The portal vein of the rat is immature at birth, and is composed of an endothelium surrounded by undifferentiated cells of mesenchymal origin. Three days after birth, these cells have begun to differentiate and aggregate around the lumen to form two separate layers of perpendicularly oriented myoblasts, while a rich calcitonin gene-related peptide (CGRP) innervation is present around the vessel. In the internal circular muscle layer of the media myofibrils first develop on the endothelial side of the myoblasts, and then progressively reach the other side. In the longitudinal muscular layer of the media, which is separated from the circular layer by a connective lamina as early as 3 days after birth, myofibrils develop randomly in the cells. At the time of the enlargement of the longitudinal layer, long close contacts and intermediate junctions between external myoblasts and adventitial fibroblast-like cells were noted, suggesting that recruitment of this cell type is necessary for the maturation of the vessel wall. At about 28 days, the vein has reached its final structure and the smooth muscle cells are fully differentiated. The dense CGRP perivascular innervation already present at birth persists for the first 14 days of postnatal life when most of the cells have not yet acquired their complete contractile differentiation and are still capable of division. This innervation decreases transiently between 15-17 days, when the vessel acquires its spontaneous contractile activity, then rises to a peak between 20 and 25 days, and falls again. CGRP innervation, which is very scarce at 28 days, slowly increases during the peripubescent stage, by which time the adult structure of the vessel is established. Similar fluctuations in the density of peptidergic innervation were observed for substance P and neuropeptide Y, although these peptides were not yet present at birth and occurred only after 5 days. Vasoactive intestinal polypeptide- and bombesin-immunoreactive fibres were not found at any stage investigated. In addition to a description of the different cell-to-cell contacts which could play a role in the maturation of the vessel wall, we discuss the possible implication of the different peptides in the differentiation, maturation or maintenance of the vessel wall.
Immunohistochemistry of alpha-smooth muscle actin and desmin, two markers of smooth muscle cell differentiation, and electron-microscopic observation of thick filaments of myosin were performed on the media of the developing rat hepatic portal vein to gain insights into the chronology of differentiation of its longitudinal and circular smooth muscles. In accordance with the ultrastructural distribution of thin filaments, staining of alpha-smooth muscle actin is lightly positive in the myoblasts at postnatal day 1 and then extends in probably all muscle cells of the developing vessel. Desmin, which appears later than alpha-smooth muscle actin in the two muscles, is distributed throughout the longitudinal layer at day 8, whereas the first arrangements of thick filaments are detectable in most longitudinal muscle cells; at this stage, desmin and thick filaments are absent from the poorly differentiated circular muscle cells. The longitudinal muscle cells differentiate in a strikingly synchronized way from day 8 onwards, conferring a homogeneous structure to the developing and mature longitudinal layer. Several desmin-positive cells and a heterogeneous distribution of thick filaments occur in the circular muscle at day 14; the subsequent extension of these filaments in this layer results in a persisting heterogeneous distribution in the young 7-week-old adult. Many features of the mature smooth muscle cells are established within the third week in the longitudinal muscle, approximately one week before those of the circular layer. These results are consistent with the function of the longitudinal muscle as a spontaneously contractile smooth muscle unit, and emphasize the need for its fast maturation to fulfil its major role in the control of portal blood flow.
Autoradiographic studies with [125I]-CGRP did not demonstrate receptors on sections from two different regions of 5-week-old rat aorta (of both sexes). By contrast, cultured smooth muscle cells isolated from similar aortic media and passaged 5 to 7 times exhibited specific binding.
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