Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1969 Jul 1;42(1):135–153. doi: 10.1083/jcb.42.1.135

THE HISTOGENESIS OF RAT INTERCOSTAL MUSCLE

A M Kelly 1, S I Zacks 1
PMCID: PMC2107573  PMID: 5786979

Abstract

Intercostal muscle from fetal and newborn rats was examined with the electron microscope. At 16 days' gestation, the developing muscle was composed of primary generations of myotubes, many of which were clustered together in groups. Within these groups, the membranes of neighboring myotubes were interconnected by specialized junctions, including tight junctions. Morphologically undifferentiated cells surrounded the muscle groups, frequently extended pseudopodia along the interspace between adjacent myotubes, and appeared to separate neighboring myotubes from one another. At 18 and 20 days' gestation, the muscle was also composed of groups of cells but the structure of the groups differed from that of the groups observed at 16 days. Single, well differentiated myotubes containing much central glycogen and peripheral myofibrils dominated each group. These large cells were interpreted as primary myotubes. Small, less differentiated muscle cells and undifferentiated cells clustered around their walls. Each cluster was ensheated by a basal lamina. The small cells were interpreted as primordia of new generations of muscle cells which differentiated by appositional growth along the walls of the large primary myotubes. All generations of rat intercostal muscle cells matured to myofibers between 20 days' gestation and birth. Coincidentally, large and small myofibers diverged from each other, leading to disintegration of the groups of muscle cells. Undifferentiated cells frequently occurred in the interspaces between neighboring muscle cells at the time of separation. Myofibers arising at different stages of muscle histogenesis intermingled in a checkerboard fashion as a result of this asynchronous mode of development. The possibility of fusion between neighboring muscle cells in this developing system is discussed.

Full Text

The Full Text of this article is available as a PDF (2.1 MB).

Selected References

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

  1. Dubowitz V., Newman D. L. Change in enzyme pattern after cross-innervation of fast and slow skeletal muscle. Nature. 1967 May 20;214(5090):840–841. doi: 10.1038/214840a0. [DOI] [PubMed] [Google Scholar]
  2. FIRKET H. Recherches sur la synthèse des acides désoxyribonucléiques et la préparation à la mitose dans des cellules cultivées in vitro; etude cytophotométrique et autoradiographique. Arch Biol (Liege) 1958;69(1):1–166. [PubMed] [Google Scholar]
  3. Fischman D. A. An electron microscope study of myofibril formation in embryonic chick skeletal muscle. J Cell Biol. 1967 Mar;32(3):557–575. doi: 10.1083/jcb.32.3.557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. HAY E. D. The fine structure of differentiating muscle in the salamander tail. Z Zellforsch Mikrosk Anat. 1963;59:6–34. doi: 10.1007/BF00321005. [DOI] [PubMed] [Google Scholar]
  5. Ishikawa H. Electron microscopic observations of satellite cells with special reference to the development of mammalian skeletal muscles. Z Anat Entwicklungsgesch. 1966;125(1):43–63. doi: 10.1007/BF00521974. [DOI] [PubMed] [Google Scholar]
  6. KONIGSBERG I. R., MCELVAIN N., TOOTLE M., HERRMANN H. The dissociability of deoxyribonucleic acid synthesis from the development of multinuclearity of muscle cells in culture. J Biophys Biochem Cytol. 1960 Oct;8:333–343. doi: 10.1083/jcb.8.2.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. LASH J. W., HOLTZER H., SWIFT H. Regeneration of mature skeletal muscle. Anat Rec. 1957 Aug;128(4):679–697. doi: 10.1002/ar.1091280404. [DOI] [PubMed] [Google Scholar]
  8. Loewenstein W. R. On the genesis of cellular communication. Dev Biol. 1967 Jun;15(6):503–520. doi: 10.1016/0012-1606(67)90050-4. [DOI] [PubMed] [Google Scholar]
  9. MACCONNACHIE H. F., ENESCO M., LEBLOND C. P. THE MODE OF INCREASE IN THE NUMBER OF SKELETAL MUSCLE NUCLEI IN THE POSTNATAL RAT. Am J Anat. 1964 Mar;114:245–253. doi: 10.1002/aja.1001140205. [DOI] [PubMed] [Google Scholar]
  10. MAURO A. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol. 1961 Feb;9:493–495. doi: 10.1083/jcb.9.2.493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. PRICE H. M., HOWES E. L., Jr, BLUMBERG J. M. ULTRASTRUCTURAL ALTERATIONS IN SKELETAL MUSCLE FIBERS INJURED BY COLD. II. CELLS ON THE SARCOLEMMAL TUBE: OBSERVATIONS ON "DISCONTINUOUS" REGENERATION AND MYOFIBRIL FORMATION. Lab Invest. 1964 Oct;13:1279–1302. [PubMed] [Google Scholar]
  12. Potter D. D., Furshpan E. J., Lennox E. S. Connections between cells of the developing squid as revealed by electrophysiological methods. Proc Natl Acad Sci U S A. 1966 Feb;55(2):328–336. doi: 10.1073/pnas.55.2.328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Przybylski R. J., Blumberg J. M. Ultrastructural aspects of myogenesis in the chick. Lab Invest. 1966 May;15(5):836–863. [PubMed] [Google Scholar]
  14. Romanul F. C., Van der Meulen J. P. Slow and fast muscles after cross innervation. Enzymatic and physiological changes. Arch Neurol. 1967 Oct;17(4):387–402. doi: 10.1001/archneur.1967.00470280053006. [DOI] [PubMed] [Google Scholar]
  15. SHAFIQ S. A. Electron microscopic studies on the indirect flight muscles of Drosophila melanogaster. II. Differentiation of myofibrils. J Cell Biol. 1963 May;17:363–373. doi: 10.1083/jcb.17.2.363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. STOCKDALE F. E., HOLTZER H. DNA synthesis and myogenesis. Exp Cell Res. 1961 Sep;24:508–520. doi: 10.1016/0014-4827(61)90450-5. [DOI] [PubMed] [Google Scholar]
  17. STREHLER B. L., KONIGSBERG I. R., KELLEY J. E. PLOIDY OF MYOTUBE NUCLEI DEVELOPING IN VITRO AS DETERMINED WITH A RECORDING DOUBLE BEAM MICRO-SPECTROPHOTOMETER. Exp Cell Res. 1963 Nov;32:232–241. doi: 10.1016/0014-4827(63)90098-3. [DOI] [PubMed] [Google Scholar]
  18. Sheridan J. D. Electrophysiological evidence for low-resistance intercellular junctions in the early chick embryo. J Cell Biol. 1968 Jun;37(3):650–659. doi: 10.1083/jcb.37.3.650. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Sheridan J. D. Electrophysiological study of special connections between cells in the early chick embryo. J Cell Biol. 1966 Oct;31(1):C1–C5. doi: 10.1083/jcb.31.1.c1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. WIRSEN C., LARSSON K. S. HISTOCHEMICAL DIFFERENTIATION OF SKELETAL MUSCLE IN FOETAL AND NEWBORN MICE. J Embryol Exp Morphol. 1964 Dec;12:759–767. [PubMed] [Google Scholar]

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

RESOURCES