Microutrophin delivery through rAAV6 increases lifespan and improves muscle function in dystrophic dystrophin/Utrophin-deficient mice

Molecular Therapy

Volumn 16, Issue 9, 2008, Pages 1539-1545

  Odom, Guy L ^a   Gregorevic, Paul ^a   Allen, James M ^a   Finn, Eric ^a   Chamberlain, Jeffrey S ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYSTROPHIN; GENE THERAPY AGENT; GLYCOPROTEIN; MICROUTROPHIN; PARVOVIRUS VECTOR; RECOMBINANT ADENO ASSOCIATED VIRUS VECTOR 6; UTROPHIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DUCHENNE MUSCULAR DYSTROPHY; FEMALE; GENE LOCATION; HISTOLOGY; KNOCKOUT MOUSE; LIFESPAN; MALE; MOUSE; MUSCLE CELL; MUSCLE FUNCTION; NONHUMAN; NUCLEOTIDE SEQUENCE; SARCOLEMMA; SURVIVAL TIME; TRANSGENE; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; DEPENDOVIRUS; DYSTROPHIN; FEMALE; GENE TRANSFER TECHNIQUES; HUMANS; LONGEVITY; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MICE, KNOCKOUT; MUSCLE CONTRACTION; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, ANIMAL; NITRIC OXIDE SYNTHASE TYPE I; SARCOLEMMA; TRANSGENES; UTROPHIN;

MURINAE; MUS;

EID: 50549098032     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2008.149     Document Type: Article

References (50)

1. Dalkilic, I and Kunkel, LM (2003). Muscular dystrophies: Genes to pathogenesis. Curr Opin Genet Dev 13: 231-238.
2. Hoffman, EP, Brown, RH Jr. and Kunkel, LM (1987). Dystrophin: The protein product of the Duchenne muscular dystrophy locus. Cell 51: 919-928.
3. Koenig, M, Hoffman, EP, Bertelson, CJ, Monaco, AP, Feener, C and Kunkel, LM (1987). Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell 50: 509-517.
4. Angelini, C (2007). The role of corticosteroids in muscular dystrophy: A critical appraisal. Muscle Nerve 36: 424-435.
5. Ervasti, JM and Campbell, KP (1993). A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol 122: 809-823.
6. Ibraghimov-Beskrovnaya, O, Ervasti, JM, Levellie, CJ, Slaughter, CA, Sernett, SW and Campbell, KP (1992). Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 355: 696-702.
7. Yoshida, M and Ozawa, E (1990). Clycoprotein complex anchoring dystrophin to sarcolemma. J Biochem (Tokyo) 108: 748-752.
8. Watchko, JF, O'Day, TL and Hoffman, EP (2002). Functional characteristics of dystrophic skeletal muscle: Insights from animal models. J Appl Physiol 93: 407-417.
9. Gregorevic, P, Blankinship, MJ, Allen, JM, Crawford, RW, Meuse, L, Miller, DG et al. (2004). Systemic delivery of genes to striated muscles using adeno-associated viral vectors. Nat Med 10: 828-834.
10. Podsakoff, G, Wong, KK Jr. and Chatterjee, S (1994). Efficient gene transfer into nondividing cells by adeno-associated vinis-based vectors. J Virol 68: 5656-5666.
11. Wakefield, PM, Tinsley, JM, Wood, MJ, Gilbert, R, Karpati, G and Davies, KE (2000). Prevention of the dystrophic phenotype in dystrophin/ utrophin-deficient muscle following adenovirus-mediated transfer of a utrophin minigene. Gene Ther 7: 201-204.
12. Huard, J, Roy, R, Bouchard, JP, Malouin, F, Richards, CL and Tremblay, JP (1992). Human myoblast transplantation between immunohistocompatible donors and recipients produces immune reactions. Transplant Proc 24: 3049-3051.
13. Karpati, G, Ajdukovic, D, Arnold, D, Gledhill, RB, Guttmann, R, Holland, P et al. (1993). Myoblast transfer in Duchenne muscular dystrophy. Ann Neurol 34: 8-17.
14. Ohtsuka, Y, Udaka, K, Yamashiro, Y, Yagita, H and Okumura, K (1998). Dystrophin acts as a transplantation rejection antigen in dystrophin-deficient mice: Implication for gene therapy. J Immunol 160: 4635-4640.
15. Love, DR, Hill, DF, Dickson, G, Spurr, NK, Byth, BC, Marsden, RF et al. (1989). An autosomal transcript in skeletal muscle with homology to dystrophin. Nature 339: 55-58.
16. Tinsley, JM, Blake, DJ, Roche, A, Fairbrother, U, Riss, J, Byth, BC et al. (1992). Primary structure of dystrophin-related protein. Nature 360: 591-593.
17. Tinsley, J, Deconinck, N, Fisher, R, Kahn, D, Phelps, S, Gillis, JM et al. (1998). Expression of full-length utrophin prevents muscular dystrophy in mdx mice. Nat Med 4: 1441-1444.
18. Squire, S, Raymackers, JM, Vandebrouck, C, Potter, A, Tinsley, J, Fisher, R et al. (2002). Prevention of pathology in mdx mice by expression of utrophin: Analysis using an inducible transgenic expression system. Hum Mol Genet 11: 3333-3344.
19. Rafael, JA, Tinsley, JM, Potter, AC, Deconinck, AE and Davies, KE (1998). Skeletal muscle-specific expression of a utrophin transgene rescues utrophin-dystrophin deficient mice. Nat Genet 19: 79-82.
20. Deconinck, AE, Rafael, JA, Skinner, JA, Brown, SC, Potter, AC, Metzinger, L et al. (1997). Utrophin-dystrophin-defident mice as a model for Duchenne muscular dystrophy. Cell 90: 717-727.
21. Tinsley, JM, Potter, AC, Phelps, SR, Fisher, R, Trickett, JI and Davies, KE (1996). Amelioration of the dystrophic phenotype of mdx mice using a truncated utrophin transgene. Nature 384: 349-353.
22. Harper, SQ, Hauser, MA, DelloRusso, C, Duan, D, Crawford, RW, Phelps, SF et al. (2002). Modular flexibility of dystrophin: Implications for gene therapy of Duchenne muscular dystrophy. Nat Med 8: 253-261.
23. Crawford, GE, Faulkner, JA, Crosbie, RH, Campbell, KP, Froehner, SC and Chamberlain, JS (2000). Assembly of the dystrophin-associated protein complex does not require the dystrophin COOH-terminal domain. J Cell Biol 150: 1399-1410.
24. Judge, LM, Haraguchiln, M and Chamberlain, JS (2006). Dissecting the signaling and mechanical functions of the dystrophin-glycoprotein complex. J Cell Sci 119: 1537-1546.
25. Yue, Y, Liu, M and Duan, D (2006). C-terminal-truncated microdystrophin recruits dystrobrevin and syntrophin to the dystrophin-associated glycoprotein complex and reduces muscular dystrophy in symptomatic utrophin/dystrophin double-knockout mice. Mol Ther 14: 79-87.
26. Townsend, D, Blankinship, MJ, Allen, JM, Gregorevic, P, Chamberlain, JS and Metzger, JM (2007). Systemic administration of micro-dystrophin restores cardiac geometry and prevents dobutamine-induced cardiac pump failure. Mol Ther 15: 1086-1092.
27. Xia, H, Mao, Q, Eliason, SL, Harper, SQ, Martins, IH, Orr, HT et al. (2004). RNAi suppresses polyglutamine-induced neurodegeneration in a model of spinocerebellar ataxia. Nat Med 10, 816-820.
28. Yokoi, K, Zhang, HS, Kachi, S, Balaggan, KS, Yu, Q, Guschin, D et al. (2007). Gene transfer of an engineered Zinc finger protein enhances the anti-angiogenic defense system. Mol Ther 15: 1917-1923.
29. Mingozzi, F, Maus, MV, Hui, DJ, Sabatino, DE, Murphy, SL, Rasko, JE et al. (2007). CD8(+) T-cell responses to adeno-associated virus capsid in humans. Nat Med 13: 419-422.
30. Hirst, RC, McCullagh, KJ and Davies, KE (2005). Utrophin upregulation in Duchenne muscular dystrophy. Acta Myol 24: 209-216.
31. Grady, RK Teng, H, Nichol, MC, Cunningham JC, Wilkinson, RS and Sanes, JR (1997). Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: A model for Duchenne muscular dystrophy. Cell 90 729-738.
32. Dowling, P, Culligan, K and Ohlendieck, K (2002). Distal mdx muscle groups exhibiting up-regulation of utrophin and rescue of dystrophin-associated glycoproteins exemplify a protected phenotype in muscular dystrophy. Naturwissenschaften 89: 75-78.
33. Porter, JD (1998). Commentary: Extraocular muscle sparing in muscular dystrophy: A critical evaluation of potential protective mechanisms. Neuromuscul Disord 8: 198-203.
34. Porter, JD, Merriam, AP, Hack, AA, Andrade, FH and McNally, EM (2001). Extraocular muscle is spared despite the absence of an intact sarcoglycan complex in γ- or δ-sarcoglycan-deficient mice. Neuromuscul Disord 11: 197-207.
35. Khurana, TS and Davies, KE (2003). Pharmacological strategies for muscular dystrophy. Nat Rev Drug Discov 2: 379-390.
36. Stocksley, MA, Chakkalakal, JV, Bradford, A, Miura, P, De Repentigny, Y, Kothary, R et al. (2005). A 1.3 kb promoter fragment confers spatial and temporal expression of utrophin A mRNA in mouse skeletal muscle fibers. Neuromuscul Disord 15: 437-449.
37. Campbell, KP (1995). Three muscular dystrophies: Loss of cytoskeleton-extracellular matrix linkage. Cell 80: 675-679.
38. Rybakova, IN, Patel, JR and Ervasti, JM (2000). The dystrophin complex forms a mechanically strong link between the sarcolemma and costameric actin. J Cell Biol 150: 1209-1214.
39. Matsumura, K, Ervasti, JM, Ohlendieck, K, Kahl, SD and Campbell, KP (1992). Association of dystrophin-related protein with dystrophin-associated proteins in mdx mouse muscle. Nature 360 588-591.
40. Rybakova, IN, Humston, JL, Sonnemann, KJ and Ervasti, JM (2006). Dystrophin and utrophin bind actin through distinct modes of contact. J Biol Chem 281: 9996-10001.
41. Ishikawa-Sakurai, M, Yoshida, M, Imamura, M, Davies, KE and Ozawa, E (2004). ZZ domain is essentially required for the physiological binding of dystrophin and utrophin to β-dystroglycan. Hum Mol Genet 13 693-702.
42. Chao, DS, Gorospe, JR, Brenman, JE, Rafael, JA, Peters, MF, Froehner, SC et al. (1996). Selective loss of sarcolemmal nitric oxide synthase in Becker muscular dystrophy. J Exp Med 184. 609-6T8.
43. Hwang, W, Kelly, NG and Boriek, AM (2005). Passive mechanks of muscle tendinous junction of canine diaphragm. J Appl Physiol 98: 1328-1333.
44. Chakkalakal, JV, Miura, P, Belanger, G, Michel, RN and Jasmin, BJ (2008). Modulation of utrophin A mRNA stability in fast versus slow muscles via an AU-rich element and calcineurin signaling. Nucleic Acids Res 36: 826-838.
45. Miura, P, Thompson, J, Chakkalakal, JV, Holcik, M and Jasmin, BJ (2005). The utrophin A 5'-untranslatLd region confers internal ribosome entry site-mediated translational control during regeneration of skeletal muscle fibers. J Biol Chem 280: 32997-33005.
46. Perkins, KJ, Basu, U, Budak, MT, Ketterer, C, Baby, SM, Lozynska, O et al. (2007). Ets-2 repressor factor silences extrasynaptic utrophin by N-box mediated repression in skeletal muscle. Mol Biol Cell 15: 2864-2872.
47. Gregorevic, P, Allen, JM, Minami, E, Blankinship, MJ, Haraguchi, M, Meuse, L et al. (2006). rAAV6-microdystrophin preserves muscle function and extends lifespan in severely dystrophic mice. Nat Med 12: 787-789.
48. Allen, JM, Halbert, CL and Miller, AD (2000). Improved adeno-associated virus vector production with transfection of a single helper adenovirus gene. E4orf6. Mol Ther 1: 88-95.
49. Blankinship, MJ, Gregorevic, P, Allen, JM, Harper, SQ, Harper, H, Halbert, CL et al. (2004). Efficient transduction of skeletal muscle using vectors based on adeno-associated virus serotype 6. Mol Ther 10: 671-678.
50. Abmayr, S (2006). The structure and function of dystrophin. In: Winder, S (ed.). Molecular Mechanisms of Muscular Dystrophies. Landes Bioscience: Georgetown, Texas. Ch. 2, pp. 1-21.