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Recovery process in sponges: morphogeneses and cell sources

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HAL Id: hal-02354447

https://hal.archives-ouvertes.fr/hal-02354447

Submitted on 7 Nov 2019

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Recovery process in sponges: morphogeneses and cell sources

Andrey Lavrov, Fyodor Bolshakov, Ilya Borisenko, Veronika Frolova, Daria Tokina, Alexander Ereskovsky

To cite this version:

Andrey Lavrov, Fyodor Bolshakov, Ilya Borisenko, Veronika Frolova, Daria Tokina, et al.. Recovery process in sponges: morphogeneses and cell sources. Omics approaches to identify and characterize Marine/Aquatic Invertebrate stam cells, Apr 2019, Peniche, Portugal. �hal-02354447�

(2)

Recovery process in sponges: morphogeneses and

cell sources

Andrey Lavrov

1,2

, Fyodor Bolshakov

1,2

, Ilya Borisenko

2

, Veronika Frolova

3

, Daria Tokina

4

,

Alexander Ereskovsky

2,4

1 Pertsov White Sea Biological Station, Biological faculty, Lomonosov Moscow State University, Moscow, Russia; 2 Department of Embryology, Biological faculty, Saint-Petersburg State University, Saint-Petersburg, Russia;

3 Department of Embryology, Biological faculty, Lomonosov Moscow State University, Moscow, Russia;

4 Institut Méditerranéen de Biodiversité et d’Ecologie marine et continentale (IMBE), Aix Marseille University, CNRS, IRD, Marseille, France

Financial support: Russian Science Foundation, no. 17-14-01089; Russian Foundation for Basic Research nos.

19-04-00545, 19-04-00563

CONCLUSION

During recovery processes, sponges utilize diverse and complex morphogenetic mechanisms, with a particular importance of cell transdifferentiation. While all sponges demonstrate high recovery abilities, the morphogeneses and cell sources for the recovery of lost structures varies in different clades.

INTRODUCTION

Sponges (phylum Porifera) are one of the most ancient multicellular animals, which have the peculiar histological structure. They demonstrate a high plasticity and mobility of all tissues and cells in their body. One of the forms of manifestation of such plasticity is outstanding recovery abilities of sponges, ranging from wound healing to re-building of a functional body from dissociated cells. Sponges show a wide diversity of regeneration mechanisms and, thus, are exceptionally important for understanding the evolution of animal regeneration mechanisms. However, only a few reliable data on the mechanisms (morphogenesis, cell behavior, and regulation) of sponge regeneration and its distribution among sponge clades exists for now.

Choanocytes

Endopinacocytes

Exopinacocytes Mineral and organic

skeletal elements

Cells with inclusions

Secreting cells Amoebocytes

Mesohyl

GENERAL ORGANIZATION OF SPONGE

STUDIED SPECIES

Leucosolenia variabilis Sycon sp. Clathrina arnesenae Halisarca dujardinii Aplysina cavernicola

CELL REAGGREGATION

Intact tissues Heterogenous pool of amoebocytes Choanocytes Sclerocytes Amoebocytes Exopinacocytes Heterogenous pool of amoebocytes Porocytes Choanocytes Exopinacocytes Primary multicellular aggregates Primmorphs

Calcarea (L. variabilis, Sycon sp., C. arnesenae)

Demospongiae (H. dujardinii)

Intact tissues Primary multicellular aggregates Choanocytes Lophocytes Nucleolar amoebocytes Exopinacocytes Endopinacocytes Primmoprhs Reconstructed sponge Heterogenous pool of nucleolar amoebocytes

Exopinacocytes Cell with inclusions Nucleolar amoebocytes Choanocytes Lophocytes Endopinacocytes Cell with inclusions

REPARATIVE REGENERATION

Pri mary multicel lular aggr egates Pri mmoprhs Aqu ifer ous system devel opment Reconstructed sponge 3 µm Functional aquiferous system Exopinacoderm formation No internal structures Aquiferous system formation Pri mary multicel lular aggr egates Pri mmoprhs Aqu ifer ous system & sk ele ton devel opment Exopinacoderm formation Choanocyte chamber Irregular structure and bubbles on the surface

Calcarea (L. variabilis)

Demospongiae (H. dujardinii, A. cavernicola)

The regeneration in Leucosolenia represents a rare example of the «true» morphallaxis. All processes occur solely through spreading and fusion of the epithelia surrounding the wound, accompanied by the transdifferentiation of the choanocytes and exopinacocytes. There are no changes in activity and distribution pattern in the proliferating cells, in both tissues, adjacent and distant from the wound. There are also no blastema nor any elements of mesenchymal-epithelial transitions. The transdifferentiation capacity of choanocytes and their involvement in regeneration supports the hypothesis that these cells combine features of somatic and stem cells. Choanocyte flattening 0 h 12 h 24 h 4-6 d Exopinacocyte Endopinacocyte Intact body wall Regenerative membrane

Endopinacocyte Intact choanocyte

1) The main mechanism during regeneration in Demospongiae is a mesenchymal morphogenesis by mesenchymal-epithelial transformations.

2) This regeneration involves intervention of polypotent cells

-archaeocytes and choanocytes - that migrate to the injured area where form

a blastema with dedifferentiated cells.

3) The regeneration in Halisarca has epimorphosis features that require blastema formation, active cellular dedifferentiation and proliferation prior to the replacement of the lost body part.

4) There are three main sources of the new exopinacoderm during regeneration: choanocytes, archaeocytes and (rarely) endopinacocytes.

Endopinacocytes Exopinacocytes

Choanocytes

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