Summary
The cytochemistry and ultrastructure of intracytoplasmic filaments of pulmonary lymphatic endothelial cells of neonatal rabbits were studied by comparison with myofilaments of the peribronchial and pulmonary vascular smooth muscle cells. Two types of endothelial filaments were observed: thin filaments (diameter: 50 Å) which lie close to the abluminal cell membrane; and thick filaments (diameter: 90 Å) which are dispersed throughout the cell cytoplasm.
Following heavy meromyosin (HMM) treatment, characteristic arrowhead complexes formed in the thin lymphatic endothelial filaments as well as in the actin filaments of the smooth muscle cells. There was no detectable reaction of HMM with the thick filaments.
After incubation with EDTA, the thin filaments were labile, and the thick filaments became the major filamentous component in the endothelial cells. In smooth muscle cells, the actin myofilaments were also labile while the 100 Å filaments were stable.
These observations support the hypothesis that the actin-like thin endothelial lymphatic filaments form part of a contractile system, while the thick filaments constitute a plastic cell skeleton. The significance of the contractile system in lymphatic endothelial cells might lie in a mechanism for the active regulation of the endothelial intercellular junctions and gaps and hence the permeability of the lymphatic endothelial cell lining.
Similar content being viewed by others
References
Allison, A.C., Davies, P., Petris, S. de: Role of contractile microfilaments in macrophage movement and endocytosis. Nature (Lond.) New Biol. 232, 153–155 (1971)
Behnke, O., Emmersen, J.: Structural identification of thrombosthenin in rat megakaryocytes. Scand. J. Haemat. 9, 130–137 (1972)
Behnke, O., Kristensen, B.I., Nielsen, L.E.: Electron microscopical observations on actinoid and myosinoid filaments in blood platelets. J. Ultrastruct. Res. 37, 351–369 (1971)
Burton, P.R., Kirkland, W.L.: Actin detected in mouse neuroblastoma cells by binding of heavy meromyosin. Nature (Lond.) New Biol. 239, 244–246 (1972)
Chang, C.M., Goldmand, R.D.: The localization of actin-like fibres in cultured neuroblastoma cells as revealed by heavy meromyosin binding. J. Cell Biol. 57, 867–874 (1973)
Cooke, P.H., Fay, F.S.: Correlation between fiber length, ultrastructure, and the length-tension relationship of mammalian smooth muscle. J. Cell Biol. 52, 105–116 (1972)
Gränicher, D., Portzehl, H.: The influence of magnesium and calcium pyrophosphate chelates, of free magnesium ions, free calcium ions, and free pyrophosphate ions on the dissociation of actomyosin in solution. Biochim. biophys. Acta (Amst.) 86, 567–578 (1964)
Huxley, H.E.: Electron microscope studies on the structure of natural and synthetic protein filaments from striated muscle. J. molec. Biol. 7, 281–308 (1963)
Ishikawa, H., Bischoff, R., Holtzer, H.: Formation of arrowhead complexes with heavy meromyosin in a variety of cell types. J. Cell Biol. 43, 312–328 (1969)
Komnick, H., Stockem, W., Wohlfarth-Bottermann, K.E.: Ursachen, Begleitphänomene und Steuerung zellulärer Bewegungserscheinungen. In: Fortschritte der Zoologie. Bd. 21. (Hrsg. Fischer), p. 1–74. Stuttgart: M. Lindauer 1972
Kristensen, B.I., Nielsen, L.E., Rostgaard, J.: A two-filament system and interaction of heavy meromyosin (HMM) with thin filaments in smooth muscle. Z. Zellforsch. 122, 350–356 (1971)
Kristensen, B.I., Simonsen, L.O., Pape, L.: Actin-like filaments in Ehrlich Ascites tumor cells and their reaction with heavy meromyosin. Virchows Archiv Abt. B13, 103–112 (1973)
Kühnel, W.: Elektronenmikroskopische Befunde am Ductus thoracicus. Z.Zellforsch. 70, 519–531 (1966)
Lauweryns, J.M.: The blood and lymphatic microcirculation of the lung. In: Pathology Annual, (S.C. Sommers, ed.), p. 365–415. New York: Appleton-Century-Crofts 1971
Lauweryns, J.M., Baert, J.H.: The role of the pulmonary lymphatics in the defenses of the distal lung: morphological and experimental studies of the transport mechanisms of intratracheally instillated particles. Ann. N.Y. Acad. Sci. 221, 244–275 (1974)
Lauweryns, J.M., Boussauw, L.: The ultrastructure of pulmonary lymphatic capillaries of newborn rabbits and of human infants. Lymphology, 2, 108–129 (1969)
Lauweryns, J.M., Boussauw, L.: The ultrastructure of lymphatic valves in the adult rabbit lung. Z. Zellforsch. 143, 149–168 (1973)
Leak, L.V.: Electron microscopic observations on lymphatic capillaries and the structural components of the connective tissue-lymph interface. Microvas. Res. 2, 361–391 (1970)
Leak, L.V., Burke, J.F.: The passage of electron-opaque tracers across the lymphatic capillary wall. J. Cell Biol. 25, 731–732 (1965)
Leak, L.V., Burke, J.F.: Fine structure of the lymphatic capillary and the adjoining connective tissue area. Amer. J. Anat. 118, 785–810 (1966)
Leak, L.V., Burke, J.F.: Ultrastructural studies on the lymphatic anchoring filaments. J. Cell Biol. 36, 129–149 (1968)
Lowey, S., Cohen, C.: Studies on the structure of myosin. J. molec. Biol. 4, 293–308 (1962)
Maruyama, K., Gergely, J.: Interaction of actomyosin with adenosine triphosphate at low ionic strength. J. biol. Chem. 237, 1095–1099 (1962)
Mommaerts, W.F.H.M.: Chemical investigation of muscular tissues. In: Methods of Medical Research, (J.V. Warren, ed.), p. 1–59. Chicago: Year Book Medical Publishers Inc. 7, 1958
Norberg, B.: Amoeboid movements and cytoplasmic fragmentation of glycerinated leucocytes induced by ATP. Expl. Cell Res. 59, 11–21 (1970)
Orci, L., Gabbay, K.H., Malaisse, W.J.: Pancreatic beta-cell web: its possible role in insulin secretion. Science 175, 1128–1130 (1972)
Panner, B.J., Honig, C.R.: Filament ultrastructure and organization in vertebrate smooth muscle. J. Cell Biol. 35, 303–321 (1967)
Perry, S.V.: Myosin adenosinetriphosphatase. Methods in enzymology II, p. 582–588. New York: Acad. Press 1955
Phelps, P.C., Luft, J.H.: Electron microscopical study of relaxation and constriction in frog arterioles. Amer. J. Anat. 125, 399–428 (1969)
Reynolds, E.S.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963)
Röhlich, P., Olah, I.: Cross-striated fibrils in the endothelium of the rat myometrial arterioles. J. Ultrastruct. Res. 18, 667–676 (1967)
Rostgaard, J., Kristensen, B.J., Nielsen, L.E.: Myofilaments in nonmuscular cells. In: Histochemistry and Cytochemistry. Proc. 4th Int. Cong. Histochem. Cytochem. Kyoto, 377, 1972
Schipp, R.: Der Feinbau filamentärer Strukturen im Endothel peripherer Lymphgefäße. Acta anat. (Basel) 71, 341–351 (1968)
Shibata, N., Tatsumi, N., Tanaka, K., Okamura, Y., Senda, N.: A contractile protein possessing Ca2++ sensitivity (natural actomyosin) from leucocytes. Its Extraction and some of its properties. Biochim. biophys. Acta (Amst.) 256, 565–576 (1972)
Spooner, B.S., Ash, J.F., Wrenn, J.T., Frater, R.B., Wessells, N.K.: Heavy meromyosin binding to microfilaments involved in cell and morphogenetic movements. Tissue and Cell 5, 37–46 (1973)
Steers, E., Marchesi, V.T.: Studies on a protein component of guinea pig erythrocyte membranes. J. gen. Physiol. 54, 65s-71s (1969)
Takada, M.: The ultrastructure of lymphatic valves in rabbits and mice. Amer. J. Anat. 132, 207–218 (1971)
Tilney, L.G., Hatano, S., Ishikawa, H., Mooseker, M.S.: The polymerization of actin: its role in the generation of the acrosomal process of certain echinoderm sperm. J. Cell Biol. 59, 109–126 (1972)
Tilney, L.G., Mooseker, M.: Actin in the brushborder of epithelial cells of the chicken intestine. Proc. nat. Acad. Sci. (Wash.) 68, 2611–2615 (1971)
Vajda, J., Tomcsik, M.: The structure of the valves of the lymphatic vessels. Acta anat. (Basel) 78, 521–531 (1971)
Wagner, R., Rosenberg, M., Estensen, R.: Endocytosis in Chang liver cells. Quantitation by sucrose3H uptake and inhibition by cytochalasin B. J. Cell Biol. 50, 804–817 (1971)
Author information
Authors and Affiliations
Additional information
This study was supported by The Council for Tobacco Research—U.S.A. The authors thank Professor Robert C. Rosan, M.D. (Saint-Louis University—U.S.A.) for expert advice. R. Renwart, B. Emanuel and R. Jullet for technical, G. Pison and St. Ons for photographical and N. Tyberghien for secretarial assistance.
Rights and permissions
About this article
Cite this article
Lauweryns, J.M., Baert, J. & De Loecker, W. Intracytoplasmic filaments in pulmonary lymphatic endothelial cells. Cell Tissue Res. 163, 111–124 (1975). https://doi.org/10.1007/BF00221720
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00221720