Abstract
Extracellular matrix components are likely to be involved in the interaction of muscle with nonmuscle cells during morphogenesis and in adult skeletal muscle. With the aim of identifying relevant molecules, we generated monoclonal antibodies that react with the endomysium, i.e., the extracellular matrix on the surface of single muscle fibers. Antibody M1, which is described here, specifically labeled the endomysium of chick anterior latissimus dorsi muscle (but neither the perimysium nor, with the exception of blood vessels and perineurium, the epimysium ). Endomysium labeling was restricted to proximal and distal portions of muscle fibers near their insertion points to tendon, but absent from medial regions of the muscle. Myotendinous junctions and tendon fascicles were intensely labeled by M1 antibody. In chick embryos, " myotendinous antigen" (as we tentatively call the epitope recognized by M1 antibody) appeared first in the perichondrium of vertebrae and limb cartilage elements, from where it gradually extended to the premuscle masses. Around day 6, tendon primordia were clearly labeled. The other structures labeled by M1 antibody in chick embryos were developing smooth muscle tissues, especially aorta, gizzard, and lung buds. In general, tissues labeled with M1 antibody appeared to be a subset of the ones accumulating fibronectin. In cell cultures, M1 antibody binds to fuzzy, fibrillar material on the substrate and cell surfaces of living fibroblast and myogenic cells, which confirms an extracellular location of the antigenic site. The appearance of myotendinous antigen during limb morphogenesis and its distribution in adult muscle and tendon are compatible with the idea that it might be involved in attaching muscle fibers to tendon fascicles. Its biochemical characterization is described in the accompanying paper ( Chiquet , M., and D. Fambrough , 1984, J. Cell Biol. 98:1937-1946).
Full Text
The Full Text of this article is available as a PDF (1.5 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Anderson M. J., Fambrough D. M. Aggregates of acetylcholine receptors are associated with plaques of a basal lamina heparan sulfate proteoglycan on the surface of skeletal muscle fibers. J Cell Biol. 1983 Nov;97(5 Pt 1):1396–1411. doi: 10.1083/jcb.97.5.1396. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bailey A. J., Shellswell G. B., Duance V. C. Identification and change of collagen types in differentiating myoblasts and developing chick muscle. Nature. 1979 Mar 1;278(5699):67–69. doi: 10.1038/278067a0. [DOI] [PubMed] [Google Scholar]
- Chiquet M., Eppenberger H. M., Turner D. C. Muscle morphogenesis: Evidence for an organizing function of exogenous fibronectin. Dev Biol. 1981 Dec;88(2):220–235. doi: 10.1016/0012-1606(81)90166-4. [DOI] [PubMed] [Google Scholar]
- Chiquet M., Fambrough D. M. Cellular origin of extracellular matrix components during muscle morphogenesis revealed by monoclonal antibodies. Prog Clin Biol Res. 1982;110(Pt B):359–368. [PubMed] [Google Scholar]
- Chiquet M., Fambrough D. M. Chick myotendinous antigen. II. A novel extracellular glycoprotein complex consisting of large disulfide-linked subunits. J Cell Biol. 1984 Jun;98(6):1937–1946. doi: 10.1083/jcb.98.6.1937. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Christ B., Jacob H. J., Jacob M. Uber den Ursprung der Flügelmuskulatur. Experimentelle Untersuchungen mit Wachtel- und Hühnerembryonen. Experientia. 1974 Dec 15;30(12):1446–1449. doi: 10.1007/BF01919688. [DOI] [PubMed] [Google Scholar]
- Dessau W., Sasse J., Timpl R., Jilek F., von der Mark K. Synthesis and extracellular deposition of fibronectin in chondrocyte cultures. Response to the removal of extracellular cartilage matrix. J Cell Biol. 1978 Nov;79(2 Pt 1):342–355. doi: 10.1083/jcb.79.2.342. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ehrismann R., Chiquet M., Turner D. C. Mode of action of fibronectin in promoting chicken myoblast attachment. Mr = 60,000 gelatin-binding fragment binds native fibronectin. J Biol Chem. 1981 Apr 25;256(8):4056–4062. [PubMed] [Google Scholar]
- GREENWOOD F. C., HUNTER W. M., GLOVER J. S. THE PREPARATION OF I-131-LABELLED HUMAN GROWTH HORMONE OF HIGH SPECIFIC RADIOACTIVITY. Biochem J. 1963 Oct;89:114–123. doi: 10.1042/bj0890114. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gardner J. M., Fambrough D. M. Fibronectin expression during myogenesis. J Cell Biol. 1983 Feb;96(2):474–485. doi: 10.1083/jcb.96.2.474. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Greenlee T. K., Jr, Ross R., Hartman J. L. The fine structure of elastic fibers. J Cell Biol. 1966 Jul;30(1):59–71. doi: 10.1083/jcb.30.1.59. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hynes R. O., Yamada K. M. Fibronectins: multifunctional modular glycoproteins. J Cell Biol. 1982 Nov;95(2 Pt 1):369–377. doi: 10.1083/jcb.95.2.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kennett R. H., Denis K. A., Tung A. S., Klinman N. R. Hybrid plasmacytoma production: fusions with adult spleen cells, monoclonal spleen fragments, neonatal spleen cells and human spleen cells. Curr Top Microbiol Immunol. 1978;81:77–91. doi: 10.1007/978-3-642-67448-8_13. [DOI] [PubMed] [Google Scholar]
- Kieny M., Chevallier A. Autonomy of tendon development in the embryonic chick wing. J Embryol Exp Morphol. 1979 Jan;49:153–165. [PubMed] [Google Scholar]
- Krieg T., Timpl R., Alitalo K., Kurkinen M., Vaheri A. Type III procollagen is the major collageneous component produced by a continuous rhabdomyosarcoma cell line. FEBS Lett. 1979 Aug 15;104(2):405–409. doi: 10.1016/0014-5793(79)80863-7. [DOI] [PubMed] [Google Scholar]
- Köhler G., Shulman M. J. Cellular and molecular restrictions of the lymphocyte fusion. Curr Top Microbiol Immunol. 1978;81:143–148. doi: 10.1007/978-3-642-67448-8_22. [DOI] [PubMed] [Google Scholar]
- Kühl U., Timpl R., von der Mark K. Synthesis of type IV collagen and laminin in cultures of skeletal muscle cells and their assembly on the surface of myotubes. Dev Biol. 1982 Oct;93(2):344–354. doi: 10.1016/0012-1606(82)90122-1. [DOI] [PubMed] [Google Scholar]
- Leung D. Y., Glagov S., Mathews M. B. Cyclic stretching stimulates synthesis of matrix components by arterial smooth muscle cells in vitro. Science. 1976 Feb 6;191(4226):475–477. doi: 10.1126/science.128820. [DOI] [PubMed] [Google Scholar]
- Linder E., Vaheri A., Ruoslahti E., Wartiovaara J. Distribution of fibroblast surface antigen in the developing chick embryo. J Exp Med. 1975 Jul 1;142(1):41–49. doi: 10.1084/jem.142.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Linsenmayer T. F., Fitch J. M., Schmid T. M., Zak N. B., Gibney E., Sanderson R. D., Mayne R. Monoclonal antibodies against chicken type V collagen: production, specificity, and use for immunocytochemical localization in embryonic cornea and other organs. J Cell Biol. 1983 Jan;96(1):124–132. doi: 10.1083/jcb.96.1.124. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McMahan U. J., Sanes J. R., Marshall L. M. Cholinesterase is associated with the basal lamina at the neuromuscular junction. Nature. 1978 Jan 12;271(5641):172–174. doi: 10.1038/271172a0. [DOI] [PubMed] [Google Scholar]
- Rucker R. B., Lefevre I. L., Tom K. Arterial elastin synthesis in the growing chick. Adv Exp Med Biol. 1977;79:461–475. doi: 10.1007/978-1-4684-9093-0_40. [DOI] [PubMed] [Google Scholar]
- Sanes J. R. Laminin, fibronectin, and collagen in synaptic and extrasynaptic portions of muscle fiber basement membrane. J Cell Biol. 1982 May;93(2):442–451. doi: 10.1083/jcb.93.2.442. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shellswell G. B., Bailey A. J., Duance V. C., Restall D. J. Has collagen a role in muscle pattern formation in the developing chick wing? 1. An immunofluorescence study. J Embryol Exp Morphol. 1980 Dec;60:245–254. [PubMed] [Google Scholar]
- Trelstad R. L., Hayashi K. Tendon collagen fibrillogenesis: intracellular subassemblies and cell surface changes associated with fibril growth. Dev Biol. 1979 Aug;71(2):228–242. doi: 10.1016/0012-1606(79)90166-0. [DOI] [PubMed] [Google Scholar]
- Trotter J. A., Corbett K., Avner B. P. Structure and function of the murine muscle-tendon junction. Anat Rec. 1981 Oct;201(2):293–302. doi: 10.1002/ar.1092010209. [DOI] [PubMed] [Google Scholar]
- Turner D. C., Lawton J., Dollenmeier P., Ehrismann R., Chiquet M. Guidance of myogenic cell migration by oriented deposits of fibronectin. Dev Biol. 1983 Feb;95(2):497–504. doi: 10.1016/0012-1606(83)90052-0. [DOI] [PubMed] [Google Scholar]
- Turner D. C., Maier V., Eppenberger H. M. Creatine kinase and aldolase isoenzyme transitions in cultures of chick skeletal muscle cells. Dev Biol. 1974 Mar;37(1):63–89. doi: 10.1016/0012-1606(74)90170-5. [DOI] [PubMed] [Google Scholar]
- Wakshull E., Bayne E. K., Chiquet M., Fambrough D. M. Characterization of a plasma membrane glycoprotein common to myoblasts, skeletal muscle satellite cells, and glia. Dev Biol. 1983 Dec;100(2):464–477. doi: 10.1016/0012-1606(83)90239-7. [DOI] [PubMed] [Google Scholar]
- von der Mark H., von der Mark H. Isolation and characterization of collagen A and B chains from chick embryos. FEBS Lett. 1979 Mar 1;99(1):101–105. doi: 10.1016/0014-5793(79)80258-6. [DOI] [PubMed] [Google Scholar]
- von der Mark K., von der Mark H., Gay S. Study of differential collagen synthesis during development of the chick embryo by immunofluroescence. II. Localization of type I and type II collagen during long bone development. Dev Biol. 1976 Oct 15;53(2):153–170. doi: 10.1016/0012-1606(76)90220-7. [DOI] [PubMed] [Google Scholar]