Long-term time-lapse live imaging reveals extensive cell migration during annelid regeneration

Zattara, Eduardo E.; Turlington, Kate W.; Bely, Alexandra E.

doi:10.1186/s12861-016-0104-2

Cited by 41 publications

(34 citation statements)

References 59 publications

(48 reference statements)

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“…For example, EdU incorporation only labels cells that are undergoing DNA synthesis at the time of exposure, and thus the 1 h pulses used in these experiments will probably only label a subset of a larger population of actively dividing cells. In addition, it is also possible that non‐dividing cells (e.g., differentiated cell types) also migrate, as reported in previous studies (see Bely, ), including in a live imaging study in Pristina leidyi (Zattara et al., ). These non‐proliferating migrating cells could then undergo a dedifferentiation or transdifferentiation step when they reach their final destination, or be part of an early immune response to the wound.…”

Section: Discussionmentioning

confidence: 71%

“…Some of these migrating cells are thought to mediate an immune response, although one population known as neoblasts (Randolph, , ), have been classified as a putative stem cell population. To date, cells that closely fit the description of neoblasts have been described mostly in clitellates, but also in some polychaetes (Bilello & Potswald, ; Cornec, Cresp, Delye, Hoarau, & Reynaud, ; Faulkner, , ; Krecker, ; Probst, ; Randolph, , ; Stephan‐Dubois, ; Stolte, ; Sugio et al., ; Tadokoro, Sugio, Kutsuna, Tochinai, & Takahashi, ; Zattara, Turlington, & Bely, ). Regeneration abilities are not limited to species with neoblasts; annelids that lack cells with obvious neoblast characteristics can regenerate (Herlant‐Meewis, ; Krecker, ; Myohara, ; Stone, ).…”

Section: Introductionmentioning

confidence: 86%

“…Annelids, the segmented worms, have long been models for regeneration studies, due to their impressive regeneration abilities and the wide range of regenerative abilities in this phylum (see Bely, ; Berrill, ). There has been an ongoing debate regarding the cellular source of the regenerated tissue in annelids, and most studies have been based on examination of fixed tissue (see Bely, ), with a recent exception of a live imaging study in the annelid Pristina leidyi (Zattara, Turlington, & Bely, ). From these studies, it appears that many of the cells that contribute to the blastema arise locally from the area of the wound site.…”

Section: Introductionmentioning

confidence: 99%

“…In addition, migration of multiple cell types to the wound site has been reported in a diverse number of animals, such as cnidarians, planarians, zebrafish, and axolotls (Bradshaw, Thompson, & Frank, 2015;McCusker, Bryant, & Gardiner, 2015;Reddien & Alvarado, 2004;Tahara, Brush, & Kawakami, 2016). the description of neoblasts have been described mostly in clitellates, but also in some polychaetes (Bilello & Potswald, 1974;Cornec, Cresp, Delye, Hoarau, & Reynaud, 1987;Faulkner, 1929Faulkner, , 1932Krecker, 1923;Probst, 1931;Randolph, 1891Randolph, , 1892Stephan-Dubois, 1954;Stolte, 1929;Sugio et al, 2008;Tadokoro, Sugio, Kutsuna, Tochinai, & Takahashi, 2006;Zattara, Turlington, & Bely, 2016). Regeneration abilities are not limited to species with neoblasts; annelids that lack cells with obvious neoblast characteristics can regenerate (Herlant-Meewis, 1964;Krecker, 1923;Myohara, 2012;Stone, 1933).…”

Section: Introductionmentioning

confidence: 99%

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Investigation into the cellular origins of posterior regeneration in the annelid Capitella teleta

Jong

Seaver

2017

Regeneration

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Many animals can regenerate, although there is great diversity in regenerative capabilities. A major question in regenerative biology is determining the cellular source of newly formed tissue. The polychaete annelid, Capitella teleta, can regenerate posterior segments following transverse amputation. However, the source, behavior and molecular characteristics of the cells that form new tissue during regeneration are largely unknown. Using an indirect cell tracking method involving 5′‐ethynyl‐2′‐deoxyuridine (EdU) incorporation, we show that cell migration occurs during C. teleta posterior regeneration. Expression of the multipotency/germ line marker CapI‐vasa led us to hypothesize that stem cells originate from a multipotent progenitor cell (MPC) cluster, migrate through the coelomic cavity, and contribute to regeneration of tissue. We show that the capacity for posterior regeneration and segment formation is greater with than without the MPC cluster. Finally, we propose a working model of posterior regeneration in C. teleta. This work is the first in C. teleta that addresses the potential source of cells contributing to posterior regeneration, and may provide clues as to why some animals are highly successful regenerators.

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Section: Discussionmentioning

confidence: 71%

Section: Introductionmentioning

confidence: 86%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Investigation into the cellular origins of posterior regeneration in the annelid Capitella teleta

Jong

Seaver

2017

Regeneration

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“…Most of these species belong to one of the two main clades of the phylum Annelida, the Sedentaria (Struck et al, 2011). In these species, indirect evidence for an involvement of neoblast-like resident stem cells during regeneration, such as the presence in non-injured animals of cells that express homologues of genes known to be expressed in flatworm neoblasts and the observation of long distance migration of cells towards the amputation site, have been obtained (e.g., Bely, 2014;de Jong and Seaver, 2017;Myohara, 2012;Özpolat and Bely, 2016;Zattara et al, 2016). In the other main annelid group, the Errantia, the presence of neoblast-like cells is much more elusive and there are in contrast experimental evidence indicating that regenerated structures only originate from cells located close to the amputation site, probably through dedifferentiation events (e.g., Boilly, 1965a,b;Boilly, 1968a,b;Boilly, 1969a,b,c).…”

Section: Introductionmentioning

confidence: 99%

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

Planques¹,

Malem²,

Parapar³

et al. 2018

Preprint

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Regeneration, the ability to restore body parts after an injury or an amputation, is a widespread but highly variable and complex phenomenon in animals. While having fascinating scientists for centuries, fundamental questions about the cellular basis of animal regeneration as well as its evolutionary history remain largely unanswered. We study regeneration of the marine annelid Platynereis dumerilii, an emerging comparative developmental biology model, which, like many other annelids, displays important regenerative abilities. If the posterior part of the body is amputated, P. dumerilii worms are able to regenerate the posteriormost differentiated part of the body and stem cell-rich growth zone that allows to make new segments which replace the amputated ones. We show that posterior regeneration is a rapid process that follows a well reproducible paths and timeline, going through specific stages that we thoroughly defined. Wound healing is achieved by one day post-amputation and a regeneration blastema forms one day later. At this time point, some tissue specification already occurs, and a functional posterior growth zone is re-established as early as three days after amputation. Regeneration is only influenced in a minor manner by worm size and position of the amputation site along the anteroposterior axis of the worm and regenerative abilities persist upon repeated amputations without important alterations of the process. We also show that intense cell proliferation occurs during regeneration and that cell divisions are strictly required for regeneration to normally proceed. Finally, through several 5-ethynyl-2'-deoxyuridine (EdU) pulse and chase experiments, we provide evidence in favor of a local origin of the blastema, whose constituting cells mostly derive from the segment immediately abutting the amputation plane. The detailed characterization of P. dumerilii posterior body regeneration presented in this article provides the foundation for future mechanistic and comparative studies of regeneration in this species.

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Distinct patterns of gene expression during regeneration and asexual reproduction in the annelid Pristina leidyi

2022

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Regeneration, the ability to replace lost body parts, is a widespread phenomenon in the animal kingdom often connected to asexual reproduction or fission, since the only difference between the two appears to be the stimulus that triggers them. Both developmental processes have largely been characterized; however, the molecular toolkit and genetic mechanisms underlying these events remain poorly unexplored.Annelids, in particular the oligochaete Pristina leidyi, provide a good model system to investigate these processes as they show diverse ways to regenerate, and can reproduce asexually through fission under laboratory conditions. Here, we used a comparative transcriptomics approach based on RNA-sequencing and differential gene expression analyses to understand the molecular mechanisms involved in anterior regeneration and asexual reproduction. We found 291 genes upregulated during anterior regeneration, including several regeneration-related genes previously reported in other annelids such as frizzled, paics, and vdra. On the other hand, during asexual reproduction, 130 genes were found upregulated, and unexpectedly, many of them were related to germline development during sexual reproduction. We also found important differences between anterior regeneration and asexual reproduction, with the latter showing a gene expression profile more similar to that of control individuals. Nevertheless, we identified 35 genes that were upregulated in both conditions, many of them related to cell pluripotency, stem cells, and cell proliferation. Overall, our results shed light on the molecular mechanisms that control anterior regeneration and asexual reproduction in annelids and reveal similarities with other animals, suggesting that the genetic machinery controlling these processes is conserved across metazoans.

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Long-term time-lapse live imaging reveals extensive cell migration during annelid regeneration

Cited by 41 publications

References 59 publications

Investigation into the cellular origins of posterior regeneration in the annelid Capitella teleta

Investigation into the cellular origins of posterior regeneration in the annelid Capitella teleta

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

Distinct patterns of gene expression during regeneration and asexual reproduction in the annelid Pristina leidyi

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