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A minor groove RNA triple helix within the catalytic core of a group I intron

Nature Structural Biology volume 5, pages 1037–1042 (1998)Cite this article

Abstract

Close packing of several double helical and single stranded RNA elements is required for the Tetrahymena group I ribozyme to achieve catalysis. The chemical basis of these packing interactions is largely unknown. Using nucleotide analog interference suppression (NAIS), we demonstrate that the P1 substrate helix and J8/7 single stranded segment form an extended minor groove triple helix within the catalytic core of the ribozyme. Because each triple in the complex is mediated by at least one 2'-OH group, this substrate recognition triplex is unique to RNA and is fundamentally different from major groove homopurine–homopyrimidine triplexes. We have incorporated these biochemical data into a structural model of the ribozyme core that explains how the J8/7 strand organizes several helices within this complex RNA tertiary structure.

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Figure 1: a, Secondary structure and modeled regions of the Tetrahymena intron.
Figure 2: NAIS experiments to define tertiary interaction partners for 2'-OH groups in the IGS.
Figure 3: Model of the elements surrounding the J8/7 region of the Tetrahymena group I intron catalytic core.

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References

  1. Cech, T.R. & Herschlag, D. In Catalytic RNA, vol. 10 (eds Eckstein, F. & Lilley, D.M.J.) 1–17 (Springer, New York; 1996).

    Book  Google Scholar 

  2. Cate, J.H. et al. Science 273, 1678–1685 (1996).

    Article  CAS  Google Scholar 

  3. Waring, R.B., Towner, P., Minter, S.J. & Davies, R.W. Nature 321, 133–139 (1986).

    Article  CAS  Google Scholar 

  4. Bevilacqua, P.C. & Turner, D.H. Biochemistry 30, 10632–10640 ( 1991).

    Article  CAS  Google Scholar 

  5. Pyle, A.M. & Cech, T.R. Nature 350, 628–631 (1991).

    Article  CAS  Google Scholar 

  6. Strobel, S.A. & Cech, T.R. Biochemistry 32, 13593–13604 (1993).

    Article  CAS  Google Scholar 

  7. Strobel, S.A. & Cech, T.R. Science 267, 675–679 (1995).

    Article  CAS  Google Scholar 

  8. Strobel, S.A., Ortoleva-Donnelly, L., Ryder, S.P., Cate, J.H. & Moncoeur, E. Nature Struct. Biol. 5, 60–66 (1998).

    Article  CAS  Google Scholar 

  9. Ortoleva-Donnelly, L., Szewczak, A.A., Gutell, R.R. & Strobel, S.A. RNA 4, 498–519 ( 1998).

    Article  CAS  Google Scholar 

  10. Pyle, A.M., Murphy, F.L. & Cech, T.R. Nature 358, 123– 128 (1992).

    Article  CAS  Google Scholar 

  11. Damberger, S.H. & Gutell, R.R. Nucleic Acids Res. 22, 3508–3510 ( 1994).

    Article  CAS  Google Scholar 

  12. Tanner, M.A., Anderson, E.M., Gutell, R.R. & Cech, T.R. RNA 3, 1037–1051 ( 1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Michel, F. & Westhof, E. J. Mol. Biol. 216, 585–610 (1990).

    Article  CAS  Google Scholar 

  14. Wang, J.F. & Cech, T.R. Science 256, 526–529 (1992).

    Article  CAS  Google Scholar 

  15. Waring, R.B., Davies, R.W., Brown, T.A. & Scazzocchio, C. Gene 28, 277–291 ( 1984).

    Article  CAS  Google Scholar 

  16. Narlikar, G.J., Khosla, M., Usman, N. & Herschlag, D. Biochemistry 36, 2465–2477 ( 1997).

    Article  CAS  Google Scholar 

  17. Michel, F. & Westhof, E. Nature Struct. Biol. 1, 5–7 (1994).

    Article  CAS  Google Scholar 

  18. Conrad, F., Hanne, A., Gaur, R.K. & Krupp, G. Nucleic Acids Res. 23, 1845–1853 ( 1995).

    Article  CAS  Google Scholar 

  19. Strobel, S.A. & Shetty, K. Proc. Natl. Acad. Sci. USA 94, 2903–2908 (1997).

    Article  CAS  Google Scholar 

  20. Strobel, S.A., Ortoleva-Donnelly, L., Ryder, S.P., Cate, J.H. & Moncoeur, E. Nature Struct. Biol. 5, 60–66 (1998).

    Article  CAS  Google Scholar 

  21. Moore, M.J. & Sharp, P.A. Science 256, 992–997 (1992).

    Article  CAS  Google Scholar 

  22. Ortoleva-Donnelly, L., Kronman, M. & Strobel, S.A. Biochemistry 37, 12933– 12942 (1998).

    Article  CAS  Google Scholar 

  23. Moser, H.E. & Dervan, P.B. Science 238, 645–650 (1987).

    Article  CAS  Google Scholar 

  24. Beal, P.A. & Dervan, P.B. Science 251, 1360–1363 (1991).

    Article  CAS  Google Scholar 

  25. Lehnert, V., Jaeger, L., Michel, F. & Westhof, E. Chem. Biol. 3, 993–1009 (1996).

    Article  CAS  Google Scholar 

  26. Pyle, A.M. Science 261, 709–714 ( 1993).

    Article  CAS  Google Scholar 

  27. Christian, E.L. & Yarus, M. J. Mol. Biol. 228, 743–758 (1992).

    Article  CAS  Google Scholar 

  28. Christian, E.L. & Yarus, M. Biochemistry 32, 4475–4480 (1993).

    Article  CAS  Google Scholar 

  29. Piccirilli, J.A., Vyle, J.S., Caruthers, M.H. & Cech, T.R. Nature 361, 85–88 ( 1993).

    Article  CAS  Google Scholar 

  30. Weinstein, L.B., Jones, B.C.N.M., Cosstick, R. & Cech, T.R. Nature 388, 805–808 ( 1997).

    Article  CAS  Google Scholar 

  31. Beren, C., Steicher, B., Schroeder, R. & Hillen, W. Chem. Biol. 5, 163–175 ( 1998).

    Article  Google Scholar 

  32. Golden, B. L., Gooding, A. R., Podell, A. R. & Cech, T. R. Science 282, 259–264 ( 1998).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank R. Sousa for the clone of the Y639F mutant T7 RNA polymerase, R.R. Gutell for analysis of group I sequences, and L. Weinstein for helpful comments on the manuscript. S.P.R. was supported by an NIH training grant. This work was funded by an NIH grant, a Beckman Young Investigator Award, a Searle Scholar award, and a Junior Faculty Research Award from the American Cancer Society to S.A.S.

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Authors and Affiliations

  1. Department of Molecular Biophysics and Biochemistry, Yale University, 260 Whitney Avenue, New Haven, 06520, Connecticut, USA

    Alexander A. Szewczak, Lori Ortoleva-Donnelly, Sean P. Ryder, Eileen Moncoeur & Scott A. Strobel

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  1. Alexander A. Szewczak
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  2. Lori Ortoleva-Donnelly
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  3. Sean P. Ryder
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  5. Scott A. Strobel
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Correspondence to Scott A. Strobel.

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Szewczak, A., Ortoleva-Donnelly, L., Ryder, S. et al. A minor groove RNA triple helix within the catalytic core of a group I intron. Nat Struct Mol Biol 5, 1037–1042 (1998). https://doi.org/10.1038/4146

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