Crystal Structure of Lsm3 Octamer from Saccharomyces cerevisiae: Implications for Lsm Ring Organisation and Recruitment

Journal of Molecular Biology

Volumn 377, Issue 5, 2008, Pages 1357-1371

  Naidoo, Nishen ^a   Harrop, Stephen J ^b,c   Sobti, Meghna ^a   Haynes, Paul A ^a   Szymczyna, Blair R ^d   Williamson, James R ^d   Curmi, Paul M G ^b,c   Mabbutt, Bridget C ^a  

^a MACQUARIE UNIVERSITY   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c ST VINCENT S HOSPITAL   (Australia)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

beta propeller; RNA processing; RNA binding protein; RNP complex; Sm like protein

Indexed keywords

FUNGAL PROTEIN; PROTEIN LSM3; PROTEIN SM; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; GEL PERMEATION CHROMATOGRAPHY; HYDROGEN BOND; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 40849094144     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.01.007     Document Type: Article

References (55)

1. Khusial P., Plaag R., and Zieve G.W. LSm proteins form heptameric rings that bind to RNA via repeating motifs. Trends Biochem. Sci. 30 (2005) 522-528
2. Beggs J.D. Lsm proteins and RNA processing. Biochem. Soc. Trans. 33 (2005) 433-438
3. Wilusz C.J., and Wilusz J. Eukaryotic Lsm proteins: lessons from bacteria. Nat. Struct. Mol. Biol. 12 (2005) 1031-1036
4. Donahue W.F., and Jarrell K.A. A BLAST from the past: ancient origin of human Sm proteins. Mol. Cell 9 (2002) 7-8
5. Walke S., Bragado-Nilsson, Séraphin B., and Nagai K. Stoichiometry of Sm proteins in yeast spliceosomal snRNPs supports the heptamer ring model of the core domain. J. Mol. Biol. 308 (2001) 49-58
6. Mayes A.E., Verdone L., Legrain P., and Beggs J.D. Characterization of Sm-like proteins in yeast and their association with U6 snRNA. EMBO J. 18 (1999) 4321-4331
7. Salgado-Garrido J., Bragado-Nilsson E., Kandels-Lewis S., and Seraphin B. Sm and Sm-like proteins assemble into two related complexes of deep evolutionary origin. EMBO J. 18 (1999) 3451-3462
8. Bouveret E., Rigaut G., Shevchenko A., Wilm M., and Seraphin B. A Sm-like protein complex that participates in mRNA degradation. EMBO J. 19 (2000) 1661-1671
9. Tharun S., He W., Mayes A.E., Lennertz P., Beggs J.D., and Parker R. Yeast Sm-like proteins function in mRNA decapping and decay. Nature 404 (2000) 515-518
10. Tharun S., and Parker R. Targeting an mRNA for decapping: displacement of translation factors and association of the Lsm1p-7p complex on deadenylated yeast mRNAs. Mol. Cell 8 (2001) 1075-1083
11. Mura C., Phillips M., Kozhukhovsky A., and Eisenberg D. Structure and assembly of an augmented Sm-like archaeal protein 14-mer. Proc. Natl Acad. Sci. USA 100 (2003) 4539-4544
12. Collins B.M., Harrop S.J., Kornfeld G.D., Dawes I.W., Curmi P.M.G., and Mabbutt B.C. Crystal structure of a heptameric Sm-like protein complex from Archaea: implications for the structure and evolution of snRNPs. J. Mol. Biol. 309 (2001) 915-923
13. Kilic T., Thore S., and Suck D. Crystal structure of an archaeal Sm protein from Sulfolobus solfataricus. Proteins 61 (2005) 689-693
14. Törö I., Thore S., Mayer C., Basquin J., Séraphin B., and Suck D. RNA binding in an Sm core domain: X-ray structure and functional analysis of an archaeal Sm protein complex. EMBO J. 20 (2001) 2293-2303
15. Törö I., Basquin J., Teo-Dreher H., and Suck D. Archaeal Sm proteins form heptameric and hexameric complexes: crystal structures of the Sm1 and Sm2 proteins from the hyperthermophile Archaeoglobus fulgidus. J. Mol. Biol. 320 (2002) 129-142
16. Achsel T., Brahms H., Kastner B., Bacji A., Wilm M., and Luhrmann R. A doughnut-shaped heteromer of human Sm-like proteins binds to the 3′-end of U6 snRNA, thereby facilitating U4/U6 duplex formation in vitro. EMBO J. 18 (1999) 5789-5802
17. Stark H., Dube P., Luhrmann R., and Kastner B. Arrangement of RNA and proteins in the spliceosomal U1 small nuclear ribonucleoprotein particle. Nature 409 (2001) 539-542
18. Kambach C., Walke S., Young R., Avis J.A., de la Fortelle E., Raker V.A., et al. Crystal structures of two Sm protein complexes and their implications for the assembly of spliceosomal snRNPs. Cell 96 (1999)
19. Pillai R.S., Grimmler M., Meister G., Will C.L., Luhrmann R., Fischer U., and Schumperli D. Unique Sm core structure of U7 snRNPs: assembly by a specialized SMN complex and the role of a new component, Lsm11, in histone RNA processing. Genes Dev. 17 (2003) 2321-2333
20. Collins B.M., Cubeddu L., Naidoo N., Harrop S.J., Kornfeld G.D., Dawes I.W., et al. Homomeric ring assemblies of eukaryotic Sm proteins have affinity for both RNA and DNA. Crystal structure of an oligomeric complex of yeast SmF. J. Biol. Chem. 278 (2003) 17291-17298
21. Urlaub H., Raker V.A., Kostka S., and Lührmann R. Sm protein-Sm site RNA interactions with the inner ring of the spliceosomal snRNP core structure. EMBO J. 20 (2001) 187-196
22. Thore S., Mayer C., Sauter C., Weeks S., and Suck D. Crystal structures of the Pyrococcus abyssi Sm core and its complex with RNA. J. Biol. Chem. 278 (2003) 1239-1247
23. Schumacher M.A., Pearson R.F., Moller T., Valentin-Hansen P., and Brennan R.G. Structures of the pleiotropic translational regulator Hfq and an Hfq-RNA complex: a bacterial Sm-like protein. EMBO J. 21 (2002) 3456-3556
24. Fernandez C.F., Pannone B.K., Chen X., Fuchs G., and Wolin S.L. An Lsm2-Lsm7 complex in Saccharomyces cerevisiae associates with the small nucleolar RNA snR5. Mol. Biol. Cell (2004)
25. Mura C., Kozhukhovsky A., Gingery M., Phillips M., and Eisenberg D. The oligomerization and ligand-binding properties of Sm-like archaeal proteins (SmAPs). Protein Sci. 12 (2003) 832-847
26. Arluison V., Mura C., Guzman M.R., Liquier J., Pellegrini O., Gingery M., et al. Three-dimensional structures of fibrillar Sm proteins: Hfq and other Sm-like proteins. J. Mol. Biol. 356 (2006) 86-96
27. Pannone B.K., and Wolin S.L. Sm-like proteins wRING the neck of mRNA. Curr. Biol. 10 (2000) R478-R481
28. Potterton E., McNicholas S., Krissinel E., Cowtan K., and Noble M. The CCP4 molecular-graphics project. Acta Crystallogr., Sect. D: Biol. Crystallogr. 58 (2002) 1955-1957
29. Zhang H., Neal S., and Wishart D.S. RefDB: a database of uniformly referenced protein chemical shifts. J. Biomol. NMR 25 (2003) 173-195
30. Achsel T., Stark H., and Luhrmann R. The Sm domain is an ancient RNA-binding motif with oligo(U) specificity. Proc. Natl Acad. Sci. USA 98 (2001) 3685-3689
31. Vedadi M., Lew J., Artz J., Amani M., Zhao Y., Dong A., et al. Genome-scale protein expression and structural biology of Plasmodium falciparum and related Apicomplexan organisms. Mol. Biochem. Parasitol. 151 (2007) 100-110
32. Sauter C., Basquin J., and Suck D. Sm-like proteins in Eubacteria: the crystal structure of the Hfq protein from Escherichia coli. Nucleic Acids. Res. 31 (2003) 4091-4098
33. Zaric B., Chami M., Remigy H., Engel A., Ballmer-Hofer K., Winkler F.K., and Kambach C. Reconstitution of two recombinant LSm protein complexes reveals aspects of their architecture, assembly, and function. J. Biol. Chem. 280 (2005) 16066-16075
34. Holm L., and Sander C. Mapping the protein universe. Science 273 (1996) 595-603
35. Tharun S., Muhlrad D., Chowdhury A., and Parker R. Mutations in the Saccharomyces cerevisiae LSM1 gene that affect mRNA decapping and 3′ end protection. Genetics 170 (2005) 33-46
36. Leslie A.G.W. Joint CP4 + ESF-EAMCB Newsletter on Protein Crystallography 26 (1992)
37. Collaborative Computational Project, N. The CCP4 Suite: programs for protein crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 (1994) 760-763
38. McCoy A.J., Grosse-Kunstleve R.W., Storoni L.C., and Read R.J. Likelihood-enhanced fast translation functions. Acta Crystallogr., Sect. D: Biol. Crystallogr. 61 (2005) 458-464
39. Winn M.D., Isupov M.N., and Murshudov M.N. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr., Sect. D: Biol. Crystallogr. 57 (2001) 122-133
40. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 2126-2132
41. Brunger A.T., Adams P.D., Clore G.M., Delano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR System: a new software suite for macromolecular structure determination. Acta Crystallogr., Sect. D: Biol. Crystallogr. 54 (1998) 905-921
42. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr., Sect. A 47 (1991) 110-119
43. Fraczkiewicz R., and Braun W. Exact and efficient analytical calculation of the accessible surface area and their gradient for macromolecules. J. Comput. Chem. 16 (1998) 1038-1044
44. Marley J., Lu M., and Bracken C. A method for efficient isotopic labeling of recombinant proteins. J. Biomol. NMR 20 (2001) 71-75
45. Grzesiek S., and Bax A. The importance of not saturating water in protein NMR. Application to sensitivity enhancement and NOE measurements. J. Am. Chem. Soc. 115 (1993) 12593-12594
46. Piotto M., Saudek V., and Sklenar V. Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR 2 (1992) 661-665
47. 15N HSQC experiments optimized to retain full sensitivity. J. Magn. Reson., Ser. A 102 (1993) 241-245
48. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., and Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6 (1995) 277-293
49. Andon N.L., Hollingworth S., Koller A., Greenland A.J., Yates III J.R., and Haynes P.A. Proteomic characterization of wheat amyloplasts using identification of proteins by tandem mass spectrometry. Proteomics 2 (2002) 1156-1168
50. Breci L., Hattrup E., Keeler M., Letarte J., Johnson R., and Haynes P.A. Comprehensive proteomics in yeast using chromatographic fractionation, gas phase fractionation, protein gel electrophoresis, and isoelectric focusing. Proteomics 5 (2005) 2018-2028
51. Cooper B., Eckert D., Andon N.L., Yates J.R., and Haynes P.A. Investigative proteomics: identification of an unknown plant virus from infected plants using mass spectrometry. J. Am. Soc. Mass. Spectrom. 14 (2003) 736-741
52. Craig R., and Beavis R.C. TANDEM: matching proteins with tandem mass spectra. Bioinformatics 20 (2004) 1466-1467
53. Peng J., Elias J.E., Thoreen C.C., Licklider L.J., and Gygi S.P. Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J. Proteome Res. 2 (2003) 43-50
54. Guex N., and Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18 (1997) 2714-2723
55. Dunbrack Jr. R.L., and Cohen F.E. Bayesian statistical analysis of protein side-chain rotamer preferences. Protein Sci. 6 (1997) 1661-1681