Recognition of atypical 5′ splice sites by shifted base-pairing to U1 snRNA

Nature Structural and Molecular Biology

Volumn 16, Issue 2, 2009, Pages 176-182

  Roca, Xavier ^a   Krainer, Adrian R ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOTIDE; SMALL NUCLEAR RNA;

ALGORITHM; ARTICLE; BASE PAIRING; CEREBELLUM HYPOPLASIA; CONTROLLED STUDY; FEMALE; GENE MUTATION; GENE REPRESSION; GENOME; HUMAN; HUMAN CELL; PHYLOGENY; PRIORITY JOURNAL; RNA SPLICING;

ANIMALS; BASE PAIRING; BASE SEQUENCE; HELA CELLS; HUMANS; NUCLEIC ACID CONFORMATION; RNA SPLICE SITES; RNA SPLICING; RNA, SMALL NUCLEAR;

EID: 59649083526     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1546     Document Type: Article

References (48)

1. Brow, D.A. Allosteric cascade of spliceosome activation. Annu. Rev. Genet. 36, 333-360 (2002).
2. Bessonov, S., Anokhina, M., Will, C.L., Urlaub, H. & Lührmann, R. Isolation of an active step I spliceosome and composition of its RNP core. Nature 452, 846-850 (2008).
3. Lerner, M.R., Boyle, J.A., Mount, S.M., Wolin, S.L. & Steitz, J.A. Are snRNPs involved in splicing? Nature 283, 220-224 (1980).
4. Rogers, J. & Wall, R. A mechanism for RNA splicing. Proc. Natl. Acad. Sci. USA 77, 1877-1879 (1980).
5. Zhuang, Y. & Weiner, A.M. A compensatory base change in U1 snRNA suppresses a 5′ splice site mutation. Cell 46, 827-835 (1986).
6. Sheth, N. et al. Comprehensive splice-site analysis using comparative genomics. Nucleic Acids Res. 34, 3955-3967 (2006).
7. Séraphin, B., Kretzner, L. & Rosbash, M. A U1 snRNA:pre-mRNA base pairing interaction is required early in yeast spliceosome assembly but does not uniquely define the 5′ cleavage site. EMBO J. 7, 2533-2538 (1988).
8. Siliciano, P.G. & Guthrie, C. 5′ splice site selection in yeast: genetic alterations in base-pairing with U1 reveal additional requirements. Genes Dev. 2, 1258-1267 (1988).
9. Carmel, I., Tal, S., Vig, I. & Ast, G. Comparative analysis detects dependencies among the 5′ splice-site positions. RNA 10, 828-840 (2004).
10. Roca, X. et al. Features of 5′-splice-site efficiency derived from disease-causing mutations and comparative genomics. Genome Res. 18, 77-87 (2008).
11. Will, C.L. & Lührmann, R. Splicing of a rare class of introns by the U12-dependent spliceosome. Biol. Chem. 386, 713-724 (2005).
12. Cartegni, L., Hastings, M.L., Calarco, J.A., de Stanchina, E. & Krainer, A.R. Determinants of exon 7 splicing in the spinal muscular atrophy genes, SMN1 and SMN2. Am. J. Hum. Genet. 78, 63-77 (2006).
13. Lorson, C.L., Hahnen, E., Androphy, E.J. & Wirth, B. A single nucleotide in the SMN gene regulates splicing and is responsible for spinal muscular atrophy. Proc. Natl. Acad. Sci. USA 96, 6307-6311 (1999).
14. Kashima, T. & Manley, J.L. A negative element in SMN2 exon 7 inhibits splicing in spinal muscular atrophy. Nat. Genet. 34, 460-463 (2003).
15. Senapathy, P., Shapiro, M.B. & Harris, N.L. Splice junctions, branch point sites, and exons: sequence statistics, identification, and applications to genome project. Methods Enzymol. 183, 252-278 (1990).
16. Shapiro, M.B. & Senapathy, P. RNA splice junctions of different classes of eukaryotes: sequence statistics and functional implications in gene expression. Nucleic Acids Res. 15, 7155-7174 (1987).
17. Serra, M.J. & Turner, D.H. Predicting thermodynamic properties of RNA. Methods Enzymol. 259, 242-261 (1995).
18. Hartmann, L., Theiss, S., Niederacher, D. & Schaal, H. Diagnostics of pathogenic splicing mutations: does bioinformatics cover all bases? Front. Biosci. 13, 3252-3272 (2008).
19. Brunak, S., Engelbrecht, J. & Knudsen, S. Prediction of human mRNA donor and acceptor sites from the DNA sequence. J. Mol. Biol. 220, 49-65 (1991).
20. Burge, C. Modeling dependencies in pre-mRNA splicing signals. in Computational Methods in Molecular Biology, Ch. 8, 129-164 (eds. Salzberg, S.L., Searls, D.B. & Kasif, S.) (Elsevier, Philadelphia, 1998).
21. Yeo, G. & Burge, C.B. Maximum entropy modeling of short sequence motifs with applications to RNA splicing signals. J. Comput. Biol. 11, 377-394 (2004).
22. Roca, X., Sachidanandam, R. & Krainer, A.R. Determinants of the inherent strength of human 5′ splice sites. RNA 11, 683-698 (2005).
23. Mount, S.M. & Anderson, P. Expanding the definition of informational suppression. Trends Genet. 16, 157 (2000).
24. Lo, P.C., Roy, D. & Mount, S.M. Suppressor U1 snRNAs in Drosophila. Genetics 138, 365-378 (1994).
25. Cohen, J.B., Snow, J.E., Spencer, S.D. & Levinson, A.D. Suppression of mammalian 5′ splice-site defects by U1 small nuclear RNAs from a distance. Proc. Natl. Acad. Sci. USA 91, 10470-10474 (1994).
26. Kyriakopoulou, C. et al. U1-like snRNAs lacking complementarity to canonical 5′ splice sites. RNA 12, 1603-1611 (2006).
27. Newman, A.J. & Norman, C. U5 snRNA interacts with exon sequences at 5′ and 3′ splice sites. Cell 68, 743-754 (1992).
28. Wassarman, D.A. & Steitz, J.A. Interactions of small nuclear RNA's with precursor messenger RNA during in vitro splicing. Science 257, 1918-1925 (1992).
29. Kandels-Lewis, S. & Séraphin, B. Involvement of U6 snRNA in 5′ splice site selection. Science 262, 2035-2039 (1993).
30. Lesser, C.F. & Guthrie, C. Mutations in U6 snRNA that alter splice site specificity: implications for the active site. Science 262, 1982-1988 (1993).
31. Staley, J.P. & Guthrie, C. Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell 92, 315-326 (1998).
32. Hwang, D.Y. & Cohen, J.B. U1 snRNA promotes the selection of nearby 5′ splice sites by U6 snRNA in mammalian cells. Genes Dev. 10, 338-350 (1996).
33. Brackenridge, S., Wilkie, A.O. & Screaton, G.R. Efficient use of a 'dead-end' GA 5′ splice site in the human fibroblast growth factor receptor genes. EMBO J. 22, 1620-1631 (2003).
34. Konarska, M.M., Vilardell, J. & Query, C.C. Repositioning of the reaction intermediate within the catalytic center of the spliceosome. Mol. Cell 21, 543-553 (2006).
35. Rhode, B.M., Harmuth, K., Westhof, E. & Lührmann, R. Proximity of conserved U6 and U2 snRNA elements to the 5′ splice site region in activated spliceosomes. EMBO J. 25, 2475-2486 (2006).
36. Du, H. & Rosbash, M. Yeast U1 snRNP-pre-mRNA complex formation without U1snRNA-pre-mRNA base pairing. RNA 7, 133-142 (2001).
37. Du, H. & Rosbash, M. The U1 snRNP protein U1C recognizes the 5′ splice site in the absence of base pairing. Nature 419, 86-90 (2002).
38. Lu, X.B., Heimer, J., Rekosh, D. & Hammarskjöld, M.L. U1 small nuclear RNA plays a direct role in the formation of a rev-regulated human immunodeficiency virus env mRNA that remains unspliced. Proc. Natl. Acad. Sci. USA 87, 7598-7602 (1990).
39. Boelens, W.C. et al. The human U1 snRNP-specific U1A protein inhibits polyadenylation of its own pre-mRNA. Cell 72, 881-892 (1993).
40. Leu, J.Y. & Roeder, G.S. Splicing of the meiosis-specific HOP2 transcript utilizes a unique 5′ splice site. Mol. Cell. Biol. 19, 7933-7943 (1999).
41. Edvardson, S. et al. Deleterious mutation in the mitochondrial arginyl-transfer RNA synthetase gene is associated with pontocerebellar hypoplasia. Am. J. Hum. Genet. 81, 857-862 (2007).
42. Buratti, E. et al. Aberrant 5′ splice sites in human disease genes: mutation pattern, nucleotide structure and comparison of computational tools that predict their utilization. Nucleic Acids Res. 35, 4250-4263 (2007).
43. Lund, M. & Kjems, J. Defining a 5′ splice site by functional selection in the presence and absence of U1 snRNA 5′ end. RNA 8, 166-179 (2002).
44. Schwartz, S.H. et al. Large-scale comparative analysis of splicing signals and their corresponding splicing factors in eukaryotes. Genome Res. 18, 88-103 (2008).
45. Stalker, J. et al. The Ensembl web site: mechanics of a genome browser. Genome Res. 14, 951-955 (2004).
46. Kent, W.J. et al. The Human Genome Browser at UCSC. Genome Res. 12, 996-1006 (2002).
47. Lobo, S.M. & Hernandez, N. A 7 bp mutation converts a human RNA polymerase II snRNA promoter into an RNA polymerase III promoter. Cell 58, 55-67 (1989).
48. Good, P.D. et al. Expression of small, therapeutic RNAs in human cell nuclei. Gene Ther. 4, 45-54 (1997).