What controls the position, number, size, and distribution of neuromuscular junctions on rat muscle fibers?

Journal of Neurocytology

Volumn 32, Issue 5-8, 2003, Pages 835-848

  Lømo, Terje ^a  

^a UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

AGRIN; CHOLINERGIC RECEPTOR;

CELL SURVIVAL; ELECTROSTIMULATION; EVOKED MUSCLE RESPONSE; MOTOR NERVE; MUSCLE CELL; NERVE CONDUCTION; NERVE FIBER; NERVE STIMULATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; REVIEW; SKELETAL MUSCLE; SOLEUS MUSCLE; SYNAPTOGENESIS; ANIMAL; CELL COUNT; CELL SIZE; CHEMISTRY; CYTOLOGY; HUMAN; METABOLISM; METHODOLOGY; PHYSIOLOGY;

ANIMALS; CELL COUNT; CELL SIZE; HUMANS; MUSCLE FIBERS; NEUROMUSCULAR JUNCTION; RATS; RECEPTORS, CHOLINERGIC;

EID: 3042624676     PISSN: 03004864     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:NEUR.0000020627.18156.b1     Document Type: Review

References (83)

1. AKAABOUNE, M., CULICAN, S. M., TURNEY, S. G. & LICHTMAN, J. W. (1999) Rapid and reversible effects of activity on acetylcholine receptor density at the neuromuscular junction in vivo (see comments). Science 286, 503-507.
2. ANDREOSE, J. S., FUMAGALLI, G. & LØMO, T. (1995) Number of junctional acetylcholine receptors: Control by neural and muscular influences in the rat. Journal of Physiology (Lond) 483, 397-406.
3. ANDREOSE, J. S., XU, R., LØMO, T., SALPETER, M. M. & FUMAGALLI, G. (1993) Degradation of two AChR populations at rat neuromuscular junctions: Regulation in vivo by electrical stimulation. Journal of Neuroscience 13, 3433-3438.
4. ANGAUT, P. D. & MALLART, A. (1979) Dual innervation of end-plate sites and its consequenses for neuromuscular transmission in muscles of adult Xenopus Laevis. Journal of Physiology (Lond) 289, 203-218.
5. ARBER, S., BURDEN, S. J. & HARRIS, A. J. (2002) Patterning of skeletal muscle. Current Opinion in Neurobiology 12, 100-103.
6. AUSONI, S., GORZA, L., SCHIAFFINO, S., GUNDERSEN, K. & LØMO, T. (1990) Expression of myosin heavy chain isoforms in stimulated fast and slow rat muscles. Journal of Neuroscience 10, 153-160.
7. BALICE-GORDON, R. J. & LICHTMAN, J. W. (1990) In vivo visualization of the growth of pre- and postsynaptic elements of neuromuscular junctions in the mouse. Journal of Neuroscience 10, 894-908.
8. BALICE-GORDON, R. J. & LICHTMAN, J. W. (1993) In vivo observations of pre- and postsynaptic changes during the transition from multiple to single innervation at developing neuromuscular junctions. Journal of Neuroscience 13, 834-855.
9. BEZAKOVA, G., HELM, J. P., FRANCOLINI, M. & LØMO, T. (2001a) Effects of purified recombinant neural and muscle agrin on skeletal muscle fibers in vivo. Journal of Cell Biology 153, 1441-1452.
10. BEZAKOVA, G. & LØMO, T. (2001) Muscle activity and muscle agrin regulate the organization of cytoskeletal proteins and attached acetylcholine receptor (AchR) aggregates in skeletal muscle fibers. Journal of Cell Biology 153, 1453-1463.
11. BEZAKOVA, G., RABBEN, I., SEELAND, I., FUMAGALLI, G. & LØMO, T. (2001b) Neural agrin controls acetylcholine receptor stability in skeletal muscle fibers. Proceedings of the National Academy of Sciences USA 98, 9924-9929.
12. BRAITHWAITE, A. W. & HARRIS, A. J. (1979) Neural influence on acetylcholine receptor clusters in embryonic development of skeletal muscles. Nature 279, 549-551.
13. BRENNER, H. R., ROTZLER, S., KUES, W. A., WITZEMANN, V. & SAKMANN, B. (1994) Nerve-dependent induction of AChR epsilon-subunit gene expression in muscle is independent of state of differentiation. Developmental Biology 165, 527-536.
14. BUFFELLI, M., BUSETTO, G., CANGIANO, L. & CANGIANO, A. (2002) Perinatal switch from synchronous to asynchronous activity of motoneurons: Link with synapse elimination. Proceedings of the National Academy of Sciences USA 99, 13200-13205.
15. BURDEN, S. J. (2002) Building the vertebrate neuromuscular synapse. Journal of Neurobiology 53, 501-511.
16. BUSETTO, G., BUFFELLI, M., TOGNANA, E., BELLICO, F. & CANGIANO, A. (2000) Hebbian mechanisms revealed by electrical stimulation at developing rat neuromuscular junctions. Journal of Neuroscience 20, 685-695.
17. CARONI, P., ROTZLER, S., BRITT, J. C. & BRENNER, H. R. (1993) Calcium influx and protein phosphorylation mediate the metabolic stabilization of synaptic acetylcholine receptors in muscle. Journal of Neuroscience 13, 1315-1325.
18. COHEN, I., RIMER, M., LØMO, T. & MCMAHAN, U. J. (1997) Agrin-induced postsynaptic-like apparatus in skeletal muscle fibers in vivo [published erratum appears in Mol. Cell Neurosci. 1997;10(3/4):208]. Molecular and Cellular Neuroscience 9, 237-253.
19. DAHM, L. M. & LANDMESSER, L. T. (1991) The regulation of synaptogenesis during normal development and following activity blockade. Journal of Neuroscience 11, 238-255.
20. DENNIS, M. J. (1981) Development of the neuromuscular junction: Inductive interactions between cells. Annual Review of Neuroscience 4, 43-68.
21. DENNIS, M. J., ZISKIND, C. L. & HARRIS, A. J. (1981) Development of neuromuscular junctions in rat embryos. Developmental Biology 81, 266-279.
22. DENZER, A. J., BRANDENBERGER, R., GESEMANN, M., CHIQUET, M. & RUEGG, M. A. (1997) Agrin binds to the nerve-muscle basal lamina via laminin. Journal of Cell Biology 137, 671-683.
23. EKEN, T. & GUNDERSEN, K. (1988) Electrical stimulation resembling normal motor-unit activity: Effects on denervated fast and slow rat muscles. Journal of Physiology (Lond) 402, 651-669.
24. FEX, S. & THESLEFF, S. (1967) The time required for innervation of denervated muscles by nerve implants. Life Sciences 6, 635-639.
25. FRANK, E. & FISCHBACH, G. D. (1979) Early events in neuromuscular junction formation in vitro: Induction of acetylcholine receptor clusters in the postsynaptic membrane and morphology of newly formed synapses. Journal of Cell Biology 83, 143-158.
26. FRANK, E., JANSEN, J. K., LØMO, T. & WESTGAARD, R. H. (1975) The interaction between foreign and original motor nerves innervating the soleus muscle of rats. Journal of Physiology (Lond) 247, 725-743.
27. FREY, D., SCHNEIDER, C., XU, L., BORG, J., SPOOREN, W. & CARONI, P. (2000) Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. Journal of Neuroscience 20, 2534-2542.
28. FUMAGALLI, G., BALBI, S., CANGIANO, A. & LØMO, T. (1990) Regulation of turnover and number of acetylcholine receptors at neuromuscular junctions. Neuron 4, 563-569.
29. GAUTAM, M., NOAKES, P. G., MOSCOSO, L., RUPP, F., SCHELLER, R. H., MERLIE, J. P. & SANES, J. R. (1996) Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85, 525-535.
30. GRIFFIN, G. E., WILLIAMS, P. E. & GOLDSPINK, G. (1971) Region of longitudinal growth in striated muscle fibres. Nature New Biology 232, 28-29.
31. HASHEMOLHOSSEINI, S., MOORE, C., LANDMANN, L., SANDER, A., SCHWARZ, H., WITZEMANN, V., SAKMANN, B. & BRENNER, H. R. (2000) Electrical activity and postsynapse formation in adult muscle: Gamma-AChRs are not required. Molecular and Cellular Neuroscience 16, 697-707.
32. HENNIG, R. & LØMO, T. (1985) Firing patterns of motor units in normal rats. Nature 314, 164-166.
33. HUME, R. I. & PURVES, D. (1981) Geometry of neonatal neurones and the regulation of synapse elimination. Nature 293, 469-471.
34. JANSEN, J. K., LØMO, T., NICOLAYSEN, K. & WESTGAARD, R. H. (1973) Hyperinnervation of skeletal muscle fibers: Dependence on muscle activity. Science 181, 559-561.
35. JONES, G., MEIER, T., LICHTSTEINER, M., WITZEMANN, V., SAKMANN, B. & BRENNER, H. R. (1997) Induction by agrin of ectopic and functional postsynaptic-like membrane in innervated muscle. Proceedings of the National Academy of Sciences USA 94, 2654-2659.
36. KELLY, A. M. & ZACKS, S. I. (1969) The fine structure of motor endplate myogenesis. Journal of Cell Biology 42, 154-169.
37. KO, P. K., ANDERSON, M. J. & COHEN, M. W. (1977) Denervated skeletal muscle fibers develop discrete patches of high acetylcholine receptor density. Science 196, 540-542.
38. KORNELIUSSEN, H. & SOMMERSCHILD, H. (1976) Ultrastructure of the new neuromuscular junctions formed during reinnervation of rat soleus muscle by a "foreign" nerve. Cell and Tissue Research 167, 439-452.
39. KUES, W. A., BRENNER, H. R., SAKMANN, B. & WITZEMANN, V. (1995) Local neurotrophic repression of gene transcripts encoding fetal AChRs at rat neuromuscular synapses. Journal of Cell Biology 130, 949-957.
40. KUEFLER, D. P., THOMPSON, W. & JANSEN, J. (1980) The fate of foreign endplates in cross-innervated rat soleus muscle. Proceedings of the Royal Society of London Series B-Biological Sciences 208, 189-222.
41. LESCHZINER, A., MOUKHLES, H., LINDENBAUM, M., GEE, S. H., BUTTERWORTH, J., CAMPBELL, K. P. & CARBONETTO, S. (2000) Neural regulation of alpha-dystroglycan biosynthesis and glycosylation in skeletal muscle. Journal of Neurochemistry 74, 70-80.
42. LEVITT, T. A. & SALPETER, M. M. (1981) Denervated end-plates have a dual population of junctional acetylcholine receptors. Nature 291, 239-241.
43. LIN, W., BURGESS, R. W., DOMINGUEZ, B., PFAFF, S. L., SANES, J. R. & LEE, K. F. (2001) Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse. Nature 410, 1057-1064.
44. LIU, D. W. & WESTERFIELD, M. (1992) Clustering of muscle acetylcholine receptors requires motoneurons in live embryos, but not in cell culture. Journal of Neuroscience 12, 1859-1866.
45. LØMO, T. (1998) Agrin and the neuromuscular junction [letter; comment]. Trends in Neurosciences 21, 426-427.
46. LØMO, T., POCKETT, S. & SOMMERSCHILD, H. (1988) Control of number and distribution of synapses during ectopic synapse formation in adult rat soleus muscles. Neuroscience 24, 673-686.
47. LØMO, T. & SLATER, C. R. (1978) Control of acetylcholine sensitivity and synapse formation by muscle activity. Journal of Physiology (Lond) 275, 391-402.
48. LØMO, T. & SLATER, C. R. (1980) Control of junctional acetylcholinesterase by neural and muscular influences in the rat. Journal of Physiology (Lond) 303, 191-202.
49. MATHIESEN, I., RIMER, M., ASHTARI, O., COHEN, I., MCMAHAN, U. J. & LØMO, T. (1999) Regulation of the size and distribution of agrin-induced postsynaptic-like apparatus in adult skeletal muscle by electrical muscle activity. Molecular and Cellular Neuroscience 13, 207-217.
50. MCMAHAN, U. J. (1990) The agrin hypothesis. Cold Spring Harbor Symposia on Quantitative Biology 50, 407-418.
51. MEIER, T., HAUSER, D. M., CHIQUET, M., LANDMANN, L., RUEGG, M. A. & BRENNER, H. R. (1997) Neural agrin induces ectopic postsynaptic specializations in innervated muscle fibers. Journal of Neuroscience 17, 6534-6544.
52. MEIER, T., MASCIULLI, F., MOORE, C., SCHOUMACHER, F., EPPENBERGER, U., DENZER, A. J., JONES, G. & BRENNER, H. R. (1998) Agrin can mediate acetylcholine receptor gene expression in muscle by aggregation of muscle-derived neuregulins. Journal of Cell Biology 141, 715-726.
53. MOODY, C. F. & COHEN, M. W. (1982) Influence of nerve on the formation and survival of acetylcholine receptor and cholinesterase patches on embryonic Xenopus muscle cells in culture. Journal of Neuroscience 2, 633-646.
54. MOORE, C., LEU, M., MULLER, U. & BRENNER, H. R. (2001) Induction of multiple signaling loops by MuSK during neuromuscular synapse formation. Proceedings of the National Academy of Sciences USA 98, 14655-14660.
55. NUDELL, B. M. & GRINNELL, A. D. (1983) Regulation of synaptic position, size, and strength in anuran skeletal muscle. Journal of Neuroscience 3, 161-176.
56. PADYKULA, H. A. & GAUTHIER, G. E. (1970) The ultrastructure of the neuromuscular junctions of mammalien red, white, and intermediate skeletal muscle fibers. Journal of Cell Biology 46, 27-41.
57. PAUL, A. C. (2001) Muscle length affects the architecture and pattern of innervation differently in leg muscles of mouse, guinea pig, and rabbit compared to those of human and monkey muscles. Anatomical Record 262, 301-309.
58. 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 and Tissue Research 308, 255-265.
59. PROPST, J. W. & KO, C. P. (1987) Correlations between active zone ultrastructure and synaptic function studied with freeze-fracture of physiologically identified neuromuscular junctions. Journal of Neuroscience 7, 3654-3664.
60. PUN, S., SIGRIST, M., SANTOS, A. E., RUEGG, M. A., SANES, J. R., JESSELL, T. M., ARBER, S. & CARONI, P. (2002) An intrinsic distinction in neuromuscular junction assembly and maintenance in different skeletal muscles. Neuron 34, 357-370.
61. REID, B., MARTINOV, V. N., NJÅ, A., LØMO, T. & BEWICK, G. S. (2003) Activity-dependent plasticity of transmitter release from nerve terminals in rat fast and slow muscles. Journal of Neuroscience 15, 9340-9348.
62. REID, B., SLATER, C. R. & BEWICK, G. S. (1999) Synaptic vesicle dynamics in rat fast and slow motor nerve terminals. Journal of Neuroscience 19, 2511-2521.
63. REINESS, C. G. & WEINBERG, C. B. (1981) Metabolic stabilization of acetylcholine receptors at newly formed neuromuscular junctions in rat. Developmental Biology 84, 247-254.
64. REIST, N. E., MAGILL, C. & MCMAHAN, U. J. (1987) Agrin-like molecules at synaptic sites in normal, denervated and damaged skeletal muscles. Journal of Cell Biology 105, 2457-2469.
65. REIST, N. E., WERLE, M. J. & MCMAHAN, U. J. (1992) Agrin released by motor neurons induces the aggregation of acetylcholine receptors at neuromuscular junctions. Neuron 8, 865-868.
66. RIMER, M., COHEN, I., LØMO, T., BURDEN, S. J. & MCMAHAN, U. J. (1998) Neuregulins and erbB receptors at neuromuscular junctions and at agrin- induced postsynaptic-like apparatus in skeletal muscle. Molecular and Cellular Neuroscience 12, 1-15.
67. ROTZLER, S. & BRENNER, H. R. (1990) Metabolic stabilization of acetylcholine receptors in vertebrate neuromuscular junction by muscle activity. Journal of Cell Biology 111, 655-661.
68. SALPETER, M. M., ANDREOSE, J. S., O'MALLEY, J. P., XU, R., EUMAGALLI, G. & LØMO, T. (1993) Degradation of acetylcholine receptors at vertebrate neuromuscular junctions. Annals of the New York Academy of Sciences 681, 155-164.
69. SALPETER, M. M., MARCHATERRE, M. & HARRIS, R. (1988) Distribution of extrajunctional acetylcholine receptors on a vertebrate muscle: Evaluated by using a scanning electron microscope autoradiographic procedure. Journal of Cell Biology 106, 2087-2093.
70. SALTOE, M., SCHWARTZ, T. L., UMBACH, J. A., GUNDERSEN, C. B. & KIDOKORO, Y. (2001) Absence of junctional glutamate receptor clusters in Drosophila mutants lacking spontaneous transmitter release. Science 293, 514-517.
71. SAMUELS, P. L., RIML, H. & COHEN, M. W. (1990) Formation and survival or a postsynaptic specialization in cultures of embryonic Xenopus nerve and muscle cells. Developmental Biology 141, 399-411.
72. SANES, J. R. & LICHTMAN, J. W. (1999) Development of the vertebrate neuromuscular junction. Annual Review of Neuroscience 22, 389-442.
73. SKORPEN, J., LAFOND-BENESTAD, S. & LØMO, T. (1999) Regulation of the size and distribution of ectopic neuromuscular junctions in adult skeletal muscle by nerve-derived trophic factor and electrical muscle activity. Molecular and Cellular Neuroscience 13, 192-206.
74. SLATER, C. R. (1982) Postnatal maturation of nerve-muscle junctions in hindlimb muscles of the mouse. Developmental Biology 94, 11-22.
75. STERZ, R., PAGALA, M. & PEPER, K. (1983) Postjunctional characteristics of the endplates in mammalian fast and slow muscles. Pflügers Archiv 398, 48-54.
76. WÆRHAUG, O. (1992) Postnatal development of rat motor nerve terminals. Anatomy and Embryology 185, 115-123.
77. WÆRHAUG, O. & LØMO, T. (1994) Factors causing different properties at neuromuscular junctions in fast and slow rat skeletal muscles. Anatomy and Embryology 190, 113-125.
78. WESTGAARD, R. H. & LØMO, T. (1988) Control of contractile properties within adaptive ranges by patterns of impulse activity in the rat. Journal of Neuroscience 8, 4415-4426.
79. WETZEL, D. M. & SALPETER, M. M. (1991) Fibrillation and accelerated AChR degradation in long term muscle organ culture. Muscle & Nerve 14, 1003-1012.
80. WOOD, S. J. & SLATER, C. R. (2001) Safety factor at the neuromuscular junction. Progress in Neurobiology 64, 393-429.
81. YANG, X., ARBER, S., WILLIAM, C., LI, L., TANABE, Y., JESSELL, T. M., BIRCHMEIER, C. & BURDEN, S. J. (2001) Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron 30, 399-110.
82. YANG, X., LI, W., PRESCOTT, E. D., BURDEN, S. J. & WANG, J. C. (2000) DNA topoisomerase IIbeta and neural development. Science 287, 131-134.
83. ZISKIND-CONHAIM, L. & BENNETT, J. I. (1982) The effects of electrical inactivity and denervation on the distribution of acetylcholine receptors in developing rat muscle. Developmental Biology 90, 185-197.