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Genes (Basel)
2021 Feb 10;122:. doi: 10.3390/genes12020250.
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Molecular Aspects of Regeneration Mechanisms in Holothurians.
Dolmatov IY
.
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Holothurians, or sea cucumbers, belong to the phylum Echinodermata. They show good regenerative abilities. The present review provides an analysis of available data on the molecular aspects of regeneration mechanisms in holothurians. The genes and signaling pathways activated during the asexual reproduction and the formation of the anterior and posterior parts of the body, as well as the molecular mechanisms that provide regeneration of the nervous and digestive systems, are considered here. Damage causes a strong stress response, the signs of which are recorded even at late regeneration stages. In holothurian tissues, the concentrations of reactive oxygen species and antioxidant enzymes increase. Furthermore, the cellular and humoral components of the immune system are activated. Extracellular matrix remodeling and Wnt signaling play a major role in the regeneration in holothurians. All available morphological and molecular data show that the dedifferentiation of specialized cells in the remnant of the organ and the epithelial morphogenesis constitute the basis of regeneration in holothurians. However, depending on the type of damage, the mechanisms of regeneration may differ significantly in the spatial organization of regeneration process, the involvement of different cell types, and the depth of reprogramming of their genome (dedifferentiation or transdifferentiation).
Figure 1. Scheme of regeneration of internal organs after fission in Cladolabes schmeltzii. (a) C. schmeltzii during fission. (b) Anterior fragment just after fission. (c) Formation of gut and cloaca in anterior fragment. (d) Formation of respiratory trees in anterior fragment. (e) Posterior fragment just after fission. (f) Formation of aquapharyngeal bulb (AB) and gut anlage in posterior fragment. (g) Posterior fragment with regenerated internal organs. a, anterior part; ab, aquapharyngeal bulb; ag, anterior anlage of gut; bw, body wall; cl, cloaca; g, gut; gn, gonad; lmb, longitudinal muscle band; p, posterior part; pg, posterior anlage of gut; rt, respiratory tree; t, tentacles.
Figure 2. Scheme of regeneration of anterior part of digestive system after posterior evisceration. (a) Anterior part of holothurian just after evisceration; (b) Longitudinal section of the region of the esophagus remnant and mesentery, which is marked by the rectangle in (a). (c) Transverse section of the region of mesentery which is marked by solid line (1) in (b). (d) Transverse section of the region of esophagus remnant which is marked by solid line (2) in (b). (e) Anterior part of holothurian on third day post-evisceration; (f) Longitudinal section of the region of the esophagus remnant and connective tissue thickening, which is marked by the rectangle in (e). (g) Transverse section of the region of connective tissue thickening which is marked by solid line (1) in (f). (h) Transverse section of the region of esophagus remnant which is marked by solid line (2) in (f). (i) Anterior part of holothurian on seventh day post-evisceration; (j) Longitudinal section of the region of gut anlage, which is marked by the rectangle in (i). (k) Transverse section of the region of growing end of anterior gut anlage which is marked by solid line (1) in (j). (l) Transverse section of the region of growing end of anterior gut anlage which is marked by solid line (2) in (j). ab, aquapharyngeal bulb; bw, body wall; ce, coelomic epithelium; ct, connective tissue; ctt, connective tissue thickening; dc, de-differentiated coelomic epithelial cell; dde, de-differentiated enterocyte; dge, de-differentiating enterocyte; dm, de-differentiating myoepithelial cell; dp, de-differentiating peritoneal cell; en, enterocyte; er, esophagus remnant; ga, anterior gut anlage; le, luminal epithelium; m, mesentery; my, myoepithelial cell; nc, nerve cell; pc, peritoneal cell; sls, myofilaments grouped in spindle-like structures.
Figure 3. Schematic representation of morphological and molecular events during visceral regeneration after posterior evisceration. Timeline is represented by hours and days of regeneration after evisceration.
Figure 4. Scheme of regeneration of anterior part of digestive system after anterior evisceration. (a) Anterior part of holothurian just after evisceration; (b) Longitudinal section of the region of the mesentery, which is marked by the rectangle in (a). (c) Transverse section of the region of mesentery which is marked by solid line in (b). (d) Anterior part of holothurian on third day post-evisceration; (e) Longitudinal section of the region of the tissue thickening, which is marked by the rectangle in (d). (f) Transverse section of the region of connective tissue thickening which is marked by solid line in (e). (g) Anterior part of holothurian on seventh day post-evisceration; (h) Longitudinal section of the region of gut anlage, which is marked by the rectangle in (g). (i) Transverse section of the site of embedding of coelomic epithelial cells into connective tissue thickening which is marked by solid line in (h). ab, aquapharyngeal bulb; bw, body wall; ce, coelomic epithelium; ct, connective tissue; ctt, connective tissue thickening; dc, de-differentiated coelomic epithelial cell; dm, de-differentiating myoepithelial cell; dp, de-differentiating peritoneal cell; ga, anterior gut anlage; m, mesentery; my, myoepithelial cell; nc, nerve cell; pc, peritoneal cell; sls, myofilaments grouped into spindle-like structures, tc, coelomic epithelial cell during transdifferentiation.
Figure 5. Schematic representation of morphological and molecular events during visceral regeneration after anterior evisceration. Timeline is represented by hours and days of regeneration after evisceration. Horizontal dotted line means no data.