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Review
.2021;65(4-5-6):427-437.
doi: 10.1387/ijdb.200227dq.

A roadmap for intestinal regeneration

Affiliations
Review

A roadmap for intestinal regeneration

David Quispe-Parra et al. Int J Dev Biol.2021.

Abstract

Regeneration of lost or injured organs is an intriguing process in which numerous cellular events take place to form the new structure. Studies of this process during reconstitution of the intestine have been performed in echinoderms, particularly in holothurians. Many cellular events triggered during regeneration have been described using the sea cucumberHolothuria glaberrima as a research model. More recent experiments have targeted the molecular mechanisms behind the process, a task that has been facilitated by the new sequencing technologies now available. In this review, we present studies involving cellular processes and the genes that have been identified to be associated with the early events of gut regeneration. We also present ongoing efforts to perform functional studies necessary to establish the role(s) of the identified genes. A synopsis of the studies is given with the course of the regenerative process established so far.

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Figures

Fig 1.
Fig 1.. The model system portrayed in this review- The sea cucumberHolothuria glaberrima.
An echinoderm commonly found in rocky coastal regions from Florida to Brazil. Side view, anterior (oral) end is to the right.
Fig 2.
Fig 2.. Anatomical organization and tissue architecture of the sea cucumber digestive.
(A) Visceral anatomy of sea cucumber. The intestine is subdivided into the anterior descending small intestine, ascending small intestine, and the posterior descending large intestine.Abbreviations: short esophagus (E); anterior descending intestine (ADI); medial ascending intestine (MAI); posterior descending intestine (PDI).(B) Tissue organization of the luminal epithelium and(C) mesothelium found throughout the intestine ofH. glaberrima.Abbreviations: basal lamina (bl); bundles of intermediate filaments in peritoneocytes (if); myoepithelial cell (m); mucocyte (mc); neuron (n); neurosecretory cell (ns); nervous plexus (np); peritoneal cell (pc); secretory vacuoles (sv); vesicular enterocyte (ve). Fig. 2 A adapted from García-Arrarás et al., 2019, Seminars in Cell & Developmental Biology 92, p. 47 and fig 2 B, C from Mashanov & García-Arrarás, 2011, Biological Bulletin, 221, p. 95. Copyright 2019 by Elsevier (2 A) and 2011 by The University of Chicago Press (2 B, C). Adapted with permission.
Fig 3.
Fig 3.. Cellular dedifferentiation and proliferation at the early stage of the regenerative process.
(A) Cells in the free end of the mesentery begin to dedifferentiate soon after evisceration.(B) Cells accumulate at the free edge of mesentery forming the early blastema-like structure.(C) As regeneration proceeds, dedifferentiation spreads along the mesentery and involves regions closer to the body wall, while cell proliferation remains mainly restricted to the blastema-like structure composed of the dedifferentiated cells. White arrows point out SLSs from the dedifferentiation process. White cells represent dedifferentiated cells originated from peritoneocytes (yellow) and muscle cells (reddish-brown) of the mesothelium. Connective tissue (orange) is positioned between the layers of the mesothelium and extends to the body wall (upper part).
Fig 4.
Fig 4.. Differential gene expression and pathway enrichment analysis of day 3 regenerating intestine vs normal mesentery.
(A) Volcano plot showing downregulated (blue) and upregulated (red) genes. Gene expression shown as log2 fold change is on the x-axis and −log10 adjusted p-values are plotted on the y-axis. Expressed genes were selected with an adjusted p-value lower than 0.05 and a log2 fold change different than 0.(B) Pathway enrichment analysis obtained for differentially expressed genes that had an adjusted p-value <0.05. Gene ratio describes the representation of differentially expressed genes involved in the components of the pathway and count number describes the quantity of those genes in each pathway.
Fig 5.
Fig 5.. Correlation of survivin and mortalin expression with apoptosis in the regenerating intestine on day 7.
(A) Double labeling with in situ hybridization with a survivin riboprobe and TUNEL assay.(B) Double labeling with a mortalin riboprobe and TUNEL assay. Survivin and mortalin transcripts are showed in violet and TUNEL labeled cells are showed in green. Lower density of TUNEL-positive cells can be observed when higher signal of survivin in situ hybridization is present (white arrows). Scale bar = 100 μm. Adapted from Mashanovet al. 2010, BMC Developmental Biology, 10:117. Copyright ©2010 Mashanovet al; licensee BioMed Central Ltd.
Fig 6.
Fig 6.. Effect of pharmacological modulation on the size of the regenerating gut in vivo.
Histological cross sections of the intestine with the attached mesentery show the effect of a Wnt pathway inhibitor iCRT14(A) and a Wnt-pathway activator LiCl(C) treatment on the gut rudiment size compared with controls DMSO(B) and NaCl(D), respectively. iCRT14 treatment reduces the size of the gut rudiment compared with control DMSO, whereas treatment with LiCl increases the size compared with NaCl. Scale bars = 300 μm. Adapted from Belloet al., 2020, Developmental Biology, 458, p. 15. Copyright 2020 by Elsevier. Adapted with permission.
Fig 7.
Fig 7.. Effect RNAi inhibition on cell proliferation of regenerating gut explants in vitro.
Sections of regenerating gut in vitro treated with control RNAi targetingGFP(A) andMYC(B). BrdU labeled cells are reduced in treatment with RNAi targetingMYC compared with control targetingGFP. Cell nuclei are shown in red (DAPI) and BrdU labeled cell nuclei (white arrows) in green. Scale bar = 20 μm.
Fig 8.
Fig 8.. Schematic representation of cellular and molecular mechanisms during the first week of regeneration.
Timeline is represented by days of regeneration after de evisceration process occurs. Colors for each cellular process correspond to the same color for the genes that are associated with that process.
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