A homolog of lariat-debranching enzyme modulates turnover of branched RNA

RNA

Volumn 20, Issue 8, 2014, Pages 1337-1348

  Garrey, Stephen M ^a   Katolik, Adam ^b   Prekeris, Mantas ^a   Li, Xueni ^a   York, Kerri ^a   Bernards, Sarah ^b   Fields, Stanley ^b,c   Zhao, Rui ^a   Damha, Masad J ^b   Hesselberth, Jay R ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Branched RNA; Dbr1; Nineteen complex; Splicing

Indexed keywords

DBR1 PROTEIN; FUNGAL PROTEIN; RNA; SMALL NUCLEAR RNA; UNCLASSIFIED DRUG;

ARTICLE; IN VITRO STUDY; INTRON; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; RNA SPLICING; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; SPLICEOSOME;

BRANCHED RNA; DBR1; NINETEEN COMPLEX; SPLICING;

AMINO ACID SEQUENCE; CATALYSIS; INTRONS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; RNA NUCLEOTIDYLTRANSFERASES; RNA PRECURSORS; RNA SPLICING; RNA, FUNGAL; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; SPLICEOSOMES;

EID: 84904513583     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.044602.114     Document Type: Article

References (49)

1. Alberti S, Gitler AD, Lindquist S. 2007. A suite of Gateway cloning vectors for high-throughput genetic analysis in Saccharomyces cerevisiae. Yeast 24: 913-919. (Pubitemid 47611130)
2. Arenas J, Hurwitz J. 1987. Purification of a RNA debranching activity from HeLa cells. J Biol Chem 262: 4274-4279.
3. Barrett T, Troup DB, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, Marshall KA, Phillippy KH, Sherman PM, et al. 2010. NCBI GEO: archive for functional genomics data sets: 10 years on. Nucleic Acids Res 39: D1005-D1010.
4. Braich RS, Damha MJ. 1997. Regiospecific solid-phase synthesis of branched oligonucleotides: effect of vicinal 2′,5′- (or 2′,3′-) and 3′,5′-phosphodiester linkages on the formation of hairpin DNA. Bioconjug Chem 8: 370-377. (Pubitemid 27236502)
5. Chang KJ, Chen HC, Cheng SC. 2009. Ntc90 is required for recruiting first step factor Yju2 but not for spliceosome activation. RNA 15: 1729-1739.
6. Chen W, Shulha HP, Ashar-Patel A, Yan J, Green KM, Query CC, Rhind N, Weng Z, Moore MJ. 2014. Endogenous U2•U5•U6 snRNA complexes in S. pombe are intron lariat spliceosomes. RNA 20: 308-320.
7. Damha MJ, Braich RS. 1998. Synthesis of a branched DNA/RNA chimera similar to the msDNA molecule of Myxococcus xanthus. Tetrahedron Lett 39: 3907-3910. (Pubitemid 28228611)
8. Dix I, Russell C, Yehuda SB, Kupiec M, Beggs JD. 1999. The identification and characterization of a novel splicing protein, Isy1p, of Saccharomyces cerevisiae. RNA 5: 360-368. (Pubitemid 29124996)
9. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, et al. 2009. The Pfam protein families database. Nucleic Acids Res 38: D211-D222.
10. Finn RD, Clements J, Eddy SR. 2011. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39: W29-W37.
11. Fourmann J-B, Schmitzová J, Christian H, Urlaub H, Ficner R, Boon KL, Fabrizio P, 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.
12. Gavin A-C, Aloy P, Grandi P, Krause R, Boesche M, Marzioch M, Rau C, Jensen LJ, Bastuck S, Dümpelfeld B, et al. 2006. Proteome survey reveals modularity of the yeast cell machinery. Nature 440: 631-636.
13. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, et al. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
14. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O'Shea EK, Weissman JS. 2003. Global analysis of protein expression in yeast. Nature 425: 737-741. (Pubitemid 37314318)
15. Grainger RJ, Beggs JD. 2005. Prp8 protein: at the heart of the spliceosome. RNA 11: 533-557. (Pubitemid 40594322)
16. Guthrie C, Fink GR. 2002. Guide to yeast genetics and molecular and cell biology, Vol. 351. Academic Press, San Diego, CA.
17. Hazbun TR, Malmström L, Anderson S, Graczyk BJ, Fox B, Riffle M, Sundin BA, Aranda JD, McDonald WH, Chiu C-H, et al. 2003. Assigning function to yeast proteins by integration of technologies. Mol Cell 12: 1353-1365. (Pubitemid 38037006)
18. Hesselberth JR. 2013. Lives that introns lead after splicing. WIREs RNA 4: 677-691.
19. Hiley SL, Babak T, Hughes TR. 2005. Global analysis of yeast RNA processing identifies new targets of RNase III and uncovers a link between tRNA 5′ end processing and tRNA splicing. Nucleic Acids Res 33: 3048-3056. (Pubitemid 41511242)
20. Hilleren PJ, Parker R. 2003. Cytoplasmic degradation of splice-defective pre-mRNAs and intermediates. Mol Cell 12: 1453-1465. (Pubitemid 38037014)
21. Hu Y, Rolfs A, Bhullar B, Murthy TVS, Zhu C, Berger MF, Camargo AA, Kelley F, McCarron S, Jepson D, et al. 2007. Approaching a complete repository of sequence-verified protein-encoding clones for Saccharomyces cerevisiae. Genome Res 17: 536-543. (Pubitemid 46556458)
22. Jacquier A, Rosbash M. 1986. RNA splicing and intron turnover are greatly diminished by a mutant yeast branch point. Proc Natl Acad Sci 83: 5835-5839. (Pubitemid 16000607)
23. Kataoka N, Dobashi I, Hagiwara M, Ohno M. 2013. hDbr1 is a nucleo-cytoplasmic shuttling protein with a protein phosphatase-like motif essential for debranching activity. Sci Rep 3: 1090.
24. Katolik A, Johnsson R, Montemayor E, Lackey JG, Hart PJ, Damha MJ. 2014. Regiospecific solid-phase synthesis of branched oligoribonucleotides that mimic intronic lariat RNA intermediates. J Org Chem 79: 963-975.
25. Khalid MF, Damha MJ, Shuman S, Schwer B. 2005. Structure-function analysis of yeast RNA debranching enzyme (Dbr1), a manganese-dependent phosphodiesterase. Nucleic Acids Res 33: 6349-6360. (Pubitemid 41742572)
26. Krämer A, Keller W. 1985. Purification of a protein required for the splicing of pre-mRNA and its separation from the lariat debranching enzyme. EMBO J 4: 3571-3581.
27. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357-359.
28. Li X, Zhang W, Xu T, Ramsey J, Zhang L, Hill R, Hansen KC, Hesselberth JR, Zhao R. 2013. Comprehensive in vivo RNA-binding site analyses reveal a role of Prp8 in spliceosomal assembly. Nucleic Acids Res 41: 3805-3818.
29. Libri D, Lescure A, Rosbash M. 2000. Splicing enhancement in the yeast rp51b intron. RNA 6: 352-368. (Pubitemid 30161280)
30. Liu L, Query CC, Konarska MM. 2007. Opposing classes of prp8 alleles modulate the transition between the catalytic steps of pre-mRNA splicing. Nat Struct Mol Biol 14: 519-526. (Pubitemid 46871804)
31. Martin A, Schneider S, Schwer B. 2002. Prp43 is an essential RNA-dependent ATPase required for release of lariat-intron from the spliceosome. J Biol Chem 277: 17743-17750. (Pubitemid 34967580)
32. Mata J, Lyne R, Burns G, Bähler J. 2002. The transcriptional program of meiosis and sporulation in fission yeast. Nat Genet 32: 143-147. (Pubitemid 34977209)
33. Mayas RM, Maita H, Staley JP. 2006. Exon ligation is proofread by the DExD/H-box ATPase Prp22p. Nat Struct Mol Biol 13: 482-490. (Pubitemid 43848902)
34. Mayas RM, Maita H, Semlow DR, Staley JP. 2010. Spliceosome discards intermediates via the DEAH box ATPase Prp43p. Proc Natl Acad Sci 107: 10020-10025.
35. Moqtaderi Z, Struhl K. 2008. Expanding the repertoire of plasmids for PCR-mediated epitope tagging in yeast. Yeast 25: 287-292. (Pubitemid 351577730)
36. Nam K, Hudson RH, Chapman KB, Ganeshan K, Damha MJ, Boeke JD. 1994. Yeast lariat debranching enzyme. Substrate and sequence specificity. J Biol Chem 269: 20613-20621.
37. Ohi MD, Link AJ, Ren L, Jennings JL, McDonald WH, Gould KL. 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. (Pubitemid 34224610)
38. Rappsilber J, Ryder U, Lamond AI, Mann M. 2002. Large-scale proteomic analysis of the human spliceosome. Genome Res 12: 1231-1245. (Pubitemid 41264425)
39. Ren L, McLean JR, Hazbun TR, Fields S, Vander Kooi C, Ohi MD, Gould KL. 2011. Systematic two-hybrid and comparative proteomic analyses reveal novel yeast pre-mRNA splicing factors connected to Prp19. PLoS One 6: e16719.
40. Ruby JG, Jan CH, Bartel DP. 2007. Intronic microRNA precursors that bypass Drosha processing. Nature 448: 83-86. (Pubitemid 47037009)
41. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, Rosenbloom K, Clawson H, Spieth J, Hillier LW, Richards S, et al. 2005. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15: 1034-1050. (Pubitemid 41126859)
42. Stark C, Su T-C, Breitkreutz A, Lourenco P, Dahabieh M, Breitkreutz B-J, Tyers M, Sadowski I. 2010. PhosphoGRID: a database of experimentally verified in vivo protein phosphorylation sites from the budding yeast Saccharomyces cerevisiae. Database (Oxford) 2010: bap026.
43. Stevens SW, Abelson J. 2002. Yeast pre-mRNA splicing: methods, mechanisms, and machinery. Methods Enzymol 351: 200-220. (Pubitemid 34614990)
44. Tanaka N, Aronova A, Schwer B. 2007. Ntr1 activates the Prp43 helicase to trigger release of lariat-intron from the spliceosome. Genes Dev 21: 2312-2325. (Pubitemid 47443337)
45. Tsai R-T, Tseng C-K, Lee P-J, Chen H-C, Fu R-H, Chang K-J, Yeh F-L, Cheng S-C. 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. (Pubitemid 350234220)
46. Vijayraghavan U, Parker R, Tamm J, Iimura Y, Rossi J, Abelson J, Guthrie C. 1986. Mutations in conserved intron sequences affect multiple steps in the yeast splicing pathway, particularly assembly of the spliceosome. EMBO J 5: 1683-1695.
47. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ. 2009. Jalview version 2: a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191.
48. Yoshimoto R, Kataoka N, Okawa K, Ohno M. 2009. Isolation and characterization of post-splicing lariat-intron complexes. Nucleic Acids Res 37: 891-902.
49. Zhang C, Darnell RB. 2011. Mapping in vivo protein-RNA interactions at single-nucleotide resolution from HITS-CLIP data. Nat Biotechnol 29: 607-614.