Functional implications for a prototypical K-turn binding protein from structural and dynamical studies of 15.5K

Biochemistry

Volumn 46, Issue 51, 2007, Pages 14979-14986

  Soss, Sarah E ^a,b   Flynn, Peter F ^a  

^a UNIVERSITY OF UTAH   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

K-TURN BINDING PROTEIN; RIBONUCLEOPARTICLE ASSEMBLY; RIBOSOME; SPLICEOSOME;

BINDING SITES; CONFORMATIONS; MOLECULAR STRUCTURE; NUCLEAR MAGNETIC RESONANCE; NUCLEATION; RNA;

PROTEINS;

PROTEIN 15.5K; RNA; RNA BINDING PROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG;

ARTICLE; MOLECULAR RECOGNITION; NITROGEN NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN RNA BINDING; PROTEIN STRUCTURE; RNA PROCESSING; SPLICEOSOME;

AMIDES; AMINO ACID SEQUENCE; DEUTERIUM EXCHANGE MEASUREMENT; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEOPROTEINS, SMALL NUCLEAR;

EID: 37349039360     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701254q     Document Type: Article

References (54)

1. Moore, M. J., Query, C. C., and Sharp, P. A. (1993) in The RNA world (Gesteland, R. F., and Atkins, J. F., Eds.) pp 303-357, Cold Spring Harbor Laoratory Press, Cold Spring Harbor, NY.
2. Madhani, H. D., and Guthrie, C. (1994) Dynamic RNA-RNA interactions in the spliceosome, Annu. Rev. Genet. 28, 1-26.
3. Staley, J. P., and Guthrie, C. (1998) Mechanical devices of the spliceosome: motors, clocks, springs, and things, Cell 92, 315-326.
4. Nottrott, S., Hartmuth, K., Fabrizio, P., Urlaub, H., Vidovic, I., Ficner, R., and Luhrmann, 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.
5. Marmier-Gourrier, N., Clery, A., Senty-Segault, V., Charpentier, B., Schlotter, F., Leclerc, F., Fournier, R., and Branlant, C. (2003) A structural, phylogenetic, and functional study of 15.5-kD/Snu13 protein binding on the U3 small nucleolar RNA, RNA 9, 821-838.
6. Dobbyn, H. C., and O'Keefe, R. T. (2004) Analysis of Snu13p mutations reveals differential interactions with the U4 snRNA and U3 snoRNA, RNA 10, 308-320.
7. Watkins, N. J., Segault, V., Charpentier, B., Nottrott, S., Fabrizio, P., Bachi, A., Wilm, M., Rosbash, M., and Branlant, C. (2000) A common core RNP structure shared between the small nucleoar box C/D RNPs and the spliceosomal U4 snRNP, Cell 103, 457-466.
8. Gottschalk, A., Neubauer, G., Banroques, J., Mann, M., Luhrmann, R., and Fabrizio, P. (1999) Identification by mass spectrometry and functional analysis of novel proteins of the yeast [U4/U6.U5] tri-snRNP, EMBO J. 18, 4535-4548.
9. Nottrott, S., Urlaub, H., and Luhrmann, R. (2002) Hierarchical, clustered protein interactions with U4/U6 snRNA: a biochemical role for U4/U6 proteins, EMBO J. 21, 5527-5538.
10. Kiss, T. (2001) Small nucleolar RNA-guided post-transcriptional modification of cellular RNAs, EMBO J. 20, 3617-3622.
11. Maxwell, E. S., and Fournier, M. J. (1995) The small nucleolar RNAs, Annu. Rev. Biochem. 35, 897-934.
12. Watkins, N. J., Dickmanns, A., and Luhrmann, R. (2002) Conserved stem II of the box C/D motif is essential for nucleolar localization and is required, along with the 15.5k protein, for the hierarchical assembly of the box C/D snoRNP, Mol. Cell. Biol. 22, 8342-8352.
13. Klein, D. J., Schmeing, T. M., and Moore, P. B. (2001) The kink-turn: a new RNA secondary structure motif, EMBO J. 20, 4214-4221.
14. 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-dependant, RNA 10, 254-264.
15. Oruganti, S. v., Zhang, Y., and Li, H. (2005) Structural comparison of yeast snoRNP and spliceosomal protein Snu13p with its homologs, Biochem. Biophys. Res. Commun. 333, 550-554.
16. Moore, T., Zhang, Y., 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.
17. Hamma, T., and Ferre-D'Amare, A. R. (2004) Structure of protein L7Ae bound to a K-turn derived from an archaeal box H/ACA sRNA at 1.8 A resolution, Structure 12, 893-903.
18. Charron, C., Manival, S., Clery, A., Senty-Segault, V., Charpentier, B., Marmier-Gourrier, N., Branlant, C., and Aubry, A. (2004) The archeal sRNA binding protein L7Ae has a 3D structure very similar to that of its eukaryal counterpart while having a broader RNA-binding specificity, J. Mol. Biol. 342, 757-773.
19. Suryadi, J., Tran, E. J., Maxwell, E. S., and Brown, B. A. I. (2005) The crystal structure of the Methanocaldococcus jannaschii multifunctional L7Ae RNA-binding protein reveals an induced-fit interaction with the box C/D/RNAs, Biochemistry 44, 9657-9672.
20. Mao, H., and Williamson, J. R. (1999) Local folding coupled to RNA binding in the yeast ribosomal protein L30, J. Mol. Biol. 292, 345-359.
21. Chao, J. A., Prasad, G. S., White, S. A., Stout, C. D., and Williamson, J. R. (2003) Inherent protein structural flexibility at the RNA-binding interface of L30e, J. Mol. Biol. 326, 999-1004.
22. Chao, J. A., and Williamson, J. R. (2004) Joint x-ray and NMR refinement of the yeast L30e-mRNA complex, Structure 12, 1165-1176.
23. Vidovic, I., Nottrott, S., Hartmuth, K., Luhrmann, R., and Ficner, R. (2000) Crystal structure of the spliceosomal 15.5kD protein bound to a U4 snRNA fragment, Mol. Cell 6, 1331-1342.
24. Williamson, J. R. (2000) Induced fit in RNA-protein recognition, Nat. Struct. Biol. 7, 834-837.
25. Chen, Y., and Varani, G. (2005) Protein families and RNA recognition, FEBS J. 272, 2088-2097.
26. Goddard, T. D., and Kneller, D. G., University of California, San Fransisco.
27. Farrow, N. A., Muhandiram, R., Singer, A. U., Pascal, S. M., Kay, C. M., Gish, G., Shoelson, S. E., Pawson, T., Forman-Kay, J. D., and Kay, L. E. (1994) Backbone dynamics of a free and a phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation, Biochemistry 33, 5984-6003.
28. Guntert, P., Mumenthaler, C., and Wuthrich, K. (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA., J. Mol. Biol. 273, 283-298.
29. Hermann, T., Guntert, P., and Wuthrich, K. (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA, J. Mol. Biol. 319, 209-227.
30. Soss, S. E., and Flynn, P. F. (2007) NMR assignment of the human spliceosomal 15.5K, J. Biomol. NMR 38, 175.
31. Cornilescu, G., Delaglio, F., and Bax, A. (1999) TALOS: protein backbone angle restraints from searching a database for chemical shift and sequence homology, J. Biomol. NMR 13, 289-302.
32. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J.-S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination, Acta. Crystallogr., Sect. D: Biol. Crystallogr.54, 905-921.
33. Laskowski, R. A., Rullmann, J. A. C., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR., J. Biomol. NMR 8, 477-496.
34. Lipari, G., and Szabo, A. (1982) Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules 1. Theory and range of validity, J. Am. Chem. Soc. 104, 4546-4559.
35. Lipari, G., and Szabo, A. (1982) Model-free approach to the interpretation of nuclear magnetic resonance relaxation in Macromolecules 2. Analysis of experimental results, J. Am. Chem. Soc. 104, 4559-4570.
36. Mandel, A. M., Akke, M., and Palmer, A. G., III. (1995) Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme, J. Mol. Biol. 246, 144-163.
37. Clarkson, M. W., Gilmore, S. A., Edgell, M. H., and Lee, A. L. (2006) Dynamic coupling and allosteric behavior in a nonallosteric protein, Biochemistry 45, 7693-7699.
38. Connelly, G. P., Bai, Y., Jeng, M.-F., and Englander, S. W. (1993) Isotope effects in peptide group hydrogen exchange, Proteins 17, 87-92.
39. Bai, Y., Milne, J. S., Mayne, L., and Englander, S. W. (1993) Primary structure effects on peptide group hydrogen exchange, Proteins 17, 75-86.
40. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., and Bourne, P. E. (2000) The Protein Data Bank, Nucleic Acids Res. 28, 235-242.
41. Palmer, A. G. (2004) NMR characterization of the dynamics of biomacromolecules, Chem. Rev. 104, 3623-3640.
42. Tjandra, N., Feller, S. E., Pastor, R. W., and Bax, A. (1995) Rotational diffusion anisotropy of human ubiquitin from 15N NMR relaxation, J. Am. Chem. Soc. 117, 12562-12566.
43. Schurr, J. M., Babcock, H. P., and Fujimoto, B. S. (1994) A test of the Model-Free formulas. Effects of anisotropic rotational diffusion and dimerization, J. Magn. Reson. B105, 211-214.
44. Palmer, A. G., III, Williams, J., and McDermott, A. (1996) Nuclear magnetic resonance studies of biopolymer dynamics, J. Phys. Chem. 100, 13293-13310.
45. Massi, F., Grey, M. J., and Palmer, III, A. G. (2005) Microsecond timescale backbone conformational dynamics in ubiquitin studied with NMR R1p relaxation experiments, Protein Sci. 14, 735-742.
46. Loria, J. P., Ranee, M., and Palmer, III, A. G. (1999) A relaxation-compensated Carr-Purcell-Meiboom-Gill sequence for characterizing chemical exchange by NMR spectroscopy, J. Am. Chem. Soc. 121, 2331-2332.
47. Linderstrom-Lang, K., and Schellman, J. A. (1959) in The Enzymes (Lardy, H., and Myrback, K., Eds.) pp 443-510, Academic Press, New York.
48. Englander, S. W., and Kallenbach, N. R. (1984) Hydrogen exchange and structural dynamics of proteins and nucleic-acids, Q. Rev. Biophys. 16, 521-655.
49. Kuhn, J. F., Tran, E. J., and Maxwell, E. S. (2002) Archaeal ribosomal protein L7 is a functional homolog of the eukaryotic 15.5kD/Snu13p snoRNP core protein, Nucleic Acids Res. 30, 931-941.
50. Schultz, A., Nottrott, S., Watkins, N. J., and Luhrmann, R. (2006) Protein-protein and protein-RNA contacts both contribute to the 15.5K-mediated assembly of the U4/U6 snRNP and the box C/D snoRNPs, Mol. Cell. Biol. 26, 5146-5154.
51. Liu, S., LI, P., Dybkov, O., Nottrott, S., Hartmuth, K., Luhrmann, R., Carlomagno, T., and Wahl, M. C. (2007) Binding of the human Prp31 Nop domain to a composite RNA-protein platform in U4 snRNP, Science 316, 115-119.
52. Matsumura, S., Ikawa, Y., and Inoue, T. (2003) Biochemical characterization of the kink-turn RNA motif, Nucleic Acids Res. 31, 5544-5551.
53. Cojocaru, V., Nottrott, S., Klement, R., and Jovin, T. M. (2005) The snRNP 15.5K protein folds its cognate K-turn RNA: A combined theoretical and biochemical study, RNA 11, 197-209.
54. Razga, F., Koca, J., Sponer, J., and Leontis, N. B. (2005) Hinge-like motions in RNA Kink-turns: the role of the second A-minor motif and nominally unpaired bases, Biophys. J. 88, 3466-3485.