Investigation of neuromuscular abnormalities in neurotrophin-3-deficient mice

European Journal of Neuroscience

Volumn 31, Issue 1, 2010, Pages 29-41

  Sheard, Philip W ^a   Bewick, Guy S ^b   Woolley, Adele G ^c   Shaw, Jacqueline ^a   Fisher, Lorryn ^a   Fong, Sitt Wai ^b   Duxson, Marilyn J ^b  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Neuromuscular junction; Neurotrophin 3; Skeletal muscle; Synaptic vesicle

Indexed keywords

NEUROTROPHIN 3;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; GENETIC VARIABILITY; GENOTYPE; IMMUNOHISTOCHEMISTRY; MOTOR NERVE; MOUSE; MUSCLE CELL; MUSCLE EXCITATION; MUSCLE TONE; NERVE POTENTIAL; NERVE STIMULATION; NEUROMUSCULAR DISEASE; NONHUMAN; PRIORITY JOURNAL; SKELETAL MUSCLE; SOLEUS MUSCLE; SYNAPTIC TRANSMISSION;

ANIMALS; ANIMALS, NEWBORN; GENOTYPE; HAPLOTYPES; HETEROZYGOTE; IMMUNOHISTOCHEMISTRY; MICE; MICE, TRANSGENIC; MICROSCOPY, ELECTRON; MOTOR NEURONS; MUSCLE FIBERS, SKELETAL; MUSCLE STRENGTH; MUSCLE, SKELETAL; NEUROMUSCULAR JUNCTION; NEUROTROPHIN 3; PRESYNAPTIC TERMINALS; PYRIDINIUM COMPOUNDS; QUATERNARY AMMONIUM COMPOUNDS; SYNAPSES; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

EID: 72949087961     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2009.07032.x     Document Type: Article

References (74)

1. Beattie, E.C., Howe, C.L., Wilde, A., Brodsky, F.M. Mobley, W.C. (2000) NGF signals through TrkA to increase clathrin at the plasma membrane and enhance clathrin-mediated membrane trafficking. J. Neurosci., 20, 7325 7333.
2. Becherer, U., Guatimosim, C. Betz, W. (2001) Effects of staurosporine on exocytosis and endocytosis at frog motor nerve terminals. J. Neurosci., 21, 782 787.
3. Betz, W.J. Bewick, G.S. (1993) Optical monitoring of transmitter release and synaptic vesicle recycling at the frog neuromuscular junction. J. Physiol. (Lond.), 460, 287 309.
4. Betz, W.J., Bewick, G.S. Ridge, R.M.A.P. (1992) Intracellular movements of fluorescently labeled synaptic vesicles in frog motor nerve terminals during nerve stimulation. Neuron, 9, 805 813.
5. Betz, W.J., Ridge, R.M.A.P. Bewick, G.S. (1993) Comparison of FM1-43 staining patterns and electrophysiological measures of transmitter release at the frog neuromuscular junction. J. Physiol. Paris, 87, 193 202.
6. Bewick, G.S., Zammit, P.S. Tonge, D.A. (1993) Restoration of motor unit properties and fiber type distribution in reinnervated axolotl skeletal muscle. Dev. Biol., 158, 288 300.
7. Chevallier, A. Kieny, M. (1982) On the role of the connective tissue in the patterning of the chick limb musculature. Rouxs Arch. Dev. Biol., 191, 277 280.
8. Clase, K.L., Mitchell, P.J., Ward, P.J., Dorman, C.M., Johnson, S.E. Hannon, K. (2000) FGF5 stimulates expansion of connective tissue fibroblasts and inhibits skeletal muscle development in the limb. Dev. Dyn., 219, 368 380.
9. Copray, J.C.V.M. Brouwer, N. (1997) Neurotrophin-3 mRNA expression in rat intrafusal muscle fibres after denervation and reinnervation. Neurosci. Lett., 236, 41 44.
10. Dahm, L.M. Landmesser, L.T. (1991) The regulation of synaptogenesis during normal development and following activity blockade. J. Neurosci., 11, 238 255.
11. Donovan, M.J., Hahn, R., Tessarollo, L. Hempstead, B.L. (1996) Identification of an essential nonneuronal function of neurotrophin 3 in mammalian cardiac development. Nat. Genet., 14, 210 213.
12. Duxson, M.J. (1982) The effect of postsynaptic block on development of the neuromuscular junction in postnatal rats. J. Neurocytol., 11, 395 408.
13. Duxson, M.J. (1992) The relationship of nerve to myoblasts and newly-formed secondary myotubes in the fourth lumbrical muscle of the rat foetus. J. Neurocytol., 21, 574 588.
14. Duxson, M.J. Vrbova, G. (1985) Inhibition of acetylcholinesterase accelerates axon terminal withdrawal at the developing rat neuromuscular junction. J. Neurocytol., 14, 337 363.
15. Ernfors, P., Lee, K.F., Kucera, J. Jaenisch, R. (1994) Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of proprioceptive limb afferents. Cell, 77, 503 512.
16. Farinas, I., Yoshida, C.K., Backus, C. Reichardt, L.F. (1996) Lack of neurotrophin-3 results in death of spinal sensory neurons and premature differentiation of their precursors. Neuron, 17, 1065 1078.
17. Funakoshi, H., Belluardo, N., Arenas, E., Yamamoto, Y., Casabona, A., Persson, H. Ibanez, C.F. (1995) Muscle-derived neurotrophin-4 as an activity-dependent trophic signal for adult motor neurons. Science, 268, 1495 1499.
18. Gavazzi, I., Kumar, R.D., McMahon, S.B. Cohen, J. (1999) Growth responses of different subpopulations of adult sensory neurons to neurotrophic factors in vitro. Eur. J. Neurosci., 11, 3405 3414.
19. Gray, W.R., Olivera, B.M. Cruz, L.J. (1988) Peptide toxins from venomous Conus snails. Annu. Rev. Biochem., 57, 665 700.
20. Griesbeck, O., Parsadanian, A.S., Sendtner, M. Thoenen, H. (1995) Expression of neurotrophins in skeletal muscle: quantitative comparison and significance for motoneuron survival and maintenance of function. J. Neurosci. Res., 42, 21 33.
21. Hall, Z.W. Sanes, J.R. (1993) Synaptic structure and development - the neuromuscular junction. Cell, 72, 99 121.
22. Hess, D.M., Scott, M.O., Potluri, S., Pitts, E.V., Cisterni, C. Balice-Gordon, R.J. (2007) Localization of TrkC to Schwann cells and effects of neurotrophin-3 signaling at neuromuscular synapses. J. Comp. Neurol., 501, 465 482.
23. Hossain, W.A., D'Sa, C. Morest, D.K. (2006) Site-specific interactions of neurotrophin-3 and fibroblast growth factor (FGF2) in the embryonic development of the mouse cochlear nucleus. J. Neurobiol., 66, 897 915.
24. Hossain, W.A., D'Sa, C. Morest, D.K. (2008) Interactive roles of fibroblast growth factor 2 and neurotrophin 3 in the sequence of migration, process outgrowth, and axonal differentiation of mouse cochlear ganglion cells. J. Neurosci. Res., 86, 2376 2391.
25. Huang, T.J., Sayers, N.M., Verkhratsky, A. Fernyhough, P. (2005) Neurotrophin-3 prevents mitochondrial dysfunction in sensory neurons of streptozotocin-diabetic rats. Exp. Neurol., 194, 279 283.
26. Huijing, P.A. (1999) Muscle as a collagen fiber reinforced composite: a review of force transmission in muscle and whole limb. J. Biomech., 32, 329 345.
27. Huijing, P.A. Jaspers, R.T. (2005) Adaptation of muscle size and myofascial force transmission: a review and some new experimental results. Scand. J. Med. Sci. Sports, 15, 349 380.
28. Je, H.S., Yang, F., Zhou, J. Lu, B. (2006) Neurotrophin 3 induces structural and functional modification of synapses through distinct molecular mechanisms. J. Cell Biol., 175, 1029 1042.
29. Jessen, K.R. Mirsky, R. (1999a) Schwann cells and their precursors emerge as major regulators of nerve development. Trends Neurosci., 22, 402 410.
30. Jessen, K.R. Mirsky, R. (1999b) Why do Schwann cells survive in the absence of axons? Ann. NY Acad. Sci., 883, 109 115.
31. Jessen, K.R. Mirsky, R. (2005) The origin and development of glial cells in peripheral nerves. Nat. Rev. Neurosci., 6, 671 682.
32. Kang, H.J. Schuman, E.M. (1995) Neurotrophin-induced modulation of synaptic transmission in the adult hippocampus. J. Physiol. Paris, 89, 11 22.
33. Kardon, G. (1998) Muscle and tendon morphogenesis in the avian hind limb. Development, 125, 4019 4032.
34. Katoh-Semba, R., Kaisho, Y., Shintani, A., Nagahama, M. Kato, K. (1996) Tissue distribution and immunocytochemical localization of neurotrophin-3 in the brain and peripheral tissues of rats. J. Neurochem., 66, 330 337.
35. Kelly, A.M. Zacks, S.I. (1969) The fine structure of motor endplate morphogenesis. J. Cell Biol., 42, 154 169.
36. Klein, R., Silos-Santiago, I., Smeyne, R.J., Lira, S.A., Brambilla, R., Bryant, S., Zhang, L., Snider, W.D. Barbacid, M. (1994) Disruption of the neurotrophin-3 receptor gene trkC eliminates 1a muscle afferents and results in abnormal movements. Nature, 368, 249 251.
37. Kucera, J., Ernfors, P., Walro, J. Jaenisch, R. (1995a) Reduction in the number of spinal motor neurons in neurotrophin-3-deficient mice. Neuroscience, 69, 321 330.
38. Kucera, J., Fan, G., Jaenisch, R., Linnarsson, S. Ernfors, P. (1995b) Dependence of developing group Ia afferents on neurotrophin-3. J. Comp. Neurol., 363, 307 320.
39. Levine, E.S., Dreyfus, C.F., Black, I.B. Plummer, M.R. (1995) Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. Proc. Natl Acad. Sci. USA, 92, 8074 8077.
40. Liou, J.C. Fu, W.M. (1997) Regulation of quantal secretion from developing motoneurons by postsynaptic activity-dependent release of NT-3. J. Neurosci., 17, 2459 2468.
41. Lohof, A.M., Ip, N.Y. Poo, M.M. (1993) Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. Nature, 363, 350 353.
42. Lu, B. 2004) Acute and long-term synaptic modulation by neurotrophins. Prog. Brain Res., 146, 137 150.
43. Lu, B. Figurov, A. (1997) Role of neurotrophins in synapse development and plasticity. Rev. Neurosci., 8, 1 12.
44. Lu, B., Pang, P.T. Woo, N.H. (2005) The yin and yang of neurotrophin action. Nat. Rev. Neurosci., 6, 603 614.
45. McLachlan, E.M. Martin, A.R. (1981) Non-linear summation of end-plate potentials in the frog and mouse. J. Physiol., 311, 307 324.
46. Omura, T., Sano, M., Omura, K., Hasegawa, T., Doi, M., Sawada, T. Nagano, A. (2005) Different expressions of BDNF, NT3, and NT4 in muscle and nerve after various types of peripheral nerve injuries. J. Peripher. Nerv. Syst., 10, 293 300.
47. Paul, A.C., Sheard, P.W., Kaufman, S.J. Duxson, M.J. (2002) Localization of alpha 7 integrins and dystrophin suggests potential for both lateral and longitudinal transmission of tension in large mammalian muscles. Cell Tissue Res., 308, 255 265.
48. Plomp, J.J., van Kempen, G.T. Molenaar, P.C. (1992) Adaptation of quantal content to decreased postsynaptic sensitivity at single endplates in alpha-bungarotoxin-treated rats. J. Physiol., 458, 487 499.
49. Poo, M.M. (2001) Neurotrophins as synaptic modulators. Nat. Rev. Neurosci., 2, 24 32.
50. Pyle, J.L., Kavalali, E.T., Piedras-Renteria, E.S. Tsien, R.W. (2000) Rapid reuse of readily releasable pool vesicles at hippocampal synapses. Neuron, 28, 221 231.
51. Reddy, T. Kablar, B. (2004) Evidence for the involvement of neurotrophins in muscle transdifferentiation and acetylcholine receptor transformation in the esophagus of Myf5(-/-):MyoD(-/-) and NT-3(-/-) embryos. Dev. Dyn., 231, 683 692.
52. Reddy, L.V., Koirala, S., Sugiura, Y., Herrera, A.A. Ko, C.P. (2003) Glial cells maintain synaptic structure and function and promote development of the neuromuscular junction in vivo. Neuron, 40, 563 580.
53. Reid, B., Slater, C.R. Bewick, G.S. (1999) Synaptic vesicle dynamics in rat fast and slow motor nerve terminals. J. Neurosci., 19, 2511 2521.
54. Reid, B., Martinov, V.N., Nja, A., Lomo, T. Bewick, G.S. (2003) Activity-dependent plasticity of transmitter release from nerve terminals in rat fast and slow muscles. J. Neurosci., 23, 9340 9348.
55. Ribchester, R.R., Mao, F. Betz, W.J. (1994) Optical measurements of activity-dependent membrane recycling in motor nerve terminals of mammalian skeletal muscle. Proc. Biol. Sci., 255, 61 66.
56. Richards, D.A., Guatimosim, C., Rizzoli, S.O. Betz, W.J. (2003) Synaptic vesicle pools at the frog neuromuscular junction. Neuron, 39, 529 541.
57. Rizzoli, S.O. Betz, W.J. (2005) Synaptic vesicle pools. Nat. Rev. Neurosci., 6, 57 69.
58. Schweizer, F.E. Ryan, T.A. (2006) The synaptic vesicle: cycle of exocytosis and endocytosis. Curr. Opin. Neurobiol., 16, 298 304.
59. Sheard, P., Paul, A. Duxson, M. (2002a) Intramuscular force transmission. Adv. Exp. Med. Biol., 508, 495 499.
60. Sheard, P.W., Musaad, K. Duxson, M.J. (2002b) Distribution of neurotrophin receptors in the mouse neuromuscular system. Int. J. Dev. Biol., 46, 569 575.
61. Song, H.J., Ming, G.L. Poo, M.M. (1997) cAMP-induced switching in turning direction of nerve growth cones. Nature, 388, 275 279.
62. Sudhof, T.C. (2004) The synaptic vesicle cycle. Annu. Rev. Neurosci., 27, 509 547.
63. Takamori, S., Holt, M., Stenius, K., Lemke, E.A., Gronborg, M., Riedel, D., Urlaub, H., Schenck, S., Brugger, B., Ringler, P., Muller, S.A., Rammner, B., Grater, F., Hub, J.S., De Groot, B.L., Mieskes, G., Moriyama, Y., Klingauf, J., Grubmuller, H., Heuser, J., Wieland, F. Jahn, R. (2006) Molecular anatomy of a trafficking organelle. Cell, 127, 831 846.
64. Tessarollo, L., Vogel, K.S., Palko, M.E., Reid, S.W. Parada, L.F. (1994) Targeted mutation in the neurotrophin-3 gene results in loss of muscle sensory neurons. Proc. Natl Acad. Sci. USA, 91, 11844 11848.
65. Tessarollo, L., Tsoulfas, P., Donovan, M.J., Palko, M.E., Blair-Flynn, J., Hempstead, B.L. Parada, L.F. (1997) Targeted deletion of all isoforms of the trkC gene suggests the use of alternate receptors by its ligand neurotrophin-3 in neuronal development and implicates trkC in normal cardiogenesis. Proc. Natl Acad. Sci. USA, 94, 14776 14781.
66. Thornton, M.R., Shawcross, S.G., Mantovani, C., Kingham, P.J., Birchall, M.A. Terenghi, G. (2008) Neurotrophins 3 and 4 differentially regulate NCAM, L1 and N-cadherin expression during peripheral nerve regeneration. Biotechnol. Appl. Biochem., 49, 165 174.
67. Wang, T., Xie, K. Lu, B. (1995) Neurotrophins promote maturation of developing neuromuscular synapses. J. Neurosci., 15, 4796 4805.
68. Wang, X., Butowt, R. von Bartheld, C.S. (2003) Presynaptic neurotrophin-3 increases the number of tectal synapses, vesicle density, and number of docked vesicles in chick embryos. J. Comp. Neurol., 458, 62 77.
69. Wood, S.J. Slater, C.R. (1997) The contribution of postsynaptic folds to the safety factor for neuromuscular transmission in rat fast- and slow-twitch muscles. J. Physiol. (Lond.), 500, 165 176.
70. Woolley, A., Sheard, P., Dodds, K. Duxson, M. (1999) Alpha motoneurons are present in normal numbers but with reduced soma size in neurotrophin-3 knockout mice. Neurosci. Lett., 272, 107 110.
71. Woolley, A.G., Sheard, P.W. Duxson, M.J. (2005) Neurotrophin-3 null mutant mice display a postnatal motor neuropathy. Eur. J. Neurosci., 21, 2100 2110.
72. Woolley, A.G., Tait, K.J., Hurren, B.J., Fisher, L., Sheard, P.W. Duxson, M.J. (2008) Developmental loss of NT-3 in vivo results in reduced levels of myelin-specific proteins, a reduced extent of myelination and increased apoptosis of Schwann cells. Glia, 56, 306 317.
73. Xie, K., Wang, T., Olafsson, P., Mizuno, K. Lu, B. (1997) Activity-dependent expression of NT-3 in muscle cells in culture: implications in the development of neuromuscular junctions. J. Neurosci., 17, 2947 2958.
74. Young, M., Paul, A., Rodda, J., Duxson, M. Sheard, P. (2000) Examination of intrafascicular muscle fiber terminations: implications for tension delivery in series-fibered muscles. J. Morphol., 245, 130 145.