Regeneration in calcareous sponges (Porifera)

Padua, André; Klautau, Michelle

doi:10.1017/s0025315414002136

Cited by 9 publications

(9 citation statements)

References 27 publications

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“…S. ciliatum regeneration follows morphological and cellular trajectories at similar rates previously observed in other calcareous sponge species, with wound healing within 24 hours of injury and completed regeneration after 4-5 days [21,47,48]. The crucial morphogenetic step in early regeneration is quick wound closure by a combination of migration and spreading of endo-and exopinacoderm and transdifferentiation of exposed choanocytes to pinacocytes.…”

Section: Discussionsupporting

confidence: 65%

Fast transcriptional activation of developmental signalling pathways during wound healing of the calcareous sponge Sycon ciliatum

Ereskovsky

Caglar

Laplante

et al. 2021

Preprint

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Background: The ability to regenerate lost or damaged body parts is an ancient animal characteristic with a wide yet variable distribution across all phyla. Sponges, likely the sister group to all other animals, have remarkable regenerative abilities including whole body regeneration and re-development from dissociated cells. The calcareous sponge Sycon ciliatum has been subject to various regeneration studies since the beginning of the last century. However, the early steps of wound healing of S. ciliatum have not been addressed from the molecular perspective. Results: In this study, we combined electron microscopy with gene expression analysis to investigate wound healing after transverse sectioning of S. ciliatum. Microscopic analysis revealed massive transdifferentiation and collective migration behaviour of choanocytes and pinacocytes early upon injury (6-12h) as the main mechanisms for quick closure of the wound surface. RNA-sequencing identified upregulation of components of the conserved metazoan Wnt and TGFβ signalling pathways within 3h, preceding morphologically detectable wound healing events. De novo upregulation after a decline in expression coincides with morphologically visible polarity establishment. Moreover, by integrating the new wound healing data set with previously published data derived from intact sponge, we demonstrate similarity between gene activity during early wound healing and osculum maintenance. Whole mount in situ hybridisation of the TGFβ signalling pathway ligand SciTGFβU and signal transducer SciSmadRa show that the early activation of both is initially encompassing a large area surrounding the cut surface with gradual restriction to the edge of the forming regenerative membrane as wound healing progresses. While SciTGFβU transcripts are localised to exo- and endopinacocytes, SciSmadRa expression appears across all cell types. Using an EdU cell proliferation assay, we found that a global increase in cell proliferation is not visible before 12h into wound healing. Hence, the initial stages to cover the injury site including cell transdifferentiation and migration seem to be executed by cells remaining after injury. Gene expression clustering coupled with GO term enrichment analysis confirmed that expression of genes involved in processes related to cell proliferation, DNA repair as well as apoptotic processes at 3 and 6h of wound healing was not upregulated. On the other hand, genes associated with positive regulation of transcription, signal transduction, actin filament and chromatin organisation, as well as the Wnt signalling pathway are upregulated at early wound healing stages. Conclusion: We have analysed wound healing in the calcareous sponge Sycon ciliatum using microscopic and genomic methods. This study highlights a remarkable mechanism of interplay between cell transdifferentiation and collective migration we hypothesise to be regulated by conserved metazoan developmental pathways and numerous taxonomically restricted genes. Expression of these genes in regenerating and intact sponges sheds light on the long-standing question whether embryonic developmental pathways are redeployed in regeneration.

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Section: Discussionsupporting

confidence: 65%

Fast transcriptional activation of developmental signalling pathways during wound healing of the calcareous sponge Sycon ciliatum

Ereskovsky

Caglar

Laplante

et al. 2021

Preprint

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“…The formation of the regenerative membrane rapidly returns the process of the water pumping to the normal mode. The quick healing of the opened wound (less than 2 days) was described in other asconoid calcareous sponge Ernstia citrea (Padua & Klautau, 2016). The authors also associated the features of regeneration of this species with the asconoid structure of their aquiferous system.…”

Section: Stage Ii-formation Of the Regenerative Membranementioning

confidence: 78%

“…The main studies on the sponge reparative regeneration capacities have been conducted using mostly light microscopy technics (Korotkova, , ; Padua & Klautau, ; Simpson, ). These studies provided information on general modes of the regeneration processes in about 19 sponge species of Demospongiae, Calcarea, and Homoscleromorpha with different aquiferous system organization and could be used as a basis for future ultrastructural and molecular–biological investigations.…”

Section: Introductionmentioning

confidence: 99%

Sewing up the wounds : The epithelial morphogenesis as a central mechanism of calcaronean sponge regeneration

et al. 2018

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Sponges (Porifera) demonstrate prominent regeneration abilities and possess a wide variety of mechanisms, used during this process. In the current study, we combined in vivo observations with histological, immunohistochemical, and ultrastructural technics to elucidate the fine cellular mechanisms of the regeneration in the calcareous sponge Leucosolenia cf. variabilis. The regeneration of Leucosolenia cf. variabilis ends within 4–6 days. The crucial step of the process is the formation of the transient regenerative membrane, formed by the epithelial morphogenesis—spreading of the intact exopinacoderm and choanoderm. The spreading of the choanoderm is accompanied by the transdifferentiation of the choanocytes. The regenerative membrane develops without any contribution of the mesohyl cells. Subsequently, the membrane gradually transforms into the body wall. The cell proliferation is neither affected nor contributes to the regeneration at any stage. Thus, Leucosolenia cf. variabilis regeneration relies on the remodeling of the intact tissues through the epithelial morphogenesis, accompanied by the transdifferentiation of some differentiated cell types, which makes it similar to the regeneration in homoscleromorphs and eumetazoans.

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“…In the siliceous and calcareous sponges, stolons can take a variety of forms, including creeping stolons (e.g. the calcareous sponge Leucosolenia ; Padua & Klautau ) and reinforced structural stolons (e.g. the carnivorous demosponge Chondrocladia lyra ; Lee et al .…”

Section: Discussionmentioning

confidence: 99%

Anatomical and ontogenetic reassessment of the Ediacaran frond Arborea arborea and its placement within total group Eumetazoa

2019

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Organisms in possession of a frondose body plan are amongst the oldest and most enigmatic members of the soft-bodied Ediacaran macrobiota. Appraisal of specimens from the late Ediacaran Ediacara Member of South Australia reveals that the frondose taxon Arborea arborea probably possessed a fluid-filled holdfast disc, the size and form of which could vary within populations. Mouldic preservation of internal anatomical features provides evidence for tissue differentiation, and for bundles of tubular structures within the stalk of the organism. These structures connect in a fascicled arrangement to individual lateral branches, before dividing further into individual units

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Regeneration in calcareous sponges (Porifera)

Cited by 9 publications

References 27 publications

Fast transcriptional activation of developmental signalling pathways during wound healing of the calcareous sponge Sycon ciliatum

Fast transcriptional activation of developmental signalling pathways during wound healing of the calcareous sponge Sycon ciliatum

Sewing up the wounds : The epithelial morphogenesis as a central mechanism of calcaronean sponge regeneration

Anatomical and ontogenetic reassessment of the Ediacaran frond Arborea arborea and its placement within total group Eumetazoa

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