Abstract
RNA molecules fold into specific three-dimensional shapes to perform structural and catalytic functions. Large RNAs can form compact globular structures, but the chemical basis for close helical packing within these molecules has been unclear. Analysis of transfer, catalysis, in vitro-selected and ribosomal RNAs reveal that helical packing predominantly involves the interaction of single-stranded adenosines with a helix minor groove. Using the Tetrahymena thermophila group I ribozyme, we show here that the near-perfect shape complementarity between the adenine base and the minor groove allows for optimal van der Waals contacts, extensive hydrogen bonding and hydrophobic surface burial, creating a highly energetically favorable interaction. Adenosine is recognized in a chemically similar fashion by a combination of protein and RNA components in the ribonucleoprotein core of the signal recognition particle. These results provide a thermodynamic explanation for the noted abundance of conserved adenosines within the unpaired regions of RNA secondary structures.
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References
Leontis, N.B. & Westhof, E. Q. Rev. Biophys. 31, 399–455 (1998).
Cate, J.H. et al. Science 273, 1678–1685 (1996).
Westhof, E., Dumas, P. & Moras, D. Acta. Crystallogr. A 44, 112–123 (1988).
Ferre-D'Amare, A.R., Zhou, K. & Doudna, J.A. Nature 395, 567–574 (1998).
Conn, G.L., Draper, D.E., Lattman, E.E. & Gittis, A.G. Science 284, 1171–1174 (1999).
Wimberly, B.T., Guymon, R., McCutcheon, J.P., White, S.W. & Ramakrishnan, V. Cell 97, 491–502 (1999).
Su, L., Chen, L., Egli, M., Berger, J.M. & Rich, A. Nature Struct. Biol. 6, 285–292 (1999).
Mao, H., White, S.A. & Williamson, J.R. Nature Struct. Biol. 6, 1139–1147 (1999).
Nix, J., Sussman, D. & Wilson, C. J. Mol. Biol. 296, 1235–1244 (2000).
Sussman, D., Nix, J.C. & Wilson, C. Nature Struct. Biol. 7, 53–57 (2000).
Ban, N., Nissen, P., Hansen, J., Moore, P.B. & Steitz, T.A. Science 289, 905–920 (2000).
Pley, H.W., Flaherty, K.M. & McKay, D.B. Nature 372, 111–113 (1994).
Wimberly, B.T. et al. Nature 407, 327–339 (2000).
Schluenzen, F. et al. Cell 102, 615–623 (2000).
Costa, M. & Michel, F. EMBO J. 14, 1276–1285 (1995).
Doherty, E.A., Herschlag, D. & Doudna, J.A. Biochemistry 38, 2982–2990 (1999).
Abramovitz, D.L., Friedman, R.A. & Pyle, A.M. Science 271, 1410–1413 (1996).
Silverman, S.K. & Cech, T.R. Biochemistry 38, 8691–8702 (1999).
Xiong, Y. & Sundaralingam, M. RNA 6, 1316–1324 (2000).
Saenger, W. Principles of nucleic acid structure. (Springer-Verlag, New York; 1984).
Michel, F., Ellington, A.D., Couture, S. & Szostak, J.W. Nature 347, 578–580 (1990).
Batey, R.T., Rambo, R.P., Lucast, L., Rha, B. & Doudna, J.A. Science 287, 1232–1239 (2000).
Nissen, P., Ippolito, J.A., Ban, M., Moore, P.B. & Steitz, T.A. Proc. Natl. Acad. Sci. USA in the press (2001).
Michel, F. & Westhof, E. J. Mol. Biol. 216, 585–610 (1990).
Yoshizawa, S., Fourmy, D. & Puglisi, J.D. Science 285, 1722–1725 (1999).
Carter, A.P. et al. Nature 407, 340–348 (2000).
Gutell, R.R., Weiser, B., Woese, C.R. & Noller, H.F. Prog. Nucleic. Acid Res. Mol. Biol. 32, 155–216 (1985).
Woese, C.R., Winker, S. & Gutell, R.R. Proc. Natl. Acad. Sci. USA 87, 8467–8471 (1990).
Massire, C. & Westhof, E. J. Mol. Graph Model 16, 255–257 (1998).
Westhof, E., Dumas, P. & Moras, D. J. Mol. Biol. 184, 119–145 (1985).
Brunger, A.T. et al. Acta Crystallogr. D 54, 905–921 (1998).
Maidak, B.L. et al. Nucleic Acids Res. 28, 173–174 (2000).
Kleywegt, G.J. Acta Crystallogr. D 52, 842–857 (1996).
Nicholls, A., Sharp, K.A. & Honig, B. Proteins 11, 281–296 (1991).
Acknowledgements
We thank P. Nissen, J. Ippolito and T. Steitz for helpful discussions. This work was supported by the NIH and the David and Lucile Packard Foundation. E.A.D. was supported in part by NIH training grant. R.T.B was supported by a Jane Coffin Childs postdoctoral fellowship.
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Doherty, E., Batey, R., Masquida, B. et al. A universal mode of helix packing in RNA. Nat Struct Mol Biol 8, 339–343 (2001). https://doi.org/10.1038/86221
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DOI: https://doi.org/10.1038/86221
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