Long-term effects of systemic gene therapy in a canine model of myotubular myopathy

Muscle and Nerve

Volumn 56, Issue 5, 2017, Pages 943-953

  Elverman, Matthew ^a   Goddard, Melissa A ^b   Mack, David ^a,c   Snyder, Jessica M ^c   Lawlor, Michael W ^d   Meng, Hui ^d   Beggs, Alan H ^e   Buj Bello, Ana ^f   Poulard, Karine ^f   Marsh, Anthony P ^g   Grange, Robert W ^h   Kelly, Valerie E ^a   Childers, Martin K ^a,c  

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

^b WAKE FOREST UNIVERSITY HEALTH SCIENCES   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d MEDICAL COLLEGE OF WISCONSIN   (United States)

^e BOSTON CHILDREN S HOSPITAL   (United States)

^f GÉNÉTHON   (France)

^g WAKE FOREST UNIVERSITY   (United States)

^h VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

adeno associated virus; canine; gait; gene therapy; muscle; myotubular myopathy; neuromuscular disease

Indexed keywords

ADENO ASSOCIATED VIRUS VECTOR; AGENTS ACTING ON THE PERIPHERAL NERVOUS AND NEUROMUSCULAR SYSTEMS; PROTEIN MTM1; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; BETA GLUCURONIDASE; MYOTUBULARIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CENTRONUCLEAR MYOPATHY; CONTROLLED STUDY; DOG; FEMALE; GAIT; GENE DOSAGE; GENE EXPRESSION; GENE THERAPY; MALE; MUSCLE BIOPSY; MUSCLE DISEASE; MUSCLE STRENGTH; NERVE FUNCTION; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY FUNCTION; TRANSGENE; VECTOR COPY NUMBER; ANIMAL; COMPLICATION; DEPENDOPARVOVIRUS; DISEASE MODEL; ELECTRON MICROSCOPY; GAIT DISORDERS, NEUROLOGIC; GENETIC TRANSDUCTION; GENETICS; HUMAN; LONGITUDINAL STUDY; METABOLISM; MUTATION; MYOPATHIES, STRUCTURAL, CONGENITAL; NEUROLOGIC EXAMINATION; PATHOLOGY; RESPIRATION DISORDERS; SKELETAL MUSCLE; ULTRASTRUCTURE; VETERINARY;

ADENOSINE TRIPHOSPHATASES; ANIMALS; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; DOGS; FEMALE; GAIT DISORDERS, NEUROLOGIC; GENETIC THERAPY; GLUCURONIDASE; HUMANS; LONGITUDINAL STUDIES; MICROSCOPY, ELECTRON; MUSCLE, SKELETAL; MUTATION; MYOPATHIES, STRUCTURAL, CONGENITAL; NAD; NEUROLOGIC EXAMINATION; PROTEIN TYROSINE PHOSPHATASES, NON-RECEPTOR; RESPIRATION DISORDERS; TRANSDUCTION, GENETIC;

EID: 85019894779     PISSN: 0148639X     EISSN: 10974598     Source Type: Journal    
DOI: 10.1002/mus.25658     Document Type: Article

References (45)

1. Jungbluth H, Wallgren-Pettersson C, Laporte J. Centronuclear (myotubular) myopathy. Orphanet J Rare Dis 2008;3:26.
2. Biancalana V, Beggs AH, Das S, Jungbluth H, Kress W, Nishino I, et al. Clinical utility gene card for: centronuclear and myotubular myopathies. Eur J Hum Genet 2012;20. doi: 10.1038/ejhg.2012.91.
3. Amburgey K, McNamara N, Bennett LR, McCormick ME, Acsadi G, Dowling JJ. Prevalence of congenital myopathies in a representative pediatric united states population. Ann Neurol 2011;70:662–665.
4. Laporte J, Hu LJ, Kretz C, Mandel JL, Kioschis P, Coy JF, 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.
5. Laporte J, Guiraud-Chaumeil C, Tanner SM, Blondeau F, Hu LJ, Vicaire S, et al. Genomic organization of the MTM1 gene implicated in X-linked myotubular myopathy. Eur J Hum Genet 1998;6:325–330.
6. Kim SA, Taylor GS, Torgersen KM, Dixon JE. Myotubularin and MTMR2, phosphatidylinositol 3-phosphatases mutated in myotubular myopathy and type 4B Charcot-Marie-Tooth disease. J Biol Chem 2002;277:4526–4531.
7. Wallgren-Pettersson C, Clarke A, Samson F, Fardeau M, Dubowitz V, Moser H, et al. The myotubular myopathies: differential diagnosis of the X linked recessive, autosomal dominant, and autosomal recessive forms and present state of DNA studies. J Med Genet 1995;32:673–679.
8. McEntagart M, Parsons G, Buj-Bello A, Biancalana V, Fenton I, Little M, et al. Genotype-phenotype correlations in X-linked myotubular myopathy. Neuromuscul Disord 2002;12:939–946.
9. Kristiansen M, Knudsen GP, Tanner SM, McEntagart M, Jungbluth H, Muntoni F, et al. X-inactivation patterns in carriers of X-linked myotubular myopathy. Neuromuscul Disord 2003;13:468–471.
10. van Wijngaarden GK, Fleury P, Bethlem J, Meijer AE. Familial “myotubular” myopathy. Neurology 1969;19:901–908.
11. Herman GE, Kopacz K, Zhao W, Mills PL, Metzenberg A, Das S. Characterization of mutations in fifty North American patients with X-linked myotubular myopathy. Hum Mutat 2002;19:114–121.
12. Yu S, Manson J, White S, Bourne A, Waddy H, Davis M, et al. X-linked myotubular myopathy in a family with three adult survivors. Clin Genet 2003;64:148–152.
13. Biancalana V, Caron O, Gallati S, Baas F, Kress W, Novelli G, et al. Characterisation of mutations in 77 patients with X-linked myotubular myopathy, including a family with a very mild phenotype. Hum Genet 2003;112:135–142.
14. Hoffjan S, Thiels C, Vorgerd M, Neuen-Jacob E, Epplen JT, Kress W. Extreme phenotypic variability in a German family with X-linked myotubular myopathy associated with E404K mutation in MTM1. Neuromuscul Disord 2006;16:749–753.
15. Beggs AH, Böhm J, Snead E, Kozlowski M, Maurer M, Minor K, et al. MTM1 mutation associated with X-linked myotubular myopathy in Labrador Retrievers. Proc Natl Acad Sci U S A 2010;107:14697–14702.
16. Cosford KL, Taylor SM, Thompson L, Shelton GD. A possible new inherited myopathy in a young Labrador retriever. Can Vet J 2008;49:393–397.
17. Amoasii L, Hnia K, Chicanne G, Brech A, Cowling BS, Müller MM, et al. Myotubularin and PtdIns3P remodel the sarcoplasmic reticulum in muscle in vivo. J Cell Sci 2013;126(Pt 8):1806–1819.
18. Snead EC, Taylor SM, van der Kooij M, Cosford K, Beggs AH, Shelton GD. Clinical phenotype of x-linked myotubular myopathy in labrador retriever puppies. J Vet Intern Med 2015;29:254–260.
19. Snyder JM, Meisner A, Mack D, Goddard M, Coulter IT, Grange R, et al. Validity of a neurological scoring system for canine X-linked myotubular myopathy. Hum Gene Ther Clin Dev 2015;26:131–137.
20. Goddard MA, Mack DL, Czerniecki SM, Kelly VE, Snyder JM, Grange RW, et al. Muscle pathology, limb strength, walking gait, respiratory function and neurological impairment establish disease progression in the p.N155K canine model of X-linked myotubular myopathy. Ann Transl Med 2015;3:262–278.
21. Grange RW, Doering J, Mitchell E, Holder MN, Guan X, Goddard M, et al. Muscle function in A canine model of X-linked myotubular myopathy. Muscle Nerve 2012;46:588–591.
22. Childers MK, Joubert R, Poulard K, Moal C, Grange RW, Doering JA, et al. Gene therapy prolongs survival and restores function in murine and canine models of myotubular myopathy. Sci Transl Med 2014;6:220ra210.
23. Goddard MA, Burlingame E, Beggs AH, Buj-Bello A, Childers MK, Marsh AP, et al. Gait characteristics in a canine model of X-linked myotubular myopathy. J Neurol Sci 2014;346:221–226.
24. van der Krogt MM, Delp SL, Schwartz MH. How robust is human gait to muscle weakness? Gait Posture 2012;36:113–119.
25. Fan Z, Kocis K, Valley R, Howard JF, Chopra M, An H, et al. Safety and feasibility of high-pressure transvenous limb perfusion with 0.9% saline in human muscular dystrophy. Mol Ther 2012;20:456–461.
26. Scott OM, Hyde SA, Goddard C, Dubowitz V. Quantitation of muscle function in children: a prospective study in Duchenne muscular dystrophy. Muscle Nerve 1982;5:291–301.
27. Marsh AP, Eggebeen JD, Kornegay JN, Markert CD, Childers MK. Kinematics of gait in golden retriever muscular dystrophy. Neuromuscul Disord 2010;20:16–20.
28. Barthélémy I, Pinto-Mariz F, Yada E, Desquilbet L, Savino W, Silva-Barbosa SD, et al. Predictive markers of clinical outcome in the GRMD dog model of Duchenne muscular dystrophy. Dis Model Mech 2014;7:1253–1261.
29. Harris GF, Wertsch JJ. Procedures for gait analysis. Arch Phys Med Rehabil 1994;75:216–225.
30. Gillette RL, Angle TC. Recent developments in canine locomotor analysis: a review. Vet J 2008;178:165–176.
31. Light VA, Steiss JE, Montgomery RD, Rumph PF, Wright JC. Temporal-spatial gait analysis by use of a portable walkway system in healthy Labrador Retrievers at a walk. Am J Vet Res 2010;71:997–1002.
32. Mack DL, Poulard K, Goddard MA, Latournerie V, Snyder JM, Grange RW, et al. Systemic AAV8-Mediated gene therapy drives whole-body correction of myotubular myopathy in dogs. Mol Ther 2017. doi: 10.1016/j.ymthe.2017.02.004
33. Cumming G. Replication and p intervals: p values predict the future only vaguely, but confidence intervals do much better. Perspect Psychol Sci 2008;3:286–300.
34. Goodman SN, Berlin JA. The use of predicted confidence-intervals when planning experiments and the misuse of power when interpreting results. Ann Intern Med 1994;121:200–206.
35. Childers MK, Grange RW, Kornegay JN. In vivo canine muscle function assay. J Vis Exp 2011(50). doi: 10.3791/262
36. Coglianese CJ, Peiss CN, Wurster RD. Rhythmic phrenic nerve activity and respiratory activity in spinal dogs. Respir Physiol 1977;29:247–254.
37. Yost CS. A new look at the respiratory stimulant doxapram. CNS Drug Rev 2006;12:236–249.
38. Miller CJ, McKiernan BC, Pace J, Fettman MJ. The effects of doxapram hydrochloride (dopram-V) on laryngeal function in healthy dogs. J Vet Intern Med 2002;16:524–528.
39. Snyder JM, Meisner A, Mack D, Goddard M, Coulter IT, Grange R, et al. Validity of a Neurological scoring system for canine X-linked myotubular myopathy. Hum Gene Ther Clin Dev 2015;26:131–137.
40. Meng H, Janssen PM, Grange RW, Yang L, Beggs AH, Swanson LC, et al. Tissue triage and freezing for models of skeletal muscle disease. J Vis Exp 2014(89). doi: 10.3791/51586
41. Lawlor MW, Armstrong D, Viola MG, Widrick JJ, Meng H, Grange RW, et al. Enzyme replacement therapy rescues weakness and improves muscle pathology in mice with X-linked myotubular myopathy. Hum Mol Genet 2013;22:1525–1538.
42. Dastgir J, Rutkowski A, Alvarez R, Cossette SA, Yan K, Hoffmann RG, et al. Common data elements for muscle biopsy reporting. Arch Pathol Lab Med 2016;140:51–65.
43. Lawlor MW, Beggs AH, Buj-Bello A, Childers MK, Dowling JJ, James ES, et al. Skeletal muscle pathology in X-linked myotubular myopathy: review with cross-species comparisons. J Neuropathol Exp Neurol 2016;75:102–110.
44. Bilney B, Morris M, Webster K. Concurrent related validity of the GAITRite walkway system for quantification of the spatial and temporal parameters of gait. Gait Posture 2003;17:68–74.
45. Marsolais GS, McLean S, Derrick T, Conzemius MG. Kinematic analysis of the hind limb during swimming and walking in healthy dogs and dogs with surgically corrected cranial cruciate ligament rupture. J Am Vet Med Assoc 2003;222:739–743.