Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1981 Jul 1;90(1):128–144. doi: 10.1083/jcb.90.1.128

Development of muscle fiber specialization in the rat hindlimb

PMCID: PMC2111831  PMID: 7251670

Abstract

The appearance of fast and slow fiber types in the distal hindlimb of the rat was investigated using affinity-purified antibodies specific to adult fast and slow myosins, two-dimensional electrophoresis of myosin light chains, and electron microscope examination of developing muscle cells. As others have noted, muscle histogenesis is not synchronous; rather, a series of muscle fiber generations occurs, each generation forming along the walls of the previous generation. At the onset of myotube formation on the 15th d of gestation, the antimyosin antibodies do not distinguish among fibers. All fibers react strongly with antibody to fast myosin but not with antibody to slow myosin. The initiation of fiber type differentiation can be detected in the 17-d fetus by a gradual increase in the binding of antibody to slow myosin in the primary, but not the secondary, generation myotubes. Moreover, neuromuscular contacts at this crucial time are infrequent, primitive, and restricted predominantly, but not exclusively, to the primary generation cells, the same cells which begin to bind large amounts of antislow myosin at this time. With maturation, the primary generation cells decrease their binding of antifast myosin and become type I fibers. Secondary generation cells are initially all primitive type II fibers. In future fast muscles the secondary generation cells remain type II, while in future slow muscles most of the secondary generation cells eventually change to type I over a prolonged postnatal period. We conclude that the temporal sequence of muscle development is fundamentally important in determining the genetic expression of individual muscle cells.

Full Text

The Full Text of this article is available as a PDF (2.6 MB).

Selected References

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

  1. Adelstein R. S., Conti M. A., Johnson G. S., Pastan I., Pollard T. D. Isolation and characterization of myosin from cloned mouse fibroblasts. Proc Natl Acad Sci U S A. 1972 Dec;69(12):3693–3697. doi: 10.1073/pnas.69.12.3693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arndt I., Pepe F. A. Antigenic specificity of red and white muscle myosin. J Histochem Cytochem. 1975 Mar;23(3):159–168. doi: 10.1177/23.3.47867. [DOI] [PubMed] [Google Scholar]
  3. Ashmore C. R., Robinson D. W., Rattray P., Doerr L. Biphasic development of muscle fibers in the fetal lamb. Exp Neurol. 1972 Nov;37(2):241–255. doi: 10.1016/0014-4886(72)90071-4. [DOI] [PubMed] [Google Scholar]
  4. BULLER A. J., ECCLES J. C., ECCLES R. M. Differentiation of fast and slow muscles in the cat hind limb. J Physiol. 1960 Feb;150:399–416. doi: 10.1113/jphysiol.1960.sp006394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bagust J., Lewis D. M., Westerman R. A. Polyneuronal innervation of kitten skeletal muscle. J Physiol. 1973 Feb;229(1):241–255. doi: 10.1113/jphysiol.1973.sp010136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bennett M. R., Pettigrew A. G. The formation of synapses in striated muscle during development. J Physiol. 1974 Sep;241(2):515–545. doi: 10.1113/jphysiol.1974.sp010670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Betz W. J., Caldwell J. H., Ribchester R. R. The size of motor units during post-natal development of rat lumbrical muscle. J Physiol. 1979 Dec;297(0):463–478. doi: 10.1113/jphysiol.1979.sp013051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Billeter R., Weber H., Lutz H., Howald H., Eppenberger H. M., Jenny E. Myosin types in human skeletal muscle fibers. Histochemistry. 1980;65(3):249–259. doi: 10.1007/BF00493174. [DOI] [PubMed] [Google Scholar]
  9. Blackshaw S. E., Warner A. E. Low resistance junctions between mesoderm cells during development of trunk muscles. J Physiol. 1976 Feb;255(1):209–230. doi: 10.1113/jphysiol.1976.sp011276. [DOI] [PMC free article] [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. CLOSE R. DYNAMIC PROPERTIES OF FAST AND SLOW SKELETAL MUSCLES OF THE RAT DURING DEVELOPMENT. J Physiol. 1964 Sep;173:74–95. doi: 10.1113/jphysiol.1964.sp007444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Church J. C. Satellite cells and myogenesis; a study in the fruit-bat web. J Anat. 1969 Nov;105(Pt 3):419–438. [PMC free article] [PubMed] [Google Scholar]
  13. Dhoot G. K., Perry S. V. Distribution of polymorphic forms of troponin components and tropomyosin in skeletal muscle. Nature. 1979 Apr 19;278(5706):714–718. doi: 10.1038/278714a0. [DOI] [PubMed] [Google Scholar]
  14. Gauthier G. F., Lowey S. Distribution of myosin isoenzymes among skeletal muscle fiber types. J Cell Biol. 1979 Apr;81(1):10–25. doi: 10.1083/jcb.81.1.10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gauthier G. F., Lowey S., Hobbs A. W. Fast and slow myosin in developing muscle fibres. Nature. 1978 Jul 6;274(5666):25–29. doi: 10.1038/274025a0. [DOI] [PubMed] [Google Scholar]
  16. Gauthier G. F., Lowey S. Polymorphism of myosin among skeletal muscle fiber types. J Cell Biol. 1977 Sep;74(3):760–779. doi: 10.1083/jcb.74.3.760. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Kelly A. M. Satellite cells and myofiber growth in the rat soleus and extensor digitorum longus muscles. Dev Biol. 1978 Jul;65(1):1–10. doi: 10.1016/0012-1606(78)90174-4. [DOI] [PubMed] [Google Scholar]
  19. Kelly A. M., Zacks S. I. The fine structure of motor endplate morphogenesis. J Cell Biol. 1969 Jul;42(1):154–169. doi: 10.1083/jcb.42.1.154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Kikuchi T., Ashmore C. R. Developmental aspects of the innervation of skeletal muscle fibers in the chick embryo. Cell Tissue Res. 1976 Aug 20;171(2):233–251. doi: 10.1007/BF00219408. [DOI] [PubMed] [Google Scholar]
  22. Kugelberg E. Adaptive transformation of rat soleus motor units during growth. J Neurol Sci. 1976 Mar;27(3):269–289. doi: 10.1016/0022-510x(76)90001-0. [DOI] [PubMed] [Google Scholar]
  23. Lutz H., Weber H., Billeter R., Jenny E. Fast and slow myosin within single skeletal muscle fibres of adult rabbits. Nature. 1979 Sep 13;281(5727):142–144. doi: 10.1038/281142a0. [DOI] [PubMed] [Google Scholar]
  24. O'Farrell P. H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PMC free article] [PubMed] [Google Scholar]
  25. Pelloni-muller G., Ermini M., Jenny E. Myosin light chains of developing fast and slow rabbit skeletal muscle. FEBS Lett. 1976 Aug 1;67(1):68–74. doi: 10.1016/0014-5793(76)80872-1. [DOI] [PubMed] [Google Scholar]
  26. Pette D., Müller W., Leisner E., Vrbová G. Time dependent effects on contractile properties, fibre population, myosin light chains and enzymes of energy metabolism in intermittently and continuously stimulated fast twitch muscles of the rabbit. Pflugers Arch. 1976 Jul 30;364(2):103–112. doi: 10.1007/BF00585177. [DOI] [PubMed] [Google Scholar]
  27. Pette D., Schnez U. Coexistence of fast and slow type myosin light chains in single muscle fibres during transformation as induced by long term stimulation. FEBS Lett. 1977 Nov 1;83(1):128–130. doi: 10.1016/0014-5793(77)80656-x. [DOI] [PubMed] [Google Scholar]
  28. Pette D., Vrbová G., Whalen R. C. Independent development of contractile properties and myosin light chains in embryonic chick fast and slow muscle. Pflugers Arch. 1979 Jan 31;378(3):251–257. doi: 10.1007/BF00592743. [DOI] [PubMed] [Google Scholar]
  29. Rubinstein N. A., Holtzer H. Fast and slow muscles in tissue culture synthesise only fast myosin. Nature. 1979 Jul 26;280(5720):323–325. doi: 10.1038/280323a0. [DOI] [PubMed] [Google Scholar]
  30. Rubinstein N. A., Kelly A. M. Myogenic and neurogenic contributions to the development of fast and slow twitch muscles in rat. Dev Biol. 1978 Feb;62(2):473–485. doi: 10.1016/0012-1606(78)90229-4. [DOI] [PubMed] [Google Scholar]
  31. Rubinstein N. A., Pepe F. A., Holtzer H. Myosin types during the development of embryonic chicken fast and slow muscles. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4524–4527. doi: 10.1073/pnas.74.10.4524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Rubinstein N., Mabuchi K., Pepe F., Salmons S., Gergely J., Sreter F. Use of type-specific antimyosins to demonstrate the transformation of individual fibers in chronically stimulated rabbit fast muscles. J Cell Biol. 1978 Oct;79(1):252–261. doi: 10.1083/jcb.79.1.252. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Salmons S., Sréter F. A. Significance of impulse activity in the transformation of skeletal muscle type. Nature. 1976 Sep 2;263(5572):30–34. doi: 10.1038/263030a0. [DOI] [PubMed] [Google Scholar]
  34. Salmons S., Vrbová G. The influence of activity on some contractile characteristics of mammalian fast and slow muscles. J Physiol. 1969 May;201(3):535–549. doi: 10.1113/jphysiol.1969.sp008771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sreter F., Holtzer S., Gergely J., Holtzer H. Some properties of embryonic myosin. J Cell Biol. 1972 Dec;55(3):586–594. doi: 10.1083/jcb.55.3.586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Streter F. A., Gergely J., Salmons S., Romanul F. Synthesis by fast muscle of myosin light chains characteristic of slow muscle in response to long-term stimulation. Nat New Biol. 1973 Jan 3;241(105):17–19. doi: 10.1038/newbio241017a0. [DOI] [PubMed] [Google Scholar]
  37. Syrový I., Gutmann E. Differentiation of myosin in soleus and extensor digitorum longus muscle in differnt animal species during development. Pflugers Arch. 1977 May 6;369(1):85–89. doi: 10.1007/BF00580815. [DOI] [PubMed] [Google Scholar]
  38. Weeds A. G., Trentham D. R., Kean C. J., Buller A. J. Myosin from cross-reinnervated cat muscles. Nature. 1974 Jan 18;247(5437):135–139. doi: 10.1038/247135a0. [DOI] [PubMed] [Google Scholar]
  39. Whalen R. G., Butler-Browne G. S., Gros F. Identification of a novel form of myosin light chain present in embryonic muscle tissue and cultured muscle cells. J Mol Biol. 1978 Dec 15;126(3):415–431. doi: 10.1016/0022-2836(78)90049-9. [DOI] [PubMed] [Google Scholar]
  40. Whalen R. G., Butler-Browne G. S., Sell S., Gros F. Transitions in contractile protein isozymes during muscle cell differentiation. Biochimie. 1979;61(5-6):625–632. doi: 10.1016/s0300-9084(79)80160-1. [DOI] [PubMed] [Google Scholar]
  41. Whalen R. G., Schwartz K., Bouveret P., Sell S. M., Gros F. Contractile protein isozymes in muscle development: identification of an embryonic form of myosin heavy chain. Proc Natl Acad Sci U S A. 1979 Oct;76(10):5197–5201. doi: 10.1073/pnas.76.10.5197. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES