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

Journal of Clinical Investigation

Volumn 100, Issue 9, 1997, Pages 2204-2210

  Shiga, Nobuyuki ^a   Takeshima, Yasuhiro ^a   Sakamoto, Hiroshi ^a   Inoue, Kunio ^b   Yokota, Yoshiyuki ^a   Yokoyama, Mitsuhiro ^a   Matsuo, Masafumi ^a  

^a KOBE UNIVERSITY   (Japan)

^b NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

Dilated cardiomyopathy; In vitro splicing; Polypurine; Pre mRNA; Reading frame

Indexed keywords

MESSENGER RNA; OLIGONUCLEOTIDE;

ADULT; ARTICLE; BECKER MUSCULAR DYSTROPHY; CASE REPORT; ENHANCER REGION; EXON; GENE DISRUPTION; HUMAN; MALE; NONSENSE MUTATION; PRIORITY JOURNAL; RNA SPLICING;

EID: 0030725216     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119757     Document Type: Article

References (44)

1. Green, M.R. 1986. Pre-mRNA splicing. Annu. Rev. Genet. 20:671-708.
2. Watakabe, A., K. Tanaka, and Y. Shimura. 1993. The role of exon sequences in splice site selection. Genes Dev. 7:407-418.
3. Tanaka, K., A. Watakabe, and Y. Shimura. 1994. Polypurine sequences within a downstream exon function as a splicing enhancer. Mol. Cell. Biol. 14: 1347-1354.
4. Tian, M., and T. Maniatis. 1994. A splicing enhancer exhibits both constitutive and regulated activities. Genes Dev. 8:1703-1712.
5. Yeakley, J.M., J.-P. Morfin, M.G. Rosenfeld, and X.-D. Fu. 1996. A complex of nuclear proteins mediates SR protein binding to a purine-rich splicing enhancer. Proc. Natl. Acad. Sci. USA. 96:7582-7587.
6. Tacke, R., and J.L. Manley. 1995. The human splicing factors ASF/SF2 and SC35 possess distinct, functionally significant RNA binding specificities. EMBO (Eur. Mol. Biol. Organ.) J. 14:3540-3551.
7. Krawczak, M., J. Reiss, and D.N. Cooper. 1992. The mutational spectrum of single base-pair substitutions in mRNA splice junctions of human genes: causes and consequences. Hum. Genet. 90:41-54.
8. Dietz, H.C., D. Valle, C.A. Francomano, R.J. Kendzior, R.E. Pyeritz, and G.R. Cutting. 1993. The skipping of constitutive exons in vivo induced by nonsense mutations. Science (Wash. DC). 259:680-683.
9. Naylor, J.A., P.M. Green, C.R. Rizza, and F. Giannelli. 1992. Analysis of factor VIII mRNA reveals defects in every one of 28 haemophilia A patients. Hum. Mol. Genet. 2:11-17.
10. Gibson, R., A. Hajiapour, M. Murer-Orland, M. Buchwald, and C. Mathew. 1993. A nonsense mutation and exon skipping in the Fancomi anaemia group C gene. Hum. Mol. Genet. 2:797-799.
11. Bach, G., S.M. Moskowitz, P.T. Tieu, A. Matynia, and E.F. Neufeld. 1993. Molecular analysis of hurler syndrome in Druze and Muslim Arab patients in Israel: multiple allelic mutations of the IDUA gene in a small geographic area. Am. J. Hum. Genet. 53:330-338.
12. Das, S., B. Levinson, S. Whieney, C. Vulpe, S. Packman, and J. Gitschier. 1994. Diverse mutations in patients with Menkes disease often lead to exon skipping. Am. J. Hum. Genet. 55:883-889.
13. Hull, J., S. Shackleton, and A. Harris. 1994. The stop mutation R553X in the CFTR gene results in exon skipping. Genomics. 19:362-364.
14. Santisteban, I., F.X. Arredondo-Vega, S. Kelly, M. Loubser, N. Meydan, C. Roifman, P.L. Howell, T. Bowen, K.I. Weinberg, M.L. Schroeder, and M. Hershfield. 1995. Three new adenosine deaminase mutations that define a splicing enhancer and cause severe and partial phenotypes: implications for evolution of a CpG hotspot and expression of a transduced ADA cDNA. Hum. Mol. Genet. 4:2081-2087.
15. Will, K., T. Dork, M. Stuhrmann, H. von der Hardt, H. Ellemunter, B. Tummler, and J. Schmidthe. 1995. Transcript analysis of CFTR nonsense mutations in lymphocytes and nasal epithelial cells from cystic fibrosis patients. Hum. Mutat. 5:210-220.
16. Okamoto, Y., T. Yamazaki, A. Katsumi, T. Kojima, J. Takamatsu, M. Nishida, and H. Saito. 1996. A novel nonsense mutation associated with an exon skipping in a patient with hereditary protein S deficiency type 1. Thromb. Haemostasis. 75:877-882.
17. Bienvenu, T., C. Beldjord, J. Chelly, N. Fonknechten, D. Hubert, D. Dusser, and J.C. Kaplan. 1996. Analysis of alternative splicing patterns in the cystic fibrosis transmembrane conductance regulator gene using mRNA derived from lymphoblastoid cells of cystic fibrosis patients. Eur. J. Hum. Genet. 4:127-134.
18. Dietz, H.C., and R.J. Kendzior. 1994. Maintenance of an open reading frame as an additional level of scrutiny during splice site selection. Nat. Genet. 8:183-188.
19. Ahn, A.H., and L.M. Kunkel. 1993. The structural and functional diversity of dystrophin. Nat. Genet. 3:283-291.
20. Nishio, H., Y. Takeshima, N. Narita, H. Yanagawa, Y. Suzuki, Y. Ishikawa, Y. Ishikawa, R. Minami, H. Nakamura, and M. Matsuo. 1994. Identification of a novel first exon in the human dystrophin gene and of a new promoter located more than 500 kb upstream of the nearest known promoter. J. Clin. Invest. 94:1037-1042.
21. Matsuo, M. 1996. Duchenne/Becker muscular dystrophy: from molecular diagnosis to gene therapy. Brain Dev. 18:167-172.
22. Matsuo, M., T. Masumura, H. Nishio, T. Nakajima, Y. Kitoh, T. Takumi, J. Koga, and H. Nakamura. 1991. Exon skipping during splicing of dystrophin mRNA precursor due to an intraexon deletion in the dystrophin gene of Duchenne muscular dystrophy Kobe. J. Clin. Invest. 87:2127-2131.
23. Narita, N., H. Nishio, Y. Kitoh, Y. Ishikawa, Y. Ishikawa, R. Minami, H. Nakamura, and M. Matsuo. 1993. Insertion of a 5′ truncated L1 element into the 3′ end of exon 44 of the dystrophin gene resulted in skipping of the exon during splicing in a case of Duchenne muscular dystrophy. J. Clin. Invest. 91: 1862-1867.
24. Takeshima, Y., H. Nishio, H. Sakamoto, H. Nakamura, and M. Matsuo. 1995. Modulation of in vitro splicing of the upstream intron by modifying an intraexon sequence which is deleted from the dystrophin gene in dystrophin Kobe. J. Clin. Invest. 95:515-520.
25. Pramono, Z.A.D., Y. Takeshima, H. Alimsardjono, A. Ishii, S. Takeda, and M. Matsuo. 1996. Induction of exon skipping of the dystrophin transcript in lymphoblastoid cells by transfecting an antisense oligodeoxynucleotide complementary to an exon recognition sequence. Biochem. Biophys. Res. Commun. 226:445-449.
26. Chamberlain, J.S., R. Gibbs, J. Ranier, and C. Caskey. 1990. Multiplex PCR for the Diagnosis of Duchenne Muscular Dystrophy. Academic Press, San Diego. 272-281.
27. Beggs, A.H., M. Koenig, F.M. Boyce, and L.M. Kunkel. 1990. Detection of 98% of DMD/BMD gene deletions by polymerase chain reaction. Hum. Genet. 86:45-18.
28. Boyce, F.M., A.H. Beggs, C. Feener, and L.M. Kunkel. 1991. Dystrophin is transcribed in brain from a distant upstream promoter. Proc. Natl. Acad. Sci. USA. 88:1276-1280.
29. Roberts, R.G., M. Bobrow, and D.R. Bentley. 1992. Point mutations in the dystrophin gene. Proc. Natl. Acad Sci. USA. 89:2331-2335.
30. -1 to T) in a 5′ splice donor site of intron 13 of the dystrophin gene results in exon skipping and is responsible for Becker muscular dystrophy. Am. J. Hum. Genet. 54:53-61.
31. Pokharel, R.K., H. Alimsardjono, M. Matsuo, T. Takashima, and R. Shiba. 1997. Highly recurrent G1138A mutation of fibroblast growth factor receptor 3 (FGFR3) gene identified in achondroplasia, the commonest form of chondrodysplasia. J. Nep. Med. Assoc. 35:52-57.
32. Isegawa, Y., J. Sheng, Y. Sokawa, K. Yamanishi, O. Nakagomi, and S. Ueda. 1992. Selective amplification of cDNA sequence from total RNA by cassette-ligation mediated polymerase chain reaction (PCR): application to sequencing 6-5 kb genome segment of hantavirus strain B-1. Mol. Cell. Probes. 6: 467-475.
33. Lynch, K.W., and T. Maniatis. 1995. Synergistic interactions between two distinct elements of a regulated splicing enhancer. Genes Dev. 9:284-293.
34. Maquat, L.E. 1995. When cells stop making sense: effects of nonsense codons on RNA metabolism in vertebrate cells. RNA. 1:453-465.
35. Steingrimsdottir, H., G. Rowley, G. Dorado, J. Cole, and A.R. Lehmann. 1992. Mutations which alter splicing in the human hypoxanthine-guanine phosphoribosyltransferase. Nucl. Acids Res. 20:1201-1208.
36. Jin, Y., H.C. Dietz, R.A. Montgomery, W.R. Bell, I. McIntosh, B. Coller, and P.F. Bray. 1996. Glanzmann thrombasthenia. J. Clin. Invest. 98:1745-1754.
37. Willing, M.C., S.P. Deschenes, R.L. Slayton, and E.J. Roberts. 1996. Premature chain termination is a unifying mechanism for COL1A1 null alleles in osteogenesis imperfecta type I cell strains. Am. J. Hum. Genet. 59:799-809.
38. Xu, R., J. Teng, and T.A. Cooper. 1993. The cardiac troponin T alternative exon contains a novel purine-rich positive splicing element. Mol. Cell. Biol. 13:3660-3674.
39. Morisaki, H., T. Morisaki, L.K. Newby, and E.W. Holmes. 1993. Alternative splicing: a mechanism for phenotypic rescue of a common inherited defect. J. Clin. Invest. 91:2275-2280.
40. Monaco, A.P., C. Bertelson, S. Liechti-Gallati, H. Moser, and L. Kunkel. 1988. An explanation for the phenotypic differences between patients bearing partial deletions of the DMD locus. Genomics. 2:90-95.
41. Prior, T.W., C. Bartolo, A.C. Papp, P.J. Snyder, M.S. Sedra, A.H.M. Burghes, and J.R. Mendell. 1996. Nonsense mutations in a Becker muscular dystrophy and an intermediate patient. Hum. Mutat. 7:72-75.
42. Barbieri, A.M., N. Soriani, A. Ferlini, A. Michelato, M. Ferrari, and P. Carrera. 1996. Seven novel additional small mutations and a new alternative splicing in the human dystrophin gene detected by heteroduplex analysis and restricted RT-PCR heteroduplex analysis of illegitimate transcripts. Eur. J. Hum. Genet. 4:183-187.
43. Shapiro, M.B., and P. Senapathy. 1987. RNA splice junctions of different classes of eukaryotes: sequence statics and functional implications in gene expression. Nucl. Acids Res. 15:7155-7174.
44. Koenig, M., A.P. Monaco, and L.M. Kunkel. 1988. The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell. 53:219-228.