Functional efficacy of dystrophin expression from plasmids delivered to mdx mice by hydrodynamic limb vein injection

Human Gene Therapy

Volumn 21, Issue 2, 2010, Pages 221-237

  Zhang, Guofeng ^a,b   Wooddell, Christine I ^b   Hegge, Julia O ^b   Griffin, Jacob B ^b   Huss, Thierry ^c   Braun, Serge ^d   Wolff, Jon A ^a,b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b Roche Madison   (United States)

^c TRANSGENE S A   (France)

^d Association Francaise Contre les Myopathies   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CREATINE KINASE; DYSTROPHIN; PLASMID DNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CREATINE KINASE BLOOD LEVEL; CYTOMEGALOVIRUS; DUCHENNE MUSCULAR DYSTROPHY; FEMALE; HINDLIMB; HYDRODYNAMICS BASED TRANSFECTION; IMMUNOHISTOCHEMISTRY; INTRON; MALE; MOUSE; MUSCLE CELL; MUSCLE FUNCTION; MUSCULAR DYSTROPHY; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PROMOTER REGION; SKELETAL MUSCLE; TREADMILL EXERCISE; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ANIMALS; DYSTROPHIN; GENE THERAPY; GENE TRANSFER TECHNIQUES; HINDLIMB; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; PLASMIDS; VEINS;

CYTOMEGALOVIRUS; MUS;

EID: 77249156215     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/hum.2009.133     Document Type: Article

References (70)

1. Acsadi, G., Dickson, G., Love, D.R., Jani, A., Walsh, F.S., Gur-usinghe, A., Wolff, J.A., and Davies, K.E. (1991). Human dystrophin expression in mdx mice after intramuscular injection of DNA constructs. Nature 352, 815-818.
2. Allamand, V., and Campbell, K.P. (2000). Animal models for muscular dystrophy: Valuable tools for the development of therapies. Hum. Mol. Genet. 9, 2459-2467.
3. Argyros, O., Wong, S.P., Niceta, M., Waddington, S.N., Howe, S.J., Coutelle, C., Miller, A.D., and Harbottle, R.P. (2008). Persistent episomal transgene expression in liver following delivery of a scaffold=matrix attachment region containing non-viral vector. Gene Ther. 15, 1593-1605.
4. Blake, D.J., Weir, A., Newey, S.E., and Davies, K.E. (2002). Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol. Rev. 82, 291-329.
5. Braun, S. (2008). Muscular gene transfer using nonviral vectors. Curr. Gene Ther. 8, 391-405.
6. Braun, S., Thioudellet, C., Rodriguez, P., Ali-Hadji, D., Perraud, F., Accart, N., Balloul, J.M., Halluard, C., Acres, B., Cavallini, B., and Pavirani, A. (2000). Immune rejection of human dys-trophin following intramuscular injections of naked DNA in mdx mice. Gene Ther. 7, 1447-1457.
7. Brussee, V., Tardif, F., and Tremblay, J.P. (1997). Muscle fibers of mdx mice are more vulnerable to exercise than those of normal mice. Neuromuscul. Disord. 7, 487-492.
8. Bulfield, G., Siller, W.G., Wight, P.A., and Moore, K.J. (1984). X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc. Natl. Acad. Sci. U. S. A. 81, 1189-1192. (Pubitemid 14171480)
9. Burdi, R., Didonna, M.P., Pignol, B., Nico, B., Mangieri, D., Rolland, J.F., Camerino, C., Zallone, A., Ferro, P., Andreetta, F., Confalonieri, P., and De Luca, A. (2006). First evaluation of the potential effectiveness in muscular dystrophy of a novel chimeric compound, BN 82270, acting as calpain-inhibitor and anti-oxidant. Neuromuscul. Disord. 16, 237-248.
10. Chen, Z.Y., He, C.Y., and Kay, M.A. (2005). Improved production and purification of minicircle DNA vector free of plasmid bacterial sequences and capable of persistent transgene expression in vivo. Hum. Gene Ther. 16, 126-131.
11. Cossu, G., and Sampaolesi, M. (2007). New therapies for Duchenne muscular dystrophy: Challenges, prospects and clinical trials. Trends Mol. Med. 13, 520-526.
12. Coulton, G.R., Morgan, J.E., Partridge, T.A., and Sloper, J.C. (1988). The mdx mouse skeletal muscle myopathy. I. A histo-logical, morphometric and biochemical investigation. Neuro-pathol. Appl. Neurobiol. 14, 53-70.
13. Danko, I., Chapman, V., and Wolff, J.A. (1992). The frequency of revertants in mdx mouse genetic models for Duchenne muscular dystrophy. Pediatr. Res. 32, 128-131.
14. Danko, I., Fritz, J.D., Latendresse, J.S., Herweijer, H., Schultz, E., and Wolff, J.A. (1993). Dystrophin expression improves myofiber survival in mdx muscle following intramuscular plasmid DNA injection. Hum. Mol. Genet. 2, 2055-2061.
15. Danko, I., Williams, P., Herweijer, H., Zhang, G., Latendresse, J.S., Bock, I., and Wolff, J.A. (1997). High expression of naked plasmid DNA in muscles of young rodents. Hum. Mol. Genet. 6, 1435-1443.
16. Darquet, A.M., Rangara, R., Kreiss, P., Schwartz, B., Naimi, S., Delaere, P., Crouzet, J., and Scherman, D. (1999). Minicircle: An improved DNA molecule for in vitro and in vivo gene transfer. Gene Ther. 6, 209-218.
17. Deconinck, N., and Dan, B. (2007). Pathophysiology of Du-chenne muscular dystrophy: Current hypotheses. Pediatr. Neurol. 36, 1-7.
18. De la Porte, S., Morin, S., and Koenig, J. (1999). Characteristics of skeletal muscle in mdx mutant mice. Int. Rev. Cytol. 191, 99-148.
19. Dellorusso, C., Crawford, R.W., Chamberlain, J.S., and Brooks, S.V. (2001). Tibialis anterior muscles in mdx mice are highly susceptible to contraction-induced injury. J. Muscle Res. Cell Motil. 22, 467-475.
20. De Luca, A., Pierno, S., Liantonio, A., Cetrone, M., Camerino, C., Fraysse, B., Mirabella, M., Servidei, S., Ruegg, U.T., and Conte Camerino, D. (2003). Enhanced dystrophic progression in mdx mice by exercise and beneficial effects of taurine and insulinlike growth factor-1. J. Pharmacol. Exper. Ther. 304, 453-463.
21. Den Dunnen, J.T., Grootscholten, P.M., Bakker, E., Blonden, L.A., Ginjaar, H.B., Wapenaar, M.C., Van Paassen, H.M., Van Broeckhoven, C., Pearson, P.L., and Van Ommen, G.J. (1989). Topography of the Duchenne muscular dystrophy (DMD) gene: FIGE and cDNA analysis of 194 cases reveals 115 deletions and 13 duplications. Am. J. Hum. Genet. 45, 835-847.
22. Denti, M.A., Rosa, A., D'Antona, G., Sthandier, O., De Angelis, F.G., Nicoletti, C., Allocca, M., Pansarasa, O., Parente, V., Musaro, A., Auricchio, A., Bottinelli, R., and Bozzoni, I. (2006). Body-wide gene therapy of Duchenne muscular dystrophy in the mdx mouse model. Proc. Natl. Acad. Sci. U. S. A. 103, 3758-3763.
23. Duan, D. (2008). Myodys, a full-length dystrophin plasmid vector for Duchenne and Becker muscular dystrophy gene therapy. Curr. Opin. Mol. Ther. 10, 86-94.
24. Durieux, A.C., Bonnefoy, R., Busso, T., and Freyssenet, D. (2004). In vivo gene electrotransfer into skeletal muscle: Effects of plasmid DNA on the occurrence and extent of muscle damage. J. Gene Med. 6, 809-816.
25. Ervasti, J.M., and Campbell, K.P. (1991). Membrane organization of the dystrophin-glycoprotein complex. Cell 66, 1121-1131.
26. Ferrer, A., Wells, K.E., and Wells, D.J. (2000). Immune responses to dystrophin: Implications for gene therapy of Duchenne muscular dystrophy. Gene Ther. 7, 1439-1446.
27. Goyenvalle, A., Vulin, A., Fougerousse, F., Leturcq, F., Kaplan, J.C., Garcia, L., and Danos, O. (2004). Rescue of dystrophic muscle through U7 snRNA-mediated exon skipping. Science 306, 1796-1799.
28. Grounds, M.D., Radley, H.G., Lynch, G.S., Nagaraju, K., and De Luca, A. (2008). Towards developing standard operating procedures for pre-clinical testing in the mdx mouse model of Duchenne muscular dystrophy. Neurobiol. Dis. 31, 1-19.
29. Hagstrom, J.E., Hegge, J., Zhang, G., Noble, M., Budker, V., Lewis, D.L., Herweijer, H., and Wolff, J.A. (2004). A facile nonviral method for delivering genes and siRNAs to skeletal muscle of mammalian limbs. Mol. Ther. 10, 386-398.
30. Hartikka, J., Sukhu, L., Buchner, C., Hazard, D., Bozoukova, V., Margalith, M., Nishioka, W.K., Wheeler, C.J., Manthorp, M., and Sawdey, M. (2001). Electroporation-facilitated delivery of plasmid DNA in skeletal muscle: Plasmid dependence of muscle damage and effect of poloxamer 188. Mol. Ther. 4, 407-415.
31. Hodgetts, S., Radley, H., Davies, M., and Grounds, M.D. (2006). Reduced necrosis of dystrophic muscle by depletion of host neutrophils, or blocking TNFa function with Etanercept in mdx mice. Neuromuscul. Disord. 16, 591-602.
32. Jiao, S., Williams, P., Berg, R.K., Hodgeman, B.A., Liu, L., Re-petto, G., and Wolff, J.A. (1992). Direct gene transfer into nonhuman primate myofibers in vivo. Hum. Gene Ther. 3, 21-33.
33. Kimura, E., Han, J.J., Li, S., Fall, B., Ra, J., Haraguchi, M., Tapscott, S.J., and Chamberlain, J.S. (2008). Cell-lineage regulated myogenesis for dystrophin replacement: A novel therapeutic approach for treatment of muscular dystrophy. Hum. Mol. Genet. 17, 2507-2517.
34. Koenig, M., Hoffman, E.P., Bertelson, C.J., Monaco, A.P., Feener, C., and Kunkel, L.M. (1987). Complete cloning of the Du-chenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell 50, 509-517.
35. Le, T.P., Coonan, K.M., Hedstrom, R.C., Charoenvit, Y., Sede-gah, M., Epstein, J.E., Kumar, S., Wang, R., Doolan, D.L., Maguire, J.D., Parker, S.E., Hobart, P., Norman, J., and Hoffman, S.L. (2000). Safety, tolerability and humoral immune responses after intramuscular administration of a malaria DNA vaccine to healthy adult volunteers. Vaccine 18, 1893-1901.
36. Lefaucheur, J.P., Pastoret, C., and Sebille, A. (1995). Phenotype of dystrophinopathy in old mdx mice. Anat. Rec. 242, 70-76.
37. Li, D., Yue, Y., and Duan, D. (2008). Preservation of muscle force in Mdx3cv mice correlates with low-level expression of a near full-length dystrophin protein. Am. J. Pathol. 172, 1332-1341.
38. Matsuda, R., Nishikawa, A., and Tanaka, H. (1995). Visualization of dystrophic muscle fibers in mdx mouse by vital staining with Evans blue: Evidence of apoptosis in dystrophin-deficient muscle. J. Biochem. 118, 959-964.
39. Matsumura, C.Y., Pertille, A., Albuquerque, T.C., Santo Neto, H., and Marques, M.J. (2009). Diltiazem and verapamil protect dystrophin-deficient muscle fibers of MDX mice from degeneration: A potential role in calcium buffering and sarcolemmal stability. Muscle Nerve 39, 167-176.
40. Matsumura, K., Ohlendieck, K., Ionasescu, V.V., Tome, F.M., Nonaka, I., Burghes, A.H., Mora, M., Kaplan, J.C., Fardeau, M., and Campbell, K.P. (1993). The role of the dystrophin-glycoprotein complex in the molecular pathogenesis of muscular dystrophies. Neuromuscul. Disord. 3, 533-535.
41. McGeachie, J.K., Grounds, M.D., Partridge, T.A., and Morgan, J.E. (1993). Age-related changes in replication of myogenic cells in mdx mice: Quantitative autoradiographic studies. J. Neurol. Sci. 119, 169-179.
42. McMahon, J.M., Wells, K.E., Bamfo, J.E., Cartwright, M.A., and Wells, D.J. (1998). Inflammatory responses following direct injection of plasmid DNA into skeletal muscle. Gene Ther. 5, 1283-1290.
43. Miao, C.H., Ohashi, K., Patijn, G.A., Meuse, L., Ye, X., Thompson, A.R., and Kay, M.A. (2000). Inclusion of the hepatic locus control region, an intron, and untranslated region increases and stabilizes hepatic factor IX gene expression in vivo but not in vitro. Mol. Ther. 1, 522-532.
44. Miura, P., and Jasmin, B.J. (2006). Utrophin upregulation for treating Duchenne or Becker muscular dystrophy: How close are we? Trends Mol. Med. 12, 122-129.
45. Monaco, A.P., Bertelson, C.J., Middlesworth, W., Colletti, C.A., Aldridge, J., Fischbeck, K.H., Bartlett, R., Pericak-Vance, M.A., Roses, A.D., and Kunkel, L.M. (1985). Detection of deletions spanning the Duchenne muscular dystrophy locus using a tightly linked DNA segment. Nature 316, 842-845.
46. Oblack, D.L., and Holder, I.A. (1979). Active immunisation of mice against muscle damage mediated by Candida albicans. J. Med. Microbiol. 12, 503-506.
47. Odom, G.L., Gregorevic, P., and Chamberlain, J.S. (2007). Viral-mediated gene therapy for the muscular dystrophies: Successes, limitations and recent advances. Biochim. Biophys. Acta 1772, 243-262.
48. Okano, T., Yoshida, K., Nakamura, A., Sasazawa, F., Oide, T., Takeda, S., and Ikeda, S. (2005). Chronic exercise accelerates the degeneration- regeneration cycle and downregulates insulin-like growth factor-1 in muscle of mdx mice. Muscle Nerve 32, 191-199.
49. Pegoraro, E., Schimke, R.N., Garcia, C., Stern, H., Cadaldini, M., Angelini, C., Barbosa, E., Carroll, J., Marks, W.A., Neville, H.E., Marks, H., Appleton, S., Toriello, H., Wessel, H.B., Donnelly, J., Bernes, S.M., Taber, J.W., Weiss, L., and Hoffman, E.P. (1995). Genetic and biochemical normalization in female carriers of Duchenne muscular dystrophy: Evidence for failure of dystrophin production in dystrophin-competent myonuclei. Neurology 45, 677-690.
50. Petrof, B.J., Shrager, J.B., Stedman, H.H., Kelly, A.M., and Sweeney, H.L. (1993). Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc. Natl. Acad. Sci. U. S. A. 90, 3710-3714.
51. Phelps, S.F., Hauser, M.A., Cole, N.M., Rafael, J.A., Hinkle, R.T., Faulkner, J.A., and Chamberlain, J.S. (1995). Expression of full-length and truncated dystrophin mini-genes in transgenic mdx mice. Hum. Mol. Genet. 4, 1251-1258.
52. Rodino-Klapac, L.R., Janssen, P.M., Montgomery, C.L., Coley, B.D., Chicoine, L.G., Clark, K.R., and Mendell, J.R. (2007). A trans-lational approach for limb vascular delivery of the micro-dys-trophin gene without high volumeorhigh pressure for treatment of Duchenne muscular dystrophy. J. Transl. Med. 5, 45.
53. Romero, N.B., Braun, S., Benveniste, O., Leturcq, F., Hogrel, J.Y., Morris, G.E., Barois, A., Eymard, B., Payan, C., Ortega, V., Boch, A.L., Lejean, L., Thioudellet, C., Mourot, B., Escot, C., Choquel, A., Recan, D., Kaplan, J.C., Dickson, G., Klatzmann, D., Molinier-Frenckel, V., Guillet, J.G., Squiban, P., Herson, S., and Fardeau, M. (2004). Phase I study of dystrophin plasmid-based gene therapy in Duchenne=Becker muscular dystrophy. Hum. Gene Ther. 15, 1065-1076.
54. Sampaolesi, M., Blot, S., D'Antona, G., Granger, N., Tonlorenzi, R., Innocenzi, A., Mognol, P., Thibaud, J.L., Galvez, B.G., Barthelemy, I., Perani, L., Mantero, S., Guttinger, M., Pansar-asa, O., Rinaldi, C., Cusella de Angelis, M.G., Torrente, Y., Bordignon, C., Bottinelli, R., and Cossu, G. (2006). Me-soangioblast stem cells ameliorate muscle function in dystro-phic dogs. Nature 444, 574-579.
55. Sebestyen, M.G., Hegge, J.O., Noble, M.A., Lewis, D.L., Her-weijer, H., and Wolff, J.A. (2007). Progress toward a nonviral gene therapy protocol for the treatment of anemia. Hum. Gene Ther. 18, 269-285.
56. Straub, V., Rafael, J.A., Chamberlain, J.S., and Campbell, K.P. (1997). Animal models for muscular dystrophy show different patterns of sarcolemmal disruption. J. Cell Biol. 139, 375-385.
57. Toumi, H., Hegge, J., Subbotin, V., Noble, M., Herweijer, H., Best, T.M., and Hagstrom, J.E. (2006). Rapid intravascular injection into limb skeletal muscle: A damage assessment study. Mol. Ther. 13, 229-236.
58. Vandebrouck, C., Martin, D., Colson-Van Schoor, M., Debaix, H., and Gailly, P. (2002). Involvement of TRPC in the abnormal calcium influx observed in dystrophic (mdx) mouse skeletal muscle fibers. J. Cell Biol. 158, 1089-1096.
59. Vigen, K.K., Hegge, J.O., Zhang, G., Mukherjee, R., Braun, S., Grist, T.M., and Wolff, J.A. (2007). Magnetic resonance imaging-monitored plasmid DNA delivery in primate limb muscle. Hum. Gene Ther. 18, 257-268.
60. Voisin, V., and De la Porte, S. (2004). Therapeutic strategies for Duchenne and Becker dystrophies. Int. Rev. Cytol. 240, 1-30.
61. Wells, D.J., Wells, K.E., Asante, E.A., Turner, G., Sunada, Y., Campbell, K.P., Walsh, F.S., and Dickson, G. (1995). Expression of human full-length and minidystrophin in transgenic mdx mice: Implications for gene therapy of Duchenne muscular dystrophy. Hum. Mol. Genet. 4, 1245-1250.
62. Wells, D.J., Maule, J., McMahon, J., Mitchell, R., Damien, E., Poole, A., and Wells, K.E. (1998). Evaluation of plasmid DNA for in vivo gene therapy: Factors affecting the number of transfected fibers. J. Pharm. Sci. 87, 763-768.
63. Wolff, J.A., Ludtke, J.J., Acsadi, G., Williams, P., and Jani, A. (1992). Long-term persistence of plasmid DNA and foreign gene expression in mouse muscle. Hum. Mol. Genet. 1, 363-369.
64. Wooddell, C.I., Van Hout, C.V., Reppen, T., Lewis, D.L., and Herweijer, H. (2005). Long-term RNA interference from optimized siRNA expression constructs in adult mice. Biochem. Biophys. Res. Commun. 334, 117-127.
65. Wooddell, C.I., Reppen, T., Wolff, J.A., and Herweijer, H. (2008). Sustained liver-specific transgene expression from the albumin promoter in mice following hydrodynamic plasmid DNA delivery. J. Gene Med. 10, 551-563.
66. Wooddell, C.I., Zhang, G., Griffin, J.B., Hegge, J.O., Huss, T., and Wolff, J.A. (2009). Use of Evans blue dye to compare limb muscles in exercised young and old mdx mice. Muscle Nerve (in press).
67. Yew, N.S., Przybylska, M., Ziegler, R.J., Liu, D., and Cheng, S.H. (2001). High and sustained transgene expression in vivo from plasmid vectors containing a hybrid ubiquitin promoter. Mol. Ther. 4, 75-82.
68. Yokota, T., Pistilli, E., Duddy, W., and Nagaraju, K. (2007). Potential of oligonucleotide-mediated exon-skipping therapy for Duchenne muscular dystrophy. Expert Opin. Biol. Ther. 7, 831-842.
69. Zhang, G., Budker, V., Williams, P., Subbotin, V., and Wolff, J.A. (2001). Efficient expression of naked DNA delivered in-traarterially to limb muscles of nonhuman primates. Hum. Gene Ther. 12, 427-438.
70. Zhang, G., Ludtke, J.J., Thioudellet, C., Kleinpeter, P., Antoniou, M., Herweijer, H., Braun, S., and Wolff, J.A. (2004). Intraarterial delivery of naked plasmid DNA expressing full-length mouse dystrophin in the mdx mouse model of Duchenne muscular dystrophy. Hum. Gene Ther. 15, 770-782.