Identification, characterization and crystal structure analysis of the human spliceosomal U5 snRNP-specific 15 kD protein

Journal of Molecular Biology

Volumn 294, Issue 2, 1999, Pages 515-525

  Reuter, Klaus ^a   Nottrott, Stephanie ^a   Fabrizio, Patrizia ^a   Lührmann, Reinhard ^a,b   Ficner, Ralf ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

Cell cycle; MAD; snRNP; Spliceosome; Thioredoxin; X ray

Indexed keywords

PROTEIN; PROTEIN DISULFIDE ISOMERASE; RNA; SMALL NUCLEAR RIBONUCLEOPROTEIN; THIOREDOXIN;

ARTICLE; BINDING SITE; CELL CYCLE; CRYSTAL STRUCTURE; DISULFIDE BOND; ENZYME ACTIVITY; GENE DELETION; HUMAN; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; RNA BINDING; RNA SPLICING; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; SPLICEOSOME;

SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE;

EID: 0033607476     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.3258     Document Type: Article

References (59)

1. Abrahams J. P., Leslie A. G. W. Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallog. sect. D. 52:1996;30-42.
2. Achsel T., Ahrens K., Brahms H., Teigelkamp S., Lührmann R. The human U5-220kD protein (hPrp8) forms a stable RNA-free complex with several U5-specific proteins, including an RNA unwindase, a homologue of ribosomal elongation factor EF-2, and a novel WD-40 protein. Mol. Cell. Biol. 18:1998;6756-6766.
3. Bach M., Winkelmann G., Lührmann R. 20 S small nuclear ribonucleoprotein U5 shows a surprisingly complex protein composition. Proc. Natl Acad. Sci. USA. 86:1989;6038-6042.
4. Behrens S. E., Lührmann R. Immunoaffinity purification of a [U4/U6. U5] tri-snRNP from human cells. Genes Dev. 5:1991;1439-1452.
5. Berry L. D., Gould K. L. Fission yeast dim1(+) encodes a functionally conserved polypeptide essential for mitosis. J. Cell. Biol. 137:1997;1337-1354.
6. Berry L. D., Feoktistova A., Wright M. D., Gould K. L. The Schizosaccharomyces pombe dim1(+) gene interacts with the anaphase-promoting complex or cyclosome (APC/C) component lid1(+) and is required for APC/C function. Mol. Cell. Biol. 19:1999;2535-2546.
7. Brünger A. T. X-PLOR Version 3.1. 1993;Yale University Press, New Haven.
8. Burge C. B., Tuschl T. H., Sharp P. A. Splicing of precursors to mRNAs by the spliceosome. Gesteland R. F., Cech T., Atkins J. F. The RNA World. 1999;525-560 Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
9. Choi H. J., Kang S. W., Yang C. H., Rhee S. G., Ryu S. E. Crystal structure of a novel human peroxidase enzyme at 2. 0 Å resolution. Nature Struct. Biol. 5:1998;400-406.
10. De La Fortelle E., Bricogne G. Maximum-likelihood heavy-atom parameter refinement in the MIR and MAD methods. Methods Enzymol. 276:1997;472-494.
11. Doublie S., Tabor S., Long A. M., Richardson C. C., Ellenberger T. Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 Å resolution. Nature. 391:1998;251-258.
12. Enroth C., Neujahr H., Schneider G., Lindqvist Y. The crystal structure of phenol hydroxylase in complex with FAD and phenol provides evidence for a concerted conformational change in the enzyme and its cofactor during catalysis. Structure. 6:1998;605-617.
13. Fabrizio P., Laggerbauer B., Lauber J., Lane W. S., Lührmann R. An evolutionarily conserved U5 snRNP-specific protein is a GTP-binding factor closely related to the ribosomal translocase EF-2. EMBO J. 16:1997;4092-4106.
14. Forrester W., Stutz F., Rosbash M., Wickens M. Defects in mRNA 3′-end formation, transcription initiation, and mRNA transport associated with the yeast mutation prp20: possible coupling of mRNA processing and chromatin structure. Genes Dev. 6:1992;1914-1926.
15. Gaudet R., Bohm A., Sigler P. B. Crystal structure at 2.4 angstroms resolution of the complex of transducin betagamma and its regulator, phosducin. Cell. 87:1996;577-588.
16. Gottschalk A., Neubauer G., Banroques J., Mann M., Lührmann R., Fabrizio P. Identification by mass spectrometry and functional analysis of novel proteins of the yeast [U4/U6. U5] tri-snRNP. EMBO J. 18:1999;4535-4548.
17. Gross T., Lutzelberger M., Weigmann H., Klingenhoff A., Shenoy S., Kaufer N. F. Functional analysis of the fission yeast Prp4 protein kinase involved in pre-mRNA splicing and isolation of a putative mammalian homologue. Nucl. Acids Res. 25:1997;1028-1035.
18. Hendrickson W. A., Horton J. R., LeMaster D. M. Selenomethionyl proteins produced for analysis by multiwavelength anomalous diffraction (MAD): a vehicle for direct determination of three-dimensional structure. EMBO J. 9:1990;1665-1672.
19. Holmgren A. Thioredoxin catalyzes the reduction of insulin disulfides by dithiothreitol and dihydrolipoamide. J. Biol. Chem. 254:1979;9627-9632.
20. Holmgren A. Thioredoxin structure and mechanism: conformational changes on oxidation of the active-site sulfhydryls to a disulfide. Structure. 3:1995;239-243.
21. Holmgren A., Soderberg B. O., Eklund H., Branden C. I. Three-dimensional structure of Escherichia coli thioredoxin-S2 to 2.8 Å resolution. Proc. Natl Acad. Sci. USA. 72:1975;2305-2309.
22. Humphrey W., Dalke A., Schulten K. VMD - visual molecular dynamics. J. Mol. Graph. 14:1996;33-38.
23. Hwang L. H., Murray A. W. A novel yeast screen for mitotic arrest mutants identifies DOC1, a new gene involved in cyclin proteolysis. Mol. Biol. Cell. 8:1997;1877-1887.
24. Imamura O., Saiki K., Tani T., Ohshima Y., Sugawara M., Furuichi Y. Cloning and characterization of a human DEAH-box RNA helicase, a functional homolog of fission yeast Cdc28/Prp8. Nucl. Acids Res. 26:1998;2063-2068.
25. Jones T. A., Kjeldgaard M. Electron-density map interpretation. Methods Enzymol. 277:1997;173-208.
26. Kambach C., Walke S., Young R., Avis J. M., de la Fortelle E., Raker V. A., Lührmann R., Li J., Nagai K. Crystal structures of two Sm protein complexes and their implications for the assembly of the spliceosomal snRNPs. Cell. 96:1999;375-387.
27. Kastner B., Lührmann R. Purification of U small nuclear ribonucleoprotein particles. Haynes S. Methods in Molecular Biology. 1999;289-298 Humana Press Inc. Totowa.
28. Kemmink J., Darby N. J., Dijkstra K., Nilges M., Creighton T. E. The folding catalyst protein disulfide isomerase is constructed of active and inactive thioredoxin modules. Curr. Biol. 7:1997;239-245.
29. Kharrat A., Macias M. J., Gibson T. J., Nilges M., Pastore A. Structure of the dsRNA binding domain of E. coli RNase III. EMBO J. 14:1995;3572-3584.
30. Krämer A. The structure and function of proteins involved in mammalian pre-mRNA splicing. Annu. Rev. Biochem. 65:1996;367-409.
31. Kraulis P. J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
32. Laggerbauer B., Achsel T., Lührmann R. The human U5-200kD DEXH-box protein unwinds U4/U6 RNA duplices in vitro. Proc. Natl Acad. Sci. USA. 95:1998;4188-4192.
33. Lamzin V. S., Wilson K. S. Automated refinement for protein crystallography. Methods Enzymol. 277:1997;269-305.
34. Lauber J., Fabrizio P., Teigelkamp S., Lane W. S., Hartmann E., Lührmann R. The HeLa 200 kDa U5 snRNP-specific protein and its homologue in Saccharomyces cerevisiae are members of the DEXH-box protein family of putative RNA helicases. EMBO J. 15:1996;4001-4015.
35. Lauber J., Plessel G., Prehn S., Will C. L., Fabrizio P., Groning K., Lane W. S., Lührmann R. The human U4/U6 snRNP contains 60 and 90kD proteins that are structurally homologous to the yeast splicing factors Prp4p and Prp3p. RNA. 3:1997;926-941.
36. Lundgren K., Allan S., Urushiyama S., Tani T., Ohshima Y., Frendewey D., Beach D. A connection between pre-mRNA splicing and the cell cycle in fission yeast: cdc28+ is allelic with prp8+ and encodes an RNA-dependent ATPase/helicase. Mol. Biol. Cell. 7:1996;1083-1094.
37. Madhani H. D., Guthrie C. Dynamic RNA-RNA interactions in the spliceosome. Annu. Rev. Genet. 28:1994;1-26.
38. Martin J. L. Thioredoxin - a fold for all reasons. Structure. 3:1995;245-250.
39. Merrit E. A., Bacon D. J. Raster3D: photorealistic molecular graphics. Methods Enzymol. 277:1997;505-524.
40. Nicholls A., Sharp K. A., Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins: Struct. Funct. Genet. 11:1991;281-296.
41. Nilsen T. W. RNA-RNA interactions in the spliceosome: unraveling the ties that bind. Cell. 78:1994;1-4.
42. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:1997;307-326.
43. Potashkin J., Kim D., Fons M., Humphrey T., Frendewey D. Cell-division-cycle defects associated with fission yeast pre-mRNA splicing mutants. Curr. Genet. 34:1998;153-163.
44. Reuter K., Ficner R. Overproduction, purification, crystallization and preliminary X-ray diffraction studies of the human spliceosomal protein U5-15kD. Acta Crystallog. sect. D. 55:1999;888-890.
45. Reyes J. L., Kois P., Konforti B. B., Konarska M. M. The canonical GU dinucleotide at the 5′ splice site is recognized by p220 of the U5 snRNP within the spliceosome. RNA. 2:1996;213-225.
46. Ryter J. M., Schultz S. C. Molecular basis of double-stranded RNA-protein interactions: structure of a dsRNA-binding domain complexed with dsRNA. EMBO J. 17:1998;7505-7513.
47. Seghezzi W., Chua K., Shanahan F., Gozani O., Reed R., Lees E. Cyclin E associates with components of the pre-mRNA splicing machinery in mammalian cells. Mol. Cell. Biol. 18:1998;4526-4536.
48. Shea J. E., Toyn J. H., Johnston L. H. The budding yeast U5 snRNP Prp8 is a highly conserved protein which links RNA splicing with cell cycle progression. Nucl. Acids Res. 22:1994;5555-5564.
49. Staley J. P., Guthrie C. Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell. 92:1998;315-326.
50. Stevens S. W., Abelson J. Purification of the yeast U4/U6. U5 small nuclear ribonucleoprotein particle and identification of its proteins. Proc. Natl Acad. Sci. USA. 96:1999;7226-7231.
51. Tabor S., Huber H. E., Richardson C. C. Escherichia coli thioredoxin confers processivity on the DNA polymerase activity of the gene 5 protein of bacteriophage T7. J. Biol. Chem. 262:1987;16212-16223.
52. Teigelkamp S., Newman A. J., Beggs J. D. Extensive interactions of PRP8 protein with the 5′ and 3′ splice sites during splicing suggest a role in stabilization of exon alignment by U5 snRNA. EMBO J. 14:1995;2602-2612.
53. Teigelkamp S., Mundt C., Achsel T., Will C. L., Luhrmann R. The human U5 snRNP-specific 100-kD protein is an RS domain-containing, putative RNA helicase with significant homology to the yeast splicing factor Prp28p. RNA. 3:1997;1313-1326.
54. Urushiyama S., Tani T., Ohshima Y. Isolation of novel pre-mRNA splicing mutants of Schizosaccharomyces pombe. Mol. Gen. Genet. 253:1996;118-127.
55. Vijayraghavan U., Company M., Abelson J. Isolation and characterization of pre-mRNA splicing mutants of Saccharomyces cerevisiae. Genes Dev. 3:1989;1206-1216.
56. Wang S., Trumble W. R., Liao H., Wesson C. R., Dunker A. K., Kang C. H. Crystal structure of calsequestrin from rabbit skeletal muscle sarcoplasmic reticulum. Nature Struct. Biol. 5:1998;476-483.
57. Weichsel A., Gasdaska J. R., Powis G., Montfort W. R. Crystal structures of reduced, oxidized, and mutated human thioredoxins: evidence for a regulatory homodimer. Structure. 4:1996;735-751.
58. Will C. L., Lührmann R. Protein functions in pre-mRNA splicing. Curr. Opin. Cell Biol. 9:1997;320-328.
59. Wyatt J. R., Sontheimer E. J., Steitz J. A. Site-specific cross-linking of mammalian U5 snRNP to the 5′ splice site before the first step of pre-mRNA splicing. Genes Dev. 6:1992;2542-2553.