Regeneration of the enteric nervous system in the sea cucumberHolothuria glaberrima

Abstract

Among higher metazoans, echinoderms exhibit the most impressive capacity for regeneration. Holothurians, or sea cucumbers, respond to adverse stimuli by autotomizing and ejecting their visceral organs, which are then regenerated. Neuronal fibers and cell bodies are present within the viscera, but previous regeneration studies have not accounted for the nervous component. We used light microscopic immunocytochemistry and ultrastructural studies to describe the regeneration of the enteric nervous system in the sea cucumber Holothuria glaberrima. This study provides evidence that the enteric nervous system of this echinoderm regenerates after evisceration and that in 3–5 weeks the regenerated system is virtually identical to that of noneviscerated animals. The regeneration of the enteric nervous system occurs parallel to the regeneration of other organ components. Nerve fibers and cells are observed within the mesenterial thickenings that give rise to the new intestine and within the internal connective tissue prior to lumen formation. We also used bromodeoxyuridine incorporation to show that proliferation of the neuronal population occurs in the regenerating intestine. The regeneration of the nervous system commands high interest because members of the closely related phylum Chordata either lack or have a very limited capacity to regenerate their nervous system. Thus, holothurians provide a model system to study enteric nervous system regeneration in deuterostomes. J. Comp. Neurol. 406:461–475, 1999. © 1999 Wiley‐Liss, Inc.

Myogenesis during holothurian intestinal regeneration

“…Animals were dissected at various days post-evisceration (dPE). Further details of animal upkeep and dissection were as given previously (García-Arrarás et al 1998, 1999.…”

“…Digestive tract regeneration implies a series of coordinated events that can be used to study the process of organogenesis in adult organisms. Our laboratory has been studying the process of intestinal regeneration in the sea cucumber Holothuria glaberrima for the past few years (García-Arrarás et al 1998, 1999García-Arrarás and Greenberg 2001;Quiñones et al 2002). Data from our group have shown that intestinal regeneration begins from a thickening of the free edges of the mesenteries and involves processes of cell migration from the esophageal and cloacal remnants and possibly from the mesentery itself.…”

“…Previous studies have focused on the cellular events that form the mucosal (luminal epithelium) and submucosal (internal connective tissue) layers and the enteric nervous system (García-Arrarás et al 1998, 1999. We have shown that the muscle layer, like other intestinal tissues, is present from early in the regenerating structure and is organized, in the 4-week regenerate, in a pattern that closely resembles the non-eviscerated organs (García-Arrarás et al 1998).…”

Visceral regeneration in the crinoid Antedon mediterranea: basic mechanisms, tissues and cells involved in gut regrowth

“…The phenomenon of visceral regeneration was studied more exstensively in holothuroids, since the first half of the 20th century [31][32][33][34][35], and in asteroids by Anderson [36][37][38]. With regard to visceral regeneration in echinoderms, the most controversial topic has been the origin of the luminal epithelium.…”

Development of respiratory trees in the holothurian Apostichopus japonicus (Aspidochirotida: Holothuroidea)

“…However, recent immunocytochemical and transmission electron microscopy studies revealed the presence of nerve cells in the luminal epithelium of the gut (García-Arrarás et al 1999). In A. japonicus, processes of nerve cells were found in the lining of the cloaca (Dolmatov and Ginanova 2009).…”