Cooperative structure of the heterotrimeric pre-mRNA retention and splicing complex

Nature Structural and Molecular Biology

Volumn 21, Issue 10, 2014, Pages 911-918

  Wysoczanski, Piotr ^a   Schneider, Cornelius ^a   Xiang, Shengqi ^a   Munari, Francesca ^a   Trowitzsch, Simon ^a,e,f   Wahl, Markus C ^b   Lührmann, Reinhard ^a   Becker, Stefan ^a   Zweckstetter, Markus ^a,c,d  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^d UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^e EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^f UNIV GRENOBLE ALPES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA PRECURSOR; BUD13 PROTEIN, S CEREVISIAE; CARRIER PROTEIN; FUNGAL RNA; IST3 PROTEIN, S CEREVISIAE; PML1 PROTEIN, S CEREVISIAE; RNA BINDING PROTEIN; RNA PRECURSOR; SACCHAROMYCES CEREVISIAE PROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HUMAN; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; RETENTION AND SPLICING COMPLEX; RNA BINDING; RNA SPLICING; RNA STRUCTURE; SACCHAROMYCES CEREVISIAE; SPLICEOSOME; WESTERN BLOTTING; CONFORMATION; GENETICS; METABOLISM; ULTRASTRUCTURE;

SACCHAROMYCES CEREVISIAE;

CARRIER PROTEINS; NUCLEIC ACID CONFORMATION; RIBONUCLEOPROTEIN, U2 SMALL NUCLEAR; RNA PRECURSORS; RNA SPLICING; RNA, FUNGAL; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPLICEOSOMES;

EID: 84920793172     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2889     Document Type: Article

References (76)

1. Will, C.L., Luhrmann, R. Spliceosome structure and function. Cold Spring Harb. Perspect. Biol. 3, a3003707 (2011).
2. Brow, D.A. Allosteric cascade of spliceosome activation. Annu. Rev. Genet. 36, 333-360 (2002).
3. Dziembowski, A. et al. Proteomic analysis identifies a new complex required for nuclear pre-mRNA retention and splicing. EMBO J. 23, 4847-4856 (2004).
4. Gottschalk, A., Bartels, C., Neubauer, G., Luhrmann, R., Fabrizio, P. A novel yeast U2 snRNP protein, Snu17p, is required for the first catalytic step of splicing and for progression of spliceosome assembly. Mol. Cell. Biol. 21, 3037-3046 (2001).
5. Tuo, S., Nakashima, K., Pringle, J.R. Apparent defect in yeast bud-site selection due to a specific failure to splice the pre-mRNA of a regulator of cell-type-specific transcription. PLoS ONE 7, e47621 (2012).
6. Scherrer, F.W. Jr., Spingola, M. A subset of Mer1p-dependent introns requires Bud13p for splicing activation and nuclear retention. RNA 12, 1361-1372 (2006).
7. Schmidlin, T. et al. Single-gene deletions that restore mating competence to diploid yeast. FEMS Yeast Res. 8, 276-286 (2008).
8. Zhou, Y., Chen, C., Johansson, M.J. The pre-mRNA retention and splicing complex controls tRNA maturation by promoting TAN1 expression. Nucleic Acids Res. 41, 5669-5678 (2013).
9. Spingola, M., Armisen, J., Ares, M. Jr. Mer1p is a modular splicing factor whose function depends on the conserved U2 snRNP protein Snu17p. Nucleic Acids Res. 32, 1242-1250 (2004).
10. Hausmann, S. et al. Genetic and biochemical analysis of yeast and human cap trimethylguanosine synthase: functional overlap of 2, 2, 7-trimethylguanosine caps, small nuclear ribonucleoprotein components, pre-mRNA splicing factors, and RNA decay pathways. J. Biol. Chem. 283, 31706-31718 (2008).
11. Wang, Q., Rymond, B.C. Rds3p is required for stable U2 U2 snRNP recruitment to the splicing apparatus. Mol. Cell. Biol. 23, 7339-7349 (2003).
12. Wang, Q., He, J., Lynn, B., Rymond, B.C. Interactions of the yeast SF3b splicing factor. Mol. Cell. Biol. 25, 10745-10754 (2005).
13. Brooks, M.A. et al. Structure of the yeast Pml1 splicing factor and its integration into the RES complex. Nucleic Acids Res. 37, 129-143 (2009).
14. Jiang, M. et al. Genome-wide analysis of developmental and sex-regulated gene expression profiles in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 98, 218-223 (2001).
15. Trowitzsch, S., Weber, G., Luhrmann, R., Wahl, M.C. An unusual RNA recognition motif acts as a scaffold for multiple proteins in the pre-mRNA retention and splicing complex. J. Biol. Chem. 283, 32317-32327 (2008).
16. Collinet, B. et al. Strategies for the structural analysis of multi-protein complexes: lessons from the 3D-Repertoire project. J. Struct. Biol. 175, 147-158 (2011).
17. Trowitzsch, S., Weber, G., Luhrmann, R., Wahl, M.C. Crystal structure of the Pml1p subunit of the yeast precursor mRNA retention and splicing complex. J. Mol. Biol. 385, 531-541 (2009).
18. Dinkel, H. et al. ELM: the database of eukaryotic linear motifs. Nucleic Acids Res. 40, D242-D251 (2012).
19. Korneta, I., Bujnicki, J.M. Intrinsic disorder in the human spliceosomal proteome. PLoS Comput. Biol. 8, e1002641 (2012).
20. Kielkopf, C.L., Rodionova, N.A., Green, M.R., Burley, S.K. A novel peptide recognition mode revealed by the X-ray structure of a core U2AF35/U2AF65 heterodimer. Cell 106, 595-605 (2001).
21. Corsini, L. et al. U2AF-homology motif interactions are required for alternative splicing regulation by SPF45. Nat. Struct. Mol. Biol. 14, 620-629 (2007).
22. Selenko, P. et al. Structural basis for the molecular recognition between human splicing factors U2AF65 and SF1/mBBP. Mol. Cell 11, 965-976 (2003).
23. Thickman, K.R., Swenson, M.C., Kabogo, J.M., Gryczynski, Z., Kielkopf, C.L. Multiple U2AF65 binding sites within SF3b155: thermodynamic and spectroscopic characterization of protein-protein interactions among pre-mRNA splicing factors. J. Mol. Biol. 356, 664-683 (2006).
24. Shen, Y., Bax, A. Protein backbone and sidechain torsion angles predicted from NMR chemical shifts using artificial neural networks. J. Biomol. NMR 56, 227-241 (2013).
25. Adam, S.A., Nakagawa, T., Swanson, M.S., Woodruff, T.K., Dreyfuss, G. mRNA polyadenylate-binding protein: gene isolation and sequencing and identification of a ribonucleoprotein consensus sequence. Mol. Cell. Biol. 6, 2932-2943 (1986).
26. Fabrizio, P. et al. The evolutionarily conserved core design of the catalytic activation step of the yeast spliceosome. Mol. Cell 36, 593-608 (2009).
27. Ohrt, T. et al. Prp2-mediated protein rearrangements at the catalytic core of the spliceosome as revealed by dcFCCS. RNA 18, 1244-1256 (2012).
28. Warkocki, Z. et al. Reconstitution of both steps of Saccharomyces cerevisiae splicing with purified spliceosomal components. Nat. Struct. Mol. Biol. 16, 1237-1243 (2009).
29. Gozani, O., Feld, R., Reed, R. Evidence that sequence-independent binding of highly conserved U2 snRNP proteins upstream of the branch site is required for assembly of spliceosomal complex A. Genes Dev. 10, 233-243 (1996).
30. McPheeters, D.S., Muhlenkamp, P. Spatial organization of protein-RNA interactions in the branch site-3? splice site region during pre-mRNA splicing in yeast. Mol. Cell. Biol. 23, 4174-4186 (2003).
31. Will, C.L. et al. A novel U2 and U11/U12 snRNP protein that associates with the pre-mRNA branch site. EMBO J. 20, 4536-4546 (2001).
32. Schellenberg, M.J. et al. Crystal structure of a core spliceosomal protein interface. Proc. Natl. Acad. Sci. USA 103, 1266-1271 (2006).
33. Kuwasako, K. et al. Complex assembly mechanism and an RNA-binding mode of the human p14-SF3b155 spliceosomal protein complex identified by NMR solution structure and functional analyses. Proteins 71, 1617-1636 (2008).
34. Martin-Tumasz, S., Richie, A.C., Clos, L.J. II, Brow, D.A., Butcher, S.E. A novel occluded RNA recognition motif in Prp24 unwinds the U6 RNA internal stem loop. Nucleic Acids Res. 39, 7837-7847 (2011).
35. Netter, C., Weber, G., Benecke, H., Wahl, M.C. Functional stabilization of an RNA recognition motif by a noncanonical N-terminal expansion. RNA 15, 1305-1313 (2009).
36. Avis, J.M. et al. 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 (1996).
37. Golovanov, A.P., Hautbergue, G.M., Tintaru, A.M., Lian, L.Y., Wilson, S.A. The solution structure of REF2-I reveals interdomain interactions and regions involved in binding mRNA export factors and RNA. RNA 12, 1933-1948 (2006).
38. Cléry, A. et al. Molecular basis of purine-rich RNA recognition by the human SR-like protein Tra2-?1. Nat. Struct. Mol. Biol. 18, 443-450 (2011).
39. Singh, M. et al. Structural basis for telomerase RNA recognition and RNP assembly by the holoenzyme La family protein p65. Mol. Cell 47, 16-26 (2012).
40. Weber, G., Trowitzsch, S., Kastner, B., Luhrmann, R., Wahl, M.C. Functional organization of the Sm core in the crystal structure of human U1 snRNP. EMBO J. 29, 4172-4184 (2010).
41. Varani, L. et al. 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 (2000).
42. Williamson, J.R. Cooperativity in macromolecular assembly. Nat. Chem. Biol. 4, 458-465 (2008).
43. Berglund, J.A., Abovich, N., Rosbash, M. A cooperative interaction between U2AF65 and mBBP/SF1 facilitates branchpoint region recognition. Genes Dev. 12, 858-867 (1998).
44. Corsini, L. et al. Dimerization and protein binding specificity of the U2AF homology motif of the splicing factor Puf60. J. Biol. Chem. 284, 630-639 (2009).
45. De Guzman, R.N., Goto, N.K., Dyson, H.J., Wright, P.E. Structural basis for cooperative transcription factor binding to the CBP coactivator. J. Mol. Biol. 355, 1005-1013 (2006).
46. Brüschweiler, S. et al. Direct observation of the dynamic process underlying allosteric signal transmission. J. Am. Chem. Soc. 131, 3063-3068 (2009).
47. Hom, R.A. et al. Molecular mechanism of MLL PHD3 and RNA recognition by the Cyp33 RRM domain. J. Mol. Biol. 400, 145-154 (2010).
48. Cléry, A., Blatter, M., Allain, F.H. RNA recognition motifs: boring? Not quite. Curr. Opin. Struct. Biol. 18, 290-298 (2008).
49. Daubner, G.M., Clery, A., Allain, F.H. RRM-RNA recognition: NMR or crystallography.and new findings. Curr. Opin. Struct. Biol. 23, 100-108 (2013).
50. Daubner, G.M., Clery, A., Jayne, S., Stevenin, J., Allain, F.H. A syn-anti conformational difference allows SRSF2 to recognize guanines and cytosines equally well. EMBO J. 31, 162-174 (2012).
51. Oberstrass, F.C. et al. Structure of PTB bound to RNA: specific binding and implications for splicing regulation. Science 309, 2054-2057 (2005).
52. Tsuda, K. et al. Structural basis for the dual RNA-recognition modes of human Tra2-beta RRM. Nucleic Acids Res. 39, 1538-1553 (2011).
53. Cléry, A. et al. Isolated pseudo-RNA-recognition motifs of SR proteins can regulate splicing using a noncanonical mode of RNA recognition. Proc. Natl. Acad. Sci. USA 110, E2802-E2811 (2013).
54. Williams, S.G., Hall, K.B. Binding affinity and cooperativity control U2B?/snRNA/U2A? RNP formation. Biochemistry 53, 3727-3737 (2014).
55. Williams, S.G., Hall, K.B. Linkage and allostery in snRNP protein/RNA complexes. Biochemistry 53, 3529-3539 (2014).
56. Sattler, M., Schleucher, J., Griesinger, C. Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Prog. Nucl. Magn. Reson. Spectrosc. 34, 93-158 (1999).
57. Yamazaki, T., Forman-Kay, J.D., Kay, L.E. Two-dimensional NMR experiments for correlating 13C? and 1H?/?. chemical shifts of aromatic residues in 13C-labeled proteins via scalar couplings. J. Am. Chem. Soc. 115, 11054-11055 (1993).
58. Bax, A., Clore, G.M., Gronenborn, A.M. 1H-1H correlation via isotropic mixing of 13C magnetization, a new three-dimensional approach for assigning 1H and 13C spectra of 13C-enriched proteins. J. Magn. Reson. 88, 425-431 (1990).
59. Zwahlen, C. et al. Methods for measurement of intermolecular NOEs by multinuclear NMR spectroscopy: application to a bacteriophage ? N-peptide/boxB RNA complex. J. Am. Chem. Soc. 119, 6711-6721 (1997).
60. Delaglio, F. et al. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293 (1995).
61. Vranken, W.F. et al. The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59, 687-696 (2005).
62. Yao, L., Ying, J., Bax, A. Improved accuracy of 15N-1H scalar and residual dipolar couplings from gradient-enhanced IPAP-HSQC experiments on protonated proteins. J. Biomol. NMR 43, 161-170 (2009).
63. Permi, P., Heikkinen, S., Kilpelainen, I., Annila, A. Measurement of 1JNC? and 2JHNC? couplings from spin-state-selective two-dimensional correlation spectrum. J. Magn. Reson. 140, 32-40 (1999).
64. Zweckstetter, M. NMR: prediction of molecular alignment from structure using the PALES software. Nat. Protoc. 3, 679-690 (2008).
65. Pagano, K. et al. Direct and allosteric inhibition of the FGF2/HSPGs/FGFR1 ternary complex formation by an antiangiogenic, thrombospondin-1-mimic small molecule. PLoS ONE 7, e36990 (2012).
66. Schanda, P., Kupce, E., Brutscher, B. SOFAST-HMQC experiments for recording two-dimensional heteronuclear correlation spectra of proteins within a few seconds. J. Biomol. NMR 33, 199-211 (2005).
67. Güntert, P., Mumenthaler, C., Wuthrich, K. Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 273, 283-298 (1997).
68. Nederveen, A.J. et al. RECOORD: a recalculated coordinate database of 500+ proteins from the PDB using restraints from the BioMagResBank. Proteins 59, 662-672 (2005).
69. Schwieters, C.D., Kuszewski, J.J., Tjandra, N., Clore, G.M. The Xplor-NIH NMR molecular structure determination package. J. Magn. Reson. 160, 65-73 (2003).
70. Humphrey, W., Dalke, A., Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38 (1996).
71. Baker, N.A., Sept, D., Joseph, S., Holst, M.J., McCammon, J.A. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. USA 98, 10037-10041 (2001).
72. Yean, S.L., Lin, R.J. U4 small nuclear RNA dissociates from a yeast spliceosome and does not participate in the subsequent splicing reaction. Mol. Cell. Biol. 11, 5571-5577 (1991).
73. Puig, O. et al. The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 24, 218-229 (2001).
74. Moore, M.J., Sharp, P.A. Site-specific modification of pre-mRNA: the 2?-hydroxyl groups at the splice sites. Science 256, 992-997 (1992).
75. Silverman, S.K., Baum, D.A. Use of deoxyribozymes in RNA research. Methods Enzymol. 469, 95-117 (2009).
76. Urlaub, H., Hartmuth, K., Kostka, S., Grelle, G., Luhrmann, R. A general approach for identification of RNA-protein cross-linking sites within native human spliceosomal small nuclear ribonucleoproteins (snRNPs). Analysis of RNA-protein contacts in native U1 and U4/U6.U5 snRNPs. J. Biol. Chem. 275, 41458-41468 (2000).