The craniosacral progression of muscle development influences the emergence of neuromuscular junction alterations in a severe murine model for spinal muscular atrophy

Neuropathology and Applied Neurobiology

Volumn 40, Issue 4, 2014, Pages 416-434

  Voigt, Tilman ^a   Neve, Anuja ^b   Schümperli, Daniel ^b  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF BERN   (Switzerland)

Author keywords

Development; Neuromuscular junctions; Perineurial cells; Perisynaptic Schwann cells; Skeletal muscle; Spinal muscular atrophy

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BASEMENT MEMBRANE; CAVEOLA; DIAPHRAGM; FASCICULATION; FLUORESCENCE MICROSCOPY; GASTROCNEMIUS MUSCLE; GENOTYPE; GOLGI COMPLEX; IMMUNOFLUORESCENCE; INNERVATION; INTERCOSTAL MUSCLE; KINETOSOME; MATURATION; MICROTUBULE; MITOCHONDRION SWELLING; MORPHOLOGY; MOUSE; MULTINUCLEAR CELL; MUSCLE DEVELOPMENT; MUSCLE FIBRIL; MYOTUBE; NERVE ENDING; NERVE FIBER; NEUROMUSCULAR SYNAPSE; NONHUMAN; NONMYELINATED NERVE; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; SARCOPLASM; SARCOPLASMIC RETICULUM; SCHWANN CELL; SOLEUS MUSCLE; SPINAL MUSCULAR ATROPHY; SYNAPTIC MEMBRANE; THIN FILAMENT; TISSUE DIFFERENTIATION; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; DISEASE COURSE; DISEASE MODEL; FEMALE; PATHOLOGY; SKELETAL MUSCLE; ULTRASTRUCTURE;

ANIMALS; DIAPHRAGM; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; INTERCOSTAL MUSCLES; MICE; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; MUSCULAR ATROPHY, SPINAL; NEUROMUSCULAR JUNCTION;

EID: 84898825696     PISSN: 03051846     EISSN: 13652990     Source Type: Journal    
DOI: 10.1111/nan.12064     Document Type: Article

References (61)

1. Burghes AH, Beattie CE. Spinal muscular atrophy: why do low levels of survival motor neuron protein make motor neurons sick? Nat Rev Neurosci 2009; 10: 597-609
2. Talbot K, Davies KE. Spinal muscular atrophy. Semin Neurol 2001; 21: 189-197
3. Kariya S, Park GH, Maeno-Hikichi Y, Leykekhman O, Lutz C, Arkovitz MS, Landmesser LT, Monani UR. Reduced SMN protein impairs maturation of the neuromuscular junctions in mouse models of spinal muscular atrophy. Hum Mol Genet 2008; 17: 2552-2569
4. Dachs E, Hereu M, Piedrafita L, Casanovas A, Caldero J, Esquerda JE. Defective neuromuscular junction organization and postnatal myogenesis in mice with severe spinal muscular atrophy. J Neuropathol Exp Neurol 2011; 70: 444-461
5. Lee YI, Mikesh M, Smith I, Rimer M, Thompson W. Muscles in a mouse model of spinal muscular atrophy show profound defects in neuromuscular development even in the absence of failure in neuromuscular transmission or loss of motor neurons. Dev Biol 2011; 356: 432-444
6. Murray LM, Talbot K, Gillingwater TH. Review: neuromuscular synaptic vulnerability in motor neurone disease: amyotrophic lateral sclerosis and spinal muscular atrophy. Neuropathol Appl Neurobiol 2010; 36: 133-156
7. Voigt T, Meyer K, Baum O, Schümperli D. Ultrastructural changes in diaphragm neuromuscular junctions in a severe mouse model for Spinal Muscular Atrophy and their prevention by bifunctional U7 snRNA correcting SMN2 splicing. Neuromuscul Disord 2010; 20: 744-752
8. Martinez-Hernandez R, Bernal S, Also-Rallo E, Alías L, Barceló MJ, Hereu M, Esquerda JE, Tizzano EF. Synaptic defects in type i spinal muscular atrophy in human development. J Pathol 2013; 229: 49-61
9. Monani UR, Sendtner M, Coovert DD, Parsons DW, Andreassi C, Le TT, Jablonka S, Schrank B, Rossoll W, Prior TW, Morris GE, Burghes AH. The human centromeric survival motor neuron gene (SMN2) rescues embryonic lethality in Smn(-/-) mice and results in a mouse with spinal muscular atrophy. Hum Mol Genet 2000; 9: 333-339
10. Le TT, Pham LT, Butchbach ME, Zhang HL, Monani UR, Coovert DD, Gavrilina TO, Xing L, Bassell GJ, Burghes AH. SMNDelta7, the major product of the centromeric survival motor neuron (SMN2) gene, extends survival in mice with spinal muscular atrophy and associates with full-length SMN. Hum Mol Genet 2005; 14: 845-857
11. McGovern VL, Gavrilina TO, Beattie CE, Burghes AH. Embryonic motor axon development in the severe SMA mouse. Hum Mol Genet 2008; 17: 2900-2909
12. Murray LM, Lee S, Baumer D, Parson SH, Talbot K, Gillingwater TH. Pre-symptomatic development of lower motor neuron connectivity in a mouse model of severe spinal muscular atrophy. Hum Mol Genet 2010; 19: 420-433
13. Cifuentes-Diaz C, Nicole S, Velasco ME, Borra-Cebrian C, Panozzo C, Frugier T, Millet G, Roblot N, Joshi V, Melki J. Neurofilament accumulation at the motor endplate and lack of axonal sprouting in a spinal muscular atrophy mouse model. Hum Mol Genet 2002; 11: 1439-1447
14. Murray LM, Comley LH, Thomson D, Parkinson N, Talbot K, Gillingwater TH. 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 2008; 17: 949-962
15. Ling KK, Gibbs RM, Feng Z, Ko CP. Severe neuromuscular denervation of clinically relevant muscles in a mouse model of spinal muscular atrophy. Hum Mol Genet 2012; 21: 185-195
16. Dubowitz V. Ramblings in the history of spinal muscular atrophy. Neuromuscul Disord 2009; 19: 69-73
17. Meyer K, Marquis J, Trüb J, Nlend Nlend R, Verp S, Ruepp MD, Imboden H, Barde I, Trono D, Schümperli D. Rescue of a severe mouse model for spinal muscular atrophy by U7 snRNA-mediated splicing modulation. Hum Mol Genet 2009; 18: 546-555
18. Marquis J, Meyer K, Angehrn L, Kämpfer SS, Rothen-Rutishauser B, Schümperli D. Spinal muscular atrophy: SMN2 pre-mRNA splicing corrected by a U7 snRNA derivative carrying a splicing enhancer sequence. Mol Ther 2007; 15: 1479-1486
19. Charrier S, Stockholm D, Seye K, Opolon P, Taveau M, Gross DA, Bucher-Laurent S, Delenda C, Vainchenker W, Danos O, Galy A. A lentiviral vector encoding the human Wiskott-Aldrich syndrome protein corrects immune and cytoskeletal defects in WASP knockout mice. Gene Ther 2005; 12: 597-606
20. De Troyer A, Kirkwood PA, Wilson TA. Respiratory action of the intercostal muscles. Physiol Rev 2005; 85: 717-756
21. Sieck GC, Sacks RD, Blanco CE. Absence of regional differences in the size and oxidative capacity of diaphragm muscle fibers. J Appl Physiol 1987; 63: 1076-1082
22. Richardson KC, Jarett L, Finke EH. Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol 1960; 35: 313-323
23. Lewis WH. The development of the muscular system. In Manual of Human Embryology. Eds F Keibel, F Mall. Philadelphia, PA: Lippincott, 1910; 454-552
24. Carry MR, Morita M, Nornes HO. Morphogenesis of motor endplates along the proximodistal axis of the mouse hindlimb. Anat Rec 1983; 207: 473-485
25. Duxson MJ, Ross JJ, Harris AJ. Transfer of differentiated synaptic terminals from primary myotubes to newly-formed muscle-cells during embryonic-development in the rat. Neurosci Lett 1986; 71: 147-152
26. Gamble HJ, Fenton J, Allsopp G. Electron microscope observations on human fetal striated muscle. J Anat 1978; 126: 567-589
27. Kelly AM, Zacks SI. The histogenesis of rat intercostal muscle. J Cell Biol 1969; 42: 135-153
28. Ontell M, Kozeka K. The organogenesis of murine striated-muscle - a cytoarchitectural study. Am J Anat 1984; 171: 133-148
29. Ontell M, Hughes D, Bourke D. Morphometric analysis of the developing mouse soleus muscle. Am J Anat 1988; 181: 279-288
30. Ross JJ, Duxson MJ, Harris AJ. Formation of primary and secondary myotubes in rat lumbrical muscles. Development 1987; 100: 383-394
31. Rubinstein NA, Kelly AM. Development of muscle-fiber specialization in the rat hindlimb. J Cell Biol 1981; 90: 128-144
32. Teravainen H. Development of the myoneural junction in the rat. Z Zellforsch Mikrosk Anat 1968; 87: 249-265
33. Witzemann V. Development of the neuromuscular junction. Cell Tissue Res 2006; 326: 263-271
34. Chen FJ, Liu Y, Sugiura Y, Allen PD, Gregg RG, Lin WC. Neuromuscular synaptic patterning requires the function of skeletal muscle dihydropyridine receptors. Nat Neurosci 2011; 14: 570-U52
35. Ontell M, Bourke D, Hughes D. Cytoarchitecture of the fetal murine soleus muscle. Am J Anat 1988; 181: 267-278
36. Desaki J, Uehara Y. Formation and maturation of subneural apparatuses at neuromuscular-junctions in postnatal rats - a scanning and transmission electron-microscopic study. Dev Biol 1987; 119: 390-401
37. Vautrin J, Mambrini J. Synaptic current between neuromuscular junction folds. J Theor Biol 1989; 140: 479-498
38. Voigt T, Dauber W, Härtel X, Schönemann R. On the connections between the T-System and the subsynaptic folds in the motor end plate of amphibians. J Neurocytol 2000; 30: 157-164
39. Dauber W, Voigt T, Härtel X, Meyer J. The t-tubular network and its triads in the sole plate sarcoplasm of the motor end-plate of mammals. J Muscle Res Cell Motil 2000; 21: 443-449
40. Kelly AM. Sarcoplasmic reticulum and T tubules in differentiating rat skeletal muscle. J Cell Biol 1971; 49: 335-344
41. Jorgensen AO, Shen AC, Arnold W, Leung AT, Campbell KP. Subcellular distribution of the 1, 4-dihydropyridine receptor in rabbit skeletal muscle in situ: an immunofluorescence and immunocolloidal gold-labeling study. J Cell Biol 1989; 109: 135-147
42. 2+ influx associated with muscle activity. Nature 1991; 349: 337-339
43. Feng Z, Ko CP. The role of glial cells in the formation and maintenance of the neuromuscular junction. Ann N Y Acad Sci 2008; 1132: 19-28
44. Hall ZW, Sanes JR. Synaptic structure and development: the neuromuscular junction. Cell 1993; 72 (Suppl.): 99-121
45. Chiu AY, Sanes JR. Development of basal lamina in synaptic and extrasynaptic portions of embryonic rat muscle. Dev Biol 1984; 103: 456-467
46. Sutterlin C, Colanzi A. The Golgi and the centrosome: building a functional partnership. J Cell Biol 2010; 188: 621-628
47. Molla-Herman A, Ghossoub R, Blisnick T, Meunier A, Serres C, Silbermann F, Emmerson C, Romeo K, Bourdoncle P, Schmitt A, Saunier S, Spassky N, Bastin P, Benmerah A. The ciliary pocket: an endocytic membrane domain at the base of primary and motile cilia. J Cell Sci 2010; 123: 1785-1795
48. Praetorius HA, Spring KR. A physiological view of the primary cilium. Annu Rev Physiol 2005; 67: 515-529
49. Yoshimura K, Kawate T, Takeda S. Signaling through the primary cilium affects glial cell survival under a stressed environment. Glia 2011; 59: 333-344
50. Yoshimura K, Takeda S. Hedgehog signaling regulates myelination in the peripheral nervous system through primary cilia. Differentiation 2012; 83: S78-S85
51. Mentis GZ, Blivis D, Liu WF, Drobac E, Crowder ME, Kong L, Alvarez FJ, Sumner CJ, O'Donovan MJ. Early functional impairment of sensory-motor connectivity in a mouse model of spinal muscular atrophy. Neuron 2011; 69: 453-467
52. Kong L, Wang X, Choe DW, Polley M, Burnett BG, Bosch-Marcé M, Griffin JW, Rich MM, Sumner CJ. Impaired synaptic vesicle release and immaturity of neuromuscular junctions in spinal muscular atrophy mice. J Neurosci 2009; 29: 842-851
53. McWhorter ML, Monani UR, Burghes AH, Beattie CE. Knockdown of the survival motor neuron (Smn) protein in zebrafish causes defects in motor axon outgrowth and pathfinding. J Cell Biol 2003; 162: 919-931
54. Winkler C, Eggert C, Gradl D, Meister G, Giegerich M, Wedlich D, Laggerbauer B, Fischer U. Reduced U snRNP assembly causes motor axon degeneration in an animal model for spinal muscular atrophy. Genes Dev 2005; 19: 2320-2330
55. Parra J, Martinez-Hernandez R, Also-Rallo E, Alias L, Barcelo M, Amenedo M, Medina C, Senosiain R, Calaf J, Baiget M, Bernal S, Tizzano EF. Ultrasound evaluation of fetal movements in pregnancies at risk for severe spinal muscular atrophy. Neuromuscul Disord 2011; 21: 97-101
56. Martin AR. Amplification of neuromuscular-transmission by postjunctional folds. Proc R Soc Lond B Biol Sci 1994; 258: 321-326
57. Ruff RL. Endplate contributions to the safety factor for neuromuscular transmission. Muscle Nerve 2011; 44: 854-861
58. Wood SJ, Slater CR. Safety factor at the neuromuscular junction. Prog Neurobiol 2001; 64: 393-429
59. Lupa MT, Krzemien DM, Schaller KL, Caldwell JH. Aggregation of sodium channels during development and maturation of the neuromuscular junction. J Neurosci 1993; 13: 1326-1336
60. Martinou JC, Merlie JP. Nerve-dependent modulation of acetylcholine receptor epsilon-subunit gene expression. J Neurosci 1991; 11: 1291-1299
61. Villarroel A, Sakmann B. Calcium permeability increase of endplate channels in rat muscle during postnatal development. J Physiol 1996; 496: 331-338