Functional innervation of cultured human skeletal muscle proceeds by two modes with regard to agrin effects

Neuroscience

Volumn 118, Issue 1, 2003, Pages 87-97

  Mars, T ^a   King, M P ^b   Miranda, A F ^c   Walker, W F ^c   Mis, K ^a   Grubic, Z ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c Columbia University ^*  (United States)

Author keywords

Acetylcholine receptor; Anti agrin antibody; End plate; In vitro innervation; Neuromuscular junction; Synaptogenesis

Indexed keywords

AGRIN; ANTIBODY AGR 33; NICOTINIC RECEPTOR; PROTEIN ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; COCULTURE; CONTROLLED STUDY; EMBRYO; EXPLANT; HUMAN; HUMAN TISSUE; IN VITRO STUDY; MUSCLE CONTRACTION; MUSCLE DEVELOPMENT; MUSCLE FIBER CULTURE; MUSCLE INNERVATION; MYOTUBE; NEUROMUSCULAR SYNAPSE; NEUROMUSCULAR TRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; SKELETAL MUSCLE; SPINAL CORD; SYNAPTOGENESIS;

EID: 0037466262     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(02)00765-0     Document Type: Article

References (40)

1. Anderson M.J., Cohen M.W. Nerve-induced and spontaneous redistribution of acetylcholine receptors on cultured muscle cells. J Physiol. 268:1977;757-773.
2. Askanas V., Kwan H., Alvarez R.B., Engel W.K., Kobayashi T., Martinuzzi A., Hawkins E.F. De novo neuromuscular junction formation on human muscle fibres cultured in monolayer and innervated by foetal rat spinal cord ultrastructural and ultrastructural-cytochemical studies . J Neurocytol. 16:1987;523-537.
3. Burden S.J. The formation of neuromuscular synapses. Gene Dev. 12:1998;133-148.
4. Bowe M.A., Deyst K.A., Leszyk J.D., Fallon J.R. Identification and purification of an agrin receptor from Torpedo postsynaptic membranes a heteromeric complex related to the dystroglycans . Neuron. 12:1994;1173-1180.
5. Burgess R.W., Skarnes W.C., Sanes J.R. Agrin isoforms with distinct amino termini differential expression, localization, and function . J Cell Biol. 151:2000;41-52.
6. Cohen S.A., Fischbach G.D. Regulation of muscle acetylcholine sensitivity by muscle activity in cell culture. Science. 181:1973;76-78.
7. DeChiara T.M., Bowen D.C., Valenzuela D.M., Simmons M.V., Poueymirou W.T., Thomas S., Kinetz E., Compton D.L., Rojas E., Park J.S., Smith C., DiStefano P.S., Glass D.J., Burden S.J., Yancopoulos G.D. The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell. 85:1996;501-512.
8. Fallon J.R., Nitkin R.M., Reist N.E., Wallace B.G., McMahan U.J. Acetylcholine receptor-aggregating factor is similar to molecules concentrated at neuromuscular junctions. Nature. 315:1985;571-574.
9. Ferns M.J., Campanelli J.T., Hoch W., Scheller R.H., Hall Z. The ability of agrin to cluster AChRs depends on alternative splicing and on cell surface proteoglycans. Neuron. 11:1993;491-502.
10. Fuentes M.E., Taylor P. Control of acetylcholinesterase gene expression during myogenesis. Neuron. 10:1993;679-687.
11. Gautam M., DeChiara T.M., Glass D.J., Yancopoulos G.D., Sanes J.R. Distinct phenotypes of mutant mice lacking agrin, MuSK, or rapsyn. Brain Res Dev Brain Res. 114:1999;171-178.
12. Gautam M., Noakes P.G., Moscoso L., Rupp F., Scheller R.H., Merlie J.P., Sanes J.R. Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell. 85:1996;525-535.
13. Grubic Z., Komel R., Walker W.F., Miranda A.F. Myoblast fusion and innervation with rat motor nerve alter distribution of acetylcholinesterase and its mRNA in cultures of human muscle. Neuron. 14:1995;317-327.
14. Guettier-Sigrist S., Coupin G., Warter J.M., Poindron P. Cell types required to efficiently innervate human muscle cells in vitro. Exp Cell Res. 259:2000;204-212.
15. Hirano Y., Kidokoro Y. Heparin and heparan sulfate partially inhibit induction of acetylcholine receptor accumulation by nerve in Xenopus culture. J Neurosci. 9:1989;1555-1561.
16. Hoch W. Formation of the neuromuscular junction agrin and its unusual receptors . Eur J Biochem. 265:1999;1-10.
17. Hoch W., Campanelli J.T., Harrison S., Scheller R.H. Structural domains of agrin required for clustering of nicotinic acetylcholine receptors. EMBO J. 13:1994;2814-2821.
18. Hopf C., Hoch W. Heparin inhibits acetylcholine receptor aggregation at two distinct steps in the agrin-induced pathway. Eur J Neurosci. 9:1997;1170-1177.
19. Inestrosa N.C., Miller J.B., Silberstein L., Ziskind-Conhaim L., Hall Z.W. Developmental regulation of 16S acetylcholinesterase and acetylcholine receptors in a mouse muscle cell line. Exp Cell Res. 147:1988;393-405.
20. Jacobson C., Cote P.D., Rossi S.G., Rotundo R.L., Carbonetto S. The dystroglycan complex is necessary for stabilization of acetylcholine receptor clusters at neuromuscular junctions and formation of the synaptic basement membrane. J Cell Biol. 152:2001;435-450.
21. Kobayashi T., Askanas V. Acetylcholine receptors and acetylcholinesterase accumulate at the nerve-muscle contacts of de novo grown human monolayer muscle cocultured with fetal rat spinal cord. Exp Neurol. 88:1985;327-335.
22. Kobayashi T., Askanas V., King Engel W. Human muscle cultured in monolayer and cocultured with fetal rat spinal cord importance of dorsal root ganglia for achieving successful functional innervation . J Neurosci. 7:1987;3131-3141.
23. Lin W., Burgess R.W., Dominguez B., Pfaff S.L., Sanes J.R., Lee K.F. Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse. Nature. 410:2001;1057-1064.
24. Lisak R.R., Barchi R.L. Myastenia gravis. 1982;Saunders, Philadelphia.
25. Mars T., King M.P., Miranda A.F., Grubic Z. Heparin blocks functional innervation of cultured human muscle by rat motor nerve. Pflug Arch Eur J Physiol. 439:((suppl 3):):2000;R36-37.
26. Mars T., Yu K.J., Tang X.-M., Miranda A.F., Grubic Z., Cambi F., King M.P. Differentiation of glial cells and motor neurons during the formation of neuromuscular junctions in co-cultures of rat spinal cord explant and human muscle. J Comp Neurol. 438:2001;239-251.
27. Martin P.T., Sanes J.R. Role for a synapse-specific carbohydrate in agrin-induced clustering of acetylcholine receptors. Neuron. 14:1995;743-754.
28. McMahan U.J. The agrin hypothesis. Cold Spring Harb Symp Quant Biol. 55:1990;407-418.
29. Montanaro F., Gee S.H., Jacobson C., Lindenbaum M.H., Froehner S.C., Carbonetto S. Laminin and alpha-dystroglycan mediate acetylcholine receptor aggregation via a MuSK-independent pathway. J Neurosci. 18:1998;1250-1260.
30. Moody-Corbett F., Cohen M.W. Localization of cholinesterase at sites of high acetylcholine receptor density on embryonic amphibian muscle cells cultured without nerve. J Neurosci. 1:1981;596-605.
31. Reist N.E., Werle M.J., McMahan U.J. Agrin released by motor neurons induces the aggregation of acetylcholine receptors at neuromuscular junctions. Neuron. 8:1992;865-868.
32. Sanes J.R., Apel E.D., Gautam M., Glass D., Grady R.M., Martin P.T., Nichol M.C., Yancopoulos G.D. Agrin receptors at the skeletal neuromuscular junction. Ann NY Acad Sci. 841:1998;1-13.
33. Sanes J.R., Jessell T.M. The formation and regeneration of synapses. Kandel E.R., Schwartz J.H., Jessel T.M. Principles of neuronal science. 2000;1087-1114 Elsevier, New York.
34. Sanes J.R., Lichtman J.W. Development of the vertebrate neuromuscular junction. Annu Rev Neurosci. 22:1999;389-442.
35. Sanes J.R., Lichtman J.W. Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat Rev Neurosci. 2:2001;791-805.
36. Schaeffer L., de Kerchove d'Exaerde A., Changeux J.P. Targeting transcription to the neuromuscular synapse. Neuron. 31:2001;15-222.
37. Sugiyama J.E., Glass D.J., Yancopoulos G.D., Hall Z.W. Laminininduced acetylcholine receptor clustering an alternative pathway . J Cell Biol. 139:1997;181-191.
38. Tanji K., Sancho S., Miranda A.F. Innervation of MyoD-converted human amniocytes and fibroblast by fetal rodent spinal cord neurons. Neuromuscul Disord. 4:1994;317-324.
39. Wallace B.G. Inhibition of agrin-induced acetylcholine-receptor aggregation by heparin, heparan sulfate, and other polyanions. J Neurosci. 10:1990;3576-3582.
40. Yang X., Arber S., William C., Li L., Tanabe Y., Jessell T.M., Birchmeier C., Burden S.J. Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron. 30:2001;399-410.