Wound healing and arm regeneration in Ophioderma longicaudum and Amphiura filiformis (Ophiuroidea, Echinodermata): comparative morphogenesis and histogenesis

Abstract

All species of the Ophiuroidea have exceptional regenerative capabilities; in particular, they can replace arms lost following traumatic or self-induced amputation. In order to reconstruct this complex phenomenon, we studied arm regeneration in two diVerent ophiuroids, Ophioderma longicaudum (Retzius, 1805) and Amphiura Wliformis O. F. Müller, 1776, which are quite distantly related. These species present contrasting regeneration and diVerentiation rates and diVer in several ecological traits. The aim of this paper is to interpret the primary sequence of morphogenetic and histogenetic events leading to the complete reconstruction of a new arm, comparing the arm regenerative processes of these two ophiuroid species with those described in crinoids. Arm regeneration in ophiuroids is considered an epimorphic process in which new structures develop from a typical blastema formed from an accu-mulation of presumptive undiVerentiated cells. Our results showed that although very diVerent in some respects such as, for instance, the regeneration rate (0.17 mm/week for O. longicaudum and 0.99 mm/week for A. Wliformis), morphogenetic and histogenetic aspects are surprisingly similar in both species. The regenerative process presents similar characteristics and follows a developmental scheme which can be subdivided into four phases: a repair phase, an early regenerative phase, an intermediate regenerative phase and an advanced regenerative phase. In terms of histogenesis, the regenerative events involve the development of new structures from migratory pluripotent cells, which proliferate actively, in addition in both cases there is a signiWcant contribution from dediVerentiated cells, in particular ded-iVerentiating myocytes, although to varying extents. This evidence conWrms the plasticity of the regenerative phenomenon in echinoderms, which can apparently follow diVerent pathways in terms of growth and morphogenesis, but nevertheless involve both epimorphic and morphallactic contributions at the cellular level.

Energy metabolism and regeneration impaired by seawater acidification in the infaunal brittlestar,Amphiura filiformis

“…Based on histological studies, Wood et al (Wood et al, 2008) suggested that unfed A. filiformis increases protein metabolism by the breakdown of muscle tissues to fuel increased energetic demands in response to seawater acidification. It is likely that enhanced catabolism and cell turnover/dedifferentiation of muscle tissues following traumatic amputation in brittlestars and crinoids is related to cell differentiation to produce stem cells to regenerate lost tissues rather that fueling calcification processes (Candia Carnevali and Bonasoro, 2001;Biressi et al, 2010). However, despite increased NH 4 + excretion rates, the present study could not demonstrate any changes in ratios between ADM and DM between pH treatments, which would have indicated an increased utilization of muscle tissue or other amino acid compounds as an energy source.…”

Towards an integrated network of coral immune mechanisms

“…Immune cells with phagocytic potential have been identified across the invertebrates, e.g. within Arthropoda [81] and Echinodermata [89]. During wound repair, after clot formation, specialized immune cells infiltrate the wound site and phagocytose cell debris and foreign organisms [90].…”

“…During wound repair, after clot formation, specialized immune cells infiltrate the wound site and phagocytose cell debris and foreign organisms [90]. Infiltrated cells then proliferate, forming granulation tissue, which consists of multiple cell types, collagen and a basic ECM, and provides a platform for re-epithelialization [81,89]. Although there are differences among species, these cellular phases of wound healing have been documented within numerous invertebrates [81,91].…”

Slow arm regeneration in the Antarctic brittle star Ophiura crassa (Echinodermata, Ophiuroidea)

“…Histological studies have divided arm regeneration in brittle stars into 4 main phases: wound repair with re-epithelialisation; early regeneration with complete healing and cell proliferation at the site of damage; intermediate regeneration resulting in blastema formation; and, finally, advanced regeneration with the development of a miniature arm (Biressi et al 2010). Based on gross morphological observations, it is production of a regenerative bud and arm elongation that constitutes the delayed phase in Ophionotus victoriae (Clark et al 2007).…”

“…Recently, regeneration in the temperate brittle star Ophioderma longicaudum has been described to have an even slower regeneration rate of 0.17 mm wk −1 ; although, it took only 3 wk to initiate regeneration and generate a blastema and measureable regenerative bud (Biressi et al 2010). Here we describe further regeneration studies on another common Antarctic brittle star, Ophiura crassa Mortensen, 1936, to further elucidate regeneration processes in ophiuroids and in particular to understand the effect of temperature.…”