The spliceosome: Disorder and dynamics defined

Current Opinion in Structural Biology

Volumn 24, Issue 1, 2014, Pages 141-149

  Chen, Weijun ^a   Moore, Melissa J ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RIBONUCLEOPROTEIN; RNA;

ANIMAL; BIOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; METABOLISM; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; RNA SPLICING; SPLICEOSOME; AMINO ACID SEQUENCE; CONFORMATIONAL TRANSITION; INTERACTIONS WITH RNA; INTRINSICALLY DISORDERED REGION; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; NONHUMAN; PROTEIN RNA BINDING; PROTEIN STRUCTURE; REVIEW; RNA STRUCTURE; UBIQUITINATION;

ANIMALS; COMPUTATIONAL BIOLOGY; HUMANS; MODELS, MOLECULAR; PROTEIN INTERACTION MAPS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RIBONUCLEOPROTEINS; RNA; RNA SPLICING; SPLICEOSOMES;

EUKARYOTA;

EID: 84893716781     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2014.01.009     Document Type: Review

References (59)

1. Bhattacharya A. Protein structures: structures of desire. Nature 2009, 459:24-27.
2. Nilsen T.W., Graveley B.R. Expansion of the eukaryotic proteome by alternative splicing. Nature 2010, 463:457-463.
3. Graveley B.R. Alternative splicing: increasing diversity in the proteomic world. Trends Genet 2001, 17:100-107.
4. Galej W.P., Duong Nguyen T.H., Newman A.J., Nagai K. Structural studies of the spliceosome: zooming into the heart of the machine. Curr Opin Struct Biol 2014, 25:57-66. 10.1016/j.sbi.2013.12.002.
5. Jurica M.S., Moore M.J. Pre-mRNA splicing: awash in a sea of proteins. Mol Cell 2003, 12:5-14.
6. Will C.L., Luhrmann R. Spliceosome structure and function. Cold Spring Harbor Perspect Biol 2011, 3:a003707.
7. Turunen J.J., Niemelä E.H., Verma B., Frilander M.J. The significant other: splicing by the minor spliceosome. Wiley Interdiscip Rev RNA 2012, 4:61-76.
8. Younis I., Dittmar K., Wang W., Foley S.W., Berg M.G., Hu K.Y., Wei Z., Wan L., Dreyfuss G., Nilsen T. Minor introns are embedded molecular switches regulated by highly unstable U6atac snRNA. eLife 2013, 2.
9. Anokhina M., Bessonov S., Miao Z., Westhof E., Hartmuth K., LUhrmann R. RNA structure analysis of human spliceosomes reveals a compact 3D arrangement of snRNAs at the catalytic core. EMBO J 2013, 10.1038/emboj.2013.198.
10. Worth C.L., Gong S., Blundell T.L. Structural and functional constraints in the evolution of protein families. Nat Rev Mol Cell Biol 2009, 10:709-720.
11. Grainger R.J. Prp8 protein: at the heart of the spliceosome. RNA 2005, 11:533-557.
12. Nancollis V., Ruckshanthi J.P.D., Frazer L.N., O'Keefe R.T. The U5 snRNA internal loop 1 is a platform for Brr2, Snu114 and Prp8 protein binding during U5 snRNP assembly. J Cell Biochem 2013, 114:2770-2784.
13. Schneider C., Will C.L., Makarova O.V., Makarov E.M., Luhrmann R. Human U4/U6.U5 and U4atac/U6atac.U5 tri-snRNPs exhibit similar protein compositions. Mol Cell Biol 2002, 22:3219-3229.
14. Du H., Tardiff D., Moore M.J., Rosbash M. Effects of the U1C L13 mutation and temperature regulation of yeast commitment complex formation. Proc Natl Acad Sci U S A 2004, 101:14841-14846.
15. Cho S., Hoang A., Sinha R., Zhong X.-Y., Fu X.-D., Krainer A.R., Ghosh G. Interaction between the RNA binding domains of Ser-Arg splicing factor 1 and U1-70K snRNP protein determines early spliceosome assembly. Proc Natl Acad Sci U S A 2011, 108:8233-8238.
16. Gunderson S.I., Polycarpou-Schwarz M., Mattaj I.W. U1 snRNP inhibits pre-mRNA polyadenylation through a direct interaction between U1 70K and poly(A) polymerase. Mol Cell 1998, 1:255-264.
17. Kaida D., Berg M.G., Younis I., Kasim M., Singh L.N., Wan L., Dreyfuss G. U1 snRNP protects pre-mRNAs from premature cleavage and polyadenylation. Nature 2010, 468:664-668.
18. Berg M.G., Singh L.N., Younis I., Liu Q., Pinto A.M., Kaida D., Zhang Z., Cho S., Sherrill-Mix S., Wan L., et al. U1 snRNP determines mRNA length and regulates isoform expression. Cell 2012, 150:53-64.
19. Radivojac P., Iakoucheva L.M., Oldfield C.J., Obradovic Z., Uversky V.N., Dunker A.K. Intrinsic disorder and functional proteomics. Biophys J 2007, 92:1439-1456.
20. Korneta I., Bujnicki J.M. Intrinsic disorder in the human spliceosomal proteome. PLoS Comput Biol 2012, 8:e1002641.
21. Ribeiro M., Espinosa J., Islam S., Martinez O., Thanki J.J., Mazariegos S., Nguyen T., Larina M., Xue B., Uversky V.N. Malleable ribonucleoprotein machine: protein intrinsic disorder in the Saccharomyces cerevisiae spliceosome. PeerJ 2013, 1:1-58. 10.7717/peerj.2.
22. Gsponer J., Babu M.M. Cellular strategies for regulating functional and nonfunctional protein aggregation. Cell Rep 2012, 2:1425-1437.
23. Polymenidou M., Lagier-Tourenne C., Hutt K.R., Bennett C.F., Cleveland D.W., Yeo G.W. Misregulated RNA processing in amyotrophic lateral sclerosis. Brain Res 2012, 1462:3-15.
24. Moore M.J., Sharp P.A. Evidence for two active sites in the spliceosome provided by stereochemistry of pre-mRNA splicing. Nat Methods 1993, 365:364-368.
25. Tseng C.K., Cheng S.C. Both catalytic steps of nuclear pre-mRNA splicing are reversible. Science 2008, 320:1782-1784.
26. Hahn D., Kudla G., Tollervey D., Beggs J.D. Brr2p-mediated conformational rearrangements in the spliceosome during activation and substrate repositioning. Genes Dev 2012, 26:2408-2421.
27. Konarska M.M., Vilardell J., Query C.C. Repositioning of the reaction intermediate within the catalytic center of the spliceosome. Mol Cell 2006, 21:543-553.
28. Tseng C.K., Cheng S.C. The spliceosome catalyzes debranching in competition with reverse of the first chemical reaction. RNA 2013, 19:971-981.
29. Hahn D., Beggs J.D. Brr2p RNA helicase with a split personality: insights into structure and function. Biochem Soc Trans 2010, 38:1105-1109.
30. Liu L., Query C.C., Konarska M.M. Opposing classes of prp8 alleles modulate the transition between the catalytic steps of pre-mRNA splicing. Nat Struct Mol Biol 2007, 14:519-526.
31. Abelson J., Blanco M., Ditzler M.A., Fuller F., Aravamudhan P., Wood M., Villa T., Ryan D.E., Pleiss J.A., Maeder C., et al. Conformational dynamics of single pre-mRNA molecules during in vitro splicing. Nat Struct Mol Biol 2010, 17:504-512.
32. Guo Z., Karunatilaka K.S., Rueda D. Single-molecule analysis of protein-free U2-U6 snRNAs. Nat Struct Mol Biol 2009, 16:1154-1159.
33. Mefford M.A., Staley J.P. Evidence that U2/U6 helix I promotes both catalytic steps of pre-mRNA splicing and rearranges in between these steps. RNA 2009, 15:1386-1397.
34. Hoskins A.A., Gelles J., Moore M.J. New insights into the spliceosome by single molecule fluorescence microscopy. Curr Opin Chem Biol 2011, 15:864-870.
35. Hoskins A.A., Friedman L.J., Gallagher S.S., Crawford D.J., Anderson E.G., Wombacher R., Ramirez N., Cornish V.W., Gelles J., Moore M.J. Ordered and dynamic assembly of single spliceosomes. Science 2011, 331:1289-1295.
36. Shcherbakova I., Hoskins A.A., Friedman L.J., Serebrov V., Corrêa I.R., Xu M.-Q., Gelles J., Moore M.J. Alternative spliceosome assembly pathways revealed by single-molecule fluorescence microscopy. Cell Rep 2013, 5:151-165.
37. Hodson M.J., Hudson A.J., Cherny D., Eperon I.C. The transition in spliceosome assembly from complex E to complex A purges surplus U1 snRNPs from alternative splice sites. Nucleic Acids Res 2012, 40:6850-6862.
38. David C.J., Boyne A.R., Millhouse S.R., Manley J.L. The RNA polymerase II C-terminal domain promotes splicing activation through recruitment of a U2AF65-Prp19 complex. Genes Dev 2011, 25:972-983.
39. Schneider M., Will C.L., Anokhina M., Tazi J., Urlaub H., LUhrmann R. Exon definition complexes contain the tri-snRNP and can be directly converted into B-like precatalytic splicing complexes. Mol Cell 2010, 38:223-235.
40. Crawford D.J., Hoskins A.A., Friedman L.J., Gelles J., Moore M.J. Single-molecule colocalization FRET evidence that spliceosome activation precedes stable approach of 5' splice site and branch site. Proc Natl Acad Sci U S A 2013, 110:6783-6788.
41. Hegele A., Kamburov A., Grossmann A., Sourlis C., Wowro S., Weimann M., Will C.L., Pena V., LUhrmann R., Stelzl U. Dynamic protein-protein interaction wiring of the human spliceosome. Mol Cell 2012, 45:567-580.
42. Ren L., McLean J.R., Hazbun T.R., Fields S., Vander Kooi C., Ohi M.D., Gould K.L. Systematic two-hybrid and comparative proteomic analyses reveal novel yeast pre-mRNA splicing factors connected to Prp19. PLoS ONE 2011, 6:e16719.
43. Yu M.C. The role of protein arginine methylation in mRNP dynamics. Mol Biol Int 2011, 2011:1-10.
44. Nishi H., Hashimoto K., Panchenko A.R. Phosphorylation in protein-protein binding: effect on stability and function. Structure 2011, 19:1807-1815.
45. Nishi H., Fong J.H., Chang C., Teichmann S.A., Panchenko A.R. Regulation of protein-protein binding by coupling between phosphorylation and intrinsic disorder: analysis of human protein complexes. Mol Biosyst 2013, 9:1620-1626.
46. Ohi M.D., Vander Kooi C.W., Rosenberg J.A., Chazin W.J., Gould K.L. Structural insights into the U-box, a domain associated with multi-ubiquitination. Nat Struct Biol 2003, 10:250-255.
47. Bellare P., Small E.C., Huang X., Wohlschlegel J.A., Staley J.P., Sontheimer E.J. A role for ubiquitin in the spliceosome assembly pathway. Nat Struct Mol Biol 2008, 15:444-451.
48. Song E.J., Werner S.L., Neubauer J., Stegmeier F., Aspden J., Rio D., Harper J.W., Elledge S.J., Kirschner M.W., Rape M. The Prp19 complex and the Usp4Sart3 deubiquitinating enzyme control reversible ubiquitination at the spliceosome. Genes Dev 2010, 24:1434-1447.
49. Martin-Tumasz S., Reiter N.J., Brow D.A., Butcher S.E. Structure and functional implications of a complex containing a segment of U6 RNA bound by a domain of Prp24. RNA 2010, 16:792-804.
50. Martin-Tumasz S., Richie A.C., Clos L.J., Brow D.A., Butcher S.E. A novel occluded RNA recognition motif in Prp24 unwinds the U6 RNA internal stem loop. Nucleic Acids Res 2011, 39:7837-7847.
51. Krummel D.A.P., Oubridge C., Leung A.K.W., Li J., Nagai K. Crystal structure of human spliceosomal U1 snRNP at 5.5Å resolution. Nature 2009, 458:475-480.
52. Leung A.K.W., Nagai K., Li J. Structure of the spliceosomal U4 snRNP core domain and its implication for snRNP biogenesis. Nature 2011, 10.1038/nature09956.
53. Behzadnia N., Golas M.M., Hartmuth K., Sander B., Kastner B., Deckert J., Dube P., Will C.L., Urlaub H., Stark H., et al. Composition and three-dimensional EM structure of double affinity-purified, human prespliceosomal A complexes. EMBO J 2007, 26:1737-1748.
54. Wolf E., Kastner B., Deckert J., Merz C., Stark H., hrmann R.L.U. Exon, intron and splice site locations in the spliceosomal B complex. EMBO J 2009, 28:2283-2292.
55. Bessonov S., Anokhina M., Krasauskas A., Golas M.M., Sander B., Will C.L., Urlaub H., Stark H., Luhrmann R. Characterization of purified human Bact spliceosomal complexes reveals compositional and morphological changes during spliceosome activation and first step catalysis. RNA 2010, 16:2384-2403.
56. Grote M., Wolf E., Will C.L., Lemm I., Agafonov D.E., Schomburg A., Fischle W., Urlaub H., Luhrmann R. Molecular architecture of the human Prp19/CDC5L complex. Mol Cell Biol 2010, 30:2105-2119.
57. Jurica M.S., Sousa D., Moore M.J., Grigorieff N. Three-dimensional structure of C complex spliceosomes by electron microscopy. Nat Struct Mol Biol 2004, 11:265-269.
58. Ohi M.D., Ren L., Wall J.S., Gould K.L., Walz T. Structural characterization of the fission yeast U5.U2/U6 spliceosome complex. Proc Natl Acad Sci U S A 2007, 104:3195-3200.
59. Golas M.M., Sander B., Will C.L., LUhrmann R., Stark H. Major conformational change in the complex SF3b upon integration into the spliceosomal U11/U12 di-snRNP as revealed by electron cryomicroscopy. Mol Cell 2005, 17:869-883.