Efficient bypass of mutations in dysferlin deficient patient cells by antisense-induced exon skipping

Human Mutation

Volumn 31, Issue 2, 2010, Pages 136-142

  Wein, Nicolas ^a   Avril, Aurélie ^b   Bartoli, Marc ^a   Beley, Cyriaque ^b   Chaouch, Soraya ^b   Laforêt, Pascal ^c   Behin, Anthony ^c   Butler Browne, Gillian ^b   Mouly, Vincent ^b   Krahn, Martin ^a,d   Garcia, Luis ^b   Lévy, Nicolas ^a,d  

^a AIX MARSEILLE UNIVERSITY   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^d TIMONE HOSPITAL   (France)

Author keywords

DYSF; Dysferlin; Exon skipping; Gene therapy; Myoblast

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; DYSFERLIN; LENTIVIRUS VECTOR; MYOD PROTEIN;

ARTICLE; CONTROLLED STUDY; EXON; FRAMESHIFT MUTATION; GENE MUTATION; GENE REPRESSION; GENE SEQUENCE; GENE TARGETING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MYOBLAST; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; SKIN FIBROBLAST;

ANIMALS; BASE SEQUENCE; CELLS, CULTURED; CODON, NONSENSE; DNA MUTATIONAL ANALYSIS; EXONS; FIBROBLASTS; FRAMESHIFT MUTATION; HUMANS; LENTIVIRUS; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; MUSCLE PROTEINS; MUTATION; OLIGONUCLEOTIDES, ANTISENSE;

EID: 75149170176     PISSN: 10597794     EISSN: 10981004     Source Type: Journal    
DOI: 10.1002/humu.21160     Document Type: Article

References (28)

1. Aartsma-Rus A, Janson AA, Kaman WE, Bremmer-Bout M, van Ommen GJ, den Dunnen JT, van Deutekom JC. 2004. Antisense-induced multiexon skipping for Duchenne muscular dystrophy makes more sense. Am J Hum Genet 74:83-92.
2. Bansal D, Miyake K, Vogel SS, Groh S, Chen CC,Williamson R, McNeil PL, Campbell KP. 2003. Defective membrane repair in dysferlin-deficient muscular dystrophy. Nature 423:168-172.
3. Barde I, Zanta-Boussif MA, Paisant S, Leboeuf M, Rameau P, Delenda C, Danos O. 2006. Efficient control of gene expression in the hematopoietic system using a single Tet-on inducible lentiviral vector. Mol Ther 13:382-390.
4. Bashir R, Britton S, Strachan T, Keers S, Vafiadaki E, Lako M, Richard I, Marchand S, Bourg N, Argov Z, Sadeh M, Mahjneh I, Marconi G, Passos-Bueno MR, Moreira Ede S, Zatz M, Beckmann JS, Bushby K. 1998. A gene related to Caenorhabditis elegans spermatogenesis factor fer-1 is mutated in limb-girdle muscular dystrophy type 2B. Nat Genet 20:37-42.
5. Benchaouir R, Meregalli M, Farini A, D'Antona G, Belicchi M, Goyenvalle A, Battistelli M, Bresolin N, Bottinelli R, Garcia L, Torrente Y. 2007. Restoration of human dystrophin following transplantation of exon-skipping-engineered DMD patient stem cells into dystrophic mice. Cell Stem Cell 1:646-657.
6. Beroud C, Tuffery-Giraud S, Matsuo M, Hamroun D, Humbertclaude V, Monnier N, Moizard MP, Voelckel MA, Calemard LM, Boisseau P, Blayau M, Philippe C, Cossée M, Pagès M, Rivier F, Danos O, Garcia L, Claustres M. 2007. Multiexon skipping leading to an artificial DMD protein lacking amino acids from exons 45 through 55 could rescue up to 63% of patients with Duchenne muscular dystrophy. Hum Mutat 28:196-202.
7. Cartegni L, Krainer AR. 2003. Correction of disease-associated exon skipping by synthetic exon-specific activators. Nat Struct Biol 10:120-125.
8. Chaouch S, Mouly V, Goyenvalle A, Vulin A, Mamchaoui K, Negroni E, Di Santo J, Butler-Browne G, Torrente Y, Garcia L, Furling D. 2009. Immortalized skin fibroblasts expressing conditional MyoD as a renewable and reliable source of converted human muscle cells to assess therapeutic strategies for muscular dystrophies: validation of an exon-skipping approach to restore dystrophin in duchenne muscular dystrophy cells. Hum Gene Ther 20:784-790.
9. Charrier S, Stockholm D, Seye K, Opolon P, Taveau M, Gross DA, Bucher-Laurent S, Delenda C, Vainchenker W, Danos O, Galy A. 2005. A lentiviral vector encoding the human Wiskott-Aldrich syndrome protein corrects immune and cytoskeletal defects in WASP knockout mice. Gene Ther 12:597-606.
10. De Luna N, Freixas A, Gallano P, Caselles L, Rojas-Garcia R, Paradas C, Nogales G, Dominguez-Perles R, Gonzalez-Quereda L, Vilchez JJ, Márquez C, Bautista J, Guerrero A, Salazar JA, Pou A, Illa I, Gallardo E. 2007. Dysferlin expression in monocytes: a source of mRNA for mutation analysis. Neuromuscul Disord 17:69-76.
11. Desmet FO, Hamroun D, Lalande M, Collod-Beroud G, Claustres M, Beroud C. 2009. Human Splicing Finder: an online bioinformatics tool to predict splicing signals. Nucleic Acids Res 37:e67.
12. Edom F, Mouly V, Barbet JP, Fiszman MY, Butler-Browne GS. 1994. Clones of human satellite cells can express in vitro both fast and slow myosin heavy chains. Dev Biol 164:219-229.
13. Gorman L, Suter D, Emerick V, Schumperli D, Kole R. 1998. Stable alteration of pre-mRNA splicing patterns by modified U7 small nuclear RNAs. Proc Natl Acad Sci USA 95:4929-4934.
14. Goyenvalle A, Vulin A, Fougerousse F, Leturcq F, Kaplan JC, Garcia L, Danos O. 2004. Rescue of dystrophic muscle through U7 snRNA-mediated exon skipping. Science 306:1796-1799.
15. Heemskerk HA, de Winter CL, de Kimpe SJ, van Kuik-Romeijn P, Heuvelmans N, Platenburg GJ, van Ommen GJ, van Deutekom JC, Aartsma-Rus A. 2009. In vivo comparison of 2′-O-methyl phosphorothioate and morpholino antisense oligonucleotides for Duchenne muscular dystrophy exon skipping. J Gene Med 11:257-266.
16. Krahn M, Beroud C, Labelle V, Nguyen K, Bernard R, Bassez G, Figarella-Branger D, Fernandez C, Bouvenot J, Richard I, Ollagnon-Roman E, Bevilacqua JA, Salvo E, Attarian S, Chapon F, Pellissier JF, Pouget J, Hammouda el H, Laforêt P, Urtizberea JA, Eymard B, Leturcq F, Lévy N. 2009a. Analysis of the DYSF mutational spectrum in a large cohort of patients. Hum Mutat 30:E345-E375.
17. Krahn M, Borges A, Navarro C, Schuit R, Stojkovic T, Torrente Y,Wein N, Pecheux C, Levy N. 2009b. Identification of different genomic deletions and one duplication in the dysferlin gene using multiplex ligation-dependent probe amplification and genomic quantitative PCR. Genet Test Mol Biomarkers 13:439-442.
18. Krahn M, Wein N, Lostal W, Bourg-Alibert N, Nguyen K, Courrier S, Vial C, Labelle V, De Petris D, Borges A, Mattei MG, Roudaut C, Miyake K, McNeil P, Cau P, Leturcq F, Bartoli M, Lévy N, Richard I. 2008. G.O.5 Partial functionality of a Mini-dysferlin molecule identified in a patient affected with moderately severe primary dysferlinopathy. Neuromusc Disord 18:781.
19. Liu J, Aoki M, Illa I, Wu C, Fardeau M, Angelini C, Serrano C, Urtizberea JA, Hentati F, Hamida MB, Bohlega S, Culper EJ, Amato AA, Bossie K, Oeltjen J, Bejaoui K, McKenna-Yasek D, Hosler BA, Schurr E, Arahata K, de Jong PJ, Brown Jr RH. 1998. Dysferlin, a novel skeletal muscle gene, is mutated in Miyoshi myopathy and limb girdle muscular dystrophy. Nat Genet 20:31-36.
20. Lu QL, Rabinowitz A, Chen YC, Yokota T, Yin H, Alter J, Jadoon A, Bou-Gharios G, Partridge T. 2005. Systemic delivery of antisense oligoribonucleotide restores dystrophin expression in body-wide skeletal muscles. Proc Natl Acad Sci USA 102:198-203.
21. Naldini L. 1998. Lentiviruses as gene transfer agents for delivery to non-dividing cells. Curr Opin Biotechnol 9:457-463.
22. Nguyen K, Bassez G, Krahn M, Bernard R, Laforet P, Labelle V, Urtizberea JA, Figarella-Branger D, Romero N, Attarian S, Leturcq F, Pouget J, Lévy N, Eymard B. 2007. Phenotypic study in 40 patients with dysferlin gene mutations: high frequency of atypical phenotypes. Arch Neurol 64:1176-1182.
23. Sinnreich M, Therrien C, Karpati G. 2006. Lariat branch point mutation in the dysferlin gene with mild limb-girdle muscular dystrophy. Neurology 66:1114-1116.
24. Smith PJ, Zhang C, Wang J, Chew SL, Zhang MQ, Krainer AR. 2006. An increased specificity score matrix for the prediction of SF2/ASF-specific exonic splicing enhancers. Hum Mol Genet 15:2490-2508.
25. Therrien C, Dodig D, Karpati G, Sinnreich M. 2006. Mutation impact on dysferlin inferred from database analysis and computer-based structural predictions. J Neurol Sci 250:71-78.
26. Tuffery-Giraud S, Béroud C, Leturcq F, Yaou RB, Hamroun D, Michel-Calemard L, Moizard MP, Bernard R, Cossée M, Boisseau P, Blayau M, Creveaux I, Guiochon-Mantel A, de Martinville B, Philippe C, Monnier N, Bieth E, Khau Van Kien P, Desmet FO, Humbertclaude V, Kaplan JC, Chelly J, Claustres M. 2009. Genotype-phenotype analysis in 2,405 patients with a dystrophinopathy using the UMD-DMD database: a model of nationwide knowledge base. Hum Mutat 30:934-945.
27. Urtizberea JA, Bassez G, Leturcq F, Nguyen K, Krahn M, Levy N. 2008. Dysferlinopathies. Neurol India 56:289-297.
28. Wein N, Krahn M, Courrier S, Bartoli M, Salort-Campana E, Nguyen K, Fernandez C, Pouget J, Fossat C, Depetris D, Leturcq F, Cau P, Levy N. 2009. Immunolabelling and flow cytometry as new tools to explore dysferlinopathies. Neuromuscul Disord [Epub ahead of print].