Gene therapy strategies for X-linked myotubular myopathy

References

• Ravenscroft G, Laing NG, Bonnemann CG. Pathophysiological concepts in the congenital myopathies: blurring the boundaries, sharpening the focus. Brain. 2015;138(Pt 2):246–268.
   PubMed Web of Science ®Google Scholar
• Sewry CA, Wallgren-Pettersson C. Myopathology in congenital myopathies. Neuropathol Appl Neurobiol. 2017;43(1):5–23.
   PubMed Web of Science ®Google Scholar
• Romero NB. Centronuclear myopathies: a widening concept. Neuromuscul Disord. 2010;20(4):223–228.
   PubMed Web of Science ®Google Scholar
• 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(2):175–182.
   PubMed Web of Science ®Google Scholar
• Raess MA, Friant S, Cowling BS, et al. WANTED – dead or alive: myotubularins, a large disease-associated protein family. Adv Biol Regul. 2017;63:49–58.
   PubMedGoogle Scholar
• Amburgey K, Tsuchiya E, de Chastonay S, et al. A natural history study of X-linked myotubular myopathy. Neurology. 2017;89(13):1355–1364.
   PubMed Web of Science ®Google Scholar
• Herman GE, Finegold M, Zhao W, et al. Medical complications in long-term survivors with X-linked myotubular myopathy. J Pediatr. 1999;134(2):206–214.
   PubMed Web of Science ®Google Scholar
• Blondeau F, Laporte J, Bodin S, et al. Myotubularin, a phosphatase deficient in myotubular myopathy, acts on phosphatidylinositol 3-kinase and phosphatidylinositol 3-phosphate pathway. Hum Mol Genet. 2000;9(15):2223–2229.
   PubMed Web of Science ®Google Scholar
• Taylor GS, Maehama T, Dixon JE. Myotubularin, a protein tyrosine phosphatase mutated in myotubular myopathy, dephosphorylates the lipid second messenger, phosphatidylinositol 3-phosphate. Proc Natl Acad Sci U S A. 2000;97(16):8910–8915.
   PubMed Web of Science ®Google Scholar
• Tronchere H, Buj-Bello A, Mandel JL, et al. Implication of phosphoinositide phosphatases in genetic diseases: the case of myotubularin. Cell Mol Life Sci. 2003;60(10):2084–2099.
   PubMed Web of Science ®Google Scholar
• Di Paolo G, De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature. 2006;443(7112):651–657.
   PubMed Web of Science ®Google Scholar
• Nicot AS, Laporte J. Endosomal phosphoinositides and human diseases. Traffic. 2008;9(8):1240–1249.
   PubMed Web of Science ®Google Scholar
• Robinson FL, Dixon JE. Myotubularin phosphatases: policing 3-phosphoinositides. Trends Cell Biol. 2006;16(8):403–412.
   PubMed Web of Science ®Google Scholar
• Staiano L, De Leo MG, Persico M, et al. Mendelian disorders of PI metabolizing enzymes. Biochim Biophys Acta. 2015;1851(6):867–881.
   PubMed Web of Science ®Google Scholar
• Dowling JJ, Vreede AP, Low SE, et al. Loss of myotubularin function results in T-tubule disorganization in zebrafish and human myotubular myopathy. PLoS Genet. 2009;5(2):e1000372.
   PubMed Web of Science ®Google Scholar
• Kutchukian C, Lo Scrudato M, Tourneur Y, et al. Phosphatidylinositol 3-kinase inhibition restores Ca2+ release defects and prolongs survival in myotubularin-deficient mice. Proc Natl Acad Sci U S A. 2016;113(50):14432–14437.
   PubMed Web of Science ®Google Scholar
• Sabha N, Volpatti JR, Gonorazky H, et al. PIK3C2B inhibition improves function and prolongs survival in myotubular myopathy animal models. J Clin Invest. 2016;126(9):3613–3625.
   PubMed Web of Science ®Google Scholar
• Agrawal PB, Pierson CR, Joshi M, et al. SPEG interacts with myotubularin, and its deficiency causes centronuclear myopathy with dilated cardiomyopathy. Am J Hum Genet. 2014;95(2):218–226.
   PubMed Web of Science ®Google Scholar
• Royer B, Hnia K, Gavriilidis C, et al. The myotubularin-amphiphysin 2 complex in membrane tubulation and centronuclear myopathies. EMBO Rep. 2013;14(10):907–915.
   PubMed Web of Science ®Google Scholar
• Amoasii L, Hnia K, Chicanne G, et al. Myotubularin and PtdIns3P remodel the sarcoplasmic reticulum in muscle in vivo. J Cell Sci. 2013;126(Pt 8):1806–1819.
   PubMed Web of Science ®Google Scholar
• Dowling JJ, Joubert R, Low SE, et al. Myotubular myopathy and the neuromuscular junction: a novel therapeutic approach from mouse models. Dis Model Mech. 2012;5(6):852–859.
   PubMed Web of Science ®Google Scholar
• Robb SA, Sewry CA, Dowling JJ, et al. Impaired neuromuscular transmission and response to acetylcholinesterase inhibitors in centronuclear myopathies. Neuromuscul Disord. 2011;21(6):379–386.
   PubMed Web of Science ®Google Scholar
• 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(14):2132–2143.
   PubMed Web of Science ®Google Scholar
• Pierson CR, Dulin-Smith AN, Durban AN, et al. Modeling the human MTM1 p.R69C mutation in murine Mtm1 results in exon 4 skipping and a less severe myotubular myopathy phenotype. Hum Mol Genet. 2012;21(4):811–825.
   PubMed Web of Science ®Google Scholar
• Razidlo GL, Katafiasz D, Taylor GS. Myotubularin regulates Akt-dependent survival signaling via phosphatidylinositol 3-phosphate. J Biol Chem. 2011;286(22):20005–20019.
   PubMed Web of Science ®Google Scholar
• De Matteis MA, Luini A. Mendelian disorders of membrane trafficking. N Engl J Med. 2011;365(10):927–938.
   PubMed Web of Science ®Google Scholar
• Cowling BS, Toussaint A, Muller J, et al. Defective membrane remodeling in neuromuscular diseases: insights from animal models. PLoS Genet. 2012;8(4):e1002595.
   PubMed Web of Science ®Google Scholar
• Al-Qusairi L, Weiss N, Toussaint A, et al. T-tubule disorganization and defective excitation-contraction coupling in muscle fibers lacking myotubularin lipid phosphatase. Proc Natl Acad Sci U S A. 2009;106(44):18763–18768.
   PubMed Web of Science ®Google Scholar
• Beggs AH, Bohm J, Snead E, et al. MTM1 mutation associated with X-linked myotubular myopathy in Labrador retrievers. Proc Natl Acad Sci U S A. 2010;107(33):14697–14702.
   PubMed Web of Science ®Google Scholar
• Lawlor MW, Beggs AH, Buj-Bello A, et al. Skeletal muscle pathology in X-linked myotubular myopathy: review with cross-species comparisons. J Neuropathol Exp Neurol. 2016;75(2):102–110.
   PubMed Web of Science ®Google Scholar
• Amoasii L, Bertazzi DL, Tronchere H, et al. Phosphatase-dead myotubularin ameliorates X-linked centronuclear myopathy phenotypes in mice. PLoS Genet. 2012;8(10):e1002965.
   PubMed Web of Science ®Google Scholar
• Hnia K, Tronchere H, Tomczak KK, et al. Myotubularin controls desmin intermediate filament architecture and mitochondrial dynamics in human and mouse skeletal muscle. J Clin Invest. 2011;121(1):70–85.
   PubMed Web of Science ®Google Scholar
• Amoasii L, Hnia K, Laporte J. Myotubularin phosphoinositide phosphatases in human diseases. Curr Top Microbiol Immunol. 2012;362:209–233.
   PubMed Web of Science ®Google Scholar
• Cowling BS, Chevremont T, Prokic I, et al. Reducing dynamin 2 expression rescues X-linked centronuclear myopathy. J Clin Invest. 2014;124(3):1350–1363.
   PubMed Web of Science ®Google Scholar
• Romero NB, Clarke NF. Congenital myopathies. Handb Clin Neurol. 2013;113:1321–1336.
   PubMedGoogle Scholar
• Wang Y, Pessin JE. Mechanisms for fiber-type specificity of skeletal muscle atrophy. Curr Opin Clin Nutr Metab Care. 2013;16(3):243–250.
   PubMed Web of Science ®Google Scholar
• Schiaffino S, Mammucari C. Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skelet Muscle. 2011;1(1):4.
   PubMed Web of Science ®Google Scholar
• Perera S, Mankoo B, Gautel M. Developmental regulation of MURF E3 ubiquitin ligases in skeletal muscle. J Muscle Res Cell Motil. 2012;33(2):107–122.
   PubMed Web of Science ®Google Scholar
• Velichkova M, Juan J, Kadandale P, et al. Drosophila Mtm and class II PI3K coregulate a PI(3)P pool with cortical and endolysosomal functions. J Cell Biol. 2010;190(3):407–425.
   PubMed Web of Science ®Google Scholar
• Amthor H, Hoogaars WM. Interference with myostatin/ActRIIB signaling as a therapeutic strategy for Duchenne muscular dystrophy. Curr Gene Ther. 2012;12(3):245–259.
   PubMed Web of Science ®Google Scholar
• Giannesini B, Vilmen C, Amthor H, et al. Lack of myostatin impairs mechanical performance and ATP cost of contraction in exercising mouse gastrocnemius muscle in vivo. Am J Physiol Endocrinol Metab. 2013;305(1):E33–E40.
   PubMed Web of Science ®Google Scholar
• Gungor D, Kruijshaar ME, Plug I, et al. Impact of enzyme replacement therapy on survival in adults with Pompe disease: results from a prospective international observational study. Orphanet J Rare Dis. 2013;8:49.
   PubMed Web of Science ®Google Scholar
• Lawlor MW, Armstrong D, Viola MG, et al. Enzyme replacement therapy rescues weakness and improves muscle pathology in mice with X-linked myotubular myopathy. Hum Mol Genet. 2013;22(8):1525–1538.
   PubMed Web of Science ®Google Scholar
• Colella P, Ronzitti G, Mingozzi F. Emerging issues in AAV-mediated in vivo gene therapy. Mol Ther Methods Clin Dev. 2018;8:87–104.
   PubMed Web of Science ®Google Scholar
• Grimm D, Buning H. Small but increasingly mighty: latest advances in AAV vector research, design, and evolution. Hum Gene Ther. 2017;28(11):1075–1086.
   PubMed Web of Science ®Google Scholar
• Naso MF, Tomkowicz B, Perry WL 3rd, et al. Adeno-associated virus (AAV) as a vector for gene therapy. BioDrugs. 2017;31(4):317–334.
   PubMed Web of Science ®Google Scholar
• Sharon D, Kamen A. Advancements in the design and scalable production of viral gene transfer vectors. Biotechnol Bioeng. 2018;115(1):25–40.
   PubMed Web of Science ®Google Scholar
• Guan X, Goddard MA, Mack DL, et al. Gene therapy in monogenic congenital myopathies. Methods. 2016;99:91–98.
   PubMed Web of Science ®Google Scholar
• Gregorevic P, Blankinship MJ, Chamberlain JS. Viral vectors for gene transfer to striated muscle. Curr Opin Mol Ther. 2004;6(5):491–498.
   PubMedGoogle Scholar
• Lovric J, Mano M, Zentilin L, et al. Terminal differentiation of cardiac and skeletal myocytes induces permissivity to AAV transduction by relieving inhibition imposed by DNA damage response proteins. Mol Ther. 2012;20(11):2087–2097.
   PubMed Web of Science ®Google Scholar
• Asokan A, Conway JC, Phillips JL, et al. Reengineering a receptor footprint of adeno-associated virus enables selective and systemic gene transfer to muscle. Nat Biotechnol. 2010;28(1):79–82.
   PubMed Web of Science ®Google Scholar
• Pulicherla N, Shen S, Yadav S, et al. Engineering liver-detargeted AAV9 vectors for cardiac and musculoskeletal gene transfer. Mol Ther. 2011;19(6):1070–1078.
   PubMed Web of Science ®Google Scholar
• Qiao C, Zhang W, Yuan Z, et al. Adeno-associated virus serotype 6 capsid tyrosine-to-phenylalanine mutations improve gene transfer to skeletal muscle. Hum Gene Ther. 2010;21(10):1343–1348.
   PubMed Web of Science ®Google Scholar
• Mingozzi F, High KA. Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat Rev Genet. 2011;12(5):341–355.
   PubMed Web of Science ®Google Scholar
• 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;6(220):220ra210.
   Web of Science ®Google Scholar
• Acsadi G, Dickson G, Love DR, et al. Human dystrophin expression in mdx mice after intramuscular injection of DNA constructs. Nature. 1991;352(6338):815–818.
   PubMed Web of Science ®Google Scholar
• Conlon TJ, Erger K, Porvasnik S, et al. Preclinical toxicology and biodistribution studies of recombinant adeno-associated virus 1 human acid alpha-glucosidase. Hum Gene Ther Clin Dev. 2013;24(3):127–133.
   PubMed Web of Science ®Google Scholar
• Hoshijima M, Ikeda Y, Iwanaga Y, et al. Chronic suppression of heart-failure progression by a pseudophosphorylated mutant of phospholamban via in vivo cardiac rAAV gene delivery. Nat Med. 2002;8(8):864–871.
   PubMed Web of Science ®Google Scholar
• Fan Z, Kocis K, Valley R, et al. Safety and feasibility of high-pressure transvenous limb perfusion with 0.9% saline in human muscular dystrophy. Mol Ther. 2012;20(2):456–461.
   PubMed Web of Science ®Google Scholar
• Gregorevic P, Blankinship MJ, Allen JM, et al. Systemic delivery of genes to striated muscles using adeno-associated viral vectors. Nat Med. 2004;10(8):828–834.
   PubMed Web of Science ®Google Scholar
• 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(12):1944–1952.
   PubMed Web of Science ®Google Scholar
• Arruda VR. The role of immunosuppression in gene- and cell-based treatments for duchenne muscular dystrophy. Mol Ther. 2007;15(6):1040–1041.
   PubMed Web of Science ®Google Scholar
• Arruda VR, Stedman HH, Haurigot V, et al. Peripheral transvenular delivery of adeno-associated viral vectors to skeletal muscle as a novel therapy for hemophilia B. Blood. 2010;115(23):4678–4688.
   PubMed Web of Science ®Google Scholar
• Al-Zaidy S, Rodino-Klapac L, Mendell JR. Gene therapy for muscular dystrophy: moving the field forward. Pediatr Neurol. 2014;51(5):607–618.
   PubMed Web of Science ®Google Scholar
• Chamberlain JR, Chamberlain JS. Progress toward gene therapy for Duchenne muscular dystrophy. Mol Ther. 2017;25(5):1125–1131.
   PubMed Web of Science ®Google Scholar
• Begley MJ, Dixon JE. The structure and regulation of myotubularin phosphatases. Curr Opin Struct Biol. 2005;15(6):614–620.
   PubMed Web of Science ®Google Scholar
• Elverman M, Goddard MA, Mack D, et al. Long-term effects of systemic gene therapy in a canine model of myotubular myopathy. Muscle Nerve. 2017;56(5):943–953.
   PubMed Web of Science ®Google Scholar
• 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(4):839–854.
   PubMed Web of Science ®Google Scholar
• Nowend KL, Starr-Moss AN, Murphy KE. The function of dog models in developing gene therapy strategies for human health. Mamm Genome. 2011;22(7–8):476–485.
   PubMed Web of Science ®Google Scholar
• Smith BK, Goddard M, Childers MK. Respiratory assessment in centronuclear myopathies. Muscle Nerve. 2014;50(3):315–326.
   PubMed Web of Science ®Google Scholar
• Shelton GD, Rider BE, Child G, et al. X-linked myotubular myopathy in Rottweiler dogs is caused by a missense mutation in Exon 11 of the MTM1 gene. Skelet Muscle. 2015;5(1):1.
   PubMed Web of Science ®Google Scholar
• Lawlor MW, Read BP, Edelstein R, et al. Inhibition of activin receptor type IIb increases strength and lifespan in myotubularin-deficient mice. Am J Pathol. 2011;178(2):784–793.
   PubMed Web of Science ®Google Scholar
• Mingozzi F, High KA. Overcoming the host immune response to adeno-associated virus gene delivery vectors: the race between clearance, tolerance, neutralization, and escape. Annu Rev Virol. 2017;4(1):511–534.
   PubMed Web of Science ®Google Scholar
• Flanigan KM, Campbell K, Viollet L, et al. Anti-dystrophin T cell responses in Duchenne muscular dystrophy: prevalence and a glucocorticoid treatment effect. Hum Gene Ther. 2013;24(9):797–806.
   PubMed Web of Science ®Google Scholar
• Halbert CL, Rutledge EA, Allen JM, et al. Repeat transduction in the mouse lung by using adeno-associated virus vectors with different serotypes. J Virol. 2000;74(3):1524–1532.
   PubMed Web of Science ®Google Scholar
• Mendell JR, Campbell K, Rodino-Klapac L, et al. Dystrophin immunity in Duchenne’s muscular dystrophy. N Engl J Med. 2010;363(15):1429–1437.
   PubMed Web of Science ®Google Scholar
• Mendell JR, Rodino-Klapac LR, Rosales XQ, et al. Sustained alpha-sarcoglycan gene expression after gene transfer in limb-girdle muscular dystrophy, type 2D. Ann Neurol. 2010;68(5):629–638.
   PubMed Web of Science ®Google Scholar
• Mendell JR, Rodino-Klapac LR, Rosales-Quintero X, et al. Limb-girdle muscular dystrophy type 2D gene therapy restores alpha-sarcoglycan and associated proteins. Ann Neurol. 2009;66(3):290–297.
   PubMed Web of Science ®Google Scholar
• Toromanoff A, Adjali O, Larcher T, et al. Lack of immunotoxicity after regional intravenous (RI) delivery of rAAV to nonhuman primate skeletal muscle. Mol Ther. 2010;18(1):151–160.
   PubMed Web of Science ®Google Scholar
• Toromanoff A, Cherel Y, Guilbaud M, et al. Safety and efficacy of regional intravenous (RI) versus intramuscular (IM) delivery of rAAV1 and rAAV8 to nonhuman primate skeletal muscle. Mol Ther. 2008;16(7):1291–1299.
   Web of Science ®Google Scholar
• Boutin S, Monteilhet V, Veron P, et al. Prevalence of serum IgG and neutralizing factors against adeno-associated virus (AAV) types 1, 2, 5, 6, 8, and 9 in the healthy population: implications for gene therapy using AAV vectors. Hum Gene Ther. 2010;21(6):704–712.
   PubMed Web of Science ®Google Scholar
• Calcedo R, Morizono H, Wang L, et al. Adeno-associated virus antibody profiles in newborns, children, and adolescents. Clin Vaccine Immunol. 2011;18(9):1586–1588.
   PubMed Web of Science ®Google Scholar
• Erles K, Sebokova P, Schlehofer JR. Update on the prevalence of serum antibodies (IgG and IgM) to adeno-associated virus (AAV). J Med Virol. 1999;59(3):406–411.
   PubMed Web of Science ®Google Scholar
• Jiang H, Couto LB, Patarroyo-White S, et al. Effects of transient immunosuppression on adenoassociated, virus-mediated, liver-directed gene transfer in rhesus macaques and implications for human gene therapy. Blood. 2006;108(10):3321–3328.
   PubMed Web of Science ®Google Scholar
• Li C, Narkbunnam N, Samulski RJ, et al. Joint outcome study I: neutralizing antibodies against adeno-associated virus examined prospectively in pediatric patients with hemophilia. Gene Ther. 2012;19(3):288–294.
   PubMed Web of Science ®Google Scholar