Background: Tissues of multicellular animals are maintained due to a tight balance between cell proliferation and programmed cell death. Phylum Porifera is an early branching group of metazoans essential to understanding the key mechanisms of tissue homeostasis. This paper is dedicated to the comparative analysis of proliferation and apoptosis in intact tissues of two sponges belonging to distinct Porifera lineages, Halisarca dujardinii (class Demospongiae) and Leucosolenia variabilis (class Calcarea). Results: Labeled nucleotides EdU and anti-phosphorylated histone 3 antibodies reveal a considerable number of cycling cells in intact tissues of both species. The main type of cycling cells are choanocytes -flagellated cells of the aquiferous system. The rate of proliferation remains constant in areas containing choanoderm. Cell cycle distribution assessed by the quantitative DNA stain reveals the classic cell cycle distribution curve. During EdU pulse-chase experiments conducted in H. dujardinii, the contribution of the choanocytes to the total amount of EdU-positive cells decreases, while contribution of the mesohyl cells increases. These findings could indicate that the proliferation of the choanocytes is not solely limited to the renewal of the choanoderm, and that choanocytes may participate in the general cell turnover through migration. The number of apoptotic cells in intact tissues of both species is insignificant. In vivo studies in both species with TMRE and CellEvent Caspase-3/7 indicate that apoptosis might be independent of mitochondrial outer membrane permeabilization. Conclusions: A combination of confocal laser scanning microscopy and flow cytometry provides a quantitative description of cell turnover in intact sponge tissues. Intact tissues of H. dujardinii (Demospongiae) and L. variabilis (Calcarea) are highly proliferative, indicating either high rates of growth or cell turnover. Although the number of apoptotic cells is low, apoptosis could still be involved in the regular cell turnover..
The crucial step in any regeneration process is epithelization, i.e. the restoration of epithelium structural and functional integrity. Epithelialization requires cytoskeletal rearrangements, primarily of actin filaments and microtubules. Sponges (phylum Porifera) are early branching metazoans with pronounced regenerative abilities. Calcareous sponges have a unique step during regeneration: formation of a temporary structure, regenerative membrane which initially covers a wound. It forms due to the morphallactic rearrangements of exo- and choanoderm epithelial-like layers. The current study quantitatively evaluates morphological changes and characterises underlying actin cytoskeleton rearrangements during regenerative membrane formation in asconoid calcareous sponge Leucosolenia variabilis, through a combination of time-lapse imaging, immunocytochemistry, and confocal laser scanning microscopy. Regenerative membrane formation has non-linear stochastic dynamics with numerous fluctuations. The pinacocytes at the leading edge of regenerative membrane form a contractile actomyosin cable. Regenerative membrane formation either depend on its contraction or being coordinated through it. The cell morphology changes significantly during regenerative membrane formation. Exopinacocytes flatten, their area increases, while circularity decreases. Choanocytes transdifferentiate into endopinacocytes, losing microvilli collar and flagellum. Their area increases and circularity decreases. Subsequent redifferentiation of endopinacocytes into choanocytes is accompanied by inverse changes in cell morphology. All transformations are based on actin filament rearrangements similar to those characteristic of higher metazoans. Altogether, we provide here a qualitative and quantitative description of cell transformations during reparative epithelial morphogenesis in a calcareous sponge.
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