Functional organization of the Sm core in the crystal structure of human U1 snRNP

EMBO Journal

Volumn 29, Issue 24, 2010, Pages 4172-4184

  Weber, Gert ^a,b   Trowitzsch, Simon ^a,c   Kastner, Berthold ^a   Lührmann, Reinhard ^a   Wahl, Markus C ^a,b  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

Author keywords

pre mRNA splicing; RNA protein complex; Sm core RNP; U1 small nuclear ribonucleoprotein particle; X ray crystallography

Indexed keywords

CHYMOTRYPSIN; PROTEIN SM; PROTEIN SM1; PROTEIN SM2; SMALL NUCLEAR RIBONUCLEOPROTEIN; SMALL NUCLEAR RNA; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; CRYSTALLIZATION; HUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN SECONDARY STRUCTURE;

CRYSTALLOGRAPHY, X-RAY; HUMANS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; RIBONUCLEOPROTEIN, U1 SMALL NUCLEAR; RNA;

EID: 78650273324     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.295     Document Type: Article

References (47)

1. 0- end of U6 snRNA, thereby facilitating U4/U6 duplex formation in vitro. EMBO J 18: 5789-5802
2. Avis JM, Allain FH, Howe PW, Varani G, Nagai K, 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
3. Bessonov S, Anokhina M, Will CL, Urlaub H, Lührmann R (2008) Isolation of an active step I spliceosome and composition of its RNP core. Nature 452: 846-850
4. Branlant C, Krol A, Ebel JP, Lazar E, Haendler B, Jacob M (1982) U2 RNA shares a structural domain with U1, U4, and U5 RNAs. EMBO J 1: 1259-1265
5. Chari A, Paknia E, Fischer U (2009) The role of RNP biogenesis in spinal muscular atrophy. Curr Opin Cell Biol 21 : 387-393
6. 0 end of U2 snRNA is in close proximity to U1 and functional sites of the pre-mRNA in early spliceosomal complexes. Mol Cell 25: 399-411
7. Duckett DR, Murchie AI, Lilley DM (1995) The global folding of four-way helical junctions in RNA, including that in U1 snRNA. Cell 83: 1027-1036
8. Fabrizio P, Dannenberg J, Dube P, Kastner B, Stark H, Urlaub H, Lührmann R (2009) The evolutionarily conserved core design of the catalytic activation step of the yeast spliceosome. Mol Cell 36: 593-608
9. Friesen WJ, Paushkin S, Wyce A, Massenet S, Pesiridis GS, Van Duyne G, Rappsilber J, Mann M, Dreyfuss G (2001) The methylosome, a 20S complex containing JBP1 and pICln, produces dimethylarginine-modified Sm proteins. Mol Cell Biol 21: 8289-8300
10. Fury MG, Zhang W, Christodoulopoulos I, Zieve GW (1997) Multiple protein: protein interactions between the snRNP common core proteins. Exp Cell Res 237: 63-69
11. Graveley BR, Maniatis T (1998) Arginine/serine-rich domains of SR proteins can function as activators of pre-mRNA splicing. Mol Cell 1: 765-771
12. Hartmuth K, Raker VA, Huber J, Branlant C, 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
13. Hu J, Xu D, Schappert K, Xu Y, Friesen JD (1995) Mutational analysis of Saccharomyces cerevisiae U4 small nuclear RNA identifies functionally important domains. Mol Cell Biol 15: 1274-1285
14. Jarmolowski A, Mattaj IW (1993) The determinants for Sm protein binding to Xenopus U1 and U5 snRNAs are complex and non-identical. EMBO J 12: 223-232
15. Jones MH, Guthrie C (1990) Unexpected flexibility in an evolutio-narily conserved protein-RNA interaction: genetic analysis of the Sm binding site. EMBO J 9: 2555-2561
16. Kambach C, Walke S, Young R, Avis JM, de la Fortelle E, Raker VA, Lührmann R, Li J, Nagai K (1999) Crystal structures of two Sm protein complexes and their implications for the assembly of the spliceosomal snRNPs. Cell 96: 375-387
17. Kastner B, Bach M, Lührmann R (1990) Electron microscopy of small nuclear ribonucleoprotein (snRNP) particles U2 and U5: evidence for a common structure-determining principle in the major U snRNP family. Proc Natl Acad Sci USA 87: 1710-1714
18. Kastner B, Lührmann R (1999) Purification of U small nuclear ribonucleoprotein particles. Methods Mol Biol 118: 289-298
19. Keel AY, Rambo RP, Batey RT, Kieft JS (2007) A general strategy to solve the phase problem in RNA crystallography. Structure 15: 761-772
20. Khusial P, Plaag R, Zieve GW (2005) LSm proteins form heptameric rings that bind to RNA via repeating motifs. Trends Biochem Sci 30: 522-528
21. Kolb SJ, Battle DJ, Dreyfuss G (2007) Molecular functions of the SMN complex. J Child Neurol 22: 990-994
22. Kolev NG, Steitz JA (2006) In vivo assembly of functional U7 snRNP requires RNA backbone flexibility within the Sm-binding site. Nat Struct Mol Biol 13: 347-353
23. Krol A, Westhof E, Bach M, Lührmann R, Ebel JP, Carbon P (1990) Solution structure of human U1 snRNA. Derivation of a possible three-dimensional model. Nucleic Acids Res 18: 3803-3811
24. Liautard JP, Sri-Widada J, Brunel C, Jeanteur P (1982) Structural organization of ribonucleoproteins containing small nuclear RNAs from HeLa cells. Proteins interact closely with a similar structural domain of U1, U2, U4 and U5 small nuclear RNAs. J Mol Biol 162: 623-643
25. McConnell TS, Lokken RP, Steitz JA (2003) Assembly of the U1 snRNP involves interactions with the backbone of the terminal stem of U1 snRNA. RNA 9: 193-201
26. Meinhart A, Kamenski T, Hoeppner S, Baumli S, Cramer P (2005) A structural perspective of CTD function. Genes Dev 19: 1401-1415
27. Meister G, Eggert C, Buhler D, Brahms H, Kambach C, Fischer U (2001) Methylation of Sm proteins by a complex containing PRMT5 and the putative U snRNP assembly factor pICln. Curr Biol 11 : 1990-1994
28. Nelissen RL, Will CL, van Venrooij WJ, Lührmann R (1994) The association of the U1-specific 70K and C proteins with U1 snRNPs is mediated in part by common U snRNP proteins. EMBO J 13: 4113-4125
29. Oubridge C, Ito N, Evans PR, Teo CH, Nagai K (1994) Crystal structure at 1.92 A resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin. Nature 372: 432-438
30. Pillai RS, Grimmler M, Meister G, Will CL, Lührmann R, Fischer U, Schumperli D (2003) Unique Sm core structure of U7 snRNPs: assembly by a specialized SMN complex and the role of a new component, Lsm11, in histone RNA processing. Genes Dev 17: 2321-2333
31. Pomeranz Krummel DA, Oubridge C, Leung AK, Li J, Nagai K (2009) Crystal structure of human spliceosomal U1 snRNP at 5.5 A resolution. Nature 458: 475-480
32. Raker VA, Hartmuth K, Kastner B, Lührmann R (1999) Spliceosomal U snRNP core assembly: Sm proteins assemble onto an Sm site RNA nonanucleotide in a specific and thermodynamically stable manner. Mol Cell Biol 19: 6554-6565
33. Raker VA, Plessel G, Lührmann 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
34. Sander B, Golas MM, Makarov EM, Brahms H, Kastner B, Lührmann R, 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
35. Schröder GF, Levitt M, Brunger AT (2010) Super-resolution biomo-lecular crystallography with low-resolution data. Nature 464: 1218-1222
36. Scofield DG, Lynch M (2008) Evolutionary diversification of the Sm family of RNA-associated proteins. Mol Biol Evol 25: 2255-2267
37. Seraphin B (1995) Sm and Sm-like proteins belong to a large family: identification of proteins of the U6 as well as the U1, U2, U4 and U5 snRNPs. EMBO J 14: 2089-2098
38. Staley JP, Guthrie C (1998) Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell 92: 315-326
39. Stark H, Dube P, Lührmann R, Kastner B (2001) Arrangement of RNA and proteins in the spliceosomal U1 small nuclear ribonu-cleoprotein particle. Nature 409: 539-542
40. Törö I, Thore S, Mayer C, Basquin J, Seraphin B, Suck D (2001) RNA binding in an Sm core domain: X-ray structure and functional analysis of an archaeal Sm protein complex. EMBO J 20: 2293-2303
41. Urlaub H, Hartmuth K, Kostka S, Grelle G, Lührmann R (2000) A general approach for identification of RNA-protein cross-linking sites within native human spliceosomal small nuclear ribonu-cleoproteins (snRNPs). Analysis of RNA-protein contacts in native U1 and U4/U6.U5 snRNPs. J Biol Chem 275: 41458-41468
42. Urlaub H, Raker VA, Kostka S, Lührmann R (2001) Sm protein-Sm site RNA interactions within the inner ring of the spliceosomal snRNP core structure. EMBO J 20: 187-196
43. Wahl MC, Will CL, Lührmann R (2009) The spliceosome: design principles of a dynamic RNP machine. Cell 136: 701-718
44. Warkocki Z, Odenwalder P, Schmitzova J, Platzmann F, Stark H, Urlaub H, Ficner R, Fabrizio P, Lührmann R (2009) Reconstitution of both steps of Saccharomyces cerevisiae splicing with purified spliceosomal components. Nat Struct Mol Biol 16: 1237-1243
45. Xiao SH, Manley JL (1997) Phosphorylation of the ASF/SF2 RS domain affects both protein-protein and protein-RNA interactions and is necessary for splicing. Genes Dev 11 : 334-344
46. Zhang D, Abovich N, Rosbash M (2001) A biochemical function for the Sm complex. Mol Cell 7: 319-329
47. Zhang D, Rosbash M (1999) Identification of eight proteins that cross-link to pre-mRNA in the yeast commitment complex. Genes Dev 13: 581-592