RNA structure replaces the need for U2AF2 in splicing

Genome Research

Volumn 26, Issue 1, 2016, Pages 12-23

  Lin, Chien Ling ^a   Taggart, Allison J ^a   Lim, Kian Huat ^a   Cygan, Kamil J ^a,b   Ferraris, Luciana ^a   Creton, Robbert ^a   Huang, Yen Tsung ^b   Fairbrother, William G ^a,b  

^a BROWN UNIVERSITY   (United States)

^b BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; COMPLEMENTARY DNA; RNA; U2AF2 PROTEIN; UNCLASSIFIED DRUG; NUCLEAR PROTEIN; RIBONUCLEOPROTEIN; RNA PRECURSOR;

ARTICLE; CONTROLLED STUDY; GENE MUTATION; HUMAN; INTRON; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; RNA SPLICING; RNA STRUCTURE; SPLICEOSOME; TELEOST; TETRAPOD; ZEBRA FISH; ANIMAL; BIOLOGY; CONFORMATION; EXON; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; REPORTER GENE; SEQUENCE ANALYSIS;

ANIMALS; BASE SEQUENCE; COMPUTATIONAL BIOLOGY; EXONS; GENES, REPORTER; INTRONS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; NUCLEIC ACID CONFORMATION; PHYLOGENY; RIBONUCLEOPROTEINS; RNA PRECURSORS; RNA SPLICING; SEQUENCE ANALYSIS, RNA; SPLICEOSOMES; ZEBRAFISH;

EID: 84956677418     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.181008.114     Document Type: Article

References (72)

1. Auweter SD, Oberstrass FC, Allain FH. 2006. Sequence-specific binding of single-stranded RNA: Is there a code for recognition? Nucleic Acids Res 34: 4943-4959.
2. Bellamy-Royds AB, Turcotte M. 2007. Can Clustal-style progressive pairwise alignment of multiple sequences be used in RNA secondary structure prediction? BMC Bioinformatics 8: 190.
3. Be nnett M, Michaud S, Kingston J, Reed R. 1992. Protein components specifically associated with prespliceosome and spliceosome complexes. Genes Dev 6: 1986-2000.
4. Bernstein FC,Koetzle TF,Williams GJ,Meyer EF Jr.,Brice MD,Rodgers JR,Kennard O,Shimanouchi T,Tasumi M. 1977 The Protein Data Bank: a computer-based archival file for macromolecular structures J Mol Biol 112 535-542.
5. Bhardwaj A, Myers MP, Buratti E, Baralle FE. 2013. Characterizing TDP-43 interaction with its RNA targets. Nucleic Acids Res 41: 5062-5074.
6. Brown TS, Bevilacqua PC. 2005. Method for assigning double-stranded RNA structures. BioTechniques 38: 368-372.
7. Buratti E, Brindisi A, Pagani F, Baralle FE. 2004. Nuclear factor TDP-43 binds to the polymorphic TG repeats in CFTR intron 8 and causes skipp ing of exon 9: a functional link with disease penetrance. Am J Hum Genet 74: 1322-1325.
8. Cech TR, Zaug AJ, Grabowski PJ. 1981. In vitro splicing of the ribosomal RNA precursor of Tetrahymena: involvement of a guanosine nucleotide in the excision of the intervening sequence. Cell 27: 487-496.
9. Celotto AM, Graveley BR. 2001. Alternative splicing of the Drosophila Dscam pre-mRNA is both temporally and spatially regulated. Genetics 159: 599-608.
10. Celotto AM, Graveley BR. 2004. Using single-strand conformational polymorphism gel electrophoresis to analyze mutually exclusive alternative splicing. Methods Mol Biol 257: 65-74.
11. Charpentier B, Rosbash M. 1996. Intramolecular structure in yeast introns aids the early steps of in vitro spliceosome assembly. RNA 2: 509-522.
12. Chen Y, StephanW. 2003. Compensatory evolution of a precursor messenger RNA secondary structure in the Drosophila melanogaster Adh gene. Proc Natl Acad Sci 100: 11499-11504.
13. Clark F, Thanaraj TA. 2002. Categorization and characterization of transcript-confi rmed constitutively and alternatively spliced introns and exons from human. Hum Mol Genet 11: 451-464.
14. Conrad DF, Keebler JE, DePristo MA, Lindsay SJ, Zhang Y, Casals F, Idaghdour Y, Hartl CL, Torroja C, Garimella KV, et al. 2011. Variation in genome-wide mutation rates within and between human families. Nat Genet 43: 712-714.
15. Crawford AM, Cuthbertson RP. 1996. Mutations in sheep microsatellites. Genome Res 6: 876-879.
16. de Koning AP, Gu W, Castoe TA, Batzer MA, Pollock DD. 2011. Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet 7: e1002384.
17. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29: 15-21.
18. Folco EG, Lei H, Hsu JL, Reed R. 2012. Small-scale nuclear extracts for functional assays of gene-expression machineries. J Vis Exp doi: 10.3791/4140.
19. Gama-Carvalho M, Krauss RD, Chiang L, Valcá rcel J, Green MR, Carmo-Fonseca M. 1997. Targeting of U2AF65 to sites of active splicing in the nucleus. J Cell Biol 137: 975-987.
20. Goguel V, Rosbash M. 1993. Splice site choice and splicing efficiency are positively influenced by pre-mRNA intramolecular base pairing in yeast. Cell 72: 893-901.
21. Graveley BR. 2005. Mutually exclusive splicing of the insect Dscam premRNA directed by competing intronic RNA secondary structures. Cell 123: 65-73.
22. Graveley BR, Kaur A, Gunning D, Zipursky SL, Rowen L, Clemens JC. 2004. The organization and evolution of the dipteran and hymenopteran Down syndrom e cell adhesion molecule (Dscam) genes. RNA 10: 1499-1506.
23. Groman JD, Hefferon TW, Casals T, Bassas L, Estivill X, Des Georges M, Guittard C, Koudova M, Fallin MD, Nemeth K, et al. 2004. Variation in a repeat sequence determines whether a common variant of the cystic fibrosis transmembrane conductance regulator gene is pathogenic or benign. Am J Hum Genet 74: 176-179.
24. Hinrichs AS, Karolchik D, Baertsch R, Barber GP, Bejerano G, Clawson H, Diekhans M, Furey TS, Harte RA, Hsu F, et al. 2006. The UCSC Genome Browser Database: update 2006. Nucleic Acids Res 34: D590-D598.
25. Howe KJ, AresMJr. 1997. Intron self-complementarity enforces exon inclusion in a yeast pre-mRNA. Proc Natl Acad Sci 94: 12467-12472.
26. Huang PR,Tsai ST,Hsieh KH,Wang TC. 2008 Heterog eneous nuclear ribonucleoprotein A3 binds single-stranded telomeric DNA and inhibits telomerase extension in vitro Biochim Biophys Acta 1783, 193-202.
27. 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.
28. Kreahling JM, Graveley BR. 2005. The iStem, a long-range RNA second ary structure element required for efficient exon inclusion in the Drosophila Dscam pre-mRNA. Mol Cell Biol 25: 10251-10260.
29. Kumar A, Wilson SH. 1990. Studies of the strand-Annealing activity of mammalian hnRNP complex protein A1. Biochemistry 29: 10717-10722.
30. Lambowitz AM, Zimmerly S. 2004. Mobile group II introns. Annu Rev Genet 38: 1-35.
31. Lee JE, Cooper TA. 2009. Pathog enic mechanisms of myotonic dystrophy. Biochem Soc Trans 37: 1281-1286.
32. Lee CG, Zamore PD, Green MR, Hurwitz J. 1993. RNA annealing activity is intrinsically associated with U2AF. J Biol Chem 268: 13472-13478.
33. Liao Y, Smyth GK, ShiW. 2014. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30: 923-930.
34. Libri D, Stutz F, McCarthy T, Rosbash M. 1995. RNA structural patterns and splicing: molecular basis for an RNA-based enhancer. RNA 1: 425-436.
35. Lim KH, Ferraris L, Filloux ME, Raphael BJ, Fairbrother WG. 2011. Using positional distribution to identify splicing elements and predict pre-mRNA processing defects in human genes. Proc Natl Acad Sci 108: 11093-11098.
36. Lovci MT, Ghanem D, Marr H, Arnold J, Gee S, Parra M, Liang TY, Stark TJ, Gehman LT, Hoon S, et al. 2013. Rbfox proteins regulate alternative mRNA splicing through evolutionarily conserved RNA bridges. Nat Struct Mol Biol 20: 1434-1442.
37. Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15: 550.
38. Low JT, Weeks KM. 2010. SHAPE-directed RNA secondary structure prediction. Methods 52: 150-158.
39. Mangan ME, Williams JM, Lathe SM, Karolchik D, Lathe WC III. 2008. UCSC Genome Browser: deep support for molecular biomedical research. Biotechnol Annu Rev 14: 63-108.
40. Marquis J, Paillard L, Audic Y, Cosson B, Danos O, Le Bec C, Osborne HB. 2006. CUG-BP1/CELF1 requires UGU-rich sequences for high-Affinity binding. Biochem J 400: 291-301.
41. Mathews DH. 2006. Revolutions in RNA secondary structure prediction. J Mol Biol 359: 526-532.
42. Mathews DH, Turner DH, Zuker M. 2007. RNA secondary structure prediction. Curr Protoc Nucleic Acid Chem 28: 11.12.11-11.12.17.
43. Matlin AJ, Moore MJ. 2007. Spliceosome assembly and composition. Adv Exp Med Biol 623: 14-35.
44. May GE, Ol son S,McManus CJ, Graveley BR. 2011. Competing RNA secondary structures are required for mutually exclusive splicing of the Dscam exon 6 cluster. RNA 17: 222-229.
45. McCullough AJ, Berget SM. 2000. An intronic splicing enhancer binds U1 snRNPs to enhance splicing and select 5? splice sites. Mol Cell Biol 20: 9225-9235.
46. McManus CJ, Graveley BR. 2011. RNA structure and the mechanisms of alternative splicing. Curr Opin Genet Dev 21: 373-379.
47. Munroe SH,Dong XF. 1992 Heterogeneous nuclear ribonucleoprotein A1 catalyzes RNA.RNA annealing Proc Natl Acad Sci 89 895-899.
48. Olson S, Blanchett e M, Park J, Savva Y, Yeo GW, Yeakley JM, Rio DC, Graveley BR. 2007. A regulator of Dscam mutually exclusive splicing fidelity. Nat Struct Mol Biol 14: 1134-1140.
49. Passoni M, De Conti L, Baralle M, Buratti E. 2012. UG repeats/TDP-43 interactions near 5? splice sites exert unpredictable effects on splicing modulation. J Mol Biol 415: 46-60.
50. Robberson BL, Cote GJ, Berget SM. 1990. Exon definition may facilitate splice site selection in RNAs with multiple exons. Mol Cell Biol 10: 84-94.
51. Rudner DZ, Breger KS, Kanaar R, Adams MD, Rio DC. 1998a . RNA binding activity of heterodimeric splicing factor U2AF: At least one RS domain is required for high-Affinity binding. Mol Cell Biol 18: 4004-4011.
52. Rudner DZ, Breger KS, Rio DC. 1998b . Molecular genetic analysis of the heterodimeric splicing factor U2AF: The RS domain on either the large or small Drosophila subunit is dispensable in vivo. Genes Dev 12: 1010-1021.
53. Schenkel J, Sekeris CE, Alonso A, Bautz EK. 1988. RNA-binding properties of hnRNP proteins. Eur J Biochem 171: 565-569.
54. Seetin MG, Mathews DH. 2012. RNA structure prediction: an overview of methods. Methods Mol Biol 905: 99-122.
55. Shelley CS, Baralle FE. 1987. Deletion analysis of a unique 3? splice site indicates that alternating guanine and thymine residues represent an efficient splicing si gnal. Nucleic Acids Res 15: 3787-3799.
56. Shen H, Green MR. 2006. RS domains contact splicing signals and promote splicing by a common mechanism in yeast through humans. Genes Dev 20: 1755-1765.
57. Shimoda N, Knapik EW, Ziniti J, Sim C, Yamada E, Kaplan S, Jackson D, de Sauvage F, Jacob H, Fishman MC. 1999. Zebrafish genetic map with 2000 microsatellite markers. Genomics 58: 219-232.
58. Singh R, Valcarcel J, Green MR. 1995. Distinct binding specificities and functions of higher eukaryotic polypyrimidine tract-binding proteins. Science 268: 1173-1176.
59. Skabkin MA, Evdokimova V, Thomas AA, Ovchinnikov LP. 2001. The major messenger ribonucleoprotein particle protein p50 (YB-1) promotes nucleic acid strand annealing. J Biol Chem 276: 44841-44847.
60. Solnick D, Lee S I. 1987. Amount of RNA secondary structure required to induce an alternative splice. Mol Cell Biol 7: 3194-3198.
61. 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.
62. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. 201 2. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7: 562-578.
63. Trauger RJ, Talbott R, Wilson SH, Karpel RL, Elder JH. 1990. A single -stranded nucleic acid binding sequence common to the heterogeneous nuclear ribonucleoparticle protein A1 and murine recombinant virus gp70. J Biol Chem 265: 3674-3678.
64. Valcarcel J, Gaur RK, Singh R, Green MR. 1996. Interaction of U2AF65 RS region with pre-mRNA branch point and promotion of base pairing with U2 snRNA [corrected]. Science 273: 1706-1709.
65. Wang Z, Rolish ME, Yeo G, Tung V, Mawson M, Burge CB. 2004. Systematic identification and analysis of exonic splicing silencers. Cell 119: 831-845.
66. Warf MB, Berglund JA. 2007. MBNL binds similar RNA structures in the CUG repeats of myotonic dystrophy and its pre-mRNA substrate cardiac troponin T. RNA 13: 2238-2251.
67. Warf MB, Berglund JA. 2010. Role of RNA structure in regulating pre-mRNA splicing. Trends Biochem Sci 35: 169-178.
68. Weber JL,Wong C. 1993 Mutation of human short tandem repeats Hum Mol Genet 2, 1123-1128.
69. Yang Y, Zhan L, ZhangW, Sun F, WangW, Tian N, Bi J, Wang H, Shi D, Jiang Y, e t al. 2011. RNA secondary structure in mutually exclusive splicing. Nat Struct Mol Biol 18: 159-168.
70. Yeo G, Hoon S, Venkatesh B, Burge CB. 2004. Variation in sequence and organization of splicing regulatory elements in vertebrate genes. Proc Natl Acad Sci 101: 15700-15705.
71. Zuker M, Stiegler P. 1981. Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information. Nucleic Acids Res 9: 133-148.
72. Zuo P, Maniatis T. 1996. The splicing factor U2AF35 mediates critical protein-protein interactions in constitutive and enhancer-dependent splicing. Genes Dev 10: 1356-1368.