Antagonistic regulation of α-actinin alternative splicing by CELF proteins and polypyrimidine tract binding protein

RNA

Volumn 9, Issue 4, 2003, Pages 443-456

  Gromak, Natalia ^a   Matlin, Arianne J ^a   Cooper, Thomas A ^b   Smith, Christopher W J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Bruno like proteins; CUG BP; HnRNP; Polypyrimidine tract binding protein; PTB

Indexed keywords

ALPHA ACTININ; BINDING PROTEIN; BRUNO LIKE PROTEIN; CUG BP PROTEIN; ETR3 LIKE PROTEIN; POLYPYRIMIDINE TRACT BINDING PROTEIN; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ARTICLE; CELL TYPE; CROSS LINKING; EXON; GENE OVEREXPRESSION; L CELL; MOUSE; MUSCULAR DYSTROPHY; MYOTONIC DYSTROPHY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RNA SPLICING;

ACTININ; ALTERNATIVE SPLICING; BASE SEQUENCE; GENE EXPRESSION REGULATION; HUMANS; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; POLYPYRIMIDINE TRACT-BINDING PROTEIN; RNA PRECURSORS; RNA-BINDING PROTEINS;

ANIMALIA;

EID: 0037377379     PISSN: 13558382     EISSN: None     Source Type: Journal    
DOI: 10.1261/rna.2191903     Document Type: Article

References (58)

1. Black, D.L. 2000. Protein diversity from alternative splicing: A challenge for bioinformatics and post-genome biology. Cell 103: 367-370.
2. Blencowe, B.J. 2000. Exonic splicing enhancers: Mechanism of action, diversity and role in human genetic diseases. Trends Biochem. Sci. 25:106-110.
3. Burge, C., Tuschl, T., and Sharp, P. 1999. Splicing of precursors to mRNAs by the spliceosomes. In The RNA world, 2nd ed. (eds. R.F. Gestetland et al.), pp. 525-560. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
4. Caceres, J.F. and Kornblihtt, A.R. 2002. Alternative splicing: Multiple control mechanisms and involvement in human disease. Trends Genet. 18: 186-193.
5. Caceres, J.F., Stamm, S., Helfman, D.M., and Krainer, A.R. 1994. Regulation of alternative splicing in vivo by overexpression of antagonistic splicing factors. Science 265: 1706-1709.
6. Caputi, M., Mayeda, A., Krainer, A.R., and Zahler, A.M. 1999. hnRNP A/B proteins are required for inhibition of HIV-1 pre-mRNA splicing. EMBO J. 18: 4060-4067.
7. 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.
8. Charlet, B.N., Logan, P., Singh, G., and Cooper, T.A. 2002a. Dynamic antagonism between ETR-3 and PTB regulates cell type-specific alternative splicing. Mol. Cell 9: 649-658.
9. Charlet, B.N., Savkur, R.S., Singh, G., Philips, A.V., Grice, E.A., and Cooper, T.A. 2002b. Loss of the muscle-specific chloride channel in type 1 myotonic dystrophy due to misregulated alternative splicing. Mol. Cell 10: 45-53.
10. Choi, D.K., Ito, T., Tsukahara, F., Hirai, M., and Sakaki, Y. 1999. Developmentally regulated expression of mNapor encoding an apoptosis-induced ELAV-type RNA binding protein. Gene 237: 135-142.
11. Chou, M.-Y., Underwood, J.G., Nikolic, J., Luu, M.H.T., and Black, D.L. 2000. Multisite RNA binding and release of polypyrimidine tract binding protein during the regulation of c-src neural-specific splicing. Mol. Cell 5: 949-957.
12. Cooper, T.A. 1998. Muscle-specific splicing of a heterologous exon mediated by a single muscle-specific splicing enhancer from the cardiac troponin T gene. Mol. Cell. Biol. 18: 4519-4525.
13. Del Gatto Konczak, F., Olive, M., Gesnel, M.C., and Breathnach, R. 1999. hnRNP A1 recruited to an exon in vivo can function as an exon splicing silencer. Mol. Cell. Biol. 19: 251-260.
14. Fu, X.D. 1995. The superfamily of arginine/serine-rich splicing factors. RNA 1: 663-680.
15. Good, P.J., Chen, Q., Warner, S.J., and Herring, D.C. 2000. A family of human RNA-binding proteins related to the Drosophila Bruno translational regulator. J. Biol. Chem. 275: 28583-28592.
16. Gooding, C., Roberts, G.C., Moreau, G., Nadal Ginard, B., and Smith, C.W.J. 1994. Smooth muscle-specific switching of α-tropomyosin mutually exclusive exon selection by specific inhibition of the strong default exon. EMBO J. 13: 3861-3872.
17. Gooding, C.G., Roberts, G.C., and Smith, C.W.J. 1998. Role of an inhibitory pyrimidine-element and general pyrimidine-tract binding proteins in regulation of α-tropomyosin alternative splicing. RNA 4:85-100.
18. Graveley, B.R. 2000. Sorting out the complexity of SR protein functions. RNA 6: 1197-1211.
19. -. 2001. Alternative splicing: Increasing diversity in the proteomic world. Trends Genet. 17: 100-107.
20. Gromak, N. and Smith, C.W. 2002. A splicing silencer that regulates smooth muscle specific alternative splicing is active in multiple cell types. Nucleic Acids Res. 30: 3548-3557.
21. Hunt, S.L., Hsuan, J.J., Totty, N., and Jackson, R.J. 1999. Unr, a cellular cytoplasmic RNA-binding protein with five cold shock domains, is required for internal initiation of translation of human rhinovirus RNA. Genes & Dev. 13: 437-448.
22. Jensen, K.B., Dredge, B.K., Stefani, G., Zhong, R., Buckanovich, R.J., Okano, H.J., Yang, Y.Y., and Darnell, R.B. 2000. Nova-1 regulates neuron-specific alternative splicing and is essential for neuronal viability [see comments]. Neuron 25: 359-371.
23. Krecic, A.M. and Swanson, M.S. 1999. hnRNP complexes: Composition, structure, and function. Curr. Opin. Cell. Biol. 11: 363-371.
24. Kremerskothen, J., Teber, I., Wendholt, D., Liedtke, T., Böckers, T.M., and Bernekow, A. 2002. Brain-specific splicing of a-actinin 1 mRNA. Biochem. Biophys. Res. Commun. 295: 678-681.
25. Ladd, A.N., Charlet-B.N., and Cooper, T.A. 2001. The CELF family of RNA binding proteins is implicated in cell-specific and developmentally regulated alternative splicing. Mol. Cell. Biol. 21: 1285-1296.
26. Lin, C.H. and Patton, J.G. 1995. Regulation of alternative 3′ splice site selection by constitutive splicing factors. RNA 1: 234-245.
27. Lopez, A.J. 1998. Alternative splicing of pre-mRNA: Developmental consequences and mechanisms of regulation. Annu. Rev. Genet. 32: 279-305.
28. Lu, X., Timchenko, N.A., and Timchenko, L.T. 1999. Cardiac elav-type RNA-binding protein (ETR-3) binds to RNA CUG repeats expanded in myotonic dystrophy. Hum. Mol. Genet. 8: 53-60.
29. Maniatis, T. and Tasic, B. 2002. Alternative pre-mRNA splicing and proteome expansion in metazoans. Nature 418: 236-243.
30. 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 ClC-1 chloride channel pre-mRNA and hyperexcitability of skeletal muscle in myotonic dystrophy. Mol. Cell 10: 35-44.
31. Markovtsov, V., Nikolic, J.M., Goldman, J.A., Turck, C.W., Chou, M.-Y., and Black, D.L. 2000. Cooperative assembly of an hnRNP complex induced by a tissue-specific homolog of polypyrimidine tract binding protein. Mol. Cell. Biol. 20: 7463-7479.
32. McAfee, J.G., Huang, M., Soltaninassab, S., Rech, J.E., Iyengar, S., and Lesturgeon, W.M. 1997. The packaging of pre-mRNA. In Eukaryotic mRNA processing (ed. A.R. Krainer), pp. 68-102. Oxford University Press, Oxford/New York.
33. Modrek, B. and Lee, C. 2002. A genomic view of alternative splicing. Nat. Genet. 30: 13-19.
34. Moore, M.J. and Query, C.C. 1998. Uses of site-specifically modified RNAs constructed by RNA ligation. In RNA protein interactions: A practical approach (ed. C.W.J. Smith), Vol. 192, pp. 75-108. Oxford University Press, Oxford.
35. Perez, I., Lin, C.-H., McAfee, J.G., and Patton, J.G. 1997. Mutation of PTB binding sites causes misregulation of alternative 3′ splice site selection in vivo. RNA 3: 764-778.
36. Philips, A.V., Timchenko, L.T., and Cooper, T.A. 1998. Disruption of splicing regulated by a CUG-binding protein in myotonic dystrophy [see comments]. Science 280: 737-741.
37. Polydorides, A.D., Okano, H.J., Yang, Y.Y., Stefani, G., and Darnell, R.B. 2000. A brain-enriched polypyrimidine tract-binding protein antagonizes the ability of Nova to regulate neuron-specific alternative splicing. Proc. Natl. Acad. Sci. 97: 6350-6355.
38. Reed, R. 2000. Mechanisms of fidelity in pre-mRNA splicing. Curr. Opin. Cell. Biol. 12: 340-345.
39. Roberts, G.C. and Smith, C.W. 2002. Alternative splicing: Combinatorial output from the genome. Curr. Opin. Chem. Biol. 6: 375-383.
40. Sambrook, J., Fritsch, E.F., and Maniatis, T. 1989. Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
41. 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.
42. Scadden, A.D.J. and Smith, C.W.J. 1995. Interactions between the terminal bases of mammalian introns are retained in inosine-containing pre-mRNAs. EMBO J. 14: 3236-3246.
43. Singh, R., Valcarcel, J., and Green, M.R. 1995. Distinct binding specificities and functions of higher eukaryotic polypyrimidine tract-binding proteins. Science 268: 1173-1176.
44. Smith, C.W.J. and Valcárcel, J. 2000. Alternative pre-mRNA splicing: The logic of combinatorial control. Trends Biochem. Sci. 25: 381-388.
45. Smith, C.W.J., Gooding, C., Roberts, G.C., and Scadden, A.D.J. 1996. Analyzing patterns of alternative splicing. In A laboratory guide to RNA. Isolation, analysis and synthesis (ed. P.A. Kreig), pp. 411-440. John Wiley & Sons, Inc., New York.
46. Southby, J., Gooding, C., and Smith, C.W. 1999. Polypyrimidine tract binding protein functions as a repressor to regulate alternative splicing of α-actinin mutally exclusive exons. Mol. Cell. Biol. 19: 2699-2711.
47. Suzuki, H., Jin, Y., Otani, H., Yasuda, K., and Inoue, K. 2002. Regulation of alternative splicing of α-actinin transcript by Bruno-like proteins. Genes Cells 7: 133-141.
48. Takahashi, N., Sasagawa, N., Suzuki, K., and Ishiura, S. 2000. The CUG-binding protein binds specifically to UG dinucleotide repeats in a yeast three-hybrid system [In Process citation]. Biochem. Biophys. Res. Commun. 277: 518-523.
49. Timchenko, L.T., Miller, J.W., Timchenko, N.A., DeVore, D.R., Datar, K.V., Lin, L., Roberts, R., Caskey, C.T., and Swanson, M.S. 1996a. Identification of a (CUG)n triplet repeat RNA-binding protein and its expression in myotonic dystrophy. Nucleic Acids Res. 24: 4407-4414.
50. Timchenko, L.T., Timchenko, N.A., Caskey, C.T., and Roberts, R. 1996b. Novel proteins with binding specificity for DNA CTG repeats and RNA CUG repeats: Implications for myotonic dystrophy. Hum. Mol. Genet. 5: 115-121.
51. Valcarcel, J. and Gebauer, F. 1997. Post-transcriptional regulation: The dawn of PTB. Curr. Biol. 7: R705-R708.
52. Wagner, E.J. and Garcia-Blanco, M.A. 2001. Polypyrimidine tract binding protein antagonizes exon definition. Mol. Cell. Biol. 21: 3281-3288.
53. -. 2002. RNAi-mediated PTB depletion leads to enhanced exon definition. Mol. Cell 10: 943-949.
54. Waites, G.T., Graham, I.R., Jackson, P., Millake, D.B., Patel, B., Blanchard, A.D., Weller, P.A., Eperon, I.C., and Critchley, D.R. 1992. Mutually exclusive splicing of calcium-binding domain exons in chick α-actinin. J. Biol. Chem. 267: 6263-6271.
55. Wollerton, M., Gooding, C., Robinson, F., Brown, E., Jackson, R., and Smith, C. 2001. Differential alternative splicing activity of isoforms of polypyrimidine tract binding protein. RNA 7: 819-832.
56. Zhang, L., Liu, W., and Grabowski, P.J. 1999. Coordinate repression of a trio of neuron-specific splicing events by the splicing regulator PTB. RNA 5:117-130.
57. Zhang, W., Liu, H., Han, K., and Grabowski, P.J. 2002. Region-specific alternative splicing in the nervous system: Implications for regulation by the RNA-binding protein NAPOR. RNA 8: 671-685.
58. Zhu, J., Mayeda, A., and Krainer, A.R. 2001. Exon identity established through differential antagonism between exonic splicing silencer-bound hnRNP Al and enhancer-bound SR proteins. Mol. Cell 8:1351-1361.