Skip to main content
SpringerLink
Log in

Cell junctions and their role in transmural diffusion in the embryonic chick heart

  • Published:
Zeitschrift für Zellforschung und Mikroskopische Anatomie Aims and scope Submit manuscript

Summary

Studies of cardiogenesis in the chick embryo focus attention upon the intercellular junctions of epicardial, myocardial, and endocardial cells, and the role they play in diffusion across the cardiac wall. Cell membranes of apposed epicardial cells approach as close together as 40 Å; those of the endocardium additionally form focal tight junctions. In the myocardium focal tight junctions are restricted to the apposed membranes of the superficial layer of cells. The majority of close appositions in all parts of the myocardium are 40 Å gap junctions. Desmosomes and fascia adherens are distributed throughout the myocardium.

Diffusion of horseradish peroxidase through the epicardium and endocardium occurs primarily through the intercellular junctions. The width of the cleft between cells, 200–300 Å, also permits the diffusion between cells of the larger ferritin particles. Pinocytotic activity, responsible for ferritin transfer across mesothelial and endothelial cells in the adult, is not significant.

Tracers injected into the pericardial cavity or vasculature can be observed passing through the heart in the direction of their respective diffusion gradients. Unlike the apical junctions of epithelial cells, to which they have been compared, membrane specializations of the superficial myocytes do not form a seal separating the pericardial cavity, or subepicardial space, from the extracellular spaces of the myocardium.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Barr, L., Dewey, M. M., Berger, W.: Propagation of action potentials and the structure of the nexus in cardiac muscle. J. gen. Physiol. 48, 797–823 (1965).

    Google Scholar 

  • —: Electrical transmission at the nexus between smooth muscle cells. J. gen. Physiol. 51, 347–368 (1968).

    Google Scholar 

  • Becker, C. G., Murphy, G. E.: Demonstration of contractile protein in endothelium and cells of the heart valves, endocardium, intima, arteriosclerotic plaques, and Aschoff bodies of rheumatic heart disease. Amer. J. Path. 55, 1–38 (1969).

    Google Scholar 

  • Brightman, M. W., Reese, T. S.: Junctions between intimately apposed cell membranes in the vertebrate brain. J. Cell Biol. 40, 648–677 (1969).

    Google Scholar 

  • Bulger, R. E., Trump, B. F.: A mechanism for rapid transport of colloidal particles by flounder renal epithelium. J. Morph. 127, 205–224 (1969).

    Google Scholar 

  • Clementi, F., Palade, G. E.: Intestinal capillaries. I. Permeability to peroxidase and ferritin. J. Cell Biol. 41, 33–58 (1969).

    Google Scholar 

  • Cotran, R. S., Karnovsky, M. J.: Ultrastructural studies on the permeability of the mesothelium to horseradish peroxidase. J. Cell Biol. 37, 123–137 (1968).

    Google Scholar 

  • Dewey, M. M., Barr, L.: Intercellular connection between smooth muscle cells: the nexus. Science 137, 670–672 (1962).

    Google Scholar 

  • —: A study of the structure and distribution of the nexus. J. Cell Biol. 23, 553–585 (1964).

    Google Scholar 

  • Farquhar, M., Palade, G. E.: Cell junctions in amphibian skin. J. Cell Biol. 26, 263–267 (1965).

    Google Scholar 

  • Farrant, J. L.: An electron microscopic study of ferritin. Biochim. biophys. Acta (Amst.) 13, 569–576 (1954).

    Google Scholar 

  • Fawcett, D. W.: The cell: Its organelles and inclusions. Philadelphia: W. B. Saunders 1966.

    Google Scholar 

  • Gessner, I. H., Lorincz, A. E., Bostrom, H.: Acid mucopolysaecharide content of the cardiac jelly of the chick embryo. J. exp. Zool. 160, 291–298 (1965).

    Google Scholar 

  • Giacomelli, F., Wiener, J., Spiro, D.: Cross-striated arrays of filaments in endothelium. J. Cell Biol. 45, 188–192 (1970).

    Google Scholar 

  • Graham, R. C., Karnovsky, M. J.: The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney. Ultrastructural cytochemistry by a new technique. J. Histochem. Cytochem. 14, 291–302 (1966).

    Google Scholar 

  • Hama, K.: On the existence of filamentous structures in endothelial cells of the amphibian capillary. Anat. Rec. 139, 437–442 (1961).

    Google Scholar 

  • Hamburger, V., Hamilton, H. L.: A series of normal stages in the development of the chick embryo. J. Morph. 88, 49–92 (1951).

    Google Scholar 

  • Henningsen, B., Schiebler, T. H.: Zur Frühentwicklung der herzeigenen Strombahn. Elektronenmikroskopische Untersuchung an der Ratte. Z. Anat. Entwickl.-Gesch. 130, 101–114 (1970).

    Google Scholar 

  • Hirakow, R.: Ultrastructural characteristics of the mammalian and sauropsidian heart. Amer. J. Cardiol. 25, 195–203 (1970).

    Google Scholar 

  • Huang, C. Y.: Electron microscopic study of the development of heart muscle of the frog Rana pipiens. J. Ultrastruct. Res. 20, 211–226 (1967).

    Google Scholar 

  • Huxley, H. E.: Evidence for continuity between central elements of the triads and extracellular space in frog sartorius muscle. Nature (Lond.) 202, 1067–1071 (1964).

    Google Scholar 

  • Jennings, M. A., Florey, Lord.: An investigation of some properties of endothelium related to capillary permeability. Proc. roy. Soc. B 167, 39–63 (1967).

    Google Scholar 

  • Karnovsky, M. J.: A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J. Cell Biol. 27, 137 A (1965).

    Google Scholar 

  • —: The ultrastructural basis of capillary permeability studied with peroxidase as a tracer. J. Cell Biol. 35, 213–236 (1967).

    Google Scholar 

  • Kaye, G. I., Pappas, G. D., Donn, A., Mallett, N.: Studies on the cornea. II. The uptake and transport of colloidal particles by the living rabbit cornea in vitro. J. Cell Biol. 12, 481–502 (1962).

    Google Scholar 

  • Krzyzowska-Gruca, St., Schiebler, T. H.: Experimentelle Untersuchungen am Dottersackepithel der Ratte. Z. Zellforsch. 79, 151–171 (1967).

    Google Scholar 

  • Majno, G., Shea, S. M., Leventhal, M.: Endothelial contraction induced by histamine-type mediators. An electron microscopic study. J. Cell Biol. 42, 647–672 (1969).

    Google Scholar 

  • Manasek, F. J.: Embryonic development of the heart. I. A light and electron microscopic study of myocardial development in the early chick embryo. J. Morph. 125, 329–366 (1968).

    Google Scholar 

  • —: Embryonic development of the heart. II. Formation of the epicardium. J. Embryol. exp. Morph. 22, 333–348 (1969a).

    Google Scholar 

  • —: The appearance of granules in the Golgi complex of embryonic cardiac myocytes. J. Cell Biol. 43, 605–610 (1969b).

    Google Scholar 

  • —: Sulfated extracellular matrix production in the embryonic heart and adjacent tissues. J. exp. Zool. 174, 415–440 (1970).

    Google Scholar 

  • McNutt, N. S., Weinstein, R. S.: The ultrastructure of the nexus. A correlated thin-section and freeze cleave study. J. Cell Biol. 47, 666–688 (1970).

    Google Scholar 

  • Muir, A. R.: The effect of divalent cations on the ultrastructure of the perfused rat heart. J. Anat. (Lond.) 101, 239–261 (1967).

    Google Scholar 

  • New, D. A. T.: The culture of vertebrate embryos. London: Logos Press 1966.

    Google Scholar 

  • Palade, G. E.: Blood capillaries of the heart and other organs. Circulation 24, 368–384 (1961).

    Google Scholar 

  • Payton, B. W., Bennett, M. V. L., Pappas, G. D.: Permeability and structure of junctional membranes at an electrotonic synapse. Science 166, 1641–1643 (1969).

    Google Scholar 

  • Rash, J. E., Shay, J. W., Biesele, J. J.: Urea extraction of Z bands, intercalated disks, and desmosomes. J. Ultrastruct. Res. 24, 181–189 (1968).

    Google Scholar 

  • Revel, J. P., Karnovsky, M. J.: Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J. Cell Biol. 33, C7-C12 (1967).

    Google Scholar 

  • Romanoff, A. L.: Differentiation in respiratory activity of isolated embryonic tissues. J. exp. Zool. 93, 1–26 (1943).

    Google Scholar 

  • Sedar, A. W.: Uptake of peroxidase into the smooth-surfaced tubular system of the gastric acid-secreting cell. J. Cell Biol. 43, 179–184 (1969).

    Google Scholar 

  • Sheridan, J. D.: Electrophysiological evidence for low resistance intercellular junctions in in the early chick embryo. J. Cell Biol. 37, 650–659 (1968).

    Google Scholar 

  • Sommer, J. R., Johnson, E. A.: Cardiac muscle. A comparative ultrastructural study with special reference to frog and chicken hearts. Z. Zellforsch. 98, 437–468 (1969).

    Google Scholar 

  • Spira, A. W.: The nexus in the intercalated disc of the canine heart: Quantitative data for an estimate of its resistance. J. Ultrastruct. Res. 34, 409–425 (1971).

    Google Scholar 

  • Staubesand, J.: Zur Histophysiologie des Herzbeutels. II. Elektronenmikroskopische Untersuchungen über die Passage von Metallsolen durch mesotheliale Membranen. Z. Zellforsch. 58, 915–952 (1963).

    Google Scholar 

  • Trelstad, R. L., Hay, E. D., Revel, J.-P.: Cell contact during early morphogenesis in the chick embryo. Develop. Biol. 16, 78–106 (1967).

    Google Scholar 

  • Trump, B. F., Bulger, R. E.: New ultrastructural characteristics of cells fixed in a glutaraldehyde-osmium tetroxide mixture. Lab. Invest. 15, 368–380 (1966).

    Google Scholar 

  • Venable, J. H., Coggleshall, R.: A simplified lead citrate stain for use in electron microscopy. J. Cell Biol. 25, 407–408 (1965).

    Google Scholar 

  • Vobořil, Z., Schiebler, T. H.: Über die Entwicklung der Gefäßversorgung des Rattenherzens. Z. Anat. Entwickl.-Gesch. 129, 24–40 (1969).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, The University of British Columbia, Vancouver, British Columbia, Canada

    Arthur W. Spira

Authors
  1. Arthur W. Spira
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Supported by the Medical Research Council of Canada.

The author wishes to express his gratitude to Mrs. J. Blackbourn for her excellent technical assistance.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Spira, A.W. Cell junctions and their role in transmural diffusion in the embryonic chick heart. Z. Zellforsch. 120, 463–487 (1971). https://doi.org/10.1007/BF00340585

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00340585

Key-Words

Search

Navigation