Halichondria panicea (Porifera, Demospongiae) Reparative Regeneration: An Integrative Approach to Better Understand Wound Healing

Abstract

Sponges have a remarkable capacity to rapidly regenerate in response to injury. In addition, sponges rapidly renew their aquiferous system to maintain a healthy. This study describes the reparative regeneration in the cold-water demosponge Halichondria panicea. The wide range of methods allow us to make a comprehensive analysis of mechanisms, which contribute to the regeneration in this species, including morphogenetic process, cell proliferation, apoptosis and cytotoxicity. The regeneration in H. panicea includes three main stages: internal milieu isolation, wound healing - epithelization, and restoration of damaged structures. The main morphogenetical mechanisms of regeneration are epithelial-to-mesenchymal transition during the first 12 h post operation (hpo) followed by blastema formation and mesenchymal-to-epithelial transformation leading to the restoration of damaged structures. These processes can be explained by active cell dedifferentiation and transdifferentiation, participation of resident pluripotent cells (archaeocyte-like cells and choanocytes), by migration of pluripotent cells (archaeocyte-like cells), and by activation of proliferation and apoptosis. The rate of apoptosis becomes homogeneous in regeneration area and in intact tissues at 12 hpo at a significantly higher rate than at 0 hpo. The reduction of sponge toxicity at 6 hpo looks like a necessary step for activation of repair processes. However, after 24 hpo, the toxicity exceeded the initial (0 hpo) level. At 96 hpo, the aquiferous system is completely restored. The ability for rapid wound epithelialization, as well as the morphological and functional restoration of damaged tissues, can be considered as a form of sponge's adaptation to extreme conditions in cold shallow water, acquired in the course of evolution.