Na+, Mg2+, and Zn2+ Binding to All Tautomers of Adenine, Cytosine

J. Phys. Chem. B 2006, 110, 14515-14523

14515

Na+, Mg2+, and Zn2+ Binding to All Tautomers of Adenine, Cytosine, and Thymine and the Eight Most Stable Keto/Enol Tautomers of Guanine: A Correlated ab Initio Quantum Chemical Study Martin Kabela´ cˇ and Pavel Hobza* Institute of Organic Chemistry and Biochemistry, Academy of Sciences of the Czech Republic, and Center for Complex Molecular Systems and Biomolecules, 166 10 Prague 6, Czech Republic ReceiVed: April 11, 2006

Interactions of adenine, cytosine, guanine, and thymine with Na+, Mg2+, and Zn2+ cations were studied using an approximate resolution of identity correlated second-order MP2 (RI-MP2) method with the TZVPP ([5s3p2d1f/3s2p1d]) basis set. All existing tautomers of adenine, cytosine, and thymine and the eight most stable keto/enol tautomers of guanine were considered. Cations bind mostly in a bidentate manner, and stabilization energies of these complexes are larger than those in the case when cations bind in a unidentate manner. The cation‚‚‚Y (Y equal to N or O) distances for divalent metals are shorter than those for Na+ and for Zn2+ are mostly shorter than the Mg2+‚‚‚Y distance. The intermolecular distances between the cation and the base for complexes containing adenine and cytosine are systematically shorter than those for complexes containing guanine and thymine. Only for cytosine the canonical keto/amino tautomer structure with ions represents the global minimum. For guanine, the metalated canonical form is again the most stable, but its stabilization energy is within less than 5% of the stabilization energies of the two other rare tautomers, which indicates that the canonical form and these two rare tautomers could coexist. The canonical structures of adenine and thymine in the presence of ions are considerably less stable (by more than 10%) than the complexes of the rare tautomers. It can be concluded that the interaction of Na+, Mg2+, and Zn2+ cations with cytosine in the gas phase will not induce the change of the canonical form to the rare tautomeric form. In the case of isolated guanine, the equilibrium of the canonical form with rare tautomers can be found. For isolated adenine and thymine the presence of rare tautomers is highly probable.

Introduction Metal ions play an important role in biological processes by forming noncovalent bonds, and they act as nonspecific binders as well.1 In DNA they interact dominantly with phosphate groups and thus neutralize their negative charges, which contributes to the stabilization of the helix. Neutralization of the phosphate negative charge can be also realized when ions interact with nucleic acid (NA) bases, and in this case, a zwitterionic form of bases can appear. While the alkali metals prefer positions binding to the phosphate groups, transition metal ions are more frequently localized near bases.1 The presence of metal ions near bases can strongly affect the electron distribution in the bases and thus also the tautomeric equlibria. In other words, the effect of the metal ions can favor the formation of the rare tautomers, which are believed to be involved in various biochemical processes including point mutation.1 Tautomeric equilibria of NA bases in a vacuum and in a microhydrated environment as well as interactions of bases with ions have been studied frequently, and we are going to mention here only the recent studies.2-43 Since the NA bases are strongly polar, water might play an important role in their stabilization and can dramatically change the relative stabilities of various tautomers. For example, unusual tautomers of guanine being strongly destabilized in a vacuum become stabilized in an aqueous environment.35 When the NA base reacts instead * Author to whom correspondence should be addressed. Fax +420 220 410 320. E-mail: [email protected].

with water with a metal cation, the preference of the unusual tautomer can be even more pronounced. The aim of the present paper is to study the interactions of Na+, Mg2+, and Zn2+ ions with NA bases. The interaction energies of these ions with bases are very large and can thus dramatically affect the tautomeric equilibria. This concerns also rare unusual tautomers, which are strongly unfavored (by several to tens of kcal/mol) over the most stable tautomer in a vacuum. It is thus not advisable to consider only the most stable tautomer or several tautomers (as is mostly done), but instead, all tautomers should be taken into account. In the present study we consider, for the first time, the interaction of the selected cations mentioned above with the 14 amino/imino tautomers of adenine, the 13 amino/imino/keto/enol tautomers of cytosine, the 13 keto/enol tautomers of thymine, and the 8 most stable keto/enol tautomers of guanine. Except for guanine, where 46 different tautomers exist,28 all possible tautomers of the remaining nitrogenous bases were taken into account. Methods Starting geometries of complexes containing a nitrogeneous base and a cation were generated using the program MOLDEN.44 All possible planar sigma complexes of the cation with donor atoms (nitrogens and oxygens) were considered, and they are shown in Figures 1-4. Cations were located mostly between two donor atoms, but in some cases an interaction with just one donor atom was possible.

10.1021/jp062249u CCC: $33.50 © 2006 American Chemical Society Published on Web 07/04/2006

14516 J. Phys. Chem. B, Vol. 110, No. 29, 2006

Kabelaćˇ and Hobza

Interactions of Nucleic Acid Bases with Cations

J. Phys. Chem. B, Vol. 110, No. 29, 2006 14517

Figure 1. Schematic drawings of the optimized structures of metalated adenine (a). A position of the ion is symbolized by a cross. Each structural code covers the tautomeric form of the base and also information on the binding site(s) and the stabilization energies in kcal/mol for Na+, Mg2+, and Zn2+ complexes in this order. The relative stability of the tautomers in respect to the canonical form (the first set structures for each base, i.e., a9, c1, g19, t1) can be found next to the right edge of the picture. A letter “a” above the energy value means that the geometry of the amino group was distorted. The letters “b” and “c” instead of energy values mean that orientation of the NH or OH group, respectively, was changed during the optimization to the another rotameric form giving the same results as the second rotameric structure.

The structures of stationary points were determined by a gradient optimization using an approximate resolution of identity MP2 (RI-MP2) method45,46 with Ahlrichs’ TZVPP ([5s3p2d1f/ 3s2p1d]) basis set. The stabilization energies were corrected for the basis set superposition error (BSSE)47 and the deformation energies of the nitrogeneous base. The frozen-core approximation was applied throughout this study. In this work the zero-point vibration energies as well as entropies were not included, because in previous studies34-37 on tautomeric equilibria of cytosine, guanine, adenine, and thymine it had been shown convincingly that the relative energies agree closely with relative enthalpies as well as free energies. The higher correlation energy contributions were not covered, since the present stabilization energies are very high and their relative values will be affected by the higher correlation energy contributions only marginally. All the calculations were carried out using the TURBOMOLE 5.6 program suite.48 Results and Discussion The final interaction energy data (covering deformation energy and BSSE correction) are shown in Figures 1-4 where, after description of the tautomer and binding motif, the three numbers associated with each structure give relative interaction energies (in kcal/mol) for Na+, Mg2+, and Zn2+ complexes. The relative tautomers’ energies are depicted at the right edge of Figures 1-4. The relative stabilities of the tautomers agree well with these obtained in our previous papers at higher theoretical levels (CCSD(T)).34-37 The standard atom numbering of each base can be found in Figure 5. The binding distances of the cations and a more detailed description of the energetical characteristics of the binding of ions can be found in Table 1S of the Supporting Information. The interaction energies of the most stable complexes with the cations investigated are large, which is especially true for divalent cations, where the stabilization energies exceeded 150 kcal/mol. The stabilization energies of Mg2+ ion are about 5 times larger than those of Na+, and even larger stabilization energies were found for the interaction with Zn2+. The energy difference with respect to Mg2+ is about 35 kcal/mol and should be ascribed to the partially covalent character of the bonding.

For other tautomers, we found that the order of stability is systematically the same, i.e., Na+ < Mg2+ < Zn2+, and the difference between single ions remains practically unchanged. The position of an ion in the global minimum of the particular tautomer remains the same; i.e., the ions favor the same binding site independently of the type of ion. The ion binding motifs of each of the NA bases will now be discussed separately. Adenine. In the case of the canonical tautomer a9, the global minimum structure favors the binding of cations in the bidentate position between the N6 and N7 atoms (N6‚‚‚X+‚‚‚N7). Here, as well as in other structures, the amino group is distorted from the original position, allowing a direct interaction of the ion with the nitrogen lone pairs of the amino group. When the ion interacts with the N1 and N6 atoms, a similar effect occurs, but the stabilization energies are smaller. The smallest stabilization energies were found when the ion interacted with a single acceptor only (i.e., the N3 atom). The a1 tautomer does not allow the distortion mentioned above, since it is hindered by the N1-H hydrogen. The most preferred binding site is in this case N3‚‚‚ X+‚‚‚N9, characterized by large stabilization energy. Considering, however, the tautomer penalization energy (18 kcal/mol), we obtain smaller values of the total stabilization energy than in the canonical form. For the a3 tautomer the most preferred binding site for Na+ corresponds to the N9 position, as is shown in Figure 1. When, however, passing to divalent cations, the N7‚‚‚X+ complexes become more stable, since the amino group distorts, thus allowing better interaction of the cations with the amino nitrogen (Table 1S). Since the penalization energy of this tautomer is only 8 kcal/mol, the resulting final stabilization energies (i.e., stabilization energies also taking into account the difference of stability of the tautomers with respect to the canonical tautomer) are almost as large as in the case of the canonical structure. In the case of the a7 amino and a17r,l imino tautomers the bidentate N3‚‚‚X+‚‚‚N9 position is available, and the global minima of all three tautomers correspond to this motif. Since the penalization energy of the a7 tautomer is modest, the final stabilization energies found for the metalated complexes of this tautomer are for all ions studied larger than that of the canonical structure.





Figure 2. Schematic drawings of the optimized structures of metalated cytosine (c). A position of the ion is symbolized by a cross. Each structural code covers the tautomeric form of the base and also information on the binding site(s) and the stabilization energies in kcal/mol for Na+, Mg2+, and Zn2+ complexes in this order. The relative stability of the tautomers in respect to the canonical form (the first set structures for each base, i.e., a9, c1, g19, t1) can be found next to the right edge of the picture. A letter “a” above the energy value means that the geometry of the amino group was distorted. The letters “b” and “c” instead of energy values mean that orientation of the NH or OH group, respectively, was changed during the optimization to the another rotameric form giving the same results as the second rotameric structure.

For the a19l tautomer we found that the presence of divalent ions led to the change of the orientation of the imino group to another rotameric form of the tautomer. The sodium cation is not strong enough for making such a change. This observation is quite general for all bases where this change can occur; the same conclusion can be even made for rotation of the OH group of the rare tautomers of thymine. The metalated a19r tautomer exhibits the largest interaction energy (at the bidentate position N6‚‚‚X+‚‚‚N7) among all adenine complexes. Since its deformation, as well as penalization energies, are not too high, the final stabilization energy is the largest for all the ions as well. We must thus expect that binding of an ion to the N6‚‚‚X+‚‚‚N7 position will change the tautomeric equilibrium in favor of the a19r tautomer in comparison with the canonical a9 form preferred in a vacuum. The a37l tautomer possesses the same binding motif as the a19r one, which is again characterized by large stabilization energies. Since its penalization energy is larger than that of a19r, the final stabilization energy became smaller. Nevertheless, the participation of the imino nitrogen in the binding of the cation in both these very stable structures seems to be essential. This is fully confirmed in the a39 tautomer, which has identical binding motifs. All these structures exhibit unusually large stabilization energies, much larger than those of the canonical form. Larger penalization energies, however, lower the final stabilization energies of these tautomers. The a79 tautomers possess a zwitterionic structure characterized by a large dipole moment and by very high tautomeric penalization energy. It is thus not surprising that the largest stabilization energy for all the ions was detected for this tautomer having the N1‚‚‚X+‚‚‚N6 binding motif. A substantial penalization energy of about 50 kcal/mol causes the final stabilization energy (being still larger than that of the canonical tautomer) to be the third largest after the a19r and a39r metalated tautomers. This tautomer represents an example that even the rare unusual tautomers having large penalization energies should be considered. Cytosine. In general, cytosine has fewer available binding positions than adenine, as can be deduced from Figure 2. For most binding motifs only two minima were located. For the canonical tautomers, only one metalated structure can be found, and it corresponds to the O2‚‚‚X+‚‚‚N3 position. The deformation energy is smaller than that for adenine, and it is valid also for the other tautomers of cytosine. Figure 2 and Table 1S show that in the case of cytosine the largest stabilization energies were found for the canonical structure, which is in sharp contrast to

adenine, where as many as five other structures containing rare tautomeric forms of the bases have larger stabilization energies than the canonical structure. The stabilization energy of the Na+ cation with the canonical structure of cytosine is remarkably large, and no other tautomers possess such a stabilization energy in more than the 10% stabilization energy limit. The O2‚‚‚X+‚ ‚‚N3 motif occurs also in the cases of the co2r and the cn4r enol tautomers, in which the presence of the enolic oxygen explains the fact that the respective stabilization energies are smaller than that in the canonical keto form. The similar O2‚ ‚‚X+‚‚‚N1 motif was found in the metalated c1o2l tautomer and in both cbn4 tautomers. The imino N‚‚‚X+‚‚‚ring N binding motif was localized as a global minimum in the cn4lo2 tautomers, in which the cn4lo2r N3‚‚‚X+‚‚‚N4 structure possesses the highest stabilization energy. These stabilization energies are the highest among all cytosine tautomers (including the canonical form). However, due to the very high unstability of these tautomers themselves the final stabilization energies are smaller than those of the canonical form. Guanine. Contrary to the other NA bases, here we studied only the eight most stable tautomers. Similarly as in the case of cytosine the canonical form is characterized by the highest stabilization energies. The surprisingly large stabilization energy of the canonical form with the sodium cation should be mentioned. Total stabilization energies of the g39 and g79 tautomers with divalent cations are comparable to those of the canonical form, but their stabilization energies with the sodium cation are considerably lower (by about 15%). By investigating the stabilization energies of the metalated guanine complexes shown in Figure 3 and Table 1S corrected by tautomeric penalization, we found higher values in the case of the canonical form than those for the g39 and g79 complexes. The large penalization energies of these tautomers cause them to possess only the second and third highest total stabilization energies. It should be, however, mentioned that the energy differences between these three tautomers are small, and their coexistence can be thus expected.35 Our findings fully agree with experimental results33 showing an unexpected stabilization of the g79 tautomer over the canonical one upon the interaction with the aluminum atom. Similar results supporting this finding were found in our previous paper studying the guanine tautomeric equilibria in the aqueous phase. All three forms mentioned possess the O6‚‚‚X+‚‚‚N binding motif (which is also present in the fourth most stable tautomer), and only the fifth and sixth most stable tautomers show the N3‚‚‚X+‚‚‚N9 binding motif.



Figure 3. Schematic drawings of the optimized structures of metalated guanine (g). A position of the ion is symbolized by a cross. Each structural code covers the tautomeric form of the base and also information on the binding site(s) and the stabilization energies in kcal/mol for Na+, Mg2+, and Zn2+ complexes in this order. The relative stability of the tautomers in respect to the canonical form (the first set structures for each base, i.e., a9, c1, g19, t1) can be found next to the right edge of the picture. A letter “a” above the energy value means that the geometry of the amino group was distorted. The letters “b” and “c” instead of energy values mean that orientation of the NH or OH group, respectively, was changed during the optimization to the another rotameric form giving the same results as the second rotameric structure.

Thymine. Similarly to cytosine, thymine possesses fewer binding motifs than both purines. Contrary to cytosine, the canonical structure of thymine with ions represents the sixth local minimum, which means that the six complexes of the rare tautomers with ions have higher stabilization energies. Figure 4 shows an explanation: The canonical thymine has only the unidentate binding sites available. It is important to mention that the most favorable structure of the metalated rare tautomer exceeds the canonical form by as much as 20 kcal/mol. Only the cases of the Na+ cation canonical and rare tautomer complexes have similar stabilization energies. The stabilization energies of thymine complexes are considerably smaller than these of adenine and cytosine, and in fact the final stabilization energies generally never exceed 190 kcal/mol. The largest stabilization energies were found for the t3o2r, t1o4, and t3o4l

tautomers, all exhibiting the N‚‚‚X+‚‚‚O binding sites. The largest total stabilization energy was found for the t3o4l tautomer due to the smallest penalization energy. All the most stable tautomers possess the carbonyl O‚‚‚ring N binding motif. This motif is evidently more stable than the hydroxyl O‚‚‚ring N motif. Due to the presence of the two oxygens and the two adjacent nitrogens there exists a rather large number of possibilities for the N‚‚‚X+‚‚‚O binding types, and it also explains why as many as six rare tautomers exhibit larger stabilization energies than the canonical form. However, neither of the thymine tautomers exhibit the N‚‚‚X+‚‚‚N bonding motif known from both purines as well as from cytosine. The bidentate motifs are clearly preferential for the interaction of divalent cations, but this is not the case for the sodium cation. The total stabilization energies of the canonical form and two rare





Figure 4. Schematic drawings of the optimized structures of metalated thymine (t). A position of the ion is symbolized by a cross. Each structural code covers the tautomeric form of the base and also information on the binding site(s) and the stabilization energies in kcal/mol for Na+, Mg2+, and Zn2+ complexes in this order. The relative stability of the tautomers in respect to the canonical form (the first set structures for each base, i.e., a9, c1, g19, t1) can be found next to the right edge of the picture. A letter “a” above the energy value means that the geometry of the amino group was distorted. The letters “b” and “c” instead of energy values mean that orientation of the NH or OH group, respectively, was changed during the optimization to the another rotameric form giving the same results as the second rotameric structure.

the case of isolated guanine the coexistence of the canonical form with the rare tautomers will not exclude such a change, while this is probable in the cases of isolated adenine and thymine. We are aware that the conclusions made concern the thermodynamic and not kinetic equilibria and the structure and the energetics of the saddle points are required, which will be the aim of our future projects. Figure 5. Standard atom numbering of the canonical form of base adenine (a), cytosine (c), guanine (g), and thymine (t).

tautomers with the sodium cation are comparable (within 1 kcal/ mol). It must be, however, mentioned that the corrected stabilization energies of these rare tautomers are considerably higher and only due to their large penalization energies the final stabilization energies are comparable. Conclusions The cations interact mostly in a bidentate manner with NA bases. The stabilization energies in these cases are larger than those when ions bind in a unidentate manner. The cation‚‚‚Y (Y ) N or O) distances are for the divalent cations shorter than those for sodium, and these distances for Zn2+ are mostly shorter than the Mg2+‚‚‚X ones. The intermolecular distances for the complexes containing adenine and cytosine are systematically shorter than those for complexes containing guanine and thymine. The largest stabilization energies belong to the adenine a19r rare tautomer and the guanine canonical complexes. The Zn2+ stabilization energies are systematically the largest, and the partial covalent character of the bonding can be considered. Both of the divalent cations exhibit considerably larger stabilization energies than the sodium cation. The deformation energies for the divalent cations are again systematically larger than these of sodium, and the largest deformation energies were found for adenine. The canonical structure doubtlessly represents the global minimum only in the case of cytosine. In the case of guanine the canonical is again the most stable, but its stabilization energy is within less than 5% of the stabilization energies of the two other rare tautomers, which indicates that the canonical form and these two rare tautomers could coexist. The canonical structures of adenine and thymine are considerably less stable (by more than 10%) than their unusual tautomers. It must be thus concluded that the interaction of Na+, Mg2+, and Zn2+ cations with isolated (gas-phase) cytosine will not induce any change of the canonical form to the rare tautomeric form. In

Acknowledgment. This work was a part of research project Z40550506 of the Institute of Organic Chemistry and Biochemistry, Academy of Sciences of the Czech Republic, and it was supported by Grants LC512 (Ministry of Education of the Czech Republic), 203/05/009 (P.H.), and KJB400550518 (M.K.) from the Grant Agency of the Czech Republic. Supporting Information Available: Geometries and interaction energies of adenine, cytosine, guanine, and thymine with Na+, Mg2+, and Zn2+ ions. This material is available free of charge via the Internet at http://pubs.acs.org. References and Notes (1) Saenger, W. Principles of Nucleic Acid Structure; SpringerVerlag: New York, 1983. (2) Hobza, P.; Sˇ poner, J. Chem. ReV. 1999, 99, 3247. (3) Sˇ poner, J.; Leszczynski, J.; Hobza, P. Biopolymers 2002, 61, 3. (4) Fogarasi, G. J. Mol. Struct. 1997, 413, 271. (5) Aleman, C. Chem. Phys. 2000, 253, 13. (6) Les, A.; Adamowicz, L.; Bartlett, R. J. J. Phys. Chem. 1989, 93, 4001. (7) Estrin, D. A.; Paglieri, L.; Corongiu, G. J. Phys. Chem. 1994, 98, 5653. (8) Ha, T. K.; Keller, H. J.; Gunde R.; Gunthard, H. H. J. Phys. Chem. A 1999, 103, 6612. (9) Russo, N.; Toscano M.; Grand, A. J. Phys. Chem. B 2001, 105, 4735. (10) Russo, N.; Toscano, M.; Grand, A. J. Am. Chem. Soc. 2001, 23, 10272. (11) Nowak, M. J.; Lapinski, L.; Fulara, J. Spectrochim. Acta, Part A 1989, 45, 229. (12) Fogarasi, G. J. Phys. Chem. A 2002, 106, 1381. (13) van Mourik, T.; Benoit, D. M.; Price, S. L.; Clary, D. C. Phys. Chem. Chem. Phys. 2000, 2, 1281. (14) Clary, D. C.; Benoit, D. M.; van Mourik, T. Acc. Chem. Res. 2000, 33, 441. (15) Kobayashi, R. J. Phys. Chem. A 1998, 102, 10813. (16) Sambrano, J. R.; Souza, A. R.; Queralt, J. J.; Andre´s, J. Chem. Phys. Lett. 2000, 317, 437. (17) Kryachko, E. S.; Nguyen, M. T.; Zeegers-Huyskens, T. J. Phys. Chem. A 2001, 105, 1288. (18) Kryachko, E. S.; Nguyen, M. T.; Zeegers-Huyskens, T. J. Phys. Chem. A 2001, 105, 1934. (19) Chandra, A. K.; Nguyen, M. T.; Zeegers-Huyskens, T. J. Mol. Struct. 2000, 519, 1. (20) Colominas, C.; Luque, F. J.; Orozco, M. J. Am. Chem. Soc. 1996, 118, 6811.

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Na+, Mg2+, and Zn2+ Binding to All Tautomers of Adenine, Cytosine

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