Abstract
In the course of studies about the cellular and molecular mechanisms of motor end plate formation, the distribution of the Golgi apparatus (GA) has been investigated by immunofluorescence methods in chick skeletal muscle in primary culture and in innervated muscles of 15-day-old chicks. By using a monoclonal antibody directed against the GA, we confirmed the known distribution of the GA in myogenic cells: a juxtanuclear polarized organization in myoblasts and a perinuclear nonpolarized distribution in myotubes. In contrast, the innervated anterior latissimus dorsi muscle of "young adult" chicks displayed a focal distribution of GA that appeared restricted to areas located underneath the motor end plates identified by alpha-bungarotoxin fluorescent labeling of the acetylcholine receptor. Five days after denervation of anterior latissimus dorsi muscle, a striking reorganization and expansion of the GA was observed. The GA now showed a perinuclear distribution in close association with every nucleus of the muscle fibers as observed in myotubes. The focal distribution of the GA in innervated muscle fibers and its remodeling upon denervation are interpreted in terms of a model of local synthesis, processing, and routing of acetylcholine receptor to the end plate and of regulation of these processes by functional motor innervation.
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- Atsumi S. Localization of surface and internal acetylcholine receptors in developing fast and slow muscles of the chick embryo. Dev Biol. 1981 Aug;86(1):122–135. doi: 10.1016/0012-1606(81)90323-7. [DOI] [PubMed] [Google Scholar]
- Berger E. G., Mandel T., Schilt U. Immunohistochemical localization of galactosyltransferase in human fibroblasts and HeLa cells. J Histochem Cytochem. 1981 Mar;29(3):364–370. doi: 10.1177/29.3.6787115. [DOI] [PubMed] [Google Scholar]
- Betz H., Changeux J. P. Regulation of muscle acetylcholine receptor synthesis in vitro by cyclic nucleotide derivatives. Nature. 1979 Apr 19;278(5706):749–752. doi: 10.1038/278749a0. [DOI] [PubMed] [Google Scholar]
- Brehm P., Henderson L. Regulation of acetylcholine receptor channel function during development of skeletal muscle. Dev Biol. 1988 Sep;129(1):1–11. doi: 10.1016/0012-1606(88)90156-x. [DOI] [PubMed] [Google Scholar]
- Englander L. L., Rubin L. L. Acetylcholine receptor clustering and nuclear movement in muscle fibers in culture. J Cell Biol. 1987 Jan;104(1):87–95. doi: 10.1083/jcb.104.1.87. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fambrough D. M. Control of acetylcholine receptors in skeletal muscle. Physiol Rev. 1979 Jan;59(1):165–227. doi: 10.1152/physrev.1979.59.1.165. [DOI] [PubMed] [Google Scholar]
- Fambrough D. M., Devreotes P. N. Newly synthesized acetylcholine receptors are located in the Golgi apparatus. J Cell Biol. 1978 Jan;76(1):237–244. doi: 10.1083/jcb.76.1.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fontaine B., Changeux J. P. Localization of nicotinic acetylcholine receptor alpha-subunit transcripts during myogenesis and motor endplate development in the chick. J Cell Biol. 1989 Mar;108(3):1025–1037. doi: 10.1083/jcb.108.3.1025. [DOI] [PMC free article] [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]
- Kordeli E., Cartaud J., Nghiêm H. O., Devillers-Thiéry A., Changeux J. P. Asynchronous assembly of the acetylcholine receptor and of the 43-kD nu1 protein in the postsynaptic membrane of developing Torpedo marmorata electrocyte. J Cell Biol. 1989 Jan;108(1):127–139. doi: 10.1083/jcb.108.1.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kronebusch P. J., Singer S. J. The microtubule-organizing complex and the Golgi apparatus are co-localized around the entire nuclear envelope of interphase cardiac myocytes. J Cell Sci. 1987 Aug;88(Pt 1):25–34. doi: 10.1242/jcs.88.1.25. [DOI] [PubMed] [Google Scholar]
- Kupfer A., Louvard D., Singer S. J. Polarization of the Golgi apparatus and the microtubule-organizing center in cultured fibroblasts at the edge of an experimental wound. Proc Natl Acad Sci U S A. 1982 Apr;79(8):2603–2607. doi: 10.1073/pnas.79.8.2603. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Laufer R., Changeux J. P. Activity-dependent regulation of gene expression in muscle and neuronal cells. Mol Neurobiol. 1989 Spring-Summer;3(1-2):1–53. doi: 10.1007/BF02935587. [DOI] [PubMed] [Google Scholar]
- Meiniel R., Bourgeois J. P. Appearance and distribution "in situ" of nicotinic acetylcholine receptors in cervical myotomes of young chick embryos. Radioautographic studies by light and electron microscopy. Anat Embryol (Berl) 1982;164(3):349–368. doi: 10.1007/BF00315757. [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]
- Merlie J. P., Smith M. M. Synthesis and assembly of acetylcholine receptor, a multisubunit membrane glycoprotein. J Membr Biol. 1986;91(1):1–10. doi: 10.1007/BF01870209. [DOI] [PubMed] [Google Scholar]
- Meunier J. C., Sealock R., Olsen R., Changeux J. P. Purification and properties of the cholinergic receptor protein from Electrophorus electricus electric tissue. Eur J Biochem. 1974 Jun 15;45(2):371–394. doi: 10.1111/j.1432-1033.1974.tb03563.x. [DOI] [PubMed] [Google Scholar]
- Miller S. C., Pavlath G. K., Blakely B. T., Blau H. M. Muscle cell components dictate hepatocyte gene expression and the distribution of the Golgi apparatus in heterokaryons. Genes Dev. 1988 Mar;2(3):330–340. doi: 10.1101/gad.2.3.330. [DOI] [PubMed] [Google Scholar]
- Palade G. Intracellular aspects of the process of protein synthesis. Science. 1975 Aug 1;189(4200):347–358. doi: 10.1126/science.1096303. [DOI] [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]
- Pfeffer S. R., Rothman J. E. Biosynthetic protein transport and sorting by the endoplasmic reticulum and Golgi. Annu Rev Biochem. 1987;56:829–852. doi: 10.1146/annurev.bi.56.070187.004145. [DOI] [PubMed] [Google Scholar]
- Roth J., Berger E. G. Immunocytochemical localization of galactosyltransferase in HeLa cells: codistribution with thiamine pyrophosphatase in trans-Golgi cisternae. J Cell Biol. 1982 Apr;93(1):223–229. doi: 10.1083/jcb.93.1.223. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rotundo R. L., Fambrough D. M. Secretion of acetylcholinesterase: relation to acetylcholine receptor metabolism. Cell. 1980 Nov;22(2 Pt 2):595–602. doi: 10.1016/0092-8674(80)90369-4. [DOI] [PubMed] [Google Scholar]
- Salpeter M. M., Loring R. H. Nicotinic acetylcholine receptors in vertebrate muscle: properties, distribution and neural control. Prog Neurobiol. 1985;25(4):297–325. doi: 10.1016/0301-0082(85)90018-8. [DOI] [PubMed] [Google Scholar]
- Shyng S. L., Salpeter M. M. Degradation rate of acetylcholine receptors inserted into denervated vertebrate neuromuscular junctions. J Cell Biol. 1989 Feb;108(2):647–651. doi: 10.1083/jcb.108.2.647. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Singer S. J., Kupfer A. The directed migration of eukaryotic cells. Annu Rev Cell Biol. 1986;2:337–365. doi: 10.1146/annurev.cb.02.110186.002005. [DOI] [PubMed] [Google Scholar]
- Tassin A. M., Maro B., Bornens M. Fate of microtubule-organizing centers during myogenesis in vitro. J Cell Biol. 1985 Jan;100(1):35–46. doi: 10.1083/jcb.100.1.35. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tassin A. M., Paintrand M., Berger E. G., Bornens M. The Golgi apparatus remains associated with microtubule organizing centers during myogenesis. J Cell Biol. 1985 Aug;101(2):630–638. doi: 10.1083/jcb.101.2.630. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vandlen R. L., Wu W. C., Eisenach J. C., Raftery M. A. Studies of the composition of purified Torpedo californica acetylcholine receptor and of its subunits. Biochemistry. 1979 May 15;18(10):1845–1854. doi: 10.1021/bi00577a001. [DOI] [PubMed] [Google Scholar]