Abstract
Antibodies to muscle-specific proteins were used in immunofluorescence to monitor the development of skeletal muscle during mouse embryogenesis. At gestation day (g.d.) 9 a single layer of vimentin filament containing cells in the myotome domain of cervical somites begins to stain positively for myogenic proteins. The muscle-specific proteins are expressed in a specific order between g.d. 9 and 9.5. Desmin is detected first, then titin, then the muscle specific actin and myosin heavy chains, and finally nebulin. At g.d. 9.5 fibrous desmin structures are already present, while for the other myogenic proteins no structure can be detected. Some prefusion myoblasts display at g.d. 11 and 12 tiny and immature myofibrils. These reveal a periodic pattern of myosin, nebulin, and those titin epitopes known to occur at and close to the Z line. In contrast titin epitopes, which are present in mature myofibrils along the A band and at the A-I junction, are still randomly distributed. We propose, that the Z line connected structures and the A bands (myosin filaments) assemble independently, and that the known interaction of the I-Z-I brushes with the A bands occurs at a later developmental stage. After fusion of myoblasts to myotubes at g.d. 13 and 14 all titin epitopes show the myofibrillar banding pattern. The predominantly longitudinal orientation of desmin filaments seen in myoblasts and in early myotubes is transformed at g.d. 17 and 18 to distinct Z line connected striations. Vimentin, still present together with desmin in the myoblasts, is lost from the myotubes. Our results indicate that the putative elastic titin filaments act as integrators during skeletal muscle development. Some developmental aspects of eye and limb muscles are also described.
Full Text
The Full Text of this article is available as a PDF (5.8 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- ALLEN E. R., PEPE F. A. ULTRASTRUCTURE OF DEVELOPING MUSCLE CELLS IN THE CHICK EMBRYO. Am J Anat. 1965 Jan;116:115–147. doi: 10.1002/aja.1001160107. [DOI] [PubMed] [Google Scholar]
- Antin P. B., Forry-Schaudies S., Friedman T. M., Tapscott S. J., Holtzer H. Taxol induces postmitotic myoblasts to assemble interdigitating microtubule-myosin arrays that exclude actin filaments. J Cell Biol. 1981 Aug;90(2):300–308. doi: 10.1083/jcb.90.2.300. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bennett G. S., Fellini S. A., Toyama Y., Holtzer H. Redistribution of intermediate filament subunits during skeletal myogenesis and maturation in vitro. J Cell Biol. 1979 Aug;82(2):577–584. doi: 10.1083/jcb.82.2.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bignami A., Dahl D. Early appearance of desmin, the muscle-type intermediate filament protein, in the rat embryo. J Histochem Cytochem. 1984 May;32(5):473–476. doi: 10.1177/32.5.6371130. [DOI] [PubMed] [Google Scholar]
- Brûlet P., Babinet C., Kemler R., Jacob F. Monoclonal antibodies against trophectoderm-specific markers during mouse blastocyst formation. Proc Natl Acad Sci U S A. 1980 Jul;77(7):4113–4117. doi: 10.1073/pnas.77.7.4113. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bähler M., Moser H., Eppenberger H. M., Wallimann T. Heart C-protein is transiently expressed during skeletal muscle development in the embryo, but persists in cultured myogenic cells. Dev Biol. 1985 Dec;112(2):345–352. doi: 10.1016/0012-1606(85)90405-1. [DOI] [PubMed] [Google Scholar]
- Chacko K. J. Observations on the ultrastructure of developing myocardium of rat embryos. J Morphol. 1976 Nov;150(3):681–709. doi: 10.1002/jmor.1051500305. [DOI] [PubMed] [Google Scholar]
- Debus E., Weber K., Osborn M. Monoclonal antibodies to desmin, the muscle-specific intermediate filament protein. EMBO J. 1983;2(12):2305–2312. doi: 10.1002/j.1460-2075.1983.tb01738.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dlugosz A. A., Antin P. B., Nachmias V. T., Holtzer H. The relationship between stress fiber-like structures and nascent myofibrils in cultured cardiac myocytes. J Cell Biol. 1984 Dec;99(6):2268–2278. doi: 10.1083/jcb.99.6.2268. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fürst D. O., Osborn M., Nave R., Weber K. The organization of titin filaments in the half-sarcomere revealed by monoclonal antibodies in immunoelectron microscopy: a map of ten nonrepetitive epitopes starting at the Z line extends close to the M line. J Cell Biol. 1988 May;106(5):1563–1572. doi: 10.1083/jcb.106.5.1563. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gard D. L., Lazarides E. The synthesis and distribution of desmin and vimentin during myogenesis in vitro. Cell. 1980 Jan;19(1):263–275. doi: 10.1016/0092-8674(80)90408-0. [DOI] [PubMed] [Google Scholar]
- Granger B. L., Lazarides E. Desmin and vimentin coexist at the periphery of the myofibril Z disc. Cell. 1979 Dec;18(4):1053–1063. doi: 10.1016/0092-8674(79)90218-6. [DOI] [PubMed] [Google Scholar]
- Grove B. K., Cerny L., Perriard J. C., Eppenberger H. M. Myomesin and M-protein: expression of two M-band proteins in pectoral muscle and heart during development. J Cell Biol. 1985 Oct;101(4):1413–1421. doi: 10.1083/jcb.101.4.1413. [DOI] [PMC free article] [PubMed] [Google Scholar]
- HOLTZER H., MARSHALL J. M., Jr, FINCK H. An analysis of myogenesis by the use of fluorescent antimyosin. J Biophys Biochem Cytol. 1957 Sep 25;3(5):705–724. doi: 10.1083/jcb.3.5.705. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hill C. S., Duran S., Lin Z. X., Weber K., Holtzer H. Titin and myosin, but not desmin, are linked during myofibrillogenesis in postmitotic mononucleated myoblasts. J Cell Biol. 1986 Dec;103(6 Pt 1):2185–2196. doi: 10.1083/jcb.103.6.2185. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hill C., Weber K. Monoclonal antibodies distinguish titins from heart and skeletal muscle. J Cell Biol. 1986 Mar;102(3):1099–1108. doi: 10.1083/jcb.102.3.1099. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hiruma T., Hirakow R. An ultrastructural topographical study on myofibrillogenesis in the heart of the chick embryo during pulsation onset period. Anat Embryol (Berl) 1985;172(3):325–329. doi: 10.1007/BF00318980. [DOI] [PubMed] [Google Scholar]
- Kelly A. M., Zacks S. I. The histogenesis of rat intercostal muscle. J Cell Biol. 1969 Jul;42(1):135–153. doi: 10.1083/jcb.42.1.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kuruc N., Franke W. W. Transient coexpression of desmin and cytokeratins 8 and 18 in developing myocardial cells of some vertebrate species. Differentiation. 1988 Sep;38(3):177–193. doi: 10.1111/j.1432-0436.1988.tb00212.x. [DOI] [PubMed] [Google Scholar]
- Manasek F. J. Embryonic development of the heart. I. A light and electron microscopic study of myocardial development in the early chick embryo. J Morphol. 1968 Jul;125(3):329–365. doi: 10.1002/jmor.1051250306. [DOI] [PubMed] [Google Scholar]
- Markwald R. R. Distribution and relationship of precursor Z material to organizing myofibrillar bundles in embryonic rat and hamster ventricular myocytes. J Mol Cell Cardiol. 1973 Aug;5(4):341–350. doi: 10.1016/0022-2828(73)90026-6. [DOI] [PubMed] [Google Scholar]
- Maruyama K. Connectin, an elastic filamentous protein of striated muscle. Int Rev Cytol. 1986;104:81–114. doi: 10.1016/s0074-7696(08)61924-5. [DOI] [PubMed] [Google Scholar]
- McLennan I. S. Differentiation of muscle fiber types in the chicken hindlimb. Dev Biol. 1983 May;97(1):222–228. doi: 10.1016/0012-1606(83)90079-9. [DOI] [PubMed] [Google Scholar]
- Miller J. B., Crow M. T., Stockdale F. E. Slow and fast myosin heavy chain content defines three types of myotubes in early muscle cell cultures. J Cell Biol. 1985 Nov;101(5 Pt 1):1643–1650. doi: 10.1083/jcb.101.5.1643. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Obinata T., Reinach F. C., Bader D. M., Masaki T., Kitani S., Fischman D. A. Immunochemical analysis of C-protein isoform transitions during the development of chicken skeletal muscle. Dev Biol. 1984 Jan;101(1):116–124. doi: 10.1016/0012-1606(84)90122-2. [DOI] [PubMed] [Google Scholar]
- Osborn M., Franke W., Weber K. Direct demonstration of the presence of two immunologically distinct intermediate-sized filament systems in the same cell by double immunofluorescence microscopy. Vimentin and cytokeratin fibers in cultured epithelial cells. Exp Cell Res. 1980 Jan;125(1):37–46. doi: 10.1016/0014-4827(80)90186-x. [DOI] [PubMed] [Google Scholar]
- Osborn M., Geisler N., Shaw G., Sharp G., Weber K. Intermediate filaments. Cold Spring Harb Symp Quant Biol. 1982;46(Pt 1):413–429. doi: 10.1101/sqb.1982.046.01.040. [DOI] [PubMed] [Google Scholar]
- Peng H. B., Wolosewick J. J., Cheng P. C. The development of myofibrils in cultured muscle cells: a whole-mount and thin-section electron microscopic study. Dev Biol. 1981 Nov;88(1):121–136. doi: 10.1016/0012-1606(81)90224-4. [DOI] [PubMed] [Google Scholar]
- Tokuyasu K. T., Maher P. A. Immunocytochemical studies of cardiac myofibrillogenesis in early chick embryos. I. Presence of immunofluorescent titin spots in premyofibril stages. J Cell Biol. 1987 Dec;105(6 Pt 1):2781–2793. doi: 10.1083/jcb.105.6.2781. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tokuyasu K. T., Maher P. A. Immunocytochemical studies of cardiac myofibrillogenesis in early chick embryos. II. Generation of alpha-actinin dots within titin spots at the time of the first myofibril formation. J Cell Biol. 1987 Dec;105(6 Pt 1):2795–2801. doi: 10.1083/jcb.105.6.2795. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tokuyasu K. T., Maher P. A., Singer S. J. Distributions of vimentin and desmin in developing chick myotubes in vivo. I. Immunofluorescence study. J Cell Biol. 1984 Jun;98(6):1961–1972. doi: 10.1083/jcb.98.6.1961. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Toyama Y., Forry-Schaudies S., Hoffman B., Holtzer H. Effects of taxol and Colcemid on myofibrillogenesis. Proc Natl Acad Sci U S A. 1982 Nov;79(21):6556–6560. doi: 10.1073/pnas.79.21.6556. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Van Muijen G. N., Ruiter D. J., Warnaar S. O. Coexpression of intermediate filament polypeptides in human fetal and adult tissues. Lab Invest. 1987 Oct;57(4):359–369. [PubMed] [Google Scholar]
- Wang K. Sarcomere-associated cytoskeletal lattices in striated muscle. Review and hypothesis. Cell Muscle Motil. 1985;6:315–369. doi: 10.1007/978-1-4757-4723-2_10. [DOI] [PubMed] [Google Scholar]
- Wang S. M., Greaser M. L., Schultz E., Bulinski J. C., Lin J. J., Lessard J. L. Studies on cardiac myofibrillogenesis with antibodies to titin, actin, tropomyosin, and myosin. J Cell Biol. 1988 Sep;107(3):1075–1083. doi: 10.1083/jcb.107.3.1075. [DOI] [PMC free article] [PubMed] [Google Scholar]