Structural and functional insights into the N-terminus of Schizosaccharomyces pombe Cdc5

Biochemistry

Volumn 53, Issue 41, 2014, Pages 6439-6451

  Collier, Scott E ^a   Voehler, Markus ^a   Peng, Dungeng ^a   Ohi, Ryoma ^a   Gould, Kathleen L ^a   Reiter, Nicholas J ^a   Ohi, Melanie D ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

N TERMINUS; SCHIZOSACCHAROMYCES POMBE;

DOUBLE STRANDED RNA; SCHIZOSACCHAROMYCES POMBE CDC5; SCHIZOSACCHAROMYCES POMBE PROTEIN; UNCLASSIFIED DRUG; CDC5 PROTEIN, S POMBE; CELL CYCLE PROTEIN; FUNGAL RNA; MUTANT PROTEIN; PEPTIDE FRAGMENT; RECOMBINANT PROTEIN; RNA BINDING PROTEIN; SMALL NUCLEAR RNA;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; DELETION MUTANT; FUNGAL GENETICS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN RNA BINDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; RNA SPLICING; RNA STRUCTURE; SEQUENCE ALIGNMENT; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVE SITE; GENE DELETION; GENETICS; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN STABILITY; SPLICEOSOME; TITRIMETRY;

BINDING SITES; CATALYTIC DOMAIN; CELL CYCLE PROTEINS; GENE DELETION; MODELS, MOLECULAR; MUTANT PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STABILITY; RECOMBINANT PROTEINS; RNA SPLICING; RNA, DOUBLE-STRANDED; RNA, FUNGAL; RNA, SMALL NUCLEAR; RNA-BINDING PROTEINS; SCHIZOSACCHAROMYCES POMBE PROTEINS; SPLICEOSOMES; TITRIMETRY;

EID: 84908170400     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi5008639     Document Type: Article

References (102)

1. Tarn, W. Y., Hsu, C. H., Huang, K. T., Chen, H. R., Kao, H. Y., Lee, K. R., and Cheng, S. C. (1994) Functional association of essential splicing factor(s) with PRP19 in a protein complex EMBO J. 13, 2421-2431
2. Ajuh, P., Kuster, B., Panov, K., Zomerdijk, J. C., Mann, M., and Lamond, A. I. (2000) Functional analysis of the human CDC5L complex and identification of its components by mass spectrometry EMBO J. 19, 6569-6581
3. Grote, M., Wolf, E., Will, C. L., Lemm, I., Agafonov, D. E., Schomburg, A., Fischle, W., Urlaub, H., and Luhrmann, R. (2010) Molecular architecture of the human Prp19/CDC5L complex Mol. Cell. Biol. 30, 2105-2119
4. Chen, H. R., Jan, S. P., Tsao, T. Y., Sheu, Y. J., Banroques, J., and Cheng, S. C. (1998) Snt309p, a component of the Prp19p-associated complex that interacts with Prp19p and associates with the spliceosome simultaneously with or immediately after dissociation of U4 in the same manner as Prp19p Mol. Cell. Biol. 18, 2196-2204
5. Tsai, W. Y., Chow, Y. T., Chen, H. R., Huang, K. T., Hong, R. I., Jan, S. P., Kuo, N. Y., Tsao, T. Y., Chen, C. H., and Cheng, S. C. (1999) Cef1p is a component of the Prp19p-associated complex and essential for pre-mRNA splicing J. Biol. Chem. 274, 9455-9462
6. Chen, C. H., Tsai, W. Y., Chen, H. R., Wang, C. H., and Cheng, S. C. (2001) Identification and characterization of two novel components of the Prp19p-associated complex, Ntc30p and Ntc20p J. Biol. Chem. 276, 488-494
7. Chen, C.-H., Yu, W.-C., Tsao, T. Y., Wang, L.-Y., Chen, H.-R., Lin, J.-Y., Tsai, W.-Y., and Cheng, S.-C. (2002) Functional and physical interactions between components of the Prp19p-associated complex Nucleic Acids Res. 30, 1029-1037
8. Ohi, M. D. and Gould, K. L. (2002) Characterization of interactions among the Cef1p-Prp19p-associated splicing complex RNA 8, 798-815
9. Ben-Yehuda, S., Dix, I., Russell, C. S., McGarvey, M., Beggs, J. D., and Kupiec, M. (2000) Genetic and physical interactions between factors involved in both cell cycle progression and pre-mRNA splicing in Saccharomyces cerevisiae Genetics 156, 1503-1517
10. Chan, S. P., Kao, D. I., Tsai, W. Y., and Cheng, S. C. (2003) The Prp19p-associated complex in spliceosome activation Science 302, 279-282
11. Chan, S.-P. and Cheng, S.-C. (2005) The Prp19-associated complex is required for specifying interactions of U5 and U6 with pre-mRNA during spliceosome activation J. Biol. Chem. 280, 31190-31199
12. Villa, T. and Guthrie, C. (2005) The Isy1p component of the NineTeen complex interacts with the ATPase Prp16p to regulate the fidelity of pre-mRNA splicing Genes Dev. 19, 1894-1904
13. Pleiss, J. A., Whitworth, G. B., Bergkessel, M., and Guthrie, C. (2007) Transcript specificity in yeast pre-mRNA splicing revealed by mutations in core spliceosomal components PLoS Biol. 5, e90
14. Ohi, R., McCollum, D., Hirani, B., Den Haese, G. J., Zhang, X., Burke, J. D., Turner, K., and Gould, K. L. (1994) The Schizosaccharomyces pombe cdc5+ gene encodes an essential protein with homology to c-Myb EMBO J. 13, 471-483
15. McGrail, J. C., Krause, A., and O'Keefe, R. T. (2009) The RNA binding protein Cwc2 interacts directly with the U6 snRNA to link the nineteen complex to the spliceosome during pre-mRNA splicing Nucleic Acids Res. 37, 4205-4217
16. Rasche, N., Dybkov, O., Schmitzova, J., Akyildiz, B., Fabrizio, P., and Luhrmann, R. (2012) Cwc2 and its human homologue RBM22 promote an active conformation of the spliceosome catalytic centre EMBO J. 31, 1591-1604
17. Nurse, P., Thuriaux, P., and Nasmyth, K. (1976) Genetic control of the cell division cycle in the fission yeast Schizosaccharomyces pombe Mol. Gen. Genet. 146, 167-178
18. McDonald, W. H., Ohi, R., Smelkova, N., Frendewey, D., and Gould, K. L. (1999) Myb-related fission yeast cdc5p is a component of a 40S snRNP-containing complex and is essential for pre-mRNA splicing Mol. Cell. Biol. 19, 5352-5362
19. Burns, C. G., Ohi, R., Krainer, A. R., and Gould, K. L. (1999) Evidence that Myb-related CDC5 proteins are required for pre-mRNA splicing Proc. Natl. Acad. Sci. U.S.A. 96, 13789-13794
20. Ohi, M. D., Link, A. J., Ren, L., Jennings, J. L., McDonald, W. H., and Gould, K. L. (2002) Proteomics analysis reveals stable multiprotein complexes in both fission and budding yeasts containing Myb-related Cdc5p/Cef1p, novel pre-mRNA splicing factors, and snRNAs Mol. Cell. Biol. 22, 2011-2024
21. Liu, L., Gräub, R., Hlaing, M., Epting, C. L., Turck, C. W., Xu, X.-Q., Zhang, L., and Bernstein, H. S. (2003) Distinct domains of human CDC5 direct its nuclear import and association with the spliceosome Cell Biochem. Biophys. 39, 119-132
22. Burns, C. G., Ohi, R., Mehta, S., O'Toole, E. T., Winey, M., Clark, T. A., Sugnet, C. W., Ares, M., and Gould, K. L. (2002) Removal of a single alpha-tubulin gene intron suppresses cell cycle arrest phenotypes of splicing factor mutations in Saccharomyces cerevisiae Mol. Cell. Biol. 22, 801-815
23. Zhou, Z., Licklider, L. J., Gygi, S. P., and Reed, R. (2002) Comprehensive proteomic analysis of the human spliceosome Nature 419, 182-185
24. Lin, Z., Yin, K., Zhu, D., Chen, Z., Gu, H., and Qu, L. J. (2007) AtCDC5 regulates the G2 to M transition of the cell cycle and is critical for the function of Arabidopsis shoot apical meristem Cell Res. 17, 815-828
25. Zhang, N., Kaur, R., Lu, X., Shen, X., Li, L., and Legerski, R. J. (2005) The Pso4 mRNA splicing and DNA repair complex interacts with WRN for processing of DNA interstrand cross-links J. Biol. Chem. 280, 40559-40567
26. Zhang, N., Kaur, R., Akhter, S., and Legerski, R. J. (2009) Cdc5L interacts with ATR and is required for the S-phase cell-cycle checkpoint EMBO Rep. 10, 1029-1035
27. Maréchal, A., Li, J. M., Ji, X. Y., Wu, C. S., Yazinski, S. A., Nguyen, H. D., Liu, S., Jiménez, A. E., Jin, J., and Zou, L. (2014) PRP19 transforms into a sensor of RPA-ssDNA after DNA damage and drives ATR activation via a ubiquitin-mediated circuitry Mol. Cell 53, 235-246
28. Wan, L. and Huang, J. (2014) The PSO4 protein complex associates with replication protein A (RPA) and modulates the activation of ataxia telangiectasia-mutated and Rad3-related (ATR) J. Biol. Chem. 289, 6619-6626
29. Hofmann, J. C., Tegha-Dunghu, J., Dräger, S., Will, C. L., Lührmann, R., and Gruss, O. J. (2013) The Prp19 complex directly functions in mitotic spindle assembly PLoS One 8, e74851
30. Zhang, S., Xie, M., Ren, G., and Yu, B. (2013) CDC5, a DNA binding protein, positively regulates posttranscriptional processing and/or transcription of primary microRNA transcripts Proc. Natl. Acad. Sci. U.S.A. 110, 17588-17593
31. Ohi, R., Feoktistova, A., McCann, S., Valentine, V., Look, A. T., Lipsick, J. S., and Gould, K. L. (1998) Myb-related Schizosaccharomyces pombe cdc5p is structurally and functionally conserved in eukaryotes Mol. Cell. Biol. 18, 4097-4108
32. Query, C. C. and Konarska, M. M. (2012) CEF1/CDC5 alleles modulate transitions between catalytic conformations of the spliceosome RNA 18, 1001-1013
33. Prouse, M. B. and Campbell, M. M. (2012) The interaction between MYB proteins and their target DNA binding sites Biochim. Biophys. Acta 1819, 67-77
34. Ogata, K., Hojo, H., Aimoto, S., Nakai, T., Nakamura, H., Sarai, A., Ishii, S., and Nishimura, Y. (1992) Solution structure of a DNA-binding unit of Myb: a helix-turn-helix-related motif with conserved tryptophans forming a hydrophobic core Proc. Natl. Acad. Sci. U.S.A. 89, 6428-6432
35. Hirayama, T. and Shinozaki, K. (1996) A cdc5+ homolog of a higher plant, Arabidopsis thaliana Proc. Natl. Acad. Sci. U.S.A. 93, 13371-13376
36. Lei, X. H., Shen, X., Xu, X. Q., and Bernstein, H. S. (2000) Human Cdc5, a regulator of mitotic entry, can act as a site-specific DNA binding protein J. Cell Sci. 113, 4523-4531
37. Hogg, R., de Almeida, R. A., Ruckshanthi, J. P., and O'Keefe, R. T. (2014) Remodeling of U2-U6 snRNA helix I during pre-mRNA splicing by Prp16 and the NineTeen Complex protein Cwc2 Nucleic Acids Res. 42, 8008-8023
38. Keeney, J. B. and Boeke, J. D. (1994) Efficient targeted integration at leu1-32 and ura4-294 in Schizosaccharomyces pombe Genetics 136, 849-856
39. Livesay, S. B., Collier, S. E., Bitton, D. A., Bähler, J., and Ohi, M. D. (2013) Structural and functional characterization of the N terminus of Schizosaccharomyces pombe Cwf10 Eukaryotic Cell 12, 1472-1489
40. Wilkins, M. R., Gasteiger, E., Bairoch, A., Sanchez, J. C., Williams, K. L., Appel, R. D., and Hochstrasser, D. F. (1999) Protein identification and analysis tools in the ExPASy server Methods Mol. Biol. 112, 531-552
41. Cheng, H., Westler, W. M., Xia, B., Oh, B. H., and Markley, J. L. (1995) Protein expression, selective isotopic labeling, and analysis of hyperfine-shifted NMR signals of Anabaena 7120 vegetative [2Fe-2S]ferredoxin Arch. Biochem. Biophys. 316, 619-634
42. Zhou, Z., Sim, J., Griffith, J., and Reed, R. (2002) Purification and electron microscopic visualization of functional human spliceosomes Proc. Natl. Acad. Sci. U.S.A. 99, 12203-12207
43. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling Biophys. J. 78, 1606-1619
44. Schleucher, J., Schwendinger, M., Sattler, M., Schmidt, P., Schedletzky, O., Glaser, S. J., Sørensen, O. W., and Griesinger, C. (1994) A general enhancement scheme in heteronuclear multidimensional NMR employing pulsed field gradients J. Biomol NMR 4, 301-306
45. Grzesiek, S. and Bax, A. (1993) The importance of not saturating water in protein NMR. Application to sensitivity enhancement and NOE measurements J. Am. Chem. Soc. 115, 12593-12594
46. Palmer, A., Cavanagh, J., Byrd, R., and Rance, M. (1992) Sensitivity improvement in 3-dimensional heteronuclear correlation NMR spectroscopy J. Magn. Reson. 96, 416-424
47. Lewis, K. E., Keifer, P., and Saarinen, T. (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity J. Am. Chem. Soc. 114, 10663-10665
48. Grzesiek, S. and Bax, A. (1992) An efficient experiment for sequential backboneassignment of medium-sized isotopically enriched protein J. Magn. Reson. 99, 201-207
49. 15N-enriched proteins J. Biomol. NMR 3, 185-204
50. Wittekind, M. and Mueller, L. (1993) HNCACB, a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the alpha- and beta-carbon resonances in proteins J. Magn. Reson. B 101, 201-205
51. 13C-labelled proteins J. Magn. Reson. 97, 213-217
52. Davis, A. L., Keeler, J., Laue, E. D., and Moskau, D. (1992) Experiments for recording pure-absorption heteronuclear correlation spectra using pulsed field gradients J. Magn. Reson. 98, 207-216
53. Shen, Y., Delaglio, F., Cornilescu, G., and Bax, A. (2009) TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts J. Biomol. NMR 44, 213-223
54. Shen, Y., Vernon, R., Baker, D., and Bax, A. (2009) De novo protein structure generation from incomplete chemical shift assignments J. Biomol. NMR 43, 63-78
55. Shen, Y., Lange, O., Delaglio, F., Rossi, P., Aramini, J. M., Liu, G., Eletsky, A., Wu, Y., Singarapu, K. K., Lemak, A., Ignatchenko, A., Arrowsmith, C. H., Szyperski, T., Montelione, G. T., Baker, D., and Bax, A. (2008) Consistent blind protein structure generation from NMR chemical shift data Proc. Natl. Acad. Sci. U.S.A. 105, 4685-4690
56. Dyballa, N. and Metzger, S. (2009) Fast and sensitive colloidal coomassie G-250 staining for proteins in polyacrylamide gels J. Visualized Exp. 30, 1431
57. Rasband, W. S. (1997-2004) ImageJ, U. S. National Institutes of Health, Bethesda, MD, http://imagej.nih.gov/ij/.
58. Martin-Tumasz, S., Reiter, N. J., Brow, D. A., and Butcher, S. E. (2010) Structure and functional implications of a complex containing a segment of U6 RNA bound by a domain of Prp24 RNA 16, 792-804
59. Barrett, P. J., Song, Y., Van Horn, W. D., Hustedt, E. J., Schafer, J. M., Hadziselimovic, A., Beel, A. J., and Sanders, C. R. (2012) The amyloid precursor protein has a flexible transmembrane domain and binds cholesterol Science 336, 1168-1171
60. Saikumar, P., Murali, R., and Reddy, E. P. (1990) Role of tryptophan repeats and flanking amino acids in Myb-DNA interactions Proc. Natl. Acad. Sci. U.S.A. 87, 8452-8456
61. Kanei-Ishii, C., Sarai, A., Sawazaki, T., Nakagoshi, H., He, D. N., Ogata, K., Nishimura, Y., and Ishii, S. (1990) The tryptophan cluster: a hypothetical structure of the DNA-binding domain of the myb protooncogene product J. Biol. Chem. 265, 19990-19995
62. Sauer, R. T., Yocum, R. R., Doolittle, R. F., Lewis, M., and Pabo, C. O. (1982) Homology among DNA-binding proteins suggests use of a conserved super-secondary structure Nature 298, 447-451
63. Ohlendorf, D. H., Anderson, W. F., and Matthews, B. W. (1983) Many gene-regulatory proteins appear to have a similar alpha-helical fold that binds DNA and evolved from a common precursor J. Mol. Evol. 19, 109-114
64. Li, X., Zhang, W., Xu, T., Ramsey, J., Zhang, L., Hill, R., Hansen, K. C., Hesselberth, J. R., and Zhao, R. (2013) Comprehensive in vivo RNA-binding site analyses reveal a role of Prp8 in spliceosomal assembly Nucleic Acids Res. 41, 3805-3818
65. Vander Kooi, C. W., Ren, L., Xu, P., Ohi, M. D., Gould, K. L., and Chazin, W. J. (2010) The Prp19 WD40 domain contains a conserved protein interaction region essential for its function Structure 18, 584-593
66. Schmitzová, J., Rasche, N., Dybkov, O., Kramer, K., Fabrizio, P., Urlaub, H., Lührmann, R., and Pena, V. (2012) Crystal structure of Cwc2 reveals a novel architecture of a multipartite RNA-binding protein EMBO J. 31, 2222-2234
67. Greenfield, N. and Fasman, G. D. (1969) Computed circular dichroism spectra for the evaluation of protein conformation Biochemistry 8, 4108-4116
68. Shen, Y. and Bax, A. (2012) Identification of helix capping and b-turn motifs from NMR chemical shifts J. Biomol. NMR 52, 211-232
69. Jurica, M. S., Licklider, L. J., Gygi, S. R., Grigorieff, N., and Moore, M. J. (2002) Purification and characterization of native spliceosomes suitable for three-dimensional structural analysis RNA 8, 426-439
70. Stevens, S. W., Ryan, D. E., Ge, H. Y., Moore, R. E., Young, M. K., Lee, T. D., and Abelson, J. (2002) Composition and functional characterization of the yeast spliceosomal penta-snRNP Mol. Cell 9, 31-44
71. Makarov, E. M., Makarova, O. V., Urlaub, H., Gentzel, M., Will, C. L., Wilm, M., and Lührmann, R. (2002) Small nuclear ribonucleoprotein remodeling during catalytic activation of the spliceosome Science 298, 2205-2208
72. Deckert, J., Hartmuth, K., Boehringer, D., Behzadnia, N., Will, C. L., Kastner, B., Stark, H., Urlaub, H., and Luhrmann, R. (2006) Protein composition and electron microscopy structure of affinity-purified human spliceosomal B complexes isolated under physiological conditions Mol. Cell. Biol. 26, 5528-5543
73. Bessonov, S., Anokhina, M., Will, C. L., Urlaub, H., and Lührmann, R. (2008) Isolation of an active step I spliceosome and composition of its RNP core Nature 452, 846-850
74. Warkocki, Z., Odenwalder, P., Schmitzova, J., Platzmann, F., Stark, H., Urlaub, H., Ficner, R., Fabrizio, P., and Luhrmann, R. (2009) Reconstitution of both steps of Saccharomyces cerevisiae splicing with purified spliceosomal components Nat. Struct. Mol. Biol. 16, 1237-1243
75. Fabrizio, P., Dannenberg, J., Dube, P., Kastner, B., Stark, H., Urlaub, H., and Lührmann, R. (2009) The evolutionarily conserved core design of the catalytic activation step of the yeast spliceosome Mol. Cell 36, 593-608
76. act spliceosomal complexes reveals compositional and morphological changes during spliceosome activation and first step catalysis RNA 16, 2384-2403
77. Ren, L., McLean, J. R., Hazbun, T. R., Fields, S., Vander Kooi, C., Ohi, M. D., and Gould, K. L. (2011) Systematic two-hybrid and comparative proteomic analyses reveal novel yeast pre-mRNA splicing factors connected to Prp19 PLoS One 6, e16719
78. Cvitkovic, I. and Jurica, M. S. (2013) Spliceosome database: a tool for tracking components of the spliceosome Nucleic Acids Res. 41, D132-141
79. Lardelli, R. M., Thompson, J. X., Yates, J. R., and Stevens, S. W. (2010) Release of SF3 from the intron branchpoint activates the first step of pre-mRNA splicing RNA 16, 516-528
80. Fourmann, J. B., Schmitzová, J., Christian, H., Urlaub, H., Ficner, R., Boon, K. L., Fabrizio, P., and Lührmann, R. (2013) Dissection of the factor requirements for spliceosome disassembly and the elucidation of its dissociation products using a purified splicing system Genes Dev. 27, 413-428
81. Lesser, C. F. and Guthrie, C. (1993) Mutations in U6 snRNA that alter splice site specificity: implications for the active site Science 262, 1982-1988
82. Yean, S. L., Wuenschell, G., Termini, J., and Lin, R. J. (2000) Metal-ion coordination by U6 small nuclear RNA contributes to catalysis in the spliceosome Nature 408, 881-884
83. 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
84. Sontheimer, E. J. and Steitz, J. A. (1993) The U5 and U6 small nuclear RNAs as active site components of the spliceosome Science 262, 1989-1996
85. Burke, J. E., Sashital, D. G., Zuo, X., Wang, Y.-X., and Butcher, S. E. (2012) Structure of the yeast U2/U6 snRNA complex RNA 18, 673-683
86. Montemayor, E. J., Curran, E. C., Liao, H. H., Andrews, K. L., Treba, C. N., Butcher, S. E., and Brow, D. A. (2014) Core structure of the U6 small nuclear ribonucleoprotein at 1.7-Å resolution Nat. Struct. Mol. Biol. 21, 544-551
87. Sashital, D. G., Cornilescu, G., McManus, C. J., Brow, D. A., and Butcher, S. E. (2004) U2-U6 RNA folding reveals a group II intron-like domain and a four-helix junction Nat. Struct. Mol. Biol. 11, 1237-1242
88. Ogata, K., Morikawa, S., Nakamura, H., Sekikawa, A., Inoue, T., Kanai, H., Sarai, A., Ishii, S., and Nishimura, Y. (1994) Solution structure of a specific DNA complex of the Myb DNA-binding domain with cooperative recognition helices Cell 79, 639-648
89. Ogata, K., Morikawa, S., Nakamura, H., Hojo, H., Yoshimura, S., Zhang, R., Aimoto, S., Ametani, Y., Hirata, Z., and Sarai, A. (1995) Comparison of the free and DNA-complexed forms of the DNA-binding domain from c-Myb Nat. Struct. Biol. 2, 309-320
90. Hausner, T. P., Giglio, L. M., and Weiner, A. M. (1990) Evidence for base-pairing between mammalian U2 and U6 small nuclear ribonucleoprotein particles Genes Dev. 4, 2146-2156
91. Datta, B. and Weiner, A. M. (1991) Genetic evidence for base pairing between U2 and U6 snRNA in mammalian mRNA splicing Nature 352, 821-824
92. Luukkonen, B. G. and Séraphin, B. (1998) Genetic interaction between U6 snRNA and the first intron nucleotide in Saccharomyces cerevisiae RNA 4, 167-180
93. Seetharaman, M., Eldho, N. V., Padgett, R. A., and Dayie, K. T. (2006) Structure of a self-splicing group II intron catalytic effector domain 5: parallels with spliceosomal U6 RNA RNA 12, 235-247
94. Reiter, N. J., Blad, H., Abildgaard, F., and Butcher, S. E. (2004) Dynamics in the U6 RNA intramolecular stem-loop: a base flipping conformational change Biochemistry 43, 13739-13747
95. Fica, S. M., Mefford, M. A., Piccirilli, J. A., and Staley, J. P. (2014) Evidence for a group II intron-like catalytic triplex in the spliceosome Nat. Struct Mol. Biol. 21, 464-471
96. Valadkhan, S., Mohammadi, A., Jaladat, Y., and Geisler, S. (2009) Protein-free small nuclear RNAs catalyze a two-step splicing reaction Proc. Natl. Acad. Sci. U.S.A. 106, 11901-11906
97. Valadkhan, S. and Manley, J. L. (2001) Splicing-related catalysis by protein-free snRNAs Nature 413, 701-707
98. Buchan, D. W., Minneci, F., Nugent, T. C., Bryson, K., and Jones, D. T. (2013) Scalable web services for the PSIPRED protein analysis workbench Nucleic Acids Res. 41, W349-357
99. Jones, D. T. (1999) Protein secondary structure prediction based on position-specific scoring matrices J. Mol. Biol. 292, 195-202
100. Hiraoka, Y., Toda, T., and Yanagida, M. (1984) The NDA3 gene of fission yeast encodes beta-tubulin: a cold-sensitive nda3 mutation reversibly blocks spindle formation and chromosome movement in mitosis Cell 39, 349-358
101. Vander Kooi, C. W., Ohi, M. D., Rosenberg, J. A., Oldham, M. L., Newcomer, M. E., Gould, K. L., and Chazin, W. J. (2006) The Prp19 U-box crystal structure suggests a common dimeric architecture for a class of oligomeric E3 ubiquitin ligases Biochemistry 45, 121-130
102. Lu, P., Lu, G., Yan, C., Wang, L., Li, W., and Yin, P. (2012) Structure of the mRNA splicing complex component Cwc2: insights into RNA recognition Biochem. J. 441, 591-597