Adult stem cells in animals: a paradigm shift from a spongiologist perspective

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Abstract

The paradigm within which the scientific community views animal adult stem cells (ASCs) and the concept of “stemness” itself was changed significantly over the past five years. According to the previously dominant paradigm, formed during the study of mammals, adult stem cells are extremely few in number, committed lineage-specific cells; their fates are limited to the tissues/organs in which they are located. However, studies performed on aquatic invertebrates have shown that ASCs, on the contrary, are very numerous, morphologically diverse, and demonstrate a wide range of states and levels of “stemness”. Moreover, ASCs of a number of invertebrates can arise de novo by transdifferentiation from differentiated somatic cells. One of the key roles in the formation of the new paradigm was played by the study of representatives of the phylum Porifera. This brief review examines the state of the arts of the modern concept of stem cells and the role of spongiology in the formation of the new paradigm.

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About the authors

A. V. Ereskovsky

Koltzov Institute of Developmental Biology RAS

Author for correspondence.
Email: aereskovsky@gmail.com
Russian Federation, Moscow

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Supplementary files

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2. Fig. 1. Plasticity of animal somatic stem cells (somatic stem cells = adult stem cells = ASC). ASC are highlighted in color, differentiation products are shown in black and white diagrams. (a, b) Representatives of sponges: (a) Amphimedon queenslandica, Ephydatia fluviatilis; (b) Oscarella lobularis (ac — archaeocyte, cc — choanocyte, tc — thesocyte, sc — sclerocyte, lc — lophocytes, gc — granule cells, pc — pinacocytes, fc — follicular cells, g — gametes, vc — vacuolar cells, ap — apopilary cells). (c) Mammals (for comparison) (hsc — hematopoietic stem cells, msc — myeloid progenitors, lsc — lymphoid progenitors, mk — megakaryocyte, gr — granulocytes, mp — macrophages, rbc — red blood cells, tc — T cells, bc — B cells, nk — killer lymphocytes). Sponges are characterized by the conversion of one type of ASC into another, as well as the differentiation of gametes from ASC descendants. (From Rinkevich et al., 2022, with modifications; © 2021 The Authors, published by John Wiley & Sons Ltd. under a CC-BY-4.0 license.)

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3. Fig. 2. A graphical metaphor for the new concept of somatic stem cells. (a) “Penrose oscillating landscape” by Rinkevich et al. (2022). The color code (from dark blue to light blue) shows the cell states (from totipotent to fully differentiated). Note that a cell (orange ball) can either “fall” to the lower light blue level from the funnel or return to the upper dark blue level via one or more ladders or ropes (from Rinkevich et al., 2022; © 2021 The Authors, published by John Wiley & Sons Ltd. under a CC BY4.0 license). (b) Penrose's staircase, one of his "impossible objects" (Penrose L. S., Penrose R., 1958) (image from https://en.wikipedia.org/wiki/Penrose_stairs). (c) Waddington landscape as applied to cell differentiation (orange ball); orange arrows show differentiation trajectories, brown circles show bifurcation (trajectory choice) points (adapted from Waddington C. H. © (1957) George Allen and Unwin (London)).

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4. Fig. 3. Summary of the structure and properties of the stem cell (SC) niche in model organisms. The most important basic structures that are thought to define the SC are shown. At the top are listed four physiological properties associated with niche functionality. Below are shown the different components of the niche associated with SC activity: different cells, signaling molecules, and the extracellular matrix (modified from Martinez et al., 2022; © 2022 The Authors, published by BMC Biology under a CC-BY-4.0 license).

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5. Fig. 4. Conceptual diagram representing three different types of stem cell niche architecture in metazoans. (a, b), (c, d), and (e, f) refer to three structural states (A, B, and C) defined to describe progressively more complex niche architectures and their localization in the animal body. CTVT, canine transmissible venereal tumor (modified from Martinez et al., 2022; © 2022 The Authors, published by BMC Biology under a CC-BY-4.0 license).

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6. Fig. 5. Archaeocytes of different demospongia (data from transmission electron microscopy). (a) Ephydatia muelleri (order Spongillida); (b) Lubomirskia baicalensis (order Spongillida); (c) Spongia officinalis (order Dyctyoceratida); (d) Halisarca dujardinii (order Chondrillida); (e) Crellomima imparides (order Poecilosclerida); (e) Suberites domuncula (order Suberitida). n — nucleus; nu — nucleolus; ph — phagosome; zo — endosymbiotic zoochlorella. Scale bars: a, c–e = 2 μm; b = 5 μm (from Ereskovsky et al., 2024; permission to reproduce the figure was obtained from John Wiley and Sons, License Number 5916501382860).

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