Light and Electron Microscopy of the Bulbus arteriosus of the European Eel <i>(Anguilla anguilla)</i>

Abstract

The bulbus arteriosus of teleost fish acts as an elastic reservoir that dilates during ventricular systole to store a large part of the cardiac stroke volume. Despite its functional importance, the knowledge of the structure of the bulbus wall is still fragmentary. We have undertaken a series of studies in order to establish a general morphological plan of the teleost bulbus. The bulbus arteriosus of the European eel is studied here by means of conventional light, and transmission and scanning electron microscopy. The inner surface of the bulbus wall is irregular due to the presence of branching ridges that flatten and disappear toward the ventral aorta. The ridge surface is covered by flattened endocardial cells that show moderately dense bodies. In the ridge tissue, cells near the endocardium are mostly undifferentiated and appear isolated in a loose filamentous matrix. Ridge cells progressively cluster toward the middle layer, become surrounded by a dense matrix, and adopt characteristics typical of smooth muscle cells. This suggests the existence of a differentiation gradient. The middle layer is formed by typical smooth muscle cells embedded in a meshwork matrix that contains thin and thick filaments. Stretching of this meshwork suggests an active role of smooth muscle cells in bulbus wall dynamics. Furthermore, large areas of the extracellular space are occupied by elastin-like material. The amount of this material decreases toward the external layer. Collagen is demonstrated across the entire thickness of the bulbus wall, its amount and organization increasing from the inner toward the outer bulbus surface. The existence of matrix gradients should progressively increase wall strength, maintaining bulbus dilation within safe physiological parameters. The epicardium is formed by flattened cells that contain numerous pinocytotic vesicles, suggesting an active interchange of solutes with the pericardial cavity.

Cardiac morphology and blood pressure in the adult zebrafish

“…The bulbus arteriosus of different species each presents unique and specific characteristics that make it different from the bulbus among other species of the same class (Icardo et al, 1999a(Icardo et al, ,b, 2000. Both conus and truncus arise in early heart development.…”

Conus arteriosus of the teleost heart: Dismissed, but not missed

“…It is a single, thick-walled segment whose main function is to act as an elastic reservoir or "windkessel": the bulbus dilates to receive the systolic volume and subsequently allows gradual liberation of the blood volume and protects the delicate gill vasculature. Despite the existence of a wide variety of structural organizations (Icardo et al, 1999a(Icardo et al, , 1999b(Icardo et al, , 2000a(Icardo et al, , 2000b, the bulbus seems to perform the same function in all species. Finally, three sets of cardiac valves are deployed at the sinoatrial, atrioventricular, and bulboventricular regions (for review, see Yamauchi, 1980;Santer, 1985;Satchell, 1991;Farrell and Jones, 1992;Burggren et al, 1997).…”

The eel heart: multilevel insights into functional organ plasticity

“…The bulbus arteriosus of the eel shows, in the inner wall, an irregular surface because of the presence of branching ridges, covered by flattened EE cells that contain dense bodies with a secretory function (Icardo et al, 2000). The middle layer is formed by smooth muscle cells, embedded in a meshwork matrix containing thin and thick filaments (Icardo et al, 2000).…”

“…A receptor with high CNP affinity, presumably NPRB, was also reported in the endothelial and epicardial layers of the bulbus arteriosus of A. anguilla (Cerra et al, 1996), where it may mediate a CNPdependent modulation of the bulbar hemodynamics (e.g. the Windkessel function) (see Icardo et al, 2000).In all vertebrates, the primary stimulus for acute atrial NP release is the hypervolemia-induced stretch (Ruskoaho, 1992). Once released, NPs activate complex signaling networks that control heart-vessel and volume-ion homeostasis at various levels [for references, see Tota et al (Tota et al, 2010)].…”

“…Nervous and humoral mechanisms may also contribute to compensate for ventricular heterogeneity. In fact, it is important to note that eel ventricular myocardiocytes of both the spongiosa and the compacta express an 'eNOS-like' isoform [for terminology and references in fish, see Imbrogno et al (Imbrogno et al, 2011)] that, by linking multiple extracellular signals that converge to regulate eNOS activity in the cells, acts as a spatio-temporal integrator of the heart function, as discussed below.The bulbus arteriosus of the eel shows, in the inner wall, an irregular surface because of the presence of branching ridges, covered by flattened EE cells that contain dense bodies with a secretory function (Icardo et al, 2000). The middle layer is formed by smooth muscle cells, embedded in a meshwork matrix containing thin and thick filaments (Icardo et al, 2000).…”