Sequencing of lariat termini in S. cerevisiae reveals 5' splice sites, branch points, and novel splicing events

RNA

Volumn 22, Issue 2, 2016, Pages 237-253

  Qin, Daoming ^a   Huang, Lei ^a   Wlodaver, Alissa ^a   Andrade, Jorge ^a   Staley, Jonathan P ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Branch point; Lariat intron; Pre mRNA splicing; RNA seq; Splice site

Indexed keywords

ADENOSINE; MESSENGER RNA PRECURSOR; NUCLEOTIDE; RIBONUCLEASE; TRANSCRIPTOME; FUNGAL RNA; LARIAT DEBRANCHING ENZYME; RNA POLYMERASE; RNA PRECURSOR; RNA SPLICE SITE;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; CONSENSUS SEQUENCE; CONTROLLED STUDY; EXOSOME; GENE LIBRARY; GENE SEQUENCE; GENETIC ANALYSIS; INTRON; LARIAT INTRON TERMINUS SEQUENCING; MOLECULAR GENETICS; NONHUMAN; PRIORITY JOURNAL; RNA SEQUENCE; RNA SPLICING; SACCHAROMYCES CEREVISIAE; SENSITIVITY ANALYSIS; SPLICEOSOME; CHEMISTRY; CONFORMATION; FUNGAL GENOME; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; RNA SPLICE SITE;

BASE SEQUENCE; GENE EXPRESSION REGULATION, FUNGAL; GENOME, FUNGAL; INTRONS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; RNA NUCLEOTIDYLTRANSFERASES; RNA PRECURSORS; RNA SPLICE SITES; RNA SPLICING; RNA, FUNGAL; SACCHAROMYCES CEREVISIAE; SPLICEOSOMES;

EID: 84956833485     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.052829.115     Document Type: Article

References (79)

1. Alexander RC, Johnson AK, Thorpe JA, Gevedon T, Testa SM. 2003. Canonical nucleosides can be utilized by T4 DNA ligase as universal template bases at ligation junctions. Nucleic Acids Res 31: 3208-3216.
2. Awan AR, Manfredo A, Pleiss JA. 2013. Lariat sequencing in a unicellular yeast identifies regulated alternative splicing of exons that are evolutionarily conserved with humans. Proc Natl Acad Sci 110: 12762-12767.
3. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. 2009. MEME SUITE: Tools for motif discovery and searching. Nucleic Acids Res 37: W202-W208.
4. Barrett SP, Wang PL, Salzman J. 2015. Circular RNA biogenesis can proceed through an exon-containing lariat precursor. eLife 4: E07540.
5. Berglund JA, Chua K, Abovich N, Reed R, Rosbash M. 1997. The splicing factor BBP interacts specifically with the pre-mRNA branchpoint sequence UACUAAC. Cell 89: 781-787.
6. Bitton DA, Rallis C, Jeffares DC, Smith GC, Chen YY, Codlin S, Marguerat S, Bähler J. 2014. LaSSO, a strategy for genome-wide mapping of intronic lariats and branch points using RNA-seq. Genome Res 24: 1169-1179.
7. Bitton DA, Atkinson SR, Rallis C, Smith GC, Ellis DA, Chen Y, Malecki M, Codlin S, Cotobal C, Lemay J-F, et al. 2015. Widespread exon skipping triggers degradation by nuclear RNA surveillance in fission yeast. Genome Res 25: 884-896.
8. Bouck J, Fu XD, Skalka AM, Katz RA. 1995. Genetic selection for balanced retroviral splicing: Novel regulation involving the second step can be mediated by transitions in the polypyrimidine tract. Mol Cell Biol 15: 2663-2671.
9. Bousquet-Antonelli C, Presutti C, Tollervey D. 2000. Identification of a regulated pathway for nuclear pre-mRNA turnover. Cell 102: 765-775.
10. Burgess SM, 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.
11. Chapman KB, Boeke JD. 1991. Isolation and characterization of the gene encoding yeast debranching enzyme. Cell 65: 483-492.
12. 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.
13. Churchman LS, Weissman JS. 2011. Nascent transcript sequencing visualizes transcription at nucleotide resolution. Nature 469: 368-373.
14. Clark TA, Sugnet CW, Ares M Jr. 2002. Genomewide analysis of mRNA processing in yeast using splicing-specific microarrays. Science 296: 907-910.
15. Danin-Kreiselman M, Lee CY, Chanfreau G. 2003. RNAse III-mediated degradation of unspliced pre-mRNAs and lariat introns. Mol Cell 11: 1279-1289.
16. Davis CA, Grate L, Spingola M, Ares M Jr. 2000. Test of intron predictions reveals novel splice sites, alternatively spliced mRNAs and new introns in meiotically regulated genes of yeast. Nucleic Acids Res 28: 1700-1706.
17. Deutsch M, Long M. 1999. Intron-exon structures of eukaryotic model organisms. Nucleic Acids Res 27: 3219-3228.
18. Duff MO, Olson S, Wei X, Garrett SC, Osman A, Bolisetty M, Plocik A, Celniker SE, Graveley BR. 2015. Genome-wide identification of zero nucleotide recursive splicing in Drosophila. Nature 521: 376-379.
19. Egecioglu DE, Kawashima TR, Chanfreau GF. 2012. Quality control of MATa1 splicing and exon skipping by nuclear RNA degradation. Nucleic Acids Res 40: 1787-1796.
20. Fullwood MJ, Wei CL, Liu ET, Ruan Y. 2009. Next-generation DNA sequencing of paired-end tags (PET) for transcriptome and genome analyses. Genome Res 19: 521-532.
21. Gao K, Masuda A, Matsuura T, Ohno K. 2008. Human branch point consensus sequence is yUnAy. Nucleic Acids Res 36: 2257-2267.
22. Garrey SM, Katolik A, Prekeris M, Li X, York K, Bernards S, Fields S, Zhao R, Damha MJ, Hesselberth JR. 2014. A homolog of lariatdebranching enzyme modulates turnover of branched RNA. RNA 20: 1337-1348.
23. Girard C, Will CL, Peng J, Makarov EM, Kastner B, Lemm I, Urlaub H, Hartmuth K, Lührmann R. 2012. Post-Transcriptional spliceosomes are retained in nuclear speckles until splicing completion. Nat Commun 3: 994.
24. Harigaya Y, Parker R. 2012. Global analysis of mRNA decay intermediates in Saccharomyces cerevisiae. Proc Natl Acad Sci 109: 11764-11769.
25. Hatton AR, Subramaniam V, Lopez AJ. 1998. Generation of alternative Ultrabithorax isoforms and stepwise removal of a large intron by resplicing at exon-exon junctions. Mol Cell 2: 787-796.
26. Hesselberth JR. 2014. Lives that introns lead after splicing. Wiley Interdiscip Rev RNA 4: 677-691.
27. Hon CC, Weber C, Sismeiro O, Proux C, Koutero M, Deloger M, Das S, Agrahari M, Dillies MA, Jagla B, et al. 2013. Quantification of stochastic noise of splicing and polyadenylation in Entamoeba histolytica. Nucleic Acids Res 41: 1936-1952.
28. Houseley J, LaCava J, Tollervey D. 2006. RNA-quality control by the exosome. Nat Rev Mol Cell Biol 7: 529-539.
29. Jeck WR, Sorrentino JA, Wang K, Slevin MK, Burd CE, Liu J, Marzluff WF, Sharpless NE. 2013. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 19: 141-157.
30. Jia H, Wang X, Liu F, Guenther U-P, Srinivasan S, Anderson JT, Jankowsky E. 2011. The RNA helicase Mtr4p modulates polyadenylation in the TRAMP complex. Cell 145: 890-901.
31. Juneau K, Palm C, Miranda M, Davis RW. 2007. High-density yeast-Tiling array reveals previously undiscovered introns and extensive regulation of meiotic splicing. Proc Natl Acad Sci 104: 1522-1527.
32. Kalsotra A, Cooper TA. 2011. Functional consequences of developmentally regulated alternative splicing. Nat Rev Genet 12: 715-729.
33. Kawashima T, Douglass S, Gabunilas J, Pellegrini M, Chanfreau GF. 2014. Widespread use of non-productive alternative splice sites in Saccharomyces cerevisiae. PLoS Genet 10: E1004249.
34. Kellis M, Patterson N, Endrizzi M, Birren B, Lander ES. 2003. Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 423: 241-254.
35. 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.
36. LaCava J, Houseley J, Saveanu C, Petfalski E, Thompson E, Jacquier A, Tollervey D. 2005. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121: 713-724.
37. Lallena MJ, Chalmers KJ, Llamazares S, Lamond AI, Valcárcel J. 2002. Splicing regulation at the second catalytic step by Sex-lethal involves 3' splice site recognition by SPF45. Cell 109: 285-296.
38. Lebreton A, Tomecki R, Dziembowski A, Séraphin B. 2008. Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature 456: 993-996.
39. 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.
40. Lopez PJ, Séraphin B. 2000. Uncoupling yeast intron recognition from transcription with recursive splicing. EMBO Rep 1: 334-339.
41. Martin JA, Wang Z. 2011. Next-generation transcriptome assembly. Nat Rev Genet 12: 671-682.
42. 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.
43. McGlincy NJ, Smith CW. 2008. Alternative splicing resulting in nonsense-mediated mRNA decay: What is the meaning of nonsense? Trends Biochem Sci 33: 385-393.
44. Melamud E, Moult J. 2009. Stochastic noise in splicing machinery. Nucleic Acids Res 37: 4873-4886.
45. Mercer TR, Clark MB, Andersen SB, Brunck ME, Haerty W, Crawford J, Taft RJ, Nielsen LK, Dinger ME, Mattick JS. 2015. Genome-wide discovery of human splicing branchpoints. Genome Res 25: 290-303.
46. Miura F, Kawaguchi N, Sese J, Toyoda A, Hattori M, Morishita S, Ito T. 2006. A large-scale full-length cDNA analysis to explore the budding yeast transcriptome. Proc Natl Acad Sci 103: 17846-17851.
47. Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, Snyder M. 2008. The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320: 1344-1349.
48. Nilsen TW, Graveley BR. 2010. Expansion of the eukaryotic proteome by alternative splicing. Nature 463: 457-463.
49. Nojima T, Gomes T, Grosso ARF, Kimura H, Dye MJ, Dhir S, Carmo-Fonseca M, Proudfoot NJ. 2015. Mammalian NET-seq reveals genome-wide nascent transcription coupled to RNA processing. Cell 161: 526-540.
50. Ooi SL, Samarsky DA, Fournier MJ, Boeke JD. 1998. Intronic snoRNA biosynthesis in Saccharomyces cerevisiae depends on the lariatdebranching enzyme: Intron length effects and activity of a precursor snoRNA. RNA 4: 1096-1110.
51. Pelechano V, Wei W, Steinmetz LM. 2013. Extensive transcriptional heterogeneity revealed by isoform profiling. Nature 497: 127-131.
52. Pickrell JK, Pai AA, Gilad Y, Pritchard JK. 2010. Noisy splicing drives mRNA isoform diversity in human cells. PLoS Genet 6: E1001236.
53. Pleiss JA, Whitworth GB, Bergkessel M, Guthrie C. 2007a. Rapid, transcript-specific changes in splicing in response to environmental stress. Mol Cell 27: 928-937.
54. Pleiss JA, Whitworth GB, Bergkessel M, Guthrie C. 2007b. Transcript specificity in yeast pre-mRNA splicing revealed by mutations in core spliceosomal components. PLoS Biol 5: E90.
55. Roy SW, Gilbert W. 2006. The evolution of spliceosomal introns: Patterns, puzzles and progress. Nat Rev Genet 7: 211-221.
56. San Paolo S, Vanacova S, Schenk L, Scherrer T, Blank D, Keller W, Gerber AP. 2009. Distinct roles of non-canonical poly(A) polymerases in RNA metabolism. PLoS Genet 5: E1000555.
57. Sayani S, Janis M, Lee CY, Toesca I, Chanfreau GF. 2008. Widespread impact of nonsense-mediated mRNA decay on the yeast intronome. Mol Cell 31: 360-370.
58. Schneider C, Kudla G, Wlotzka W, Tuck A, Tollervey D. 2012. Transcriptome-wide analysis of exosome targets. Mol Cell 48: 422-433.
59. Schwer B, Guthrie C. 1991. PRP16 is an RNA-dependent ATPase that interacts transiently with the spliceosome. Nature 349: 494-499.
60. Shiroguchi K, Jia TZ, Sims PA, Xie XS. 2012. Digital RNA sequencing minimizes sequence-dependent bias and amplification noise with optimized single-molecule barcodes. Proc Natl Acad Sci 109: 1347-1352.
61. Sibley CR, Emmett W, Blazquez L, Faro A, Haberman N, Briese M, Trabzuni D, Ryten M, Weale ME, Hardy J, et al. 2015. Recursive splicing in long vertebrate genes. Nature 521: 371-375.
62. Small EC, Leggett SR, Winans AA, Staley JP. 2006. The EF-G-like GTPase Snu114p regulates spliceosome dynamics mediated by Brr2p, a DExD/H box ATPase. Mol Cell 23: 389-399.
63. Spieth J, Brooke G, Kuersten S, Lea K, Blumenthal T. 1993. Operons in C. elegans: Polycistronic mRNA precursors are processed by trans-splicing of SL2 to downstream coding regions. Cell 73: 521-532.
64. Spingola M, Grate L, Haussler D, Ares M Jr. 1999. Genome-wide bioinformatic and molecular analysis of introns in Saccharomyces cerevisiae. RNA 5: 221-234.
65. Staley JP, Guthrie C. 1998. Mechanical devices of the spliceosome: Motors, clocks, springs, and things. Cell 92: 315-326.
66. Stepankiw N, Raghavan M, Fogarty EA, Grimson A, Pleiss JA. 2015. Widespread alternative and aberrant splicing revealed by lariat sequencing. Nucleic Acids Res 43: 8488-8501.
67. Stevens SW, Abelson J. 2002. Yeast pre-mRNA splicing: Methods, mechanisms, and machinery. Methods Enzymol 351: 200-220.
68. Suzuki H, Zuo Y, Wang J, Zhang MQ, Malhotra A, Mayeda A. 2006. Characterization of RNase R-digested cellular RNA source that consists of lariat and circular RNAs from pre-mRNA splicing. Nucleic Acids Res 34: E63.
69. Taggart AJ, DeSimone AM, Shih JS, Filloux ME, Fairbrother WG. 2012. Large-scale mapping of branchpoints in human pre-mRNA transcripts in vivo. Nat Struct Mol Biol 19: 719-721.
70. Talhouarne GJ, Gall JG. 2014. Lariat intronic RNAs in the cytoplasm of Xenopus tropicalis oocytes. RNA 20: 1476-1487.
71. Volanakis A, Passoni M, Hector RD, Shah S, Kilchert C, Granneman S, Vasiljeva L. 2013. Spliceosome-mediated decay (SMD) regulates expression of nonintronic genes in budding yeast. Genes Dev 27: 2025-2038.
72. Wahl MC, Will CL, Lührmann R. 2009. The spliceosome: Design principles of a dynamic RNP machine. Cell 136: 701-718.
73. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB. 2008. Alternative isoform regulation in human tissue transcriptomes. Nature 456: 470-476.
74. Windhager L, Bonfert T, Burger K, Ruzsics Z, Krebs S, Kaufmann S, Malterer G, L'Hernault A, Schilhabel M, Schreiber S, et al. 2012. Ultrashort and progressive 4sU-Tagging reveals key characteristics of RNAprocessing at nucleotide resolution. Genome Res 22: 2031-2042.
75. Wlotzka W, Kudla G, Granneman S, Tollervey D. 2011. The nuclear RNA polymerase II surveillance system targets polymerase III transcripts. EMBO J 30: 1790-1803.
76. Yassour M, Kaplan T, Fraser HB, Levin JZ, Pfiffner J, Adiconis X, Schroth G, Luo S, Khrebtukova I, Gnirke A, et al. 2009. Ab initio construction of a eukaryotic transcriptome by massively parallel mRNA sequencing. Proc Natl Acad Sci 106: 3264-3269.
77. Zhang Z, Hesselberth JR, Fields S. 2007. Genome-wide identification of spliced introns using a tiling microarray. Genome Res 17: 503-509.
78. Zhang Y, Zhang XO, Chen T, Xiang JF, Yin QF, Xing YH, Zhu S, Yang L, Chen LL. 2013. Circular intronic long noncoding RNAs. Mol Cell 51: 792-806.
79. Zhuang F, Fuchs RT, Sun Z, Zheng Y, Robb GB. 2012. Structural bias in T4 RNA ligase-mediated 3'-Adapter ligation. Nucleic Acids Res 40: E54.