Alternative pre-mRNA splicing in the human system: Unexpected role of repetitive sequences as regulatory elements

Biological Chemistry

Volumn 386, Issue 12, 2005, Pages 1265-1271

  Hui, Jingyi ^a   Bindereif, Albrecht ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

RNA processing; Simple sequence repeats; Splicing enhancer; Splicing regulation; Splicing silencer

Indexed keywords

DNA BINDING PROTEIN; MESSENGER RNA; RNA;

BINDING SITE; BIOINFORMATICS; CYSTIC FIBROSIS; DEFENSE MECHANISM; DEVELOPMENT; EVOLUTION; EXON; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE INTERACTION; GENE SEQUENCE; GENE STRUCTURE; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENOMICS; HOMEOSTASIS; HUMAN; INTRON; MOLECULAR CLONING; MUTATIONAL ANALYSIS; MYOTONIC DYSTROPHY; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEOMICS; RNA SPLICING; SHORT SURVEY; SPLICEOSOME;

ALTERNATIVE SPLICING; ENHANCER ELEMENTS (GENETICS); GENE EXPRESSION REGULATION; GENE SILENCING; HUMANS; POLYMORPHISM, GENETIC; PROTEOME; REPETITIVE SEQUENCES, NUCLEIC ACID; RNA PRECURSORS;

EID: 29044447700     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2005.143     Document Type: Short Survey

References (65)

1. Bilbao, D. and Valcárcel, J. (2003). Getting to the heart of a splicing enhancer. Nat. Struct. Biol. 10, 6-7.
2. Black, D.L. (1995). Finding splice sites within a wilderness of RNA. RNA 1, 763-771.
3. Black, D.L. (2003). Mechanism of alternative pre-messenger RNA splicing. Annu. Rev. Biochem. 72, 291-336.
4. Blencowe, B.J. (2000). Exonic splicing enhancers: mechanism of action, diversity and role in human genetic diseases. Trends Biochem. Sci. 25, 106-110.
5. Brow, D.A. (2002). Allosteric cascade of spliceosome activation. Annu. Rev. Genet. 36, 333-360.
6. Buratti, E., Dork, T., Zuccato, E., Pagani, F., Romano, M., and Baralle, F.E. (2001). Nuclear factor TDP-43 and SR proteins promote in vitro and in vivo CFTR exon 9 skipping. EMBO J. 20, 1774-1784.
7. Cáceres, J.F. and Kornblihtt, A.R. (2002). Alternative splicing: multiple control mechanisms and involvement in human disease. Trends Genet. 18, 186-193.
8. Cartegni, L., Chew, S.L., and Krainer, A.R. (2002). Listening to silence and understanding nonsense: exonic mutations that affect splicing. Nat. Rev. Genet. 3, 285-298.
9. Cartegni, L., Wang, J., Zhu, Z., Zhang, M.Q., and Krainer, A.R. (2003). ESEfinder: a web resource to identify exonic splicing enhancers. Nucleic Acids Res. 31, 3568-3571.
10. Charlet-B, N., Savkur, R.S., Singh, G., Philips, A.V., Grice, E.A., and Cooper, T.A. (2002). Loss of the muscle-specific chloride channel in type 1 myotonic dystrophy due to misregulated alternative splicing. Mol. Cell 70, 45-53.
11. Chu, C.S., Trapnell, B.C., Curristin, S., Cutting, G.R., and Crystal, R.G. (1993). Genetic basis of variable exon 9 skipping in cystic fibrosis transmembrane conductance regulator mRNA. Nat. Genet. 3, 151-156.
12. Coulter, L.R., Landree, M.A., and Cooper, T.A. (1997). Identification of a new class of exonic splicing enhancers by in vivo selection. Mol. Cell. Biol. 77, 2143-2150.
13. Cuppens, H., Lin, W., Jaspers, M., Costes, B., Teng, H., Vankeerberghen, A., Jorissen, M., Droogmans, G., Reynaert, I., Goossens, M., Nilius, B., Cassiman, J.J. (1998). Polyvariant mutant cystic fibrosis transmembrane conductance regulator genes. The polymorphic (TG)m locus explains the partial penetrance of the T5 polymorphism as a disease mutation. J. Clin. Invest. 101, 487-496.
14. Cutting, G.R. (2005). Modifier genetics: cystic fibrosis. Annu. Rev. Genomics Hum. Genet. 6, 237-260.
15. Dansithong, W., Paul, S., Comai, L., and Reddy, S. (2005). MBNL1 is the primary determinant of focus formation and aberrant insulin receptor splicing in DM1. J. Biol. Chem. 280, 5773-5780.
16. Deutsch, M. and Long, M. (1999). Intron-exon structures of eukaryotic model organisms. Nucleic Acids Res. 27, 3219-3228.
17. Dredge, B.K., Stefani, G., Engelhard, C.C., and Darnell, R.B. (2005). Nova autoregulation reveals dual functions in neuronal splicing. EMBO J. 24, 1608-1620.
18. Fairbrother, W.G. and Chasin, L.A. (2000). Human genomic sequences that inhibit splicing. Mol. Cell. Biol. 20, 6816-6825.
19. Fairbrother, W.G., Yeh, R.F., Sharp, P.A., and Burge, C.B. (2002). Predictive identification of exonic splicing enhancers in human genes. Science 297, 1007-1013.
20. Fairbrother, W.G., Yeo, G.W., Yeh, R., Goldstein, P., Mawson, M., Sharp, P.A., and Burge, C.B. (2004). RESCUE-ESE identifies candidate exonic splicing enhancers in vertebrate exons. Nucleic Acids Res. 32, W187-190.
21. 2+ exchanger intron 2 activates splicing. Eur. J. Biochem. 268, 1076-1083.
22. Graveley, B.R. (2000). Sorting out the complexity of SR protein functions. RNA 6, 1197-1211.
23. Groman, J.D., Hefferon, T.W., Casals, T., Bassas, L., Estivill, X., Des Georges, M., Guittard, C., Koudova, M., Fallin, M.D., 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. Hedjran, F., Yeakley, J.M., Huh, G.S., Hynes, R.O., and Rosenfeld, M.G. (1997). Control of alternative pre-mRNA splicing by distributed pentameric repeats. Proc. Natl. Acad. Sci. USA 94, 12343-12347.
25. Hefferon, T.W., Groman, J.D., Yurk, C.E., and Cutting, G.R. (2004). A variable dinucleotide repeat in the CFTR gene contributes to phenotype diversity by forming RNA secondary structures that alter splicing. Proc. Natl. Acad. Sci. USA 101, 3504-3509.
26. Huh, G.S. and Hynes, R.O. (1994). Regulation of alternative pre-mRNA splicing by a novel repeated hexanucleotide element. Genes Dev. 8, 1561-1574.
27. Hui, J., Stangl, K., Lane, W.S., and Bindereif, A. (2003). HnRNP L stimulates splicing of the eNOS gene by binding to variable-length CA repeats. Nat. Struct. Biol. 40, 33-37.
28. Hui, J., Hung, L.H., Heiner, M., Schreiner, S., Neumuller, N., Reither, G., Haas, S.A., and Bindereif, A. (2005). Intronic CA-repeat and CA-rich elements: a new class of regulators of mammalian alternative splicing. EMBO J. 24, 1988-1998.
29. Jensen, K.B., Musunuru, K., Lewis, H.A., Burley, S.K., and Darnell, R.B. (2000). The tetranucleotide UCAY directs the specific recognition of RNA by the Nova K-homology 3 domain. Proc. Natl. Acad. Sci. USA 97, 5740-5745.
30. Johnson, J.M., Castle, J., Garrett-Engele, P., Kan, Z., Loerch, P.M., Armour, C.D., Santos, R., Schadt, E.E., Stoughton, R., and Shoemaker, D.D. (2003). Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science 302, 2141-2144.
31. Kino, Y., Mori, D., Oma, Y., Takeshita, Y., Sasagawa, N., and Ishiura, S. (2004). Muscleblind protein, MBNL1/EXP, binds specifically to CHHG repeats. Hum. Mol. Genet. 13, 495-507.
32. Krecic, A.M. and Swanson, M.S. (1999). hnRNP complexes: composition, structure, and function. Curr. Opin. Cell Biol. 11, 363-371.
33. Kriventseva, E.V., Koch, I., Apweiler, R., Vingron, M., Bork, P., Gelfand, M.S., and Sunyaev, S. (2003). Increase of functional diversity by alternative splicing. Trends Genet. 79, 124-128.
34. Ladd, A.N. and Cooper T.A. (2002). Finding signals that regulate alternative splicing in the post-genomic era. Genome Biol. 3, reviews0008.
35. Lander, E.S., Linton, L.M., Birren, B., Nusbaum, C., Zody, M.C., Baldwin, J., Devon, K., Dewar, K., Doyle M., et al. (2001). Initial sequencing and analysis of the human genome. Nature 409, 860-921.
36. Lim, L.P. and Burge, C.B. (2001). A computational analysis of sequence features involved in recognition of short introns. Proc. Natl. Acad. Sci. USA 98, 11193-11198.
37. Liu, H.X., Zhang, M., and Krainer, A.R. (1998). Identification of functional exonic splicing enhancer motifs recognized by individual SR proteins. Genes Dev. 12, 1998-2012.
38. Liu, H.X., Chew, S.L., Cartegni, L., Zhang, M.Q., and Krainer, A.R. (2000). Exonic splicing enhancer motif recognized by human SC35 under splicing conditions. Mol. Cell. Biol. 20, 1063-1071.
39. Lynch, K.W. and Maniatis, T. (1996). Assembly of specific SR protein complexes on distinct regulatory elements of the Drosophila doublesex splicing enhancer. Genes Dev. 10, 2089-2101.
40. Maniatis, T. and Tasic, B. (2002). Alternative pre-mRNA splicing and proteome expansion in metazoans. Nature 478, 236-243.
41. Mankodi, A., Takahashi, M.P., Jiang, H., Beck, C.L., Bowers, W.J., Moxley, R.T., Cannon, S.C., and Thornton, C.A. (2002). Expanded CUG repeats trigger aberrant splicing of CIC-1 chloride channel pre-mRNA and hyperexcitability of skeletal muscle in myotonic dystrophy. Mol. Cell 10, 35-44.
42. Matter, N., Herrlich, P., and König, H. (2002). Signal-dependent regulation of splicing via phosphorylation of Sam68. Nature 420, 691-695.
43. McCullough, A.J. and Berget, S.M. (1997). G triplets located throughout a class of small vertebrate introns enforce intron borders and regulate splice site selection. Mol. Cell. Biol. 77, 4562-4571.
44. McCullough, A.J. and Berget, S.M. (2000). An intronic splicing enhancer binds U1 snRNPs to enhance splicing and select 5′ splice sites. Mol. Cell. Biol. 20, 9225-9235.
45. Modrek, B. and Lee, C. (2002). A genomic view of alternative splicing. Nat. Genet. 30, 13-19.
46. Niksic, M., Romano, M., Buratti, E., Pagani, F., and Baralle, F.E. (1999). Functional analysis of cis-acting elements regulating the alternative splicing of human CFTR exon 9. Hum. Mol. Genet. 8, 2339-2349.
47. Nilsen, T.W. (2003). The spliceosome: the most complex macromolecular machine in the cell? Bioessays 25, 1147-1149.
48. Philips, A.V. and Cooper, T.A. (2000). RNA processing and human disease. Cell. Mol. Life Sci. 57, 235-249.
49. Philips, A.V., Timchenko, L.T., and Cooper, T.A. (1998). Disruption of splicing regulated by a CUG-binding protein in myotonic dystrophy. Science 280, 737-741.
50. Ranum, L.P. and Day, J.W. (2004). Myotonic dystrophy: RNA pathogenesis comes into focus. Am. J. Hum. Genet. 74, 793-804.
51. Rothrock, C.R., House, A.E., and Lynch, K.W. (2005). HnRNP L represses exon splicing via a regulated exonic splicing silencer. EMBO J. 24, 2792-2802.
52. Savkur, R.S., Philips, A.V., and Cooper, T.A. (2001). Aberrant regulation of insulin receptor alternative splicing is associated with insulin resistance in myotonic dystrophy. Nat. Genet. 29, 40-47.
53. Schaal, T.D. and Maniatis, T. (1999). Selection and characterization of pre-mRNA splicing enhancers: identification of novel SR protein-specific enhancer sequences. Mol. Cell. Biol. 19, 1705-1719.
54. Schmucker, D., Clemens, J.C., Shu, H., Worby, C.A., Xiao, J., Muda, M., Dixon, J.E., and Zipursky, S.L. (2000). Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101, 671-684.
55. Sharp, P.A. (1994). Split genes and RNA splicing. Cell 77, 805-815.
56. Shelley, C.S. and Baralle, F.E. (1987). Deletion analysis of a unique 3′ splice site indicates that alternating guanine and thymine residues represent an efficient splicing signal. Nucleic Acids Res. 15, 3787-3799.
57. Shin, C. and Manley, J.L. (2004). Cell signalling and the control of pre-mRNA splicing. Nat. Rev. Mol. Cell. Biol. 5, 727-738.
58. Staley, J.P. and Guthrie, C. (1998). Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell 92, 315-326.
59. Stangl, K., Cascorbi, I., Laule, M., Klein, T., Stangl, V., Rost, S., Wernecke, K.D., Felix, S.B., Bindereif, A., Baumann, G., and Roots, I. (2000). High CA repeat numbers in intron 13 of the endothelial nitric oxide synthase gene and increased risk of coronary artery disease. Pharmacogenetics 10, 133-140.
60. Stickeler, E., Fraser, S.D., Honig, A., Chen, A.L., Berget, S.M., and Cooper, T.A. (2001). The RNA binding protein YB-1 binds A/C-rich exon enhancers and stimulates splicing of the CD44 alternative exon v4. EMBO J. 20, 3821-3830.
61. Stoss, O., Stoilov, P., Daoud, R., Hartmann, A.M., Olbrich, M., and Stamm, S. (2000). Misregulation of pre-mRNA splicing that causes human diseases. Concepts and therapeutic strategies. Gene Ther. Mol. Biol. 5, 1-20.
62. Ule, J., Jensen, K.B., Ruggiu, M., Mele, A., Ule, A., and Darnell, R.B. (2003). CLIP identifies Nova-regulated RNA networks in the brain. Science 302, 1212-1215.
63. Venter, J.C., Adams, M.D., Myers, E.W., Li, P.W., Mural, R.J., Sutton, G.G., Smith, H.O., Yandell, M., Evans, C.A., Holt, R.A., et al. (2001). The sequence of the human genome. Science 291, 1304-1351.
64. Weg-Remers, S., Ponta, H., Herrlich, P., and König, H. (2001). Regulation of alternative pre-mRNA splicing by the ERK MAP-kinase pathway. EMBO J. 20, 4194-4203.
65. Woerfel, G. and Bindereif, A. (2001). In vitro selection of exonic splicing enhancer sequences: identification of novel CD44 enhancers. Nucleic Acids Res. 29, 3204-3211.