Deficient development and maintenance of postsynaptic specializations in mutant mice lacking an 'adult' acetylcholine receptor subunit

Development

Volumn 124, Issue 24, 1997, Pages 5075-5086

  Missias, Andrea C ^a   Mudd, Jacqueline ^a   Cunningham, Jeanette M ^a   Steinbach, Joseph H ^a   Merlie, John P ^a   Sanes, Joshua R ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Department of Anatomy ^*

Author keywords

Acetylcholine receptor; Mouse; Neuromuscular junction; Synapse formation

Indexed keywords

CHOLINERGIC RECEPTOR; RECEPTOR SUBUNIT;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; GENE DELETION; MOUSE; MOUSE MUTANT; NERVE ENDING; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; RECEPTOR DENSITY; RECEPTOR GENE;

ANIMALS; BINDING SITES; BUNGAROTOXINS; CYTOSKELETAL PROTEINS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MICE, NEUROLOGIC MUTANTS; MOTOR ENDPLATE; MUSCLE WEAKNESS; MUSCLE, SKELETAL; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, CHOLINERGIC; SYNAPTIC MEMBRANES;

EID: 0031457057     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (75)

1. Balice-Gordon, R. J. and Lichtman, J. W. (1993). In vivo observations or pre and postsynaptic changes during the transition from multiple to single innervation at developing neuromuscular junctions. J. Neurosci. 13, 834-855.
2. Balice-Gordon, R. J. and Lichtman, J. W. (1994). Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature 372, 519-524.
3. Brenner, H. R., Witzemann, V. and Sakmann, B. (1990). Imprinting of acetylcholine receptor messenger RNA accumulation in mammalian neuromuscular synapses. Nature 344, 544-547.
4. Brooks-Kayal, A. R. and Pritchett, D. B. (1993). Developmental changes in human gamma-aminobutyric acidA receptor subunit composition. Annals Neurol. 34, 687-693.
5. Brown, M. C., Holland, R. L. and Hopkins, W. G. (1981) Motor nerve sprouting. Ann. Rev. Neurosci. 4, 17-42.
6. Brown, M. C., Hopkins, W. G., Keynes, R. J. and White, I. (1982) A comparison of early morphological changes at denervated and paralyzed endplates in fast and slow muscles of the mouse, Brain Res. 248, 382-386.
7. Buonanno, A., Mudd, J. and Merlie, J. P. (1989) Isolation and characterization of the beta and epsilon subunit genes of mouse muscle acetylcholine receptor. J. Biol. Chem. 264, 7611-7616.
8. Colman, H. and Lichtman, J. W. (1993) Interactions between nerve and muscle: synapse elimination at the developing neuromuscular junction. Dev. Biol. 156, 1-10.
9. Chomcznski, P. and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocynanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
10. Decker, E. R. and Dani, J. A. (1990). Calcium permeability of the nicotinic acetylcholine receptor: the single-channel calcium influx is significant. J. Neurosci. 10, 3413-3420.
11. Donoghue, M. J., Merlie, J. P., Rosenthal, N. and Sanes, J. R. (1991). Rostrocaudal gradient of transgene expression in adult skeletal muscle. Proc. Natl. Acad. Sci. USA 88, 5847-5851.
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. Engel, A. G. (1994a). Congenital myasthenic syndromes. Neurol. Clin. North Amer. 12, 401-437.
14. Engel, A. G. (1994b). Acquired autoimmune myasthenia gravis. In Myology (ed. A. G. Engel and C. Franzini-Armstrong). pp. 1769-1797. New York. McGraw Hill.
15. Engel, A. G., Lambert, E. H., Mulder, D.M., Torres, G.F., Sahashi, K., Bertorini, T.E., Whitaker, J.N. (1982). A newly recognized congenital myasthenic syndrome attributed to a prolonged open time of the acetylcholine-induced ion channel. Ann. Neurol. 11, 553-569.
16. Fambrough, D. M., Drachman, D. B. and Satyamurti, S. (1973). Neuromuscular junction in myasthenia gravis: decreased acetylcholine receptors. Science 182, 293-295.
17. Fischbach, G. D. and Schuetze, S. M. (1980). A post-natal decrease in acetylcholine channel open time at rat end-plates. J. Physiol. 303, 125-137.
18. Froehner, S. C., Douville, K., Klink, S. and Culp, W. J. (1983). Monoclonal antibodies to cytoplasmic domains of the acetylcholine receptor. J. Biol. Chem. 258, 7112-7120.
19. Froehner, S. C., Luetje, C. W., Scotland, P. B. and Patrick, J. (1990) The postsynaptic 43K protein clusters muscle nicotinic acetylcholine receptors in Xenopus oocytes. Neuron 5, 403-410.
20. Fumagalli, G., Balbi, S., Cangiano, A. and Lømo, T. (1990). Regulation of turnover and number of acetslcholine recepors at neuromuscular junctions. Neuron 4, 563-569.
21. Gautam, M., Noakes, P. G., Moscoso, L., Rupp, F. Scheller, R. H., Merlie, J. P. and Sanes, J. R. (1996). Detective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85, 525-535.
22. Gautam, M., Noakes, P. G., Mudd, J., Nichol, M., Chu, G. C., Sanes, J. R. and Merlie, J. P. (1995). Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature 377, 232-236.
23. Goldman, D. and Staple, J. (1989). Spatial and temporal expression of acetylcholine receptor RNAs in innervated and denervated rat solcus muscle. Neuron 3, 219-228.
24. Gomez, C.M., Bhattacharyya, B.B., Charnet, P., Day, J.W., Labarca, C., Wollmann, R.L. and Lambert, E. H. (1996). A transgenic mouse model of the slow-channel syndrome. Muscle and Nerve 19, 79-87.
25. Gu, Y. and Hall, Z. W. (1988). Immunological evidence for a change in subunits of the acetylcholine receptor in developing and denervated rat muscle. Neuron 1, 117-125.
26. Gundersen, K., Sanes, J. R. and Merlie, J. P. (1993). Neural regulation of muscle acetycholine receptor epsilon and alpha subunit gene promoters in transgenic mice. J. Cell Biol. 123, 1535-1544.
27. Hall, Z. W. and Sanes, J. R. (1993) Synaptic structure and development: the neuromuscular junction. Cell/Neuron 72 (Supplement). 99-121.
28. Jaramillo F., Vicini, S., Schuetze, S.M., (1988) Embryonic acetylcholine receptors guarantee spontaneous contractions in rat developing muscle. Nature 335, 66-68.
29. Karnovsky, M. J. (1964). The localization of cholinesterase activity in rat cardiac muscle by electron microscopy. J. Cell Biol. 23, 117-232.
30. Katz., B. and Miledi, R. (1973). The binding of acetylcholine to receptors and its removal from the synaptic cleft. J. Physiol. 231, 549-574.
31. kopta, C. and Steinbach, J. H. (1994). Comparison of mammalian adult and fetal nicotinic acetylcholine receptors stably expressed in fibroblasts. J. Neurosci. 14, 3922-3933.
32. kreienkamp, H.-J., Maeda, R. K., Sine, S. M. and Taylor, P. (1995). Intersubunit contacts governing assembly of the mammalian nicotinic acetylcholine receptor. Neuron 14, 635-644.
33. Kuhse, J., Laube, B., Magalei, D. and Betz, H. (1993) Assembly of the inhibitory glycine receptor: identification of amino acid sequence motifs governing subunit stoichiometry. Neuron 11, 1049-1056.
34. Lingle, C. J. and Steinbach, J. H. (1988). Neuromuscular blocking agents. Intl. Anesthesiol. Clin. 26, 288-301.
35. Martinou, J. C. and Merlie, J. P. (1991). Nerve-dependent modulation of acetylcholine receptor epsilon-subunit gene expression. J. Neurosci. 11, 1291-1299.
36. McGhee, D.S. and Role, L.W. (1993). Physiological diversity of nicotinic acetylcholine receptors expressed by vertebrate neurons. Annu. Rev. Physiol. 57, 521-546.
37. Miner, J. H. and Sanes, J. R. (1994). Collagen IV alpha 3, alpha 4 and alpha 5 chains in rodent basal laminae: sequence, distribution, association with laminins and developmental switches. J. Cell Biol. 127, 879-891.
38. Mishina, M., Takai, T., Imoto, K., Noda, M., Takahashi, T., Numa, S., Methfessel, C. and Sakmann, B. (1986). Molecular distinction between fetal and adult forms of muscle acetylcholine receptor. Nature 321, 406-411.
39. Missias, A. C., Chu, G. C., Klocke, B., R., S. J. and Merlie, J. P. (1996) Maturation of the acetylcholine receptor in skeletal muscle: regulation of the AChR γ-to-∈ switch. Dev. Biol. 179, 223-238.
40. Moscoso, L. M., Chu, G. C., Gautam, M., Noakes, P. G., Merlie, J. P. and Sanes, J. R. (1995a). Synapse-associated expression of an acetylcholine receptor-inducing protein. ARIA/heregulin and its putative receptors. erhB2 and erbB3. in developing mammalian muscle. Dev. Biol. 172, 158-169.
41. Moscoso, L. M., Merlie, J. P. and Sanes, J. R. (1995b) N-CAM. 43K-rapsyn and s-laminin mRNAs are concentrated at synaptic sites in muscle fibers. Mol. Cell. Neurosci. 6, 80-89.
42. Nagy, A., Rossant, J., Nagy, R., Abramow-Newerly, W. and Roder, J. C. (1993). Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. USA 90, 8424-8428.
43. Noakes, P. G., Gautam, M., Mudd, J., Sanes, J. R. and Merlie, J. P. (1995). Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/laminin β2 Nature 374, 258-262.
44. Noakes, P. G., Phillips, W. D., Hanley, T. A., Sanes, J. R. and Merlie, J. P. (1993). 43k protein and acetylcholine receptors colocalize during the initial stages of neuromuscular synapse formation in vivo. Dev. Biol. 155, 275-280.
45. Ohno, K., Hutchinson, D.O., Milone, M., Brengman, J. M., Bouzat, C., Sine, S. M. and Engel, A. G. (1995). Congenital myasthenic syndrome caused by prolonged acetylcholine receptor channel openings due to a mutation in the M2 domain of the ∈ subunit, Proc. Natl. Acad. Sci. USA 92, 758-762.
46. Ortells, M. O. and Lunt, G. G. (1995). Evolutionary history of the ligand-gated ion-channel superfamily of receptors. Trends in Neurosci. 18, 121-127.
47. Paton, W. D. M. and Waud, D. R. (1967). The margin of safety of neuromuscular transmission. J. Physiol. 191, 59-90.
48. Phillips, W. D., Kopta, C., Blount, P., Gardner, P. D., Steinbach, J. H. and Merlie, J. P. (1991). ACh receptor-rich membrane domains organized in fibroblasts by recombinant 43-kildalton protein. Science 251, 568-570.
49. Rajendra, S., Lynch, J. W. and Schofield, P. R. (1997) The glycine receptor Pharmacol. Ther. 73, 121-146.
50. Reiness, C. G. and Weinberg, C. B. (1981). Metabolic stabilization of acetylcholine receptors at newly formed neuromuscular junctions in rat. Dev. Biol. 84, 247-254.
51. Salpeter, M. M. (1987). Development and neural control ot'the neuromuscular junction and of the junctional acetylcholine receptor. In The Vertebrate Neuromuscular Junction. M. M. Salpeter. ed. (New York: Alan R. Liss, Inc.), pp. 55-115.
52. Salpeter, M. M., Marchaterre, M. and Harris, R. (1988) Distribution of extrajunctional acetylcholine receptors on a vertebrate muscle: evaluated by using a scanning electron microscope autoradiographic procedure. J. Cell Biol. 106, 2087-2093.
53. Sanes, J. R. (1997). Genetic analysis of postsynaptic differentiation at the vertebrate neuromuscular junction. Curr. Opin. Neurobiol. 7, 93-100.
54. Sanes, J. R., Johnson, Y. R., Kotzbauer, P. T., Mudd, J., Hanley, T., Martinou, J. C. and Merlie, J. P. (1991). Selective expression of an acetylcholine receptor-lacZ transgene in synaptic nuclei of adult muscle fibers. Development 113, 1181-1191.
55. Schuetzc, S. M. and Role, L. W. (1987). Developmental regulation of nicotinic acetylcholine receptors. Ann. Rev. Neurosci. 10, 403-457.
56. Scott, L. J., Bacou, F. and Sanes, J. R. (1988). A synapse-specific carbohydrate at the neuromuscular junction: association with both acetylcholmesterase and a glycolipid. J. Neurosci. 8, 932-44.
57. Sheng, M., Cummings, J., Roldan, L. A., Jan, Y. N. and Jan, L. Y. (1994). Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 368, 144-147.
58. Siegelbaum, S. A., Trautmann, A. and Koenig, J. (1984). Single acetylcholine-activaled channel currents in developing muscle cells. Dev. Biol. 104, 366-379.
59. Slater, C. R. (1982). Postnatal maturation of nerve-muscle junctions in hindlimb muscles of the mouse. Dev. Biol. 94, 11-22.
60. Snedecor, G. W. and Cochran, W. G. (1967). Statistical Methods 6th Edition Ames, Iowa: Iowa Stale University Press.
61. Steinbach, J. H. (1981). Developmental changes in acetylcholine receptor aggregates at rat skeletal neuromuscular junctions. Dev. Biol. 84, 267-276.
62. Straus, W. (1982). Imidazole increases the sensitivity of the cytochemical reaction for peroxidase with diaminohenzidine at a neutral pH. J. Histochem. Cytochem. 30, 491-493.
63. Takahashi, T., Momiyama, A., Hirai, K., Hishinuma, F. and Akagi, H. (1992). Functional correlation of fetal and adult forms of glycine receptors with developmental changes in inhibitory synaptic receptor channels. Neuron 9, 1155-1161.
64. Thompson, W. J. (1985). Activity and synapse elimination at the neuromuscular junction. Cell. Mol. Neurobiol. 5, 167-182.
65. Tyhulewicz, V. L., Crawford, C. E., Jackson, P. K., Bronson, R. T. and Mulligan, R. C. (1991). Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl proto-oncogene. Cell 65, 1153-1163.
66. Tzartos, S., Langeberg, L., Hochschwender, S., Swanson, L. W. and Lindstrom, J. (1986). Characteristics of monoclonal antibodies to denatured Torpedo and to native calf acetylcholine receptors: species, subunit and region specificity. J. Neuroimmunol. 10, 235-253.
67. Tzartos, S. J., Rand, D. E., Einarson, B. L. and Lindstrom, J. M. (1981). Mapping of surface structures of electrophorus acetylcholine receptor using monoclonal antibodies. J. Biol. Chem. 256, 8635-8645.
68. Verrall, S. and Hall, Z. W. (1992). The N-terminal domains of acetylcholine receptor subunits contain recognition signals for the initial steps ot receptor assembly. Cell 68, 23-31.
69. Villarroel, A. and Sakmann, B. (1996). Calcium permeability increase of endplate channels in rat muscle during postnatal development. J. Physiol. 496, 331-338.
70. Westerfield, M., Liu, D. W., Kimmel, C. B. and Walker, C. (1990) Pathfinding and synapse formation in a zebrafish mutant lacking functional acetylcholine receptors. Neuron 4, 867-874.
71. Witzemann, V., Barg, B., Criado, M., Stein, E. and Sakmann, B. (1989) Developmental regulation of five subunit specific mRNAs encoding acetylcholine receptor subtypes in rat muscle. FEBS Lets. 242, 419-424.
72. Witzemann, V., Schwrz, H., Koenen, M., Berberich, C., Villarroel, A., Wernig, A., Brenner, H. R. and Sakmann, B. (1996) Acetylcholine receptor ∈-subunit deletion causes muscle weakness and atrophy in juvenile and adult mice. Proc. Natl. Acad. Sci. USA 93, 13286-13291.
73. Witzemann, V., Barg, B., Nishikawa, Y., Sakmann, B. and Numa, S. (1987). Differential regulation of muscle acetylcholine receptor gamma-and epsilon-subunit mRNAs. FEBS Lets 223, 104-12.
74. Zacks, S. I.(1973). The Motor Endplate Huntington. NY: Krieger Publishing.
75. Zhu, X. J., Lai, C., Thomas, S. and Burden, S. J. (1995). Neuregulin receptors, erbb3 and erbb4 are localized at neuromuscular synapses. EMBO J. 14, 5842-5848.