Correcting Neuromuscular Deficits with Gene Therapy in Pompe Disease

Annals of Neurology

Volumn 78, Issue 2, 2015, Pages 222-234

  Todd, Adrian G ^a   McElroy, Jessica A ^a   Grange, Robert W ^b   Fuller, David D ^c   Walter, Glenn A ^c   Byrne, Barry J ^a   Falk, Darin J ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

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

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GLUCOSIDASE; CHOLINERGIC RECEPTOR; GLYCOGEN; MESSENGER RNA;

ADENO ASSOCIATED VIRUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; ENZYME ACTIVITY; GENE EXPRESSION; GENE THERAPY; GLYCOGEN STORAGE DISEASE TYPE 2; HISTOCHEMISTRY; MOUSE; MUSCLE INNERVATION; MUSCLE STRENGTH; NERVE ENDING; NEUROMUSCULAR DISEASE; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TIBIALIS ANTERIOR MUSCLE; VIRAL GENE DELIVERY SYSTEM; ANIMAL; DEPENDOPARVOVIRUS; DISEASE MODEL; GENE VECTOR; GENETICS; HINDLIMB; INTRAMUSCULAR DRUG ADMINISTRATION; KNOCKOUT MOUSE; METABOLISM; MUSCLE ISOMETRIC CONTRACTION; NEUROMUSCULAR JUNCTION; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SKELETAL MUSCLE; TIME FACTOR;

ALPHA-GLUCOSIDASES; ANIMALS; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; GENETIC THERAPY; GENETIC VECTORS; GLYCOGEN; GLYCOGEN STORAGE DISEASE TYPE II; HINDLIMB; INJECTIONS, INTRAMUSCULAR; ISOMETRIC CONTRACTION; MICE; MICE, KNOCKOUT; MUSCLE STRENGTH; MUSCLE, SKELETAL; NEUROMUSCULAR JUNCTION; RECEPTORS, CHOLINERGIC; RNA, MESSENGER; TIME FACTORS;

EID: 84937728678     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.24433     Document Type: Article

References (49)

1. 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.
2. Raben N, Plotz P, Byrne BJ,. Acid alpha-glucosidase deficiency (glycogenosis type II, Pompe disease). Curr Mol Med 2002; 2: 145-166.
3. van der Ploeg AT, Reuser AJ,. Pompe's disease. Lancet 2008; 372: 1342-1353.
4. Falk DJ, Mah CS, Soustek MS, et al., Intrapleural administration of AAV9 improves neural and cardiorespiratory function in Pompe disease. Mol Ther 2013; 21: 1661-1667.
5. Mah C, Pacak CA, Cresawn KO, et al., Physiological correction of Pompe disease by systemic delivery of adeno-associated virus serotype 1 vectors. Mol Ther 2007; 15: 501-507.
6. Mah CS, Falk DJ, Germain SA, et al., Gel-mediated delivery of AAV1 vectors corrects ventilatory function in Pompe mice with established disease. Mol Ther 2010; 18: 502-510.
7. Raben N, Nagaraju K, Lee E, et al., Targeted disruption of the acid alpha-glucosidase gene in mice causes an illness with critical features of both infantile and adult human glycogen storage disease type II. J Biol Chem 1998; 273: 19086-19092.
8. DeRuisseau LR, Fuller DD, Qiu K, et al., Neural deficits contribute to respiratory insufficiency in Pompe disease. Proc Natl Acad Sci U S A 2009; 106: 9419-9424.
9. Elmallah MK, Falk DJ, Nayak S, et al., Sustained correction of motoneuron histopathology following intramuscular delivery of AAV in Pompe Mice. Mol Ther 2014; 22: 702-712.
10. Falk DJ, Todd AG, Lee S, et al., Peripheral nerve and neuromuscular junction pathology in Pompe disease. Hum Mol Genet 2015; 24: 625-636.
11. Bockstael O, Foust KD, Kaspar B, Tenenbaum L,. Recombinant AAV delivery to the central nervous system. Methods Mol Biol 2011; 807: 159-177.
12. Byrne BJ, Falk DJ, Pacak CA, et al., Pompe disease gene therapy. Hum Mol Genet 2011; 20: R61-R68.
13. Dellorusso C, Crawford RW, Chamberlain JS, Brooks SV,. Tibialis anterior muscles in mdx mice are highly susceptible to contraction-induced injury. J Muscle Res Cell Motil 2001; 22: 467-475.
14. Huguet A, Medja F, Nicole A, et al., Molecular, physiological, and motor performance defects in DMSXL mice carrying >1,000 CTG repeats from the human DM1 locus. PLoS Genet 2012; 8: e1003043.
15. Metzger F, Sajid W, Saenger S, et al., Separation of fast from slow anabolism by site-specific PEGylation of insulin-like growth factor I (IGF-I). J Biol Chem 2011; 286: 19501-19510.
16. Schertzer JD, Ryall JG, Lynch GS,. Systemic administration of IGF-I enhances oxidative status and reduces contraction-induced injury in skeletal muscles of mdx dystrophic mice. Am J Physiol Endocrinol Metab 2006; 291: E499-E505.
17. de Chaumont F, Dallongeville S, Chenouard N, et al., Icy: an open bioimage informatics platform for extended reproducible research. Nat Methods 2012; 9: 690-696.
18. 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: 852-859.
19. Kong L, Wang X, Choe DW, et al., Impaired synaptic vesicle release and immaturity of neuromuscular junctions in spinal muscular atrophy mice. J Neurosci 2009; 29: 842-851.
20. Joubert R, Vignaud A, Le M, et al., Site-specific Mtm1 mutagenesis by an AAV-Cre vector reveals that myotubularin is essential in adult muscle. Hum Mol Genet 2013; 22: 1856-1866.
21. Corti M, Smith BK, Falk DJ, et al., Altered activation of the tibialis anterior in individuals with pompe disease: implications for motor unit dysfunction. Muscle Nerve 2014 Sep 3. doi: 10.1002/mus.24444. [Epub ahead of print]
22. 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: 127-133.
23. Ziegler RJ, Bercury SD, Fidler J, et al., Ability of adeno-associated virus serotype 8-mediated hepatic expression of acid alpha-glucosidase to correct the biochemical and motor function deficits of presymptomatic and symptomatic Pompe mice. Hum Gene Ther 2008; 19: 609-621.
24. Corti M, Elder M, Falk D, et al., B-cell depletion is protective against anti-AAV capsid immune response: a human subject case study. Mol Ther Methods Clin Dev 2014; 1. pii: 14033.
25. Pratt SJ, Shah SB, Ward CW, et al., Recovery of altered neuromuscular junction morphology and muscle function in mdx mice after injury. Cell Mol Life Sci 2015; 72: 153-164.
26. Harris JB, Ribchester RR,. The relationship between end-plate size and transmitter release in normal and dystrophic muscles of the mouse. J Physiol 1979; 296: 245-265.
27. Muller-Felber W, Horvath R, Gempel K, et al., Late onset Pompe disease: clinical and neurophysiological spectrum of 38 patients including long-term follow-up in 18 patients. Neuromuscul Disord 2007; 17: 698-706.
28. American Association of Neuromuscular & Electrodiagnostic Medicine. Diagnostic criteria for late-onset (childhood and adult) Pompe disease. Muscle Nerve 2009; 40: 149-160.
29. Burrow TA, Bailey LA, Kinnett DG, Hopkin RJ,. Acute progression of neuromuscular findings in infantile Pompe disease. Pediatr Neurol 2010; 42: 455-458.
30. Pongratz D, Kotzner H, Hubner G, Deufel T, Wieland OH,. [Adult form of acid maltase deficiency presenting as progressive spinal muscular atrophy]. [Article in German]. Dtsch Med Wochenschr 1984; 109: 537-541.
31. Gambetti P, DiMauro S, Baker L,. Nervous system in Pompe's disease. Ultrastructure and biochemistry. J Neuropathol Exp Neurol 1971; 30: 412-430.
32. Chien YH, Hwu WL, Lee NC,. Pompe disease: early diagnosis and early treatment make a difference. Pediatr Neonatol 2013; 54: 219-227.
33. Qiu K, Falk DJ, Reier PJ, et al., Spinal delivery of AAV vector restores enzyme activity and increases ventilation in Pompe mice. Mol Ther 2012; 20: 21-27.
34. Parenti G, Fecarotta S, la Marca G, et al., A chaperone enhances blood alpha-glucosidase activity in Pompe disease patients treated with enzyme replacement therapy. Mol Ther 2014; 22: 2004-2012.
35. Kishnani PS, Nicolino M, Voit T, et al., Chinese hamster ovary cell-derived recombinant human acid alpha-glucosidase in infantile-onset Pompe disease. J Pediatr 2006; 149: 89-97.
36. Van den Hout JM, Kamphoven JH, Winkel LP, et al., Long-term intravenous treatment of Pompe disease with recombinant human alpha-glucosidase from milk. Pediatrics 2004; 113: e448-e457.
37. Klinge L, Straub V, Neudorf U, Voit T,. Enzyme replacement therapy in classical infantile pompe disease: results of a ten-month follow-up study. Neuropediatrics 2005; 36: 6-11.
38. Elmallah MK, Falk DJ, Nayak S, et al., Sustained correction of motoneuron histopathology following intramuscular delivery of AAV in pompe mice. Mol Ther 2014; 22: 702-712.
39. Foust KD, Nurre E, Montgomery CL, et al., Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat Biotechnol 2009; 27: 59-65.
40. Ahad MA, Narayanaswami P, Kasselman LJ, Rutkove SB,. The effect of subacute denervation on the electrical anisotropy of skeletal muscle: implications for clinical diagnostic testing. Clin Neurophysiol 2010; 121: 882-886.
41. Rakhilin S, Turner G, Katz M, et al., Electrical impedance as a novel biomarker of myotube atrophy and hypertrophy. J Biomol Screen 2011; 16: 565-574.
42. Horvath JJ, Austin SL, Case LE, et al., Correlation between quantitative whole-body muscle MRI and clinical muscle weakness in Pompe disease. Muscle Nerve 2015; 51: 722-730.
43. Kassardjian CD, Engel AG, Sorenson EJ,. Electromyographic findings in 37 patients with adult-onset acid maltase deficiency. Muscle Nerve 2015; 51: 759-761.
44. Zaidman CM, Wang LL, Connolly AM, et al., Electrical impedance myography in duchenne muscular dystrophy and healthy controls: a multi-center study of reliability and validity. Muscle Nerve 2015 Feb 20. doi: 10.1002/mus.24611. [Epub ahead of print]
45. Li J, Geisbush TR, Rosen GD, et al., Electrical impedance myography for the in vivo and ex vivo assessment of muscular dystrophy (mdx) mouse muscle. Muscle Nerve 2014; 49: 829-835.
46. Li J, Geisbush TR, Arnold WD, et al., A comparison of three electrophysiological methods for the assessment of disease status in a mild spinal muscular atrophy mouse model. PLoS One 2014; 9: e111428.
47. Takikita S, Schreiner C, Baum R, et al., Fiber type conversion by PGC-1alpha activates lysosomal and autophagosomal biogenesis in both unaffected and Pompe skeletal muscle. PLoS One 2010; 5: e15239.
48. Nascimbeni AC, Fanin M, Masiero E, et al., Impaired autophagy contributes to muscle atrophy in glycogen storage disease type II patients. Autophagy 2012; 8: 1697-1700.
49. Smith BK, Collins SW, Conlon TJ, et al., Phase I/II trial of adeno-associated virus-mediated alpha-glucosidase gene therapy to the diaphragm for chronic respiratory failure in Pompe disease: initial safety and ventilatory outcomes. Hum Gene Ther 2013; 24: 630-640.