Articles

The Fine Structure of the Vascular System of Amnphioxus: Implications in the Development of Lymphatics and Fenestrated Blood Capillaries

Author
  • J.R. Casley-Smith

Abstract

The blood and lymph vessels of a few mammals have been quite extensively studied by electron microscopy (3, 4, 5, 15, 22, 23, 2.J). By contrast, in lower animals even the blood vessels have been relatively neglected, to say nothing of the lymphatics. The few studies which have been made indicate that in reptiles (2), amphibians {31) and teleosts (15) the blood vessels are similar to those in the mammals. In the elasmobranchs, however, the interendothclial junctions appear less firmly closed, the basement membranes are more tenuous and the venous vessels are intermittently attached to the connective tissue by fine fibrils (11). These three features are strongly reminiscent of mammalian lymphatics and arc probably associated with the low blood pressure of these fish, which is sometimes "negative" in the venous vessels (13, 30).

It is of great interest that even in the fairly primitive elasmobranchs, those which lack true lymphatics (32) still have fenestrated capillaries in some organs (11). There is evidence that the fenestrae allow the entry of large molecules and fluid into the venous limbs of capillaries (7, 8, 11), both in these animals and in the higher vertebrates, where they are very common in some regions. They may well supplement the lymphatic system, especially in relatively motionless regions, or where the lymphatics are infrequent. It appears, however, that the hagfishes lack fenestrae, but have some open junctions in their endocrine capillaries (9a). Thus their blood capillaries have some features in common with the lymphatics of higher vertebrates. (Neither open junctions nor fenestrae seem to be present in the cerebral capillaries of the myxines (27), but we have no information about the rest of their vessels.)

The invertebrates have had even fewer studies of their vasculature. Only the cephalopocis (1) and earth-worms {17, 19, 20) have had any detailed description. The crustaceans have been briefly mentioned (19) and the leech's neural "endothelium" has been described (12), but it is evident that this is very unusual in site, structure and function. In their major vessels the cephalopods have pericytes with myofibrils, thick basement membranes and endothelium which is nearly continuous, but with a few open junctions. In the more peripheral vessels, the endothelial cells gradually come to lie further and further apart, until there are quite wide gaps 1- 10μ between them. However, the basement membranes are always present, as is a complete investment of pericytes - which come to lack the myofibrils. The pericytes have closed junctions which, though they are not "tight junctions" (16), contain dense material which may present a considerable barrier to the passage of large molecules. The higher blood pressures and plasma protein concentrations in the cephalopods have obviously caused developments analogous to those in the higher vertebrates, but differing in detail. The situation in the more primitive earthworm is similar, but the endothelium is discontinuous even in the major vessels (17, 19, 20). (A point of nomenclature should be noted here: Workers on the earthworm have called the pericytes "endothelium", or "myoendothelium" and considered the endothelium to be "amoebocytes lying on the basement membrane", which they considered lay on the "lumenal side of the endothelium." It was pointed out by Barber and Grazialdei (1), however, that the true amoebocytes arc morphologically, and presumably functionally, distinct from the true endothelium since they contain many granules, more mitodlondria, etc. Hence they considered that there was true endothelium - though often very discontinuous - inside the basement membrane, as in the mammals, and that it was pericytes which contained the myofibrils.)

In order to help bridge the gap between the invertebrates and the vertebrates, it was decided to study amphioxus, one of the most primitive of chordates. Its low blood pressure and plasma protein levels. and generally primitive development might be expected to be associated with vascular structural and functional peculiarities. These would not only be interesting in themselves, but, by their contrasts, might help to clarify what is found in the higher vertebrates. In particular, the way in which large molecules enter these vessels from the tissues would be of significance both for the study of the lymphatic system, and of the fenestrated blood capillaries.

The vascular structure of amphioxus detectable with the light microscope has been well reviewed by Kampmeier (21), whose description has been used as the basis for this paper. Briefly, there is a contractile ventral aorta, which pumps blood through the gill arches and nephridiae, which then flows into the pair of dorsal aortae. These merge on the stomach and intestine and supply the intestinal sinusoids, which run forwards on the "liver". Some of these converge into the contractile subintestinal vein, which supplies the "liver" sinusoids, which in turn flow into the hepatic vein, and thence into the ventral aortae. In addition to this branchioenteric circulation, the dorsal aortae supplies sinusoids to the segments of the body wall, which flow into the "cardinal" veins. (I shall use "central" or "major" vessel to include the aortae and the main veins; "peripheral" vessels refers to the rest of the vessels, which are basically sinusoids, i.e. they have wide, irregular, often flattened lumens, with - electron microscopically - gaps between the endothelial cells.) Kampmeier mentions a number of problems which have been answered in the present work, viz. the nature of the sinusoids, whether only the aortae have endothelial linings, and the nature of the "lymph" spaces. The way in which large molecules and particles enter the sinusoids of the gut and the vessels of the body wall has also been studied.

How to Cite:

Casley-Smith, J., (1971) “The Fine Structure of the Vascular System of Amnphioxus: Implications in the Development of Lymphatics and Fenestrated Blood Capillaries”, Lymphology 4(3), 79-94.

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Published on
29 Sep 1971
Peer Reviewed