The snRNP 15.5K protein folds its cognate K-turn RNA: A combined theoretical and biochemical study

RNA

Volumn 11, Issue 2, 2005, Pages 197-209

  Cojocaru, Vlad ^a   Nottrott, Stephanie ^a,b   Klement, Reinhard ^a   Jovin, Thomas M ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Induced fit; K turn motif; Locally enhanced sampling; Molecular dynamics; RNA folding; Splicing

Indexed keywords

SMALL NUCLEAR RIBONUCLEOPROTEIN; SMALL NUCLEAR RNA;

ARTICLE; BASE PAIRING; CANONICAL ANALYSIS; CHEMICAL MODIFICATION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; HUMAN; MOLECULAR DYNAMICS; MOLECULAR WEIGHT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN MOTIF; RNA ANALYSIS; RNA SPLICING; RNA STABILITY; RNA STRUCTURE;

BASE SEQUENCE; HUMANS; MACROMOLECULAR SUBSTANCES; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; RIBONUCLEOPROTEIN, U4-U6 SMALL NUCLEAR; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA, SMALL NUCLEAR; THERMODYNAMICS;

EID: 12844270442     PISSN: 13558382     EISSN: None     Source Type: Journal    
DOI: 10.1261/rna.7149605     Document Type: Article

References (64)

1. Aboul-ela, F. and Varani, G. 1998. Recognition of HIV-1 TAR RNA by Tat protein and Tat-derived peptides. J. Mol. Struct. 423: 29-39.
2. Auffinger, P. and Westhof, E. 2000. Water and ion binding around RNA and DNA (C,G) oligomers. J. Mol. Biol. 300: 1113-1131.
3. 2+ binding sites of the 5S rRNA loop E motif as investigated by molecular dynamics simulations. Chem. Biol. 10: 551-561.
4. 2+ ion-binding sites in the 5S rRNA loop E inferred from molecular dynamics simulations. J. Mol. Biol. 335: 555-571.
5. _. 2004b. Anion binding to nucleic acids. Structure 12: 379-388.
6. Avis, J.M., Allain, F.H.T., Howe, P.W.A., Varani, G., Nagai, K., and Neuhaus, D. 1996. Solution structure of the N-terminal RNP domain of U1A protein: The role of C-terminal residues in structure stability and RNA binding. J. Mol. Biol. 257: 398-411.
7. Berendsen, H.J.C., Postma, J.P.M., Vangunsteren, W.F., Dinola, A., and Haak, J.R. 1984. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81: 3684-3690.
8. Blakaj, D.M., McConnell, K.J., Beveridge, D.L., and Baranger, A.M. 2001. Molecular dynamics and thermodynamics of protein-RNA interactions: Mutation of a conserved aromatic residue modifies stacking interactions and structural adaptation in the U1A-stem loop 2 RNA complex. J. Am. Chem. Soc. 123: 2548-2551.
9. Bringmann, P., Appel, B., Rinke, J., Reuter, R., Theissen, H., and Lührmann, R. 1984. Evidence for the existence of snRNAs U4 and U6 in a single ribonucleoprotein complex and for their association by intermolecular base-pairing. EMBO J. 3: 1357-1363.
10. Brow, D.A. and Guthrie, C. 1988. Spliceosomal RNA U6 is remarkably conserved from yeast to mammals. Nature 334: 213-218.
11. Burge, C.B., Tuschl, T.H., and Sharp, P.A. 1999. Splicing of precursors to mRNAs by the spliceosome. In The RNA world (eds. R.F. Gesteland et al.), pp. 525-560. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
12. Butcher, S.E., Dieckmann, T., and Feigon, J. 1997. Solution structure of the conserved 16 S-like ribosomal RNA UGAA tetraloop. J. Mol. Biol. 268: 348-358.
13. Chao, J.A. and Williamson, J.R. 2004. Joint X-Ray and NMR refinement of the yeast L30e-mRNA complex. Structure 12: 1165-1176.
14. Cheatham, T.E. and Brooks, B.R. 1998. Recent advances in molecular dynamics simulation towards the realistic representation of biomolecules in solution. Theor. Chem. Acc. 99: 279-288.
15. Cheatham, T.E. and Kollman, P.A. 2000. Molecular dynamics simulation of nucleic acids. Annu. Rev. Phys. Chem. 51: 435-471.
16. Cheatham, T.E., Miller, J.L., Fox, T., Darden, T.A., and Kollman, P.A. 1995. Molecular dynamics simulations on solvated biomolecular systems - The particle mesh Ewald method leads to stable trajectories of DNA, RNA, and proteins. J. Am. Chem. Soc. 117: 4193-4194.
17. Cornell, W.D., Cieplak, P., Bayly, C.I., Gould, I.R., Merz, K.M., Ferguson, D.M., Spellmeyer, D.C., Fox, T., Caldwell, J.W., and Kollman, P.A. 1996. A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc. 117: 5179-5197.
18. Darden, T., York, D., and Pedersen, L. 1993. Particle mesh Ewald - An N.Log(N) method for Ewald sums in large systems. J. Chem. Phys. 98: 10089-10092.
19. Ehresmann, C., Baudin, F., Mougel, M., Romby, P., Ebel, J.P., and Ehresmann, B. 1987. Probing the structure of RNAs in solution. Nucleic Acids Res. 15: 9109-9128.
20. Elber, R. and Karplus, M. 1990. Enhanced sampling in molecular dynamics - Use of the time-dependent Hartree approximation for a simulation of carbon monoxide diffusion through myoglobin. J. Am. Chem. Soc. 112: 9161-9175.
21. Goody, T.A., Melcher, S.E., Norman, D.G., and Lilley, D.M.J. 2004. The kink-turn motif in RNA is dimorphic, and metal ion-dependent. RNA 10: 254-264.
22. Gubser, C.C. and Varani, G. 1996. Structure of the polyadenylation regulatory element of the human U1A pre-mRNA 3′-untranslated region and interaction with the U1A protein. Biochemistry 35: 2253-2267.
23. Guo, J., Daizadeh, I., and Gmeiner, W.H. 2000. Structure of Sm binding site from human U4 snRNA derived from a 3 ns PME molecular dynamics simulation. J. Biomol. Struct. Dyn. 18: 335-344.
24. Hartmuth, K., Raker, V.A., Huber, J., Branlant, C., and Lührmann, R. 1999. An unusual chemical reactivity of Sm site adenosines strongly correlates with proper assembly of core U snRNP particles. J. Mol. Biol. 285: 133-147.
25. Hashimoto, C. and Steitz, J.A. 1984. U4 and U6 RNAs coexist in a single small nuclear ribonucleoprotein particle. Nucleic Acids Res. 12: 3283-3293.
26. Humphrey, W., Dalke, A., and Schulten, K. 1996. VMD: Visual molecular dynamics. J. Mol. Graph. 14: 33-38.
27. Kale, L., Skeel, R., Bhandarkar, M., Brunner, R., Gursoy, A., Krawetz, N., Phillips, J., Shinozaki, A., Varadarajan, K., and Schulten, K. 1999. NAMD2: Greater scalability for parallel molecular dynamics. J. Comput. Phys. 151: 283-312.
28. Klein, D.J., Schmeing, T.M., Moore, P.B., and Steitz, T.A. 2001. The kink-turn: A new RNA secondary structure motif. EMBO J. 20: 4214-4221.
29. Leontis, N.B. and Westhof, E. 2002. The non-Watson-Crick base pairs and their associated isostericity matrices. RNA 7: 499-512.
30. _. 2003. Analysis of RNA motifs. Curr. Opin. Struct. Biol. 13: 300-308.
31. Leulliot, N. and Varani, G. 2001. Current topics in RNA-protein recognition: Control of specificity and biological function through induced fit and conformational capture. Biochemistry 40: 7947-7956.
32. Li, W., Ma, B., and Shapiro, B. 2001. Molecular dynamics simulations of the denaturation and refolding of an RNA tetraloop. J. Biomol. Struct. Dyn. 19: 381-396.
33. Macke, T. and Case, D.A. 1998. Modeling unusual nucleic acid structures. In Molecular modeling of nucleic acids (eds. N.B. Leontes and J. Santalucia), pp. 379-393. American Chemical Society, Washington, DC.
34. Matsumura, S., Ikawa, Y., and Inoue, T. 2003. Biochemical characterization of the kink-turn RNA motif. Nucleic Acids Res. 31: 5544-5551.
35. Misra, V.K. and Draper, D.E. 1998. On the role of magnesium ions in RNA stability. Biopolymers 48: 113-135.
36. Moore, T., Zhang, Y.M., Fenley, M.O., and Li, H. 2004. Molecular basis of box C/D RNA-protein interactions: Cocrystal structure of archaeal L7Ae and a box C/D RNA. Structure 12: 807-818.
37. Nottrott, S., Hartmuth, K., Fabrizio, P., Urlaub, H., Vidovic, I., Ficner, R., and Lührmann, R. 1999. Functional interaction of a novel 15.5kD [U4/U6·U5] tri-snRNP protein with the 5′ stem-loop of U4 snRNA. EMBO J. 18: 6119-6133.
38. Nottrott, S., Urlaub, H., and Lührmann, R. 2002. Hierarchical, clustered protein interactions with U4/U6 snRNA: A biochemical role for U4/U6 proteins. EMBO J. 21: 5527-5538.
39. Noy, A., Perez, A., Lankas, F., Javier Luque, F., and Orozco, M. 2004. Relative flexibility of DNA and RNA: A molecular dynamics study. J. Mol. Biol. 343: 627-638.
40. Oubridge, C., Ito, N., Evans, P.R., Teo, C.H., and Nagai, K. 1994. Crystal structure at 1.92 Å resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin. Nature 372: 432-438.
41. Pearlman, D.A., Case, D.A., Caldwell, J.W., Ross, W.S., Cheatham, T.E., Debolt, S., Ferguson, D., Seibel, G., and Kollman, P. 1995. AMBER, a package of computer programs for applying molecular mechanics, normal-mode analysis, molecular dynamics and free-energy calculations to simulate the structural and energetic properties of molecules. Comput. Phys. Commun. 91: 1-41.
42. Pitici, F., Beveridge, D.L., and Baranger, A.M. 2002. Molecular dynamics simulation studies of induced fit and conformational capture in U1A-RNA binding: Do molecular substates code for specificity? Biopolymers 65: 424-435.
43. Puglisi, J.D., Tan, R.Y., Calnan, B.J., Frankel, A.D., and Williamson, J.R. 1992. Conformation of the Tar RNA-arginine complex by NMR spectroscopy. Science 257: 76-80.
44. Puglisi, J.D., Chen, L., Blanchard, S., and Frankel, A.D. 1995. Solution structure of a bovine immunodeficiency virus Tat-Tar peptide-RNA complex. Science 270: 1200-1203.
45. Rázga, F., Špačková, N., Ré blová, K., Koča, J., Leontis, N.B., and Sponer, J. 2004. Ribosomal RNA kink-turn motif - A flexible molecular hinge. J. Biomol. Str. Dyn. 22: 183-193.
46. Réblová, K., Špačková, N., Štefl, R., Csaszar, K., Koča, J., Leontis, N.B., and Šponer, J. 2003a. Non Watson-Crick basepairing and hydration in RNA motifs: Molecular dynamics of 5S rRNA loop E. Biophys. J. 84: 3564-3582.
47. Réblová, K., Špačková, N., Šponer, J.E., Koča, J., and Šponer, J. 2003b. Molecular dynamics simulations of RNA kissing-loop motifs reveal structural dynamics and formation of cation-binding pockets. Nucleic Acids Res. 31: 6942-6952.
48. Réblová, K., Špačková, N., Štefl, R., Csaszar, K., Koča, J., Leontis, N.B., and Šponer, J. 2004. Long-residency hydration, cation binding, and dynamics of Loop E/Helix IV rRNA-L25 protein complex. Biophys. J. 87: 3397-3412.
49. Reyes, C.M. and Kollman, P.A. 2000. Structure and thermodynamics of RNA-protein binding: Using molecular dynamics and free energy analyses to calculate the free energy of binding and conformational change. J. Mol. Biol. 297: 1145-1158.
50. Reyes, C.M., Nifosi, R., Frankel, A.D., and Kollman, P.A. 2001. Molecular dynamics and binding specificity analysis of the bovine immunodeficiency virus BIV Tat-TAR complex. Biophys. J. 80: 2833-2842.
51. Rinke, J., Appel, B., Digweed, M., and Lührmann, R. 1985. Localization of a base-paired interaction between small nuclear RNAs U4 and U6 in intact U4 U6 ribonucleoprotein-particles by psoralen cross-linking. J. Mol. Biol. 185: 721-731.
52. Ryckaert, J.P., Ciccotti, G., and Berendsen, H.J.C. 1977. Numerical integration of Cartesian equations of motion of a system with constraints - Molecular dynamics of N-alkanes. J. Comput. Phys. 23: 327-341.
53. Schneider, C., Will, C.L., Makarova, O.V., Makarov, E.M., and Lührmann, R. 2002. Human U4/U6.U5 and U4atac/U6atac.U5 tri-sn-RNPs exhibit similar protein compositions. Mol. Cell. Biol. 22: 3219-3229.
54. Simmerling, C. and Elber, R. 1994. Hydrophobic collapse in a cyclic hexapeptide - Computer simulations of chdlfc and caaaac in water. J. Am. Chem. Soc. 116: 2534-2547.
55. Simmerling, C. and Kollman, P. 1996. Improved simulation of flexible systems through locally enhanced sampling. Abstracts of Papers of the American Chemical Society 212: 153-COMP.
56. Simmerling, C., Fox, T., and Kollman, P.A. 1998a. Use of locally enhanced sampling in free energy calculations: Testing and application to α → β anomerization of glucose. J. Am. Chem. Soc. 120: 5771-5782.
57. Simmerling, C., Miller, J.L., and Kollman, P.A. 1998b. Combined locally enhanced sampling and particle mesh Ewald as a strategy to locate the experimental structure of a nonhelical nucleic acid. J. Am. Chem. Soc. 120: 7149-7155.
58. Simmerling, C., Lee, M.R., Ortiz, A.R., Kolinski, A., Skolnick, J., and Kollman, P.A. 2000. Combining MONSSTER and LES/PME to predict protein structure from amino acid sequence: Application to the small protein CMTI-1. J. Am. Chem. Soc. 122: 8392-8402.
59. Varani, L., Gunderson, S.I., Mattaj, I.W., Kay, L.E., Neuhaus, D., and Varani, G. 2000. 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. Nat. Struct. Biol. 7: 329-335.
60. Vidovic, I., Nottrott, S., Hartmuth, K., Lührmann, R., and Ficner, R. 2000. Crystal structure of the spliceosomal 15.5kD protein bound to a U4 snRNA fragment. Mol. Cell 6: 1331-1342.
61. Wang, W., Donini, O., Reyes, C.M., and Kollman, P.A. 2001. Biomolecular simulations: Recent developments in force fields, simulations of enzyme catalysis, protein-ligand, protein-protein, and protein-nucleic acid noncovalent interactions. Annu. Rev. Biophy. Biom. 30: 211-243.
62. Watkins, N.J., Segault, V., Charpentier, B., Nottrott, S., Fabrizio, P., Bachi, A., Wilm, M., Rosbash, M., Branlant, C., and Lührmann, R. 2000. A common core RNP structure shared between the small nucleolar box C/D RNPs and the spliceosomal U4 snRNP. Cell 103: 457-466.
63. Williamson, J.R. 2000. Induced fit in RNA-protein recognition. Nat. Struct. Biol. 7: 834-837.
64. Zhang, H., Fountain, M.A., and Krugh, T.R. 2001. Structural characterization of a six-nucleotide RNA hairpin loop found in Escherichia coli, r(UUAAGU). Biochemistry 40: 9879-9886.