Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

The structure of r(UUCGCG) has a 5′-UU-overhang exhibiting Hoogsteen-like trans U•U base pairs

Nature Structural Biology volume 3, pages 24–31 (1996)Cite this article

Abstract

The crystal structure of the RNA fragment, 5′-r(UUCGCG)-3′, has been determined at 1.4 Å resolution by a combination of single isomorphous replacement and molecular search methods. The 3′-terminal CGCG portion of the hexamer engages in Watson–Crick hydrogen bonding while the S′-terminal UU-overhang forms novel Hoogsteen-like UU self-base pairs with the overhang of an adjacent duplex. The U·U pairs display a single conventional hydrogen bond between O4 (U1) and N3 (U8) and a CH–O hydrogen bond between C5-H (U1) and O4(U8), through the Hoogsteen face of the pyrimidine base U1. This unusual arrangement of one of the bases results in a trans U·U pair on antiparallel strands in contrast to the usual cis base pairs. The structure emphasizes the pronounced polymorphism of U·U pairs and has implications for folding of RNA molecules.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Pley, H.W., Flaherty, K.M. & McKay, D.B. Three-dimensional structure of a hammerhead ribozyme. Nature 372, 68–74 (1994).

    Article  CAS  Google Scholar 

  2. Scott, W.G., Finch, J.T. & Klug, A. The crystal structure of an all-RNA hammerhead ribozyme: A proposed mechanism for RNA catalytic cleavage. Cell 81, 991–1002 (1995).

    Article  CAS  Google Scholar 

  3. Michel, F. & Westhof, E. Modeling of the three-dimensional architecture of group I catalytic introns on comparative sequence analysis. J. molec. Biol. 216, 585–610 (1990).

    Article  CAS  Google Scholar 

  4. Holbrook, S.R.C., Tinoco Jr., I.S Kim, S. H. Crystal structure of an RNA double helix incorporating a track of non-Watson–Crick base pairs. Nature 353, 579–581 (1991).

    Article  CAS  Google Scholar 

  5. Baeyens, K.J., De Bondt, H.L. & Holbrook, S.R. Structure of an RNA double helix including uracil-uracil base pairs in an internal loop. Nature struct. Biol. 2, 56–62 (1995).

    Article  CAS  Google Scholar 

  6. Bhattacharyya, D. & Bansal, M. Local variability and base sequence effects in DNA crystal structures. J. Biomol. struct. Dyn. 8, 539–572 (1990).

    Article  CAS  Google Scholar 

  7. Calladine, C.R. Mechanism of sequence-dependent stacking of bases in B-DNA. J. molec. Biol. 161, 343–352 (1982).

    Article  CAS  Google Scholar 

  8. Westhof, E. & Sundaralingam, M. X-ray structure of a cytidyl-3′,5′- adenosine-proflavine complex: A self-paired parallel-chain double helical dimer with an intercalated acridine dye. Proc. natn. Acad. Sci. U.S.A. 77, 1852–1856 (1980).

    Article  CAS  Google Scholar 

  9. Kang, C.H. et al. Crystal structure of intercalated four-stranded d(C3T) at 1.4A resolution. Proc. natn. Acad. Sci. U.S.A. 91, 11636–11640 (1994).

    Article  CAS  Google Scholar 

  10. Westhof, E. Westhof's rule. Nature 358, 459–460 (1992).

    Article  CAS  Google Scholar 

  11. Lavery, R., Zakrezewska, K., Sun, J.S. & Harvey, S.C. A comprehensive classification of nucleic acid structural families based on strand direction and base pairing. Nucleic Acids Res. 20, 5011–5016 (1992).

    Article  CAS  Google Scholar 

  12. Leonard, G.A., McAuley-Hecht, K.E., Brown, T. & Hunter, W.N. Do CH-O hydrogen bonds contribute to the stability of nucleic acid base pairs? Acta Crystallogr. D51, 136–139 (1995).

    CAS  Google Scholar 

  13. Derewenda, Z.S., Lee, L. & Derewenda, U. The occurrence of C-H–O hydrogen bonds in proteins. J. molec. Biol. 252, 248–262 (1995).

    Article  CAS  Google Scholar 

  14. Michel, F., Ellington, A.D., Couture, S. & Szostak, J. Phylogenetic and genetic evidence for base-triples in the catalytic domain of group I introns. Nature 347, 578–580 (1990).

    Article  CAS  Google Scholar 

  15. Cruse, W. et al. The structure of a mispaired RNA double helix at 1.6Å resolution and implications for the prediction of RNA secondary structure. Proc. natn. Acad. Sci. U.S.A. 91, 4160–4164 (1994).

    Article  CAS  Google Scholar 

  16. Wang, A.H.J. et al. Molecular structure of a left-handed double helical DNA fragment at atomic resolution. Nature 282, 680–686 (1979).

    Article  CAS  Google Scholar 

  17. Bugg, C.E., Thomas, J.M., Sundaralingam, M. & Rao, S.T. Stereochemistry of nucleic acids and their constituents. X. Solid-state base-stacking patterns in nucleic acid constituents and polynucleotides. Biopolymers 10, 175–219 (1971).

    Article  CAS  Google Scholar 

  18. Betzel, C., Lorenz, S., Fiirste, J.P., Bald, R., Zhang, M., Schneider, T.R., Wilson, K.S. & Erdmann, V.A. Crystal structure of domain A of Thermus Flavus 55 rRNA and the contribution of water molecules to its structure. FEBSLett. 351, 1509–164 (1994).

    Article  Google Scholar 

  19. Hall, K., Cruz, P., Tinoco Jr, I., Jovin, T. & van de Sande, J. H. ‘Z-RNA’ - a left-handed RNA double helix. Nature 311, 584–586 (1984).

    Article  CAS  Google Scholar 

  20. Westhof, E. & Michel, F. Prediction and experimental investigation of RNA secondary and tertiary foldings, in RNA-protein interactions (eds K. Nagai, & I. W. Mattaj) 25–51 (Oxford University Press Inc., New York, NY, 1994).

  21. van Meervelt, L. et al. High-resolution structure of a DNA helix forming (C–G)*G base triplets. Nature 374, 742–744 (1995).

    Article  CAS  Google Scholar 

  22. Howard, A.J., Nielsen, C. & Xuang, N.H. Software for a diffractometer with multiwire area detector. Meths. Enzymol. 144, 211–237 (1985).

    Google Scholar 

  23. Wang, B.C. Resolution of phase ambiguity in macromolecular crystallography. Meths. Enzymol. 115, 90–112 (1985).

    Article  CAS  Google Scholar 

  24. Brünger, A.T. X-PLOR - A system for x-ray crystallography and NMR (Yale University Press, New Haven, CT, 1992).

    Google Scholar 

  25. Sack, J. & Quiocho, F.A. CHAIN - Crystallographic modeling program (Baylor College of Medicine, Houston, TX, 1992).

    Google Scholar 

  26. Brunger, A.T. Crystallographic refinement by simulated annealing, in Crystallographic computing 4: Techniques and new technologies (eds N. W.Isaacs, & M.R. Taylor) 126–140 (Clarendon Press, Oxford, 1988).

    Google Scholar 

  27. Bernstein, F.C. et al. The protein data bank: a computer-based archival file for macromolecule structures. J. molec. Biol. 112, 535–542 (1977).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. The Ohio State University Laboratory of Biological Macromolecular Structure, Department of Chemistry, 1060 Carmack Road, Columbus, Ohio, 43210, USA

    Markus C. Wahl & Muttaiya Sundaralingam

  2. The Ohio State University Laboratory of Biological Macromolecular Structure, Department of Biochemistry, 1060 Carmack Road, Columbus, Ohio, 43210, USA

    Sambhorao T. Rao & Muttaiya Sundaralingam

Authors
  1. Markus C. Wahl
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sambhorao T. Rao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Muttaiya Sundaralingam
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wahl, M., Rao, S. & Sundaralingam, M. The structure of r(UUCGCG) has a 5′-UU-overhang exhibiting Hoogsteen-like trans U•U base pairs. Nat Struct Mol Biol 3, 24–31 (1996). https://doi.org/10.1038/nsb0196-24

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nsb0196-24

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing