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

Abstract

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.

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

“…A long-standing debate in the annelid regeneration field is the cellular source of the cells of the regenerated region (e.g., Bely, 2014;de Jong and Seaver, 2017;Zattara et al, 2016). This debate covers in fact two distinct questions.…”

“…In addition, targeted destructions of cells of different segments have indicated that only the cells of the segment abutting the amputation site were required for regeneration. A very different view has emerged from studies made on Sedentaria annelids, which suggested the involvement of migratory stem cells in regeneration of some species (e.g., Bely, 2014;de Jong and Seaver, 2017;Myohara, 2012;Özpolat and Bely, 2016;Zattara et al, 2016), opening the possibility that profoundly different mechanisms of blastema formation may exist in Errantia and Sedentaria annelids.…”

“…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).…”

Expression of vasa, piwi, and nanos during gametogenesis in Typosyllis antoni (Annelida, Syllidae)

“…These three putative stem-cell markers are usually linked to the differentiation of PGCs, the development of gonads, and the post-embryonic posterior growth. They have been studied in A. virens (Kozin & Kostyuchenko, 2015), C. teleta (de Jong & Seaver, 2017;Dill & Seaver, 2008;Giani, Yamaguchi, Boyle, & Seaver, 2011), Enchytraeus japonensis (Sugio et al, 2008;Sugio, Yoshida-Noro, Ozawa, & Tochinai, 2012;Tadokoro, Sugio, Kutsuna, Tochinai, & Takahashi, 2006;Yoshida-Noro & Tochinai, 2010), Helobdella robusta (Agee, Lyons, & Weisblat, 2006;Cho, Vallès, & Weisblat, 2014;Kang, Pilon, & Weisblat, 2002), Myzostoma cirriferum (Weigert, Helm, Hausen, Zakrzewski, & Bleidorn, 2013), P. dumerilii Rebscher, Lidke, & Ackermann, 2012;Rebscher, Zelada-González, Banisch, Raible, & Arendt, 2007), Pristina leidyi (Özpolat & Bely, 2015;Özpolat, Sloane, Zattara, & Bely, 2016), and T. tubifex (Oyama & Shimizu, 2007).…”

General characterization of regeneration in Aeolosoma viride

“…For example, the naidid Pristina leidyi mostly reproduce by paratomic fission and is able to complete both anterior and posterior regeneration [11]. In contrast, the capitellid polychaete Capitella teleta mostly reproduce sexually and is only capable to partially regenerate its posterior end [15]. Such a difference may reflect a connection between asexual reproduction by paratomic fission and regeneration [9, 12, 16].…”