Regulation of splicing enhancer activities by RNA secondary structures

FEBS Letters

Volumn 584, Issue 21, 2010, Pages 4401-4407

  Liu, Wei ^a   Zhou, Yu ^a,b,c   Hu, Zexi ^a   Sun, Tao ^a   Denise, Alain ^c,d,e   Fu, Xiang Dong ^a,b   Zhang, Yi ^a,f  

^a WUHAN UNIVERSITY   (China)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d CNRS   (France)

^e INRIA   (France)

^f ABLife Inc   (China)

Author keywords

Alternative splicing; ESE; Secondary structure

Indexed keywords

ADENINE; CYTOSINE; GUANINE; URACIL;

3' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; ENHANCER REGION; EXON; GENE; GENE MUTATION; HUMAN; HUMAN CELL; POINT MUTATION; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; REGULATORY MECHANISM; RNA SEQUENCE; RNA SPLICING; RNA STABILITY; RNA STRUCTURE; SMN1 GENE; SMN2 GENE;

BASE PAIRING; BASE SEQUENCE; EXONS; HELA CELLS; HUMANS; INVERTED REPEAT SEQUENCES; NUCLEIC ACID CONFORMATION; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RNA; RNA SPLICING; RNA STABILITY; SURVIVAL OF MOTOR NEURON 1 PROTEIN; TEMPERATURE;

EID: 78049248013     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2010.09.039     Document Type: Article

References (43)

1. Black D.L. Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem. 2003, 72:291-336.
2. Wang E.T., et al. Alternative isoform regulation in human tissue transcriptomes. Nature 2008, 456(7221):470-476.
3. Cooper T.A. Alternative splicing regulation impacts heart development. Cell 2005, 120(1):1-2.
4. Schwerk C., Schulze-Osthoff K. Regulation of apoptosis by alternative pre-mRNA splicing. Mol. Cell 2005, 19(1):1-13.
5. Li Q., Lee J.A., Black D.L. Neuronal regulation of alternative pre-mRNA splicing. Nat. Rev. Neurosci. 2007, 8(11):819-831.
6. Biamonti G., Caceres J.F. Cellular stress and RNA splicing. Trends Biochem. Sci. 2009, 34(3):146-153.
7. Chen M., Manley J.L. Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat. Rev. Mol. Cell Biol. 2009, 10(11):741-754.
8. Buratti E., Baralle F.E. Influence of RNA secondary structure on the pre-mRNA splicing process. Mol. Cell Biol. 2004, 24(24):10505-10514.
9. Shepard P.J., Hertel K.J. Conserved RNA secondary structures promote alternative splicing. RNA 2008, 14(8):1463-1469.
10. Warf M.B., Berglund J.A. Role of RNA structure in regulating pre-mRNA splicing. Trends Biochem. Sci. 2010, 35(3):168-178.
11. Fairbrother W.G., et al. Predictive identification of exonic splicing enhancers in human genes. Science 2002, 297(5583):1007-1013.
12. Wang Z., et al. Systematic identification and analysis of exonic splicing silencers. Cell 2004, 119(6):831-845.
13. Fu X.D. Towards a splicing code. Cell 2004, 119(6):736-738.
14. Tejedor J.R., Valcarcel J. Gene regulation: breaking the second genetic code. Nature 2010, 465(7294):45-46.
15. Barash Y., et al. Deciphering the splicing code. Nature 2010, 465(7294):53-59.
16. Wang G.S., Cooper T.A. Splicing in disease: disruption of the splicing code and the decoding machinery. Nat. Rev. Genet. 2007, 8(10):749-761.
17. Xue Y., et al. Genome-wide analysis of PTB-RNA interactions reveals a strategy used by the general splicing repressor to modulate exon inclusion or skipping. Mol. Cell 2009, 36(6):996-1006.
18. Yeo G.W., et al. An RNA code for the FOX2 splicing regulator revealed by mapping RNA-protein interactions in stem cells. Nat. Struct. Mol. Biol. 2009, 16(2):130-137.
19. Licatalosi D.D., et al. HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 2008, 456(7221):464-469.
20. Buratti E., et al. RNA folding affects the recruitment of SR proteins by mouse and human polypurinic enhancer elements in the fibronectin EDA exon. Mol. Cell Biol. 2004, 24(3):1387-1400.
21. Muro A.F., et al. Regulation of fibronectin EDA exon alternative splicing: possible role of RNA secondary structure for enhancer display. Mol. Cell Biol. 1999, 19(4):2657-2671.
22. Hiller M. Pre-mRNA secondary structures influence exon recognition. PLoS Genet. 2007, 3(11):e204.
23. Liu H., Naismith J.H. An efficient one-step site-directed deletion, insertion, single and multiple-site plasmid mutagenesis protocol. BMC Biotechnol. 2008, 8:91.
24. Eperon L.P., et al. Effects of RNA secondary structure on alternative splicing of pre-mRNA: is folding limited to a region behind the transcribing RNA polymerase?. Cell 1988, 54(3):393-401.
25. Schroeder R., et al. RNA folding in vivo. Curr. Opin. Struct. Biol. 2002, 12(3):296-300.
26. Shapiro B.A., et al. Bridging the gap in RNA structure prediction. Curr. Opin. Struct. Biol. 2007, 17(2):157-165.
27. Mahen E.M., et al. mRNA secondary structures fold sequentially but exchange rapidly in vivo. PLoS Biol. 2010, 8(2):e1000307.
28. Yang G., et al. An erythroid differentiation-specific splicing switch in protein 4.1R mediated by the interaction of SF2/ASF with an exonic splicing enhancer. Blood 2005, 105(5):2146-2153.
29. Shen L.X., Cai Z., Tinoco I. RNA structure at high resolution. FASEB J. 1995, 9(11):1023-1033.
30. Baumruk V., et al. Comparison between CUUG and UUCG tetraloops: thermodynamic stability and structural features analyzed by UV absorption and vibrational spectroscopy. Nucleic Acids Res. 2001, 29(19):4089-4096.
31. Denisov A.Y., et al. A novel RNA motif based on the structure of unusually stable 2′, 5′-linked r(UUCG) loops. J. Am. Chem. Soc. 2003, 125(38):11525-11531.
32. Desmet F.O., et al. Human Splicing Finder: an online bioinformatics tool to predict splicing signals. Nucleic Acids Res. 2009, 37(9):e67.
33. Wang J., et al. Distribution of SR protein exonic splicing enhancer motifs in human protein-coding genes. Nucleic Acids Res. 2005, 33(16):5053-5062.
34. Gralla J., Crothers D.M. Free energy of imperfect nucleic acid helices II. Small hairpin loops. J. Mol. Biol. 1973, 73(4):497-511.
35. Ravetch J., Gralla J., Crothers D.M. Thermodynamic and kinetic properties of short RNA helices: the oligomer sequence AnGCUn. Nucleic Acids Res. 1974, 1(1):109-127.
36. Darzacq X., et al. In vivo dynamics of RNA polymerase II transcription. Nat. Struct. Mol. Biol. 2007, 14(9):796-806.
37. Liebega A., Waldsich C. Probing RNA structure within living cells. Methods Enzymol 2009, 468:219-318.
38. Pagani F., Raponi M., Baralle F.E. Synonymous mutations in CFTR exon 12 affect splicing and are not neutral in evolution. Proc. Natl. Acad. Sci. USA 2005, 102(18):6368-6372.
39. Cooper T.A., Wan L., Dreyfuss G. RNA and disease. Cell 2009, 136(4):777-793.
40. Cartegni L., Krainer A.R. Disruption of an SF2/ASF-dependent exonic splicing enhancer in SMN2 causes spinal muscular atrophy in the absence of SMN1. Nat. Genet. 2002, 30(4):377-384.
41. Kashima T., Manley J.L. A negative element in SMN2 exon 7 inhibits splicing in spinal muscular atrophy. Nat. Genet. 2003, 34(4):460-463.
42. Singh N.N., Singh R.N., Androphy E.J. Modulating role of RNA structure in alternative splicing of a critical exon in the spinal muscular atrophy genes. Nucleic Acids Res. 2007, 35(2):371-389.
43. Cartegni L., et al. ESEfinder: a web resource to identify exonic splicing enhancers. Nucleic Acids Res. 2003, 31(13):3568-3571.