Insights into the activation of the helicase Prp43 by biochemical studies and structural mass spectrometry

Nucleic Acids Research

Volumn 42, Issue 2, 2014, Pages 1162-1179

  Christian, Henning ^a   Hofele, Romina V ^b   Urlaub, Henning ^b,c   Ficner, Ralf ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^c UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HELICASE; HELICASE PRP43; NTR1 PROTEIN; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME LOCALIZATION; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEIN SECONDARY STRUCTURE; STRUCTURAL PROTEOMICS; STRUCTURE ANALYSIS;

AMINO ACID MOTIFS; DEAD-BOX RNA HELICASES; ENZYME ACTIVATION; INTRINSICALLY DISORDERED PROTEINS; MASS SPECTROMETRY; MODELS, MOLECULAR; PROTEIN INTERACTION DOMAINS AND MOTIFS; RNA; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84893249767     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt985     Document Type: Article

References (78)

1. Hocine, S., Singer, R. and Grunwald, D. (2010) RNA processing and export. Cold Spring Harb. Perspect. Biol., 2, a000752.
2. Moore, M. and Proudfoot, N. (2009) Pre-mRNA processing reaches back to transcription and ahead to translation. Cell, 136, 688-700.
3. Will, C. and Luhrmann, R. (2011) Spliceosome structure and function. Cold Spring Harb. Perspect. Biol., 3, pii: a003707.
4. Wahl, M., Will, C. and Luhrmann, R. (2009) The spliceosome: design principles of a dynamic RNP machine. Cell, 136, 701-718.
5. Tarn, W. and Steitz, J. (1996) A novel spliceosome containing U11, U12, and U5 snRNPs excises a minor class (AT-AC) intron in vitro. Cell, 84, 801-811.
6. Turunen, J., Niemela, E., Verma, B. and Frilander, M. (2012) The significant other: splicing by the minor spliceosome. Wiley Interdiscip. Rev. RNA, 4, 61-76.
7. Fabrizio, P., Dannenberg, J., Dube, P., Kastner, B., Stark, H., Urlaub, H. and Luhrmann, R. (2009) The evolutionarily conserved core design of the catalytic activation step of the yeast spliceosome. Mol. Cell, 36, 593-608.
8. Staley, J. and Guthrie, C. (1998) Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell, 92, 315-326.
9. Cordin, O., Hahn, D. and Beggs, J. (2012) Structure, function and regulation of spliceosomal RNA helicases. Curr. Opin. Cell Biol., 24, 431-438.
10. Kistler, A. and Guthrie, C. (2001) Deletion of MUD2, the yeast homolog of U2AF65, can bypass the requirement for sub2, an essential spliceosomal ATPase. Genes Dev., 15, 42-49.
11. Xu, Y. and Query, C. (2007) Competition between the ATPase Prp5 and branch region-U2 snRNA pairing modulates the fidelity of spliceosome assembly. Mol. Cell, 28, 838-849.
12. Raghunathan, P. and Guthrie, C. (1998) A spliceosomal recycling factor that reanneals U4 and U6 small nuclear ribonucleoprotein particles. Science, 279, 857-860.
13. Small, E., Leggett, S., Winans, A. and Staley, J. (2006) The EF-Glike GTPase Snu114p regulates spliceosome dynamics mediated by Brr2p, a DExD/H box ATPase. Mol. Cell, 23, 389-399.
14. Tseng, C., Liu, H. and Cheng, S. (2011) DEAH-box ATPase Prp16 has dual roles in remodeling of the spliceosome in catalytic steps. RNA, 17, 145-154.
15. Umen, J. and Guthrie, C. (1995) Prp16p, Slu7p, and Prp8p interact with the 3' splice site in two distinct stages during the second catalytic step of pre-mRNA splicing. RNA, 1, 584-597.
16. 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.
17. Company, M., Arenas, J. and Abelson, J. (1991) Requirement of the RNA helicase-like protein PRP22 for release of messenger RNA from spliceosomes. Nature, 349, 487-493.
18. Schwer, B. (2008) A conformational rearrangement in the spliceosome sets the stage for Prp22-dependent mRNA release. Mol. Cell, 30, 743-754.
19. Arenas, J. and Abelson, J. (1997) Prp43: An RNA helicase-like factor involved in spliceosome disassembly. Proc. Natl Acad. Sci. USA, 94, 11798-11802.
20. Fourmann, J., Schmitzova, J., Christian, H., Urlaub, H., Ficner, R., Boon, K., Fabrizio, P. and Luhrmann, 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.
21. Lebaron, S., Froment, C., Fromont-Racine, M., Rain, J., Monsarrat, B., Caizergues-Ferrer, M. and Henry, Y. (2005) The splicing ATPase prp43p is a component of multiple preribosomal particles. Mol. Cell. Biol., 25, 9269-9282.
22. Bohnsack, M., Martin, R., Granneman, S., Ruprecht, M., Schleiff, E. and Tollervey, D. (2009) Prp43 bound at different sites on the pre-rRNA performs distinct functions in ribosome synthesis. Mol. Cell, 36, 583-592.
23. Burgess, S. and Guthrie, C. (1993) A mechanism to enhance mRNA splicing fidelity: the RNA-dependent ATPase Prp16 governs usage of a discard pathway for aberrant lariat intermediates. Cell, 73, 1377-1391.
24. Semlow, D. and Staley, J. (2012) Staying on message: ensuring fidelity in pre-mRNA splicing. Trends Biochem. Sci., 37, 263-273.
25. Yang, F., Wang, X.-Y., Zhang, Z.-M., Pu, J., Fan, Y.-J., Zhou, J., Query, C.C. and Xu, Y.-Z. (2013) Splicing proofreading at 5' splice sites by ATPase Prp28p. Nucleic Acids Res., 41, 4660-4670.
26. Fairman-Williams, M., Guenther, U. and Jankowsky, E. (2010) SF1 and SF2 helicases: family matters. Curr. Opin. Struct. Biol., 20, 313-324.
27. Subramanya, H., Bird, L., Brannigan, J. and Wigley, D. (1996) Crystal structure of a DExx box DNA helicase. Nature, 384, 379-383.
28. Rocak, S. and Linder, P. (2004) DEAD-box proteins: the driving forces behind RNA metabolism. Nat. Rev. Mol. Cell Biol., 5, 232-241.
29. Pyle, A. (2008) Translocation and unwinding mechanisms of RNA and DNA helicases. Ann. Rev. Biophys., 37, 317-336.
30. Silverman, E., Maeda, A., Wei, J., Smith, P., Beggs, J. and Lin, R. (2004) Interaction between a G-patch protein and a spliceosomal DEXD/H-box ATPase that is critical for splicing. Mol. Cell. Biol., 24, 10101-10110.
31. Tsai, R., Tseng, C., Lee, P., Chen, H., Fu, R., Chang, K., Yeh, F. and Cheng, S. (2007) Dynamic interactions of Ntr1-Ntr2 with Prp43 and with U5 govern the recruitment of Prp43 to mediate spliceosome disassembly. Mol. Cell. Biol., 27, 8027-8037.
32. Aravind, L. and Koonin, E. (1999) G-patch: a new conserved domain in eukaryotic RNA-processing proteins and type D retroviral polyproteins. Trends Biochem. Sci., 24, 342-344.
33. Tanaka, N., Aronova, A. and Schwer, B. (2007) Ntr1 activates the Prp43 helicase to trigger release of lariat-intron from the spliceosome. Genes Dev., 21, 2312-2325.
34. Buttner, K., Nehring, S. and Hopfner, K. (2007) Structural basis for DNA duplex separation by a superfamily-2 helicase. Nat. Struct. Mol. Biol., 14, 647-652.
35. He, Y., Andersen, G. and Nielsen, K. (2010) Structural basis for the function of DEAH helicases. EMBO Rep., 11, 180-186.
36. Walbott, H., Mouffok, S., Capeyrou, R., Lebaron, S., Humbert, O., van Tilbeurgh, H., Henry, Y. and Leulliot, N. (2010) Prp43p contains a processive helicase structural architecture with a specific regulatory domain. EMBO J., 29, 2194-2204.
37. Kudlinzki, D., Schmitt, A., Christian, H. and Ficner, R. (2012) Structural analysis of the C-terminal domain of the spliceosomal helicase Prp22. Biol. Chem., 393, 1131-1140.
38. Herzog, F., Kahraman, A., Boehringer, D., Mak, R., Bracher, A., Walzthoeni, T., Leitner, A., Beck, M., Hartl, F.-U., Ban, N. et al. (2012) Structural probing of a protein phosphatase 2A network by chemical cross-linking and mass spectrometry. Science, 337, 1348-1352.
39. Schmitzova, J., Rasche, N., Dybkov, O., Kramer, K., Fabrizio, P., Urlaub, H., Luhrmann, R. and Pena, V. (2012) Crystal structure of Cwc2 reveals a novel architecture of a multipartite RNA-binding protein. EMBO J., 31, 2222-2234.
40. Wang, L. and Chance, M. (2011) Structural mass spectrometry of proteins using hydroxyl radical based protein footprinting. Anal. Chem., 83, 7234-7241.
41. Belon, C. and Frick, D. (2008) Monitoring helicase activity with molecular beacons. BioTechniques, 45, 433-440, 442.
42. Dosztanyi, Z., Csizmok, V., Tompa, P. and Simon, I. (2005) IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics, 21, 3433-3434.
43. Mezaros, B., Simon, I. and Dosztanyi, Z. (2009) Prediction of protein binding regions in disordered proteins. PLoS Comput. Biol., 5, e1000376.
44. Sharp, J.S., Becker, J.M. and Hettich, R.L. (2003) Protein surface mapping by chemical oxidation: Structural analysis by mass spectrometry. Anal. Biochem., 313, 216-225.
45. Rappsilber, J., Mann, M. and Ishihama, Y. (2007) Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protoc., 2, 1896-1906.
46. Kramer, K., Hummel, P., Hsiao, H., Luo, X., Wahl, M. and Urlaub, H. (2011) Mass-spectrometric analysis of proteins crosslinked to 4-thio-uracil-and 5-bromo-uracil-substituted RNA. Int. J. Mass Spectrom., 304, 184-194.
47. Schmidt, C. and Urlaub, H. (2009) iTRAQ-labeling of in-gel digested proteins for relative quantification. Methods Mol. Biol., 564, 207-226.
48. Cox, J. and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol., 26, 1367-1372.
49. Cox, J., Neuhauser, N., Michalski, A., Scheltema, R.A., Olsen, J.V. and Mann, M. (2011) Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res., 10, 1794-1805.
50. Charvatova, O., Foley, B.L., Bern, M.W., Sharp, J.S., Orlando, R. and Woods, R.J. (2008) Quantifying protein interface footprinting by hydroxyl radical oxidation and molecular dynamics simulation: application to galectin-1. J. Am. Soc. Mass Spectrom., 19, 1692-1705.
51. Sturm, M., Bertsch, A., Gropl, C., Hildebrandt, A., Hussong, R., Lange, E., Pfeifer, N., Schulz-Trieglaff, O., Zerck, A., Reinert, K. et al. (2008) OpenMS-an open-source software framework for mass spectrometry. BMC Bioinformatics, 9, 163.
52. Bertsch, A., Gropl, C., Reinert, K. and Kohlbacher, O. (2011) OpenMS and TOPP: open source software for LC-MS data analysis. Methods Mol. Biol., 696, 353-367.
53. Geer, L.Y., Markey, S.P., Kowalak, J.A., Wagner, L., Xu, M., Maynard, D.M., Yang, X., Shi, W. and Bryant, S.H. (2004) Open mass spectrometry search algorithm. J. Proteome Res., 3, 958-964.
54. Kessner, D., Chambers, M., Burke, R., Agus, D. and Mallick, P. (2008) ProteoWizard: open source software for rapid proteomics tools development. Bioinformatics, 24, 2534-2536.
55. Xu, H. and Freitas, M.A. (2009) MassMatrix: a database search program for rapid characterization of proteins and peptides from tandem mass spectrometry data. Proteomics, 9, 1548-1555.
56. Xu, H., Zhang, L. and Freitas, M.A. (2008) Identification and characterization of disulfide bonds in proteins and peptides from tandem MS data by use of the MassMatrix MS/MS search engine research articles. J. Proteome Res., 7, 138-144.
57. Luo, P. and Baldwin, R. (1997) Mechanism of helix induction by trifluoroethanol: a framework for extrapolating the helix-forming properties of peptides from trifluoroethanol/water mixtures back to water. Biochemistry, 36, 8413-8421.
58. Martin, A., Schneider, S. and Schwer, B. (2002) Prp43 is an essential RNA-dependent ATPase required for release of lariatintron from the spliceosome. J. Biol. Chem., 277, 17743-17750.
59. Chamieh, H., Ballut, L., Bonneau, F. and Le Hir, H. (2008) NMD factors UPF2 and UPF3 bridge UPF1 to the exon junction complex and stimulate its RNA helicase activity. Nat. Struct. Mol. Biol., 15, 85-93.
60. Clerici, M., Mourão, A., Gutsche, I., Gehring, N., Hentze, M., Kulozik, A., Kadlec, J., Sattler, M. and Cusack, S. (2009) Unusual bipartite mode of interaction between the nonsense-mediated decay factors, UPF1 and UPF2. EMBO J., 28, 2293-2306.
61. Chakrabarti, S., Jayachandran, U., Bonneau, F., Fiorini, F., Basquin, C., Domcke, S., Le Hir, H. and Conti, E. (2011) Molecular mechanisms for the RNA-dependent ATPase activity of Upf1 and its regulation by Upf2. Mol. Cell, 41, 693-703.
62. Oberer, M., Marintchev, A. and Wagner, G. (2005) Structural basis for the enhancement of eIF4A helicase activity by eIF4G. Genes Dev., 19, 2212-2223.
63. Schutz, P., Bumann, M., Oberholzer, A., Bieniossek, C., Trachsel, H., Altmann, M. and Baumann, U. (2008) Crystal structure of the yeast eIF4A-eIF4G complex: an RNA-helicase controlled by protein-protein interactions. Proc. Natl Acad. Sci. USA, 105, 9564-9569.
64. Weirich, C., Erzberger, J., Flick, J., Berger, J., Thorner, J. and Weis, K. (2006) Activation of the DExD/H-box protein Dbp5 by the nuclear-pore protein Gle1 and its coactivator InsP6 is required for mRNA export. Nat. Cell Biol., 8, 668-676.
65. Montpetit, B., Thomsen, N., Helmke, K., Seeliger, M., Berger, J. and Weis, K. (2011) A conserved mechanism of DEAD-box ATPase activation by nucleoporins and InsP6 in mRNA export. Nature, 472, 238-242.
66. Edwalds-Gilbert, G., Kim, D., Silverman, E. and Lin, R. (2004) Definition of a spliceosome interaction domain in yeast Prp2 ATPase. RNA, 10, 210-220.
67. Hotz, H. and Schwer, B. (1998) Mutational analysis of the yeast DEAH-box splicing factor Prp16. Genetics, 149, 807-815.
68. Schneider, S. and Schwer, B. (2001) Functional domains of the yeast splicing factor Prp22p. J. Biol. Chem., 276, 21184-21191.
69. Tanaka, N. and Schwer, B. (2005) Characterization of the NTPase, RNA-binding, and RNA helicase activities of the DEAH-box splicing factor Prp22. Biochemistry, 44, 9795-9803.
70. Tanaka, N. and Schwer, B. (2006) Mutations in PRP43 that uncouple RNA-dependent NTPase activity and pre-mRNA splicing function. Biochemistry, 45, 6510-6521.
71. Freal, K., Callebaut, I., Wecker, K., Prochnicka-Chalufour, A., Dendouga, N., Zinn-Justin, S., Delepierre, M., Tomavo, S. and Wolff, N. (2006) Structural and functional characterization of the TgDRE multidomain protein, a DNA repair enzyme from Toxoplasma gondii. Biochemistry, 45, 4867-4874.
72. Svec, M., Bauerova, H., Pichova, I., Konvalinka, J. and Strovsky, K. (2004) Proteinases of betaretroviruses bind singlestranded nucleic acids through a novel interaction module, the G-patch. FEBS Lett., 576, 271-276.
73. Lebaron, S., Papin, C., Capeyrou, R., Chen, Y., Froment, C., Monsarrat, B., Caizergues-Ferrer, M., Grigoriev, M. and Henry, Y. (2009) The ATPase and helicase activities of Prp43p are stimulated by the G-patch protein Pfa1p during yeast ribosome biogenesis. EMBO J., 28, 3808-3819.
74. Tsai, R., Fu, R., Yeh, F., Tseng, C., Lin, Y., Huang, Y. and Cheng, S. (2005) Spliceosome disassembly catalyzed by Prp43 and its associated components Ntr1 and Ntr2. Genes Dev., 19, 2991-3003.
75. Pandit, S., Lynn, B. and Rymond, B. (2006) Inhibition of a spliceosome turnover pathway suppresses splicing defects. Proc. Natl Acad. Sci. USA, 103, 13700-13705.
76. Behrens, M., He, Y., Oliveira, C., Andersen, G., Pedersen, J. and Nielsen, K. (2012) Structural Analysis of RNA Helicases with Small-Angle X-ray Scattering. Methods Enzymol., 511, 191-212.
77. Zhang, Y., Stec, B. and Godzik, A. (2007) Between order and disorder in protein structures: analysis of "dual personality" fragments in proteins. Structure, 15, 1141-1147.
78. Appleby, T., Anderson, R., Fedorova, O., Pyle, A., Wang, R., Liu, X., Brendza, K. and Somoza, J. (2011) Visualizing ATP-dependent RNA translocation by the NS3 helicase from HCV. J. Mol. Biol., 405, 1139-1153.