Abstract
Interstrand purine-purine stacks originate from tandem sheared purine•purine pairing and represent one of the most important motifs in both DNA and RNA structures. Several RNA and DNA structures, solved recently in both solution and the solid state, contain these special motifs, which greatly increase the structural diversity of nucleic acid molecules. The direct evidence for the sheared purine-purine pairing at neutral pH in solution remains, however, elusive. In this manuscript, we have used high resolution NMR methods to study a series of symmetrical DNA duplexes containing two non-symmetrical 5′-(PuGAPu)/(PyGAPy)-3′ motifs. Many strong- and medium-strength NOEs across the G•A base pair were detected in the H2O-NOESY spectra collected at a relatively low temperature (−5 °C ). These NOEs, especially those from A-6NH2 to G-H1′, G-H4′, and G-2NH2, clearly define the proposed side-by-side sheared G•A pairing nature. Another interesting feature is the strong NOEs exhibited by the unpaired G-imino proton in the G•A pair to its own G-2NH2, which implies that G-2NH2 is involved in H-bonding with a base in the minor groove edge. The finding that non-symmetrical (PuGAPu):(PyGAPy) motif also form similarly stable structures loosens the requirement for a more restricted (PyGAPu)2 motif in forming the interstrand purine-purine stacks.
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Altona, C. (1982) Recl. Trav. Chim. Pays-Bas, 101, 413–433.
Cate, J.H., Gooding, A.R., Podell, E., Zhou, K., Golden, B.L., Kundrot, C.E., Cech, T.R. and Doudna, J.A. (1996) Science, 273, 1678–1685.
Cheng, J.-W., Chou, S.-H. and Reid, B.R. (1992) J. Mol. Biol., 228, 1037–1041.
Chou, S.-H., Cheng, J.-W., Fedoroff, O. and Reid, B.R. (1994a) J. Mol. Biol., 241, 467–479.
Chou, S.-H., Cheng, J.-W. and Reid, B. (1992) J. Mol. Biol., 228, 138–155.
Chou, S.-H., Flynn, P. and Reid, B. (1989) Biochemistry, 28, 2422–2435.
Chou, S.-H., Hare, D.R., Wemmer, D.E. and Reid, B.R. (1983) Biochemistry, 22, 3037–3041.
Chou, S.-H. and Tseng, Y.-Y. (1999) J. Mol. Biol., 285, 41–48.
Chou, S.-H., Tseng, Y.-Y. and Wang, S.-W. (1999) J. Mol. Biol., in press.
Chou, S.-H., Zhu, L., Gao, Z., Cheng, J.-W. and Reid, B.R. (1996) J. Mol. Biol., 264, 981–1001.
Chou, S.-H., Zhu, L. and Reid, B.R. (1994b) J. Mol. Biol., 244, 259–268.
Chou, S.-H., Zhu, L. and Reid, B.R. (1997) J. Mol. Biol., 267, 1055–1067.
Correll, C.C., Freeborn, B., Moore, P.B. and Steitz, T.A. (1997) Cell, 91, 705–712.
Crook, S.T. and Bennett, C.T. (1996) Annu. Rev. Pharmacol. Toxicol., 36, 107–129.
Dallas, A. and Moore, P.B. (1997) Structure, 5, 1639–1653.
Delihas, N., Rokita, S.E. and Zheng, P. (1997) Nat. Biotechnol., 15, 751–753.
Ferrer, N., Azorin, F., Villasante, A., Gutierrez, C. and Abad, J.P. (1995) J. Mol. Biol., 245, 8–21.
Han, G.W., Kopka, M.L., Cascio, D., Grzeskowiak, K. and Dickerson, R.E. (1997) J. Mol. Biol., 269, 811–826.
Hare, D.R., Wemmer, D.E., Chou, S.-H., Drobny, G. and Reid, B.R. (1983) J. Mol. Biol., 171, 319–336.
Huang, C.-H., Lin, Y.-S., Yang, Y.-L., Huang, S.-w. and Chen, C.W. (1998) Mol. Microbiol., 28, 905–916.
James, K.D. and Ellington, A.D. (1997) Chem. Biol., 4, 595–605.
Katahira, M.H.S., Mishima, K., Uesugi, S. and Fujii, S. (1993) Nucleic Acids Res., 21, 5418–5424.
Li, Y. and Agrawal, S. (1995) Biochemistry, 34, 10056–10062.
Li, Y., Zon, G. and Wilson, W.D. (1991a) Proc. Natl. Acad. Sci. USA, 88, 26–30.
Li, Y., Zon, G. and Wilson, W.D. (1991b) Biochemistry, 30, 7566–7572.
Lin, C.-H., Wang, W., Jones, R.A. and Patel, D.J. (1998) Chem. Biol., 5, 555–572.
Maskos, K., Gunn, B.M., LeBlanc, D.A. and Morden, K. M. (1993) Biochemistry, 32, 3583–3595.
Mooren, M.M.W., Pulleyblank, D.E., Wijmenga, S.S., van de Ven, F.J.M. and Hilbers, C.W. (1994) Biochemistry, 33, 7315–7325.
Mueller, L., Legault, P. and Pardi, A. (1995) J. Am. Chem. Soc., 117, 11043–11048.
Ortiz-Lombardia, M., Cortes, A., Huertas, D., Eritia, R. and Azorin, F. (1998) J. Mol. Biol., 277, 757–762.
Pley, H.W., Flaherty, K.M. and McKay, D.B. (1994) Nature, 372, 68–74.
Radhakrishnan, I., Gao, X., de los Santos, C., Live, D. and Patel, D.J. (1991) Biochemistry, 30, 9022–9030.
Rajagopal, P. and Feigon, J. (1989) Nature, 339, 637–640.
Sarma, R.H., Mynott, R.J., Wood, D.J. and Hruska, F.E. (1973) J. Am. Chem. Soc., 95, 6457–6459.
Shepard, W., Cruse, W.B.T., Fourme, R., Fortelle, E.d.l. and Prange, T. (1998) Structure, 6, 849–861.
Shlomai, J. and Kornberg, A. (1980) Proc. Natl. Acad. Sci. USA, 77, 799–803.
Walter, A.E., Wu, M. and Turner, D.H. (1994) Biochemistry, 33, 11349–11354.
Wu, M. and Turner, D.H. (1996) Biochemistry, 35, 9677–9689.
Zhu, L., Chou, S.-H. and Reid, R.B. (1995) J. Mol. Biol., 254, 623–637.
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Chou, SH., Tseng, YY., Chen, YR. et al. Structural studies of symmetric DNA undecamers containing non-symmetrical sheared (PuGAPu):(PyGAPy) motifs. J Biomol NMR 14, 157–167 (1999). https://doi.org/10.1023/A:1008351213029
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DOI: https://doi.org/10.1023/A:1008351213029