION One of the possible pathways of the formation of the triplet state of GC pair follows two crucial steps: (1) the formation of radical anion of GC pair, and (2) photoinduced electron detachment from the radical anion of GC to its triplet state. The details of both steps have been carefully investigated in this study using a reliable computational approach. Formation of Radical Anion of GC Pair. Because different research groups have reported their results of studies on the formation of the radical anion of GC pair, here we only summarize our results briefly. The unpaired electron in the radical anionic GC pair resides on the cytosine moiety, as revealed by both the molecular orbital analysis and electron density analysis. The AEA of the GC pair in the WC form is calculated to be 0.28 eV in the gas phase and 1.91 eV in aqueous solutions (with M06-2X/aug-ccpVDZ approach, without zero point vibrational energy corrections). These values are ∼0.1−0.2 eV lower than those reported previously on the basis of studies with other functionals of the density functional theory.27 Interbase proton transfer from G (N1) to C (N3) further stabilizes the anionic GC radical (by 0.12 eV in the gas phase and by 0.19 eV in aqueous solutions), forming the distonic radical anion G(−H)−C(H)• pair, in which the charge-radical centers are separated. The activation barrier corresponding to this proton transfer process is evaluated to be 1.6 kcal/mol (0.07 eV) in the gas phase, and it is 1.1 kcal/mol (0.05 eV) in aqueous solutions.
Figure 1. Energy profiles for the electron attachment and detachment pathways toward the formation of the triplet state of GC pair. 2455
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Figure 2. Spin density of the triplet state of GC pair in the gas phase, GC2•(a), and in PCM modeled aqueous solutions, G+•C−• (b). The isovalue of the surface is 0.0004 au. All the excess α spin density resides on C in part a, signifying that the two unpaired electrons are localized on C, and that is indeed different from what is seen in part b.
to be 5 eV in the gas phase,50 the predicted tVDE value (4.29 eV) seems to imply that the detached electron is not likely from the guanine moiety in the gas phase. However, the value of tVDE (5.86 eV) in aqueous solutions suggests that for the formation of the triplet state, the electron detachment might take place on the guanine moiety. The analysis of the spin density of the triplet state of GC pair (obtained by vertically electron detachment) demonstrates that the vertical electron detachment originates from the radical anionic cytosine moiety in the gas phase, resulting in formation of the G(singlet)C(triplet) pair. In contrast, the electron is detached from G in aqueous solution, and this complex is, in fact, a H-bonded ionic base radical pair G+•C−• (Figure 2). GC Triplet. The vertical electron detachment-induced triplet state of the GC pair is energetically less favorable than that the formation of its tautomers. The energy analysis of the optimized triplet state geometry of the GC pair reveals that the subsequent structural relaxation after the photoinduced electron detachment leads to an energy release of 24.1 kcal/mol in the gas phase and of 21.8 kcal/mol in aqueous solutions. On examination of the structural features of the optimized structures of the triplet state of the GC pair, it is clear that the structure relaxation results in H transfer from N1 of G to N3 of C, both in the gas phase and in aqueous solutions (see Figure 3). Subsequent electron density analysis confirms that these geometrically optimized GC triplets represent G(−H)•C(H)• radical−radical pairs; therefore, the structure relaxation in the gas phase is accomplished by the H atom transfer from the
N1 of G to the N3 of the triplet state of C. In aqueous solutions, this is accompanied by the proton transfer from the N1 of G+• to the N3 of C−•. Large energy release during the structure relaxation suggests that this H transfer (or proton transfer) should be a barrier-free process. The H-bonding pattern of the G(−H)•C(H)• pair is depicted in Figure 3. The O6(G)−N4(C) distance (3.007 Å) of the triplet state is ∼0.23 Å longer than that of the singlet state GC pair (2.779 Å). On the other hand, the N2(G)− O2(C) bond distance of the triplet state is ∼0.13 Å shorter than that of the singlet state (2.773 vs 2.907 Å). In the third Hbond, N1(G)−N3(C), the bond distance is almost the same for the triplet and singlet states (2.939 vs 2.933 Å). A similar Hbonding pattern is found in the PCM optimized structures. The base pairing energy of the triplet GC pair is calculated to be 23.26 kcal/mol in the gas phase. For comparison, the pairing energy of the singlet state is 28.78 kcal/mol, and that of the radical anion GC−• is 40.86 kcal/mol. The influence of the polarizable medium reduces the base pairing energy significantly. The base pairing energy in aqueous solutions is evaluated to be 13.81 kcal/mol for the GC pair in the triplet state. This energy is 16.64 kcal/mol for the GC in the singlet state and 20.22 kcal/mol for the radical anion GC−•. Solvent effects reduce the pairing energies by stabilizing the separated base monomers. Tautomerism of GC Triplet. Double proton transfer between the monomers of the triplet state GC pair leads to the formation of its tautomeric form, G(N2−H)•C(O2H)• (see Figure 3). The details of transition state structure corresponding to this tautomerization indicate a double proton transfer process in which one proton at the N3 of C(H)• migrates to the N1 of G(−H)•; meanwhile, the proton at the N2 of G transfers to the O2 of C. This tautomer is found to be 9.39 kcal/mol higher in energy as compared with the normal triplet G(−H)•C(H)• radical−radical pair in the gas phase. Similarly, the tautomeric form in aqueous solutions is 10.41 kcal/mol above the normal form of the triplet GC pair. The activation barrier for the formation of the tautomer G(N2−H)•C(O2H)• is predicted to be 12.30 kcal/mol in the gas phase and 12.96 kcal/mol in aqueous solutions, respectively (see Figure 4). We conclude that both thermodynamics and kinetics favor the normal triplet state of G(−H)•C(H)• pair. The H-bonding pattern of the G(N2−H)•C(O2H)• pair shown in Figure 3 demonstrates that the bases are bonded more tightly in the tautomeric form than in the normal form of the triplet state GC pair. The O6(G)−N4(C) atomic distance (3.020 Å) of the G(N2−H)•C(O2H)• pair is close to that of the G(−H)•C(H)• pair (3.007 Å); however, the N2(G)− O2(C) distance of G(N2−H)•C(O2H)• is ∼0.10 Å shorter
Figure 3. Optimized structures of the singlet and triplet states of the GC pair. Atomic distances in angstroms. Plain font refers to the gas phase values, and bold is for the PCM aqueous solutions. Color: red for O, blue for N, gray for C, and white for H. Orange arrows represent the vibration mode with the single imaginary frequency in the transition state. 2456
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AUTHOR INFORMATION
Corresponding Authors
*E-mail:
[email protected]. *E-mail:
[email protected]. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS
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REFERENCES
Work in the U.S.A. was jointly supported by the NSF and the NASA Astrobiology Program under the NSF Center for Chemical Evolution, CHE1004570. We would like to thank the Mississippi Center for Supercomputing Research for a generous allotment of computer time.
Figure 4. Energy profiles along the pathway displaying formation of the triplet state of GC pair and its tautomer.
than that of the G(−H)•C(H)• (2.669 vs 2.773 Å). Moreover, N1(G)−N3(C) atomic distance is also ∼0.10 Å shorter in G(N2−H)•C(O2H)•, as compared with that in G(N2− H)•C(O2H)• (2.834 vs 2.939 Å). A similar H-bonding pattern is found in the PCM results. In the gas phase, the base pairing energy of the double proton transferred tautomer of the triplet state of GC pair is predicted to be 21.18 kcal/mol (compared with the separated G(N2−H)• and C(O2H)•). This is ∼2.08 kcal/mol less than that of the normal triplet state of GC pair (compared with the separated G(−H)• and C(H)•). However, this energy in the PCM modeled aqueous solutions is computed to be 17.25 kcal/ mol for the tautomer, ∼3.44 kcal/mol larger than that of the normal form. The polarizable environment stabilization effects for the monomers in the tautomeric form seems to be weaker, as compared with those in their canonical forms.
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CONCLUDING REMARKS The triplet state of the GC Watson−Crick pair can be formed through the following pathway: a low-energy electron is captured by cytosine in the GC pair, forming the cytosine base-centered radical anion GC− •. Interbase proton transfer may take place for this radical anion, forming the charge-radical center separated radical G(−H)−C(H)•. For the former radical anion, photoradiation with energy around 5 eV initiates the electron detachment from either cytosine (in the gas phase) or guanine (in aqueous solutions). This triggers interbase proton transfer from G to C, creating the triplet state of the GC pair. For the distonic radical, photoinduced electron detachment occurs directly at G, resulting in formation of the triplet state of the GC pair. Double proton transfer between the triplet state of GC pair leads to the formation of a less stable tautomer, G(N2−H)•C(O2H)•. This tautomerization is accomplished through a double proton transfer process in which one proton at the N3 of C(H)• migrates to the N1 of G(−H)•; meanwhile, the proton at the N2 of G transfers to the O2 of C. The above process is energetically viable, and the corresponding activation energy is ∼12−13 kcal/mol. The base-pairing energy of the triplet is found to be ∼3−5 kcal/mol smaller than that of the singlet state. Thus, the formation of the triplet state of GC pair in DNA double strand only slightly weakens its stability. However, as the DNA dissolves into single strands, both radical G and radical C will be exposed, and these highly reactive radicals are expected to cause serious damage in the DNA involved biochemical process. 2457
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