Solution structure of the first RNA recognition motif domain of human spliceosomal protein SF3b49 and its mode of interaction with a SF3b145 fragment

Protein Science

Volumn 26, Issue 2, 2017, Pages 280-291

  Kuwasako, Kanako ^a,b   Nameki, Nobukazu ^c   Tsuda, Kengo ^b   Takahashi, Mari ^b   Sato, Atsuko ^d   Tochio, Naoya ^b,e   Inoue, Makoto ^b   Terada, Takaho ^b   Kigawa, Takanori ^b   Kobayashi, Naohiro ^b   Shirouzu, Mikako ^b   Ito, Takuhiro ^b   Sakamoto, Taiichi ^f   Wakamatsu, Kaori ^c   Güntert, Peter ^g,h   Takahashi, Seizo ^d   Yokoyama, Shigeyuki ^b   Muto, Yutaka ^a,b  

^a MUSASHINO UNIVERSITY   (Japan)

^b RIKEN   (Japan)

^c GUNMA UNIVERSITY   (Japan)

^d JAPAN WOMEN'S UNIVERSITY   (Japan)

^e HIROSHIMA UNIVERSITY   (Japan)

^f CHIBA INSTITUTE OF TECHNOLOGY   (Japan)

^g RIKEN YOKOHAMA INSTITUTE   (Japan)

^h FRANKFURT INSTITUTE FOR ADVANCED STUDIES   (Germany)

Author keywords

nuclear magnetic resonance; RNA recognition motif; SF3b145; SF3b49; U2 snRNP

Indexed keywords

PROTEIN; PROTEIN SF3B145; PROTEIN SF3B49; UNCLASSIFIED DRUG; PROTEIN BINDING; RNA SPLICING FACTOR; SF3B2 PROTEIN, HUMAN; SF3B4 PROTEIN, HUMAN;

ALPHA HELIX; ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CONTROLLED STUDY; HUMAN; MOLECULAR DOCKING; MUTATIONAL ANALYSIS; NITROGEN NUCLEAR MAGNETIC RESONANCE; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RNA RECOGNITION MOTIF; CHEMISTRY; GENETICS; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN MOTIF;

AMINO ACID MOTIFS; HUMANS; MOLECULAR DOCKING SIMULATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN DOMAINS; PROTEIN FOLDING; RNA SPLICING FACTORS;

EID: 85005765115     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.3080     Document Type: Article

References (46)

1. Nelson KK, Green MR (1989) Mammalian U2 snRNP has a sequence-specific RNA-binding activity. Genes Dev 3:1562–1571.
2. Pan ZQ, Prives C (1989) U2 snRNA sequences that bind U2-specific proteins are dispensable for the function of U2 snRNP in splicing. Genes Dev 3:1887–1898.
3. Champion-Arnaud P, Reed R (1994) The prespliceosome components SAP 49 and SAP 145 interact in a complex implicated in tethering U2 snRNP to the branch site. Genes Dev 8:1974–1983.
4. Das BK, Xia L, Palandjian L, Gozani O, Chyung Y, Reed R (1999) Characterization of a protein complex containing spliceosomal proteins SAPs 49, 130, 145, and 155. Mol Cell Biol 19:6796–6802.
5. Gozani O, Feld R, Reed R (1996) 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.
6. Gozani O, Potashkin J, Reed R (1998) A potential role for U2AF-SAP 155 interactions in recruiting U2 snRNP to the branch site. Mol Cell Biol 18:4752–4760.
7. MacMillan AM, Query CC, Allerson CR, Chen S, Verdine GL, Sharp PA (1994) Dynamic association of proteins with the pre-mRNA branch region. Genes Dev 8:3008–3020.
8. Will CL, Urlaub H, Achsel T, Gentzel M, Wilm M, Luhrmann R (2002) Characterization of novel SF3b and 17S U2 snRNP proteins, including a human Prp5p homologue and an SF3b DEAD-box protein. EMBO J 21:4978–4988.
9. Thompson JD, Gibson TJ, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics Chapter 2:Unit 2 3.
10. Tanaka Y, Ohta A, Terashima K, Sakamoto H (1997) Polycistronic expression and RNA-binding specificity of the C. elegans homologue of the spliceosome-associated protein SAP49. J Biochem 121:739–745.
11. Igel H, Wells S, Perriman R, Ares M, Jr (1998) Conservation of structure and subunit interactions in yeast homologues of splicing factor 3b (SF3b) subunits. RNA 4:1–10.
12. Pauling MH, McPheeters DS, Ares M Jr. (2000) Functional Cus1p is found with Hsh155p in a multiprotein splicing factor associated with U2 snRNA. Mol Cell Biol 20:2176–2185.
13. 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.
14. Nagai K, Oubridge C, Ito N, Avis J, Evans P (1995) The RNP domain: a sequence-specific RNA-binding domain involved in processing and transport of RNA. Trends Biochem Sci 20:235–240.
15. Bandziulis RJ, Swanson MS, Dreyfuss G (1989) RNA-binding proteins as developmental regulators. Genes Dev 3:431–437.
16. Burd CG, Dreyfuss G (1994) Conserved structures and diversity of functions of RNA-binding proteins. Science 265:615–621.
17. Perez-Canadillas JM, Varani G (2001) Recent advances in RNA-protein recognition. Curr Opin Struct Biol 11:53–58.
18. Clery A, Blatter M, Allain FH (2008) RNA recognition motifs: boring? Not quite. Curr Opin Struct Biol 18:290–298.
19. Kuwasako K, Dohmae N, Inoue M, Shirouzu M, Taguchi S, Guntert P, Seraphin B, Muto Y, Yokoyama S (2008) 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.
20. Schellenberg MJ, Edwards RA, Ritchie DB, Kent OA, Golas MM, Stark H, Luhrmann R, Glover JN, MacMillan AM (2006) Crystal structure of a core spliceosomal protein interface. Proc Natl Acad Sci USA 103:1266–1271.
21. Kielkopf CL, Lucke S, Green MR (2004) U2AF homology motifs: protein recognition in the RRM world. Genes Dev 18:1513–1526.
22. Güntert P, Buchner L (2015) Combined automated NOE assignment and structure calculation with CYANA. J Biomol NMR 62:453–471.
23. Koradi R, Billeter M, Wüthrich K (1996) MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graph 14:51–55, 29–32.
24. Kurt Wüthrich (1986) NMR of proteins and nucleic acids. New York: Wiley.
25. Case DA, Cheatham TE, III, Darden T, Gohlke H, Luo R, Merz KM, Jr, Onufriev A, Simmerling C, Wang B, Woods RJ (2005) The Amber biomolecular simulation programs. J Comput Chem 26:1668–1688.
26. Murachelli AG, Ebert J, Basquin C, Le Hir H, Conti E (2012) The structure of the ASAP core complex reveals the existence of a Pinin-containing PSAP complex. Nat Struct Mol Biol 19:378–386.
27. Joshi A, Coelho MB, Kotik-Kogan O, Simpson PJ, Matthews SJ, Smith CW, Curry S (2011) Crystallographic analysis of polypyrimidine tract-binding protein-Raver1 interactions involved in regulation of alternative splicing. Structure 19:1816–1825.
28. Wysoczanski P, Becker S, Zweckstetter M (2015) Structures of intermediates during RES complex assembly. Sci Rep 5:12545.
29. Tunnicliffe RB, Hautbergue GM, Kalra P, Jackson BR, Whitehouse A, Wilson SA, Golovanov AP (2011) Structural basis for the recognition of cellular mRNA export factor REF by herpes viral proteins HSV-1 ICP27 and HVS ORF57. PLoS Pathog 7:e1001244.
30. Tunnicliffe RB, Hautbergue GM, Wilson SA, Kalra P, Golovanov AP (2014) Competitive and cooperative interactions mediate RNA transfer from herpesvirus saimiri ORF57 to the mammalian export adaptor ALYREF. PLoS Pathog 10:e1003907.
31. Hashizume C, Kuramitsu M, Zhang X, Kurosawa T, Kamata M, Aida Y (2007) Human immunodeficiency virus type 1 Vpr interacts with spliceosomal protein SAP145 to mediate cellular pre-mRNA splicing inhibition. Microbes Infect 9:490–497.
32. Terada Y, Yasuda Y (2006) Human immunodeficiency virus type 1 Vpr induces G2 checkpoint activation by interacting with the splicing factor SAP145. Mol Cell Biol 26:8149–8158.
33. Yan C, Wan R, Bai R, Huang G, Shi Y (2016) Structure of a yeast activated spliceosome at 3.5 A resolution. Science 353:904–911.
34. Kigawa T, Yabuki T, Matsuda N, Matsuda T, Nakajima R, Tanaka A, Yokoyama S (2004) Preparation of Escherichia coli cell extract for highly productive cell-free protein expression. J Struct Funct Genomics 5:63–68.
35. Kigawa T, Yabuki T, Yoshida Y, Tsutsui M, Ito Y, Shibata T, Yokoyama S (1999) Cell-free production and stable-isotope labeling of milligram quantities of proteins. FEBS Lett 442:15–19.
36. 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.
37. Clore GM, Gronenborn AM (1994) Multidimensional heteronuclear nuclear magnetic resonance of proteins. Methods Enzymol 239:349–363.
38. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6:277–293.
39. Johnson BA (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol Biol 278:313–352.
40. Kobayashi N, Iwahara J, Koshiba S, Tomizawa T, Tochio N, Güntert P, Kigawa T, Yokoyama S (2007) KUJIRA, a package of integrated modules for systematic and interactive analysis of NMR data directed to high-throughput NMR structure studies. J Biomol NMR 39:31–52.
41. Herrmann T, Güntert P, Wüthrich K (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J Mol Biol 319:209–227.
42. Güntert P, Mumenthaler C, Wüthrich K (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J Mol Biol 273:283–298.
43. Cornilescu G, Delaglio F, Bax A (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 13:289–302.
44. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8:477–486.
45. Hagihara M, Takei A, Ishii T, Hayashi F, Kubota K, Wakamatsu K, Nameki N (2012) Inhibitory effects of choline-O-sulfate on amyloid formation of human islet amyloid polypeptide. FEBS Open Bio 2:20–25.
46. Xiang L, Ishii T, Hosoda K, Kamiya A, Enomoto M, Nameki N, Inoue Y, Kubota K, Kohno T, Wakamatsu K (2008) Interaction of anti-aggregation agent dimethylethylammonium propane sulfonate with acidic fibroblast growth factor. J Magn Reson 194:147–151.