Three-dimensional Structure Determined for a Subunit of Human tRNA Splicing Endonuclease (Sen15) Reveals a Novel Dimeric Fold

Journal of Molecular Biology

Volumn 366, Issue 1, 2007, Pages 155-164

  Song, Jikui ^a   Markley, John L ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

beta barrel dimer interface; homodimeric protein assembly; NMR solution structure; tRNA splicing endonuclease

Indexed keywords

ENDONUCLEASE; PROTEIN SUBUNIT; TRANSFER RNA;

AMINO ACID SEQUENCE; ARCHAEBACTERIUM; ARTICLE; ENZYME STRUCTURE; EVOLUTION; INTRON; METHANOCALDOCOCCUS JANNASCHII; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FOLDING; RNA SPLICING; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; SEQUENCE ALIGNMENT;

EUKARYOTA; METHANOCALDOCOCCUS JANNASCHII;

EID: 33846321147     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.11.024     Document Type: Article

References (53)

1. Woese C.R., Kandler O., and Wheelis M.L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl Acad. Sci. USA 87 (1990) 4576-4579
2. Cech T. In: Gesteland R.F., and Atkins J.F. (Eds). RNA World (1993), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 239-270
3. Peebles C.L., Gegenheimer P., and Abelson J. Precise excision of intervening sequences from precursor tRNAs by a membrane-associated yeast endonuclease. Cell 32 (1983) 525-536
4. Thompson L.D., and Daniels C.J. Recognition of exon-intron boundaries by the Halobacterium volcanii tRNA intron endonuclease. J. Biol. Chem. 265 (1990) 18104-18111
5. Trotta C.R., Miao F., Arn E.A., Stevens S.W., Ho C.K., Rauhut R., et al. The yeast tRNA splicing endonuclease: a tetrameric enzyme with two active site subunits homologous to the archaeal tRNA endonucleases. Cell 89 (1997) 849-858
6. Englert M., and Beier H. Plant tRNA ligases are multifunctional enzymes that have diverged in sequence and substrate specificity from RNA ligases of other phylogenetic origins. Nucl. Acids Res. 33 (2005) 388-399
7. Greer C.L., Peebles C.L., Gegenheimer P., and Abelson J. Mechanism of action of a yeast RNA ligase in tRNA splicing. Cell 32 (1983) 537-546
8. Phizicky E.M., Schwartz R.C., and Abelson J. Saccharomyces cerevisiae tRNA ligase. Purification of the protein and isolation of the structural gene. J. Biol. Chem. 261 (1986) 2978-2986
9. + to transfer the splice junction 2′-phosphate from ligated tRNA to an acceptor molecule. J. Biol. Chem. 266 (1991) 11986-11992
10. McCraith S.M., and Phizicky E.M. A highly specific phosphatase from Saccharomyces cerevisiae implicated in tRNA splicing. Mol. Cell Biol. 10 (1990) 1049-1055
11. Trotta C.R., Paushkin S.V., Patel M., Li H., and Peltz S.W. Cleavage of pre-tRNAs by the splicing endonuclease requires a composite active site. Nature 441 (2006) 375-377
12. Xue S., Calvin K., and Li H. RNA recognition and cleavage by a splicing endonuclease. Science 312 (2006) 906-910
13. Abelson J., Trotta C.R., and Li H. tRNA splicing. J. Biol. Chem. 273 (1998) 12685-12688
14. Thompson L.D., and Daniels C.J. Recognition of exon-intron boundaries by the Halobacterium volcanii tRNA intron endonuclease. J. Biol. Chem. 265 (1990) 18104-18111
15. Reyes V.M., and Abelson J. Substrate recognition and splice site determination in yeast tRNA splicing. Cell 55 (1988) 719-730
16. Tang T.H., Rozhdestvensky T.S., d'Orval B.C., Bortolin M.L., Huber H., Charpentier B., et al. RNomics in Archaea reveals a further link between splicing of archaeal introns and rRNA processing. Nucl. Acids Res. 30 (2002) 921-930
17. Kjems J., and Garrett R.A. Novel splicing mechanism for the ribosomal RNA intron in the archaebacterium Desulfurococcus mobilis. Cell 54 (1988) 693-703
18. Watanabe Y., Yokobori S., Inaba T., Yamagishi A., Oshima T., Kawarabayasi Y., et al. Introns in protein-coding genes in Archaea. FEBS Letters 510 (2002) 27-30
19. Diener J.L., and Moore P.B. Solution structure of a substrate for the archaeal pre-tRNA splicing endonucleases: the bulge-helix-bulge motif. Mol. Cell 1 (1998) 883-894
20. Armbruster D.W., and Daniels C.J. Splicing of intron-containing tRNATrp by the archaeon Haloferax volcanii occurs independent of mature tRNA structure. J. Biol. Chem. 272 (1997) 19758-19762
21. Thompson L.D., and Daniels C.J. A tRNA(Trp) intron endonuclease from Halobacterium volcanii. Unique substrate recognition properties. J. Biol. Chem. 263 (1988) 17951-17959
22. Reyes V.M., and Abelson J. Substrate recognition and splice site determination in yeast tRNA splicing. Cell 55 (1988) 719-730
23. Baldi M.I., Mattoccia E., Bufardeci E., Fabbri S., and Tocchini-Valentini G.P. Participation of the intron in the reaction catalyzed by the Xenopus tRNA splicing endonuclease. Science 255 (1992) 1404-1408
24. Li H., and Abelson J. Crystal structure of a dimeric archaeal splicing endonuclease. J. Mol. Biol. 302 (2000) 639-648
25. Li H., Trotta C.R., and Abelson J. Crystal structure and evolution of a transfer RNA splicing enzyme. Science 280 (1998) 279-284
26. Lykke-Andersen J., and Garrett R.A. RNA-protein interactions of an archaeal homotetrameric splicing endoribonuclease with an exceptional evolutionary history. EMBO J. 16 (1997) 6290-6300
27. Calvin K., Hall M.D., Xu F., Xue S., and Li H. Structural characterization of the catalytic subunit of a novel RNA splicing endonuclease. J. Mol. Biol. 353 (2005) 952-960
28. Tocchini-Valentini G.D., Fruscoloni P., and Tocchini-Valentini G.P. Structure, function, and evolution of the tRNA endonucleases of Archaea: an example of subfunctionalization. Proc. Natl Acad. Sci. USA 102 (2005) 8933-8938
29. Randau L., Calvin K., Hall M., Yuan J., Podar M., Li H., et al. The heteromeric Nanoarchaeum equitans splicing endonuclease cleaves noncanonical bulge-helix-bulge motifs of joined tRNA halves. Proc. Natl Acad. Sci. USA 102 (2005) 17934-17939
30. Paushkin S.V., Patel M., Furia B.S., Peltz S.W., and Trotta C.R. Identification of a human endonuclease complex reveals a link between tRNA splicing and pre-mRNA 3′ end formation. Cell 117 (2004) 311-321
31. Ho C.K., Rauhut R., Vijayraghavan U., and Abelson J. Accumulation of pre-tRNA splicing ′2/3′ intermediates in a Saccharomyces cerevisiae mutant. EMBO J. 9 (1990) 1245-1252
32. McGuffin L.J., Bryson K., and Jones D.T. The PSIPRED protein structure prediction server. Bioinformatics 16 (2000) 404-405
33. Song J., Tyler R.C., Lee M.S., Tyler E.M., and Markley J.L. Solution structure of isoform 1 of Roadblock/LC7, a light chain in the dynein complex. J. Mol. Biol. 354 (2005) 1043-1051
34. Altieri A.S., Hinton D.P., and Byrd R.A. Association of biomolecular systems via PFG-NMR diffusion measurements. J. Am. Chem. Soc. 117 (1995) 7566-7567
35. Güntert P., Mumenthaler C., and Wüthrich K. Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 273 (1997) 283-298
36. Herrmann T., Güntert P., and Wüthrich K. Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol. 319 (2002) 209-227
37. Linge J.P., Williams M.A., Spronk C.A., Bonvin A.M., and Nilges M. Refinement of protein structures in explicit solvent. Proteins: Struct. Funct. Genet. 50 (2003) 496-506
38. Schwieters C.D., Kuszewski J.J., Tjandra N., and Clore G.M. The Xplor-NIH NMR molecular structure determination package. J. Magn. Reson. 160 (2003) 65-73
39. Zweckstetter M., and Bax A. Prediction of sterically induced alignment in a dilute liquid crystalline phase: aid to protein structure determination by NMR. J. Am. Chem. Soc. 122 (2000) 3791-3792
40. Laskowski R.A., Rullmann J.A.C., MacArthur M.W., Kaptein R., and Thornton J.M. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8 (1996) 477-486
41. Koradi R., Billeter M., and Wüthrich K. MOLMOL- a program for display and analysis of macromolecular sstructures. J. Mol. Graph. 14 (1996) 51-55
42. Kleman-Leyer K., Armbruster D.W., and Daniels C.J. Properties of H. volcanii tRNA intron endonuclease reveal a relationship between the archaeal and eucaryal tRNA intron processing systems. Cell 89 (1997) 839-847
43. Tocchini-Valentini G.D., Fruscoloni P., and Tocchini-Valentini G.P. Coevolution of tRNA intron motifs and tRNA endonuclease architecture in Archaea. Proc. Natl Acad. Sci. USA 102 (2005) 15418-15422
44. 15N. J. Struct. Funct. Genomics 5 (2004) 87-93
45. Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M.D., et al. Measurement of protein using bicinchoninic acid. Anal. Biochem. 150 (1985) 76-85
46. Zwahlen C., Legault P., Vincent S.J.F., Greenblatt J., Konrat R., and Kay L.E. Methods for measurement of intermolecular NOEs by multinuclear NMR spectroscopy: application to a bacteriophage lambda N-peptide/boxB RNA complex. J. Am. Chem. Soc. 119 (1997) 6711-6721
47. Ottiger M., Delaglio F., and Bax A. Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra. J. Magn. Reson. 131 (1998) 373-378
48. 15N NMR relaxation. Biochemistry 33 (1994) 5984-6003
49. 13C alpha nuclear spin relaxation. J. Biomol. NMR 9 (1997) 287-298
50. 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
51. Bartels C., Billeter M., Güntert P., and Wüthrich K. Auto sequence-specific NMR assignment of homologous proteins using the program GARANT. J. Biomol. NMR 7 (1996) 207-213
52. Cornilescu G., Delaglio F., and Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13 (1999) 289-302
53. 13C chemical shifts. J. Biomol. NMR 4 (1994) 171-180