Putative stem cells in the hemolymph and in the intestinal submucosa of the solitary ascidian Styela plicata

Abstract

BackgroundIn various ascidian species, circulating stem cells have been documented to be involved in asexual reproduction and whole-body regeneration. Studies of these cell population(s) are mainly restricted to colonial species. Here, we investigate the occurrence of circulating stem cells in the solitary Styela plicata, a member of the Styelidae, a family with at least two independent origins of coloniality.ResultsUsing flow cytometry, we characterized a population of circulating putative stem cells (CPSCs) in S. plicata and determined two gates likely enriched with CPSCs based on morphology and aldehyde dehydrogenase (ALDH) activity. We found an ALDH + cell population with low granularity, suggesting a stem-like state. In an attempt to uncover putative CPSCs niches in S. plicata, we performed a histological survey for hemoblast-like cells, followed by immunohistochemistry with stem cell and proliferation markers. The intestinal submucosa (IS) showed high cellular proliferation levels and high frequency of undifferentiated cells and histological and ultrastructural analyses revealed the presence of hemoblast aggregations in the IS suggesting a possible niche. Finally, we document the first ontogenetic appearance of distinct metamorphic circulatory mesenchyme cells, which precedes the emergence of juvenile hemocytes.ConclusionsWe find CPSCs in the hemolymph of the solitary ascidian Styela plicata, presumably involved in the regenerative capacity of this species. The presence of proliferating and undifferentiated mesenchymal cells suggests IS as a possible niche.

<p>From Primary Cell and Tissue Cultures to Aquatic Invertebrate Cell Lines: An Updated Overview</p> <p>&nbsp;</p>

“…We have previously performed extensive lectin profiling of ascidian (Ciona intestinalis) larvae focusing on their sensory adhesive organs (papillae, palps) and have detected interesting similarities in three model organisms (Ciona, Phallusia, and Botryllus), suggesting a possible functional conservation of certain sugar residues, at least related to their papillary function (Zeng et al 2019a(Zeng et al , 2019b. Since we also observed specific lectin binding to migratory cell types, which were suggested to include haemocytes (Cloney and Grimm 1970;Sotgia et al 1993;Sato et al 1997;Davidson and Swalla 2002;Jimenez-Merino et al 2019), we here aimed to profile and compare lectin patterns of the well accessible migratory haemocytes and provide useful markers and tools to access the molecules behind their epitopes.…”

Crayfish hemocytes develop along the granular cell lineage

“…Most of our knowledge comes from research in insects 1 , 6 , 7 . In addition, there are some studies concerning blood cell formation in tunicates 8 , 9 , echinoderms 10 , 11 , mollusks 12 , 13 and crustaceans 14 – 19 . Investigation of hematopoiesis in various species will help us understand how this critical process evolved in the animal kingdom.…”

The eventful history of nonembryonic development in tunicates

“…For example, one can explore the function of undifferentiated mesenchymal cells (referred to as hemoblasts or lymphocyte-like cells), which have been reported in both solitary and colonial ascidians. In the solitary Styela plicata these cells show characteristics of stem cells, and they have been suggested to play a role during regeneration (Jimenez-Merino et al, 2019). In Botrylloides leachii, also a stylelid, cells with similar characteristics have been shown to initiate vascular budding (Kassmer et al, 2019).…”