Possibility of mixed progenitor cells in sea star arm regeneration

Abstract

In contrast to most vertebrates, invertebrate deuterostome echinoderms, such as the sea star Asterias rubens, undergo regeneration of lost body parts. The current hypothesis suggests that differentiated cells are the main source for regenerating arm in sea stars, but there is little information regarding the origin and identity of these cells. Here, we show that several organs distant to the regenerating arm responded by proliferation, most significantly in the coelomic epithelium and larger cells of the pyloric caeca. Analyzing markers for proliferating cells and parameters indicating cell ageing, such as levels of DNA damage, pigment, and lipofuscin contents as well as telomere length and telomerase activity, we suggest that cells contributing to the new arm likely originate from progenitors rather than differentiated cells. This is the first study showing that cells of mixed origin may be recruited from more distant sources of stem/progenitor cells in a sea star, and the first described indication of a role for pyloric caeca in arm regeneration. Data on growth rate during arm regeneration further indicate that regeneration is at the expense of whole animal growth. We propose a new working hypothesis for arm regeneration in sea stars involving four phases: wound healing by coelomocytes, migration of distant progenitor cells of mixed origin including from pyloric caeca, proliferation in these organs to compensate for cell loss, and finally, local proliferation in the regenerating arm.

Long telomeres are associated with clonality in wild populations of the fissiparous starfish Coscinasterias tenuispina

“…In Asterias rubens, a sexually reproducing starfish, telomerase activity is high throughout the animal irrespectively of mitotic activity and there was no difference in telomerase activity nor telomere length between regenerating and non-regenerating arms (Hernroth et al, 2010), but clonal starfishes may have higher telomerase activities after fission as other asexual species. In flatworms, maintenance of somatic telomere length seems to be an adaptation of asexual but not sexual strains, and is based on different levels of telomerase activity (Tan et al, 2012).…”

“…Pyloric caeca tissue was considered in the present analysis because it is a distinct tissue that has further been shown to be involved in arm regeneration (Hernroth et al, 2010). Although gonads may be also considered for the telomere length analysis, they cannot be used in this study because more than 50% of the individuals of the species lack gonads, even during the reproductive season (Crozier, 1921).…”

Potential for clonal animals in longevity and ageing studies

“…Recent work on arm regeneration in the sea star Asterias rubens has shown regenerating arms to have less DNA damage, lipofuscin and overall tissue pigmentation than the other 'old' arms in the same animal. A degree of rejuvenation is therefore evident during arm regeneration where the new arm is physiologically younger (Hernroth et al 2010). Whilst A. rubens is not clonal, we can presume that rejuvenation during arm regeneration is also present in clonal sea stars, given that the new arms that grow out after somatic fission in such animals also are considerably less pigmented (Fig.…”

“…Arrows indicate regenerating arms and arrowhead a normal arm. Note the lesser degree of tissue pigmentation in the regenerating arms of the clonal individual not known whether the characteristically uneven distribution of 'young' versus 'old' material in these animals is due to repair or physical segregation, or both, in many species the new body parts appear to be commonly derived from progenitor cells (Laird et al 2005;Salo 2006;Bosch 2009;Watanabe et al 2009;Nilsson Sköld et al 2009;Hernroth et al 2010). Work on stem cells and progenitor cells in humans shows evidence of both elevated repair and maintenance systems, as well as uneven segregation of old material (Quyn et al 2010).…”

The coelomic epithelium transcriptome from a clonal sea star, Coscinasterias muricata

“…1A). It responds to several stimuli by extensive cell proliferation and it is involved in a range of important processes such as wound healing, regeneration and haematopoiesis (Holm et al, 2008;Hernroth et al, 2010). Despite the obvious wide relevance of this tissue, a molecular survey of its transcriptome has not been conducted, limiting deeper analysis of its functions.…”