FUBP1: A new protagonist in splicing regulation of the DMD gene

Nucleic Acids Research

Volumn 43, Issue 4, 2015, Pages 2378-2389

  Miro, Julie ^a,b   Laaref, Abdelhamid Mahdi ^a,b,h   Rofidal, Valerie ^c   Lagrafeuille, Rosyne ^a,b,i   Hem, Sonia ^c   Thorel, Delphine ^d   Mechin, Deborah ^d   Mamchaoui, Kamel ^e,f,g   Mouly, Vincent ^e,f,g   Claustres, Mireille ^a,b,d   Tuffery Giraud, Sylvie ^a,b  

^a UNIV MONTPELLIER   (France)

^b INSERM   (France)

^c CEMAGREF   (France)

^d HÔPITAL ARNAUD DE VILLENEUVE   (France)

^e SORBONNE UNIVERSITÉ   (France)

^f Sorbonne Université   (France)

^g University of Versailles Saint Quentin en Yvelines   (France)

^h INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

ⁱ UNIVERSITÉ BLAISE PASCAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DMD PROTEIN, HUMAN; DNA BINDING PROTEIN; DNA HELICASE; DYSTROPHIN; FUBP1 PROTEIN, HUMAN; REGULATORY RNA SEQUENCE; RNA BINDING PROTEIN; STOP CODON;

ALTERNATIVE RNA SPLICING; BINDING SITE; CELL LINE; EXON; GENETICS; HUMAN; INTRON; METABOLISM; PHYSIOLOGY; REGULATORY RNA SEQUENCE; STOP CODON;

ALTERNATIVE SPLICING; BINDING SITES; CELL LINE; CODON, NONSENSE; DNA HELICASES; DNA-BINDING PROTEINS; DYSTROPHIN; EXONS; HUMANS; INTRONS; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RNA-BINDING PROTEINS;

EID: 84941101710     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv086     Document Type: Article

References (43)

1. Lee, Y., Gamazon, E.R., Rebman, E., Lee, Y., Lee, S., Dolan, M.E., Cox, N.J., Lussier, Y.A. (2012) Variants affecting exon skipping contribute to complex traits. PLoS Genet., 8, e1002998.
2. Cooper, T.A., Wan, L., Dreyfuss, G. (2009) RNA and disease. Cell, 136, 777-793.
3. Braunschweig, U., Gueroussov, S., Plocik, A.M., Graveley, B.R., Blencowe, B.J. (2013) Dynamic integration of splicing within gene regulatory pathways. Cell, 152, 1252-1269.
4. Barash, Y., Calarco, J.A., Gao, W., Pan, Q., Wang, X., Shai, O., Blencowe, B.J., Frey, B.J. (2010) Deciphering the splicing code. Nature, 465, 53-59.
5. Long, J.C., Caceres, J.F. (2009) The SR protein family of splicing factors: master regulators of gene expression. Biochem. J., 417, 15-27.
6. Smith, C.W., Valcárcel, J. (2000) Alternative pre-mRNA splicing: the logic of combinatorial control. Trends Biochem. Sci., 25, 381-388.
7. Dreyfuss, G., Kim, V.N., Kataoka, N. (2002) Messenger-RNA-binding proteins and the messages they carry. Nat. Rev. Mol. Cell Biol., 3, 195-205.
8. Tuffery-Giraud, S., Béroud, C., Leturcq, F., Yaou, R.B., Hamroun, D., Michel-Calemard, L., Moizard, M.-P., Bernard, R., Cosseé, M., Boisseau, P. et al. (2009) Genotype-phenotype analysis in 2, 405 patients with a dystrophinopathy using the UMD-DMD database: a model of nationwide knowledgebase. Hum. Mutat., 30, 934-945.
9. Flanigan, K.M., Dunn, D.M., von Niederhausern, A., Soltanzadeh, P., Howard, M.T., Sampson, J.B., Swoboda, K.J., Bromberg, M.B., Mendell, J.R., Taylor, L.E. et al. (2011) Nonsense mutation-associated Becker muscular dystrophy: interplay between exon definition and splicing regulatory elements within the DMD gene. Hum. Mutat., 32, 299-308.
10. Nishiyama, A., Takeshima, Y., Zhang, Z., Habara, Y., Tran, T.H.T., Yagi, M., Matsuo, M. (2008) Dystrophin nonsense mutations can generate alternative rescue transcripts in lymphocytes. Ann. Hum. Genet., 72, 717-724.
11. Shiga, N., Takeshima, Y., Sakamoto, H., Inoue, K., Yokota, Y., Yokoyama, M., Matsuo, M. (1997) Disruption of the splicing enhancer sequence within exon 27 of the dystrophin gene by a nonsense mutation induces partial skipping of the exon and is responsible for Becker muscular dystrophy. J. Clin. Invest., 100, 2204-2210.
12. Ginjaar, I.B., Kneppers, A.L., Meulen, J.D., Anderson, L.V., Bremmer-Bout, M., van Deutekom, J.C., Weegenaar, J., den Dunnen, J.T., Bakker, E. (2000) Dystrophin nonsense mutation induces different levels of exon 29 skipping and leads to variable phenotypes within one BMD family. Eur. J. Hum. Genet., 8, 793-796.
13. Fajkusová, L., Lukás, Z., Tvrdková, M., Kuhrová, V., Hájek, J., Fajkus, J. (2001) Novel dystrophin mutations revealed by analysis of dystrophin mRNA: alternative splicing suppresses the phenotypic effect of a nonsense mutation. Neuromuscul. Disord., 11, 133-138.
14. Tran, V.K., Takeshima, Y., Zhang, Z., Yagi, M., Nishiyama, A., Habara, Y., Matsuo, M. (2006) Splicing analysis disclosed a determinant single nucleotide for exon skipping caused by a novel intraexonic four-nucleotide deletion in the dystrophin gene. J. Med. Genet., 43, 924-930.
15. Fairclough, R.J., Wood, M.J., Davies, K.E. (2013) Therapy for Duchenne muscular dystrophy: renewed optimism from genetic approaches. Nat. Rev. Genet., 14, 373-378.
16. Tuffery-Giraud, S., Saquet, C., Thorel, D., Disset, A., Rivier, F., Malcolm, S., Claustres, M. (2005) Mutation spectrum leading to an attenuated phenotype in dystrophinopathies. Eur. J. Hum. Genet., 13, 1254-1260.
17. Mamchaoui, K., Trollet, C., Bigot, A., Negroni, E., Chaouch, S., Wolff, A., Kandalla, P.K., Marie, S., Di Santo, J., St Guily, J.L. et al. (2011) Immortalized pathological human myoblasts: towards a universal tool for the study of neuromuscular disorders. Skelet. Muscle, 1, 34.
18. Skoko, N., Baralle, M., Buratti, E., Baralle, F.E. (2008) The pathological splicing mutation c.6792C>G in NF1 exon 37 causes a change of tenancy between antagonistic splicing factors. FEBS Lett., 582, 2231-2236.
19. Li, H., Wang, Z., Zhou, X., Cheng, Y., Xie, Z., Manley, J.L., Feng, Y. (2013) Far upstream element-binding protein 1 and RNA secondary structure both mediate second-step splicing repression. Proc. Natl. Acad. Sci. U.S.A., 110, E2687-E2695.
20. Le Guédard-Méreuze, S., Vaché, C., Molinari, N., Vaudaine, J., Claustres, M., Roux, A.-F., Tuffery-Giraud, S. (2009) Sequence contexts that determine the pathogenicity of base substitutions at position +3 of donor splice-sites. Hum. Mutat., 30, 1329-1339.
21. Thompson, J.R., Marcelino, L.A., Polz, M.F. (2002) Heteroduplexes in mixed-template amplifications : formation, consequence and elimination by "reconditioning PCR". RNA, 30, 2083-2088.
22. Cavaloc, Y., Bourgeois, C.F., Kister, L., Stévenin, J. (1999) The splicing factors 9G8 and SRp20 transactivate splicing through different and specific enhancers. RNA, 5, 468-483.
23. Venables, J.P., Bourgeois, C.F., Dalgliesh, C., Kister, L., Stevenin, J., Elliott, D.J. (2005) Up-regulation of the ubiquitous alternative splicing factor Tra2beta causes inclusion of a germ cell-specific exon. Hum. Mol. Genet., 14, 2289-2303.
24. Michlewski, G., Cáceres, J.F. (2010) RNase-assisted RNA chromatography. RNA, 16, 1673-1678.
25. Pavlidis, P., Noble, W.S. (2003) Matrix2png: a utility for visualizing matrix data. Bioinformatics, 19, 295-296.
26. Goina, E., Skoko, N., Pagani, F. (2008) Binding of DAZAP1 and hnRNPA1/A2 to an exonic splicing silencer in a natural BRCA1 exon 18 mutant. Mol. Cell. Biol., 28, 3850-3860.
27. Zhang, J., Chen, Q.M. (2013) Far upstream element binding protein 1: a commander of transcription, translation and beyond. Oncogene, 32, 2907-2916.
28. Braddock, D.T., Louis, J.M., Baber, J.L., Levens, D., Clore, G.M. (2002) Structure and dynamics of KH domains from FBP bound to single-stranded DNA. Nature, 415, 1051-1056.
29. Benjamin, L.R., Chung, H., Sanford, S., Kouzine, F., Liu, J., Levens, D. (2008) Hierarchical mechanisms build the DNA-binding specificity of FUSE binding protein. Proc Natl Acad Sci U.S.A., 105, 18296-18301.
30. Sterne-Weiler, T., Howard, J., Mort, M., Cooper, D.N., Sanford, J.R. (2011) Loss of exon identity is a common mechanism of human inherited disease. Genome Res., 21, 1563-1571.
31. Haque, A., Buratti, E., Baralle, F.E. (2010) Functional properties and evolutionary splicing constraints on a composite exonic regulatory element of splicing in CFTR exon 12. Nucleic Acids Res., 38, 647-659.
32. Disset, A., Bourgeois, C.F., Benmalek, N., Claustres, M., Stevenin, J., Tuffery-Giraud, S. (2006) An exon skipping-associated nonsense mutation in the dystrophin gene uncovers a complex interplay between multiple antagonistic splicing elements. Hum. Mol. Genet., 15, 999-1013.
33. Burd, C.G., Dreyfuss, G. (1994) RNA binding specificity of hnRNP A1: significance of hnRNP A1 high-affinity binding sites in pre-mRNA splicing. EMBO J., 13, 1197-1204.
34. Chen, M., Manley, J.L. (2009) Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat. Rev. Mol. Cell Biol., 10, 741-754.
35. Chen, H.-Y., Yu, Y.-H., Yen, P.H. (2013) DAZAP1 regulates the splicing of Crem, Crisp2 and Pot1a transcripts. Nucleic Acids Res., 41, 9858-9869.
36. Wang, Y., Ma, M., Xiao, X., Wang, Z. (2012) Intronic splicing enhancers, cognate splicing factors and context-dependent regulation rules. Nat. Struct. Mol. Biol., 19, 1044-1052.
37. Choudhury, R., Roy, S.G., Tsai, Y.S., Tripathy, A., Graves, L.M., Wang, Z. (2014) The splicing activator DAZAP1 integrates splicing control into MEK/Erk-regulated cell proliferation and migration. Nat. Commun., 5, 3078.
38. Wang, G.-S., Cooper, T.A. (2007) Splicing in disease: disruption of the splicing code and the decoding machinery. Nat. Rev. Genet., 8, 749-761.
39. Jacob, A.G., Singh, R.K., Mohammad, F., Bebee, T.W., Chandler, D.S. (2014) The splicing factor FUBP1 is required for the efficient splicing of oncogene MDM2 pre-mRNA. J. Biol. Chem., 289, 17350-17364.
40. Davis-Smyth, T., Duncan, R.C., Zheng, T., Michelotti, G., Levens, D. (1996) The far upstream element-binding proteins comprise an ancient family of single-strand DNA-binding transactivators. J. Biol. Chem., 271, 31679-31687.
41. Valverde, R., Edwards, L., Regan, L. (2008) Structure and function of KH domains. FEBS J., 275, 2712-2726.
42. Garcá-Mayoral, M.F., Hollingworth, D., Masino, L., Dáz-Moreno, I., Kelly, G., Gherzi, R., Chou, C.-F., Chen, C.-Y., Ramos, A. (2007) The structure of the C-terminal KH domains of KSRP reveals a noncanonical motif important for mRNA degradation. Structure, 15, 485-498.
43. Lorain, S., Peccate, C., Le Hir, M., Griffith, G., Philippi, S., Précigout, G., Mamchaoui, K., Jollet, A., Voit, T., Garcia, L. (2013) Dystrophin rescue by trans-splicing: a strategy for DMD genotypes not eligible for exon skipping approaches. Nucleic Acids Res., 41, 8391-8402.