Derivation of muscles of the Aristotle’s lantern from coelomic epithelia

Abstract

Transmission electron microscopy was employed to study structural changes in the lantern muscles occurring during the transition from young to adult in the sea urchin Strongylocentrotus nudus. A comparative examination of four major lantern muscles (compass depressors, compass elevators, protractors and retractors) suggests that myogenesis involves four consecutive stages. At the initial stage, the muscles show the organization of a mesentery delimited by pseudostratified coelomic epithelia, which are composed of peritoneal cells spanning the whole height of each epithelium, and myoepithelial cells, which are clustered together to fill the interstices between the basal processes of the peritoneal cells. During the next stage, the clusters of myoepithelial cells partly "sink" into the underlying connective tissue. At the third stage of muscularization, the myoepithelial cells increase in size and further invade the underlying connective tissue so that the myoepithelium splits into an apical peritoneal layer and a deeper mass of myoepithelial cells immersed in the connective tissue. However, these two layers are connected by a continuous basal lamina. This is thus the first description of an intermediate developmental stage between pseudostratified myoepithelim and genuine echinoderm muscles. For such a myoepithelium, we propose the term "immersed myoepithelium". At the most advanced stage of myogenesis, the myocytes detach completely from the epithelium to form subepithelial muscle bundles. Myogenesis in the sea urchin takes a long time during which continuous myogenic differentiation occurs in the coelomic epithelium and the newly formed myocytes and associated neurons penetrate into the underlying connective tissue.

Echinoderms: Potential Model Systems for Studies on Muscle Regeneration

“…In addition, the coelomic epithelium contains much nervous tissue [10, 14, 17-19]. Nerve cells and their processes are located in-between peritoneal and myoepithelial cells.…”

“…Muscle bundles contain no connective tissue and most of the area is filled with myocyte processes. Basal bodies (kinetosomes) of cilia can sometimes be observed in myocytes [19]. …”

“…Connective tissue also comprises fibroblasts, nerve cells and different coelomocytes. In some muscles of the Aristotle's lantern, juxtaligamental-like cells embedded into the connective tissue between the muscle bundles were observed [19, 25]. Such a combination of contractile cells and mutable connective tissue is very interesting from both physiological and evolutionary points of view.…”

“…Jensen [41] revealed SLS in coelomic epithelium of dorsal hemal vessel in the holothurian Parastichopus tremulus . Later on, SLS were found in the muscles of Aristotle's lantern in the adults of the sea urchin Strongylocentrotus nudus [19]. …”

“…On the other hand, the formation of SLS might not be solely due to regeneration events, but might well be part of a housekeeping process that serves to recycle the molecular machinery of cells that have undergone cell death or damage. This might explain the finding of SLSs in the normal tissues of echinoderms [19, 39-41]. …”