Myogenesis in the mouse embryo: differential onset of expression of myogenic proteins and the involvement of titin in myofibril assembly

doi:10.1083/jcb.109.2.517

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Myogenesis in the mouse embryo: differential onset of expression of myogenic proteins and the involvement of titin in myofibril assembly

DO Furst, M Osborn and K Weber
Max Planck Institute of Biophysical Chemistry, Goettingen, Federal Republic of Germany.

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.
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Pizon, V., Iakovenko, A., van der Ven, P. F. M., Kelly, R., Fatu, C., Furst, D. O., Karsenti, E., Gautel, M. (2002). Transient association of titin and myosin with microtubules in nascent myofibrils directed by the MURF2 RING-finger protein. J. Cell Sci. 115: 4469-4482 [Abstract] [Full Text]
Boriek, A. M., Capetanaki, Y., Hwang, W., Officer, T., Badshah, M., Rodarte, J., Tidball, J. G. (2001). Desmin integrates the three-dimensional mechanical properties of muscles. Am. J. Physiol. Cell Physiol. 280: C46-C52 [Abstract] [Full Text]
Fougerousse, F., Bullen, P., Herasse, M., Lindsay, S., Richard, I., Wilson, D., Suel, L., Durand, M., Robson, S., Abitbol, M., Beckmann, J. S., Strachan, T. (2000). Human-mouse differences in the embryonic expression patterns of developmental control genes and disease genes. Hum Mol Genet 9: 165-173 [Abstract] [Full Text]
Person, V, Kostin, S, Suzuki, K, Labeit, S, Schaper, J (2000). Antisense oligonucleotide experiments elucidate the essential role of titin in sarcomerogenesis in adult rat cardiomyocytes in long-term culture. J. Cell Sci. 113: 3851-3859 [Abstract]
Georgiades, P, Watkins, M, Surani, M., Ferguson-Smith, A. (2000). Parental origin-specific developmental defects in mice with uniparental disomy for chromosome 12. Development 127: 4719-4728 [Abstract]
Langa, F, Kress, C, Colucci-Guyon, E, Khun, H, Vandormael-Pournin, S, Huerre, M, Babinet, C (2000). Teratocarcinomas induced by embryonic stem (ES) cells lacking vimentin: an approach to study the role of vimentin in tumorigenesis. J. Cell Sci. 113: 3463-3472 [Abstract]
Zhang, Y, Featherstone, D, Davis, W, Rushton, E, Broadie, K (2000). Drosophila D-titin is required for myoblast fusion and skeletal muscle striation. J. Cell Sci. 113: 3103-3115 [Abstract]
Eckes, B, Colucci-Guyon, E, Smola, H, Nodder, S, Babinet, C, Krieg, T, Martin, P (2000). Impaired wound healing in embryonic and adult mice lacking vimentin. J. Cell Sci. 113: 2455-2462 [Abstract]
van der Ven, P., Bartsch, J., Gautel, M, Jockusch, H, Furst, D. (2000). A functional knock-out of titin results in defective myofibril assembly. J. Cell Sci. 113: 1405-1414 [Abstract]
Auerbach, D., Bantle, S., Keller, S., Hinderling, V., Leu, M., Ehler, E., Perriard, J.-C. (1999). Different Domains of the M-Band Protein Myomesin Are Involved in Myosin Binding and M-Band Targeting. Mol. Biol. Cell 10: 1297-1308 [Abstract] [Full Text]
Ojima, K, Lin, Z., Zhang, Z., Hijikata, T, Holtzer, S, Labeit, S, Sweeney, H., Holtzer, H (1999). Initiation and maturation of I-Z-I bodies in the growth tips of transfected myotubes. J. Cell Sci. 112: 4101-4112 [Abstract]
Ehler, E, Rothen, B., Hammerle, S., Komiyama, M, Perriard, J. (1999). Myofibrillogenesis in the developing chicken heart: assembly of Z-disk, M-line and the thick filaments. J. Cell Sci. 112: 1529-1539 [Abstract]
Gregorio, C. C., Trombitas, K., Centner, T., Kolmerer, B., Stier, G., Kunke, K., Suzuki, K., Obermayr, F., Herrmann, B., Granzier, H., Sorimachi, H., Labeit, S. (1998). The NH2 Terminus of Titin Spans the Z-Disc: Its Interaction with a Novel 19-kD Ligand (T-cap) Is Required for Sarcomeric Integrity. JCB 143: 1013-1027 [Abstract] [Full Text]
Obermann, W. M.J., van der Ven, P. F.M., Steiner, F., Weber, K., Fürst, D. O. (1998). Mapping of a Myosin-binding Domain and a Regulatory Phosphorylation Site in M-Protein, a Structural Protein of the Sarcomeric M Band. Mol. Biol. Cell 9: 829-840 [Abstract] [Full Text]
Gao, J., Li, Z., Paulin, D. (1998). A Novel Site, Mt, in the Human Desmin Enhancer Is Necessary for Maximal Expression in Skeletal Muscle. J. Biol. Chem. 273: 6402-6409 [Abstract] [Full Text]
Gautel, M., Furst, D. O., Cocco, A., Schiaffino, S. (1998). Isoform Transitions of the Myosin Binding Protein C Family in Developing Human and Mouse Muscles : Lack of Isoform Transcomplementation in Cardiac Muscle. Circ. Res. 82: 124-129 [Abstract] [Full Text]
Eckes, B, Dogic, D, Colucci-Guyon, E, Wang, N, Maniotis, A, Ingber, D, Merckling, A, Langa, F, Aumailley, M, Delouvee, A, Koteliansky, V, Babinet, C, Krieg, T (1998). Impaired mechanical stability, migration and contractile capacity in vimentin-deficient fibroblasts. J. Cell Sci. 111: 1897-1907 [Abstract]
Li, Z., Mericskay, M., Agbulut, O., Butler-Browne, G., Carlsson, L., Thornell, L.-E., Babinet, C., Paulin, D. (1997). Desmin Is Essential for the Tensile Strength and Integrity of Myofibrils but Not for Myogenic Commitment, Differentiation, and Fusion of Skeletal Muscle. JCB 139: 129-144 [Abstract] [Full Text]
Gautel, M, Goulding, D, Bullard, B, Weber, K, Furst, D. (1996). The central Z-disk region of titin is assembled from a novel repeat in variable copy numbers. J. Cell Sci. 109: 2747-2754 [Abstract]
Castellani, L, Reedy, M, Airey, J., Gallo, R, Ciotti, M., Falcone, G, Alema, S (1996). Remodeling of cytoskeleton and triads following activation of v-Src tyrosine kinase in quail myotubes. J. Cell Sci. 109: 1335-1346 [Abstract]
Mangan, M., Olmsted, J. (1996). A muscle-specific variant of microtubule-associated protein 4 (MAP4) is required in myogenesis. Development 122: 771-781 [Abstract]
Belkin, A. M., Burridge, K. (1994). Expression and localization of the phosphoglucomutase-related cytoskeletal protein, aciculin, in skeletal muscle. J. Cell Sci. 107: 1993-2003 [Abstract]
van der Ven, P., Schaart, G, Croes, H., Jap, P., Ginsel, L., Ramaekers, F. (1993). Titin aggregates associated with intermediate filaments align along stress fiber-like structures during human skeletal muscle cell differentiation. J. Cell Sci. 106: 749-759 [Abstract]
Li, Z, Marchand, P, Humbert, J, Babinet, C, Paulin, D (1993). Desmin sequence elements regulating skeletal muscle-specific expression in transgenic mice. Development 117: 947-959 [Abstract]
McElhinny, A. S., Kakinuma, K., Sorimachi, H., Labeit, S., Gregorio, C. C. (2002). Muscle-specific RING finger-1 interacts with titin to regulate sarcomeric M-line and thick filament structure and may have nuclear functions via its interaction with glucocorticoid modulatory element binding protein-1. JCB 157: 125-136 [Abstract] [Full Text]