A naturally occurring human minidysferlin protein repairs sarcolemmal lesions in a mouse model of dysferlinopathy

Science Translational Medicine

Volumn 2, Issue 50, 2010, Pages

  Krahn, Martin ^a,b   Wein, Nicolas ^a   Bartoli, Marc ^a,c   Lostal, William ^c   Courrier, Sébastien ^a   Bourg Alibert, Nathalie ^c   Nguyen, Karine ^a,b   Vial, Christophe ^d   Streichenberger, Nathalie ^d   Labelle, Véronique ^b   DePetris, Danielle ^a   Pécheux, Christophe ^b   Leturcq, France ^e   Cau, Pierre ^a   Richard, Isabelle ^c   Lévy, Nicolas ^a,b  

^a AIX MARSEILLE UNIVERSITY   (France)

^b TIMONE HOSPITAL   (France)

^c GÉNÉTHON   (France)

^d HÔPITAL NEUROLOGIQUE   (France)

^e CHU de Lyon ^*  (France)

Author keywords

[No Author keywords available]

Indexed keywords

DYSFERLIN; MINIDYSFERLIN; PARVOVIRUS VECTOR; UNCLASSIFIED DRUG; DYSF PROTEIN, HUMAN; MEMBRANE PROTEIN; MUSCLE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOSOMAL RECESSIVE DISORDER; CONTROLLED STUDY; DRUG TARGETING; DYSFERLIN GENE; DYSFERLINOPATHY; GENE; GENE DELETION; GENE FUNCTION; GENE STRUCTURE; HOMOZYGOTE; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; MUSCLE DISEASE; MUSCLE FIBER MEMBRANE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SARCOLEMMA LESION; VIRAL GENE DELIVERY SYSTEM; ADENO ASSOCIATED VIRUS; ANIMAL; DISEASE MODEL; GENE THERAPY; GENETICS; LIMB GIRDLE MUSCULAR DYSTROPHY; METABOLISM;

ANIMALS; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; GENE THERAPY; HUMANS; MEMBRANE PROTEINS; MICE; MUSCLE PROTEINS; MUSCULAR DYSTROPHIES, LIMB-GIRDLE;

EID: 77958065739     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3000951     Document Type: Article

References (40)

1. R. Bashir, S. Britton, T. Strachan, S. Keers, E. Vafiadaki, M. Lako, I. Richard, S. Marchand, N. Bourg, Z. Argov, M. Sadeh, I. Mahjneh, G. Marconi, M. R. Passos-Bueno, S. Moreira Ede, M. Zatz, J. S. Beckmann, K. Bushby, A gene related to Caenorhabditis elegans spermatogenesis factor fer-1 is mutated in limb-girdle muscular dystrophy type 2B. Nat. Genet. 20, 37-42 (1998).
2. J. Liu, M. Aoki, I. Illa, C. Wu, M. Fardeau, C. Angelini, C. Serrano, J. A. Urtizberea, F. Hentati, M. B. Hamida, S. Bohlega, E. J. Culper, A. A. Amato, K. Bossie, J. Oeltjen, K. Bejaoui, D. McKenna-Yasek, B. A. Hosler, E. Schurr, K. Arahata, P. J. de Jong, R. H. Brown Jr., Dysferlin, a novel skeletal muscle gene, is mutated in Miyoshi myopathy and limb girdle muscular dystrophy. Nat. Genet. 20, 31-36 (1998).
3. M. Aoki, K. Arahata, R. H. Brown Jr., Positional cloning of the gene for Miyoshi myopathy and limb-girdle muscular dystrophy. Rinsho Shinkeigaku 39, 1272-1275 (1999).
4. K. M. Bushby, Dysferlin and muscular dystrophy. Acta Neurol. Belg. 100, 142-145 (2000).
5. K. Nguyen, G. Bassez, M. Krahn, R. Bernard, P. Laforêt, V. Labelle, J. A. Urtizberea, D. Figarella-Branger, N. Romero, S. Attarian, F. Leturcq, J. Pouget, N. Lévy, B. Eymard, Phenotypic study in 40 patients with dysferlin gene mutations: High frequency of atypical phenotypes. Arch. Neurol. 64, 1176-1182 (2007).
6. J. Meldolesi, Surface wound healing: A new, general function of eukaryotic cells. J. Cell. Mol. Med. 7, 197-203 (2003).
7. D. Bansal, K. Miyake, S. S. Vogel, S. Groh, C. C. Chen, R. Williamson, P. L. McNeil, K. P. Campbell, Defective membrane repair in dysferlin-deficient muscular dystrophy. Nature 423, 168-172 (2003).
8. L. V. Anderson, K. Davison, J. A. Moss, C. Young, M. J. Cullen, J. Walsh, M. A. Johnson, R. Bashir, S. Britton, S. Keers, Z. Argov, I. Mahjneh, F. Fougerousse, J. S. Beckmann, K. M. Bushby, Dysferlin is a plasma membrane protein and is expressed early in human development. Hum. Mol. Genet. 8, 855-861 (1999).
9. D. B. Davis, K. R. Doherty, A. J. Delmonte, E. M. McNally, Calcium-sensitive phospholipid binding properties of normal and mutant ferlin C2 domains. J. Biol. Chem. 277, 22883-22888 (2002).
10. N. De Luna, A. Freixas, P. Gallano, L. Caselles, R. Rojas-García, C. Paradas, G. Nogales, R. Dominguez-Perles, L. Gonzalez-Quereda, J. J. Vilchez, C. Márquez, J. Bautista, A. Guerrero, J. A. Salazar, A. Pou, I. Illa, E. Gallardo, Dysferlin expression in monocytes: A source of mRNA for mutation analysis. Neuromuscul. Disord. 17, 69-76 (2007).
11. N. Wein, M. Krahn, S. Courrier, M. Bartoli, E. Salort-Campana, K. Nguyen, C. Fernandez, J. Pouget, C. Fossat, D. Depetris, F. Leturcq, P. Cau, N. Levy, Immunolabelling and flow cytometry as new tools to explore dysferlinopathies. Neuromuscul. Disord. 20, 57-60 (2010).
12. E. A. Nalefski, J. J. Falke, The C2 domain calcium-binding motif: Structural and functional diversity. Protein Sci. 5, 2375-2390 (1996).
13. C. Therrien, D. Dodig, G. Karpati, M. Sinnreich, Mutation impact on dysferlin inferred from database analysis and computer-based structural predictions. J. Neurol. Sci. 250, 71-78 (2006).
14. M. Aoki, J. Liu, I. Richard, R. Bashir, S. Britton, S. M. Keers, J. Oeltjen, H. E. Brown, S. Marchand, N. Bourg, C. Beley, D. McKenna-Yasek, K. Arahata, S. Bohlega, E. Cupler, I. Illa, I. Majneh, R. J. Barohn, J. A. Urtizberea, M. Fardeau, A. Amato, C. Angelini, K. Bushby, J. S. Beckmann, R. H. Brown Jr., Genomic organization of the dysferlin gene and novel mutations in Miyoshi myopathy. Neurology 57, 271-278 (2001).
15. R. Cagliani, F. Fortunato, R. Giorda, C. Rodolico, M. C. Bonaglia, M. Sironi, M. G. D'Angelo, A. Prelle, F. Locatelli, A. Toscano, N. Bresolin, G. P. Comi, Molecular analysis of LGMD-2B and MM patients: Identification of novel DYSF mutations and possible founder effect in the Italian population. Neuromuscul. Disord. 13, 788-795 (2003).
16. K. Nguyen, G. Bassez, R. Bernard, M. Krahn, V. Labelle, D. Figarella-Branger, J. Pouget, H. Hammouda el, C. Béroud, A. Urtizberea, B. Eymard, F. Leturcq, N. Lévy, Dysferlin mutations in LGMD2B, Miyoshi myopathy, and atypical dysferlinopathies. Hum. Mutat. 26, 165 (2005).
17. M. Guglieri, K. Bushby, How to go about diagnosing and managing the limb-girdle muscular dystrophies. Neurol. India 56, 271-280 (2008).
18. M. Krahn, C. Béroud, V. Labelle, K. Nguyen, R. Bernard, G. Bassez, D. Figarella-Branger, C. Fernandez, J. Bouvenot, I. Richard, E. Ollagnon-Roman, J. A. Bevilacqua, E. Salvo, S. Attarian, F. Chapon, J. F. Pellissier, J. Pouget, H. Hammouda el, P. Laforêt, J. A. Urtizberea, B. Eymard, F. Leturcq, N. Lévy, Analysis of the DYSF mutational spectrum in a large cohort of patients. Hum. Mutat. 30, E345-E375 (2009).
19. M. Krahn, A. Borges, C. Navarro, R. Schuit, T. Stojkovic, Y. Torrente, N. Wein, C. Pécheux, N. Lévy, 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 (2009).
20. J. C. Grieger, R. J. Samulski, Packaging capacity of adeno-associated virus serotypes: Impact of larger genomes on infectivity and postentry steps. J. Virol. 79, 9933-9944 (2005).
21. W. Lostal, M. Bartoli, N. Bourg, C. Roudaut, A. Bentaïb, K. Miyake, N. Guerchet, F. Fougerousse, P. McNeil, I. Richard, Efficient recovery of dysferlin deficiency by dual adeno-associated vector-mediated gene transfer. Hum. Mol. Genet. 19, 1897-1907 (2010).
22. B. Wang, J. Li, X. Xiao, Adeno-associated virus vector carrying human minidystrophin genes effectively ameliorates muscular dystrophy in mdx mouse model. Proc. Natl. Acad. Sci. U.S.A. 97, 13714-13719 (2000).
23. P. Gregorevic, J. M. Allen, E. Minami, M. J. Blankinship, M. Haraguchi, L. Meuse, E. Finn, M. E. Adams, S. C. Froehner, C. E. Murry, J. S. Chamberlain, rAAV6-microdystrophin preserves muscle function and extends lifespan in severely dystrophic mice. Nat. Med. 12, 787-789 (2006).
24. A. Goyenvalle, A. Vulin, F. Fougerousse, F. Leturcq, J. C. Kaplan, L. Garcia, O. Danos, Rescue of dystrophic muscle through U7 snRNA-mediated exon skipping. Science 306, 1796-1799 (2004).
25. T. Ragot, N. Vincent, P. Chafey, E. Vigne, H. Gilgenkrantz, D. Couton, J. Cartaud, P. Briand, J. C. Kaplan, M. Perricaudet, A. Kahn, Efficient adenovirus-mediated transfer of a human mini-dystrophin gene to skeletal muscle of mdx mice. Nature 361, 647-650 (1993).
26. X. Li, E. M. Eastman, R. J. Schwartz, R. Draghia-Akli, Synthetic muscle promoters: Activities exceeding naturally occurring regulatory sequences. Nat. Biotechnol. 17, 241-245 (1999).
27. L. Klinge, J. Harris, C. Sewry, R. Charlton, L. Anderson, S. Laval, Y. H. Chiu, M. Hornsey, V. Straub, R. Barresi, H. Lochmüller, K. Bushby, Dysferlin associates with the developing T-tubule system in rodent and human skeletal muscle. Muscle Nerve 41, 166-173 (2010).
28. L. Klinge, S. Laval, S. Keers, F. Haldane, V. Straub, R. Barresi, K. Bushby, From T-tubule to sarcolemma: Damage-induced dysferlin translocation in early myogenesis. FASEB J. 21, 1768-1776 (2007).
29. D. P. Millay, M. Maillet, J. A. Roche, M. A. Sargent, E. M. McNally, R. J. Bloch, J. D. Molkentin, Genetic manipulation of dysferlin expression in skeletal muscle: Novel insights into muscular dystrophy. Am. J. Pathol. 175, 1817-1823 (2009).
30. D. J. Hernández-Deviez, S. Martin, S. H. Laval, H. P. Lo, S. T. Cooper, K. N. North, K. Bushby, R. G. Parton, Aberrant dysferlin trafficking in cells lacking caveolin or expressing dystrophy mutants of caveolin-3. Hum. Mol. Genet. 15, 129-142 (2006).
31. 2+-regulated exocytosis of lysosomes. Cell 106, 157-169 (2001).
32. C. Béroud, S. Tuffery-Giraud, M. Matsuo, D. Hamroun, V. Humbertclaude, N. Monnier, M. P. Moizard, M. A. Voelckel, L. M. Calemard, P. Boisseau, M. Blayau, C. Philippe, M. Cossée, M. Pagès, F. Rivier, O. Danos, L. Garcia, M. Claustres, 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 (2007).
33. A. Aartsma-Rus, I. Fokkema, J. Verschuuren, I. Ginjaar, J. van Deutekom, G. J. van Ommen, J. T. den Dunnen, Theoretic applicability of antisense-mediated exon skipping for Duchenne muscular dystrophy mutations. Hum. Mutat. 30, 293-299 (2009).
34. M. Sinnreich, C. Therrien, G. Karpati, Lariat branch point mutation in the dysferlin gene with mild limb-girdle muscular dystrophy. Neurology 66, 1114-1116 (2006).
35. N. Wein, A. Avril, M. Bartoli, C. Beley, S. Chaouch, P. Laforêt, A. Behin, G. Butler-Browne, V. Mouly, M. Krahn, L. Garcia, N. Lévy, Efficient bypass of mutations in dysferlin deficient patient cells by antisense-induced exon skipping. Hum. Mutat. 31, 136-142 (2010).
36. Y. Saillour, M. Cossée, F. Leturcq, A. Vasson, C. Beugnet, K. Poirier, V. Commere, S. Sublemontier, M. Viel, F. Letourneur, J. C. Barbot, N. Deburgrave, J. Chelly, T. Bienvenu, Detection of exonic copy-number changes using a highly efficient oligonucleotide-based comparative genomic hybridization-array method. Hum. Mutat. 29, 1083-1090 (2008).
37. V. Delague, M. Souaid, E. Chouery, D. Depetris, D. Sanlaville, M. G. Mattei, A. Mégarbané, Screening for subtelomeric rearrangements using automated fluorescent genotyping of microsatellite markers: A Lebanese study. Eur. J. Med. Genet. 49, 117-126 (2006).
38. M. Bartoli, C. Roudaut, S. Martin, F. Fougerousse, L. Suel, J. Poupiot, E. Gicquel, F. Noulet, O. Danos, I. Richard, Safety and efficacy of AAV-mediated calpain 3 gene transfer in a mouse model of limb-girdle muscular dystrophy type 2A. Mol. Ther. 13, 250-259 (2006).
39. S. Duque, B. Joussemet, C. Riviere, T. Marais, L. Dubreil, A. M. Douar, J. Fyfe, P. Moullier, M. A. Colle, M. Barkats, Intravenous administration of self-complementary AAV9 enables transgene delivery to adult motor neurons. Mol. Ther. 17, 1187-1196 (2009).
40. U. P. Rohr, M. A. Wulf, S. Stahn, U. Steidl, R. Haas, R. Kronenwett, Fast and reliable titration of recombinant adeno-associated virus type-2 using quantitative real-time PCR. J. Virol. Methods 106, 81-88 (2002).