Structure and assembly of the SF3a splicing factor complex of U2 snRNP

EMBO Journal

Volumn 31, Issue 6, 2012, Pages 1579-1590

  Lin, Pei Chun ^a   Xu, Rui Ming ^a,b  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUTE OF BIOPHYSICS   (China)

Author keywords

protein structure; RNA splicing; U2 snRNP; X ray crystallography

Indexed keywords

PRION PROTEIN; PRION PROTEIN 11; PRION PROTEIN 21; PRION PROTEIN 9; PROTEIN SF3A; SMALL NUCLEAR RNA; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BIOCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

BINDING SITES; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN SUBUNITS; RIBONUCLEOPROTEIN, U2 SMALL NUCLEAR; RNA SPLICING; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84858800333     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.7     Document Type: Article

References (55)

1. Abovich N, Legrain P, Rosbash M (1990) The yeast PRP6 gene encodes a U4/U6 small nuclear ribonucleoprotein particle (snRNP) protein, and the PRP9 gene encodes a protein required for U2 snRNP binding. Mol Cell Biol 10: 6417-6425 (Pubitemid 120004585)
2. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung L-W, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D 66: 213-221
3. Aravind L, Koonin EV (2000) The U box is a modified RING finger-a common domain in ubiquitination. Curr Biol 10: R132-R134 (Pubitemid 30146770)
4. Arenas JE, Abelson JN (1993) The Saccharomyces cerevisiae PRP21 gene product is an integral component of the prespliceosome. Proc Natl Acad Sci USA 90: 6771-6775 (Pubitemid 23207295)
5. Ares Jr M, Igel AH (1990) Lethal and temperature-sensitive mutations and their suppressors identify an essential structural element in U2 small nuclear RNA. Genes Dev 4: 2132-2145 (Pubitemid 120034520)
6. Behrens SE, Tyc K, Kastner B, Reichelt J, Lührmann R (1993) Small nuclear ribonucleoprotein (RNP) U2 contains numerous additional proteins and has a bipartite RNP structure under splicing conditions. Mol Cell Biol 13: 307-319 (Pubitemid 23006908)
7. Bennett M, Reed R (1993) Correspondence between a mammalian spliceosome component and an essential yeast splicing factor. Science 262: 105-108
8. Berget SM, Moore C, Sharp PA (1977) Spliced segments at the 50 terminus of adenovirus 2 late mRNA. Proc Natl Acad Sci USA 74: 3171-3175 (Pubitemid 8180310)
9. Bessonov S, Anokhina M, Krasauskas A, Golas MM, Sander B, Will CL, Urlaub H, Stark H, Luhrmann R (2010) Characterization of purified human Bact spliceosomal complexes reveals compositional and morphological changes during spliceosome activation and first step catalysis. RNA 16: 2384-2403
10. Boelens W, Scherly D, Beijer RP, Jansen EJR, Dathan NA, Mattaj lW, Venrooij WJv (1991) Aweak interaction between the U2A0 protein and U2 snRNA helps to stabilize their complex with the U2B00 protein. Nucleic Acids Res 19: 455-460 (Pubitemid 21897026)
11. Brody E, Abelson J (1985) The 'spliceosome': yeast pre-messenger RNA associates with a 40S complex in a splicing-dependent reaction. Science 228: 963-967 (Pubitemid 15028386)
12. Brosi R, Groning K, Behrens SE, Lührmann R, Krämer A (1993a) Interaction of mammalian splicing factor SF3a with U2 snRNP and relation of its 60-kD subunit to yeast PRP9. Science 262: 102-105 (Pubitemid 23338878)
13. Brosi R, Hauri HP, Krämer A (1993b) Separation of splicing factor SF3 into two components and purification of SF3a activity. J Biol Chem 268: 17640-17646 (Pubitemid 23237012)
14. Chang TH, Clark MW, Lustig AJ, Cusick ME, Abelson J (1988) RNA11 protein is associated with the yeast spliceosome and is localized in the periphery of the cell nucleus. Mol Cell Biol 8: 2379-2393
15. Chiara MD, Champion-Arnaud P, Buvoli M, Nadal-Ginard B, Reed R (1994) Specific protein-protein interactions between the essential mammalian spliceosome-associated proteins SAP 61 and SAP 114. Proc Natl Acad Sci USA 91: 6403-6407 (Pubitemid 24200669)
16. Chow LT, Gelinas RE, Broker TR, Roberts RJ (1977) An amazing sequence arrangement at the 50 ends of adenovirus 2 messenger RNA. Cell 12: 1-8 (Pubitemid 8193727)
17. 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
18. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D 66: 486-501
19. Golas MM, Sander B, Will CL, Lührmann R, Stark H (2003) Molecular architecture of the multiprotein splicing factor SF3b. Science 300: 980-984 (Pubitemid 36548885)
20. Hilliker AK, Mefford MA, Staley JP (2007) U2 toggles iteratively between the stem IIa and stem IIc conformations to promote premRNA splicing. Genes Dev 21: 821-834 (Pubitemid 46572361)
21. Huang CJ, Ferfoglia F, Raleff F, Krämer A (2011) Interaction domains and nuclear targeting signals in subunits of the U2 small nuclear ribonucleoprotein particle-associated splicing factor SF3a. J Biol Chem 286: 13106-13114
22. Igel AH, Ares M (1988) Internal sequences that distinguish yeast from metazoan U2 snRNA are unnecessary for pre-mRNA splicing. Nature 334: 450-453
23. Jurica MS, Moore MJ (2003) Pre-mRNA splicing: awash in a sea of proteins. Mol Cell 12: 5-14 (Pubitemid 36945033)
24. Kim KK, Kim R, Kim SH (1998) Crystal structure of a small heatshock protein. Nature 394: 595-599 (Pubitemid 28366837)
25. Krämer A (1996) The structure and function of proteins involved in mammalian pre-mRNA splicing. Annl Rev Biochem 65: 367-409 (Pubitemid 26250614)
26. Krämer A, Ferfoglia F, Huang CJ, Mulhaupt F, Nesic D, Tanackovic G (2005) Structure-function analysis of the U2 snRNP-associated splicing factor SF3a. Biochem Soc Trans 33: 439-442 (Pubitemid 40873860)
27. Krämer A, Gruter P, Groning K, Kastner B (1999) Combined biochemical and electron microscopic analyses reveal the architecture of the mammalian U2 snRNP. J Cell Biol 145: 1355-1368 (Pubitemid 29309995)
28. Krämer A, Legrain P, Mulhauser F, Gröning K, Brosi R, Bilbe G (1994) Splicing factor SF3a60 is the mammalian homologue of PRP9 of S. cerevisiae: the conserved zinc finger-like motif is functionally exchangeable in vivo. Nucleic Acids Res 22: 5223-5228
29. Krämer A, Mulhauser F, Wersig C, Gröning K, Bilbe G (1995) Mammalian splicing factor SF3a120 represents a new member of the SURP family of proteins and is homologous to the essential splicing factor PRP21p of Saccharomyces cerevisiae. RNA 1: 260-272
30. Kuwasako K, He F, Inoue M, Tanaka A, Sugano S, Güntert P, Muto Y, Yokoyama S (2006) Solution structures of the SURP domains and the subunit-assembly mechanism within the splicing factor SF3a complex in 17S U2 snRNP. Structure 14: 1677-1689 (Pubitemid 46107275)
31. Lardelli RM, Thompson JX, Yates III JR, Stevens SW (2010) Release of SF3 from the intron branchpoint activates the first step of premRNA splicing. RNA 16: 516-528
32. Legrain P, Chapon C (1993) Interaction between PRP11 and SPP91 yeast splicing factors and characterization of a PRP9-PRP11-SPP91 complex. Science 262: 108-110 (Pubitemid 23338880)
33. Legrain P, Choulika A (1990) The molecular characterization of PRP6 and PRP9 yeast genes reveals a new cysteine/histidine motif common to several splicing factors. EMBO J 9: 2775-2781
34. Leung AK, Nagai K, Li J (2011) Structure of the spliceosomal U4 snRNP core domain and its implication for snRNP biogenesis. Nature 473: 536-539
35. Muto Y, Pomeranz Krummel D, Oubridge C, Hernandez H, Robinson CV, Neuhaus D, Nagai K (2004) The structure and biochemical properties of the human spliceosomal protein U1C. J Mol Biol 341: 185-198 (Pubitemid 39090644)
36. Nesic D, Krämer A (2001) Domains in human splicing factors SF3a60 and SF3a66 required for binding to SF3a120, assembly of the 17S U2 snRNP, and prespliceosome formation. Mol Cell Biol 21: 6406-6417 (Pubitemid 32927409)
37. Ohi MD, Vander Kooi CW, Rosenberg JA, Chazin WJ, Gould KL (2003) Structural insights into the U-box, a domain associated with multi-ubiquitination. Nat Struct Biol 10: 250-255 (Pubitemid 36418748)
38. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326 (Pubitemid 27085611)
39. Perriman RJ, Ares Jr M (2007) Rearrangement of competing U2 RNA helices within the spliceosome promotes multiple steps in splicing. Genes Dev 21: 811-820 (Pubitemid 46572360)
40. 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
41. Price SR, Evans PR, Nagai K (1998) Crystal structure of the spliceosomal U2B00-U2A0 protein complex bound to a fragment of U2 small nuclear RNA. Nature 394: 645-650 (Pubitemid 28389783)
42. Rain JC, Tartakoff AM, Kramer A, Legrain P (1996) Essential domains of the PRP21 splicing factor are implicated in the binding to PRP9 and PRP11 proteins and are conserved through evolution. RNA 2: 535-550 (Pubitemid 26374226)
43. Ritchie DB, Schellenberg MJ, MacMillan AM (2009) Spliceosome structure: piece by piece. Biochim Biophys Acta 1789: 624-633
44. Ruby SW, Chang TH, Abelson J (1993) Four yeast spliceosomal proteins (PRP5, PRP9, PRP11, and PRP21) interact to promote U2 snRNP binding to pre-mRNA. Genes Dev 7: 1909-1925 (Pubitemid 23312945)
45. Schellenberg MJ, Edwards RA, Ritchie DB, Kent OA, Golas MM, Stark H, Lührmann R, Glover JNM, MacMillan AM (2006) Crystal structure of a core spliceosomal protein interface. Proc Natl Acad Sci USA 103: 1266-1271 (Pubitemid 43191154)
46. Scherly D, Boelens W, Dathan NA, van Venrooij WJ, Mattaj IW (1990) Major determinants of the specificity of interaction between small nuclear ribonucleoproteins U1A and U2B00 and their cognate RNAs. Nature 345: 502-506
47. Shuster EO, Guthrie C (1988) Two conserved domains of yeast U2 snRNA are separated by 945 nonessential nucleotides. Cell 55: 41-48
48. Shuster EO, Guthrie C (1990) Human U2 snRNA can function in premRNA splicing in yeast. Nature 345: 270-273
49. Spikes DA, Kramer J, Bingham PM, Doren KV (1994) SWAP premRNA splicing regulators are a novel, ancient protein family sharing a highly conserved sequence motif with the prp21 family of constitutive splicing proteins. Nucleic Acids Res 22: 4510-4519 (Pubitemid 24336425)
50. Staley JP, Guthrie C (1998) Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell 92: 315-326 (Pubitemid 28093010)
51. Valadkhan S, Jaladat Y (2010) The spliceosomal proteome: at the heart of the largest cellular ribonucleoprotein machine. Proteomics 10: 4128-4141
52. Wahl MC, Will CL, Lührmann R (2009) The spliceosome: design principles of a dynamic RNP machine. Cell 136: 701-718
53. Wells SE, Ares Jr M (1994) Interactions between highly conserved U2 small nuclear RNA structures and Prp5p, Prp9p, Prp11p, and Prp21p proteins are required to ensure integrity of the U2 small nuclear ribonucleoprotein in Saccharomyces cerevisiae. Mol Cell Biol 14: 6337-6349
54. Will CL, Luhrmann R (2011) Spliceosome structure and function. Cold Spring Harb Perspect Biol 3: pii: a003707
55. Yan D, Ares Jr M (1996) Invariant U2 RNA sequences bordering the branchpoint recognition region are essential for interaction with yeast SF3a and SF3b subunits [published erratum appears in Mol Cell Biol 1996 Jul;16(7):3980]. Mol Cell Biol 16: 818-828 (Pubitemid 26061651)