Crystal structure of U2 snRNP SF3b components: Hsh49p in complex with Cus1p-binding domain

RNA

Volumn 23, Issue 6, 2017, Pages 968-981

  Van Roon, Anne Marie M ^a   Oubridge, Chris ^a   Obayashi, Eiji ^a,c   Sposito, Benedetta ^a   Newman, Andrew J ^a   Séraphin, Bertrand ^b   Nagai, Kiyoshi ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c SHIMANE UNIVERSITY   (Japan)

Author keywords

RNA binding; RRM; SF3b; Splicing; U2 snRNP

Indexed keywords

CUS1P PROTEIN; DIMER; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HYDROGEN; MONOMER; PROTEIN; RNA; RRM1 PROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN; SMALL NUCLEAR RNA; UNCLASSIFIED DRUG; MULTIPROTEIN COMPLEX; PROTEIN BINDING; RNA BINDING PROTEIN; U2 SMALL NUCLEAR RNA;

AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CROSS LINKING; CRYSTAL; CRYSTAL STRUCTURE; CRYSTALLIZATION; DENSITY; FLUORESCENCE; HILL COEFFICIENT; HYDROGEN BOND; HYDROPHOBICITY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN STRUCTURE; PURIFICATION; RNA BINDING; SACCHAROMYCES CEREVISIAE; SPLICEOSOME; SURFACE AREA; SURFACE PROPERTY; AMINO ACID SEQUENCE; CHEMISTRY; CONSERVED SEQUENCE; GENETICS; METABOLISM; MOLECULAR MODEL; PROLINE RICH PROTEIN DOMAIN; PROTEIN CONFORMATION; PROTEIN DOMAIN;

AMINO ACID SEQUENCE; BINDING SITES; CONSERVED SEQUENCE; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; PROLINE-RICH PROTEIN DOMAINS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; RIBONUCLEOPROTEIN, U2 SMALL NUCLEAR; RNA; RNA, SMALL NUCLEAR; RNA-BINDING PROTEINS;

EID: 85019934461     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.059378.116     Document Type: Article

References (59)

1. Afroz T, Skrisovska L, Belloc E, Guillén-Boixet J, Méndez R, Allain FH-T. 2014. A fly trap mechanism provides sequence-specific RNA recognition by CPEB proteins. Genes Dev 28: 1498-1514.
2. Bae E, Reiter NJ, Bingman CA, Kwan SS, Lee D, Phillips GN, Butcher SE, Brow DA 2007. Structure and interactions of the first three RNA recognition motifs of splicing factor prp24. J Mol Biol 367: 1447-1458.
3. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. 2001. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci 98: 10037-10041.
4. Barraud P, Allain FHT. 2013. Solution structure of the two RNA recognition motifs of hnRNP A1 using segmental isotope labeling: how the relative orientation between RRMs influences the nucleic acid binding topology. J Biomol NMR 55: 119-138.
5. Bertram K, Agafonov DE, Liu W-T, Dybkov O, Will CL, Hartmuth K, Urlaub H, Kastner B, Stark H, Lührmann R. 2017. Cryo-EM structure of a human spliceosome activated for step 2 of splicing. Nature 542: 318-323.
6. Blatter M, Dunin-Horkawicz S, Grishina I, Maris C, Thore S, Maier T, Bindereif A, Bujnicki JM, Allain FHT. 2015. The signature of the five-stranded vRRM fold defined by functional, structural and computational analysis of the hnRNP L protein. J Mol Biol 427: 3001-3022.
7. Cléry A., Blatter M, Allain FHT. 2008. RNA recognition motifs: boring? Not quite. Curr Opin Struct Biol 18: 290-298.
8. Collaborative Computational Project, Number 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
9. Cretu C, Schmitzová J, Ponce-Salvatierra A, Dybkov O, De Laurentiis EI, Sharma K, Will CL, Urlaub H, Lührmann R, Pena V. 2016. Molecular architecture of SF3b and structural consequences of its cancer-related mutations. Mol Cell 64: 307-319.
10. Deo RC, Bonanno JB, Sonenberg N, Burley SK 1999. Recognition of polyadenylate RNA by the poly(A)-binding protein. Cell 98: 835-845.
11. Dolinsky TJ, Czodrowski P, Li H, Nielsen JE, Jensen JH, Klebe G, Baker NA 2007. PDB2PQR: expanding and upgrading automated preparation of biomolecular structures for molecular simulations. Nucleic Acids Res 35: W522-W525.
12. Dybkov O, Will CL, Deckert J, Behzadnia N, Hartmuth K, Lührmann R. 2006. U2 snRNA-protein contacts in purified human 17S U2 snRNPs and in spliceosomal A and B complexes. Mol Cell Biol 26: 2803-2816.
13. Dziembowski A, Ventura AP, Rutz B, Caspary F, Faux C, Halgand F, Laprevote O, Séraphin B. 2004. Proteomic analysis identifies a new complex required for nuclear pre-mRNA retention and splicing. EMBO J 23: 4847-4856.
14. Elantak L, Wagner S, Herrmannová A, Karásková M, Rutkai E, Lukavsky PJ, Valásek L. 2010. The indispensable N-terminal half of eIF3j/HCR1 cooperates with its structurally conserved binding partner eIF3b/PRT1-RRM and with eIF1A in stringent AUG selection. J Mol Biol 396: 1097-1116.
15. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486-501.
16. Evans P. 2006. Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62: 72-82.
17. Falk S, Finogenova K, Melko M, Benda C, Lykke-Andersen S, Jensen TH, Conti E. 2016. Structure of the RBM7-ZCCHC8 core of the NEXT complex reveals connections to splicing factors. Nat Commun 7: 13573.
18. Fica SM, Oubridge C, Galej WP, Wilkinson ME, Bai X-C, Newman AJ, Nagai K. 2017. Structure of a spliceosome remodelled for exon ligation. Nature 542: 377-380.
19. Galej WP, Wilkinson ME, Fica SM, Oubridge C, Newman AJ, Nagai K. 2016. Cryo-EM structure of the spliceosome immediately after branching. Nature 537: 197-201.
20. García-Nafría J, Watson JF, Greger IH. 2016. IVA cloning: a single-tube universal cloning system exploiting bacterial In Vivo Assembly. Sci Rep 6: 27459.
21. Golas MM, Sander B, Will CL, Lührmann R, Stark H. 2003. Molecular architecture of the multiprotein splicing factor SF3b. Science 300: 980-984.
22. Hardin JW, Warnasooriya C, Kondo Y, Nagai K, Rueda D. 2015. Assembly and dynamics of the U4/U6 di-snRNP by single-molecule FRET. Nucleic Acids Res 43: 10963-10974.
23. Hom RA, Chang P-Y, Roy S, Musselman CA, Glass KC, Selezneva AI, Gozani O, Ismagilov RF, Cleary ML, Kutateladze TG. 2010. Molecular mechanism of MLL PHD3 and RNA recognition by the Cyp33 RRM domain. J Mol Biol 400: 145-154.
24. Igel H, Wells S, Perriman R, Ares MJ 1998. Conservation of structure and subunit interactions in yeast homologues of splicing factor 3b (SF3b) subunits. RNA 4: 1-10.
25. Joosten RP, Joosten K, Cohen SX, Vriend G, Perrakis A. 2011. Automatic rebuilding and optimization of crystallographic structures in the Protein Data Bank. Bioinformatics 27: 3392-3398.
26. Kabsch W. 2010. XDS. Acta Crystallogr D Biol Crystallogr 66: 125-132.
27. Kielkopf CL, Rodionova NA, Green MR, Burley SK 2001. A novel peptide recognition mode revealed by the X-ray structure of a core U2AF35/U2AF65 heterodimer. Cell 106: 595-605.
28. Kielkopf CL, Lücke S, Green MR 2004. U2AF homology motifs: protein recognition in the RRM world. Genes Dev 18: 1513-1526.
29. Krämer A., Grüter P, Gröning K, Kastner B. 1999. Combined biochemical and electron microscopic analyses reveal the architecture of the mammalian U2 snRNP. J Cell Biol 145: 1355-1368.
30. Krissinel E, Henrick K. 2007. Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: 774-797.
31. Kuwasako K, Nameki N, Tsuda K, Takahashi M, Sato A, Tochio N, Inoue M, Terada T, Kigawa T, Kobayashi N, et al. 2016. Solution structure of the first RNA recognition motif domain of human spli-ceosomal protein SF3b49 and its mode of interaction with a SF3b145 fragment. Protein Sci 26: 280-291.
32. Langer G, Cohen SX, Lamzin VS, Perrakis A. 2008. Automated macro-molecular model building for X-ray crystallography using ARP/ wARP version 7. Nat Protoc 3: 1171-1179.
33. Long F, Vagin AA, Young P, Murshudov GN 2008. BALBES: a molecular-replacement pipeline. Acta Crystallogr D Biol Crystallogr 64: 125-132.
34. Massenet S, Motorin Y, Lafontaine DL, Hurt EC, Grosjean H, Branlant C. 1999. Pseudouridine mapping in the Saccharomyces cer-evisiae spliceosomal U small nuclear RNAs (snRNAs) reveals that pseudouridine synthase pus1p exhibits a dual substrate specificity for U2 snRNA and tRNA. Mol Cell Biol 19: 2142-2154.
35. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
36. McLeod M, Stein M, Beach D. 1987. The product of the mei3+ gene, expressed under control of the mating-type locus, induces meiosis and sporulation in fission yeast. EMBO J 6: 729-736.
37. Milligan JF, Groebe DR, Witherell GW, Uhlenbeck OC 1987. Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucleic Acids Res 15: 8783-8798.
38. Montemayor EJ, Curran EC, Liao HH, Andrews KL, Treba CN, Butcher SE, Brow DA 2014. Core structure of the U6 small nuclear ribonucleoprotein at 1.7-Å resolution. Nat Struct Mol Biol 21: 544-551.
39. Murshudov GN, Skubák P, Lebedev AA, Pannu NS, Steiner RA, Nicholls RA, Winn MD, Long F, Vagin AA 2011. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr D Biol Crystallogr 67: 355-367.
40. Muto Y, Yokoyama S. 2012. Structural insight into RNA recognition motif: versatile molecular Lego building blocks for biological systems. WIREs RNA 3: 229-246.
41. Ohrt T, Prior M, Dannenberg J, Odenwälder P, Dybkov O, Rasche N, Schmitzová J, Gregor I, Fabrizio P, Enderlein J, et al. 2012. Prp2-me-diated protein rearrangements at the catalytic core of the spliceo-some as revealed by dcFCCS. RNA 18: 1244-1256.
42. Pauling MH, McPheeters DS, Ares MJ. 2000. Functional Cus1p is found with Hsh155p in a multiprotein splicing factor associated with U2 snRNA. Mol Cell Biol 20: 2176-2185.
43. Perrakis A, Sixma TK, Wilson KS, Lamzin VS 1997. wARP: improvement and extension of crystallographic phases by weighted averaging of multiple-refined dummy atomic models. Acta Crystallogr D Biol Crystallogr 53: 448-455.
44. Price SR, Evans PR, Nagai K. 1998. Crystal structure of the spliceosomal U2B''-U2A' protein complex bound to a fragment of U2 small nuclear RNA. Nature 394: 645-650.
45. Rauhut R, Fabrizio P, Dybkov O, Hartmuth K, Pena V, Chari A, Kumar V, Lee C-T, Urlaub H, Kastner B, et al. 2016. Molecular architecture of the Saccharomyces cerevisiae activated spliceosome. Science 353: 1399-1405.
46. Schneider C, Agafonov DE, Schmitzová J, Hartmuth K, Fabrizio P, Lührmann R. 2015. Dynamic contacts of U2, RES, Cwc25, Prp8 and Prp45 proteins with the pre-mRNA branch-site and 3' splice site during catalytic activation and step 1 catalysis in yeast spliceo-somes. PLoS Genet 11: e1005539.
47. Thorn A, Sheldrick GM 2013. Extending molecular-replacement solutions with SHELXE. Acta Crystallogr D Biol Crystallogr 69: 2251-2256.
48. van der Feltz C, Anthony K, Brilot A, Pomeranz Krummel DA. 2012. Architecture of the spliceosome. Biochemistry 51: 3321-3333.
49. van Roon AMM, Loening NM, Obayashi E, Yang J-C, Newman AJ, Hernández H, Nagai K, Neuhaus D. 2008. Solution structure of the U2 snRNP protein Rds3p reveals a knotted zinc-finger motif. Proc Natl Acad Sci 105: 9621-9626.
50. Vitali F, Henning A, Oberstrass FC, Hargous Y, Auweter SD, Erat M, Allain FHT. 2006. Structure of the two most C-terminal RNA recognition motifs of PTB using segmental isotope labeling. EMBO J 25: 150-162.
51. Wahl MC, Will CL, Lührmann R. 2009. The spliceosome: design principles of a dynamic RNP machine. Cell 136: 701-718.
52. Wan R, Yan C, Bai R, Huang G, Shi Y. 2016. Structure of a yeast catalytic step I spliceosome at 3.4 Å resolution. Science 353: 895-904.
53. Wells SE, Neville M, Haynes M, Wang J, Igel H, Ares M. 1996. CUS1, a suppressor of cold-sensitive U2 snRNA mutations, is a novel yeast splicing factor homologous to human SAP 145. Genes Dev 10: 220-232.
54. Will CL, Lührmann R. 2011. Spliceosome structure and function. Cold Spring Harb Perspect Biol 3: a003707.
55. Will CL, Schneider C, MacMillan AM, Katopodis NF, Neubauer G, Wilm M, Lührmann R, Query CC. 2001. A novel U2 and U11/ U12 snRNP protein that associates with the pre-mRNA branch site. EMBO J 20: 4536-4546.
56. Winter G. 2010. xia2: an expert system for macromolecular crystallography data reduction. J Appl Crystallogr 43: 186-190.
57. Yan C, Wan R, Bai R, Huang G, Shi Y. 2016. Structure of a yeast activated spliceosome at 3.5 Å resolution. Science 353: 904-911.
58. Yan C, Wan R, Bai R, Huang G, Shi Y. 2017. Structure of a yeast step II catalytically activated spliceosome. Science 355: 149-155.
59. Zhang Z, Sauter NK, van den Bedem H, Snell G, Deacon AM. 2006. Automated diffraction image analysis and spot searching for high-throughput crystal screening. J Appl Crystallogr 39: 112-119.