Distinct stem-like cell populations facilitate functional regeneration of theCladonemamedusa tentacle

Abstract

Blastema formation is a crucial process that provides a cellular source for regenerating tissues and organs. While bilaterians have diversified blastema formation methods, its mechanisms in non-bilaterians remain poorly understood. Cnidarian jellyfish, or medusae, represent early-branching metazoans that exhibit complex morphology and possess defined appendage structures highlighted by tentacles with stinging cells (nematocytes). Here we investigate the mechanisms of tentacle regeneration, using the hydrozoan jellyfish Cladonema pacificum. We show that proliferative cells accumulate at the tentacle amputation site and form a blastema composed of cells with stem-like cell morphology. Lineage tracing experiments indicate that repair-specific proliferative cells in the blastema are distinct from resident stem-like cells. We further demonstrate that resident stem-like cells control nematogenesis and tentacle elongation during both homeostasis and regeneration, while repair-specific proliferative cells preferentially differentiate into epithelial cells in the newly formed tentacle, analogous to lineage-restricted stem/progenitor cells observed in salamander limbs. Taken together, our findings reveal a regeneration mechanism that utilizes both resident stem-like cells and repair-specific proliferative cells, which in conjunction efficiently enable functional appendage regeneration, and provide novel insight into the diversification of blastema formation across animal evolution.

Characterization of eight newHydractiniai-cell markers reveals underlying heterogeneity in the adult pluripotent stem cell population

“…We show the two i-cell clusters in the Hydractinia single-cell atlas represent real biological heterogeneity, likely being a mixture of pluripotent stem cells and multipotent progenitor cells responsible for diverse processes with at least two distinguishable subsets: those involved in contributing to somatic lineages, and those involved in providing the germ cell lineage. These results are similar to recent work in acoels, planarians, annelids, and the jellyfish Cladonema, where adult stem cells exhibit transcriptional heterogeneity rather than being a molecularly homogeneous population [3,5,15,66]. In conclusion, we provide eight new markers of i-cells and progenitors in Hydractinia, demonstrate substantial heterogeneity in the spatial expression patterns of the new markers and Piwi1, and highlight the importance of examining multiple biological contexts to better understand cell clusters and genetic markers obtained from single-cell expression analyses, and i-cells in general.…”

“…In contrast, the cell types required for homeostasis of the mature feeding polyp might be expected to be predominantly nematocytes, which must be replaced after firing, therefore requiring nematoblasts and their progenitors to be a dominant cell type within the i-cell band. Recent findings from a study on tentacle regeneration in the medusa stage of the hydrozoan Cladonema pacificum support the idea that blastema i-cells and homeostatic i-cells represent heterogeneous stem cell populations [66]. In Cladonema medusa tentacle regeneration, the stem cells in the blastema primarily consist of repair-specific proliferative cells (RSPCs) that lack expression of classical i-cell markers like Piwi and do not appear to originate from the known resident homeostatic stem cells (RHSCs) in the tentacle bulb.…”

Cnidofest 2022: hot topics in cnidarian research

“…In recent years, the community has expanded into many other cnidarians to address regenerative biology questions. Sosuke Fujita (Postdoc, Nakajima lab, Tohoku University) discussed work on the cellular basis of tentacle regeneration in the Cladonema pacificum medusa [ 42 ]. The tentacles have a population of stem cells which reside at the proximal side.…”