Crystal structures of two Sm protein complexes and their implications for the assembly of the spliceosomal snRNPs

Cell

Volumn 96, Issue 3, 1999, Pages 375-387

  Kambach, Christian ^a   Walke, Stefan ^a   Young, Robert ^a,c   Avis, Johanna M ^a,d   De La Fortelle, Eric ^a   Raker, Veronica A ^b   Lührmann, Reinhard ^b   Li, Jade ^a   Nagai, Kiyoshi ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c ST GEORGE S HOSPITAL   (United Kingdom)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

SMALL NUCLEAR RIBONUCLEOPROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; DIMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; SPLICEOSOME;

EID: 0033524941     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)80550-4     Document Type: Article

References (59)

1. Abrahams, J.P., and Leslie, A.G.W. (1996). Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallogr. D 52, 30-42.
2. Antson, A.A., Otridge, J., Brzozowski, A.M., Dodson, E.J., Dodson, G.G., Wilson, K.S., Smith,T.M., Yang, M., Kureski,T., and Gollnick, P. (1995). The structure of trp RNA-binding attenuation protein. Nature 374, 693-700.
3. Baserga, S.J., and Steitz, U.A. (1993). The diverse world of small ribonucleoproteins. In The RNA World, R.F. Gesteland and J.F. Atkins, eds. (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press), pp. 359-381.
4. Bordonné, R., and Tarassov, I. (1996). The yeast SmE gene encodes the homologue of the human E core protein. Gene 776, 111-117.
5. Camasses, A., Bragado-Nilsson, E., Martin, R., Séraphin, B., and Bordonné, R. (1997). Interactions within the yeast Sm core complex: from proteins to amino acids. Mol. Cell. Biol. 18, 1956-1966.
6. Asp recognition by its cognate class II aminoacyl tRNA synthetase. Nature 362, 181-184.
7. Cech, T.R. (1985). RNA splicing: three themes with variations. Cell 43, 713-716.
8. Chu, J.-L, and Elkon, K.B. (1991). The small nuclear ribonucleoproteins, SmB and B′ are products of a single gene. Gene 97, 311-312.
9. Cooper, M., Johnston, L.H., and Beggs, J.D. (1995). Identification and characterisation of Usslp (Sdb23p): a novel U6 snRNA-associated protein with significant similarity to core proteins of small nuclear ribonucleoproteins. EMBO J. 14, 2066-2075.
10. De la Fortelle, E., and Bricogne, G. (1997). Maximum-likelihood heavy atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276, 472-494.
11. Dodson, E.J., Winn, M., and Ralph, A. (1997). Collaborative Computational Project, Number 4: Providing Programs for Crystallography. Methods Enzymol. 277, 620-634.
12. Evans, S.V. (1993). SETOR: hardware-lighted three-dimensional solid model representations of macromolecules. J. Mol. Graph. 11, 134-138.
13. Feeney, R.J., Sauterer, R.A., Feeney, J.L, and Zieve, G.W. (1989). Cytoplasmic assembly and nuclear accumulation of mature small nuclear ribonucleoprotein particles. J. Biol. Chem. 264, 5776-5783.
14. Fischer, U., Sumpter, V., Sekine, M., Satoh, T., and Lührmann, R. (1993). Nucleo-cytoplasmic transport of U snRNPs: definition of a nuclear location signal in the Sm core domain that binds a transport receptor independently of the m3G cap. EMBO J. 12, 573-583.
15. Fisher, D.E., Conner, G.E., Reeves, N.H., Wisniewolski, R., and Blobel, G. (1985). Small nuclear ribonucleoprotein particle assembly in vivo: demonstration of a 6S RNA-free core precursor and posttranslational modification. Cell 42, 751-758.
16. Frank, D.N., Roiha, H., and Guthrie, C. (1994). Architecture of the U5 small nuclear RNA. Mol. Cell. Biol. 14, 2180-2190.
17. Fury, M.G., Zhang, W., Christodoulopoulos, I., and Zieve, G.W. (1997). Multiple protein:protein interactions between the snRNP common core proteins. Exp. Cell. Res. 237, 63-69.
18. Geiger, J.H., Hahn, S., Lee, S., and Sigler, P.B. (1996). Crystal structure of the yeast TFIIA/TBP/DNA complex. Science 272, 830-836.
19. Hamm, J., Darzynkiewicz, E., Tahara, S.M., and Mattaj, I.W. (1990). The trimethylguanosine cap structure of U1 snRNA is a component of a bipartite nuclear targeting signal. Cell 62, 569-577.
20. Hartmuth, K., Raker, V.A., Huber, J., Branlant, C., and 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.
21. Heinrichs, V., Hackl, W., and Lührmann, R. (1992). Direct binding of small nuclear ribonucleoprotein G to the Sm site of small nuclear RNA. Ultraviolet light cross-linking of protein G to the AAU stretch within the Sm site (AAUUUGUGG) of U1 small nuclear ribonucleoprotein reconstituted in vitro. J. Mol. Biol. 227, 15-28.
22. Hermann, H., Fabrizio, P., Raker, V.A., Foulaki, K., Hornig, H., Brahms, H., and Lührmann, R. (1995). snRNP Sm proteins share two evolutionarily conserved sequence motifs which are involved in Sm protein-protein interactions. EMBO J. 14, 2076-2088.
23. Huber, J., Cronshagen, U., Kadokura, M., Marshallsay, C., Wada, T., Seikine, M., and Lührmann, R. (1998). Snurportinl, an m3G-capspecific nuclear import receptor with a novel domain structure. EMBO J. 17, 4114-4126.
24. Ikemura, T. (1982). Correlation between the abundance of yeast transfer-RNAs and the occurrence of the respective codons in protein genes-differences in synonymous codon choice patterns of yeast and Escherichia coli with reference to the abundance of isoaccepting transfer RNAs. J. Mol. Biol. 758, 573-597.
25. Jones, T.A., and Kjeldgaard, M.O. (1994). O - The Manual. (Uppsala University, Uppsala, Sweden).
26. Kastner, B., Bach, M., and 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.
27. Kastner, B., Kornstadt, U., Bach, M., and Lührmann, R. (1992). Structure of the small nuclear RNP particle U1 : identification of the two structural protuberances with RNP-antigens A and 70K. J. Cell Biol. 116, 839-849.
28. Lehmeier, T., Raker, V., Hermann, H., and Lührmann, R. (1994). cDNA cloning of the Sm proteins D2 and D3 from human small nuclear ribonucleoproteins: evidence for a direct D1-D2 interaction. Proc. Natl. Acad. Sci. USA 97, 12317-12321.
29. Lerner, M.R., and Steitz, U.A. (1979). Antibodies to small nuclear RNAs complexed with proteins are produced by patients with systemic lupus erythematosus. Proc. Natl. Acad. Sci. USA 76, 5495-5499.
30. Lo Conte, L., Chothia, C. and Janin, J. (1999). The atomic structure of protein-protein recognition sites. J. Mol. Biol. 285, 2177-2198.
31. Lührmann, R., Kastner, B., and Bach, M. (1990). Structure of spliceosomal snRNPs and their role in pre-mRNA splicing. Biochim. Biophys. Acta 7087, 265-292.
32. Mattaj, I.W. (1986). Cap trimethylation of U snRNA is cytoplasmic and dependent on U snRNP protein binding. Cell 46, 905-911.
33. Moore, M. J., Query, C., and Sharp, P.A. (1993). Splicing of precursors to mRNA by the spliceosome. In The RNA World, R.F. Gesteland and J.F. Atkins, eds. (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press), pp. 303-357.
34. Murshudov, G.N., Vagin, A.A., and Dodson, E.J. (1997). Refinement of macromolecular structures by the maximum likelihood method. Acta Crystallogr. D 53, 240-255.
35. Musacchio, A., Noble, M., Pauptit, R., Wierenga, R., and Saraste, M. (1992). Crystal structure of a Src-homology-3 (SH3) domain. Nature 359, 851-855.
36. Nagai, K., and Mattaj, I.W. (1994). RNA-protein interactions in the splicing snRNPs. In RNA-Protein Interactions, K. Nagai and I.W. Mattaj, eds. (Oxford, Oxford University Press), pp. 150-177.
37. Nelissen, R.L., Will, C.L, van Venrooij, W.J., and 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. 73,4113-4125.
38. Newman, A.J. (1997). The role of U5 snRNP in pre-mRNA splicing. EMBO J. 76, 5797-5800.
39. Newman, A., and Norman, C. (1992). U5 snRNA interacts with exon sequences at 5′ and 3′ splice sites. Cell 68, 743-754.
40. Nicholls, K.A., Sharp, B., and Honig, B. (1991). Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 77, 281-296.
41. Nilsen, T.W. (1994) RNA-RNA interactions in the spliceosome: unraveling the ties that bind. Cell 78, 1-4.
42. Oubridge, C., Ito, N., Evans, P.R., Teo, H.C., and Nagai, K. (1994). Crystal structure at 1.92 Å resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin. Nature 372, 432-438.
43. Palacios, l., Hetzer, M., Adam, S.A., and Mattaj, I.W. (1997). Nuclear import of U snRNPs requires importin b. EMBO J. 76, 6783-6792.
44. Parks, T.D., Leuther, K.K., Howard, E.D., Johnson, S.A., and Dougherty, W.G. (1994). Release of proteins and peptides from fusion proteins using a recombinant plant virus proteinase. Anal. Biochem. 276, 413-417.
45. Plessel, G., Fischer, U., and Lührmann, R. (1994). m3G cap hypermethylation of U1 small nuclear ribonucleoprotein (snRNP) in vitro: evidence that the U1 small nuclear RNA-(guanosine-N2)-methyltransferase is a non-snRNP cytoplasmic protein that requires a binding site on the Sm core domain. Mol. Cell. Biol 14, 4160-4172.
46. Plessel, G., Lührmann, R., and Kastner, B. (1997). Electron microscopy of assembly intermediates of the snRNP core: morphological similarities between the RNA-free (E.F.G) protein heteromer and the intact snRNP core. J. Mol. Biol. 265, 87-94.
47. Price, S.R., Evans, P.R., and Nagai, K. (1998). Crystal structure of the spliceosomal U2B″-U2A′ protein complex bound to a fragment of U2 small nuclear RNA. Nature 394, 645-650.
48. Raker, V.A., Plessel, G., and 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.
49. Séraphin, 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.
50. Sharp, P.A. (1985). On the origins of RNA splicing and introns. Cell 42, 397-400.
51. Sharp, P.A. (1987). Splicing of messenger RNA precursors. Science 23, 766-771.
52. Sheldrick, G. (1991). Heavy atom location using SHELXS-90. In Isomorphous Replacement and Anomalous Scattering, W. Wolf, P.R. Evans, and A.G.W. Leslie, eds. (Daresbury, CCP4), pp. 23-38.
53. Steitz, J.A., Black, D.L., Gerke, V., Parker, K.A., Krämer, A., Frendewey, D., and Keller, W. (1988). Functions of the abundant U-snRNPs. In Structure and Function of Major and Minor Small Nuclear Ribonucleoprotein Particles, M.L. Birnstiel, ed. (Berlin, Springer-Verlag), pp. 115-154.
54. Studier, F.W., Rosenberg, A.H., Dunn, J.J., and Dubendorff, U.A. (1990). Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185, 60-89.
55. Tan, S., Hunziker, Y., Sargent, D.F., and Richmond, T.J. (1996). Crystal structure of a yeast TFIIA/TBP/DNA complex. Nature 387, 127-134.
56. Tarn, W.Y., and Steitz, J.A. (1997). Pre-mRNA splicing: the discovery of a new spliceosome doubles the challenge. Trends Biochem. Sci. 22, 132-137.
57. Valegård, K., Murray, J.B., Stockley, P.G., Stonehouse, N.J., and Lilijas, L (1994). Crystal structure of an RNA bacteriophage coat protein-operator complex. Nature 371, 623-626.
58. van Dam, A., Winkel, I., Zijlstra-Baalbergen, J., Smeenk, R., and Cuypers, H.T. (1989). Cloned human snRNP proteins B and B' differ only in their caboxy-terminal part. EMBO J. 8, 3853-3860.
59. Weiner, A.M. (1993). mRNA splicing and autocatalytic introns: distant cousins or the products of chemical determinism. Cell 72, 161-164.