Abstract
ABSTRACTAdult stem cells (ASCs) in vertebrates and model invertebrates (e.g. Drosophila melanogaster) are typically long‐lived, lineage‐restricted, clonogenic and quiescent cells with somatic descendants and tissue/organ‐restricted activities. Such ASCs are mostly rare, morphologically undifferentiated, and undergo asymmetric cell division. Characterized by ‘stemness’ gene expression, they can regulate tissue/organ homeostasis, repair and regeneration. By contrast, analysis of other animal phyla shows that ASCs emerge at different life stages, present both differentiated and undifferentiated phenotypes, and may possess amoeboid movement. Usually pluri/totipotent, they may express germ‐cell markers, but often lack germ‐line sequestering, and typically do not reside in discrete niches. ASCs may constitute up to 40% of animal cells, and participate in a range of biological phenomena, from whole‐body regeneration, dormancy, and agametic asexual reproduction, to indeterminate growth. They are considered legitimate units of selection. Conceptualizing this divergence, we present an alternative stemness metaphor to the Waddington landscape: the ‘wobbling Penrose’ landscape. Here, totipotent ASCs adopt ascending/descending courses of an ‘Escherian stairwell’, in a lifelong totipotency pathway. ASCs may also travel along lower stemness echelons to reach fully differentiated states. However, from any starting state, cells can change their stemness status, underscoring their dynamic cellular potencies. Thus, vertebrate ASCs may reflect just one metazoan ASC archetype.
Highlights
Adult stem cells (ASCs) in vertebrates and model invertebrates (e.g. Drosophila melanogaster) are typically long-lived, lineagerestricted, clonogenic and quiescent cells with somatic descendants and tissue/organ-restricted activities
A glance at the metazoan phylogenetic tree puts in stark relief the fact that ASCs have only been studied in a limited number of taxa, mainly those capable of asexual reproduction and/or with high competency for regeneration, including some spiralian protostomes and deuterostomes, as well as many non-bilaterian lineages
To fill this conceptual lacuna, we evaluate the distribution and the properties of ASCs in non-vertebrate metazoans in the context of the vertebrate ASC exemplar, excluding invertebrates such as fruit flies and nematodes, which while excellent genetic model systems are by all accounts highly derived ecdysozoans
Summary
Apart from two fundamental properties of stem cells, i.e. selfrenewal and differentiation potential, it appears that many cardinal ASC traits differ between vertebrates and other phyla. ASCs are generally rare in vertebrates (e.g. only 0.001–0.01% of mononuclear cells isolated from a Ficoll density gradient of feline bone marrow aspirate are mesenchymal stem cells; Martin et al, 2002) and pluripotent at best; they are slow cycling and reside in compartmentalized niches, with restricted migration potential (Moore & Lyle, 2011). These vertebrate traits are inconsistent with many of the ASC attributes found in other groups (Table 1). The aforementioned disparate characters have emerged in long-lived and indeterminately growing animals, where organismal senescence (sensu Rinkevich & Loya, 1986) has not been documented or is delayed (e.g. sponges, corals, and the immortal Hydra)
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