More than a simple epithelial layer: multifunctional role of echinoderm coelomic epithelium

Abstract

In echinoderms, the coelomic epithelium (CE) is reportedly the source of new circulating cells (coelomocytes) as well as the provider of molecular factors such as immunity-related molecules. However, its overall functions have been scarcely studied in detail. In this work, we used an integrated approach based on both microscopy (light and electron) and proteomic analyses to investigate the arm CE in the starfish Marthasterias glacialis during different physiological conditions (i.e., non-regenerating and/or regenerating). Our results show that CE cells share both ultrastructural and proteomic features with circulating coelomocytes (echinoderm immune cells). Additionally, microscopy and proteomic analyses indicate that CE cells are actively involved in protein synthesis and processing, and membrane trafficking processes such as phagocytosis (particularly of myocytes) and massive secretion phenomena. The latter might provide molecules (e.g., immune factors) and fluids for proper arm growth/regrowth. No stem cell marker was identified and no pre-existing stem cell was observed within the CE. Rather, during regeneration, CE cells undergo dedifferentiation and epithelial-mesenchymal transition to deliver progenitor cells for tissue replacement. Overall, our work underlines that echinoderm CE is not a “simple epithelial lining” and that instead it plays multiple functions which span from immunity-related roles as well as being a source of regeneration-competent cells for arm growth/regrowth.

Regeneration of Starfish Radial Nerve Cord restores animal mobility and unveils a new coelomocyte population

“…Similarly, a moderate hypertrophy was observed in the nearby haemal sinus, a non-coelomic system of lacunae also involved in immune functions, that contain coelomocytes as well. This phenomenon could be explained by the overuse of the coelomic/coelomic-derived canals for the transport of both molecules and immune or other migrating cells from the neighbor tissues, as suggested by other authors (Hernroth et al 2010;Guatelli et al 2022). The changes in coelomocyte composition that we found during the period of RNC regeneration and discussed below are perfectly in line with this idea.…”

“…The origin of the P3 coelomocyte remains unknown. The axial organ (Leclerc and Bajelan 1992), the Tiedemann’s bodies (Kaneshiro and Karp 1980), the hemal organs (Ferguson 1966), and the coelomic epithelium (Guatelli et al 2022; Sharlaimova et al 2021; Bosshe and Jangoux 1976) were suggested as candidates for the so-called hematopoietic tissue in starfish. Nonetheless, this last tissue is, nowadays, the most accepted tissue candidate to carry out the mentioned functions.…”

“…A particular relevant issue here is understanding the source of circulating coelomocytes, and their constituent populations. Initial microscopy analysis showed that the coelomic epithelial cells share similar ultrastructural features with the circulating coelomocytes (Holm et al 2008; Gorshkov et al 2009; Sharlaimova et al 2010), in particular, with thrombocytes-like cells (Guatelli et al 2022). Moreover, proteomic analysis showed the presence of some common proteins in the coelomic epithelium and the circulating coelomocytes of M. glacialis , including proteins related with the cell motility, which would suggest the migratory behaviour of cells from the coelomic epithelium, moving from this to the coelomic cavity.…”

“…This would point to the direct involvement of coelomic epithelial-derived cells to the rebuilding of regenerating structures. However, a direct release of free wandering coelomocytes from the apical part of the coelomic epithelium towards the coelomic lumen was never observed, either in non–regenerating or in regenerating conditions (Guatelli et al 2022). Alternatively, and as pointed out above, coelomic epithelium could be involved in the hypertrophy of the coelomic and coelomic-derived canals by providing immune response through immune factors.…”

Morphological and Physiological Aspects of Mutable Collagenous Tissue at the Autotomy Plane of the Starfish Asterias rubens L. (Echinodermata, Asteroidea): An Echinoderm Paradigm

“…The coelothelium is a pseudostratified myoepithelium with both apical peritoneocytes and subapical, longitudinally orientated myocytes attached to a basal lamina. On the dorsal side of this basal lamina there are several tissue layers that include circumferentially orientated myocytes and have been interpreted as belonging to the dermis [ 28 ], although in A. rubens they are separated from the densely fibrous layer of the inner dermis (see below) by a space delimited by a thin layer of squamous cells ( Figure 4 B,C). In the midline of the dorsalmost body wall, the longitudinal myocyte layer is greatly expanded to form the apical muscle ( Figure 2 and Figure 4 G).…”