A unique spatial arrangement of the snRNPs within the native spliceosome emerges from in silico studies

Structure

Volumn 20, Issue 6, 2012, Pages 1097-1106

  Frankenstein, Ziv ^a   Sperling, Joseph ^a   Sperling, Ruth ^b   Eisenstein, Miriam ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

SMALL NUCLEAR RIBONUCLEOPROTEIN;

ARTICLE; COMPUTER MODEL; PRIORITY JOURNAL; RNA CONFORMATION; RNA SPLICING; SPLICEOSOME;

COMPUTER SIMULATION; FUNGAL PROTEINS; HUMANS; MODELS, MOLECULAR; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, QUATERNARY; RIBONUCLEOPROTEINS, SMALL NUCLEAR; SPLICEOSOMES; SURFACE PROPERTIES;

EID: 84861981718     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2012.03.022     Document Type: Article

References (52)

1. Ast, G., and Weiner, A.M. (1997). A novel U1/U5 interaction indicates proximity between U1 and U5 snRNAs during an early step of mRNA splicing. RNA 3, 371-381.
2. Azubel, M., Wolf, S.G., Sperling, J., and Sperling, R. (2004). Three-dimensional structure of the native spliceosome by cryo-electron microscopy. Mol. Cell 15, 833-839.
3. Azubel, M., Habib, N., Sperling, R., and Sperling, J. (2006). Native spliceosomes assemble with pre-mRNA to form supraspliceosomes. J. Mol. Biol. 356, 955-966.
4. Bahar, I., and Rader, A.J. (2005). Coarse-grained normal mode analysis in structural biology. Curr. Opin. Struct. Biol. 15, 586-592.
5. Behzadnia, N., Golas, M.M., Hartmuth, K., Sander, B., Kastner, B., Deckert, J., Dube, P., Will, C.L., Urlaub, H., Stark, H., and Lührmann, R. (2007). Composition and three-dimensional EM structure of double affinity-purified, human prespliceosomal A complexes. EMBO J. 26, 1737-1748.
6. Ben-Shimon, A., and Eisenstein, M. (2005). Looking at enzymes from the inside out: the proximity of catalytic residues to the molecular centroid can be used for detection of active sites and enzyme-ligand interfaces. J. Mol. Biol. 351, 309-326.
7. Ben-Zeev, E., and Eisenstein, M. (2003). Weighted geometric docking: incorporating external information in the rotation-translation scan. Proteins 52, 24-27.
8. Boehringer, D., Makarov, E.M., Sander, B., Makarova, O.V., Kastner, B., Lührmann, R., and Stark, H. (2004). Three-dimensional structure of a precatalytic human spliceosomal complex B. Nat. Struct. Mol. Biol. 11, 463-468.
9. Brow, D.A. (2002). Allosteric cascade of spliceosome activation. Annu. Rev. Genet. 36, 333-360.
10. Burge, C.B., Tuschl, T.H., and Sharp, P.A. (1999). Splicing of precursors to mRNAs by the spliceosomes. In The RNA World, Second Edition, R.F. Gesteland, T.R. Cech, and J.F. Atkins, eds. (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press), pp. 525-560.
11. Chacón, P., Tama, F., and Wriggers, W. (2003). Mega-Dalton biomolecular motion captured from electron microscopy reconstructions. J. Mol. Biol. 326, 485-492.
12. Cohen-Krausz, S., Sperling, R., and Sperling, J. (2007). Exploring the architecture of the intact supraspliceosome using electron microscopy. J. Mol. Biol. 368, 319-327.
13. Dönmez, G., Hartmuth, K., Kastner, B., Will, C.L., and Lührmann, R. (2007). The 5′ 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.
14. Dybkov, O., Will, C.L., Deckert, J., Behzadnia, N., Hartmuth, K., and 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.
15. Eisenstein, M., Shariv, I., Koren, G., Friesem, A.A., and Katchalski-Katzir, E. (1997). Modeling supra-molecular helices: extension of the molecular surface recognition algorithm and application to the protein coat of the tobacco mosaic virus. J. Mol. Biol. 266, 135-143.
16. Frankenstein, Z., Sperling, J., Sperling, R., and Eisenstein, M. (2008). FitEM2EM - tools for low resolution study of macromolecular assembly and dynamics. PLoS ONE 3, e3594.
17. Golas, M.M., Sander, B., Will, C.L., Lührmann, R., and Stark, H. (2003). Molecular architecture of the multiprotein splicing factor SF3b. Science 300, 980-984.
18. Golas, M.M., Sander, B., Will, C.L., Lührmann, R., and Stark, H. (2005). Major conformational change in the complex SF3b upon integration into the spliceosomal U11/U12 di-snRNP as revealed by electron cryomicroscopy. Mol. Cell 17, 869-883.
19. Häcker, I., Sander, B., Golas, M.M., Wolf, E., Karagöz, E., Kastner, B., Stark, H., Fabrizio, P., and Lührmann, R. (2008). Localization of Prp8, Brr2, Snu114 and U4/U6 proteins in the yeast tri-snRNP by electron microscopy. Nat. Struct. Mol. Biol. 15, 1206-1212.
20. Heinrich, B., Zhang, Z., Raitskin, O., Hiller, M., Benderska, N., Hartmann, A.M., Bracco, L., Elliott, D., Ben-Ari, S., Soreq, H., et al. (2009). Heterogeneous nuclear ribonucleoprotein G regulates splice site selection by binding to CC(A/C)-rich regions in pre-mRNA. J. Biol. Chem. 284, 14303-14315.
21. Henrick, K., Newman, R., Tagari, M., and Chagoyen, M. (2003). EMDep: a webbased system for the deposition and validation of high-resolution electron microscopy macromolecular structural information. J. Struct. Biol. 144, 228-237.
22. Igel, H., Wells, S., Perriman, R., and Ares, M., Jr. (1998). Conservation of structure and subunit interactions in yeast homologues of splicing factor 3b (SF3b) subunits. RNA 4, 1-10.
23. Jurica, M.S., and Moore, M.J. (2003). Pre-mRNA splicing: awash in a sea of proteins. Mol. Cell 12, 5-14.
24. Jurica, M.S., Sousa, D., Moore, M.J., and Grigorieff, N. (2004). Threedimensional structure of C complex spliceosomes by electron microscopy. Nat. Struct. Mol. Biol. 11, 265-269.
25. Kowalsman, N., and Eisenstein, M. (2007). Inherent limitations in proteinprotein docking procedures. Bioinformatics 23, 421-426.
26. Krämer, A., Grüter, P., Gröning, K., and Kastner, B. (1999). Combined biochemical and electron microscopic analyses reveal the architecture of the mammalian U2 snRNP. J. Cell Biol. 145, 1355-1368.
27. Leung, A.K., Nagai, K., and Li, J. (2011). Structure of the spliceosomal U4 snRNP core domain and its implication for snRNP biogenesis. Nature 473, 536-539.
28. Levitt, M., and Gerstein, M. (1998). A unified statistical framework for sequence comparison and structure comparison. Proc. Natl. Acad. Sci. USA 95, 5913-5920.
29. Madhani, H.D., and Guthrie, C. (1992). A novel base-pairing interaction between U2 and U6 snRNAs suggests a mechanism for the catalytic activation of the spliceosome. Cell 71, 803-817.
30. Malca, H., Shomron, N., and Ast, G. (2003). The U1 snRNP base pairs with the 50 splice site within a penta-snRNP complex. Mol. Cell. Biol. 23, 3442-3455.
31. McConnell, T.S., and Steitz, J.A. (2001). Proximity of the invariant loop of U5 snRNA to the second intron residue during pre-mRNA splicing. EMBO J. 20, 3577-3586.
32. McGrail, J.C., and O'Keefe, R.T. (2008). The U1, U2 and U5 snRNAs crosslink to the 50 exon during yeast pre-mRNA splicing. Nucleic Acids Res. 36, 814-825.
33. Medalia, O., Typke, D., Hegerl, R., Angenitzki, M., Sperling, J., and Sperling, R. (2002). Cryoelectron microscopy and cryoelectron tomography of the nuclear pre-mRNA processing machine. J. Struct. Biol. 138, 74-84.
34. Müller, S., Wolpensinger, B., Angenitzki, M., Engel, A., Sperling, J., and Sperling, R. (1998). A supraspliceosome model for large nuclear ribonucleoprotein particles based on mass determinations by scanning transmission electron microscopy. J. Mol. Biol. 283, 383-394.
35. Newman, A.J., and Nagai, K. (2010). Structural studies of the spliceosome: blind men and an elephant. Curr. Opin. Struct. Biol. 20, 82-89.
36. Ohi, M.D., Ren, L., Wall, J.S., Gould, K.L., and Walz, T. (2007). Structural characterization of the fission yeast U5.U2/U6 spliceosome complex. Proc. Natl. Acad. Sci. USA 104, 3195-3200.
37. Pomeranz Krummel, D.A., Oubridge, C., Leung, A.K., Li, J., and Nagai, K. (2009). Crystal structure of human spliceosomal U1 snRNP at 5.5 A resolution. Nature 458, 475-480.
38. Raitskin, O., Cho, D.S., Sperling, J., Nishikura, K., and Sperling, R. (2001). RNA editing activity is associated with splicing factors in lnRNP particles: The nuclear pre-mRNA processing machinery. Proc. Natl. Acad. Sci. USA 98, 6571-6576.
39. Raitskin, O., Angenitzki, M., Sperling, J., and Sperling, R. (2002). Large nuclear RNP particles-the nuclear pre-mRNA processing machine. J. Struct. Biol. 140, 123-130.
40. Sander, B., Golas, M.M., Makarov, E.M., Brahms, H., Kastner, B., Lührmann, R., and 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.
41. Sperling, R., Koster, A.J., Melamed-Bessudo, C., Rubinstein, A., Angenitzki, M., Berkovitch-Yellin, Z., and Sperling, J. (1997). Three-dimensional image reconstruction of large nuclear RNP (lnRNP) particles by automated electron tomography. J. Mol. Biol. 267, 570-583.
42. Sperling, J., Azubel, M., and Sperling, R. (2008). Structure and function of the Pre-mRNA splicing machine. Structure 16, 1605-1615.
43. Staley, J.P., and Guthrie, C. (1998). Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell 92, 315-326.
44. Stark, H., and Lührmann, R. (2006). Cryo-electron microscopy of spliceosomal components. Annu. Rev. Biophys. Biomol. Struct. 35, 435-457.
45. Stark, H., Dube, P., Lührmann, R., and Kastner, B. (2001). Arrangement of RNA and proteins in the spliceosomal U1 small nuclear ribonucleoprotein particle. Nature 409, 539-542.
46. Suhre, K., and Sanejouand, Y.H. (2004). ElNemo: a normal mode web server for protein movement analysis and the generation of templates for molecular replacement. Nucleic Acids Res. 32 (Web Server issue), W610-4.
47. Sun, J.S., and Manley, J.L. (1995). A novel U2-U6 snRNA structure is necessary for mammalian mRNA splicing. Genes Dev. 9, 843-854.
48. Tama, F., Wriggers, W., and Brooks, C.L., 3rd. (2002). Exploring global distortions of biological macromolecules and assemblies from low-resolution structural information and elastic network theory. J. Mol. Biol. 321, 297-305.
49. Tirion, M.M. (1996). Large Amplitude Elastic Motions in Proteins from a Single- Parameter, Atomic Analysis. Phys. Rev. Lett. 77, 1905-1908.
50. Tycowski, K.T., Kolev, N.G., Conard, N.K., Fok, V., and Steitz, J.A. (2006). The ever-growing world of small nuclear ribonucleoproteins. In The RNA World, Third Edition, R.F. Gesteland, T.R. Cech, and J.F. Atkins, eds. (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press), pp. 327-368.
51. Will, C.L., and Luhrmann, R. (2011). Spliceosome Structure and Function. Cold Spring Harb. Perspect. Biol. 3.
52. Yitzhaki, S., Miriami, E., Sperling, R., and Sperling, J. (1996). Phosphorylated Ser/Arg-rich proteins: limiting factors in the assembly of 200S large nuclear ribonucleoprotein particles. Proc. Natl. Acad. Sci. USA 93, 8830-8835.