Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1986 Dec 1;103(6):2197–2208. doi: 10.1083/jcb.103.6.2197

Developmental regulation of the multiple myogenic cell lineages of the avian embryo

PMCID: PMC2114613  PMID: 3782296

Abstract

The developmental regulation of myoblasts committed to fast, mixed fast/slow, and slow myogenic cell lineages was determined by analyzing myotube formation in high density and clonal cultures of myoblasts isolated from chicken and quail embryos of different ages. To identify cells of different myogenic lineages, myotubes were analyzed for content of fast and slow classes of myosin heavy chain (MHC) isoforms by immunocytochemistry and immunoblotting using specific monoclonal antibodies. Myoblasts from the hindlimb bud, forelimb bud, trunk, and pectoral regions of the early chicken embryo and hindlimb bud of the early quail embryo (days 3-6 in ovo) were committed to three distinct lineages with 60-90% of the myoblasts in the fast lineage, 10-40% in the mixed fast/slow lineage, and 0-3% in the slow lineage depending on the age and species of the myoblast donor. In contrast, 99-100% of the myoblasts in the later embryos (days 9-12 in ovo) were in the fast lineage. Serial subculturing from a single myoblast demonstrated that commitment to a particular lineage was stably inherited for over 30 cell doublings. When myoblasts from embryos of the same age were cultured, the percentage of muscle colonies of the fast, fast/slow, and slow types that formed in clonal cultures was the same as the percentage of myotubes of each of these types that formed in high density cultures, indicating that intercellular contact between myoblasts of different lineages did not affect the type of myotube formed. An analysis in vivo showed that three types of primary myotubes- -fast, fast/slow, and slow--were also found in the chicken thigh at day 7 in ovo and that synthesis of both the fast and slow classes of MHC isoforms was concomitant with the formation of primary myotubes. On the basis of these results, we propose that in the avian embryo, there is an early phase of muscle fiber formation in which primary myotubes with differing MHC contents are formed from myoblasts committed to three intrinsically different primary myogenic lineages independent of innervation and a later phase in which secondary myotubes are formed from myoblasts in a single, secondary myogenic lineage with maturation and maintenance of fiber diversity dependent on innervation.

Full Text

The Full Text of this article is available as a PDF (3.0 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. 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]
  2. Bandman E., Matsuda R., Strohman R. C. Developmental appearance of myosin heavy and light chain isoforms in vivo and in vitro in chicken skeletal muscle. Dev Biol. 1982 Oct;93(2):508–518. doi: 10.1016/0012-1606(82)90138-5. [DOI] [PubMed] [Google Scholar]
  3. Bennett M. R., Davey D. F., Uebel K. E. The growth of segmental nerves from the brachial myotomes into the proximal muscles of the chick forelimb during development. J Comp Neurol. 1980 Jan 15;189(2):335–357. doi: 10.1002/cne.901890209. [DOI] [PubMed] [Google Scholar]
  4. Bennett M. R. Development of neuromuscular synapses. Physiol Rev. 1983 Jul;63(3):915–1048. doi: 10.1152/physrev.1983.63.3.915. [DOI] [PubMed] [Google Scholar]
  5. Bonner P. H., Hauschka S. D. Clonal analysis of vertebrate myogenesis. I. Early developmental events in the chick limb. Dev Biol. 1974 Apr;37(2):317–328. doi: 10.1016/0012-1606(74)90152-3. [DOI] [PubMed] [Google Scholar]
  6. Buckley P. A., Konigsberg I. R. Myogenic fusion and the duration of the post-mitotic gap (G1). Dev Biol. 1974 Mar;37(1):193–212. doi: 10.1016/0012-1606(74)90179-1. [DOI] [PubMed] [Google Scholar]
  7. Buckley P. A., Konigsberg I. R. The avoidance of stimulatory artifacts in cell cycle determinations in vitro. Dev Biol. 1974 Mar;37(1):186–192. doi: 10.1016/0012-1606(74)90178-x. [DOI] [PubMed] [Google Scholar]
  8. Burnette W. N. "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate--polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal Biochem. 1981 Apr;112(2):195–203. doi: 10.1016/0003-2697(81)90281-5. [DOI] [PubMed] [Google Scholar]
  9. Butler J., Cosmos E., Brierley J. Differentiation of muscle fiber types in aneurogenic brachial muscles of the chick embryo. J Exp Zool. 1982 Nov 20;224(1):65–80. doi: 10.1002/jez.1402240108. [DOI] [PubMed] [Google Scholar]
  10. Bárány M. ATPase activity of myosin correlated with speed of muscle shortening. J Gen Physiol. 1967 Jul;50(6 Suppl):197–218. doi: 10.1085/jgp.50.6.197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Crow M. T., Olson P. S., Stockdale F. E. Myosin light-chain expression during avian muscle development. J Cell Biol. 1983 Mar;96(3):736–744. doi: 10.1083/jcb.96.3.736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Crow M. T., Stockdale F. E. Myosin expression and specialization among the earliest muscle fibers of the developing avian limb. Dev Biol. 1986 Jan;113(1):238–254. doi: 10.1016/0012-1606(86)90126-0. [DOI] [PubMed] [Google Scholar]
  13. Dennis M. J. Development of the neuromuscular junction: inductive interactions between cells. Annu Rev Neurosci. 1981;4:43–68. doi: 10.1146/annurev.ne.04.030181.000355. [DOI] [PubMed] [Google Scholar]
  14. Gauthier G. F., Lowey S., Benfield P. A., Hobbs A. W. Distribution and properties of myosin isozymes in developing avian and mammalian skeletal muscle fibers. J Cell Biol. 1982 Feb;92(2):471–484. doi: 10.1083/jcb.92.2.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jolesz F., Sreter F. A. Development, innervation, and activity-pattern induced changes in skeletal muscle. Annu Rev Physiol. 1981;43:531–552. doi: 10.1146/annurev.ph.43.030181.002531. [DOI] [PubMed] [Google Scholar]
  16. Keller L. R., Emerson C. P., Jr Synthesis of adult myosin light chains by embryonic muscle cultures. Proc Natl Acad Sci U S A. 1980 Feb;77(2):1020–1024. doi: 10.1073/pnas.77.2.1020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Konieczny S. F., Emerson C. P., Jr 5-Azacytidine induction of stable mesodermal stem cell lineages from 10T1/2 cells: evidence for regulatory genes controlling determination. Cell. 1984 Oct;38(3):791–800. doi: 10.1016/0092-8674(84)90274-5. [DOI] [PubMed] [Google Scholar]
  18. Konigsberg I. R. Skeletal myoblasts in culture. Methods Enzymol. 1979;58:511–527. doi: 10.1016/s0076-6879(79)58166-x. [DOI] [PubMed] [Google Scholar]
  19. Laing N. G., Lamb A. H. Development and motor innervation of a distal pair of fast and slow wing muscles in the chick embryo. J Embryol Exp Morphol. 1983 Dec;78:53–66. [PubMed] [Google Scholar]
  20. Marston S. B., Taylor E. W. Comparison of the myosin and actomyosin ATPase mechanisms of the four types of vertebrate muscles. J Mol Biol. 1980 Jun 5;139(4):573–600. doi: 10.1016/0022-2836(80)90050-9. [DOI] [PubMed] [Google Scholar]
  21. Matsuda R., Bandman E., Strohman R. C. The two myosin isoenzymes of chicken anterior latissimus dorsi muscle contain different myosin heavy chains encoded by separate mRNAs. Differentiation. 1982;23(1):36–42. doi: 10.1111/j.1432-0436.1982.tb01265.x. [DOI] [PubMed] [Google Scholar]
  22. Matsuda R., Obinata T., Shimada Y. Types of troponin components during development of chicken skeletal muscle. Dev Biol. 1981 Feb;82(1):11–19. doi: 10.1016/0012-1606(81)90424-3. [DOI] [PubMed] [Google Scholar]
  23. Matsuda R., Spector D., Strohman R. C. Denervated skeletal muscle displays discoordinate regulation for the synthesis of several myofibrillar proteins. Proc Natl Acad Sci U S A. 1984 Feb;81(4):1122–1125. doi: 10.1073/pnas.81.4.1122. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. McLennan I. S. Neural dependence and independence of myotube production in chicken hindlimb muscles. Dev Biol. 1983 Aug;98(2):287–294. doi: 10.1016/0012-1606(83)90359-7. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Miller J. B., Stockdale F. E. Developmental origins of skeletal muscle fibers: clonal analysis of myogenic cell lineages based on expression of fast and slow myosin heavy chains. Proc Natl Acad Sci U S A. 1986 Jun;83(11):3860–3864. doi: 10.1073/pnas.83.11.3860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Montarras D., Fiszman M. Y. A new muscle phenotype is expressed by subcultured quail myoblasts isolated from future fast and slow muscles. J Biol Chem. 1983 Mar 25;258(6):3883–3888. [PubMed] [Google Scholar]
  29. Montarras D., Fiszman M. Y., Gros F. Changes in tropomyosin during development of chick embryonic skeletal muscles in vivo and during differentiation of chick muscle cells in vitro. J Biol Chem. 1982 Jan 10;257(1):545–548. [PubMed] [Google Scholar]
  30. O'Neill M. C., Stockdale F. E. A kinetic analysis of myogenesis in vitro. J Cell Biol. 1972 Jan;52(1):52–65. doi: 10.1083/jcb.52.1.52. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Obinata T., Masaki T., Takano H. Types of myosin light chains present during the development of fast skeletal muscle in chick embryo. J Biochem. 1980 Jan;87(1):81–88. doi: 10.1093/oxfordjournals.jbchem.a132755. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Phillips W. D., Bennett M. R. Differentiation of fiber types in wing muscles during embryonic development: effect of neural tube removal. Dev Biol. 1984 Dec;106(2):457–468. doi: 10.1016/0012-1606(84)90245-8. [DOI] [PubMed] [Google Scholar]
  34. Reiser P. J., Moss R. L., Giulian G. G., Greaser M. L. Shortening velocity and myosin heavy chains of developing rabbit muscle fibers. J Biol Chem. 1985 Nov 25;260(27):14403–14405. [PubMed] [Google Scholar]
  35. Roy R. K., Sreter F. A., Sarkar S. Changes in tropomyosin subunits and myosin light chains during development of chicken and rabbit striated muscles. Dev Biol. 1979 Mar;69(1):15–30. doi: 10.1016/0012-1606(79)90271-9. [DOI] [PubMed] [Google Scholar]
  36. Rubinstein N. A., Kelly A. M. Development of muscle fiber specialization in the rat hindlimb. J Cell Biol. 1981 Jul;90(1):128–144. doi: 10.1083/jcb.90.1.128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Rushbrook J. I., Stracher A. Comparison of adult, embryonic, and dystrophic myosin heavy chains from chicken muscle by sodium dodecyl sulfate/polyacrylamide gel electrophoresis and peptide mapping. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4331–4334. doi: 10.1073/pnas.76.9.4331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Rutz R., Hauschka S. Clonal analysis of vertebrate myogenesis. VII. Heritability of muscle colony type through sequential subclonal passages in vitro. Dev Biol. 1982 May;91(1):103–110. doi: 10.1016/0012-1606(82)90013-6. [DOI] [PubMed] [Google Scholar]
  39. Seed J., Hauschka S. D. Temporal separation of the migration of distinct myogenic precursor populations into the developing chick wing bud. Dev Biol. 1984 Dec;106(2):389–393. doi: 10.1016/0012-1606(84)90237-9. [DOI] [PubMed] [Google Scholar]
  40. Sréter F. A., Bálint M., Gergely J. Structural and functional changes of myosin during development: comparison with adult fast, slow and cardiac myosin. Dev Biol. 1975 Oct;46(2):317–325. doi: 10.1016/0012-1606(75)90108-6. [DOI] [PubMed] [Google Scholar]
  41. Stockdale F. E., Baden H., Raman N. Slow muscle myoblasts differentiating in vitro synthesize both slow and fast myosin light chains. Dev Biol. 1981 Feb;82(1):168–171. doi: 10.1016/0012-1606(81)90438-3. [DOI] [PubMed] [Google Scholar]
  42. Stockdale F. E., Raman N., Baden H. Myosin light chains and the developmental origin of fast muscle. Proc Natl Acad Sci U S A. 1981 Feb;78(2):931–935. doi: 10.1073/pnas.78.2.931. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Umeda P. K., Sinha A. M., Jakovcic S., Merten S., Hsu H. J., Subramanian K. N., Zak R., Rabinowitz M. Molecular cloning of two fast myosin heavy chain cDNAs from chicken embryo skeletal muscle. Proc Natl Acad Sci U S A. 1981 May;78(5):2843–2847. doi: 10.1073/pnas.78.5.2843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Wagner P. D., Giniger E. Hydrolysis of ATP and reversible binding to F-actin by myosin heavy chains free of all light chains. Nature. 1981 Aug 6;292(5823):560–562. doi: 10.1038/292560a0. [DOI] [PubMed] [Google Scholar]
  45. White N. K., Bonner P. H., Nelson D. R., Hauschka S. D. Clonal analysis of vertebrate myogenesis. IV. Medium-dependent classification of colony-forming cells. Dev Biol. 1975 Jun;44(2):346–361. doi: 10.1016/0012-1606(75)90405-4. [DOI] [PubMed] [Google Scholar]
  46. White N. K., Hauschka S. D. Muscle development in vitro. A new conditioned medium effect on colony differentiation. Exp Cell Res. 1971 Aug;67(2):479–482. doi: 10.1016/0014-4827(71)90437-x. [DOI] [PubMed] [Google Scholar]
  47. Womble M. D., Bonner P. H. Developmental fate of a distinct class of chick myoblasts after transplantation of cloned cells into quail embryos. J Embryol Exp Morphol. 1980 Aug;58:119–130. [PubMed] [Google Scholar]
  48. ZACCHEI A. M. [The embryonal development of the Japanese quail (Coturnix coturnix japonica T. and S.)]. Arch Ital Anat Embriol. 1961;66:36–62. [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES