Dystrophin nonsense mutations can generate alternative rescue transcripts in lymphocytes

Annals of Human Genetics

Volumn 72, Issue 6, 2008, Pages 717-724

  Nishiyama, A ^a   Takeshima, Y ^a   Zhang, Z ^a   Habara, Y ^a   Tran, T H T ^a   Yagi, M ^a   Matsuo, Masafumi ^a  

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Duchenne muscular dystrophy; Dystrophin; Exon skipping; Nonsense mutation; Splicing

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; DYSTROPHIN; MESSENGER RNA; RNA;

ADOLESCENT; ADULT; ALTERNATIVE RNA SPLICING; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; DUCHENNE MUSCULAR DYSTROPHY; ENHANCER REGION; EXON; GENE IDENTIFICATION; GENE SEQUENCE; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; LYMPHOCYTE; NONSENSE MUTATION; PRIORITY JOURNAL; SCHOOL CHILD; SCORING SYSTEM; SILENCER GENE;

ADOLESCENT; ADULT; CHILD; CHILD, PRESCHOOL; CODON, NONSENSE; DNA MUTATIONAL ANALYSIS; DYSTROPHIN; HUMANS; JAPAN; LYMPHOCYTES; MUSCULAR DYSTROPHIES; RNA SPLICING;

EID: 54049095232     PISSN: 00034800     EISSN: 14691809     Source Type: Journal    
DOI: 10.1111/j.1469-1809.2008.00468.x     Document Type: Article

References (33)

1. Barbieri, A. M., Soriani, N., Ferlini, A., Michelato, A., Ferrari, M. & Carrera, P. (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.
2. Cartegni, L., Chew, S. L. & Krainer, A. R. (2002) Listening to silence and understanding nonsense: Exonic mutations that affect splicing. Nat Rev Genet 3, 285-298.
3. Cartegni, L., Wang, J., Zhu, Z., Zhang, M. Q. & Krainer, A. R. (2003) ESEfinder: A web resource to identify exonic splicing enhancers. Nucleic Acids Res 31, 3568-3571.
4. Deburgrave, N., Daoud, F., Llense, S., Barbot, J. C., Recan, D., Peccate, C., Burghes, A. H., Beroud, C., Garcia, L., Kaplan, J. C., Chelly, J. & Leturcq, F. (2007) Protein- and mRNA-based phenotype-genotype correlations in DMD/BMD with point mutations and molecular basis for BMD with nonsense and frameshift mutations in the DMD gene. Hum Mutat 28, 183-195.
5. 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.
6. Fairbrother, W. G., Yeo, G. W., Yeh, R., Goldstein, P., Mawson, M., Sharp, P. A. & Burge, C. B. (2004) RESCUE-ESE identifies candidate exonic splicing enhancers in vertebrate exons. Nucleic Acids Res 32, W187-190.
7. Fajkusova, L., Lukas, Z., Tvrdikova, M., Kuhrova, V. V., Hajek, 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.
8. Feener, C. A., Koenig, M. & Kunkel, L. M. (1989) Alternative splicing of human dystrophin mRNA generates isoforms at the carboxy terminus. Nature 338, 509-511.
9. 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.
10. Howard, M. T., Anderson, C. B., Fass, U., Khatri, S., Gesteland, R. F., Atkins, J. F. & Flanigan, K. M. (2004) Readthrough of dystrophin stop codon mutations induced by aminoglycosides. Ann Neurol 55, 422-426.
11. Ito, T., Takeshima, Y., Yagi, M., Kamei, S., Wada, H. & Matsuo, M. (2003) Analysis of dystrophin mRNA from skeletal muscle but not from lymphocytes led to identification of a novel nonsense mutation in a carrier of Duchenne muscular dystrophy. J Neurol 250, 581-587.
12. Li, B., Wachtel, C., Miriami, E., Yahalom, G., Friedlander, G., Sharon, G., Sperling, R. & Sperling, J. (2002) Stop codons affect 5′ splice site selection by surveillance of splicing. Proc Natl Acad Sci USA 99, 5277-5282.
13. Mankin, A. S. & Liebman, S. W. (1999) Baby, don't stop! Nat Genet 23, 8-10.
14. Maquat, L. E. (2004) Nonsense-mediated mRNA decay: Splicing, translation and mRNP dynamics. Nat Rev Mol Cell Biol 5, 89-99.
15. Matsuo, M., Nishio, H., Kitoh, Y., Francke, U. & Nakamura, H. (1992) Partial deletion of a dystrophin gene leads to exon skipping and to loss of an intra-exon hairpin structure from the predicted mRNA precursor. Biochem Biophys Res Commun 182, 495-500.
16. Melis, M. A., Muntoni, F., Cau, M., Loi, D., Puddu, A., Boccone, L., Mateddu, A., Cianchetti, C. & Cao, A. (1998) Novel nonsense mutation (C->A nt 10512) in exon 72 of dystrophin gene leading to exon skipping in a patient with a mild dystrophinopathy. Hum Mutat Suppl 1, S137-S138.
17. Politano, L., Nigro, G., Nigro, V., Piluso, G., Papparella, S., Paciello, O. & Comi, L. I. (2003) Gentamicin administration in Duchenne patients with premature stop codon. Preliminary results. Acta Myol 22, 15-21.
18. Roberts, R. G., Barby, T. F., Manners, E., Bobrow, M. & Bentley, D. R. (1991) Direct detection of dystrophin gene rearrangements by analysis of dystrophin mRNA in peripheral blood lymphocytes. Am J Hum Genet 49, 298-310.
19. 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.
20. Surono, A., Takeshima, Y., Wibawa, T., Pramono, Z. A. & Matsuo, M. (1997) Six novel transcripts that remove a huge intron ranging from 250 to 800 kb are produced by alternative splicing of the 5′ region of the dystrophin gene in human skeletal muscle. Biochem Biophys Res Commun 239, 895-899.
21. Surono, A., Tran, V. K., Takshima, Y., Wada, H., Yagi, M., Takagi, M., Koizumi, M. & Matsuo, M. (2004) Chimeric RNA/ethylene bridged nucleic acids promote dystrophin expression in myocytes of Duchenne muscular dystrophy by inducing skipping of the nonsense-mutation-encoding exon. Hum Gene Ther 15, 749-757.
22. Takeshima, Y., Nishio, H., Sakamoto, H., Nakamura, H. & Matsuo, M. (1995) Modulation of in vitro splicing of the upstream intron by modifying an intra-exon sequence which is deleted from the dystrophin gene in dystrophin Kobe. J Clin Invest 95, 515-520.
23. Takeshima, Y., Yagi, M., Wada, H., Ishibashi, K., Nishiyama, A., Kakumoto, M., Sakaeda, T., Saura, R., Okumura, K. & Matsuo, M. (2006) Intravenous infusion of an antisense oligonucleotide results in exon skipping in muscle dystrophin mRNA of Duchenne muscular dystrophy. Pediatr Res 59, 690-694.
24. Tay, S. K., Khng, H. H., Low, P. S. & Lai, P. S. (2006) Diagnostic strategy for the detection of dystrophin gene mutations in Asian pateints and carriers using immortalized cell lines. J Child Neurol 21, 150-155.
25. Tran, V. K., Takeshima, Y., Zhang, Z., Habara, Y., Haginoya, K., Nishiyama, A., Yagi, M. & Matsuo, M. (2007) A nonsense mutation-created intraexonic splice site is active in the lymphocytes, but not in the skeletal muscle of a DMD patient. Hum Genet 120, 737-742.
26. 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 intra-exonic four-nucleotide deletion in the dystrophin gene. J Med Genet 43, 924-930.
27. Tuffery, S., Bareil, C., Demaille, J. & Claustres, M. (1996) Four novel dystrophin point mutations: Detection by protein truncation test and transcript analysis in lymphocytes from Duchenne muscular dystrophy patients. Eur J Hum Genet 4, 143-152.
28. Vuoristo, M. M., Pappas, J. G., Jansen, V. & Ala-Kokko, L. (2004) A stop codon mutation in COL11A2 induces exon skipping and leads to non-ocular Stickler syndrome. Am J Med Genet A 130, 160-164.
29. Wang, J., Hamilton, J. I., Carter, M. S., Li, S. & Wilkinson, M. F. (2002) Alternatively spliced TCR mRNA induced by disruption of reading frame. Science 297, 108-110.
30. Wang, Z., Rolish, M. E., Yeo, G., Tung, V., Mawson, M. & Burge, C. B. (2004) Systematic identification and analysis of exonic splicing silencers. Cell 119, 831-845.
31. Zatkova, A., Messiaen, L., Vandenbroucke, I., Wieser, R., Fonatsch, C., Krainer, A. R. & Wimmer, K. (2004) Disruption of exonic splicing enhancer elements is the principal cause of exon skipping associated with seven nonsense or missense alleles of NF1. Hum Mutat 24, 491-501.
32. Zhang, X., Lee, J. & Chasin, L. A. (2003) The effect of nonsense codons on splicing: A genomic analysis. RNA 9, 637-639.
33. Zhang, X. H., Kangsamaksin, T., Chao, M. S., Banerjee, J. K. & Chasin, L. A. (2005) Exon inclusion is dependent on predictable exonic splicing enhancers. Mol Cell Biol 25, 7323-7332.