Ferrario C et al. (2020), Beyond Adult Stem Cells: Dedifferentiation as a...

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Front Cell Dev Biol 2020 Oct 20;8:587320. doi: 10.3389/fcell.2020.587320.

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Beyond Adult Stem Cells: Dedifferentiation as a Unifying Mechanism Underlying Regeneration in Invertebrate Deuterostomes.

Ferrario C , Sugni M , Somorjai IML , Ballarin L .

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The diversity of regenerative phenomena seen in adult metazoans, as well as their underlying mechanistic bases, are still far from being comprehensively understood. Reviewing both ultrastructural and molecular data, the present work aims to showcase the increasing relevance of invertebrate deuterostomes, i.e., echinoderms, hemichordates, cephalochordates and tunicates, as invaluable models to study cellular aspects of adult regeneration. Our comparative approach suggests a fundamental contribution of local dedifferentiation -rather than mobilization of resident undifferentiated stem cells- as an important cellular mechanism contributing to regeneration in these groups. Thus, elucidating the cellular origins, recruitment and fate of cells, as well as the molecular signals underpinning tissue regrowth in regeneration-competent deuterostomes, will provide the foundation for future research in tackling the relatively limited regenerative abilities of vertebrates, with clear applications in regenerative medicine.

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	FIGURE 1. (A) Schematic showing the currently accepted phylogenetic relationships among the phyla within the deuterostomes. Echinodermata and Hemichordata are collectively referred to as Ambulacraria. Within the chordates, Cephalochordata are the sister group to Urochordata and Vertebrata, which together comprise the Olfactores. (B) Living representatives of the invertebrate deuterostome phyla discussed here. Note the considerable diversity in body plan types even within phyla. Echinodermata: Holothuroidea: Holothuria sanctori (credits: Dr Federico Betti, University of Genova), and Crinoidea: Antedon mediterranea (credits: Dr Michela Sugni, University of Milan). Hemichordata: Enteropneusta: Yoda purpurata (credits: “Smithson Picture 66” by public.resource.org, licensed under CC PDM 1.0). Cephalochordata: Branchiostoma lanceolatum (credits: Dr Ildiko Somorjai, University of St Andrews). Tunicata: Ascidiacea: Ciona robusta (credits: Dr E.A, Lazo-Wasem, Yale Peabody Museum) and Botryllus schlosseri (Dr Loriano Ballarin, University of Padova), and Thaliacea: Pyrosoma atlanticum (credits: Dr Alan Deidun, University of Malta).
	FIGURE 2. Crinoidea. (A) Schematic section through the vertical plane of the calyx and of an arm of an adult crinoid. The oral side, harboring both mouth and anus, faces the water column. The visceral mass is hosted in the calyx and is anchored to the coelomic walls by mesenteries. For simplicity, only one cirrus at the base of the calyx is shown. (B) Schematic cross section of an arm of an adult crinoid. The ambulacral groove, including rows of tube feet, faces the water column. Adjacent segments are joined by muscles and ligaments. The brachial nerve longitudinally runs along the arm within the ossicles. For clarity, pinnules and gonads are not shown. Abbreviations: rwc-radial water canal. Pink lining represents the coelomic epithelium (somatocoel) (credits: Alessandro Allievi).
	FIGURE 3. Echinoidea. (A) Schematic section through the vertical plane of an adult sea urchin. The oral side, containing the mouth with the Aristotle’s lantern, faces the substrate, whereas the aboral side, including madreporite and anus, faces the water column. The digestive tube is anchored to the internal walls of the test by mesenteries. For clarity, structures that are serially repeated along the test either externally or internally have been only partially shown. (B) Schematic longitudinal section of the test where a spine, a tube foot and a pedicellaria are present. The spine is articulated to the test by muscles and ligaments and the tube foot is directly connected to the rwc. (C) Insert of B showing the schematic cross section of a spine where the inner stereom architecture is visible. Abbreviations: rnc-radial nerve cord, rwc-radial water canal. Pink lining represents the coelomic epithelium (credits: Alessandro Allievi).
	FIGURE 4. Holothuroidea. (A) Schematic cross section of an adult sea cucumber. The body wall is mainly composed of connective tissue with only few small ossicles. The gut is anchored to the coelomic cavity walls by mesenteries. For simplicity, the gonads, located within the coelomic cavity, and the muscle layers of the coelomic cavity wall are not shown. (B) Detail of a (square) on the gut and the corresponding mesentery. Both structures are lined by coelomic epithelium. Abbreviations: rnc-radial nerve cord, rwc-radial water canal. Pink lining represents the coelomic epithelium (credits: Alessandro Allievi).
	FIGURE 5. Ophiuroidea. (A) Schematic longitudinal section of the disk and an arm of an adult brittle star. The oral side, where the mouth and madreporite are located, faces the substrate. The disk encloses the gonads and the digestive tube, which lacks an anus. The arm is subdivided into serially repeated segments and the inner adjacent vertebrae are articulated by muscles and ligaments. The acc, the rwc and the rnc longitudinally run along the arm. Both disc and arms present skeletal elements called plates, with different names depending on their position. (B) Schematic cross section of an arm of an adult brittle star where all structures are visible. Spines are articulated to the lateral arm plates and spinal ganglia are present at their bases. The acc occupies the aboral side of the arm, immediately below the aboral arm plate, and laterally branches near the lateral arm plates. The rnc is the most oral structure above the oral arm plate. Abbreviations: acc-aboral coelomic cavity, rnc-radial nerve cord, rwc-radial water canal. Pink lining represents the coelomic epithelium (credits: Alessandro Allievi).
	FIGURE 6. Asteroidea. (A) Schematic drawing of an adult starfish where both external and internal anatomy are visible. The aboral side, including the madreporite and the anus, faces the water column. Gonads and pyloric caeca are present within the coelomic cavity. The rwc and the rnc run longitudinally along the arm. The last tube foot of each arm is called the terminal tube foot; the optic cushion, the photoreceptor of the animal, is located orally at its base. (B) Schematic cross section of an arm of an adult starfish where all structures are visible. The spines are articulated with the corresponding ossicles of the body wall. Papule, evaginations of the coelomic cavity, are internally lined by coelomic epithelium. The rnc is exposed to the external environment but partially protected by the rows of tube feet. Abbreviations: oc-optic cushion, rnc-radial nerve cord, rwc-radial water canal, ttf-terminal tube foot. Pink lining represents the coelomic epithelium (credits: Alessandro Allievi).
	FIGURE 7. Hemichordata. (A) Schematic longitudinal section of an adult solitary enteropneust hemichordate (Ptychodera). Only the internal anatomy of the proboscis (prosome), collar (mesosome) and the anterior part of the trunk (metasome) containing the branchial region are shown. The external gill pores, genital wings with gonads, hepatic sacs and posterior trunk with terminal anus have been omitted for clarity. (B) Cross section through the body wall posterior to the branchial region. The dorsal and ventral nerve cords and associated blood vessels are easily distinguished (credits: Alessandro Allievi).
	FIGURE 8. Cephalochordata. (A) Schematic drawing of an adult cephalochordate (Branchiostoma). The gonads and lateral musculature (myomeres) overlying the nerve cord, notochord and digestive system have been omitted for clarity. Unlike other chordates, the notochord is a muscular structure in cephalochordates. The thickening of the anterior nerve cord corresponding to the brain is called the cerebral vesicle, and has a single photoreceptor at its terminus, the frontal eye. The circulatory system is not shown. (B) Cross section through the pharyngeal region. Although generally considered to be bilaterally symmetric as adults, with rows of gonads running along either side of the body, the hepatic diverticulum is located on the left side of the pharynx/branchial basket. The endostyle, which runs along the base of the pharynx, is a homolog of the vertebrate thyroid. (C) Cross section through the post-anal tail. Note the dorsal and ventral tail fins and the proportionally greater size of the nerve cord and notochord (credits: Alessandro Allievi).
	FIGURE 9. Schematic drawings showing the anatomy of (A) a solitary ascidian, (B) a botryllid colonial ascidian, and (C) the organization of the neural complex of a solitary ascidian (credits: Alessandro Allievi).

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Abnave, Role of the immune system in regeneration and its dynamic interplay with adult stem cells. 2019, Pubmed