Morphological, cellular and molecular characterization of posterior regeneration in the marine annelid Platynereis dumerilii

Planques, Anabelle; Malem, Julien; Parapar, Julio; Vervoort, Michel; Gazave, Eve

doi:10.1016/j.ydbio.2018.11.004

Cited by 61 publications

(190 citation statements)

References 62 publications

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“…Wound healing in M. leidyi takes place through changes in cell behavior and occurs normally in the absence of cell proliferation. This observation is consistent with the majority of animal models of regeneration found in cnidarians [12, 20, 42–44] as well as with the more phylogenetically distantly related marine annelid worm Platynereis dumerilii [37]. Following wound healing and prior to activation of cell proliferation in M. leidyi , there is remodeling of the tissue surrounding the wound and small numbers of round-shaped cells sparsely congregate at the wound site suggesting a reorganization of the tissue in order to prepare it for regeneration.…”

Section: Discussionsupporting

confidence: 87%

“…To investigate the source of cells that contribute to the formation of new tissue during ctenophore regeneration, we performed a series of EdU pulse and chase experiments in regenerating cydippids. This technique has been successfully used in different model systems as a strategy to indirectly track populations of proliferating cells and determine their contribution to the formation of new structures [19, 37]. With the aim of determining whether cells proliferating before amputation contribute to the formation of new tissues, uncut cydippids were incubated in EdU, which was incorporated into cells undergoing the S phase of cell cycle.…”

Section: Resultsmentioning

confidence: 99%

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Regeneration in the ctenophore Mnemiopsis leidyi occurs in the absence of a blastema, requires cell division, and is temporally separable from wound healing

et al. 2019

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Background The ability to regenerate is a widely distributed but highly variable trait among metazoans. A variety of modes of regeneration has been described for different organisms; however, many questions regarding the origin and evolution of these strategies remain unanswered. Most species of ctenophore (or “comb jellies”), a clade of marine animals that branch off at the base of the animal tree of life, possess an outstanding capacity to regenerate. However, the cellular and molecular mechanisms underlying this ability are unknown. We have used the ctenophore Mnemiopsis leidyi as a system to study wound healing and adult regeneration and provide some first-time insights of the cellular mechanisms involved in the regeneration of one of the most ancient extant group of multicellular animals. Results We show that cell proliferation is activated at the wound site and is indispensable for whole-body regeneration. Wound healing occurs normally in the absence of cell proliferation forming a scar-less wound epithelium. No blastema-like structure is generated at the cut site, and pulse-chase experiments and surgical intervention show that cells originating in the main regions of cell proliferation (the tentacle bulbs) do not seem to contribute to the formation of new structures after surgical challenge, suggesting a local source of cells during regeneration. While exposure to cell-proliferation blocking treatment inhibits regeneration, the ability to regenerate is recovered when the treatment ends (days after the original cut), suggesting that ctenophore regenerative capabilities are constantly ready to be triggered and they are somehow separable of the wound healing process. Conclusions Ctenophore regeneration takes place through a process of cell proliferation-dependent non-blastemal-like regeneration and is temporally separable of the wound healing process. We propose that undifferentiated cells assume the correct location of missing structures and differentiate in place. The remarkable ability to replace missing tissue, the many favorable experimental features (e.g., optical clarity, high fecundity, rapid regenerative performance, stereotyped cell lineage, sequenced genome), and the early branching phylogenetic position in the animal tree, all point to the emergence of ctenophores as a new model system to study the evolution of animal regeneration.

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Section: Discussionsupporting

confidence: 87%

Section: Resultsmentioning

confidence: 99%

Regeneration in the ctenophore Mnemiopsis leidyi occurs in the absence of a blastema, requires cell division, and is temporally separable from wound healing

et al. 2019

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“…In order to identify putative regeneration-related genes in these species, BLAST searches were performed against our transcriptomes using publicly available sequences of those genes that have been previously shown to be (highly) expressed during regeneration in other annelids (Table 2; Additional file 4) [1, 2, 12, 13, 17, 21, 23, 27, 32, 35, 45, 46, 48, 59–63].…”

Section: Resultsmentioning

confidence: 99%

“…[36–44]). Interestingly, some genes that are expressed in the SAZ during regular growth/development have been detected in different stages of posterior regeneration in annelids, for example, Hox genes [21–23, 27, 45], β- catenin [17], and genes of the germline multipotency program such as piwi , vasa , nanos , and PL10 [27, 46–48].…”

Section: Introductionmentioning

confidence: 99%

Comparative transcriptomics in Syllidae (Annelida) indicates that posterior regeneration and regular growth are comparable, while anterior regeneration is a distinct process

et al. 2019

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BackgroundAnnelids exhibit remarkable postembryonic developmental abilities. Most annelids grow during their whole life by adding segments through the action of a segment addition zone (SAZ) located in front of the pygidium. In addition, they show an outstanding ability to regenerate their bodies. Experimental evidence and field observations show that many annelids are able to regenerate their posterior bodies, while anterior regeneration is often limited or absent. Syllidae, for instance, usually show high abilities of posterior regeneration, although anterior regeneration varies across species. Some syllids are able to partially restore the anterior end, while others regenerate all lost anterior body after bisection. Here, we used comparative transcriptomics to detect changes in the gene expression profiles during anterior regeneration, posterior regeneration and regular growth of two syllid species: Sphaerosyllis hystrix and Syllis gracilis; which exhibit limited and complete anterior regeneration, respectively.ResultsWe detected a high number of genes with differential expression: 4771 genes in S. hystrix (limited anterior regeneration) and 1997 genes in S. gracilis (complete anterior regeneration). For both species, the comparative transcriptomic analysis showed that gene expression during posterior regeneration and regular growth was very similar, whereas anterior regeneration was characterized by up-regulation of several genes. Among the up-regulated genes, we identified putative homologs of regeneration-related genes associated to cellular proliferation, nervous system development, establishment of body axis, and stem-cellness; such as rup and JNK (in S. hystrix); and glutamine synthetase, elav, slit, Hox genes, β-catenin and PL10 (in S. gracilis).ConclusionsPosterior regeneration and regular growth show no significant differences in gene expression in the herein investigated syllids. However, anterior regeneration is associated with a clear change in terms of gene expression in both species. Our comparative transcriptomic analysis was able to detect differential expression of some regeneration-related genes, suggesting that syllids share some features of the regenerative mechanisms already known for other annelids and invertebrates.

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“…José García-Arrarás (University of Puerto Rico, San Juan, Purto Rico, USA) showed that Wnt signalling is crucial for dedifferentiation and regeneration of the lost tissues. Anabelle Planques (Vervoort Laboratory; Institut Jacques Monod, Paris, France) characterised posterior regeneration following amputation in the annelid Platynereis, showing that proliferating cells of the regenerating structure have a local origin, and that the process is rapid and reproducible (Planques et al, 2018). An alternative to axonal regeneration is the re-innervation after lesioning that occurs in the peripheral nervous system of the cephalopod Octopus vulgaris (Imperadore et al, 2017), as shown by Pamela Imperadore (Association for Cephalopod Research-CephRes, Naples, Italy).…”

Section: Regeneration Across the Animal Kingdommentioning

confidence: 99%

Repair, regenerate and reconstruct: meeting the state-of-the-art

2019

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The seventh EMBO meeting on the Molecular and Cellular Basis of Regeneration and Tissue Repair took place in Valletta, Malta, in September 2018. Researchers from all over the world gathered together with the aim of sharing the latest advances in wound healing, repair and regeneration. The meeting covered a wide range of regeneration models and tissues, identification of regulatory genes and signals, and striking advances toward regenerative therapies. Here, we report some of the exciting topics discussed during this conference, highlighting important discoveries in regeneration and the perspectives for regenerative medicine.

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Morphological, cellular and molecular characterization of posterior regeneration in the marine annelid Platynereis dumerilii

Cited by 61 publications

References 62 publications

Regeneration in the ctenophore Mnemiopsis leidyi occurs in the absence of a blastema, requires cell division, and is temporally separable from wound healing

Regeneration in the ctenophore Mnemiopsis leidyi occurs in the absence of a blastema, requires cell division, and is temporally separable from wound healing

Comparative transcriptomics in Syllidae (Annelida) indicates that posterior regeneration and regular growth are comparable, while anterior regeneration is a distinct process

Repair, regenerate and reconstruct: meeting the state-of-the-art

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