Splicing proofreading at 5′ splice sites by ATPase Prp28p

Nucleic Acids Research

Volumn 41, Issue 8, 2013, Pages 4660-4670

  Yang, Fei ^a   Wang, Xiu Ye ^a   Zhang, Zhi Min ^b   Pu, Jia ^a   Fan, Yu Jie ^a   Zhou, Jiahai ^b   Query, Charles C ^c   Xu, Yong Zhen ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^b SHANGHAI INSTITUTE OF ORGANIC CHEMISTRY   (China)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DOUBLE STRANDED RNA; PROTEIN PRP28; SMALL NUCLEAR RNA; UNCLASSIFIED DRUG;

ALLELE; ALTERNATIVE RNA SPLICING; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; GENE; GENE INTERACTION; GENE ISOLATION; GENE LOSS; GENETIC SCREENING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN RNA BINDING; PRP28 GENE; RNA STABILITY; SACCHAROMYCES CEREVISIAE; SPLICEOSOME;

ADENOSINE TRIPHOSPHATASES; ALLELES; ANIMALS; CELL LINE; DEAD-BOX RNA HELICASES; DROSOPHILA; MUTATION; RNA SPLICE SITES; RNA SPLICING; RNA, SMALL NUCLEAR; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84877265326     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt149     Document Type: Article

References (54)

1. Will, C.L. and Luhrmann, R. (2011) Spliceosome structure and function. Cold Spring Harb. Perspect. Biol., 3, a003707.
2. Wahl, M.C., Will, C.L. and Luhrmann, R. (2009) The spliceosome: design principles of a dynamic RNP machine. Cell, 136, 701-718.
3. Hoskins, A.A. and Moore, M.J. (2012) The spliceosome: a flexible, reversible macromolecular machine. Trends Biochem. Sci., 37, 179-188.
4. Staley, J.P. and Guthrie, C. (1998) Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell, 92, 315-326.
5. Schwer, B. (2001) A new twist on RNA helicases: DExH/D box proteins as RNPases. Nat. Struct. Biol., 8, 113-116.
6. Hahn, D. and Beggs, J.D. (2010) Brr2p RNA helicase with a split personality: insights into structure and function. Biochem. Soc. Trans., 38, 1105-1109.
7. Strauss, E.J. and Guthrie, C. (1994) PRP28, a 'DEAD-box' protein, is required for the first step of mRNA splicing in vitro. Nucleic Acids Res., 22, 3187-3193.
8. Staley, J.P. and Guthrie, C. (1999) An RNA switch at the 50 splice site requires ATP and the DEAD box protein Prp28p. Mol. Cell, 3, 55-64.
9. Maeder, C., Kutach, A.K. and Guthrie, C. (2009) ATP-dependent unwinding of U4/U6 snRNAs by the Brr2 helicase requires the C terminus of Prp8. Nat. Struct. Mol. Biol., 16, 42-48.
10. Hahn, D., Kudla, G., Tollervey, D. and Beggs, J.D. (2012) Brr2p-mediated conformational rearrangements in the spliceosome during activation and substrate repositioning. Genes Dev., 26, 2408-2421.
11. Mozaffari-Jovin, S., Santos, K.F., Hsiao, H.H., Will, C.L., Urlaub, H., Wahl, M.C. and Lü hrmann, R. (2012) The Prp8 RNase H-like domain inhibits Brr2-mediated U4/U6 snRNA unwinding by blocking Brr2 loading onto the U4 snRNA. Genes Dev., 26, 2422-2434.
12. Egecioglu, D.E. and Chanfreau, G. (2011) Proofreading and spellchecking: a two-tier strategy for pre-mRNA splicing quality control. RNA, 17, 383-389.
13. Smith, D.J., Query, C.C. and Konarska, M.M. (2008) "Nought may endure but mutability": spliceosome dynamics and the regulation of splicing. Mol. Cell, 30, 657-666.
14. Semlow, D.R. and Staley, J.P. (2012) Staying on message: ensuring fidelity in pre-mRNA splicing. Trends Biochem. Sci., 37, 263-273.
15. Query, C.C. and Konarska, M.M. (2004) Suppression of multiple substrate mutations by spliceosomal prp8 alleles suggests functional correlations with ribosomal ambiguity mutants. Mol. Cell, 14, 343-354.
16. Konarska, M.M., Vilardell, J. and Query, C.C. (2006) Repositioning of the reaction intermediate within the catalytic center of the spliceosome. Mol. Cell, 21, 543-553.
17. Liu, L., Query, C.C. and Konarska, M.M. (2007) Opposing classes of prp8 alleles modulate the transition between the catalytic steps of pre-mRNA splicing. Nat. Struct. Mol. Biol., 14, 519-526.
18. Query, C.C. and Konarska, M.M. (2012) CEF1/CDC5 alleles modulate transitions between catalytic conformations of the spliceosome. RNA, 18, 1001-1013.
19. Schwer, B. and Guthrie, C. (1991) PRP16 is an RNA-dependent ATPase that interacts transiently with the spliceosome. Nature, 349, 494-499.
20. Burgess, S., Couto, J.R. and Guthrie, C. (1990) A putative ATP binding protein influences the fidelity of branchpoint recognition in yeast splicing. Cell, 60, 705-717.
21. Burgess, S.M. 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.
22. Koodathingal, P., Novak, T., Piccirilli, J.A. and Staley, J.P. (2010) The DEAH box ATPases Prp16 and Prp43 cooperate to proofread 50 splice site cleavage during pre-mRNA splicing. Mol. Cell, 39, 385-395.
23. Tseng, C.K., Liu, H.L. and Cheng, S.C. (2011) DEAH-box ATPase Prp16 has dual roles in remodeling of the spliceosome in catalytic steps. RNA, 17, 145-154.
24. Mayas, R.M., Maita, H. and Staley, J.P. (2006) Exon ligation is proofread by the DExD/H-box ATPase Prp22p. Nat. Struct. Mol. Biol., 13, 482-490.
25. Perriman, R. and Ares, M. Jr (2010) Invariant U2 snRNA nucleotides form a stem loop to recognize the intron early in splicing. Mol. Cell, 38, 416-427.
26. Xu, Y.Z. and Query, C.C. (2007) Competition between the ATPase Prp5 and branch region-U2 snRNA pairing modulates the fidelity of spliceosome assembly. Mol. Cell, 28, 838-849.
27. Mayas, R.M., Maita, H., Semlow, D.R. and Staley, J.P. (2010) Spliceosome discards intermediates via the DEAH box ATPase Prp43p. Proc. Natl Acad. Sci. USA, 107, 10020-10025.
28. Tavanez, J.P., Madl, T., Kooshapur, H., Sattler, M. and Valcarcel, J. (2012) hnRNP A1 proofreads 30 splice site recognition by U2AF. Mol. Cell, 45, 314-329.
29. Soares, L.M., Zanier, K., Mackereth, C., Sattler, M. and Valcarcel, J. (2006) Intron removal requires proofreading of U2AF/30 splice site recognition by DEK. Science, 312, 1961-1965.
30. Tanner, N.K. and Linder, P. (2001) DExD/H box RNA helicases: from generic motors to specific dissociation functions. Mol. Cell, 8, 251-262.
31. Strauss, E.J. and Guthrie, C. (1991) A cold-sensitive mRNA splicing mutant is a member of the RNA helicase gene family. Genes Dev., 5, 629-641.
32. Murray, H.L. and Jarrell, K.A. (1999) Flipping the switch to an active spliceosome. Cell, 96, 599-602.
33. Chen, J.Y., Stands, L., Staley, J.P., Jackups, R.R. Jr, Latus, L.J. and Chang, T.H. (2001) Specific alterations of U1-C protein or U1 small nuclear RNA can eliminate the requirement of Prp28p, an essential DEAD box splicing factor. Mol. Cell, 7, 227-232.
34. Hage, R., Tung, L., Du, H., Stands, L., Rosbash, M. and Chang, T.H. (2009) A targeted bypass screen identifies Ynl187p, Prp42p, Snu71p, and Cbp80p for stable U1 snRNP/Pre-mRNA interaction. Mol. Cell Biol., 29, 3941-3952.
35. Du, H. and Rosbash, M. (2002) The U1 snRNP protein U1C recognizes the 50 splice site in the absence of base pairing. Nature, 419, 86-90.
36. Teigelkamp, S., Mundt, C., Achsel, T., Will, C.L. and Luhrmann, R. (1997) 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, 1313-1326.
37. Mathew, R., Hartmuth, K., Mohlmann, S., Urlaub, H., Ficner, R. and Luhrmann, R. (2008) Phosphorylation of human PRP28 by SRPK2 is required for integration of the U4/U6-U5 tri-snRNP into the spliceosome. Nat. Struct. Mol. Biol., 15, 435-443.
38. Ismaili, N., Sha, M., Gustafson, E.H. and Konarska, M.M. (2001) The 100-kda U5 snRNP protein (hPrp28p) contacts the 50 splice site through its ATPase site. RNA, 7, 182-193.
39. Wilson, D.S. and Keefe, A.D. (2001) Random mutagenesis by PCR. Curr. Protoc. Mol. Biol., Chapter 8, Unit 8.3.
40. Lesser, C.F. and Guthrie, C. (1993) Mutational analysis of pre-mRNA splicing in Saccharomyces cerevisiae using a sensitive new reporter gene, CUP1. Genetics, 133, 851-863.
41. Siatecka, M., Reyes, J.L. and Konarska, M.M. (1999) Functional interactions of Prp8 with both splice sites at the spliceosomal catalytic center. Genes Dev., 13, 1983-1993.
42. Xu, Y.Z., Newnham, C.M., Kameoka, S., Huang, T., Konarska, M.M. and Query, C.C. (2004) Prp5 bridges U1 and U2 snRNPs and enables stable U2 snRNP association with intron RNA. EMBO J., 23, 376-385.
43. Tanner, N.K., Cordin, O., Banroques, J., Doere, M. and Linder, P. (2003) The Q motif: a newly identified motif in DEAD box helicases may regulate ATP binding and hydrolysis. Mol. Cell, 11, 127-138.
44. Burgess, S.M. and Guthrie, C. (1993) Beat the clock: paradigms for NTPases in the maintenance of biological fidelity. Trends Biochem. Sci., 18, 381-384.
45. Alvarez, C.J., Romfo, C.M., Vanhoy, R.W., Porter, G.L. and Wise, J.A. (1996) Mutational analysis of U1 function in Schizosaccharomyces pombe: pre-mRNAs differ in the extent and nature of their requirements for this snRNA in vivo. RNA, 2, 404-418.
46. Seraphin, B. and Rosbash, M. (1989) Mutational analysis of the interactions between U1 small nuclear RNA and pre-mRNA of yeast. Gene, 82, 145-151.
47. Madhani, H.D., Bordonne, R. and Guthrie, C. (1990) Multiple roles for U6 snRNA in the splicing pathway. Genes Dev., 4, 2264-2277.
48. Kim, C.H. and Abelson, J. (1996) Site-specific crosslinks of yeast U6 snRNA to the pre-mRNA near the 50 splice site. RNA, 2, 995-1010.
49. Chapman, K.B. and Boeke, J.D. (1991) Isolation and characterization of the gene encoding yeast debranching enzyme. Cell, 65, 483-492.
50. Schwer, B. (2008) A conformational rearrangement in the spliceosome sets the stage for Prp22-dependent mRNA release. Mol. Cell, 30, 743-754.
51. Burge, C.B., Tuschl, T. and Sharp, P.A. (1999) Splicing of precursors to mRNAs by the spliceosomes. In: Gesteland, R.F., Cech, T.R. and Atkins, J.F. (eds), The RNA World, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 525-560.
52. Wolff, T., Menssen, R., Hammel, J. and Bindereif, A. (1994) Splicing function of mammalian U6 small nuclear RNA: conserved positions in central domain and helix I are essential during the first and second step of pre-mRNA splicing. Proc. Natl Acad. Sci. USA, 91, 903-907.
53. Lee, C., Jaladat, Y., Mohammadi, A., Sharifi, A., Geisler, S. and Valadkhan, S. (2010) Metal binding and substrate positioning by evolutionarily invariant U6 sequences in catalytically active protein-free snRNAs. RNA, 16, 2226-2238.
54. Luo, D., Wei, N., Doan, D.N., Paradkar, P.N., Chong, Y., Davidson, A.D., Kotaka, M., Lescar, J. and Vasudevan, S.G. (2010) Flexibility between the protease and helicase domains of the dengue virus NS3 protein conferred by the linker region and its functional implications. J. Biol. Chem., 285, 18817-18827.