Siphon regeneration capacity is compromised during aging in the ascidian Ciona intestinalis

Abstract

The ascidian Ciona intestinalis has a short life span and powerful regeneration capacities. The regeneration of the oral siphon (OS) involves wound healing, blastema formation, cell proliferation, and replacement of eight oral pigment organs (OPO), the latter via differentiation and migration of stem/precursor cells from localized siphon niches in the siphon. The restoration of OPO pattern during OS regeneration occurs with a high degree of accuracy through three successive cycles of amputation. It is shown here that oral siphons of the largest and oldest members of a wild Ciona population do not completely regenerate their siphons after amputation. The loss of regeneration capacity was accompanied by reduced cell proliferation. In contrast to arrested OS outgrowth, the stem/precursor cells responsible for OPO replacement “over-differentiate” after OS amputation in the oldest animals, the typical number of OPO is increased from eight to twelve-sixteen, and malformed OPO are produced. Also in contrast to younger animals, the oldest animals of the population show arrested OPO development after two consecutive cycles of amputation and regeneration. We conclude that there is a size and age threshold in Ciona after which the regenerative capacity of the OS is compromised due to effects of aging on cell proliferation.

Regeneration, Stem Cells, and Aging in the Tunicate Ciona

“…Although OPO replacement can occur (albeit defectively) in old animals, they do not develop a blastema of proliferating cells (Fig. 8D) (Jeffery, 2012). Accordingly, old animals do not replace muscle cells and regain the ability for siphon contraction.…”

“…Even though there is no net siphon growth after amputation in old animals, OPO replacement still occurs, although it shows several differences from normal replacement in younger animals (Jeffery, 2012). First, when the oral siphons of old animals are amputated in the tube, OPO replacement occurs, but multiple OPO are formed in the place of the original single OPO.…”

“…Recent studies of Ciona regeneration have focused on the oral siphon as a model (Auger et al, 2010;Jeffery, 2012;. The oral siphon is a thin muscular tube covered by tunic on its outer side ( Fig.…”

“…Regenerative aging of the NC and oral siphon have been observed in both natural marine environments and laboratory cultures (Dahlberg et al, 2009;Auger et al, 2010;Jeffery, 2012;. In wild collected adults, regeneration capacity during the life cycle was evaluated using size (e. g. distal to proximal length) as a proxy for age.…”

“…This situation changes as animals reach an age threshold, when the capacity for regeneration disappears (Jeffery, 2012). Oral siphon regeneration is compromised in the oldest animals collected in the wild or cultured in the laboratory (Jeffery, 2012;.…”