Rapsyn and agrin slow the metabolic degradation of the acetylcholine receptor

Molecular and Cellular Neurosciences

Volumn 10, Issue 1-2, 1997, Pages 16-26

  Phillips, William D ^a   Vladeta, Daniel ^a   Han, Hong ^a   Noakes, Peter G ^b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

AGRIN; CHOLINERGIC RECEPTOR; CYTOPLASM PROTEIN;

ANIMAL CELL; ARTICLE; CAPPING PHENOMENON; MUSCLE CELL; MYASTHENIA GRAVIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN STABILITY;

ANIMALIA;

EID: 0030708639     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1006/mcne.1997.0634     Document Type: Article

References (58)

1. Barrantes, F. J., Neugebauer, D., and Zingsheim, H. P. (1980). Peptide extraction by alkaline treatment is accompanied by rearrangement of the membrane-bound acetylcholine receptor from Torpedo Marmorata. FEBS. Lett. 112: 73-78.
2. Berg, D. K., and Hall, Z. W. (1975). Loss of alpha-bungarotoxin from junctional and extrajunctional acetylcholine receptors in rat diaphragm muscle in vivo and in organ culture. J. Physiol. 252: 771-789.
3. Bloch, R. J., Sealock, R., Pumplin, D. W., Luther, P. W., and Froehner, S. C. (1994). Association of acetylcholine receptors with peripheral membrane proteins: evidence from antibody-induced coaggregation. J. Membr. Biol. 138: 13-28.
4. Bursztajn, S., Nudleman, H. B., and Berman, S. A. (1987). Coated and smooth vesicles participate in acetylcholine receptor transport. Cell Tissue Res. 248: 535-540.
5. Caroni, P., Rotzler, S., Britt, J. C., and Brenner, H. R. (1993). Calcium influx and protein phosphorylation mediate the metabolic stabilization of synaptic acetylcholine receptors in muscle. J. Neurosci. 13: 1315-1325.
6. Cartaud, J., Sobel, A., Rousselet, A., Devaux, P. F., and Changeux, J. P. (1981). Consequences of alkaline treatment for the ultrastructure of the acetylcholine-receptor-rich membranes from Torpedo marmorata electric organ. J. Cell Biol. 90: 418-426.
7. Chang, C. C., and Huang, M. C. (1975). Turnover of junctional and extrajunctional acetylcholine receptors of the rat diaphragm. Nature 253: 643-644.
8. Chu, G. C., Moscoso, L. M., Sliwkowski, M. X., and Merlie, J. P. (1995). Regulation of the acetylcholine receptor ∈ subunit gene by recombinant ARIA: an in vitro model for transynaptic gene regulation. Neuron 14: 329-339.
9. Drachman, D. B., Angus, C. W., Adams, R. N., Michelson, J. D., and Hoffman, G. J. (1978). Myasthenic antibodies cross-link acetylcholine receptors to accelerate degradation. N. Engl. J. Med. 298: 1116-1122.
10. Dubinsky, J. M., Loftus, D. J., Fischbach, G. D., and Elson, E. L. (1989). Formation of acetylcholine receptor clusters in chick myotubes: migration or new insertion? J. Cell Biol. 109: 1733-1743.
11. 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.
12. Fumagalli, G., Engel, A. G., and Lindstrom, J. (1982). Ultrastructural aspects of acetylcholine receptor turnover at the normal end-plate and in autoimmune myasthenia gravis. J. Neuropathol. Exper. Neurol. 41: 567-579.
13. Gardner, J., and Fambrough, D. (1979). Acetylcholine receptor degradation measured by density labeling: Effects of cholinergic ligands and evidence against recycling. Cell 16: 661-674.
14. Gautam, M., Noakes, P. G., Moscoso, L., Rupp, F., Scheller, R. H., Merlie, J. P., and Sanes, J. R. (1996). Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85: 525-535.
15. 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.
16. Glass, D. J., Bowen, D. C., Stitt, T. N., Radiejewski, C., Brunno, J., Ryan, T. E., Gies, D. R., Shah, S., Mattsson, K., Burden, S. J., DiStefano, P. S., Valenzuela, D. M., DeChiara, T. M., and Yancopoulos, G. D. (1996). Agrin acts via a MuSK receptor complex. Cell 85: 513-523.
17. Graus, Y. M. F., Verschuuren, J. J. G. M., Spaans, F., Jennekens, F., van Breda Vriesman, P. J. C., and De Baets, M. H. (1993). Age-related resistance to experimental autoimmune myasthenia gravis in rats. J. Immunol. 150: 4093-4103.
18. 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.
19. Hall, Z. W., and Sanes, J. R. (1993). Synaptic structure and development: The neuromuscular junction. Cell 10: 99-121.
20. Hanley, T., and Merlie, J. P. (1991). Transgene detection in unpurified mouse tail DNA by polymerase chain reaction. BioTechniques 10: 56.
21. Heinemann, S., Bevan, S., Kullberg, R., Lindstrom, J., and Rice, J. (1977). Modulation of acetylcholine receptor by antibody against the receptor. Proc. Natl. Acad. Sci. USA 74: 3090-3094.
22. Hill, J. A., Nghiem, H. O., and Changeux, J. P. (1991). Serine-specific phosphorylation of nicotinic receptor associated 43K protein. Biochemistry 30: 5579-5585.
23. Hoch, W., Campanelli, J. T., Harrison, S., and Scheller, R. H. (1994). Structural domains of agrin required for clustering of nicotinic acetylcholine receptors. EMBO J. 13: 2814-2821.
24. Hyman, C., and Froehner, S. C. (1983). Degradation of acteylcholine receptors in muscle cells: Effect of leupeptin on turnover rate, intracellularopool sizes, and receptors properties. J. Cell Biol. 95: 1316-1324.
25. Kao, I., and Drachman, D. B. (1977). Myasthenic immunoglobulin accelerates acetylcholine receptor degradation. Science 196: 527-529.
26. Klieman, R. J., and Reichardt, L. F. (1996). Testing the agrin hypothesis. Cell 85: 461-464.
27. 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.
28. Kuncl, R. W., Drachman, D. B., and Adams, R. (1988). Inhibition of methyltransferase reduces the turnover of acetylcholine receptors. Proc. Natl. Acad. Sci. USA 85: 4032-4036.
29. Levitt, T. A., and Salpeter, M. M. (1981). Denervated endplates have a dual population of junctional acetylcholine receptors. Nature 291: 239-241.
30. Loutrari, H., Kokla, A., and Tzartos, S. J. (1992). Passive transfer of experimental myasthenia gravis via antigenic modulation of the acetylcholine receptor. Eur. J. Immunol. 22: 2449-2452.
31. Magill-Solc, C., and McMahan, U. J. (1990). Synthesis and transport of agrin-like molecules in motor neurons. J. Exp. Biol. 153: 1-10.
32. Martinou, J. C., and Merlie, J. P. (1991). Nerve dependent modulation of acetylcholine receptor ∈-subunit gene expression. J. Neurosci. 11: 1291-1299.
33. Meier, T., Perez, G. M., and Wallace, B. G. (1995). Immobilization of nicotinic acetylcholine receptors in mouse C2 myotubes by agrin-induced protein tyrosine phosphorylation. J. Cell Biol. 131: 441-451.
34. Merlie, J. P., Changeux, J.-P., and Gros, F. (1978). Skeletal muscle acetylcholine receptor purification, characterization and turnover in muscle cell cultures. J. Biol. Chem. 253: 2882-2891.
35. Morgan, J. E., Beauchamp, J. R., Pagel, C. N., Peckham, M., Ataliotis, P., Jat, P. S., Noble, M. D., Farmer, K., and Partridge, T. A. (1994). Myogenic cell lines derived from transgenic mice carrying a thermolabile T antigen: a model system for the derivation of tissue-specific and mutation-specific cell lines. Dev. Biol. 162: 486-498.
36. Nitkin, R. M., Smith, M. A., Magill, C., Fallon, J. R., Yao, Y. M., Wallace, B. G., and McMahan, U. J. (1987). Identification of agrin, a synaptic organizing protein from Torpedo electric organ. J. Cell Biol. 105: 2471-2478.
37. Patrick, J., McMillan, J., Wolfson, H., and O'Brien, J. C. (1977). Acetylcholine receptor metabolism in a non-fusing muscle cell line. J. Biol. Chem. 252: 2143-2153.
38. Phillips, W. D. (1997). Transfection in cell cultures. In A Beginners Guide to Neuroscience Methods (R. Martin, Ed.) Harwood Academic Publishers, Amsterdam. (In Press.)
39. Phillips, W. D., Kopta, C., Blount, P., Gardner, P. D., Steinbach, J. H., and Merlie, J. P. (1991a). ACh receptor-rich membrane domains organized in fibroblasts by recombinant 43-kilodalton protein. Science 251: 568-570.
40. Phillips, W. D., Maimone, M., and Merlie, J. P. (1991b). Mutagenesis of the 43-kD postsynaptic protein defines domains involved in plasma membrane targeting and AChR clustering. J. Cell Biol. 115: 1713-1723.
41. Phillips, W. D., Noakes, P. G., Roberds, S. L., Campbell, K. P., and Merlie, J. P. (1993). Clustering and immobilization of acetylcholine receptors by the 43-kD protein: A role for dystrophin-related protein. J. Cell Biol. 123: 729-740.
42. Pumplin, D. W., and Drachman, D. B. (1983). Myasthenic patients' IgG causes redistribution of acetylcholine receptors: Freeze-fracture studies. J. Neurosci. 3: 576-584.
43. Qu, Z., Apel, E. D., Doherty, C. A., Hoffman, P. W., Merlie, J. P., and Huganir, R. L. (1996). The synapse-associated protein rapsyn regulates tyrosine phosphorylation of proteins co-localized at nicotinic acetylcholine receptor clusters. Mol. Cell. Neurosci. 8: 171-184.
44. Qu, Z., and Huganir, R. L. (1994). Comparison of innervation and agrin-induced tyrosine phosphorylation of the nicotinic acetylcholine receptor. J. Neurosci. 14: 6834-6841.
45. 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.
46. Rotzler, S., Schramek, H., and Brenner, H. R. (1991). Metabolic stabilization of endplate acetylcholine receptors regulated by Ca2+ influx associated with muscle activity. Nature 349: 337-339.
47. Salpeter, M. M., Cooper, D. L., and Levitt-Gilmour, T. (1986). Degradation rates of acetylcholine receptors can be modified in the postjunctional plasma membrane of the vertebrate neuromuscular junction. J. Cell Biol. 103: 1399-1403.
48. Scotland, P. B., Colledge, M., Melnikova, Z., Dai, Z., and Froehner, S. C. (1993). Clustering of the acetylcholine receptor by the 43-kD protein: Involvement of the zinc finger domain. J. Cell Biol. 123: 719-728.
49. Sealock, R., Wray, B. E., and Froehner, S. C. (1984). Ultrastructural localization of the Mr 43,000 protein and the acetylcholine receptor in Torpedo postsynaptic membranes using monoclonal antibodies. J. Cell Biol. 98: 2239-2244.
50. Shyng, S.-L., Xu, R., and Salpeter, M. M. (1991). Cyclic AMP stabilizes the degradation of original junctional acetylcholine receptors in denervated muscle. Neuron 6: 469-475.
51. Stya, M., and Axelrod, D. (1983). Mobility and detergent extractability of acetylcholine receptors on cultured rat myotubes: A correlation. J. Cell Biol. 97: 48-51.
52. Tsui, H., Cohen, J. B., and Fischbach, G. D. (1990). Variation in the ratio of acetylcholine receptors and the Mr 43,000 receptor-associated protein in embryonic chick myotubes and myoblasts. Dev. Biol. 140: 437-446.
53. 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.
54. Tzartos, S. J., Sophianos, D., and Efthimiadis, A. (1985). Role of the main immunogenic region of acetylcholine receptor in myasthenia gravis. An Fab monoclonal antibody protects against antigenic modulation by human sera. J. Immunol. 134: 2343-2349.
55. Wallace, B. G. (1995). Regulation of the interaction of nicotinic acetylcholine receptors with the cytoskeleton by agrin-activated protein tyrosine kinase. J. Cell Biol. 128: 1121-1129.
56. Wallace, B. G., Qu, Z., and Huganir, R. L. (1991). Agrin induces phosphorylation of the nicotinic acetylcholine receptor. Neuron 6: 869-878.
57. Witzemann, V., Barg, B., Nishikawa, Y., Sakmann, B., and Numa, S. (1987). Differential regulation of muscle acetylcholine receptor γ and ∈-subunit mRNAs. FEBS Lett. 223: 104-112.
58. A Receptors by rapsyn/43-kDa protein in vitro. Mol. Cell. Neurosci. 8: 430-438.