Transdifferentiation and mesenchymal‐to‐epithelial transition during regeneration in Demospongiae (Porifera)

Abstract

Origin and early evolution of regeneration mechanisms remain among the most pressing questions in animal regeneration biology. Porifera have exceptional regenerative capacities and, as early Metazoan lineage, are a promising model for studying evolutionary aspects of regeneration. Here, we focus on reparative regeneration of the body wall in the Mediterranean demosponge Aplysina cavernicola. The epithelialization of the wound surface is completed within 2 days, and the wound is completely healed within 2 weeks. The regeneration is accompanied with the formation of a mass of undifferentiated cells (blastema), which consists of archaeocytes, dedifferentiated choanocytes, anucleated amoebocytes, and differentiated spherulous cells. The main mechanisms of A. cavernicola regeneration are cell dedifferentiation with active migration and subsequent redifferentiation or transdifferentiation of polypotent cells through the mesenchymal‐to‐epithelial transformation. The main cell sources of the regeneration are archaeocytes and choanocytes. At early stages of the regeneration, the blastema almost devoid of cell proliferation, but after 24 hr postoperation (hpo) and up to 72 hpo numerous DNA‐synthesizing cells appear there. In contrast to intact tissues, where vast majority of DNA‐synthesizing cells are choanocytes, all 5‐ethynyl‐2′‐deoxyuridine‐labeled cells in the blastema are mesohyl cells. Intact tissues, distant from the wound, retains intact level of cell proliferation during whole regeneration process. For the first time, the apoptosis was studied during the regeneration of sponges. Two waves of apoptosis were detected during A. cavernicola regeneration: The first wave at 6–12 hpo and the second wave at 48–72 hpo.

Grazing results in mobilization of spherulous cells and re-allocation of secondary metabolites to the surface in the spongeAplysina aerophoba

“…aerophoba showed a similar cellular response, peaking also after 1 day, in both mechanical damage and grazing treatments, even if in our study wounding damage was stronger than in Ereskovsky et al 40 . Therefore, the mobilisation of spherulous cells may be a common process involved in sponge defence, but also provide structure or energy for rapid regeneration.…”

“…We also observed the shedding of spherulous cells upon damage and their release into aquiferous canals; thus, spherulisation may be also occurring in A. aerophoba. Recently, Ereskovsky et al 40 described the accumulation of spherulous cells at the wound, 1 day after applying a small excision, as part of the regenerative blastema in Aplysina cavernicola. A.…”

“…Such reallocation would have the advantage of using available resources to enhance the protection of the area that has now been signalled as most vulnerable to damage, fitting the postulates of Optimal Grazing by the specialist sea slug T. perversa triggers a wound-like response in the sponge A. aerophoba. This response consisted of a local accumulation of spherulous cells, which are likely directed to enhanced regeneration 40 as well as defend the exposed wound against invading microbes and predators 25 . After one day, coinciding with the peak of spherulous cell accumulation, brominated secondary metabolites are re-.…”

Marine biomimetics: bromotyrosines loaded chitinous skeleton as source of antibacterial agents

“…The indisputable advantages of the Verongiida sponges in comparison with other demosponges include their unique ability to regenerate tissues [ 46 , 47 ], which determines the progress in their cultivation using marine farming methods [ 48 – 51 ]. These marine sponges are now considered as renewable sources of both biological materials (i.e.…”

Caspase dependent apoptosis is required for anterior regeneration in Aeolosoma viride and its related gene expressions are regulated by the Wnt signaling pathway

“…This is similar to what had been observed in the regenerating fragments of planarian, in which an initial apoptotic response peaked at approximately 1 to 4 hours after injury, and is followed by a second systemic response that peaked 3 days after amputation 43 . The two rounds of apoptosis during regeneration was also observed in Porifera Aplysina cavernicola and the caudal regeneration of zebrafish 41,44,45 .…”