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Genes (Basel)
2021 Aug 23;128:. doi: 10.3390/genes12081292.
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Expression of Piwi, MMP, TIMP, and Sox during Gut Regeneration in Holothurian Eupentacta fraudatrix (Holothuroidea, Dendrochirotida).
Dolmatov IY
,
Kalacheva NV
,
Tkacheva ES
,
Shulga AP
,
Zavalnaya EG
,
Shamshurina EV
,
Girich AS
,
Boyko AV
,
Eliseikina MG
.
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Mesodermal cells of holothurian Eupentacta fraudatrix can transdifferentiate into enterocytes during the regeneration of the digestive system. In this study, we investigated the expression of several genes involved in gut regeneration in E. fraudatrix. Moreover, the localization of progenitor cells of coelomocytes, juvenile cells, and their participation in the formation of the luminal epithelium of the digestive tube were studied. It was shown that Piwi-positive cells were not involved in the formation of the luminal epithelium of the digestive tube. Ef-72 kDa type IV collagenase and Ef-MMP16 had an individual expression profile and possibly different functions. The Ef-tensilin3 gene exhibited the highest expression and indicates its potential role in regeneration. Ef-Sox9/10 and Ef-Sox17 in E. fraudatrix may participate in the mechanism of transdifferentiation of coelomic epithelial cells. Their transcripts mark the cells that plunge into the connective tissue of the gut anlage and give rise to enterocytes. Ef-Sox9/10 probably controls the switching of mesodermal cells to the enterocyte phenotype, while Ef-Sox17 may be involved in the regulation of the initial stages of transdifferentiation.
Figure 1. Phylogenetic tree showing the relationships of the Piwi sequence of E. fraudatrix (marked with the asterisk) with homolog proteins of other animals.
Figure 2. Phylogenetic tree showing the relationships of the tensilins of E. fraudatrix with homolog proteins of the other holothurians. The tensilin used in the study is marked with red.
Figure 3. Part of the phylogenetic tree showing the relationships of Sox of the E. fraudatrix with homolog proteins of other animals. Ef-Sox9/10 is marked with a blue star, and Ef-Sox17 is marked with a red star.
Figure 4. mRNA expression profile of Piwi during different days post-evisceration and in normal intestinal tissue in E. fraudatrix. Different lowercase letters indicate significant differences (p < 0.05). The data are reported as the means ± S.D. (n = 5).
Figure 5. Localization of Piwi-positive juvenile cells in tissues of E. fraudatrix. (a) Labeled cell in the coelom at 4 hpe. (b) Labeled cells (arrowheads) in the coelomic epithelium at 4 hpe. (c) Labeled cell in the dermis of the body wall at 4 hpe. (d) Numerous labeled cells in the hypodermis at 4 hpe. (e) Rare-labeled cells (arrowheads) in the hypodermis at 24 hpe. (f) General view of the gut anlage at 7 dpe. (g) Labeled cells in the connective tissue of the gut anlage at 7 dpe. g, gut anlage; m, mesentery. Immunocytochemical staining with antibodies for the PIWI protein (red color) and DAPI-stained nuclear DNA (blue color).
Figure 6. Expression of MMPs during gut regeneration. (a) 72 kDa type IV collagenase expression in forming luminal epithelium of the gut on 5–7 dpe (histological section). (b) 72 kDa type IV collagenase expression in the coelomic epithelium of the mesentery and connective tissue thickening of the gut anlage on 5–7 dpe (histological section). (c) 72 kDa type IV collagenase expression in the posterior part of the gut on 10 dpe (whole mount). (d) 72 kDa type IV collagenase expression in the coelomic epithelium of the mesentery and gut anlage on 10 dpe (histological section). (e) Expression of MMP16 in the anterior part of gut anlage on 5–7 dpe (histological section). (f) Expression of MMP16 in the coelomic epithelium of the posterior part of the mesentery and connective tissue thickening on 5–7 dpe (histological section). (g) Expression of MMP16 in the coelomic epithelium of the mesentery and gut on 10 dpe (histological section). ab, aquapharyngeal bulb; ce, coelomic epithelium; ct, connective tissue; ctt, connective tissue thickening; g, gut; le, luminal epithelium; and m, mesentery; the insets in (b,d,f) show higher magnification views of the boxed areas.
Figure 7. Scheme of spatial distribution of the 72 kDa type IV collagenase, MMP16, tensilin3, Sox9/10, and Sox17 transcripts on 5–7 and 10 dpe. (a–c): Dotted lines indicate the planes of the gut anlage cut and a1–c3: sections of the gut anlage on the corresponding planes; ab, aquapharyngeal bulb; ga, gut anlage; le, luminal epithelium of the gut; and m, mesentery; an arrowhead indicates a site of coelomic epithelium embedding.
Figure 8. Expression of tensilin-3 during gut regeneration. (a) Tensilin-3 expression in the ventral part of the mesentery and gut anlage on 5–7 dpe (whole mount). (b) Tensilin-3 expression in the ventral part of the gut anlage on 5–7 dpe (histological section). (c) Tensilin-3 expression in the growing end of the gut on 10 dpe (whole mount). (d) Tensilin-3 expression in the coelomic and luminal epithelia of the gut anlage on 10 dpe (histological section). (e) Tensilin-3 expression in the ventral part of the growing end of the gut on 10 dpe (histological section). ab, aquapharyngeal bulb; ce, coelomic epithelium; ct, connective tissue; g, gut; le, luminal epithelium; and m, mesentery.
Figure 9. Expression of Sox9/10 and Sox17 during gut regeneration. (a) Expression of Sox9/10 in the coelomic and luminal epithelia of the gut anlage on 5–7 dpe; an arrowhead indicates a site of coelomic epithelium embedding, and arrows show the luminal epithelium (whole mount). (b) Expression of Sox9/10 in the coelomic and luminal epithelia of the gut anlage in the site of coelomic epithelium embedding (arrowhead) on 5–7 dpe (histological section). (c) Expression of Sox9/10 in the luminal epithelium of the posterior part of the gut anlage on 5–7 dpe (histological section). (d) Expression of Sox9/10 in the gut on 10 dpe (whole mount). (e) Expression of Sox9/10 in the luminal epithelium in the middle part of the gut anlage on 10 dpe (histological section). (f) Expression of Sox17 in the ventral part (arrowhead) of the gut anlage on 5–7 dpe (whole mount). (g) Expression of Sox17 in the coelomic epithelium in the site of embedding on 5–7 dpe; red spots indicate the site of the epithelium embedding, and arrowheads in the insert show the embedding epithelium (histological section). (h) Expression of Sox17 in the coelomic epithelium of the lateral and dorsal parts of the gut on 10 dpe (histological section). ab, aquapharyngeal bulb; ce, coelomic epithelium; ct, connective tissue; g, gut; le, luminal epithelium; and m, mesentery; the inset in (g) shows a higher magnification view of the boxed area.
Alexander,
A molecular pathway leading to endoderm formation in zebrafish.
1999, Pubmed
Alexander,
A molecular pathway leading to endoderm formation in zebrafish.
1999,
Pubmed
Angerer,
Sea urchin metalloproteases: a genomic survey of the BMP-1/tolloid-like, MMP and ADAM families.
2006,
Pubmed
,
Echinobase
Aravin,
Developmentally regulated piRNA clusters implicate MILI in transposon control.
2007,
Pubmed
Bankaitis,
Reserve Stem Cells in Intestinal Homeostasis and Injury.
2018,
Pubmed
Boyko,
The Eupentacta fraudatrix transcriptome provides insights into regulation of cell transdifferentiation.
2020,
Pubmed
,
Echinobase
Cary,
Analysis of sea star larval regeneration reveals conserved processes of whole-body regeneration across the metazoa.
2019,
Pubmed
,
Echinobase
Chakraborty,
Transcriptional regulation of heart valve progenitor cells.
2010,
Pubmed
Clouse,
Phylotranscriptomic analysis uncovers a wealth of tissue inhibitor of metalloproteinases variants in echinoderms.
2015,
Pubmed
,
Echinobase
Ding,
Transcriptome analysis provides insights into the molecular mechanisms responsible for evisceration behavior in the sea cucumber Apostichopus japonicus.
2019,
Pubmed
,
Echinobase
Dolmatov,
Muscle regeneration in the holothurian Stichopus japonicus.
1996,
Pubmed
,
Echinobase
Dolmatov,
Muscle regeneration in holothurians.
2001,
Pubmed
,
Echinobase
Dolmatov,
Post-autotomy regeneration of respiratory trees in the holothurian Apostichopus japonicus (Holothuroidea, Aspidochirotida).
2009,
Pubmed
,
Echinobase
Dolmatov,
Molecular Aspects of Regeneration Mechanisms in Holothurians.
2021,
Pubmed
,
Echinobase
Dolmatov,
Molecular mechanisms of fission in echinoderms: Transcriptome analysis.
2018,
Pubmed
,
Echinobase
Dolmatov,
Metalloproteinase inhibitor GM6001 delays regeneration in holothurians.
2019,
Pubmed
,
Echinobase
Dolmatov,
Matrix Metalloproteinases and Tissue Inhibitors of Metalloproteinases in Echinoderms: Structure and Possible Functions.
2021,
Pubmed
,
Echinobase
Dolmatov IYu,
Regeneration of the aquapharyngeal complex in the holothurian Eupentacta fraudatrix (Holothuroidea, Dendrochirota).
1992,
Pubmed
,
Echinobase
Frolova,
Microscopic anatomy of the digestive system in normal and regenerating specimens of the brittlestar Amphipholis kochii.
2010,
Pubmed
,
Echinobase
Furuyama,
Continuous cell supply from a Sox9-expressing progenitor zone in adult liver, exocrine pancreas and intestine.
2011,
Pubmed
García-Arrarás,
Echinoderms: potential model systems for studies on muscle regeneration.
2010,
Pubmed
,
Echinobase
García-Arrarás,
Holothurians as a Model System to Study Regeneration.
2018,
Pubmed
,
Echinobase
García-Arrarás,
Cellular mechanisms of intestine regeneration in the sea cucumber, Holothuria glaberrima Selenka (Holothuroidea:Echinodermata).
1998,
Pubmed
,
Echinobase
García-Arrarás,
The mesentery as the epicenter for intestinal regeneration.
2019,
Pubmed
,
Echinobase
Gracz,
Defining hierarchies of stemness in the intestine: evidence from biomarkers and regulatory pathways.
2014,
Pubmed
Gustafson,
Vasa genes: emerging roles in the germ line and in multipotent cells.
2010,
Pubmed
Hayakawa,
Cell growth-promoting activity of tissue inhibitor of metalloproteinases-2 (TIMP-2).
1994,
Pubmed
Hojo,
Identification of the gene-regulatory landscape in skeletal development and potential links to skeletal regeneration.
2017,
Pubmed
Jiang,
Complex roles of tissue inhibitors of metalloproteinases in cancer.
2002,
Pubmed
Juliano,
Uniting germline and stem cells: the function of Piwi proteins and the piRNA pathway in diverse organisms.
2011,
Pubmed
Juliano,
PIWI proteins and PIWI-interacting RNAs function in Hydra somatic stem cells.
2014,
Pubmed
Jung,
Identification of CD63 as a tissue inhibitor of metalloproteinase-1 interacting cell surface protein.
2006,
Pubmed
Lai,
EvoRegen in animals: Time to uncover deep conservation or convergence of adult stem cell evolution and regenerative processes.
2018,
Pubmed
Lamash,
Proteases from the regenerating gut of the holothurian Eupentacta fraudatrix.
2013,
Pubmed
,
Echinobase
Lambert,
TIMPs as multifacial proteins.
2004,
Pubmed
Leibson,
Regeneration of digestive tube in holothurians Stichopus japonicus and Eupentacta fraudatrix.
1992,
Pubmed
,
Echinobase
Liu,
Sox17 is essential for the specification of cardiac mesoderm in embryonic stem cells.
2007,
Pubmed
Ma,
Regeneration of functional alveoli by adult human SOX9+ airway basal cell transplantation.
2018,
Pubmed
Mashanov,
Gut regeneration in holothurians: a snapshot of recent developments.
2011,
Pubmed
,
Echinobase
Mashanov,
Expression of stem cell factors in the adult sea cucumber digestive tube.
2017,
Pubmed
,
Echinobase
Mashanov,
Expression of pluripotency factors in echinoderm regeneration.
2015,
Pubmed
,
Echinobase
Mashanov,
Myc regulates programmed cell death and radial glia dedifferentiation after neural injury in an echinoderm.
2015,
Pubmed
,
Echinobase
Mashanov,
Transdifferentiation in holothurian gut regeneration.
2005,
Pubmed
,
Echinobase
Mashanov,
Visceral regeneration in a sea cucumber involves extensive expression of survivin and mortalin homologs in the mesothelium.
2010,
Pubmed
,
Echinobase
Mead,
A far-upstream (-70 kb) enhancer mediates Sox9 auto-regulation in somatic tissues during development and adult regeneration.
2013,
Pubmed
Miao,
Extracellular matrix remodeling and matrix metalloproteinases (ajMMP-2 like and ajMMP-16 like) characterization during intestine regeneration of sea cucumber Apostichopus japonicus.
2017,
Pubmed
,
Echinobase
Mladenov,
Mechanisms of arm-tip regeneration in the sea star, Leptasterias hexactis.
1989,
Pubmed
,
Echinobase
Murphy,
Progress in matrix metalloproteinase research.
2008,
Pubmed
Murphy,
Tissue inhibitors of metalloproteinases.
2011,
Pubmed
Oulhen,
Regeneration in bipinnaria larvae of the bat star Patiria miniata induces rapid and broad new gene expression.
2016,
Pubmed
,
Echinobase
Page-McCaw,
Matrix metalloproteinases and the regulation of tissue remodelling.
2007,
Pubmed
Praher,
Characterization of the piRNA pathway during development of the sea anemone Nematostella vectensis.
2017,
Pubmed
Quispe-Parra,
A roadmap for intestinal regeneration.
2021,
Pubmed
,
Echinobase
Quiñones,
Extracellular matrix remodeling and metalloproteinase involvement during intestine regeneration in the sea cucumber Holothuria glaberrima.
2002,
Pubmed
,
Echinobase
Reinardy,
Tissue regeneration and biomineralization in sea urchins: role of Notch signaling and presence of stem cell markers.
2015,
Pubmed
,
Echinobase
Ribeiro,
Matrix metalloproteinases in a sea urchin ligament with adaptable mechanical properties.
2012,
Pubmed
,
Echinobase
Ricca,
Tissue inhibitor of metalloproteinase 1 expression associated with gene demethylation confers anoikis resistance in early phases of melanocyte malignant transformation.
2009,
Pubmed
Shivdasani,
Molecular regulation of vertebrate early endoderm development.
2002,
Pubmed
Solana,
Defining the molecular profile of planarian pluripotent stem cells using a combinatorial RNAseq, RNA interference and irradiation approach.
2012,
Pubmed
Song,
Regulation and function of SOX9 during cartilage development and regeneration.
2020,
Pubmed
Sun,
RNA-Seq reveals dynamic changes of gene expression in key stages of intestine regeneration in the sea cucumber Apostichopus japonicus. [corrected].
2013,
Pubmed
,
Echinobase
Tang,
TIMP1 preserves the blood-brain barrier through interacting with CD63/integrin β 1 complex and regulating downstream FAK/RhoA signaling.
2020,
Pubmed
Vagin,
A distinct small RNA pathway silences selfish genetic elements in the germline.
2006,
Pubmed
Verstappen,
Tissue inhibitors of metalloproteinases (TIMPs): their biological functions and involvement in oral disease.
2006,
Pubmed
Vogt,
Hidden treasures in stem cells of indeterminately growing bilaterian invertebrates.
2012,
Pubmed
,
Echinobase
Vázquez-Vélez,
A Proteoglycan-Like Molecule Offers Insights Into Ground Substance Changes During Holothurian Intestinal Regeneration.
2016,
Pubmed
,
Echinobase
Woessner,
Matrix metalloproteinases and their inhibitors in connective tissue remodeling.
1991,
Pubmed
Zhang,
Differential gene expression in the intestine of sea cucumber (Apostichopus japonicus) under low and high salinity conditions.
2018,
Pubmed
,
Echinobase
Zorn,
Vertebrate endoderm development and organ formation.
2009,
Pubmed