Abstract
To examine how nascent myosin heavy chains associate with the cytoskeletons of developing muscle cells, we used pulse labeling, cell fractionation, and immunoprecipitation. More than 80% of nascent myosin heavy chains associate with the cytoskeleton. More than one-third of these nascent chains are not released by puromycin and/or RNase. The fraction of nascent heavy chains that resists release increases during development of muscle cells in culture. Treatment with cytochalasin D but not nocodazole decreases myosin heavy chain cotranslational assembly. These results indicate that (i) cotranslational assembly of myosin heavy chains is developmentally regulated, (ii) structures containing actin and not microtubules may mediate initial association of the heavy chains with the cytoskeleton, and (iii) the site of translation dictates where a significant fraction of the heavy chains will be inserted into the cytoskeleton.
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- Adams A., Fey E. G., Pike S. F., Taylorson C. J., White H. A., Rabin B. R. Preparation and properties of a complex from rat liver of polyribosomes with components of the cytoskeleton. Biochem J. 1983 Oct 15;216(1):215–226. doi: 10.1042/bj2160215. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bader D., Masaki T., Fischman D. A. Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro. J Cell Biol. 1982 Dec;95(3):763–770. doi: 10.1083/jcb.95.3.763. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Blobel G., Sabatini D. Dissociation of mammalian polyribosomes into subunits by puromycin. Proc Natl Acad Sci U S A. 1971 Feb;68(2):390–394. doi: 10.1073/pnas.68.2.390. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fey E. G., Wan K. M., Penman S. Epithelial cytoskeletal framework and nuclear matrix-intermediate filament scaffold: three-dimensional organization and protein composition. J Cell Biol. 1984 Jun;98(6):1973–1984. doi: 10.1083/jcb.98.6.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fulton A. B. Assembly associated with the cytomatrix. J Cell Biol. 1984 Jul;99(1 Pt 2):209s–211s. doi: 10.1083/jcb.99.1.209s. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fulton A. B., Wan K. M. Many cytoskeletal proteins associate with the hela cytoskeleton during translation in vitro. Cell. 1983 Feb;32(2):619–625. doi: 10.1016/0092-8674(83)90481-6. [DOI] [PubMed] [Google Scholar]
- Fulton A. B., Wan K. M., Penman S. The spatial distribution of polyribosomes in 3T3 cells and the associated assembly of proteins into the skeletal framework. Cell. 1980 Jul;20(3):849–857. doi: 10.1016/0092-8674(80)90331-1. [DOI] [PubMed] [Google Scholar]
- Gilbert M., Fulton A. B. The specificity and stability of the triton-extracted cytoskeletal framework of gerbil fibroma cells. J Cell Sci. 1985 Feb;73:335–345. doi: 10.1242/jcs.73.1.335. [DOI] [PubMed] [Google Scholar]
- Goldman B. M., Blobel G. Biogenesis of peroxisomes: intracellular site of synthesis of catalase and uricase. Proc Natl Acad Sci U S A. 1978 Oct;75(10):5066–5070. doi: 10.1073/pnas.75.10.5066. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Henderson D., Weber K. Immunoelectron microscopic studies of intermediate filaments in cultured cells. Exp Cell Res. 1980 Oct;129(2):441–453. doi: 10.1016/0014-4827(80)90513-3. [DOI] [PubMed] [Google Scholar]
- Joshi H. C., Chu D., Buxbaum R. E., Heidemann S. R. Tension and compression in the cytoskeleton of PC 12 neurites. J Cell Biol. 1985 Sep;101(3):697–705. doi: 10.1083/jcb.101.3.697. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Konieczny S. F., McKay J., Coleman J. R. Isolation and characterization of terminally differentiated chicken and rat skeletal muscle myoblasts. Dev Biol. 1982 May;91(1):11–26. doi: 10.1016/0012-1606(82)90003-3. [DOI] [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Lawrence J. B., Singer R. H. Intracellular localization of messenger RNAs for cytoskeletal proteins. Cell. 1986 May 9;45(3):407–415. doi: 10.1016/0092-8674(86)90326-0. [DOI] [PubMed] [Google Scholar]
- Lazarides E., Moon R. T. Assembly and topogenesis of the spectrin-based membrane skeleton in erythroid development. Cell. 1984 Jun;37(2):354–356. doi: 10.1016/0092-8674(84)90364-7. [DOI] [PubMed] [Google Scholar]
- Lenk R., Ransom L., Kaufmann Y., Penman S. A cytoskeletal structure with associated polyribosomes obtained from HeLa cells. Cell. 1977 Jan;10(1):67–78. doi: 10.1016/0092-8674(77)90141-6. [DOI] [PubMed] [Google Scholar]
- Lodish H. F., Jacobsen M. Regulation of hemoglobin synthesis. Equal rates of translation and termination of - and -globin chains. J Biol Chem. 1972 Jun 10;247(11):3622–3629. [PubMed] [Google Scholar]
- Low R. B., Woodcock-Mitchell J., Mitchell J. J., Arnold J., Absher P. M. Synthesis of cytoskeletal and contractile proteins by cultured IMR-90 fibroblasts. J Cell Biol. 1985 Aug;101(2):500–505. doi: 10.1083/jcb.101.2.500. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saad A. D., Pardee J. D., Fischman D. A. Dynamic exchange of myosin molecules between thick filaments. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9483–9487. doi: 10.1073/pnas.83.24.9483. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Staufenbiel M., Lazarides E. Assembly of protein 4.1 during chicken erythroid differentiation. J Cell Biol. 1986 Apr;102(4):1157–1163. doi: 10.1083/jcb.102.4.1157. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Strome S., Wood W. B. Generation of asymmetry and segregation of germ-line granules in early C. elegans embryos. Cell. 1983 Nov;35(1):15–25. doi: 10.1016/0092-8674(83)90203-9. [DOI] [PubMed] [Google Scholar]
- Tomasek J. J., Hay E. D. Analysis of the role of microfilaments and microtubules in acquisition of bipolarity and elongation of fibroblasts in hydrated collagen gels. J Cell Biol. 1984 Aug;99(2):536–549. doi: 10.1083/jcb.99.2.536. [DOI] [PMC free article] [PubMed] [Google Scholar]
- van Venrooij W. J., Sillekens P. T., van Eekelen C. A., Reinders R. J. On the association of mRNA with the cytoskeleton in uninfected and adenovirus-infected human KB cells. Exp Cell Res. 1981 Sep;135(1):79–91. doi: 10.1016/0014-4827(81)90301-3. [DOI] [PubMed] [Google Scholar]