Abstract
Cultured myotubes form clusters of acetylcholine receptors (AChRs) spontaneously and at sites of nerve-muscle contact. To investigate the cellular mechanisms by which spontaneous clusters are formed, we have made hybrid myotubes between a mouse muscle cell variant, S27, that does not cluster AChRs, and one that does not make AChRs. We have also made hybrid myotubes using S27 and quail muscle cells. In both cases, clusters of AChRs were found near the non-S27 nuclei; in the case of the interspecific hybrids, mouse AChRs were associated with extracellular matrix components contributed by the quail nuclei. Our results suggest that AChRs made by one nucleus can be clustered by localized extracellular matrix produced by a different nucleus and provide an example of nuclear cooperation between the products of different nuclei within multinucleated muscle fibers.
Full text
PDF



Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Anderson M. J., Cohen M. W. Nerve-induced and spontaneous redistribution of acetylcholine receptors on cultured muscle cells. J Physiol. 1977 Jul;268(3):757–773. doi: 10.1113/jphysiol.1977.sp011880. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bayne E. K., Anderson M. J., Fambrough D. M. Extracellular matrix organization in developing muscle: correlation with acetylcholine receptor aggregates. J Cell Biol. 1984 Oct;99(4 Pt 1):1486–1501. doi: 10.1083/jcb.99.4.1486. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Black R., Goldman D., Hochschwender S., Lindstrom J., Hall Z. W. Genetic variants of C2 muscle cells that are defective in synthesis of the alpha-subunit of the acetylcholine receptor. J Cell Biol. 1987 Sep;105(3):1329–1336. doi: 10.1083/jcb.105.3.1329. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chaudhari N., Delay R., Beam K. G. Restoration of normal function in genetically defective myotubes by spontaneous fusion with fibroblasts. Nature. 1989 Oct 5;341(6241):445–447. doi: 10.1038/341445a0. [DOI] [PubMed] [Google Scholar]
- Dowding A. J., Hall Z. W. Monoclonal antibodies specific for each of the two toxin-binding sites of Torpedo acetylcholine receptor. Biochemistry. 1987 Oct 6;26(20):6372–6381. doi: 10.1021/bi00394a010. [DOI] [PubMed] [Google Scholar]
- Fontaine B., Sassoon D., Buckingham M., Changeux J. P. Detection of the nicotinic acetylcholine receptor alpha-subunit mRNA by in situ hybridization at neuromuscular junctions of 15-day-old chick striated muscles. EMBO J. 1988 Mar;7(3):603–609. doi: 10.1002/j.1460-2075.1988.tb02853.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Froehner S. C., Luetje C. W., Scotland P. B., Patrick J. The postsynaptic 43K protein clusters muscle nicotinic acetylcholine receptors in Xenopus oocytes. Neuron. 1990 Oct;5(4):403–410. doi: 10.1016/0896-6273(90)90079-u. [DOI] [PubMed] [Google Scholar]
- Froehner S. C. The submembrane machinery for nicotinic acetylcholine receptor clustering. J Cell Biol. 1991 Jul;114(1):1–7. doi: 10.1083/jcb.114.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goldman D., Staple J. Spatial and temporal expression of acetylcholine receptor RNAs in innervated and denervated rat soleus muscle. Neuron. 1989 Aug;3(2):219–228. doi: 10.1016/0896-6273(89)90035-4. [DOI] [PubMed] [Google Scholar]
- Gordon H., Hall Z. W. Glycosaminoglycan variants in the C2 muscle cell line. Dev Biol. 1989 Sep;135(1):1–11. doi: 10.1016/0012-1606(89)90152-8. [DOI] [PubMed] [Google Scholar]
- Konigsberg I. R. Skeletal myoblasts in culture. Methods Enzymol. 1979;58:511–527. doi: 10.1016/s0076-6879(79)58166-x. [DOI] [PubMed] [Google Scholar]
- Lupa M. T., Gordon H., Hall Z. W. A specific effect of muscle cells on the distribution of presynaptic proteins in neurites and its absence in a C2 muscle cell variant. Dev Biol. 1990 Nov;142(1):31–43. doi: 10.1016/0012-1606(90)90148-c. [DOI] [PubMed] [Google Scholar]
- Merlie J. P., Sanes J. R. Concentration of acetylcholine receptor mRNA in synaptic regions of adult muscle fibres. Nature. 1985 Sep 5;317(6032):66–68. doi: 10.1038/317066a0. [DOI] [PubMed] [Google Scholar]
- Nitkin R. M., Smith M. A., Magill C., Fallon J. R., Yao Y. M., Wallace B. G., McMahan U. J. Identification of agrin, a synaptic organizing protein from Torpedo electric organ. J Cell Biol. 1987 Dec;105(6 Pt 1):2471–2478. doi: 10.1083/jcb.105.6.2471. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Partridge T. A., Morgan J. E., Coulton G. R., Hoffman E. P., Kunkel L. M. Conversion of mdx myofibres from dystrophin-negative to -positive by injection of normal myoblasts. Nature. 1989 Jan 12;337(6203):176–179. doi: 10.1038/337176a0. [DOI] [PubMed] [Google Scholar]
- Pavlath G. K., Blau H. M. Expression of muscle genes in heterokaryons depends on gene dosage. J Cell Biol. 1986 Jan;102(1):124–130. doi: 10.1083/jcb.102.1.124. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pavlath G. K., Rich K., Webster S. G., Blau H. M. Localization of muscle gene products in nuclear domains. Nature. 1989 Feb 9;337(6207):570–573. doi: 10.1038/337570a0. [DOI] [PubMed] [Google Scholar]
- Phillips W. D., Kopta C., Blount P., Gardner P. D., Steinbach J. H., Merlie J. P. ACh receptor-rich membrane domains organized in fibroblasts by recombinant 43-kildalton protein. Science. 1991 Feb 1;251(4993):568–570. doi: 10.1126/science.1703661. [DOI] [PubMed] [Google Scholar]
- Ralston E., Hall Z. W. Intracellular and surface distribution of a membrane protein (CD8) derived from a single nucleus in multinucleated myotubes. J Cell Biol. 1989 Nov;109(5):2345–2352. doi: 10.1083/jcb.109.5.2345. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ralston E., Hall Z. W. Transfer of a protein encoded by a single nucleus to nearby nuclei in multinucleated myotubes. Science. 1989 Jun 2;244(4908):1066–1069. doi: 10.1126/science.2543074. [DOI] [PubMed] [Google Scholar]
- Rotundo R. L. Nucleus-specific translation and assembly of acetylcholinesterase in multinucleated muscle cells. J Cell Biol. 1990 Mar;110(3):715–719. doi: 10.1083/jcb.110.3.715. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ziskind-Conhaim L., Geffen I., Hall Z. W. Redistribution of acetylcholine receptors on developing rat myotubes. J Neurosci. 1984 Sep;4(9):2346–2349. doi: 10.1523/JNEUROSCI.04-09-02346.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]