The NMR structure of the 38 kDa U1A protein – PIE RNA complex reveals the basis of cooperativity in regulation of polyadenylation by human U1A protein (original) (raw)

References

  1. Wickens, M., Anderson, P. & Jackson, R.J. Life and death in the cytoplasm: Messages from the 3′ end. Curr. Op. Genet. Develop. 7, 220–232 (1997).
    Article CAS Google Scholar
  2. Boelens, W.C. et al. The human U1 snRNP-specific U1A protein inhibits polyadenylation of its own pre-mRNA. Cell 72, 881– 892 (1993).
    Article CAS Google Scholar
  3. van Gelder, C.W.G. et al. A complex secondary structure in U1A pre-mRNA that binds two molecules of U1A protein is required for regulation of polyadenylation. EMBO J. 12, 5191–5200 ( 1993).
    Article CAS Google Scholar
  4. Gunderson, S.I. et al. The Human U1A snRNP Protein Regulates Polyadenylation via a Direct Interaction with Poly(A) Polymerase. Cell 76, 531–541 (1994).
    Article CAS Google Scholar
  5. Gunderson, S.I., Vagner, S., Polycarpou-Schwarz, M. & Mattaj, I.W. Involvement of the carboxy terminus of vertebrate poly A polymerase in U1A autoregulation and in the coupling of splicing and polyadenylation. Genes & Dev. 11, 761–773 (1997).
    Article CAS Google Scholar
  6. Barabino, S.M.L. & Keller, W. Last but not least: regulated poly(A) tail formation. Cell 99, 9–11 (1999).
    Article CAS Google Scholar
  7. Varani, G. & Nagai, K. RNA Recognition by RNP proteins during RNA processing and maturation. Ann. Rev. Biophys. Biomol. Struct. 27, 407–445 ( 1998).
    Article CAS Google Scholar
  8. Allain, F.-H.T. et al. Specificity of ribonucleoprotein interaction determined by RNA folding during complex formation. Nature 380, 646–650 (1996).
    Article CAS Google Scholar
  9. Allain, F.H.-T., Howe, P.W.A., Neuhaus, D. & Varani, G. Structural Basis of the RNA binding specificity of human U1A protein. EMBO J. 16, 5764–5774 ( 1997).
    Article CAS Google Scholar
  10. Folkers, P.J.M., Folmer, R.H.A., Konings, R.N.H. & Hilbers, C.W. Overcoming the ambiguity problem encountered in the analysis of nuclear Overhauser magnetic resonance spectra of symmetric dimer proteins. J. Am. Chem. Soc. 115, 3798–3799 (1993).
    Article CAS Google Scholar
  11. Mittermaier, A., Varani, L., Muhandiram, D.R., Kay, L.E. & Varani, G. Changes in sidechain and backbone dynamics identify determinants of specificity in RNA recognition by human U1A protein. J. Mol. Biol. 294, 967– 979 (1999).
    Article CAS Google Scholar
  12. Pervushin, K., Riek, R., Wider, G. & Wüthrich, K. Attenuation of T2 relaxation by mutual cancellation by dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc. Natl. Acad. Sci. USA 94, 12366–12371 (1997).
    Article CAS Google Scholar
  13. Zwhalen, C. et al. Methods for Measurement of intermolecular NOEs by multinuclear NMR spectroscopy: application to a bacteriophage λ N-peptide/boxb RNA complex. J. Am. Chem. Soc. 119, 6711– 6721 (1997).
    Article Google Scholar
  14. Gillespie, J.R. & Shortle, D. Characterization of long-range structure in the denatured state of Staphyloccocal nuclease. I. Paramagnetic relaxation enhancement by nitroxide spin labels. J. Mol. Biol. 268, 158–169 (1997).
    Article CAS Google Scholar
  15. Ramos, A. & Varani, G. A new method to detect long-range protein–RNA contacts: NMR detection of electron-proton relaxation induced by nitroxide spin-labeled RNA. J. Am. Chem. Soc. 120 , 10992–10993 (1998).
    Article CAS Google Scholar
  16. Howe, P.W.A., Allain, F.H.-T., Varani, G. & Neuhaus, D. Determination of the NMR structure of the complex between U1A protein and its RNA polyadenylation inhibition element. J. Biomol. NMR 11, 59–84 (1998).
    Article CAS Google Scholar
  17. Allain, F.H.-T. & Varani, G. Structure of the P1 helix from group I self splicing introns. J. Mol. Biol. 250, 333–353 (1995).
    Article CAS Google Scholar
  18. Bayer, P., Varani, L. & Varani, G. Refinement of the structure of protein–RNA complexes by residual dipolar coupling analysis. J. Biomol. NMR 14, 149–155 (1999).
    Article CAS Google Scholar
  19. Jovine, L., Oubridge, C., Avis, J.M. & Nagai, K. Two structurally different RNA molecules are bound by the spliceosomal protein U1A using the same recognition strategy. Structure 4, 621–631 (1996).
    Article CAS Google Scholar
  20. Wolberger, C. Multiprotein–DNA complexes in transcriptional regulation. Ann. Rev. Biophys. Biomol. Struct. 28, 29– 56 (1999).
    Article CAS Google Scholar
  21. Li, T., Stark, M.R., Johnson, A.D. & Wolberger, C. Crystal structure of the MATa1/MATα2 homeodomain heterodimer bound to DNA. Science 270, 262–269 (1995).
    Article CAS Google Scholar
  22. Phillips, C.L., Stark, M.R., Johnson, A.D. & Dahlquist, F.W. Heterodimerization of the yeast homeodomain transcriptional regulator α2 and a1 induces an interfacial helix in α2. Biochemistry 33, 9294–9302 (1994).
    Article CAS Google Scholar
  23. Grainger, R.J., Norman, D.G. & Lilley, D.M.J. Conformational consequences of binding of U1A protein to the 3′ untranslated region of its pre-mRNA. J. Mol. Biol. 288, 585–594 ( 1999).
    Article CAS Google Scholar
  24. Stark, M.R. & Johnson, A.D. Interaction between two homeodomain proteins is specified by a short C-terminal tail. Nature 371, 429–432 (1994).
    Article CAS Google Scholar
  25. Klein Gunnewiek, J.M.T. et al. 14 Residues of the U1 snRNP-specific U1A protein is involved in homodimerization, cooperative RNA binding and inhibition of polyadenylation . Mol. Cell Biol. in the press (2000 ).
  26. Biamonti, G. & Riva, S. New insights into the auxiliary domains of eukaryotic RNA binding proteins. FEBS Lett. 340, 1–8 (1994).
    Article CAS Google Scholar
  27. Birney, E., Kumar, S. & Krainer, A.R. Analysis of the RNA-recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors. Nucleic Acids Res. 21, 5803–5816 (1993).
    Article CAS Google Scholar
  28. Price, S.R., Oubridge, C., Varani, G. & Nagai, K. Preparation of RNA–protein complexes for X-ray crystallography and NMR. In RNA–Protein Interaction: Practical Approach (ed. Smith, C.) (Oxford University Press, 1998), p. 48–72.
    Google Scholar
  29. Mori, S., Abeygunawardana, C., O'Neil Johnson, M. & van Zijl, P.C.M. Improved sensitivity of HSQC spectra of exchanging protons at short interscan delays using a new fast HSQC (FHSQC) detection scheme that avoids water saturation . J. Mag. Res. B 108, 94– 98 (1995).
    Article Google Scholar
  30. Bax, A., Ikura, M., Kay, L.E., Torchia, D.A. & Tschudin, R. Comparison of different modes of two-dimensional reverse-correlation NMR for the study of proteins. J. Mag. Res. 86, 304–318 (1990).
    CAS Google Scholar
  31. Talluri, S. & Wagner, G. An optimized 3D NOESY-HSQC. J. Mag. Res. B 112, 200–205 (1996).
    Article Google Scholar
  32. Gillespie, J.R. & Shortle, D. Characterization of long-range structure in the denatured state of Staphyloccocal nuclease. II. Distance restraints from paramagnetic relaxation and calculation of an ensemble of structures. J. Mol. Biol. 268, 170–184 (1997).
    Article CAS Google Scholar
  33. Ramos, A. et al. RNA Recognition by a Staufen double-stranded RNA binding domain . EMBO J. in the press (2000).
  34. Fletcher, C.M., Jones, D.N.M., Diamond, R. & Neuhaus, D. Treatment of NOE constraints involving equivalent or nonstereoassigned protons in calculations of biomacromolecular structures. J. Biomol. NMR 8, 292–310 ( 1996).
    Article CAS Google Scholar
  35. Varani, G., Aboul-ela, F. & Allain, F.H.-T. NMR investigations of RNA structure. Prog. NMR Spectr. 29, 51–127 (1996).
    Article CAS Google Scholar

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