Assembly and dynamics of the U4/U6 di-snRNP by single-molecule FRET

Nucleic Acids Research

Volumn 43, Issue 22, 2015, Pages 10963-10974

  Hardin, John W ^a,b   Warnasooriya, Chandani ^a   Kondo, Yasushi ^b,c   Nagai, Kiyoshi ^b   Rueda, David ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LSM PROTEIN; PROTEIN SM; PRP3 PROTEIN; PRP31 PROTEIN; PRP4 PROTEIN; RIBONUCLEOPROTEIN; RNA; SCAFFOLD PROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN; SNU13 PROTEIN; UNCLASSIFIED DRUG; PROTEIN BINDING; PROTEIN SERINE THREONINE KINASE; PRP31 PROTEIN, S CEREVISIAE; PRP4 PROTEIN, S CEREVISIAE; RNA SPLICING FACTOR; SACCHAROMYCES CEREVISIAE PROTEIN; SNU13 PROTEIN, S CEREVISIAE;

ARTICLE; BASE PAIRING; BINDING AFFINITY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DYNAMICS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GEL MOBILITY SHIFT ASSAY; GENE; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN STABILITY; RNA CONFORMATION; RNA STRUCTURE; SACCHAROMYCES CEREVISIAE; SNU13 GENE; CHEMISTRY; CONFORMATION; METABOLISM; SPLICEOSOME;

FLUORESCENCE RESONANCE ENERGY TRANSFER; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; RIBONUCLEOPROTEIN, U4-U6 SMALL NUCLEAR; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA SPLICING FACTORS; SACCHAROMYCES CEREVISIAE PROTEINS; SPLICEOSOMES;

EID: 84954467080     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1011     Document Type: Article

References (80)

1. Smith, D.J., Query, C.C. and Konarska, M.M. (2008) 'Nought may endure but mutability': spliceosome dynamics and the regulation of splicing. Mol. Cell, 30, 657-666.
2. Wahl, M.C., Will, C.L. and Luhrmann, R. (2009) The spliceosome: design principles of a dynamic RNP machine. Cell, 136, 701-718.
3. Shcherbakova, I., Hoskins, A.A., Friedman, L.J., Serebrov, V., Correa, I.R. Jr, Xu, M.Q., Gelles, J. and Moore, M.J. (2013) Alternative spliceosome assembly pathways revealed by single-molecule fluorescence microscopy. Cell Rep., 5, 151-165.
4. Fedorova, O., Waldsich, C. and Pyle, A.M. (2007) Group II intron folding under near-physiological conditions: collapsing to the near-native state. J. Mol. Biol., 366, 1099-1114.
5. Keating, K.S., Toor, N., Perlman, P.S. and Pyle, A.M. (2010) A structural analysis of the group II intron active site and implications for the spliceosome. RNA, 16, 1-9.
6. Robart, A.R., Chan, R.T., Peters, J.K., Rajashankar, K.R. and Toor, N. (2014) Crystal structure of a eukaryotic group II intron lariat. Nature, 514, 193-197.
7. Lauber, J., Plessel, G., Prehn, S., Will, C.L., Fabrizio, P., Groning, K., Lane, W.S. and Luhrmann, R. (1997) The human U4/U6 snRNP contains 60 and 90kD proteins that are structurally homologous to the yeast splicing factors Prp4p and Prp3p. RNA, 3, 926-941.
8. 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.
9. Will, C.L. and Luhrmann, R. (2011) Spliceosome structure and function. Cold Spring Harb. Perspect. Biol., 3, a003707.
10. Mayes, A.E., Verdone, L., Legrain, P. and Beggs, J.D. (1999) Characterization of Sm-like proteins in yeast and their association with U6 snRNA. EMBO J., 18, 4321-4331.
11. Vidal, V.P., Verdone, L., Mayes, A.E. and Beggs, J.D. (1999) Characterization of U6 snRNA-protein interactions. RNA, 5, 1470-1481.
12. Achsel, T., Brahms, H., Kastner, B., Bachi, A., Wilm, M. and Luhrmann, R. (1999) A doughnut-shaped heteromer of human Sm-like proteins binds to the 3′-end of U6 snRNA, thereby facilitating U4/U6 duplex formation in vitro. EMBO J., 18, 5789-5802.
13. Licht, K., Medenbach, J., Luhrmann, R., Kambach, C. and Bindereif, A. (2008) 3′-cyclic phosphorylation of U6 snRNA leads to recruitment of recycling factor p110 through LSm proteins. RNA, 14, 1532-1538.
14. Raker, V.A., Plessel, G. and Luhrmann, R. (1996) The snRNP core assembly pathway: identification of stable core protein heteromeric complexes and an snRNP subcore particle in vitro. EMBO J., 15, 2256-2269.
15. Salgado-Garrido, J., Bragado-Nilsson, E., Kandels-Lewis, S. and Seraphin, B. (1999) Sm and Sm-like proteins assemble in two related complexes of deep evolutionary origin. EMBO J., 18, 3451-3462.
16. Leung, A.K., Nagai, K. and Li, J. (2011) Structure of the spliceosomal U4 snRNP core domain and its implication for snRNP biogenesis. Nature, 473, 536-539.
17. 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.
18. Wozniak, A.K., Nottrott, S., Kuhn-Holsken, E., Schroder, G.F., Grubmuller, H., Luhrmann, R., Seidel, C.A. and Oesterhelt, F. (2005) Detecting protein-induced folding of the U4 snRNA kink-turn by single-molecule multiparameter FRET measurements. RNA, 11, 1545-1554.
19. 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, 115-120.
20. Banroques, J. and Abelson, J.N. (1989) PRP4: a protein of the yeast U4/U6 small nuclear ribonucleoprotein particle. Mol. Cell. Biol., 9, 3710-3719.
21. Bjorn, S.P., Soltyk, A., Beggs, J.D. and Friesen, J.D. (1989) PRP4 (RNA4) from Saccharomyces cerevisiae: its gene product is associated with the U4/U6 small nuclear ribonucleoprotein particle. Mol. Cell. Biol., 9, 3698-3709.
22. Anthony, J.G., Weidenhammer, E.M. and Woolford, J.L. Jr (1997) The yeast Prp3 protein is a U4/U6 snRNP protein necessary for integrity of the U4/U6 snRNP and the U4/U6.U5 tri-snRNP. RNA, 3, 1143-1152.
23. Ayadi, L., Callebaut, I., Saguez, C., Villa, T., Mornon, J.P. and Banroques, J. (1998) Functional and structural characterization of the prp3 binding domain of the yeast prp4 splicing factor. J. Mol. Biol., 284, 673-687.
24. Horowitz, D.S., Kobayashi, R. and Krainer, A.R. (1997) A new cyclophilin and the human homologues of yeast Prp3 and Prp4 form a complex associated with U4/U6 snRNPs. RNA, 3, 1374-1387.
25. Sander, B., Golas, M.M., Makarov, E.M., Brahms, H., Kastner, B., Luhrmann, R. and Stark, H. (2006) Organization of core spliceosomal components U5 snRNA loop I and U4/U6 Di-snRNP within U4/U6.U5 Tri-snRNP as revealed by electron cryomicroscopy. Mol. Cell, 24, 267-278.
26. Lescoute, A. and Westhof, E. (2006) Topology of three-way junctions in folded RNAs. RNA, 12, 83-93.
27. Karunatilaka, K.S. and Rueda, D. (2009) Single-Molecule Fluorescence Studies of RNA: A Decade's Progress. Chem. Phys. Lett., 476, 1-10.
28. Konig, S.L., Liyanage, P.S., Sigel, R.K. and Rueda, D. (2013) Helicase-mediated changes in RNA structure at the single-molecule level. RNA Biol., 10, 133-148.
29. Warnasooriya, C. and Rueda, D. (2014) Single-molecule fluorescence-based studies on the dynamics, assembly and catalytic mechanism of the spliceosome. Biochem. Soc. Trans., 42, 1211-1218.
30. Wagenbach, M., O'Rourke, K., Vitez, L., Wieczorek, A., Hoffman, S., Durfee, S., Tedesco, J. and Stetler, G. (1991) Synthesis of wild type and mutant human hemoglobins in Saccharomyces cerevisiae. Biotechnology (N Y), 9, 57-61.
31. Schiestl, R.H. and Gietz, R.D. (1989) High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr. Genet., 16, 339-346.
32. Kambach, C., Walke, S., Young, R., Avis, J.M., de la Fortelle, E., Raker, V.A., Luhrmann, R., Li, J. and Nagai, K. (1999) Crystal structures of two Sm protein complexes and their implications for the assembly of the spliceosomal snRNPs. Cell, 96, 375-387.
33. Ito, H., Fukuda, Y., Murata, K. and Kimura, A. (1983) Transformation of intact yeast cells treated with alkali cations. J. Bacteriol., 153, 163-168.
34. Milligan, J.F. and Uhlenbeck, O.C. (1989) Synthesis of small RNAs using T7 RNA polymerase. Methods Enzymol., 180, 51-62.
35. Cameron, V. and Uhlenbeck, O.C. (1977) 3′-Phosphatase activity in T4 polynucleotide kinase. Biochemistry, 16, 5120-5126.
36. Qin, P.Z. and Pyle, A.M. (1999) Site-specific labeling of RNA with fluorophores and other structural probes. Methods, 18, 60-70.
37. Wu, T.P., Ruan, K.C. and Liu, W.Y. (1996) A fluorescence-labeling method for sequencing small RNA on polyacrylamide gel. Nucleic Acids Res., 24, 3472-3473.
38. Ward, J.J., Sodhi, J.S., McGuffin, L.J., Buxton, B.F. and Jones, D.T. (2004) Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J. Mol. Biol., 337, 635-645.
39. Rueda, D. and Walter, N.G. (2006) Fluorescent energy transfer readout of an aptazyme-based biosensor. Methods Mol. Biol., 335, 289-310.
40. Roy, R., Hohng, S. and Ha, T. (2008) A practical guide to single-molecule FRET. Nat. Methods, 5, 507-516.
41. Zhao, R. and Rueda, D. (2009) RNA folding dynamics by single-molecule fluorescence resonance energy transfer. Methods, 49, 112-117.
42. Aitken, C.E., Marshall, R.A. and Puglisi, J.D. (2008) An oxygen scavenging system for improvement of dye stability in single-molecule fluorescence experiments. Biophys. J., 94, 1826-1835.
43. Walter, N.G. (2001) Structural dynamics of catalytic RNA highlighted by fluorescence resonance energy transfer. Methods, 25, 19-30.
44. Zaric, B.L. and Kambach, C. (2008) Reconstitution of recombinant human LSm complexes for biochemical, biophysical, and cell biological studies. Methods Enzymol., 448, 57-74.
45. Zaric, B., Chami, M., Remigy, H., Engel, A., Ballmer-Hofer, K., Winkler, F.K. and Kambach, C. (2005) Reconstitution of two recombinant LSm protein complexes reveals aspects of their architecture, assembly, and function. J. Biol. Chem., 280, 16066-16075.
46. Guo, Z., Karunatilaka, K.S. and Rueda, D. (2009) Single-molecule analysis of protein-free U2-U6 snRNAs. Nat. Struct. Mol. Biol., 16, 1154-1159.
47. Karunatilaka, K.S. and Rueda, D. (2014) Post-transcriptional modifications modulate conformational dynamics in human U2-U6 snRNA complex. RNA, 20, 16-23.
48. Rueda, D., Wick, K., McDowell, S.E. and Walter, N.G. (2003) Diffusely bound Mg2+ ions slightly reorient stems I and II of the hammerhead ribozyme to increase the probability of formation of the catalytic core. Biochemistry, 42, 9924-9936.
49. Penedo, J.C., Wilson, T.J., Jayasena, S.D., Khvorova, A. and Lilley, D.M. (2004) Folding of the natural hammerhead ribozyme is enhanced by interaction of auxiliary elements. RNA, 10, 880-888.
50. Murphy, M.C., Rasnik, I., Cheng, W., Lohman, T.M. and Ha, T. (2004) Probing single-stranded DNA conformational flexibility using fluorescence spectroscopy. Biophys. J., 86, 2530-2537.
51. Rueda, D., Bokinsky, G., Rhodes, M.M., Rust, M.J., Zhuang, X. and Walter, N.G. (2004) Single-molecule enzymology of RNA: essential functional groups impact catalysis from a distance. Proc. Natl. Acad. Sci. U.S.A., 101, 10066-10071.
52. Pereira, M.J., Nikolova, E.N., Hiley, S.L., Jaikaran, D., Collins, R.A. andWalter, N.G. (2008) Single VS ribozyme molecules reveal dynamic and hierarchical folding toward catalysis. J. Mol. Biol., 382, 496-509.
53. 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.
54. Wang, J., Fessl, T., Schroeder, K.T., Ouellet, J., Liu, Y., Freeman, A.D. and Lilley, D.M. (2012) Single-molecule observation of the induction of k-turn RNA structure on binding L7Ae protein. Biophys. J., 103, 2541-2548.
55. Lilley, D.M. (2012) The structure and folding of kink turns in RNA. Wiley Interdiscip. Rev. RNA, 3, 797-805.
56. Lafontaine, D.A., Norman, D.G. and Lilley, D.M. (2001) Structure, folding and activity of the VS ribozyme: importance of the 2-3-6 helical junction. EMBO J., 20, 1415-1424.
57. Goody, T.A., Melcher, S.E., Norman, D.G. and Lilley, D.M. (2004) The kink-turn motif in RNA is dimorphic, and metal ion-dependent. RNA, 10, 254-264.
58. McPhee, S.A., Huang, L. and Lilley, D.M. (2014) A critical base pair in k-turns that confers folding characteristics and correlates with biological function. Nat. Commun., 5, 5127.
59. Huang, L. and Lilley, D.M. (2013) The molecular recognition of kink-turn structure by the L7Ae class of proteins. RNA, 19, 1703-1710.
60. Karaduman, R., Fabrizio, P., Hartmuth, K., Urlaub, H. and Luhrmann, R. (2006) RNA structure and RNA-protein interactions in purified yeast U6 snRNPs. J. Mol. Biol., 356, 1248-1262.
61. Dahlberg, J.E. and Lund, E. (1991) How does III x II make U6? Science, 254, 1462-1463.
62. Cooper, M., Johnston, L.H. and Beggs, J.D. (1995) Identification and characterization of Uss1p (Sdb23p): a novel U6 snRNA-associated protein with significant similarity to core proteins of small nuclear ribonucleoproteins. EMBO J., 14, 2066-2075.
63. Vankan, P., McGuigan, C. and Mattaj, I.W. (1990) Domains of U4 and U6 snRNAs required for snRNP assembly and splicing complementation in Xenopus oocytes. EMBO J., 9, 3397-3404.
64. Terns, M.P., Dahlberg, J.E. and Lund, E. (1993) Multiple cis-acting signals for export of pre-U1 snRNA from the nucleus. Genes Dev., 7, 1898-1908.
65. Boelens, W.C., Palacios, I. and Mattaj, I.W. (1995) Nuclear retention of RNA as a mechanism for localization. RNA, 1, 273-283.
66. Eliceiri, G.L. (1974) Short-lived, small RNAs in the cytoplasm of HeLa cells. Cell, 3, 11-14.
67. De Robertis, E.M., Lienhard, S. and Parisot, R.F. (1982) Intracellular transport of microinjected 5S and small nuclear RNAs. Nature, 295, 572-577.
68. Zeller, R., Nyffenegger, T. and De Robertis, E.M. (1983) Nucleocytoplasmic distribution of snRNPs and stockpiled snRNA-binding proteins during oogenesis and early development in Xenopus laevis. Cell, 32, 425-434.
69. Zieve, G.W., Sauterer, R.A. and Feeney, R.J. (1988) Newly synthesized small nuclear RNAs appear transiently in the cytoplasm. J. Mol. Biol., 199, 259-267.
70. Hamm, J. and Mattaj, I.W. (1990) Monomethylated cap structures facilitate RNA export from the nucleus. Cell, 63, 109-118.
71. Nguyen, T.H.D., Galej, W.P., Bai, X.-C., Savva, C.G., Newman, A.J., Scheres, S.H.W. and Nagai, K. (2015) The architecture of the spliceosomal U4/U6.U5 tri-snRNP. Nature, 523, 47-52.
72. Schultz, A., Nottrott, S., Hartmuth, K. and Luhrmann, R. (2006) RNA structural requirements for the association of the spliceosomal hPrp31 protein with the U4 and U4atac small nuclear ribonucleoproteins. J. Biol. Chem., 281, 28278-28286.
73. Hacker, I., Sander, B., Golas, M.M., Wolf, E., Karagoz, E., Kastner, B., Stark, H., Fabrizio, P. and Luhrmann, R. (2008) Localization of Prp8, Brr2, Snu114 and U4/U6 proteins in the yeast tri-snRNP by electron microscopy. Nat. Struct. Mol. Biol., 15, 1206-1212.
74. Raghunathan, P.L. and Guthrie, C. (1998) RNA unwinding in U4/U6 snRNPs requires ATP hydrolysis and the DEIH-box splicing factor Brr2. Curr. Biol., 8, 847-855.
75. Kim, D.H. and Rossi, J.J. (1999) The first ATPase domain of the yeast 246-kDa protein is required for in vivo unwinding of the U4/U6 duplex. RNA, 5, 959-971.
76. Fica, S.M., Tuttle, N., Novak, T., Li, N.S., Lu, J., Koodathingal, P., Dai, Q., Staley, J.P. and Piccirilli, J.A. (2013) RNA catalyses nuclear pre-mRNA splicing. Nature, 503, 229-234.
77. Fica, S.M., Mefford, M.A., Piccirilli, J.A. and Staley, J.P. (2014) Evidence for a group II intron-like catalytic triplex in the spliceosome. Nat. Struct. Mol. Biol., 21, 464-471.
78. Mozaffari-Jovin, S., Santos, K.F., Hsiao, H.H., Will, C.L., Urlaub, H., Wahl, M.C. and Luhrmann, R. (2012) The Prp8 RNase H-like domain inhibits Brr2-mediated U4/U6 snRNA unwinding by blocking Brr2 loading onto the U4 snRNA. Genes Dev., 26, 2422-2434.
79. Hahn, D., Kudla, G., Tollervey, D. and Beggs, J.D. (2012) Brr2p-mediated conformational rearrangements in the spliceosome during activation and substrate repositioning. Genes Dev., 26, 2408-2421.
80. Menichelli, E., Isel, C., Oubridge, C. and Nagai, K. (2007) Protein-induced conformational changes of RNA during the assembly of human signal recognition particle. J. Mol. Biol., 367, 187-203.