Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1989 Jan 1;108(1):43–53. doi: 10.1083/jcb.108.1.43

Immunocytochemical studies of cardiac myofibrillogenesis in early chick embryos. III. Generation of fasciae adherentes and costameres

PMCID: PMC2115361  PMID: 2492024

Abstract

To study whether the first myofibrils are separate from or firmly bound to the myocytic cell membranes, whole mount preparations of 6-12-somite- stage chick embryonic hearts were examined by fluorescence microscopy after double labeling with antibodies to vinculin (fluorescein- conjugated) and rhodamine-phalloidin, or with antibodies to titin (rhodamine-conjugated) and nitrobenz-oxadiazole-phallacidin. When a small number of myofibrils appeared for the first time at the nine somite stage, most of them were already bound to the cell membranes through zonulae adherentes, fasciae adherentes, or costameres. In the outer of the two myocardial cell layers, in which the myocytes were closely in contact with each other along polygonal boundaries, fasciae adherentes and costameres developed at the boundaries, apparently by conversion of preexisting zonulae adherentes. On the other hand, in the inner cell layer, in which myocytes were more loosely associated with each other, both costameres and fasciae adherentes appeared to develop de novo, the former in association with the inner surface of the myocardial wall and the latter at the intercellular boundaries. The myofibrillar tracks in the inner layer followed long and smooth courses and were as a whole aligned in the circumferential direction of the tubular heart wall from the earliest stage of myofibril formation. Those in the outer layer were arranged in a pattern of two- or three- dimensional networks in the 9-10 somite stage, although many myofibrils were also circumferentially directed. The fact that the majority of the first myofibrils were already bound to the cell membranes in a directed manner suggests that myocytes at the earliest stage of myofibril formation are endowed with spatial information that directs the organization of nascent myofibrils. It is proposed that the myocyte cell membranes perform an essential role in cardiac myofibrillogenesis.

Full Text

The Full Text of this article is available as a PDF (5.3 MB).

Selected References

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

  1. Dlugosz A. A., Antin P. B., Nachmias V. T., Holtzer H. The relationship between stress fiber-like structures and nascent myofibrils in cultured cardiac myocytes. J Cell Biol. 1984 Dec;99(6):2268–2278. doi: 10.1083/jcb.99.6.2268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Fawcett D. W., McNutt N. S. The ultrastructure of the cat myocardium. I. Ventricular papillary muscle. J Cell Biol. 1969 Jul;42(1):1–45. doi: 10.1083/jcb.42.1.1. [DOI] [PMC free article] [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. Fujii S., Hirota A., Kamino K. Optical indications of pace-maker potential and rhythm generation in early embryonic chick heart. J Physiol. 1981 Mar;312:253–263. doi: 10.1113/jphysiol.1981.sp013627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Geiger B. A 130K protein from chicken gizzard: its localization at the termini of microfilament bundles in cultured chicken cells. Cell. 1979 Sep;18(1):193–205. doi: 10.1016/0092-8674(79)90368-4. [DOI] [PubMed] [Google Scholar]
  6. Geiger B., Dutton A. H., Tokuyasu K. T., Singer S. J. Immunoelectron microscope studies of membrane-microfilament interactions: distributions of alpha-actinin, tropomyosin, and vinculin in intestinal epithelial brush border and chicken gizzard smooth muscle cells. J Cell Biol. 1981 Dec;91(3 Pt 1):614–628. doi: 10.1083/jcb.91.3.614. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Geiger B., Tokuyasu K. T., Dutton A. H., Singer S. J. Vinculin, an intracellular protein localized at specialized sites where microfilament bundles terminate at cell membranes. Proc Natl Acad Sci U S A. 1980 Jul;77(7):4127–4131. doi: 10.1073/pnas.77.7.4127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Goldspink G. The proliferation of myofibrils during muscle fibre growth. J Cell Sci. 1970 Mar;6(2):593–603. doi: 10.1242/jcs.6.2.593. [DOI] [PubMed] [Google Scholar]
  9. Heggeness M. H., Ash J. F. Use of the avidin-biotin complex for the localization of actin and myosin with fluorescence microscopy. J Cell Biol. 1977 Jun;73(3):783–788. doi: 10.1083/jcb.73.3.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hiruma T., Hirakow R. An ultrastructural topographical study on myofibrillogenesis in the heart of the chick embryo during pulsation onset period. Anat Embryol (Berl) 1985;172(3):325–329. doi: 10.1007/BF00318980. [DOI] [PubMed] [Google Scholar]
  11. Huang C. Y. Electron microscopic study of the development of heart muscle of the frog Rana pipiens. J Ultrastruct Res. 1967 Oct 10;20(3):211–226. doi: 10.1016/s0022-5320(67)90283-3. [DOI] [PubMed] [Google Scholar]
  12. Hull B. E., Staehelin L. A. The terminal web. A reevaluation of its structure and function. J Cell Biol. 1979 Apr;81(1):67–82. doi: 10.1083/jcb.81.1.67. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Manasek F. J., Burnside M. B., Waterman R. E. Myocardial cell shape change as a mechanism of embryonic heart looping. Dev Biol. 1972 Dec;29(4):349–371. doi: 10.1016/0012-1606(72)90077-2. [DOI] [PubMed] [Google Scholar]
  14. Manasek F. J. Determinants of heart shape in early embryos. Fed Proc. 1981 May 15;40(7):2011–2016. [PubMed] [Google Scholar]
  15. Manasek F. J. Embryonic development of the heart. I. A light and electron microscopic study of myocardial development in the early chick embryo. J Morphol. 1968 Jul;125(3):329–365. doi: 10.1002/jmor.1051250306. [DOI] [PubMed] [Google Scholar]
  16. Manasek F. J. Histogenesis of the embryonic myocardium. Am J Cardiol. 1970 Feb;25(2):149–168. doi: 10.1016/0002-9149(70)90576-x. [DOI] [PubMed] [Google Scholar]
  17. Pardo J. V., Siliciano J. D., Craig S. W. A vinculin-containing cortical lattice in skeletal muscle: transverse lattice elements ("costameres") mark sites of attachment between myofibrils and sarcolemma. Proc Natl Acad Sci U S A. 1983 Feb;80(4):1008–1012. doi: 10.1073/pnas.80.4.1008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Pardo J. V., Siliciano J. D., Craig S. W. Vinculin is a component of an extensive network of myofibril-sarcolemma attachment regions in cardiac muscle fibers. J Cell Biol. 1983 Oct;97(4):1081–1088. doi: 10.1083/jcb.97.4.1081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Sanger J. M., Mittal B., Pochapin M. B., Sanger J. W. Myofibrillogenesis in living cells microinjected with fluorescently labeled alpha-actinin. J Cell Biol. 1986 Jun;102(6):2053–2066. doi: 10.1083/jcb.102.6.2053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Shear C. R., Bloch R. J. Vinculin in subsarcolemmal densities in chicken skeletal muscle: localization and relationship to intracellular and extracellular structures. J Cell Biol. 1985 Jul;101(1):240–256. doi: 10.1083/jcb.101.1.240. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Sissman N. J. Developmental landmarks in cardiac morphogenesis: comparative chronology. Am J Cardiol. 1970 Feb;25(2):141–148. doi: 10.1016/0002-9149(70)90575-8. [DOI] [PubMed] [Google Scholar]
  22. Tokuyasu K. T., Dutton A. H., Geiger B., Singer S. J. Ultrastructure of chicken cardiac muscle as studied by double immunolabeling in electron microscopy. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7619–7623. doi: 10.1073/pnas.78.12.7619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Tokuyasu K. T., Maher P. A. Immunocytochemical studies of cardiac myofibrillogenesis in early chick embryos. I. Presence of immunofluorescent titin spots in premyofibril stages. J Cell Biol. 1987 Dec;105(6 Pt 1):2781–2793. doi: 10.1083/jcb.105.6.2781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Tokuyasu K. T., Maher P. A. Immunocytochemical studies of cardiac myofibrillogenesis in early chick embryos. II. Generation of alpha-actinin dots within titin spots at the time of the first myofibril formation. J Cell Biol. 1987 Dec;105(6 Pt 1):2795–2801. doi: 10.1083/jcb.105.6.2795. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Wang K., McClure J., Tu A. Titin: major myofibrillar components of striated muscle. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3698–3702. doi: 10.1073/pnas.76.8.3698. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES