Abstract
The crucial step in any regeneration process is epithelization, i.e. the restoration of an epithelium structural and functional integrity. Epithelization requires cytoskeletal rearrangements, primarily of actin filaments and microtubules. Sponges (phylum Porifera) are early branching metazoans with pronounced regenerative abilities. Calcareous sponges have a unique step during regeneration: the formation of a temporary structure, called regenerative membrane which initially covers a wound. It forms due to the morphallactic rearrangements of exopinaco- and choanoderm epithelial-like layers. The current study quantitatively evaluates morphological changes and characterises underlying actin cytoskeleton rearrangements during regenerative membrane formation in asconoid calcareous sponge Leucosolenia variabilis through a combination of time-lapse imaging, immunocytochemistry, and confocal laser scanning microscopy. Regenerative membrane formation has non-linear stochastic dynamics with numerous fluctuations. The pinacocytes at the leading edge of regenerative membrane form a contractile actomyosin cable. Regenerative membrane formation either depends on its contraction or being coordinated through it. The cell morphology changes significantly during regenerative membrane formation. Exopinacocytes flatten, their area increases, while circularity decreases. Choanocytes transdifferentiate into endopinacocytes, losing microvillar collar and flagellum. Their area increases and circularity decreases. Subsequent redifferentiation of endopinacocytes into choanocytes is accompanied by inverse changes in cell morphology. All transformations rely on actin filament rearrangements similar to those characteristic of bilaterian animals. Altogether, we provide here a qualitative and quantitative description of cell transformations during reparative epithelial morphogenesis in a calcareous sponge.
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Data availability
Raw data were generated at Lomonosov Moscow State University, Faculty of Biology. Derived data supporting the findings of this study are available from the corresponding author Kseniia V. Skorentseva (skorentseva.ksenya.2016@post.bio.msu.ru) on request. Raw images used in this study are available in the Mendeley Data repository, https://data.mendeley.com/datasets/28g3jt3c22 (Figures, https://doi.org/10.17632/28g3jt3c22.1) and https://data.mendeley.com/datasets/s96kd597gr (Online Resources, https://doi.org/10.17632/s96kd597gr.1).
Abbreviations
- AR:
-
Aspect ratio
- CLSM:
-
Confocal laser scanning microscopy
- DAPI:
-
4′,6-Diamidino-2-phenylindole
- ECM:
-
Extracellular matrix
- EMT:
-
Epithelial-mesenchymal transition
- FSW:
-
Filtered seawater
- GTPase:
-
Nucleotide guanosine triphosphate (GTP) hydrolase
- hpo:
-
Hours post operation
- MET:
-
Mesenchymal-epithelial transition
- MLCK:
-
Myosin light-chain kinase
- RM:
-
Regenerative membrane
- PBS:
-
Phosphate-buffered saline
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Acknowledgements
The authors acknowledge the support of Lomonosov Moscow State University Program of Development (Nikon A1 CLSM) and Centre of microscopy WSBS MSU. The authors sincerely thank Daniyal Saidov (Lomonosov Moscow State University) for statistical analysis tips, Elena Voronezhskaya (Koltzov Institute of Developmental Biology of Russian Academy of Sciences) for fixation recommendations, and Nikolay Melnikov, Anastasiia Kovaleva, Anna Tvorogova, Stanislav Kremnyov (Lomonosov Moscow State University), and Alexander Ereskovsky (Koltzov Institute of Developmental Biology of Russian Academy of Sciences) for helpful tips and advice.
Funding
The research was supported by the Russian Foundation for Basic Research project no. 21-54-15006 and by Governmental Basic Research Program for the Koltzov Institute of Developmental Biology of the Russian Academy of Sciences no. 0088-2021-0009 (Kseniia Skorentseva).
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KS, AL, and AS designed the study. KS, AL, and FB collected the material, carried out CLSM cytoskeleton studies, and analysed and visualised the data. KS conducted experiments and performed statistical analysis and its visualisation as well as time-lapse imaging and its post-processing. AL, KS, and AS prepared the manuscript with contributions from all authors. All authors reviewed and approved the final manuscript.
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Online Resource 1. Scheme illustrating experimental procedures. FSW – filtered sea water; hpo – hours post operation; RM – regenerative membrane. (TIF 7776 KB)
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Online Resource 2. Morphometric cell parameters (area, circularity, aspect ratio), raw data, epithelial-like cell layers. (XLSX 44 KB)
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Online Resource 3. Morphometric cell parameters (area, circularity, aspect ratio), raw data, mesohyl cells. (XLSX 17 KB)
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Online Resource 5. Sclerocytes with stress fibers in intact tissues; ice-cold MeOH and then 4% PFA in PBS fixation; CLSM (maximum intensity projection of several focal planes); cyan – DNA, DAPI; yellow – actin filaments, antibody staining; magenta – non-muscle myosin II, antibody staining. Scale bar: 5 μm. (TIF 10447 KB)
Online Resource 6. Regenerative membrane growth and sealing (part 1); exopinacocytes trembling and mesohyl cells migration in a fully sealed regenerative membrane (part 2). Time-lapse imaging. Video runs at 225–235× real time. Red arrows indicate filopodial activity at the leading edge of RM. Scale bar 50 μm. (MP4 29751 KB)
Online Resource 7. Mechanical tension causes RM tearing and leading edge retraction. Time-lapse imaging. Video runs at 295× real time. (MP4 24410 KB)
Online Resource 8. Sclerocytes synthesising spicules in the regenerative membrane. Time-lapse imaging. Video runs at 225× real time. (MP4 14186 KB)
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Online Resource 9. Non-muscle myosin II antibodies (Sigma-Aldrich M8064) verification data. (a) – phylogenetic tree of myosin heavy chains presented in Leucosolenia variabilis. Tree constructed using with ML (IQTree-Web Server, best model LG + I + G4, 1000 bootstrap alignments with SH-aLTR test) method. Numbers on the branch indicate the ML bootstrap values. (b) IEDB “Epitope conservancy tool” results. (TIF 21533 KB)
Online Resource 10. Blebbistatin treatment causes retraction of regenerative membrane leading edge. Time-lapse imaging. Video runs at 360× real time. (MP4 26642 KB)
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Online Resource 11. Wound edge, 1 hpo. Black arrows point towards transdifferentiating choanocytes of the inner side of the body wall. Scanning electron microscopy. Sample preparation described in Lavrov et al. (2018). (TIF 14036 KB)
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Skorentseva, K.V., Bolshakov, F.V., Saidova, A.A. et al. Regeneration in calcareous sponge relies on ‘purse-string’ mechanism and the rearrangements of actin cytoskeleton. Cell Tissue Res 394, 107–129 (2023). https://doi.org/10.1007/s00441-023-03810-5
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DOI: https://doi.org/10.1007/s00441-023-03810-5