Development and epithelial organisation of muscle cells in the sea anemone Nematostella vectensis

Abstract

IntroductionNematostella vectensis, a member of the cnidarian class Anthozoa, has been established as a promising model system in developmental biology, but while information about the genetic regulation of embryonic development is rapidly increasing, little is known about the cellular organization of the various cell types in the adult. Here, we studied the anatomy and development of the muscular system of N. vectensis to obtain further insights into the evolution of muscle cells.ResultsThe muscular system of N. vectensis is comprised of five distinct muscle groups, which are differentiated into a tentacle and a body column system. Both systems house longitudinal as well as circular portions. With the exception of the ectodermal tentacle longitudinal muscle, all muscle groups are of endodermal origin. The shape and epithelial organization of muscle cells vary considerably between different muscle groups. Ring muscle cells are formed as epitheliomuscular cells in which the myofilaments are housed in the basal part of the cell, while the apical part is connected to neighboring cells by apical cell-cell junctions. In the longitudinal muscles of the column, the muscular part at the basal side is connected to the apical part by a long and narrow cytoplasmic bridge. The organization of these cells, however, remains epitheliomuscular. A third type of muscle cell is represented in the longitudinal muscle of the tentacle. Using transgenic animals we show that the apical cell-cell junctions are lost during differentiation, resulting in a detachment of the muscle cells to a basiepithelial position. These muscle cells are still located within the epithelium and outside of the basal matrix, therefore constituting basiepithelial myocytes. We demonstrate that all muscle cells, including the longitudinal basiepithelial muscle cells of the tentacle, initially differentiate from regular epithelial cells before they alter their epithelial organisation.ConclusionsA wide range of different muscle cell morphologies can already be found in a single animal. This suggests how a transition from an epithelially organized muscle system to a mesenchymal could have occurred. Our study on N. vectensis provides new insights into the organisation of a muscle system in a non-bilaterian organism.

Diversity of Cnidarian Muscles: Function, Anatomy, Development and Regeneration

“…(B) Epitheliomuscular cell type diversity in Cnidaria. After Krasińska (1914) and Doumenc (1979) in Seipel and Schmid (2006), and Jahnel et al (2014). …”

“…A recent description of the muscular system of the sea anemone Nematostella vectensis (Figures 4Ac,c') highlighted the existence of at least three different epitheliomuscular cell types (Figure 4B; Jahnel et al, 2014). Type I classical epitheliomuscular cells and type II epitheliomuscular cells, with elongated cytoplasmic bridges, constitute mainly the longitudinal component of the muscular system such as the parietal and retractor muscles (Figures 4A,B; Jahnel et al, 2014). Conversely, type III epitheliomuscular cells are basiepithelial muscle cells and are primarily encountered in the ectoderm of the tentacles.…”

“…In many anthozoan groups, the retractor muscles are arranged in a bilateral manner along the secondary body axis (called the directive axis), and constitute one of the landmarks of bilateral symmetry in these organisms (e.g., in Nematostella : Jahnel et al, 2014; Leclère and Rentzsch, 2014). Ectodermal muscles are for most anthozoans confined to the tentacles and the oral disc, except in some Ceriantharia, Antipatharia and Scleractinia that have longitudinal muscles in the body column ectoderm (Chevalier and Beauvais, 1987; Doumenc and Van Praët, 1987; Herberts, 1987; Tiffon, 1987; Van Praët et al, 1987).…”

Too many ways to make a muscle: Evolution of GRNs governing myogenesis

“…Due to the strong ultrastructural similarities of striated muscles and the conserved expression of regulatory and structural genes, a common evolutionary origin has been often considered (Muller et al, 2003;Seipel and Schmid, 2005;Spring et al, 2002). However, the sister group of bilaterians, Cnidaria, possess only ectodermally (tentacle longitudinal muscle) and endodermally derived epitheliomuscular and basiepithelial muscle cells (Jahnel et al, 2014), which differentiate from regular epithelial cells; therefore are epithelio-muscle-cells (EMC) and not true (fibre) muscles. Moreover, the sister group of all metazoans, Ctenophora (Ryan et al, 2013), appear to possess a fibre muscle cell type that significantly differs from the ones found in triploblastic animals.…”

Antagonistic BMP–cWNT signaling in the cnidarian Nematostella vectensis reveals insight into the evolution of mesoderm

“…The presence of an ancestral heart-field specification GRN kernel in the diploblastic cnidarian Nematostella provides valuable evolutionary insights into the origin of mesoderm. Diploblastic nonbilaterians lack a distinct mesodermal tissue even though the genome possesses a complex set of bilterian mesodermal orthologs (54) that are expressed in the gastrodermis (6), and cnidarian polyps have myoepithelial cells in the gastrodermis (55,56). The Nematostella muscular system is divided into a body column and a tentacle system.…”