MBNL1 and PTB cooperate to repress splicing of Tpm1 exon 3

Nucleic Acids Research

Volumn 41, Issue 9, 2013, Pages 4765-4782

  Gooding, Clare ^a   Edge, Christopher ^a   Lorenz, Mike ^b   Coelho, Miguel B ^a   Winters, Mikael ^a   Kaminski, Clemens F ^a   Cherny, Dmitry ^c   Eperon, Ian C ^c   Smith, Christopher W J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^c UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TROPOMYOSIN; MUSCLEBIND LIKE PROTEIN 1; POLYPYRIMIDINE TRACT BINDING PROTEIN; RNA; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; EXON; GENE REPRESSION; IN VITRO STUDY; IN VIVO STUDY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RNA SPLICING; TPM1 GENE;

ALTERNATIVE SPLICING; ANIMALS; CELL LINE; EXONS; HUMANS; MUSCLE, SMOOTH; POLYPYRIMIDINE TRACT-BINDING PROTEIN; RATS; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RNA, MESSENGER; RNA-BINDING PROTEINS; TROPOMYOSIN;

EID: 84877313310     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt168     Document Type: Article

References (55)

1. Wang, E.T., Sandberg, R., Luo, S., Khrebtukova, I., Zhang, L., Mayr, C., Kingsmore, S.F., Schroth, G.P. and Burge, C.B. (2008) Alternative isoform regulation in human tissue transcriptomes. Nature, 456, 470-476.
2. Pan, Q., Shai, O., Lee, L.J., Frey, B.J. and Blencowe, B.J. (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat. Genet., 40, 1413-1415.
3. Nilsen, T.W. and Graveley, B.R. (2010) Expansion of the eukaryotic proteome by alternative splicing. Nature, 463, 457-463.
4. Chen, M. and Manley, J.L. (2009) Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat. Rev. Mol. Cell Biol., 10, 741-754.
5. Matlin, A.J., Clark, F. and Smith, C.W. (2005) Understanding alternative splicing: towards a cellular code. Nat. Rev. Mol. Cell Biol., 6, 386-398.
6. Witten, J.T. and Ule, J. (2011) Understanding splicing regulation through RNA splicing maps. Trends Genet., 27, 89-97.
7. Li, Q., Lee, J.A. and Black, D.L. (2007) Neuronal regulation of alternative pre-mRNA splicing. Nat. Rev. Neurosci., 8, 819-831.
8. Llorian, M. and Smith, C.W. (2011) Decoding muscle alternative splicing. Curr. Opin. Genet. Dev., 21, 380-387.
9. Gooding, C. and Smith, C.W. (2008) Tropomyosin exons as models for alternative splicing. Adv. Exp. Med. Biol., 644, 27-42.
10. Wieczorek, D.F., Smith, C.W. and Nadal-Ginard, B. (1988) The rat alpha-tropomyosin gene generates a minimum of six different mRNAs coding for striated, smooth, and nonmuscle isoforms by alternative splicing. Mol. Cell Biol., 8, 679-694.
11. Ellis, P.D., Smith, C.W. and Kemp, P. (2004) Regulated tissue-specific alternative splicing of enhanced green fluorescent protein transgenes conferred by alpha-tropomyosin regulatory elements in transgenic mice. J. Biol. Chem., 279, 36660-36669.
12. Mullen, M.P., Smith, C.W., Patton, J.G. and Nadal-Ginard, B. (1991) Alpha-tropomyosin mutually exclusive exon selection: competition between branchpoint/polypyrimidine tracts determines default exon choice. Genes Dev., 5, 642-655.
13. Rothman, A., Kulik, T.J., Taubman, M.B., Berk, B.C., Smith, C.W. and Nadal-Ginard, B. (1992) Development and characterization of a cloned rat pulmonary arterial smooth muscle cell line that maintains differentiated properties through multiple subcultures. Circulation, 86, 1977-1986.
14. Gooding, C., Roberts, G.C., Moreau, G., Nadal-Ginard, B. and Smith, C.W. (1994) Smooth muscle-specific switching of alpha-tropomyosin mutually exclusive exon selection by specific inhibition of the strong default exon. EMBO J., 13, 3861-3872.
15. Smith, C.W. and Nadal-Ginard, B. (1989) Mutually exclusive splicing of alpha-tropomyosin exons enforced by an unusual lariat branch point location: implications for constitutive splicing. Cell, 56, 749-758.
16. 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.
17. 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.
18. Gooding, C., Roberts, G.C. and Smith, C.W. (1998) Role of an inhibitory pyrimidine element and polypyrimidine tract binding protein in repression of a regulated alpha-tropomyosin exon. RNA, 4, 85-100.
19. Wollerton, M.C., Gooding, C., Robinson, F., Brown, E.C., Jackson, R.J. and Smith, C.W. (2001) Differential alternative splicing activity of isoforms of polypyrimidine tract binding protein (PTB). RNA, 7, 819-832.
20. Cherny, D., Gooding, C., Eperon, G.E., Coelho, M.B., Bagshaw, C.R., Smith, C.W. and Eperon, I.C. (2010) Stoichiometry of a regulatory splicing complex revealed by single-molecule analyses. EMBO J., 29, 2161-2172.
21. Roberts, G.C., Gooding, C. and Smith, C.W. (1996) Smooth muscle alternative splicing induced in fibroblasts by heterologous expression of a regulatory gene. EMBO J., 15, 6301-6310.
22. Huttelmaier, S., Illenberger, S., Grosheva, I., Rudiger, M., Singer, R.H. and Jockusch, B.M. (2001) Raver1, a dual compartment protein, is a ligand for PTB/hnRNPI and microfilament attachment proteins. J. Cell Biol., 155, 775-786.
23. Gromak, N., Rideau, A., Southby, J., Scadden, A.D., Gooding, C., Huttelmaier, S., Singer, R.H. and Smith, C.W. (2003) The PTB interacting protein raver1 regulates alpha-tropomyosin alternative splicing. EMBO J., 22, 6356-6364.
24. Rideau, A.P., Gooding, C., Simpson, P.J., Monie, T.P., Lorenz, M., Huttelmaier, S., Singer, R.H., Matthews, S., Curry, S. and Smith, C.W. (2006) A peptide motif in Raver1 mediates splicing repression by interaction with the PTB RRM2 domain. Nat. Struct. Mol. Biol., 13, 839-848.
25. Joshi, A., Coelho, M.B., Kotik-Kogan, O., Simpson, P.J., Matthews, S.J., Smith, C.W.J. and Curry, S. (2011) Crystallographic analysis of polypyrimidine tract-binding protein-Raver1 interactions involved in regulation of alternative splicing. Structure, 19, 1816-1825.
26. Lee, J.H., Rangarajan, E.S., Yogesha, S.D. and Izard, T. (2009) Raver1 interactions with vinculin and RNA suggest a feed-forward pathway in directing mRNA to focal adhesions. Structure, 17, 833-842.
27. Lahmann, I., Fabienke, M., Henneberg, B., Pabst, O., Vauti, F., Minge, D., Illenberger, S., Jockusch, B.M., Korte, M. and Arnold, H.H. (2008) The hnRNP and cytoskeletal protein raver1 contributes to synaptic plasticity. Exp. Cell Res., 314, 1048-1060.
28. Ladd, A.N., Charlet, 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.
29. Hino, S., Kondo, S., Sekiya, H., Saito, A., Kanemoto, S., Murakami, T., Chihara, K., Aoki, Y., Nakamori, M., Takahashi, M.P. et al. (2007) Molecular mechanisms responsible for aberrant splicing of SERCA1 in myotonic dystrophy type 1. Hum. Mol. Genet., 16, 2834-2843.
30. Ho, T.H., Charlet, B.N., Poulos, M.G., Singh, G., Swanson, M.S. and Cooper, T.A. (2004) Muscleblind proteins regulate alternative splicing. EMBO J., 23, 3103-3112.
31. Kino, Y., Washizu, C., Oma, Y., Onishi, H., Nezu, Y., Sasagawa, N., Nukina, N. and Ishiura, S. (2009) MBNL and CELF proteins regulate alternative splicing of the skeletal muscle chloride channel CLCN1. Nucleic Acids Res., 37, 6477-6490.
32. Warf, M.B. and Berglund, J.A. (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.
33. Yuan, Y., Compton, S.A., Sobczak, K., Stenberg, M.G., Thornton, C.A., Griffith, J.D. and Swanson, M.S. (2007) Muscleblind-like 1 interacts with RNA hairpins in splicing target and pathogenic RNAs. Nucleic Acids Res., 35, 5474-5486.
34. Kalsotra, A., Xiao, X., Ward, A.J., Castle, J.C., Johnson, J.M., Burge, C.B. and Cooper, T.A. (2008) A postnatal switch of CELF and MBNL proteins reprograms alternative splicing in the developing heart. Proc. Natl Acad. Sci. USA, 105, 20333-20338.
35. He, F., Dang, W., Abe, C., Tsuda, K., Inoue, M., Watanabe, S., Kobayashi, N., Kigawa, T., Matsuda, T., Yabuki, T. et al. (2009) Solution structure of the RNA binding domain in the human muscleblind-like protein 2. Protein Sci., 18, 80-91.
36. Teplova, M. and Patel, D.J. (2008) Structural insights into RNA recognition by the alternative-splicing regulator muscleblind-like MBNL1. Nat. Struct. Mol. Biol., 15, 1343-1351.
37. Miller, J.W., Urbinati, C.R., Teng-Umnuay, P., Stenberg, M.G., Byrne, B.J., Thornton, C.A. and Swanson, M.S. (2000) Recruitment of human muscleblind proteins to (CUG)(n) expansions associated with myotonic dystrophy. EMBO J., 19, 4439-4448.
38. Du, H., Cline, M.S., Osborne, R.J., Tuttle, D.L., Clark, T.A., Donohue, J.P., Hall, M.P., Shiue, L., Swanson, M.S., Thornton, C.A. et al. (2010) Aberrant alternative splicing and extracellular matrix gene expression in mouse models of myotonic dystrophy. Nat. Struct. Mol. Biol., 17, 187-193.
39. Wang, E.T., Cody, N.A., Jog, S., Biancolella, M., Wang, T.T., Treacy, D.J., Luo, S., Schroth, G.P., Housman, D.E., Reddy, S. et al. (2012) Transcriptome-wide regulation of pre-mRNA splicing and mRNA localization by muscleblind proteins. Cell, 150, 710-724.
40. Goers, E.S., Purcell, J., Voelker, R.B., Gates, D.P. and Berglund, J.A. (2010) MBNL1 binds GC motifs embedded in pyrimidines to regulate alternative splicing. Nucleic Acids Res., 38, 2467-2484.
41. Cass, D., Hotchko, R., Barber, P., Jones, K., Gates, D.P. and Berglund, J.A. (2011) The four Zn fingers of MBNL1 provide a flexible platform for recognition of its RNA binding elements. BMC Mol. Biol., 12, 20.
42. Gooding, C., Clark, F., Wollerton, M.C., Grellscheid, S.N., Groom, H. and Smith, C.W. (2006) A class of human exons with predicted distant branch points revealed by analysis of AG dinucleotide exclusion zones. Genome Biol., 7, R1.
43. Cazalla, D., Sanford, J.R. and Caceres, J.F. (2005) A rapid and efficient protocol to purify biologically active recombinant proteins from mammalian cells. Protein Expr. Purif., 42, 54-58.
44. 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.
45. Robinson, F. and Smith, C.W. (2006) A splicing repressor domain in polypyrimidine tract-binding protein. J. Biol. Chem., 281, 800-806.
46. Dignam, J.D., Lebovitz, R.M. and Roeder, R.G. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res., 11, 1475-1489.
47. Lorenz, M. (2009) Visualizing protein-RNA interactions inside cells by fluorescence resonance energy transfer. RNA, 15, 97-103.
48. Barash, Y., Calarco, J.A., Gao, W., Pan, Q., Wang, X., Shai, O., Blencowe, B.J. and Frey, B.J. (2010) Deciphering the splicing code. Nature, 465, 53-59.
49. Llorian, M., Schwartz, S., Clark, T.A., Hollander, D., Tan, L.Y., Spellman, R., Gordon, A., Schweitzer, A.C., de la Grange, P., Ast, G. et al. (2010) Position-dependent alternative splicing activity revealed by global profiling of alternative splicing events regulated by PTB. Nat. Struct. Mol. Biol., 17, 1114-1123.
50. Charlet, B.N., Logan, P., Singh, G. and Cooper, T.A. (2002) Dynamic antagonism between ETR-3 and PTB regulates cell type-specific alternative splicing. Mol. Cell, 9, 649-658.
51. Warf, M.B., Diegel, J.V., von Hippel, P.H. and Berglund, J.A. (2009) The protein factors MBNL1 and U2AF65 bind alternative RNA structures to regulate splicing. Proc. Natl Acad. Sci. USA, 106, 9203-9208.
52. Paul, S., Dansithong, W., Kim, D., Rossi, J., Webster, N.J., Comai, L. and Reddy, S. (2006) Interaction of muscleblind, CUG-BP1 and hnRNP H proteins in DM1-associated aberrant IR splicing. EMBO J., 25, 4271-4283.
53. Grammatikakis, I., Goo, Y.H., Echeverria, G.V. and Cooper, T.A. (2011) Identification of MBNL1 and MBNL3 domains required for splicing activation and repression. Nucleic Acids Res., 39, 2769-2780.
54. Tran, H., Gourrier, N., Lemercier-Neuillet, C., Dhaenens, C.M., Vautrin, A., Fernandez-Gomez, F.J., Arandel, L., Carpentier, C., Obriot, H., Eddarkaoui, S. et al. (2011) Analysis of exonic regions involved in nuclear localization, splicing activity, and dimerization of muscleblind-like-1 isoforms. J. Biol. Chem., 286, 16435-16446.
55. Pascual, M., Vicente, M., Monferrer, L. and Artero, R. (2006) The muscleblind family of proteins: an emerging class of regulators of developmentally programmed alternative splicing. Differentiation, 74, 65-80.