Electron microscopic observations on lymphatic capillaries and the structural components of the connective tissue-lymph interface

Abstract

The lymphatic capillaries of dermal tissue in the guinea pig's ear have been examined with particular reference to their fine structure and the topographical relationship of the connective tissue-lymph interface. Lymphatic capillaries possess specific features which serve to differentiate them from blood capillaries. The lymphatics posses: (1) A much wider and more irregular lumen than the blood capillary; (2) an endothelium with an extremely attenuated cytoplasm except in the perinuclear region; (3) a discontinuous basement lamina; (4) endothelial cell junctions generally lacking the so-called tight junctions that have been described for some blood capillaries and thus many patent junctions are observed; (5) a system of anchoring filaments which terminate on the endothelial wall and serve to bind the lymphatic endothelium to the adjoining inter-stitial areas. Lumina of lymphatic capillaries in normal tissues are usually devoid of cellular elements and electron micrographs reveal a uniformly gray flocculent material which can occasionally be followed into the interstitial areas through the intercellular clefts of patent junctions. The lymphatic endothelial cell contains the usual complement of organelles. However, a striking feature of the cytoplasm is the presence of numerous fine filaments which measure approximately 60 Å in diameter and often are arranged in bundles that are oriented parallel to the long axis of the cell. These cytoplasmic filaments are very similar to those noted in cells that have been reported to serve a contractile function. The occurrence of numerous cytoplasmic filaments that are longitudinally oriented in the lymphatic endothelial cells is of particular significance, especially since recent observations suggest that cytoplasmic filaments in endothelial cells of blood vessels possess contractile properties. The presence of numerous anchoring filaments that are attached to the abluminal surface of the lymphatic wall and extend for long distances into the surrounding interstitium, provides a morphological basis for explaining how the lymphatic wall is stabilized to the adjoining interstitium. If the cytoplasmic filaments are indeed contractile elements, the lymphatic anchoring filaments could serve to stabilize the lymphatic wall to the adjoining interstitium while permitting a longitudinal contraction of the endothelial cells which would presumably cause adjacent cells to become separated, thereby providing patent intercellular channels that would be readily available for the passage of interstitial fluids. Observations on the uptake of interstitially injected electron-opaque marker substances (i.e., ferritin, thorium, carbon, and latex spheres) demonstrate the passage of these tracers into the lymphatic lumen via vesicles and across intercellular clefts of patent junctions. However, the major route for the passage of substances from the interstitium appears to be via the intercellular clefts of patent junctions. Observations also indicate that the chemical makeup of the injected particles may also influence the ability of the plasma membrane to incorporate particles into micropinocytotic vesicles that move across the endothelial cell. The larger particles that are engulfed by way of vesicles tend to accumulate in very large vesicles within the cytoplasm as noted in specimens examined up to 6 months after interstitial injections. Many of these large vesicles also contain dense homogeneous substances, and membranous components similar to those observed in lysosomes and autophagic vacuoles. Since acid phosphatase activity has been localized in lymphatic endothelial cells of the tail fin of tadpoles as well as the dermis of several mammalian species, it is conceivable that endothelial cells of dermal lymphatics are also involved in the intracellular digestion of substances engulfed from the surrounding interstitium.