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Trans-activation of group II intron splicing by nuclear U5 snRNA

Abstract

Similarities between RNA splicing during autocatalytic excision of group II introns and pre-mRNA processing led to the hypothesis that group II introns might be the evolutionary predecessors of spliceosomal small nuclear RNAs1–4. The ID3 subdomain stem-loop structure of group II introns, the proposed analogue of the spliceosomal U5 snRNA5, is thought to be essential for 5′ splice site recognition and anchoring of the free 5′ exon6. Using the group II intron bII we have analysed the role of ID3 in splicing. In the absence of ID3 the 5′ splice site was recognized accurately and efficiently, but exon anchoring was greatly reduced. This step was restored in the presence of RNA fragments consisting of either the terminal stem–loop structure of ID3 or spliceosomal U5 snRNA. This suggests that the predominant role of both RNAs is to anchor the 5′ exon during exon ligation. Furthermore, as U5 complements for the loss of ID3, a similar network of structural RNAs may form the catalytic core of both group II introns and spliceosomes.

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References

  1. Jacquier, A. Self-splicing group II introns and nucelar pre-messenger RNA introns—how similar are they? Trends Biochem. Sci. 15, 351–354 (1990).

    Article  CAS  Google Scholar 

  2. Sharp, P. A. Five easy pieces. Science 42, 663 (1991).

    Article  ADS  Google Scholar 

  3. Weiner, A. M. mRNA splicing and autocatalytic introns: distant cousins or the products of chemical determinism? Cell 72, 161–164 (1993).

    Article  CAS  Google Scholar 

  4. Wise, J. A. Guides to the heart of the spliceosome. Science 262, 1978–1979 (1993).

    Article  ADS  CAS  Google Scholar 

  5. Newman, A. J. & Norman, C. U5 snRNA interacts with exon sequences at 5′ and 3′ splice-sites. Cell 68, 743–754 (1992).

    Article  CAS  Google Scholar 

  6. Michel, F. & Ferat, J.-L. Structure and activities of group II introns. Annu. Rev. Biochem. 64, 435–461 (1994).

    Article  Google Scholar 

  7. Padgett, R. A., Podar, M., Boulanger, S. C. & Perlman, P. S. The stereochemical course of group II intron self-splicing. Science 266, 1685–1688 (1994).

    Article  ADS  CAS  Google Scholar 

  8. Moore, M. J. & Sharp, P. A. Evidence for two active sites in the spliceosome provided by stereochemistry of pre-mRNA splicing. Nature 365, 364–368 (1993).

    Article  ADS  CAS  Google Scholar 

  9. Peebles, C. L., Perlman, P. S., Mecklenburg, K. L., Petrillo, M. L. & Tabor, J. H. A self-splicing RNA excises an intorn lariat. Cell 44, 213–223 (1986).

    Article  CAS  Google Scholar 

  10. Schmelzer, C. & Schweyen, R. J. A self-splicing of group II introns in vitro: mapping of the branch point and mutational inhibition of lariat formation. Cell 46, 557–565 (1986).

    Article  CAS  Google Scholar 

  11. Van der Veen, R. et al. Excised group II introns in yeast mitochondria are lariats and can be formed by self-splicing in vitro. Cell 44, 225–234 (1986).

    Article  CAS  Google Scholar 

  12. Moore, M. J., Query, C. C. & Sharp, P. A. in Teh RNA World (eds Gesteland, R. F. & Atkins, J. F.) 303–358 (Cold Spring Harbor Laboratory Press, NY, 1993).

    Google Scholar 

  13. Jacquier, A. & Michel, F. Multiple exon-binding sites in class II self-splicing introns. Cell 50, 17–29 (1987).

    Article  CAS  Google Scholar 

  14. Harris-Kerr, C. L., Zhang, M. & Peebles, C. L. The phylogenatically predicted base-pairing interaction between α and α′ is required for group II splicing in vitro. Proc. Natl Acad. Sci. USA 90, 10658–10662 (1993).

    Article  ADS  CAS  Google Scholar 

  15. O'Keefe, R. T., Norman, C. & Newman, A. J. The invariant U5 snRNA loop 1 sequence is dispensable for the first catalytic step of pre-mRNA splicing in yeast. Cell 86, 679–689 (1996).

    Article  CAS  Google Scholar 

  16. Michel, F., Umesono, K. & Ozeki, H. Comparative and functional anatomy of group II catalytic introns—a rview. Gene 82, 5–30 (1989).

    Article  CAS  Google Scholar 

  17. Madhani, H. D. & Guthrie, C. Dynamic RNA–RNA interactions in the spliceosome. Annu. Rev. Genet. 28, 1–26 (1994).

    Article  CAS  Google Scholar 

  18. Sontheimer, E. J. & Steitz, J. A. The U5 and U6 small nuclear RNAs as active components of the spliceosome. Science 262, 1989–1996 (1993).

    Article  ADS  CAS  Google Scholar 

  19. Mueller, M. W., Stocker, P., Hetzer, M. & Schweyen, R. J. The fate of the junction phosphate in alternating forward and reverse splicing reactions of group II intron RNA. J. Mol. Biol. 222, 145–154 (1991).

    Article  CAS  Google Scholar 

  20. Mueller, M. W., Hetzer, M. & Schweyen, R. J. Group II intron RNA catalyzes progressive, site-specific, 3′ to 5′ nucleotide insertion: a model for RNA editing? Science 261, 1035–1038 (1993).

    Article  ADS  CAS  Google Scholar 

  21. Michels, J. W. & Pyle, A. M. Conversion of a group II intron into a multiple-turnover ribozyme that selectively cleaves oligonucleotides: elucidation of reaction mechanism and structure/function relationships. Biochemistry 34, 2965–2977 (1995).

    Article  CAS  Google Scholar 

  22. Bachl, J. & Schmelzer, C. Effects of deletions at structural domains of group II intron bI1 on self-splicing introns. J. Mol. Biol. 212, 113–125 (1990).

    Article  CAS  Google Scholar 

  23. Suchy, M. & Schmelzer, C. Restoration of the self-splicing activity of a defective group II intron by a small trans-acting RNA. J. Mol. Biol. 222, 179–187 (1991).

    Article  CAS  Google Scholar 

  24. Frank, D. N., Roiha, H. & Guthrie, C. Architecture of the U5 small nuclear RNA. Mol. Cell. Biol. 14, 2180–2190 (1994).

    Article  CAS  Google Scholar 

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Hetzer, M., Wurzer, G., Schweyen, R. et al. Trans-activation of group II intron splicing by nuclear U5 snRNA. Nature 386, 417–420 (1997). https://doi.org/10.1038/386417a0

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