Gene therapy for muscle disease

Experimental Cell Research

Volumn 316, Issue 18, 2010, Pages 3087-3092

  Miyagoe Suzuki, Yuko ^a   Takeda, Shin'ichi ^a  

^a NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

Author keywords

Antisense oligonucleotide; Duchenne muscular dystrophy (DMD); Dystrophin; Exon skipping; Gene therapy; Recombinant adenoassociated viral (AAV)

Indexed keywords

2' O METHYL PHOSPHOROTHIOATE OLIGOMER; ANTISENSE OLIGONUCLEOTIDE; COMPLEMENTARY DNA; DYSTROPHIN; LENTIVIRUS VECTOR; PARVOVIRUS VECTOR; PHOSPHORODIAMIDATE MORPHOLINO OLIGOMER; UNCLASSIFIED DRUG;

ADENO ASSOCIATED VIRUS; ANTISENSE THERAPY; CLINICAL TRIAL; DRUG DELIVERY SYSTEM; DRUG TOLERABILITY; DUCHENNE MUSCULAR DYSTROPHY; EXON SKIPPING; GENE EXPRESSION; GENE THERAPY; HUMAN; IN VITRO GENE TRANSFER; IN VIVO GENE TRANSFER; NONHUMAN; PRIORITY JOURNAL; REVIEW; STEM CELL; EXON; GENETICS; MUSCULAR DYSTROPHY, DUCHENNE;

DYSTROPHIN; EXONS; GENETIC THERAPY; HUMANS; MUSCULAR DYSTROPHY, DUCHENNE;

EID: 77957682833     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2010.05.022     Document Type: Review

References (48)

1. Aartsma-Rus A., Van Deutekom J.C., Fokkema I.F., Van Ommen G.J., Den Dunnen J.T. Entries in the Leiden Duchenne muscular dystrophy mutation database: an overview of mutation types and paradoxical cases that confirm the reading-frame rule. Muscle Nerve 2006, 34:135-144.
2. Campbell K.P. Three muscular dystrophies: loss of cytoskeleton-extracellular matrix linkage. Cell 1995, 80:675-679.
3. Gao G., Vandenberghe L.H., Wilson J.M. New recombinant serotypes of AAV vectors. Curr. Gene Ther. 2005, 5:285-297.
4. Trollet C., Athanasopoulos T., Popplewell L., Malerba A., Dickson G. Gene therapy for muscular dystrophy: current progress and future prospects. Expert Opin. Biol. Ther. 2009, 9:849-866.
5. Arnett A.L., Chamberlain J.R., Chamberlain J.S. Therapy for neuromuscular disorders. Curr. Opin. Genet. Dev. 2009, 19:290-297.
6. Foster K., Foster H., Dickson J.G. Gene therapy progress and prospects: Duchenne muscular dystrophy. Gene Ther. 2006, 13:1677-1685.
7. Gregorevic P., Blankinship M.J., Allen J.M., Crawford R.W., Meuse L., Miller D.G., Russell D.W., Chamberlain J.S. Systemic delivery of genes to striated muscles using adeno-associated viral vectors. Nat. Med. 2004, 10:828-834.
8. Nishiyama A., Ampong B.N., Ohshima S., Shin J.H., Nakai H., Imamura M., Miyagoe-Suzuki Y., Okada T., Takeda S. Recombinant adeno-associated virus type 8-mediated extensive therapeutic gene delivery into skeletal muscle of alpha-sarcoglycan-deficient mice. Hum. Gene Ther. 2008, 19:719-730.
9. Wang Z., Zhu T., Qiao C., Zhou L., Wang B., Zhang J., Chen C., Li J., Xiao X. Adeno-associated virus serotype 8 efficiently delivers genes to muscle and heart. Nat. Biotechnol. 2005, 23:321-328.
10. Inagaki K., Fuess S., Storm T.A., Gibson G.A., McTiernan C.F., Kay M.A., Nakai H. Robust systemic transduction with AAV9 vectors in mice: efficient global cardiac gene transfer superior to that of AAV8. Mol. Ther. 2006, 14:45-53.
11. Bish L.T., Morine K., Sleeper M.M., Sanmiguel J., Wu D., Gao G., Wilson J.M., Sweeney H.L. Adeno-associated virus (AAV) serotype 9 provides global cardiac gene transfer superior to AAV1, AAV6, AAV7, and AAV8 in the mouse and rat. Hum. Gene Ther. 2008, 19:1359-1368.
12. Pacak C.A., Mah C.S., Thattaliyath B.D., Conlon T.J., Lewis M.A., Cloutier D.E., Zolotukhin I., Tarantal A.F., Byrne B.J. Recombinant adeno-associated virus serotype 9 leads to preferential cardiac transduction in vivo. Circ. Res. 2006, 99:e3-e9.
13. Yoshimura M., Sakamoto M., Ikemoto M., Mochizuki Y., Yuasa K., Miyagoe-Suzuki Y., Takeda S. AAV vector-mediated microdystrophin expression in a relatively small percentage of mdx myofibers improved the mdx phenotype. Mol. Ther. 2004, 10:821-828.
14. Gregorevic P., Blankinship M.J., Allen J.M., Chamberlain J.S. Systemic microdystrophin gene delivery improves skeletal muscle structure and function in old dystrophic mdx mice. Mol. Ther. 2008, 16:657-664.
15. Gregorevic P., Allen J.M., Minami E., Blankinship M.J., Haraguchi M., Meuse L., Finn E., Adams M.E., Froehner S.C., Murry C.E., Chamberlain J.S. rAAV6-microdystrophin preserves muscle function and extends lifespan in severely dystrophic mice. Nat. Med. 2006, 12:787-789.
16. Townsend D., Blankinship M.J., Allen J.M., Gregorevic P., Chamberlain J.S., Metzger J.M. Systemic administration of micro-dystrophin restores cardiac geometry and prevents dobutamine-induced cardiac pump failure. Mol. Ther. 2007, 15:1086-1092.
17. Ghosh A., Yue Y., Lai Y., Duan D. A hybrid vector system expands adeno-associated viral vector packaging capacity in a transgene-independent manner. Mol. Ther. 2008, 16:124-130.
18. Yuasa K., Yoshimura M., Urasawa N., Ohshima S., Howell J.M., Nakamura A., Hijikata T., Miyagoe-Suzuki Y., Takeda S. Injection of a recombinant AAV serotype 2 into canine skeletal muscles evokes strong immune responses against transgene products. Gene Ther. 2007, 14:1249-1260.
19. Ohshima S., Shin J.H., Yuasa K., Nishiyama A., Kira J., Okada T., Takeda S. Transduction efficiency and immune response associated with the administration of AAV8 vector into dog skeletal muscle. Mol. Ther. 2009, 17:73-80.
20. Rodino-Klapac L.R., Janssen P.M., Montgomery C.L., Coley B.D., Chicoine L.G., Clark K.R., Mendell J.R. A translational approach for limb vascular delivery of the micro-dystrophin gene without high volume or high pressure for treatment of Duchenne muscular dystrophy. J. Transl. Med. 2007, 5:45.
21. Rodino-Klapac L.R., Montgomery C.L., Bremer W.G., Shontz K.M., Malik V., Davis N., Sprinkle S., Campbell K.J., Sahenk Z., Clark K.R., Walker C.M., Mendell J.R., Chicoine L.G. Persistent expression of FLAG-tagged micro dystrophin in nonhuman primates following intramuscular and vascular delivery. Mol. Ther. 2010, 18:109-117.
22. Wang Z., Allen J.M., Riddell S.R., Gregorevic P., Storb R., Tapscott S.J., Chamberlain J.S., Kuhr C.S. Immunity to adeno-associated virus-mediated gene transfer in a random-bred canine model of Duchenne muscular dystrophy. Hum. Gene Ther. 2007, 18:18-26.
23. Wang Z., Kuhr C.S., Allen J.M., Blankinship M., Gregorevic P., Chamberlain J.S., Tapscott S.J., Storb R. Sustained AAV-mediated dystrophin expression in a canine model of Duchenne muscular dystrophy with a brief course of immunosuppression. Mol. Ther. 2007, 15:1160-1166.
24. Salva M.Z., Himeda C.L., Tai P.W., Nishiuchi E., Gregorevic P., Allen J.M., Finn E.E., Nguyen Q.G., Blankinship M.J., Meuse L., Chamberlain J.S., Hauschka S.D. Design of tissue-specific regulatory cassettes for high-level rAAV-mediated expression in skeletal and cardiac muscle. Mol. Ther. 2007, 15:320-329.
25. Wang B., Li J., Fu F.H., Chen C., Zhu X., Zhou L., Jiang X., Xiao X. Construction and analysis of compact muscle-specific promoters for AAV vectors. Gene Ther. 2008, 15:1489-1499.
26. Foster H., Sharp P.S., Athanasopoulos T., Trollet C., Graham I.R., Foster K., Wells D.J., Dickson G. Codon and mRNA sequence optimization of microdystrophin transgenes improves expression and physiological outcome in dystrophic mdx mice following AAV2/8 gene transfer. Mol. Ther. 2008, 16:1825-1832.
27. Li S., Kimura E., Fall B.M., Reyes M., Angello J.C., Welikson R., Hauschka S.D., Chamberlain J.S. Stable transduction of myogenic cells with lentiviral vectors expressing a minidystrophin. Gene Ther. 2005, 12:1099-1108.
28. Ikemoto M., Fukada S., Uezumi A., Masuda S., Miyoshi H., Yamamoto H., Wada M.R., Masubuchi N., Miyagoe-Suzuki Y., Takeda S. Autologous transplantation of SM/C-2.6(+) satellite cells transduced with micro-dystrophin CS1 cDNA by lentiviral vector into mdx mice. Mol. Ther. 2007, 15:2178-2185.
29. Quenneville S.P., Chapdelaine P., Skuk D., Paradis M., Goulet M., Rousseau J., Xiao X., Garcia L., Tremblay J.P. Autologous transplantation of muscle precursor cells modified with a lentivirus for muscular dystrophy: human cells and primate models. Mol. Ther. 2007, 15:431-438.
30. Goyenvalle A., Vulin A., Fougerousse F., Leturcq F., Kaplan J.C., Garcia L., Danos O. Rescue of dystrophic muscle through U7 snRNA-mediated exon skipping. Science 2004, 306:1796-1799.
31. 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., Bozzoni I. Body-wide gene therapy of Duchenne muscular dystrophy in the mdx mouse model. Proc Natl Acad Sci U S A 2006, 103:3758-3763.
32. Wilton S.D., Fall A.M., Harding P.L., McClorey G., Coleman C., Fletcher S. Antisense oligonucleotide-induced exon skipping across the human dystrophin gene transcript. Mol. Ther. 2007, 15:1288-1296.
33. Aartsma-Rus A., van Vliet L., Hirschi M., Janson A.A., Heemskerk H., de Winter C.L., de Kimpe S., van Deutekom J.C., t Hoen P.A., van Ommen G.J. Guidelines for antisense oligonucleotide design and insight into splice-modulating mechanisms. Mol. Ther. 2009, 17:548-553.
34. Popplewell L.J., Adkin C., Arechavala-Gomeza V., Aartsma-Rus A., de Winter C.L., Wilton S.D., Morgan J.E., Muntoni F., Graham I.R., Dickson G. Comparative analysis of antisense oligonucleotide sequences targeting exon 53 of the human DMD gene: implications for future clinical trials. Neuromuscul. Disord. 2010, 20:102-110.
35. Lu Q.L., Mann C.J., Lou F., Bou-Gharios G., Morris G.E., Xue S.A., Fletcher S., Partridge T.A., Wilton S.D. Functional amounts of dystrophin produced by skipping the mutated exon in the mdx dystrophic mouse. Nat. Med. 2003, 9:1009-1014.
36. Alter J., Lou F., Rabinowitz A., Yin H., Rosenfeld J., Wilton S.D., Partridge T.A., Lu Q.L. Systemic delivery of morpholino oligonucleotide restores dystrophin expression bodywide and improves dystrophic pathology. Nat. Med. 2006, 12:175-177.
37. Yokota T., Lu Q.L., Partridge T., Kobayashi M., Nakamura A., Takeda S., Hoffman E. Efficacy of systemic morpholino exon-skipping in Duchenne dystrophy dogs. Ann. Neurol. 2009, 65:667-676.
38. Ishikawa-Sakurai M., Yoshida M., Imamura M., Davies K.E., Ozawa E. ZZ domain is essentially required for the physiological binding of dystrophin and utrophin to beta-dystroglycan. Hum. Mol. Genet. 2004, 13:693-702.
39. Aartsma-Rus A., Fokkema I., Verschuuren J., Ginjaar I., van Deutekom J., van Ommen G.J., den Dunnen J.T. Theoretic applicability of antisense-mediated exon skipping for Duchenne muscular dystrophy mutations. Hum. Mutat. 2009, 30:293-299.
40. Aartsma-Rus A., De Winter C.L., Janson A.A., Kaman W.E., Van Ommen G.J., Den Dunnen J.T., Van Deutekom J.C. Functional analysis of 114 exon-internal AONs for targeted DMD exon skipping: indication for steric hindrance of SR protein binding sites. Oligonucleotides 2005, 15:284-297.
41. Popplewell L.J., Trollet C., Dickson G., Graham I.R. Design of phosphorodiamidate morpholino oligomers (PMOs) for the induction of exon skipping of the human DMD gene. Mol. Ther. 2009, 17:554-561.
42. Kinali M., Arechavala-Gomeza V., Feng L., Cirak S., Hunt D., Adkin C., Guglieri M., Ashton E., Abbs S., Nihoyannopoulos P., Garralda M.E., Rutherford M., McCulley C., Popplewell L., Graham I.R., Dickson G., Wood M.J., Wells D.J., Wilton S.D., Kole R., Straub V., Bushby K., Sewry C., Morgan J.E., Muntoni F. Local restoration of dystrophin expression with the morpholino oligomer AVI-4658 in Duchenne muscular dystrophy: a single-blind, placebo-controlled, dose-escalation, proof-of-concept study. Lancet Neurol. 2009, 8:918-928.
43. van Deutekom J.C., Janson A.A., Ginjaar I.B., Frankhuizen W.S., Aartsma-Rus A., Bremmer-Bout M., den Dunnen J.T., Koop K., van der Kooi A.J., Goemans N.M., de Kimpe S.J., Ekhart P.F., Venneker E.H., Platenburg G.J., Verschuuren J.J., van Ommen G.J. Local dystrophin restoration with antisense oligonucleotide PRO051. N Engl J. Med. 2007, 357:2677-2686.
44. Jearawiriyapaisarn N., Moulton H.M., Buckley B., Roberts J., Sazani P., Fucharoen S., Iversen P.L., Kole R. Sustained dystrophin expression induced by peptide-conjugated morpholino oligomers in the muscles of mdx mice. Mol. Ther. 2008, 16:1624-1629.
45. Morcos P.A., Li Y., Jiang S. Vivo-Morpholinos: a non-peptide transporter delivers Morpholinos into a wide array of mouse tissues. Biotechniques 2008, 45:613-614. 616, 618 passim.
46. Aartsma-Rus A., Janson A.A., Kaman W.E., Bremmer-Bout M., van Ommen G.J., den Dunnen J.T., van Deutekom J.C. Antisense-induced multiexon skipping for Duchenne muscular dystrophy makes more sense. Am. J. Hum. Genet. 2004, 74:83-92.
47. van Vliet L., de Winter C.L., van Deutekom J.C., van Ommen G.J., Aartsma-Rus A. Assessment of the feasibility of exon 45-55 multiexon skipping for Duchenne muscular dystrophy. BMC Med. Genet. 2008, 9:105.
48. Extance A. Targeting RNA: an emerging hope for treating muscular dystrophy. Nat. Rev. Drug Discov. 2009, 8:917-918.