38. Inter-basepair Hydrogen Bonds in DNA
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1 190 Proc. Japan Acad., 70, Ser. B (1994) [Vol. 70(B), 38. Inter-basepair Hydrogen Bonds in DNA By Masashi SUZUKI*),t) and Naoto YAGI**) (Communicated by Setsuro EBASHI, M. J. A., Dec. 12, 1994) Abstract: Inter-basepair H-bonds in DNA are examined in the light of some crystal structures. An inter-basepair bond can be made on the major groove side from a C; base to the Wi+1 base. Such a bond can bridge two bases in CC/GG, CA/TG, AC/GT, and A _A/TT steps. Inter-basepair H-bonds can stabilise different conformations of the basepair steps depending on the DNA sequences, and thereby can determine particular superstructures of DNA. Key words: DNA structure; DNA superstructure; propeller twist; DNA-protein interaction. Different types of inter-basepair H-bonds. Hydrogen bonds between two neighboring basepairs are found in crystal structures of DNA. Importance of such a bond has been pointed out by Nelson et al. 1) in the context of understanding high propeller twisting of bases in an oligo(da):oligo(dt) tract. Each T base in such a tract pairs not only with its normal partner A base but also with another A base neighboring the A; T(C1) to A(Wi+1) (Figs. la, 2a, see also Fig. 3a for the Watson[W]-Crick[C] notation of the two DNA strands). This is achieved by introducing negative propeller twist of about -20 degree. The same type of H-bonds are found in other oligo(da):oligo(dt) tracts.2the distance of an inter-basepair H-bond in these structures is generally larger than that of an intra-basepair H-bond and thus the inter-basepair H-bonds are weaker. Inter-basepair H-bonding, however, is found not only in oligo(da):oligo(dt) tracts. Timsit et a1.5~ has reported that in the crystal structure of d(accggcgccaca): d(tgtggcgccggt), at the both ends, the Watson-Crick basepairs are broken and the bases pair with the ones neighboring the normal partners-i.e. C; pairs W;+1 (Figs. lc, 2c, note that inter-basepair H-bonds are made at both ends of the DNA, where one strand is composed of A and C bases and the other strand is composed of T and G, while in the centre, where the two strands have mixed sequences, only normal Watson-Crick basepairs take place, Figs. lc, 2c). A DNA complex with a protein, CAP, has been crystallised by Schultz et a1.6~ At two TG identical steps in the DNA the T bases (C;) make inter-basepair H-bonds to the C bases (Wi+1) in the neighboring basepairs. This is not mentioned in the original paper6~ but we have identified the bonds by using the crystal coordinates. The two neighboring basepairs, T:A and G:C, are kept normal and an inter-basepair H-bond between T and C is coupled with high rolling (by 35 degree) and untwisting (the helical twist angle is 22 degrees, which is much smaller than the normal 36 degree twist) of the two pairs relative to each other (Figs. lb, 2b). Inter-basepair bonds on the major groove side. Despite the apparent differences in the above three examples of inter-basepair H-bonds, if these are closely examined, one will *) MRC Laboratory of Molecular Biology, Hills Road, Cambridge CB2 2QH, U/K. **) Tohoku University, School of Medicine, Seiryo-machi, Sendai , Japan. t) Correspondence to: M. Suzuki.
2 No. 10] Inter-basepair H-bonds 191 Fig. 1. Examples of inter-basepair H-bonds (found in the Nelson, a, Scultz, b, and Timsit, c, structures) and the features used for intra or inter-basepair H-bonds in the C:G and T:A basepairs (d). (a-c) The structures are shown from the major groove side. Intra-basepair H-bonds and inter-basepair H-bonds are shown with dotted lines (...) and broken lines (-----), respectively. (d) H-bonds are numbered, 1-3, from the major (M) groove side towards the minor (m) groove side. The double helix axis is marked (x). notice some common features. These inter-basepair H-bonds are made on the major groove side. When the chemical features which can be used for intra or inter-basepair H-bonding are numbered, l from the major groove side (Fig. id), all the inter-basepair H-bonds mentioned above are made between features 1 of the two bases on the major groove side. This can be explained by the fact that the double helix axis of DNA is closer to features 1 than to features 3. If basepairs in DNA are looked down the DNA helix axis, one will notice that features 1 of the two neighboring basepairs are closer, while features 3 are less so, since the basepairs rotate from each other around the helix axis, because features 1 are close to the centre of rotation while features 3 further away. Since the A and C bases
3 192 M. SUZUKI and N. YAGI [Vol. 70(B), Fig. 2. H-bonding patterns in the Nelson (a), Schultz (b) and Timsit (c) structures. The parts shown in Fig. 1 are marked [ ]. Inter-basepair H-bonds are shown with arrows. In (b) at the TG step DNA is sharply bent (marked my ). In (c) inter-basepair H-bonds are made by using features 1, while intra-basepair H-bonds are made by using features 3. have H-bond donors as features 1, and the T and G bases have H-bond acceptors, an inter-basepair H-bond can be made only when C and A bases are positioned on the same strand, and T and G bases on the other, such as in CC/GG, CAITG, AC/GT, AA/TT. An inter-basepair H-bond on the major groove side takes place between C; and W;+1 (Fig. 3b) but not between Ci+1 and W, (Fig. 3c); the C1-W+1 distance is generally smaller than the C;+1-W; distance in a right-handed DNA.7~ In a left-handed DNA C,+1 and W; might be bridged. Propeller twisting. An A:T basepair of the normal Watson-Crick type has two H-bonds, while a G:C basepair has three. This causes differences in the ways that the two pairs use propeller twisting for inter-basepair H-bonding. The A:T pairs in the Nelson structure make inter-basepair bonds by high propeller twisting but keep normal inter-basepair H-bonds intact. Such propeller twisting is difficult for a G:C basepair, which has a more extensive flat plane fixed by the three bonds. Instead, the G:C basepair in the CAP structure rolls against the neighboring A:T basepair keeping normal planality When inter-basepair H-bonds become stronger, the A and T bases in a pair might not maintain normal intra-basepair H-bonds any longer, as is seen in the Timsit structure (Fig. lc). But in the same structure shown in Fig. 2c two G:C pairs maintain an intra-basepair H-bond between features 3, using features 1 for inter-basepair H-bonds (Fig. 2c). This can be understood since a G:C pair has H-bond 3 which is close to the sugar phosphate backbones, which can be used as the pivot of propeller twisting, while A:T does not have such a bond (note also that the major groove side of a basepair becomes more widely open
4 No. 10] Inter-basepair H-bonds 193 Fig. 3. Different types of inter-basepair H-bonds. (a) The Watson-Crick notation of base positions. The bases are looked from the major (M) groove. (b, c) In a right-handed DNA C; and W;+1 can be bridged by a H-bond, while in a left-handed DNA C;+1 and W; might be bridged. (d-f) Geometry of the UY, YY/UU, and YU steps. The separation between the pairing surfaces of the two neighboring basepairs (shown with a pair of arrows) is dependent on the three types of base steps. (g, h) Propeller twisting around H-bond 2. (i, j) Propeller twisting around H-bond 3. Note that the opening of the neighboring basepairs on the major groove side is wider in (i, j) than in (g, h). with the same propeller twist angle in G:C than in A:T, Figs. 3g j). Rolling. To make an inter-basepair H-bond on the major groove side, positive roll but not negative roll needs to be introduced so that features 1 become closer. The sugar-phosphate linkage of two consecutive bases is about 7 A and is much longer than the stacking distance of the two bases (about 3 A). It is therefore easier to introduce positive roll by widening the separation of the two bases on the minor groove, and keeping Van der Waals contacts of the bases on the major groove, rather than to introduce negative roll by keeping Van der Waals contacts on the minor groove side and forming an inter-basepair H-bond there. Sliding. As has been pointed out by Calladine8 and Dickerson9~ some characteristics of DNA structures can be understood in terms of the positioning of the purine (U-A, G) and pyrimidine (Y-T, C) bases. At a YY/UU step features 1 in the two bases are not far away from each other (Fig. 3e). Therefore, by small and negative sliding, an inter-basepair bridge can be made. This occurs at the AA/TT steps in the Nelson structure. But at a UY step, more significant and negative sliding becomes necessary (Fig. 3d). At a YU step, moderate and positive sliding seems to be necessary (Fig. 3f). Indeed, the T and G steps in
5 194 M. SUZUKI and N. YAGI [Vol. 70(B), the CAP structure slide to each other in the expected direction (by 1.3 A). Helical twisting. In the CAP structure the two TG steps are largely untwisted. This untwisting aligns the edges of the neighboring basepairs on the major groove side, which makes the inter-basepair H-bond possible. The two edges open wider on the major groove at a YU step, more parallel at YY/UU, and most parallel at UY. Thus untwisting is likely to be coupled with an inter-basepair H-bond at a YU step (such as TG) but less so at a UY step. DNA superstructure. Inter-basepair H-bonds seem to be used for stabilising particular DNA superstructures. In the Nelson structure because of the tight network of H-bonding, the DNA becomes straight and is believed to be inflexible. 1) In contrast, the TG steps in the CAP structure roll considerably and this causes sharp bending of the DNA double helix towards the major groove at the steps. We have discussed some stereochemical principles of inter-basepair H-bonding in DNA in this paper. Any base sequence can adopt perhaps more than one conformation in different circumstances. But a DNA sequence will have a preference for adopting a particular conformation, and knowing of this preference is important for understanding the sequence-structure correlation in DNA. The preferred conformation is likely to be used when DNA adopts a particular superstructure on binding around a protein surface and the inter-basepair H-bonds discussed in this paper should be borne in mind for understanding the preference. Acknowledgements. We thank Dr M. Gerstein and Mr M. ElHassan for their help for calculating the DNA parameters. We thank Dr. J. Finch for his critical reading of the manuscript. References 1) 2) 3) 4) 5) 6) 7) 8) 9) Nelson, H. C. M. et al. (1987): Nature, 330, Coll, M, et al. (1987): Proc. Natl. Acad. Sci. U.S.A., 84, Yoon, C. et al. (1988): ibid., 85, DiGabriele, A. D., Sanderson, M. R., and Steitz, T. A. (1989): ibid., 86, Timsit, Y., Vilbois, E., and Moras, D. (1991): Nature, 354, Schultz, S. C., Shields, G. C., and Steitz, T. A. (1991): Science, 253, Suzuki, M. (1994): Structure, 2, Calladine, C. R. (1982): J. Mol. Biol., 161, Dickerson, R. E. (1983): ibid., 166,
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