Peripheral nerve and neuromuscular junction pathology in pompe disease

Human Molecular Genetics

Volumn 24, Issue 3, 2015, Pages 625-636

  Falk, Darin J ^a,b   Todd, Adrian Gary ^a,b   Lee, Sooyeon ^a   Soustek, Meghan S ^a,b   Elmallah, Mai K ^a   Fuller, David D ^b   Notterpek, Lucia ^a   Byrne, Barry J ^a,b  

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

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROFILAMENT PROTEIN; GPAA1 PROTEIN, MOUSE; MEMBRANE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREATHING; CONTROLLED STUDY; DIAPHRAGM; FEMALE; GLYCOGEN STORAGE DISEASE TYPE 2; KNOCKOUT MOUSE; MALE; MOBILIZATION; MOUSE; MYOPATHY; NERVE ENDING; NERVE FIBER; NERVOUS SYSTEM; NEUROMUSCULAR SYNAPSE; NEUROPATHOLOGY; NONHUMAN; PERIPHERAL NERVE; PHENOTYPE; PHRENIC NERVE; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; SCIATIC NERVE; SKELETAL MUSCLE; TIBIALIS ANTERIOR MUSCLE; TRANSGENIC ANIMAL; WILD TYPE; ANIMAL; DISEASE MODEL; GENETICS; HUMAN; METABOLISM; PATHOLOGY; TIBIA;

ANIMALIA; MUS;

ANIMALS; DIAPHRAGM; DISEASE MODELS, ANIMAL; GLYCOGEN STORAGE DISEASE TYPE II; HUMANS; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; MUSCLE, SKELETAL; NEUROMUSCULAR JUNCTION; PHRENIC NERVE; TIBIA;

EID: 84922471642     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu476     Document Type: Article

References (56)

1. DeRuisseau, L.R., Fuller, D.D., Qiu, K., DeRuisseau, K.C., Donnelly, W.H. Jr, Mah, C., Reier, P.J. and Byrne, B.J. (2009) Neural deficits contribute to respiratory insufficiency in Pompe disease. Proc. Natl. Acad. Sci. USA, 106, 9419-9424.
2. Gambetti, P., DiMauro, S. and Baker, L. (1971) Nervous system in Pompe's disease. Ultrastructure and biochemistry. J. Neuropathol. Exp. Neurol., 30, 412-430.
3. Mah, C.S., Falk, D.J., Germain, S.A., Kelley, J.S., Lewis, M.A., Cloutier, D.A., DeRuisseau, L.R., Conlon, T.J., Cresawn, K.O., Fraites, T.J. Jr et al. (2010) Gel-mediated delivery ofAAV1vectors corrects ventilatory function in Pompe mice with established disease. Mol. Ther., 18, 502-510.
4. Lee, K.Z., Qiu, K., Sandhu, M.S., Elmallah, M.K., Falk, D.J., Lane, M.A., Reier, P.J., Byrne, B.J. and Fuller, D.D. (2011) Hypoglossal neuropathology and respiratory activity in Pompe mice. Front. Physiol., 2, 31.
5. Falk, D.J., Mah, C.S., Soustek, M.S., Lee, K.Z., Elmallah, M.K., Cloutier, D.A., Fuller, D.D. and Byrne, B.J. (2013) Intrapleural administration of AAV9 improves neural and cardiorespiratory function in Pompe disease. Mol. Ther., 21, 1661-1667.
6. Takamori, M. (2012) Structure of the neuromuscular junction: function and cooperative mechanisms in the synapse. Ann. N Y Acad. Sci., 1274, 14-23.
7. Bowerman, M., Murray, L.M., Beauvais, A., Pinheiro, B. and Kothary, R. (2012) A critical smn threshold in mice dictates onset of an intermediate spinal muscular atrophy phenotype associated with a distinct neuromuscular junction pathology. Neuromuscul. Disord., 22, 263-276.
8. Goulet, B.B., Kothary, R. and Parks, R.J. (2013) At the 'junction' of spinal muscular atrophy pathogenesis: the role of neuromuscular junction dysfunction in SMA disease progression. Curr. Mol. Med., 13, 1160-1174.
9. Jungbluth, H., Wallgren-Pettersson, C. and Laporte, J. (2008) Centronuclear (myotubular) myopathy. Orphanet. J. Rare Dis., 3, 26.
10. Dowling, J.J., Vreede, A.P., Low, S.E., Gibbs, E.M., Kuwada, J.Y., Bonnemann, C.G. and Feldman, E.L. (2009) Loss of myotubularin function results in T-tubule disorganization in zebrafish and human myotubular myopathy. PLoS Genet., 5, e1000372.
11. Dowling, J.J., Joubert, R., Low, S.E., Durban, A.N., Messaddeq, N., Li, X., Dulin-Smith, A.N., Snyder, A.D., Marshall, M.L., Marshall, J.T. et al. (2012) Myotubular myopathy and the neuromuscular junction: a novel therapeutic approach from mouse models. Dis. Model. Mech., 5, 852-859.
12. Robb, S.A., Sewry, C.A., Dowling, J.J., Feng, L., Cullup, T., Lillis, S., Abbs, S., Lees, M.M., Laporte, J., Manzur, A.Y. et al. (2011) Impaired neuromuscular transmission and response to acetylcholinesterase inhibitors in centronuclear myopathies. Neuromuscul. Disord., 21, 379-386.
13. Farah, B.L., Madden, L., Li, S., Nance, S., Bird, A., Bursac, N., Yen, P.M., Young, S.P. and Koeberl, D.D. (2014) Adjunctive beta2-agonist treatment reduces glycogen independently of receptor-mediated acid alpha-glucosidase uptake in the limb muscles of mice with Pompe disease. FASEB J., 28, 2272-2280.
14. Cardone, M., Porto, C., Tarallo, A., Vicinanza, M., Rossi, B., Polishchuk, E., Donaudy, F., Andria, G., De Matteis, M.A. and Parenti, G. (2008) Abnormal mannose-6-phosphate receptor trafficking impairs recombinant alpha-glucosidase uptake in Pompe disease fibroblasts. PathoGenetics, 1, 6.
15. Raben, N., Danon, M., Gilbert, A.L., Dwivedi, S., Collins, B., Thurberg, B.L., Mattaliano, R.J., Nagaraju, K. and Plotz, P.H. (2003) Enzyme replacement therapy in the mouse model of Pompe disease. Mol. Genet. Metab., 80, 159-169.
16. Kikuchi, T., Yang, H.W., Pennybacker, M., Ichihara, N., Mizutani, M., Van Hove, J.L. and Chen, Y.T. (1998) Clinical and metabolic correction of Pompe disease by enzyme therapy in acid maltase-deficient quail. J. Clin. Invest., 101, 827-833.
17. Fuller, D.D., ElMallah, M.K., Smith, B.K., Corti, M., Lawson, L.A., Falk, D.J. and Byrne, B.J. (2013) The respiratory neuromuscular system in Pompe disease. Respir. Physiol. Neurobiol., 189, 241-249.
18. Mellies, U. and Lofaso, F. (2009) Pompe disease: a neuromuscular disease with respiratory muscle involvement. Respir. Med., 103, 477-484.
19. Mellies, U., Ragette, R., Schwake, C., Baethmann, M., Voit, T. and Teschler, H. (2001) Sleep-disordered breathing and respiratory failure in acid maltase deficiency. Neurology, 57, 1290-1295.
20. Prigent, H., Orlikowski, D., Laforet, P., Letilly, N., Falaize, L., Pellegrini, N., Annane, D., Raphael, J.C. and Lofaso, F. (2012) Supine volume drop and diaphragmatic function in adults with Pompe disease. Eur. Respir. J., 39, 1545-1546.
21. Byrne, B.J., Falk, D.J., Pacak, C.A., Nayak, S., Herzog, R.W., Elder, M.E., Collins, S.W., Conlon, T.J., Clement, N., Cleaver, B.D. et al. (2011) Pompe disease gene therapy. Hum. Mol. Genet., 20, R61-R68.
22. Valdez, G., Tapia, J.C., Kang, H., Clemenson, G.D. Jr, Gage, F.H., Lichtman, J.W. and Sanes, J.R. (2010) Attenuation of age-related changes in mouse neuromuscular synapses by caloric restriction and exercise. Proc. Natl. Acad. Sci. USA, 107, 14863-14868.
23. Dellorusso, C., Crawford, R.W., Chamberlain, J.S. and Brooks, S.V. (2001) Tibialis anterior muscles in mdx mice are highly susceptible to contraction-induced injury. J. Muscle. Res. Cell. Motil., 22, 467-475.
24. Huguet, A., Medja, F., Nicole, A., Vignaud, A., Guiraud-Dogan, C., Ferry, A., Decostre, V., Hogrel, J.Y., Metzger, F., Hoeflich, A. et al. (2012) Molecular, physiological, and motor performance defects in DMSXL mice carrying .1, 000 CTG repeats from the human DM1 locus. PLoS Genet., 8, e1003043.
25. Metzger, F., Sajid, W., Saenger, S., Staudenmaier, C., van der Poel, C., Sobottka, B., Schuler, A., Sawitzky, M., Poirier, R., Tuerck, D. et al. (2011) Separation of fast from slow anabolism by site-specific PEGylation of insulin-like growth factor I (IGF-I). J. Biol. Chem., 286, 19501-19510.
26. Schertzer, J.D., Ryall, J.G. and Lynch, G.S. (2006) 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., 291, E499-E505.
27. Feeney, E.J., Austin, S., Chien, Y.H., Mandel, H., Schoser, B., Prater, S., Hwu, W.L., Ralston, E., Kishnani, P.S. and Raben, N. (2014) The value of muscle biopsies in Pompe disease: identifying lipofuscin inclusions in juvenile-and adult-onset patients. Acta Neuropathol. Commun., 2, 2.
28. Prater, S.N., Patel, T.T., Buckley, A.F., Mandel, H., Vlodavski, E., Banugaria, S.G., Feeney, E.J., Raben, N. and Kishnani, P.S. (2013) Skeletal muscle pathology of infantile Pompe disease during long-term enzyme replacement therapy. Orphanet J. Rare Dis., 8, 90.
29. Klionsky, D.J., Abdalla, F.C., Abeliovich, H., Abraham, R.T., Acevedo-Arozena, A., Adeli, K., Agholme, L., Agnello, M., Agostinis, P., Aguirre-Ghiso, J.A. et al. (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy, 8, 445-544.
30. Filosto, M., Todeschini, A., Cotelli, M.S., Vielmi, V., Rinaldi, F., Rota, S., Scarpelli, M.and Padovani, A. (2013) Non-muscle involvement in late-onset glycogenosis II. Acta Myol., 32, 91-94.
31. Katona, I., Weis, J. and Hanisch, F. (2014) Glycogenosome accumulation of the arrector pili muscle in Pompe disease. Orphanet J. Rare Dis., 9, 17.
32. ElMallah, M.K., Falk, D.J., Lane, M.A., Conlon, T.J., Lee, K.Z., Shafi, N.I., Reier, P.J., Byrne, B.J. and Fuller, D.D. (2012) Retrograde gene delivery to hypoglossal motoneurons using adeno-associated virus serotype 9. Hum. Gene Ther. Methods, 23, 148-156.
33. Elmallah, M.K., Falk, D.J., Nayak, S., Federico, R.A., Sandhu, M.S., Poirier, A., Byrne, B.J. and Fuller, D.D. (2013) Sustained correction of motoneuron histopathology following intramuscular delivery of AAV in Pompe mice. Mol. Ther., 22, 702-712.
34. Thurberg, B.L., Lynch Maloney, C., Vaccaro, C., Afonso, K., Tsai, A.C., Bossen, E., Kishnani, P.S. and O'Callaghan, M. (2006) Characterization of pre-and post-treatment pathology after enzyme replacement therapy for Pompe disease. Lab. Invest., 86, 1208-1220.
35. Sidman, R.L., Taksir, T., Fidler, J., Zhao, M., Dodge, J.C., Passini, M.A., Raben, N., Thurberg, B.L., Cheng, S.H. and Shihabuddin, L.S. (2008) Temporal neuropathologic and behavioral phenotype of 6neo/6neo Pompe disease mice. J. Neuropathol. Exp. Neurol., 67, 803-818.
36. Raben, N., Plotz, P. and Byrne, B.J. (2002) Acid alpha-glucosidase deficiency (glycogenosis type II, Pompe disease). Curr. Mol. Med., 2, 145-166.
37. Byrne, B.J., Kishnani, P.S., Case, L.E., Merlini, L., Muller-Felber, W., Prasad, S. and van der Ploeg, A. (2011) Pompe disease: design, methodology, and early findings from the Pompe Registry. Mol. Genet. Metab., 103, 1-11.
38. Raben, N., Wong, A., Ralston, E. and Myerowitz, R. (2012) Autophagy and mitochondria in Pompe disease: nothing is so new as what has long been forgotten. Am. J. Med. Genet. C Semin. Med. Genet., 160, 13-21.
39. Pratt, S.J., Shah, S.B., Ward, C.W., Inacio, M.P., Stains, J.P. and Lovering, R.M. (2013) Effects of in vivo injury on the neuromuscular junction in healthy and dystrophic muscles. J. Physiol., 591, 559-570.
40. Valdez, G., Tapia, J.C., Lichtman, J.W., Fox, M.A. and Sanes, J.R. (2012) Shared resistance to aging and ALS in neuromuscular junctions of specific muscles. PLoS One, 7, e34640.
41. Kong, L., Wang, X., Choe, D.W., Polley, M., Burnett, B.G., Bosch-Marce, M., Griffin, J.W., Rich, M.M. and Sumner, C.J. (2009) Impaired synaptic vesicle release and immaturity of neuromuscular junctions in spinal muscular atrophy mice. J. Neurosci., 29, 842-851.
42. Murray, L.M., Comley, L.H., Thomson, D., Parkinson, N., Talbot, K. and Gillingwater, T.H. (2008) Selective vulnerability of motor neurons and dissociation of pre-and post-synaptic pathology at the neuromuscular junction in mouse models of spinal muscular atrophy. Hum. Mol. Genet., 17, 949-962.
43. Fischer, L.R. and Glass, J.D. (2007) Axonal degeneration in motor neuron disease. Neurodegener. Dis., 4, 431-442.
44. Hunter, G., Aghamaleky Sarvestany, A., Roche, S.L., Symes, R.C. and Gillingwater, T.H. (2013) SMN-dependent intrinsic defects in Schwann cells in mouse models of spinal muscular atrophy. Hum. Mol. Genet., 23, 2235-2250.
45. Jessen, K.R. and Mirsky, R. (2010) Control of Schwann cell myelination. F1000 Biol. Rep., 2, pii: 19.
46. Trachtenberg, J.T. and Thompson, W.J. (1997) Nerve terminal withdrawal from rat neuromuscular junctions induced by neuregulin and Schwann cells. J. Neurosci., 17, 6243-6255.
47. Smith, I.W., Mikesh, M., Lee, Y. and Thompson, W.J. (2013) Terminal Schwann cells participate in the competition underlying neuromuscular synapse elimination. J. Neurosci., 33, 17724-17736.
48. Chou, H.J., Lai, D.M., Huang, C.W., McLennan, I.S., Wang, H.D. and Wang, P.Y. (2013) BMP4 is a peripherally-derived factor for motor neurons and attenuates glutamate-induced excitotoxicity in vitro. PloS One, 8, e58441.
49. Murray, L.M., Beauvais, A., Bhanot, K. and Kothary, R. (2012) Defects in neuromuscular junction remodelling in the Smn(2B/-) mouse model of spinal muscular atrophy. Neurobiol. Dis., 49C, 57-67.
50. Liu, J.X., Brannstrom, T., Andersen, P.M. and Pedrosa-Domellof, F. (2013) Distinct changes in synaptic protein composition at neuromuscular junctions of extraocular muscles versus limb muscles of ALS donors. PLoS One, 8, e57473.
51. Li, Y. and Thompson, W.J. (2011) Nerve terminal growth remodels neuromuscular synapses in mice following regeneration of the postsynaptic muscle fiber. J. Neurosci., 31, 13191-13203.
52. Sanes, J.R. and Lichtman, J.W. (2001) Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat. Rev. Neurosci., 2, 791-805.
53. Raben, N., Nagaraju, K., Lee, E., Kessler, P., Byrne, B., Lee, L., LaMarca, M., King, C., Ward, J., Sauer, B. et al. (1998) 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., 273, 19086-19092.
54. Fu, H., DiRosario, J., Kang, L., Muenzer, J. and McCarty, D.M. (2010) Restoration of central nervous system alpha-N-acetylglucosaminidase activity and therapeutic benefits in mucopolysaccharidosis IIIB mice by a single intracisternal recombinant adeno-associated viral type 2 vector delivery. J. Gene Med., 12, 624-633.
55. Auld, D.S. and Robitaille, R. (2003) Perisynaptic Schwann cells at the neuromuscular junction: nerve-and activity-dependent contributions to synaptic efficacy, plasticity, and reinnervation. Neuroscientist., 9, 144-157.
56. Notterpek, L., Shooter, E.M. and Snipes, G.J. (1997) Upregulation of the endosomal-lysosomal pathway in the trembler-J neuropathy. J. Neurosci., 17, 4190-4200.