Stem cell dynamics in Cnidaria: are there unifying principles?

Abstract

The study of stem cells in cnidarians has a history spanning hundreds of years, but it has primarily focused on the hydrozoan genus Hydra. While Hydra has a number of self-renewing cell types that act much like stem cells--in particular the interstitial cell line--finding cellular homologues outside of the Hydrozoa has been complicated by the morphological simplicity of stem cells and inconclusive gene expression data. In non-hydrozoan cnidarians, an enigmatic cell type known as the amoebocyte might play a similar role to interstitial cells, but there is little evidence that I-cells and amoebocytes are homologous. Instead, self-renewal and transdifferentiation of epithelial cells was probably more important to ancestral cnidarian development than any undifferentiated cell lineage, and only later in evolution did one or more cell types come under the regulation of a "stem" cell line. Ultimately, this hypothesis and competing ones will need to be tested by expanding genetic and developmental studies on a variety of cnidarian model systems.

Fig. 1

a A simple animal phylogeny, with special attention to the classes of cnidarians, based on Collins et al. (2006), Dunn et al. (2008), Philippe et al. (2009), and Pick et al. (2010). b Life cycles of several cnidarian genera. For Aurelia, derivations from the “canonical” life cycle are highlighted in red (based on Vagelli (2007) and personal observation)

Fig. 2

Plasticity of cell lineages in the cnidarians, based on current knowledge. A key showing major cell types is given on the left. Uncertainty is reflected by the use of dotted arrows. Numbers in the figure refer to the following references for support: (1) Bosch et al. 2010; (2) Müller and Teo 2004; (3) Schmid et al. 1982; (4) Schmid and Alder 1984; (5) Renfer et al. 2010; (6) Nakanishi et al. 2012; (7) Marlow et al. 2009; (8) Nakanishi et al. 2008; (9) Chapman 1974; (10) Eckelbarger and Larson 1988

Fig. 3

Comparisons of interstitial cells and amoebocytes in various cnidarians. a–c I-cells from hydrozoans; note the simple, rounded morphology and lack of organelles (excluding mitochondria). a Hydra (from Lentz 1965). b Halocordyle (from Martin 1988). c Clytia (from Denker et al. 2008). d–g Amoebocytes from non-hydrozoans; note the extreme variation of shapes, filopodial extensions, and abundance of granules. d Anthozoan sea anemones Actinia (from Larkman 1984b) and e–f Nematostella (from Tucker et al. 2011). g Scyphozoan jellyfish Aurelia (from Chapman 1999, arrows added for clarity)

Fig. 4

Cell proliferation (in green) in various cnidarians, labeled using 5-ethynyl-2′-deoxyuridine (EdU). a Polyp of Aurelia sp. 1 (nuclear staining in blue); b Close-up of a polyp tentacle (nuclear staining in blue); c Juvenile medusa stage of Aurelia sp. 1 (tyrosinated tubulin in red, nuclear staining in blue); d Polyp of Nematostella vectensis; and e close-up of tentacle (tyrosinated tubulin in red, nuclear staining in blue). f Ephyrae of Chrysaora colorata (fmrf-positive neurons in red, nuclear staining in blue)