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Review

The progress of AAV-mediated gene therapy in neuromuscular disorders

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Pages 681-693 | Received 05 Feb 2018, Accepted 18 May 2018, Published online: 04 Jun 2018

References

  • Wang D, Zhong L, Nahid MA, et al. The potential of adeno-associated viral vectors for gene delivery to muscle tissue. Expert Opin Drug Deliv. 2014;11:345–364.
  • Atchison RW, Casto BC, Hammon WM. Adenovirus-associated defective virus particles. Sci (80-.). 1965;149:754–756.
  • Kotin RM, Linden RM, Berns KI. Characterization of a preferred site on human chromosome 19q for integration of adeno-associated virus DNA by non-homologous recombination. EMBO J. 1992;11:5071–5078.
  • Koczot FJ, Carter BJ, Garon CF, et al. Self-complementarity of terminal sequences within plus or minus strands of adenovirus-associated virus DNA. PNAS. 1973;70:215–219.
  • Sonntag F, Schmidt K, Kleinschmidt JA. A viral assembly factor promotes AAV2 capsid formation in the nucleolus. PNAS. 2010;107:10220–10225.
  • Hermonat PL, Muzyczka N. Use of adeno-associated virus as a mammalian DNA cloning vector: transduction of neomycin resistance into mammalian tissue culture cells. PNAS. 1984;81:6466–6470.
  • Samulski RJ, Chang LS, Shenk T. Helper-free stocks of recombinant adeno-associated viruses: normal integration does not require viral gene expression. J Virol. 1989;63:3822–3828.
  • Jacobson SG, Cideciyan AV, Roman AJ, et al. Improvement and decline in vision with gene therapy in childhood blindness. N Engl J Med. 2015;372:1920–1926.
  • Kotterman MA, Chalberg TW, Schaffer DV. Viral vectors for gene therapy: translational and clinical outlook. Annu Rev Biomed Eng. 2015;17:63–89.
  • Nathwani AC, Reiss UM, Tuddenham EG, et al. Long-term safety and efficacy of factor IX gene therapy in hemophilia B. N Engl J Med. 2014;371:1994–2004.
  • Mendell JR, Sahenk Z, Malik V, et al. A phase 1/2a follistatin gene therapy trial for Becker muscular dystrophy. Mol Ther. 2015;23:192–201.
  • Srivastava A. In vivo tissue-tropism of adeno-associated viral vectors. Curr Opin Virol. 2016;21:75–80.
  • Duan D, Sharma P, Yang J, et al. Circular intermediates of recombinant adeno-associated virus have defined structural characteristics responsible for long-term episomal persistence in muscle tissue. J Virol. 1998;72:8568–8577.
  • McCarty DM, Monahan PE, Samulski RJ. Self-complementary recombinant adeno-associated virus (scAAV) vectors promote efficient transduction independently of DNA synthesis. Gene Ther. 2001;8:1248–1254.
  • Hagedorn C, Schnödt M, Boehme P, et al. S/MAR element facilitates episomal long-term persistence of adeno-associated viral (AAV) vector genomes in proliferating cells. Hum Gene Ther. 2017;28:1169–1179.
  • Flanigan KM. The muscular dystrophies. Semin Neurol. 2012;32:255–263.
  • Koenig M, Hoffman EP, Bertelsons CJ, et al. Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell. 1987;50:509–517.
  • Hoffman EP, Brown RH, Kunkel LM. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell. 1987;51:919–928.
  • England SB, Nicholson LV, Johnson MA, et al. Very mild muscular dystrophy associated with the deletion of 46% of dystrophin. Nature. 1990;343:180–182.
  • Clemens PR, Krause TL, Chan S, et al. Recombinant truncated dystrophin minigenes: construction, expression, and adenoviral delivery. Hum Gene Ther. 1995;6:1477–1485.
  • Gregorevic P, Allen JM, Minami E, et al. Systemic delivery of rAAV6-microdystrophin preserves muscle function and extends lifespan in a murine model of severe muscular dystrophy. Nat Med. 2006;12:787–789.
  • Wang B, Li J, Xiao X. Adeno-associated virus vector carrying human minidystrophin genes effectively ameliorates muscular dystrophy in mdx mouse model. PNAS. 2000;97:13714–13719.
  • Watchko J, O’Day T, Wang B, et al. Adeno-associated virus vector-mediated minidystrophin gene therapy improves dystrophic muscle contractile function in mdx mice. Hum Gene Ther. 2002;13:1451–1460.
  • Yue Y, Pan X, Hakim CH, et al. Safe and bodywide muscle transduction in young adult Duchenne muscular dystrophy dogs with adeno-associated virus. Hum Mol Genet. 2015;24:5880–5890.
  • Mendell JR, Campbell K, Rodino-Klapac L, et al. Dystrophin immunity in Duchenne’s muscular dystrophy. N Engl J Med. 2010;363:1429–1437.
  • Bowles DE, McPhee SW, Li C, et al. Phase 1 gene therapy for Duchenne muscular dystrophy using a translational optimized AAV vector. Mol Ther. 2012;20:443–455.
  • Yue Y, Ghosh A, Long C, et al. A single intravenous injection of adeno-associated virus serotype-9 leads to whole body skeletal muscle transduction in dogs. Mol Ther. 2008;16:1944–1952.
  • Kornegay JN, Li J, Bogan JR, et al. Widespread muscle expression of an AAV9 human mini-dystrophin vector after intravenous injection in neonatal dystrophin-deficient dogs. Mol Ther. 2010;18:1501–1508.
  • Koo T, Okada T, Athanasopoulos T, et al. Long-term functional adeno-associated virus-microdystrophin expression in the dystrophic CXMDj dog. J Gene Med. 2011;13:497–506.
  • Le Guiner C, Servais L, Montus M, et al. Long-term microdystrophin gene therapy is effective in a canine model of Duchenne muscular dystrophy. Nat Commun. 2017; [cited 2017 July 25]. DOI:10.1038/ncomms16105.
  • Wang Z, Kuhr CS, Allen JM, et al. 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.
  • Rodino-Klapac LR, Montgomery CL, Bremer WG, et al. Persistent expression of FLAG-tagged micro dystrophin in nonhuman primates following intramuscular and vascular delivery. Mol Ther. 2010;18:109–117.
  • Xu R, Camboni M, Martin PT. Postnatal overexpression of the CT GalNAc transferase inhibits muscular dystrophy in mdx mice without altering muscle growth or neuromuscular development: evidence for a utrophin-independent mechanism. Neuromuscul Disord. 2007;17:209–220.
  • Tsuchida K. Myostatin inhibition by a follistatin-derived peptide ameliorates the pathophysiology of muscular dystrophy model mice. Acta Myol. 2008;27:14–18.
  • Odom GL, Gregorevic P, Allen JM, et al. Microutrophin delivery through rAAV6 increases lifespan and improves muscle function in dystrophic dystrophin/utrophin-deficient mice. Mol Ther. 2008;16:1539–1545.
  • Pisani C, Strimpakos G, Gabanella F, et al. Utrophin up-regulation by artificial transcription factors induces muscle rescue and impacts the neuromuscular junction in mdx mice. Biochim Biophys Acta. 2018; [cited 2018 April]. DOI:10.1016/j.bbadis.2018.01.030.
  • Chicoine LG, Rodino-Klapac LR, Shao G, et al. Vascular delivery of rAAVrh74.MCK.GALGT2 to the gastrocnemius muscle of the rhesus macaque stimulates the expression of dystrophin and laminin α2 surrogates. Mol Ther. 2014;22:713–724.
  • McPherron AC, Lawler AM, Lee S-J. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature. 1997;387:83–90.
  • Kota J, Handy CR, Haidet AM, et al. Follistatin gene delivery enhances muscle growth and strength in nonhuman primates. Sci Transl Med. 2009;1:6–15.
  • Haidet AM, Rizo L, Handy C, et al. Long-term enhancement of skeletal muscle mass and strength by single gene administration of myostatin inhibitors. PNAS. 2008;105:4318–4322.
  • Amthor H, Macharia R, Navarrete R, et al. Lack of myostatin results in excessive growth but impaired force generation. PNAS. 2007;104:1835–1840.
  • Mariot V, Joubert R, Hourdé C, et al. Downregulation of myostatin pathway in neuromuscular diseases may explain challenges of anti-myostatin therapeutic approaches. Nat Commun. 2017; [cited 2017 Nov 30]. DOI:10.1038/s41467-017-01486-4.
  • Dumonceaux J, Marie S, Beley C, et al. Combination if myostatin pathway interference and dystrophin rescue enhances tetanic and specific force in dystrophic mdx mice. Mol Ther. 2010;18:881–887.
  • Nelson CE, Hakim CH, Ousterout DG, et al. In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy. Science. 2016;351:403–407.
  • Tabebordbar M, Zhu K, Cheng JKW, et al. In vivo gene editing in dystrophic mouse muscle and muscle stem cells. Science. 2016;351:407–411.
  • Long C, Amoasii L, Mireault AA, et al. Postnatal genome editing partially restores dystrophin expression in a mouse model of muscular dystrophy. Science. 2016;351:400–403.
  • El Refaey M, Xu L, Gao Y, et al. In vivo genome editing restores dystrophin expression and cardiac function in dystrophic mice. Circ Res. 2017;121:926–929.
  • Pini V, Morgan JE, Muntoni F, et al. Genome editing and muscle stem cells as a therapeutic tool for muscular dystrophies. Curr Stem Cell Rep. 2017;3:137–148.
  • Bengtsson NE, Hall JK, Odom GL, et al. Muscle-specific CRISPR/Cas9 dystrophin gene editing ameliorates pathophysiology in a mouse model for Duchenne muscular dystrophy. Nat Commun. 2017; [cited 2017 June 23]. DOI:10.1038/ncomms16007.
  • Wang JZ, Wu P, Shi ZM, et al. The AAV-mediated and RNA-guided CRISPR/Cas9 system for gene therapy of DMD and BMD. Brain Dev. 2017;39:547–556.
  • Cirak S, Arechavala-Gomeza V, Guglieri M, et al. Exon skipping and dystrophin restoration in patients with Duchenne muscular dystrophy after systemic phosphorodiamidate morpholino oligomer treatment: an open-label, phase 2, dose-escalation study. Lancet. 2011;378:595–605.
  • Cirak S, Feng L, Anthony K, et al. Restoration of the dystrophin-associated glycoprotein complex after exon skipping therapy in Duchenne muscular dystrophy. Mol Ther. 2012;20:462–467.
  • Goemans NM, Tulinius M, van den Hauwe M, et al. Long-term efficacy, safety, and pharmacokinetics of drisapersen in Duchenne muscular dystrophy: results from an open-label extension study. PLoS One. 2016; [cited 2016 Sep 2]. DOI:10.1371/journal.pone.0161955.
  • Stefanovic B, Hackl W, Lührmann R, et al. Assembly, nuclear import and function of U7 snRNPs studied by microinjection of synthetic U7 RNA into Xenopus oocytes. Nucleic Acids Res. 1995;23:3141–3151.
  • Goyenvalle A, Vulin A, Fougerousse F, et al. Rescue of dystrophic muscle through U7 snRNA-mediated exon skipping. Science. 2004;306:1796–1799.
  • Goyenvalle A, Babbs A, Wright J, et al. Rescue of severely affected dystrophin/utrophin-deficient mice through scAAV-U7snRNA-mediated exon skipping. Hum Mol Genet. 2012;21:2559–2571.
  • Bish LT, Sleeper MM, Forbes SC, et al. Long-term restoration of cardiac dystrophin expression in golden retriever muscular dystrophy following rAAV6-mediated exon skipping. Mol Ther. 2012;20:580–589.
  • Vulin A, Barthélémy I, Goyenvalle A, et al. Muscle function recovery in golden retriever muscular dystrophy after AAV1-U7 exon skipping. Mol Ther. 2012;20:2120–2133.
  • Lefebvre S, Bürglen L, Reboullet S, et al. Identification and characterization of a spinal muscular atrophy-determining gene. Cell. 1995;80:155–165.
  • Foust KD, Nurre E, Montgomery CL, et al. Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat Biotechnol. 2009;27:59–65.
  • Foust KD, Wang X, McGovern VL, et al. Rescue of the spinal muscular atrophy phenotype in a mouse model by early postnatal delivery of SMN. Nat Biotechnol. 2010;28:271–274.
  • Valori CF, Ning K, Wyles M, et al. Systemic delivery of scAAV9 expressing SMN prolongs survival in a model of spinal muscular atrophy. Sci Transl Med. 2010;2:35–42.
  • Benkhelifa-Ziyyat S, Besse A, Roda M, et al. Intramuscular scAAV9-SMN injection mediates widespread gene delivery to the spinal cord and decreases disease severity in SMA mice. Mol Ther. 2013;21:282–290.
  • Dominguez E, Marais T, Chatauret N, et al. Intravenous scAAV9 delivery of a codon-optimized SMN1 sequence rescues SMA mice. Human Molecular Genetics. 2011;20:681–693.
  • Passini MA, Bu J, Richards AM, et al. Translational fidelity of intrathecal delivery of self-complementary AAV9-survival motor neuron 1 for spinal muscular atrophy. Hum Gene Ther. 2014;25:619–630.
  • Duque SI, Arnold WD, Odermatt P, et al. A large animal model of spinal muscular atrophy and correction of phenotype. Ann Neurol. 2015;77:399–414.
  • Finkel RS, McDermott MP, Kaufmann P, et al. Observational study of spinal muscular atrophy type I and implications for clinical trials. Neurology. 2014;83:810–817.
  • Mendell JR, Al-Zaidy S, Shell R, et al. Single-dose gene-replacement therapy for spinal muscular atrophy. N Engl J Med. 2017;377:1713–1722.
  • Hinderer C, Katz N, Buza EL, et al. Severe toxicity in nonhuman primates and piglets following high-dose intravenous administration of an adeno-associated virus vector expressing human SMN. Hum Gene Ther. 2018;29:285–298.
  • Hordeaux J, Wang Q, Katz N, et al. The neurotropic properties of AAV-PHP.B are limited to C57BL/6J mice. Mol Ther. 2018;26:664–668.
  • Flotte TR, Büning H. Severe toxicity in nonhuman primates and piglets with systemic high-dose administration of adeno-associated virus serotype 9-like vectors: putting patients first. Hum Gene Ther. 2018;29:283–284.
  • Lorson CL, Androphy EJ. An exonic enhancer is required for inclusion of an essential exon in the SMA-determining gene SMN. Hum Mol Genet. 2000;9:259–265.
  • Nirmal K, Singh NN, Androphy EJ, et al. Splicing of a critical exon of human survival motor neuron is regulated by a unique silencer element located in the last intron. Mol Cell Biol. 2006;26:1333–1346.
  • Finkel RS, Mercuri E, Darras BT, et al. Nusinersen versus sham control in infantile-onset spinal muscular atrophy. N Engl J Med. 2017;377:1723–1732.
  • Gorman L, Mercatante DR, Kole R. Restoration of correct splicing of thalassemic β-globin pre-mRNA by modified U1 snRNAs. J Biol Chem. 2000;275:35914–35919.
  • Dal Mas A, Rogalska ME, Bussani E, et al. Improvement of SMN2 pre-mRNA processing mediated by exon-specific U1 small nuclear RNA. Am J Hum Genet. 2015;96:93–103.
  • Marquis J, Meyer K, Angehrn L, et al. Spinal muscular atrophy: SMN2 pre-mRNA splicing corrected by a U7 snRNA derivative carrying a splicing enhancer sequence. Mol Ther. 2007;15:1479–1486.
  • Odermatt P, Trüb J, Furrer L, et al. Somatic therapy of a mouse SMA model with a U7 snRNA gene correcting SMN2 splicing. Mol Ther. 2016;24:1797–1805.
  • Mayer K, Ferraiuolo L, Schmelzer L, et al. Improving single injection CSF delivery of AAV9-mediated gene therapy for SMA: a dose-response study in mice and nonhuman primates. Mol Ther. 2015;23:477–487.
  • Victor M, Hayes R, Adams RD. Oculopharyngeal muscular dystrophy. A familial disease of late life characterized by dysphagia and progressive ptosis of the eyelids. N Engl J Med. 1962;267:1267–1272.
  • Brais B, Bouchard JP, Xie YG, et al. Short GCG expansions in the PABP2 gene cause oculopharyngeal muscular dystrophy. Nat Genet. 1998;18:164–167.
  • Tomé FM, Fardeau M. Nuclear inclusions in oculopharyngeal dystrophy. Acta Neuropathol. 1980;49:85–87.
  • Malerba A, Klein P, Bachtarzi H, et al. PABPN1 gene therapy for oculopharyngeal muscular dystrophy. Nat Commun. 2017;8:14848.
  • Strings V, Malerba A, Harbaran S, et al. “Silence and replace”: development of a single AAV vector system for the treatment of oculopharyngeal muscular dystrophy (OPMD). Hum Gene Ther. 2017;12:A1–A125.
  • McEntagart M, Parsons G, Buj-Bello A, et al. Genotype-phenotype correlations in X-linked myotubular myopathy. Neuromuscul Disord. 2002;12:939–946.
  • Laporte J, Hu LJ, Kretz C, et al. A gene mutated in X-linked myotubular myopathy defines a new putative tyrosine phosphatase family conserved in yeast. Nat Genet. 1996;13:175–182.
  • Cui X, De Vivo I, Slany R, et al. Association of SET domain and myotubularin-related proteins modulates growth control. Nat Genet. 1998;18:331–337.
  • Taylor GS, Maehama T, Dixon JE. Myotubularin, a protein tyrosine phosphatase mutated in myotubular myopathy, dephosphorylates the lipid second messenger, phosphatidylinositol 3-phosphate. PNAS. 2000;97:8910–8915.
  • Gurgel-Giannetti J, Zanoteli E, de Castro Concentino EL, et al. Necklace fibers as histopathological marker in a patient with severe form of X-linked myotubular myopathy. Neuromuscul Disord. 2012;22:541–545.
  • Buj-Bello A, Fougerousse F, Schwab Y, et al. AAV-mediated intramuscular delivery of myotubularin corrects the myotubular myopathy phenotype in targeted murine muscle and suggests a function in plasma membrane homeostasis. Hum Mol Genet. 2008;17:2132–2143.
  • Childers MK, Joubert R, Poulard K, et al. Gene therapy prolongs survival and restores function in murine and canine models of myotubular myopathy. Sci Transl Med. 2014; [cited 2014 Jan 22]. DOI:10.1126/scitranslmed.3007523.
  • Mack DL, Poulard K, Goddard MA, et al. Systemic AAV8-mediated gene therapy drives whole-body correction of myotubular myopathy in dogs. Mol Ther. 2017;25:839–854.
  • Hollinger K, Chamberlain JS. Viral vector-mediated gene therapies. Curr Opin Neurol. 2015;28:522–527.
  • Sintusek P, Catapano F, Angkathunkayul N, et al. Histopathological defects in intestine in severe spinal muscular atrophy mice are improved by systemic antisense oligonucleotide treatment. PLoS One. 2016; [cited 2016 May 10]. DOI:10.1371/journal.pone.0155032.
  • Somers E, Lees RD, Hoban K, et al. Vascular defects and spinal cord hypoxia in spinal muscular atrophy. Ann Neurol. 2016;79:217–230.
  • Hamilton G, Gilingwater TH. Spinal muscular atrophy: going beyond the motor neuron. Trends Mol Med. 2013;19:40–50.
  • Zhou H, Meng J, Marrosu E, et al. Repeated low doses of morpholino antisense oligomer: an intermediate mouse model of spinal muscular atrophy to explore the window of therapeutic response. Hum Mol Genet. 2015;24:6265–6277.
  • Goncalves MA, van Nierop GP, Tijssen MR, et al. Transfer of the full-length dystrophin-coding sequence into muscle cells by a dual high-capacity hybrid viral vector with site-specific integration ability. J Virol. 2005;79:3146–3162.
  • Lostal W, Kodippili K, Yue Y, et al. Full-length dystrophin reconstitution with adeno-associated viral vectors. Hum Gene Ther. 2014;25:552–562.
  • Koo T, Popplewell L, Athanasopoulos T, et al. Triple trans-splicing adeno-associated virus vectors capable of transferring the coding sequence for full-length dystrophin protein into dystrophic mice. Hum Gene Ther. 2014;25:98–108.

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