U2 snRNA is inducibly pseudouridylated at novel sites by Pus7p and snR81 RNP

EMBO Journal

Volumn 30, Issue 1, 2011, Pages 79-89

  Wu, Guowei ^a   Xiao, Mu ^a   Yang, Chunxing ^a   Yu, Yi Tao ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

inducible RNA modification; pseudouridylation; Pus7; SnR81 RNP; U2 snRNA

Indexed keywords

FUNGAL RNA; POLYPEPTIDE PSEUDOURIDYLASE; PUS7P PROTEIN; RIBONUCLEOPROTEIN; RIBOSOME RNA; RNA 25S; SMALL NUCLEAR RNA; SMALL NUCLEAR RNA 81; TRANSFER RNA; U2 SMALL NUCLEAR RNA; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CONTROLLED STUDY; DNA MODIFICATION; GENE INDUCTION; HEAT SHOCK; NONHUMAN; NUTRIENT SUPPLY; PRIORITY JOURNAL; PSEUDOURIDYLATION; RNA ISOLATION; RNA SEQUENCE; RNA SPLICING; SACCHAROMYCES CEREVISIAE; SITE DIRECTED MUTAGENESIS;

BASE SEQUENCE; HOT TEMPERATURE; MOLECULAR SEQUENCE DATA; PSEUDOURIDINE; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA PRECURSORS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA SPLICING; RNA, FUNGAL; RNA, SMALL NUCLEAR; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 78650905534     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.316     Document Type: Article

References (42)

1. Alexandrov A, Chernyakov I, Gu W, Hiley SL, Hughes TR, Grayhack EJ, Phizicky EM (2006) Rapid tRNA decay can result from lack of nonessential modifications. Mol Cell 21 : 87-96
2. Bakin A, Ofengand J (1993) Four newly located pseudouridylate residues in Escherichia coli 23S ribosomal RNA are all at the peptidyltransferase center: analysis by the application of a new sequencing technique. Biochemistry 32: 9754-9762
3. Behm-Ansmant I, Urban A, Ma X, Yu YT, Motorin Y, Branlant C (2003) The Saccharomyces cerevisiae U2 snRNA:pseudouridine-synthase Pus7p is a novel multisite-multisubstrate RNA:Psi-synthase also acting on tRNAs. RNA 9: 1371-1382
4. Bjork GR (1995) Biosynthesis and function of modified nucleotides. In tRNA: Structure, Biosynthesis, and Function, Soll D, RajBhandary U (eds) pp 165-205. Washington, DC: ASM Press
5. Charette M, Gray MW (2000) Pseudouridine in RNA: what, where, how, and why. IUBMB Life 49: 341-351
6. Dai Q, Fong R, Saikia M, Stephenson D, Yu YT, Pan T, Piccirilli JA (2007) Identification of recognition residues for ligation-based detection and quantitation of pseudouridine and N6-methylade-nosine. Nucleic Acids Res 35: 6322-6329
7. 0 end of the human U2 snRNA are required for early spliceosome (E complex) formation in vitro. RNA 10: 1925-1933
8. Ganot P, Bortolin ML, Kiss T (1997) Site-specific pseudouridine formation in preribosomal RNA is guided by small nucleolar RNAs. Cell 89: 799-809
9. Gray JV, Petsko GA, Johnston GC, Ringe D, Singer RA, Werner-Washburne M (2004) 'Sleeping beauty': quiescence in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 68: 187-206
10. Grosjean H (2009) Nucleic acids are not boring long polymers of only four types of nucleotides: a guide tour. In DNA and RNA Modification Enzymes: Structure, Mechanism, Function and Evolution, Grosjean H (ed) pp 1-18. Austin, Texas: Landes Bioscience
11. Herman PK (2002) Stationary phase in yeast. Curr Opin Microbiol 5: 602-607
12. Hilliker AK, Mefford MA, Staley JP (2007) U2 toggles iteratively between the stem IIa and stem IIc conformations to promote pre-mRNA splicing. Genes Dev 21: 821-834
13. Jady BE, Darzacq X, Tucker KE, Matera AG, Bertrand E, Kiss T (2003) Modification of Sm small nuclear RNAs occurs in the nucleoplasmic Cajal body following import from the cytoplasm. EMBO J 22: 1878-1888
14. Karijolich J, Huang C, Yu YT (2009) Spliceosomal snRNA pseudouridylation. In DNA and RNA Modification Enzymes: Structure, Mechanism, Function and Evolution, Grosjean H (ed) pp 461-474. Austin, Texas: Landes Bioscience
15. King TH, Liu B, McCully RR, Fournier MJ (2003) Ribosome structure and activity are altered in cells lacking snoRNPs that form pseudouridines in the peptidyl transferase center. Mol Cell 11 : 425-435
16. Kolev NG, Steitz JA (2006) In vivo assembly of functional U7 snRNP requires RNA backbone flexibility within the Sm-binding site. Nat Struct Mol Biol 13: 347-353
17. Lesser CF, Guthrie C (1993) Mutational analysis of pre-mRNA splicing in Saccharomyces cerevisiae using a sensitive new reporter gene, CUP1. Genetics 133: 851-863
18. Liang XH, Liu Q, Fournier MJ (2007) rRNA modifications in an intersubunit bridge of the ribosome strongly affect both ribosome biogenesis and activity. Mol Cell 28: 965-977
19. Ma X, Yang C, Alexandrov A, Grayhack EJ, Behm-Ansmant I, Yu YT (2005) Pseudouridylation of yeast U2 snRNA is catalyzed by either an RNA-guided or RNA-independent mechanism. EMBO J 24: 2403-2413
20. Ma X, Zhao X, Yu YT (2003) Pseudouridylation (Psi) of U2 snRNA in S. cerevisiae is catalyzed by an RNA-independent mechanism. EMBO J 22: 1889-1897
21. Madhani HD, 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
22. Massenet S, Motorin Y, Lafontaine DL, Hurt EC, Grosjean H, Branlant C (1999) Pseudouridine mapping in the Saccharomyces cerevisiae spliceosomal U small nuclear RNAs (snRNAs) reveals that pseudouridine synthase pus1p exhibits a dual substrate specificity for U2 snRNA and tRNA. Mol Cell Biol 19: 2142-2154
23. Massenet S, Mougin A, Branlant C (1998) Posttranscriptional modifications in the U small nuclear RNAs. In Modification and Editing of RNA, Grosjean H (ed) pp 201-228. Washington, DC: ASM Press
24. Newby MI, Greenbaum NL (2002a) Investigation of Overhauser effects between pseudouridine and water protons in RNA helices. Proc Natl Acad Sci USA 99: 12697-12702
25. Newby MI, Greenbaum NL (2002b) Sculpting of the spliceosomal branch site recognition motif by a conserved pseudouridine. Nat Struct Biol 9: 958-965
26. Ni J, Tien AL, Fournier MJ (1997) Small nucleolar RNAs direct site-specific synthesis of pseudouridine in ribosomal RNA. Cell 89: 565-573
27. Ofengand J, Fournier M (1998) The pseudouridine residues of rRNA: number, location, biosynthesis, and function. In Modification and Editing of RNA, Grosjean H (ed) pp 229-253. Washington, DC: ASM Press
28. Perriman RJ, Ares Jr M (2007) Rearrangement of competing U2 RNA helices within the spliceosome promotes multiple steps in splicing. Genes Dev 21: 811-820
29. Piekna-Przybylska D, Przybylski P, Baudin-Baillieu A, Rousset JP, Fournier MJ (2008) Ribosome performance is enhanced by a rich cluster of pseudouridines in the A-site finger region of the large subunit. J Biol Chem 283: 26026-26036
30. Reddy R, Busch H (1988) Small nuclear RNAs: RNA sequences, structure, and modifications. In Structure and Function of Major and Minor Small Nuclear Ribonucleoprotein Particles, Birnsteil ML (ed), pp 1-37. Heidelberg: Springer-Verlag Press
31. Siatecka M, Reyes JL, Konarska MM (1999) Functional interactions of Prp8 with both splice sites at the spliceosomal catalytic center. Genes Dev 13: 1983-1993
32. Urban A, Behm-Ansmant I, Branlant C, Motorin Y (2009) RNA sequence and two-dimensional structure features required for efficient substrate modification by the Saccharomyces cerevisiae RNA:{Psi}-synthase Pus7p. J Biol Chem 284: 5845-5858
33. Xiao M, Yang C, Schattner P, Yu YT (2009) Functionality and substrate specificity of human box H/ACA guide RNAs. RNA 15: 176-186
34. Yang C, McPheeters DS, Yu YT (2005) Psi35 in the branch site recognition region of U2 small nuclear RNA is important for pre-mRNA splicing in Saccharomyces cerevisiae. J Biol Chem 280: 6655-6662
35. Yu YT, Shu MD, Narayanan A, Terns RM, Terns MP, Steitz JA (2001) Internal modification of U2 small nuclear (sn)RNA occurs in nucleoli of Xenopus oocytes. J Cell Biol 152: 1279-1288
36. 0-O-methylation in RNA molecules. RNA 3: 324-331
37. Yu YT, Shu MD, Steitz JA (1998) Modifications of U2 snRNA are required for snRNP assembly and pre-mRNA splicing. EMBO J 17: 5783-5795
38. Yu YT, Terns RM, Terns MP (2005) Mechanisms and functions of RNA-guided RNA modification. In Topics in Current Genetics, Grosjean H (ed) Vol 12, pp 223-262. New York: Springer-Verlag
39. Zebarjadian Y, King T, Fournier MJ, Clarke L, Carbon J (1999) Point mutations in yeast CBF5 can abolish in vivo pseudouridylation of rRNA. Mol Cell Biol 19: 7461-7472
40. Zhao X, Yu YT (2004a) Detection and quantitation of RNA base modifications. RNA 10: 996-1002
41. Zhao X, Yu YT (2004b) Pseudouridines in and near the branch site recognition region of U2 snRNA are required for snRNP biogenesis and pre-mRNA splicing in Xenopus oocytes. RNA 10: 681-690
42. Zhao X, Yu YT (2007) Incorporation of 5-fluorouracil into U2 snRNA blocks pseudouridylation and pre-mRNA splicing in vivo. Nucleic Acids Res 35: 550-558