Modulation of neurotransmission by reciprocal synapse-glial interactions at the neuromuscular junction

Journal of Neurocytology

Volumn 32, Issue 5-8, 2003, Pages 1003-1015

  Auld, Daniel S ^a   Colomar, Aurore ^a   Bélair, Eve Lyne ^a   Castonguay, Annie ^a   Pinard, Audrée ^a   Rousse, Isabelle ^a   Thomas, Sébastien ^a   Robitaille, Richard ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; GLUTAMIC ACID; GUANINE NUCLEOTIDE BINDING PROTEIN; NITRIC OXIDE;

CELL ACTIVITY; GLIA CELL; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NERVE CELL PLASTICITY; NEUROMODULATION; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; REDUCTION; REGULATORY MECHANISM; REVIEW; SCHWANN CELL; SYNAPSE; SYNAPTIC TRANSMISSION; ANIMAL; GLIA; HUMAN; PHYSIOLOGY;

ANIMALS; HUMANS; NEUROGLIA; NEUROMUSCULAR JUNCTION; NEURONAL PLASTICITY; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 3042585519     PISSN: 03004864     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:NEUR.0000020638.31068.9f     Document Type: Review

References (100)

1. AKASU, T. (1986) The effects of substance P on neuromuscular transmission in the frog. Neuroscience Research 3, 275-284.
2. ANDERSON, J. E. (2000) A role for nitric oxide in muscle repair: Nitric oxide-mediated activation of muscle satellite cells. Molecular Biology of the Cell 11, 1859-1874.
3. AONUMA, H., NAGAYAMA, T. & TAKAHATA, M. (2000) Modulatory effects of nitric oxide on synaptic depression in the crayfish neuromuscular system. Journal of Experimental Biology 203 (Pt 23), 3595-3602.
4. ARAQUE, A., PARPURA, V., SANZGIRI, R. P. & HAYDON, P. G. (1999) Tripartite synapses: Glia, the unacknowledged partner. Trends in Neurosciences 22, 208-215.
5. ASTROW, S. H., QIANG, H. & KO, C. P. (1998) Perisynaptic Schwann cells at neuromuscular junctions revealed by a novel monoclonal antibody. Journal of Neurocytology 27, 667-681.
6. AULD, D. S. & ROBITAILLE, R. (2003) Perisynaptic Schwann cells at the neuromuscular junction: Nerve- and activity-dependent contribuons to synaptic efficacy, plasticity and reinnervation. Neuroscientist 9, 144-157.
7. BALLIGAND, J. L., KELLY, R. A., MARSDEN, P. A., SMITH, T. W. & MICHEL, T. (1993) Control of cardiac muscle cell function by an endogenous nitric oxide signaling system. Proceeding of the National Academy of Sciences 90, 347-351.
8. BERGER, U. V., CARTER, R. E. & COYLE, J. T. (1995) Immunocytochemical localization of N-acetylaspartyl glutamate, its hydrolysing enzyme NAALADase, and the NMDAR-1 receptor at the vertebrate neuromuscular junction. Neuroscience 64, 847-850.
9. BERGLES, D. E. & JAHR, C. E. (1998) Glial contribution to glutamate uptake at Schaffer collateral-commissural synapses in the hippocampus. Journal of Neuroscience 18, 7709-7716.
10. BETZ, W. J. (1970) Depression of transmitter release at the neuromuscular junction of the frog. Journal of Physiology 206, 629-644.
11. BEVAN, S., MILEDI, R. & GRAMPP, W. (1973) Induced transmitter release from Schwann cells and its suppression by actinomycin D. Nature New Biology 241, 85-86.
12. BOURQUE, M. J. & ROBITAILLE, R. (1998) Endogenous peptidergic modulation of perisynaptic Schwann cells at the frog neuromuscular junction. Journal of Physiology 512(Pt 1), 197-209.
13. BREDT, D. S. & SNYDER, S. H. (1992) Nitric oxide, a novel neuronal messenger. Neuron 8, 3-11.
14. BRENMAN, J. E. & BREDT, D. S. (1997) Synaptic signaling by nitric oxide. Current Opinion in Neurobiology 7, 374-378.
15. CARLSON, S. S., WAGNER, J. A. & KELLY, R. B. (1978) Purification of synaptic vesicles from Elasmobranch electric organ and the use of biophysical criteria to demonstrate purity. Biochemistry 17, 1188-1199.
16. CASTONGUAY, A., LÉVESQUE, S. & ROBITAILLE, R. (2001) Glial cells as active partners in synaptic functions. Progress in Brain Research 132, 227-240.
17. 2+ internal stores at the neuromuscular synapse. Journal of Neuroscience 21, 1911-1922.
18. CHEN, L. & KO, C. P. (1994) Extension of synaptic extracellular matrix during nerve terminal sprouting in living frog neuromuscular junctions. Journal of Neuroscience 14, 796-808.
19. COHEN, J. L., WEISS, K. R. & KUPFERMANN, I. (1978) Motor control of buccal muscles in Aplysia. Journal of Neurophysiology 41, 157-180.
20. COUTEAUX, R. & PECOT-DECHAVASSINE, M. (1974) [Specialized areas of presynaptic membranes]. Comptes rendus hebdomadaires des seances de l'Academie des sciences. Serie D: Sciences Naturelles 278, 291-293.
21. DANBOLT, N. C. (2001) Glutamate uptake. Progress in Neurobiology 65, 1-105.
22. DAVIS, G. W., SCHUSTER, C. M. & GOODMAN, C. S. (1996) Genetic dissection of structural and functional components of synaptic plasticity. III. CREB is necessary for presynaptic functional plasticity. Neuron 17, 669-679.
23. DENNIS, M. J. & MILEDI, R. (1974) Electrically induced release of acetylcholine from denervated Schwann cells. Journal of Physiology 237, 431-452.
24. DESCARRIES, L. M., CAI, S. & ROBITAILLE, R. (1998) Localization and characterization of nitric oxide synthase at the frog neuromuscular junction. Journal of Neurocytology 27, 829-840.
25. DOWDALL, M. J., BOYNE, A. F. & WHITTAKER, V. P. (1974) Adenosine triphosphate: A constituant of cholinergique synaptic vesicles. Biochemical Journal 140, 1-12.
26. GEORGIOU, J. & CHARLTON, M. P. (1999) Non-myelin-forming perisynaptic schwann cells express protein zero and myelin-associated glycoprotein. Glia 27, 101-109.
27. GEORGIOU, J., ROBITAILLE, R. & CHARLTON, M. P. (1999) Muscarinic control of cytoskeleton in perisynaptic glia. Journal of Neuroscience 19, 3836-3846.
28. GEORGIOU, J., ROBITAILLE, R., TRIMBLE, W. S. & CHARLTON, M. P. (1994) Synaptic regulation of glial protein expression in vivo. Neuron 12, 443-455.
29. GROZDANOVIC, Z. & GOSSRAU, R. Co-localization of nitric oxide synthase I (NOS I) and NMDA receptor subunit 1 (NMDAR-1) at the neuromuscular junction in rat and mouse skeletal muscle. Cell Tissue Research 29, 57-63
30. HERRERA, A. A., QIANG, H. & KO, C. P. (2000) The role of perisynaptic Schwann cells in development of neuromuscular junctions in the frog (Xenopus laevis). Journal of Neurobiology 45, 237-254.
31. HINZ, I. & WERNIG, A. (1988) Prolonged nerve stimulation causes changes in transmitter release at the frog neuromuscular junction. Journal of Physiology 401, 557-565.
32. ILLES, P., KLOTZ, K.-N. & LOSHE, M. J. (2000) Signaling by extracellular nucleotides and nucleosides. Naunyn-Schmiedeberg's Archives of Pharmacology 362, 295-298.
33. JAHROMI, B. S., ROBITAILLE, R. & CHARLTON, M. P. (1992) Transmitter release increases intracellular calcium in perisynaptic Schwann cells in situ. Neuron 8, 1069-1077.
34. JORDAN, C. L. & WILLIAMS, T. J. (2001) Testosterone regulates terminal Schwann cell number and junctional size during developmental synapse elimination. Developmental Neuroscience 23, 441-451.
35. KATZ, B. (1971) Quantal mechanism of neural transmitter release. Science 173, 123-126.
36. KARHUNEN, T., VILIM, F. S., ALEXEEVA, V., WEISS, K. R., & CHURCH, P. J. (2001) Targeting of peptidergic vesicles in cotransmitting terminals. Journal of Neuroscience 21, 1-5.
37. KO, C. P. (1981) Electrophysiological and freeze-fracture studies of changes following denervation at frog neuromuscular junctions. Journal of Physiology 321, 627-639.
38. KOIRALA, S., QIANG, H. & KO, C. P. (2000) Reciprocal interactions between perisynaptic Schwann cells and regenerating nerve terminals at the frog neuromuscular junction. Journal of Neurobiology 44, 343-360.
39. KUSNER, L. L. & KAMINSKI, H. J. (1996) Nitric oxide synthase is concentrated at the skeletal muscle endplate. Brain Research 730, 238-242.
40. LEE, K. H., BAEK, M. Y., MOON, K. Y., SONG, W. K., CHUNG, C. H., HA, D. B. & KANG, M. S. (1994) Nitric oxide as a messenger molecule for myoblast fusion. Journal of Biological Chemistry 269, 14371-14374.
41. LÉVESQUE, S. & ROBITAILLE, R. (2000) Ca2+-independent ionotropic glutamate depression of transmitter release at the amphibian neuromuscular junction. Society for Neuroscience Abstract 26, 884.
42. LINDGREN, C. A. & LAIRD, M. V. (1994) Nitroprusside inhibits neurotransmitter release at the frog neuromuscular junction. Neuroreport 5, 2205-2208.
43. LIOU, H. C., YANG, R. S. & FU, W. M. (1996) Potentiation of spontaneous acetylcholine release from motor nerve terminals by glutamate in Xenopus tadpoles. Neuroscience 75, 325-331.
44. LNENICKA, G. A., ATWOOD, H. L. & MARIN, L. (1986) Morphological transformation of synaptic terminals of a phasic motoneuron by long-term tonic stimulation. Journal of Neuroscience 6, 2252-2258.
45. LNENICKA, G. A. & ZHAO, Y. G. (1991) Seasonal differences in the physiology and morphology of crayfish motor terminals. Journal of Neurobiology 22, 561-569.
46. LOVE, F. M. & THOMPSON, W. J. (1999) Glial cells promote muscle reinnervation by responding to activity-dependent postsynaptic signals. Journal of Neuroscience 19, 10390-10396.
47. LUBISCHER, J. L. & BEBINGER, D. M. (1999) Regulation of terminal Schwann cell number at the adult neuromuscular junction. Journal of Neuroscience 19, RC46.
48. MADDEN, K. S. & VAN DER KLOOT, W. (1985) Indomethacin, prostaglandin E2 and transmission at the frog neuromuscular junction. Journal of Pharmacology and Experimental Therapeutics 232, 305-314.
49. MADDEN, K. S. & VAN DER KLOOT, W. (1982) At the frog neuromuscular junction prostaglandin synthase inhibitors depress and PGE partially restores quantal acetylcholine release. Brain Research 234, 464-468.
50. MAGLEBY, K. L. & ZENGEL, J. E. (1976) Augmentation: A process that acts to increase transmitter release at the frog neuromuscular junction. Journal of Physiology 257, 449-470.
51. MALLART, A. & MARTIN, A. R. (1968) The relation between quantum content and facilitation at the neuromuscular junction of the frog. Journal of Physiology 196, 593-604.
52. MALOMUZH, A. I., MUKHTAROV, M. R., URAZAEV, A. K., NIKOL'SKII, E. E. & VYSKOCHIL, F. (2002) The effects of glutamate on spontaneous acetylcholine secretion processes in the rat neuromuscular synapse. Neuroscience and Behavioral Physiology 32, 577-582.
53. MATTEOLI, M., HAIMANN, C. & DE CAMILLI, P. (1990) Substance P-like immunoreactivity at the frog neuromuscular junction. Neuroscience 37, 271-275.
54. MATTEOLI, M., HAIMANN, C., TORRI-TARELLI, F., POLAK, J. M., CECCARELLI, B., & DE CAMILLI, P. (1988) Differential effect of a-latrotoxin on exocytosis from small synaptic vesicles and from large dense-core vesicles containing calcitonin gene-related peptide at the frog neuromuscular junction. Proceedings of National Academy of Science 85, 7366-7370.
55. MAZZANTI, M., SUL, J. Y. & HAYDON, P. G. (2001) Glutamate on demand: Astrocytes as a ready source. Neuroscientist 7, 396-405.
56. MEHTA, A., REYNOLDS, M. L. & WOOLF, C. J. (1993) Partial denervation of the medial gastrocnemius muscle results in growth-associated protein-43 immunoreactivity in sprouting axons and Schwann cells. Neuroscience 57, 433-442.
57. MEUNIER, F.-M., ISRAEL, M. & LESBATS, B. (1975) Release of ATP from stimulated nerve electroplaque junctions. Nature 257.
58. NGUYEN, P. V. & ATWOOD, H. L. (1990) Expression of long-term adaptation of synaptic transmission requires a critical period of protein synthesis. Journal of Neuroscience 10, 1099-1109.
59. OKADA, D. (1992) Two pathways of cyclic GMP production through glutamate receptor-mediated nitric oxide synthesis. Journal of Neurochemistry 59, 1203-1210.
60. O'MALLEY, J. P., WARAN, M. T. & BALICE-GORDON, R. J. (1999) In vivo observations of terminal Schwann cells at normal, denervated, and reinnervated mouse neuromuscular junctions. Journal of Neurobiology 38, 270-286.
61. PAPPAS, D., HARZATI, L. N. & ROBITAILLE, R. (1999) Arachidonic acid and PGE2 as possible glial modulators of synaptic activity at the frog neuromuscular junction. Society for Neuroscience Abstract 25, 1256.
62. PARPURA, V., BASARSKY, T. A., LIU, F., JEFTINIJA, K., JEFTINIJA, S. & HAYDON, P. G. (1994) Glutamate-mediated astrocyte-neuron signalling. Nature 369, 744-747.
63. PEPER, K., DREYER, F., SANDRI, C., AKERT, K. & MOOR, H. (1974) Structure and ultrastructure of the frog motor endplate. A freeze-etching study. Cell Tissue Research 149, 437-455.
64. PINARD, A., LÉVESQUE, S., VALLÉE, J. & ROBITAILLE, R. (2002) NO-dependence of glutamate-mediated synaptic depression at the frog neuromuscular junction. Society for Neuroscience Abstract 838.6.
65. QUINSON, N., MIOLAN, J. P. & NIEL, J. P. (2000) Muscarinic receptor activation is a prerequisite for the endogenous release of nitric oxide modulating nicotinic transmission within the coeliac ganglion in the rabbit. Neuroscience 95, 1129-1138.
66. REGEHR, W. G. & STEVENS, C. F. (2001) Physiology of synaptic transmission and short-term plasticity. In Synapses (edited by STEVENS, C. F.) pp. 135-175. Baltimore: Johns Hopkins University Press.
67. REIST, N. E. & SMITH, S. J. (1992) Neurally evoked calcium transients in terminal Schwann cells at the neuromuscular junction. Proceeding of the National Academy of Sciences 89, 7625-7629.
68. REYNOLDS, M. L. & WOOLF, C. J. (1992) Terminal Schwann cells elaborate extensive processes following denervation of the motor endplate. Journal of Neurocytology 21, 50-66.
69. ROBITAILLE, R., ADLER, E. M. & CHARLTON, M. P. (1990) Strategic location of calcium channels at transmitter release sites of frog neuromuscular synapses. Neuron 5, 773-779.
70. ROBITAILLE, R. (1995) Purinergic receptors and their activation by endogenous purines at perisynaptic glial cells of the frog neuromuscular junction. Journal of Neuroscience 15, 7121-7131.
71. ROBITAILLE, R. (1998) Modulation of synaptic efficacy and synaptic depression by glial cells at the frog neuromuscular junction. Neuron 21, 847-855.
72. 2+ channels at perisynaptic glial cells of the frog neuromuscular junction. Journal of Neuroscience 16, 148-158.
73. ROBITAILLE, R., JAHROMI, B. S. & CHARLTON, M. P. (1997) Muscarinic Ca2+ responses resistant to muscarinic antagonists at perisynaptic Schwann cells of the frog neuromuscular junction. Journal of Physiology 504(Pt 2), 337-347.
74. ROCHON, D., ROUSSE, I. & ROBITAILLE, R. (2001) Synapse-glia interactions at the mammalian neuromuscular junction. Journal of Neuroscience 21, 3819-3829.
75. ROSENTHAL, J. (1969) Post-tetanic potentiation at the neuromuscular junction of the frog. Journal of Physiology 203, 121-133.
76. ROUSSE, I. & ROBITAILLE, R. (2001) Frequency dependence of synapse-glia interactions at the mammalian neuromuscular junction. Society for Neuroscience Abstract 383.10.
77. SALPETER, M. (1987) Vertebarte neuromuscular junctions: General morphology, molecular orgaization, and functional consequences. In The Vertebrate Neuromuscular Junction (edited by Salpeter, M. & Liss, A. R.) Vol. 23, pp. 1-54. New York.
78. SMITH, D. O. (1991) Sources of adenosine released during neuromuscular transmission in the rat. Journal of Physiology 432, 343-354.
79. SOARES-MOTA, M., HENZE, I. & MENDEZ-OTERO, R. (2001) Nitric oxide synthase-positive neurons in the rat superior colliculus: Colocalization of NOS with NMDAR1 glutamate receptor, GABA, and parvalbumin. Journal of Neuroscience Research 64, 501-507.
80. SOMASEKHAR, T., NORDLANDER, R. H. & REISER, P. J. (1996) Alterations in neuromuscular junction morphology during fast-to-slow transformation of rabbit skeletal muscles. Journal of Neurocytology 25, 315-331.
81. SON, Y. J. & THOMPSON, W. J. (1995a) Nerve sprouting in muscle is induced and guided by processes extended by Schwann cells. Neuron 14, 133-141.
82. SON, Y. J. & THOMPSON, W. J. (1995b) Schwann cell processes guide regeneration of peripheral axons. Neuron 14, 125-132.
83. SON, Y. J., TRACHTENBERG, J. T. & THOMPSON, W. J. (1996) Schwann cells induce and guide sprouting and reinnervation of neuromuscular junctions. Trends in Neurosciences 19, 280-285.
84. STEINACKER, A. (1977) Calcium-dependent presynaptic action of substance P at the frog neuromuscular junciton. Nature 267, 268-270.
85. TASHIRO, T. & STADLER, H. (1978) Chemical composition of cholinergic synaptic vesicles from Torpedo marmorata based on improved purification. Journal of Biochemistry 90, 479-487.
86. 2+-ATPase. Proceedings of the National Academy of Sciences 87, 2466-2470.
87. THOMAS, S. & ROBITAILLE, R. (2001) Differential frequency-dependent regulation of transmitter release by endogenous nitric oxide at the amphibian neuromuscular synapse. Journal of Neuroscience 21, 1087-1095.
88. ULLIAN, E. M. & BARRES, B. A. (1998) The Schwann song of the glia-less synapse. Neuron 21, 651-652.
89. VAN DER KLOOT, W., BENJAMIN, W. B. & BALEZINA, O. P. (1998) Calcintonin gene-related peptide acts presynaptically to increase quantal size and output at frog neuromuscular junctions. Journal of Physiology 507, 689-695.
90. VILIM, F. S., PRICE, D. A., LESSER, W., KUPFERMANN, I. & WEISS, K. R. (1996) Costorage and corelease of modulatory peptide cotransmitters with partially antagonistic actions on the accessory radula closer muscle of Aplysia californica. Journal of Neuroscience 16, 8092-8104.
91. WAERHAUG, O. & OTTERSEN, O. P. (1993) Demonstration of glutamate-like immunoreactivity at rat neuromuscular junctions by quantitative electron microscopic immunocytochemistry. Anatomy and Embryology (Berlin) 188, 501-513.
92. WANG, T., XIE, Z. & LU, B. (1995) Nitric oxide mediates activity-dependent synaptic suppression at developing neuromuscular synapses. Nature 374, 262-266.
93. WERNIG, A., DORLOCHTER, M. & PALAZIS, P. (1996) Differential sensitivity to Mg(2+)-and tubocurarine-block of frog neuromuscular junctions in summer and winter. Neuroscience Letters 207, 41-44.
94. WHIM, M. D., LLOYD, P. E. (1989) Frequency-dependent release of peptide cotransmitters from identified cholinergic motor neurons in Aplysia. Proceedings of the National Academy of Sciences 86, 9034-9038.
95. WOOLF, C. J., REYNOLDS, M. L., CHONG, M. S., EMSON, P., IRWIN, N. & BENOWITZ, L. I. (1992) Denervation of the motor endplate results in the rapid expression by terminal Schwann cells of the growth-associated protein GAP-43. Journal of Neuroscience 12, 3999-4010.
96. YAMADA, K. & NABESHIMA, T. (1997) Two pathways of nitric oxide production through glutamate receptors in the rat cerebellum in vivo. Neuroscience Research 28, 93-102.
97. YANG, C. C., ALVAREZ, R. B., ENGEL, W. K., HAUN, C. K. & ASKANAS, V. (1997) Immunolocalization of nitric oxide synthases at the postsynaptic domain of human and rat neuromuscular junctions - light and electron microscopic studies. Exp. Neurol. 148, 34-44.
98. YOUNG, M. E., RADDA, G. K. & LEIGHTON, B. (1997) Nitric oxide stimulates glucose transport and metabolism in rat skeletal muscle in vitro. Biochem J. 322, 223-228.
99. ZIMMERMANN, H. (2000) Extracellular metabolism of ATP and other nucleotides. Naunyn-Schmiedeberg's Archives of Pharmacology 362, 299-309.
100. ZUCKER, R. S. & REGEHR, W. G. (2002) Short-term synaptic plasticity. Annual Review of Physiology 64, 355-405.