Expression of the neuropeptide SALMFamide-1 during regeneration of the seastar radial nerve cord following arm autotomy

Abstract

Arm loss through a separation at a specialized autotomy plane in echinoderms is inextricably linked to regeneration, but the link between these phenomena is poorly explored. We investigated nervous system regeneration post-autotomy in the asteriid seastar Coscinasterias muricata , focusing on the reorganization of the radial nerve cord (RNC) into the ectoneural neuroepithelium and neuropile, and the hyponeural region, using antibodies to the seastar-specific neuropeptide SALMFamide-1 (S1). Parallel changes in the associated haemal and coelomic vessels were also examined. A new arm bud appeared in 3–5 days with regeneration over three weeks. At the nerve stump and in the RNC immediately behind, the haemal sinus/hyponeural coelomic compartments enlarged into a hypertrophied space filled with migratory cells that appear to be involved in wound healing and regeneration. The haemal and coelomic compartments provided a conduit for these cells to gain rapid access to the regeneration site. An increase in the number of glia-like cells indicates the importance of these cells in regeneration. Proximal to the autotomy plane, the original RNC exhibited Wallerian-type degeneration, as seen in disorganized axons and enlarged S1-positive varicosities. The imperative to regrow lost arms quickly is reflected in the efficiency of regeneration from the autotomy plane facilitated by the rapid appearance of progenitor-like migratory cells. In parallel to its specialization for defensive arm detachment, the autotomy plane appears to be adapted to promote regeneration. This highlights the importance of examining autotomy-induced regeneration in seastars as a model system to study nervous system regeneration in deuterostomes and the mechanisms involved with the massive migration of stem-like cells to facilitate rapid recovery.

The Link between Autotomy and CNS Regeneration: Echinoderms as Non‐Model Species for Regenerative Biology

“…Prominent peptidergic varicosities are present in the axons in the original and regenerating nerve cord (Figure 4F), contrasting with the normal homogeneous appearance of S1‐immunoreactivity in the normal nerve cord (Figure 4A). These varicosities are suggested to be a site of neurochemical release and indicate that the S1 neuropeptide in these structures has an active role in regeneration, potentially acting as a neuromodulatory hormone in control of cell proliferation . Varicosities are also characteristic of regenerating vertebrate neurons …”

“…Autotomy and regeneration in echinoderms present a highly tractable and suitable system to address the long‐standing problem of evolutionary loss of regenerative capacities in mammals. Stellate echinoderms that readily autotomize their arms (e.g., starfish, brittle stars, feather stars) are the best candidates for regeneration research . Autotomy and regeneration are inextricably linked due to the imperative to efficiently regrow lost arms (Figure ).…”

“…F) Although the tissue layers are reorganizing (D), peptidergic immunoreactivity in the axonal layer is highly varicose (arrows, varicosities). (A–C,E,F Reproduced with permission 1. Copyright 2019, The Royal Society).…”

“…The inability of higher vertebrates, particularly mammals, to replace a damaged central nervous system (CNS) contrasts with the amazing regenerative powers of their deuterostome kin, the echinoderms (starfish and allies, Figures 1 and 2). Echinoderms with a propensity to release their arms at a specialized autotomy plane in response to disturbance are particularly proficient at regeneration ( Figure 2). The autotomy plane is morphologically specialized so that the arms are shed with minimum tissue trauma and fluid loss to maintain hemostasis, thereby facilitating rapid initiation of regeneration and return to full functionality .…”

“…D) The brittle star Ophionereis schayeri with two regenerating arms following autotomy near the base (arrows). E,F) C. muricata : A new arm bud is evident where the arm had detached, 21 days after autotomy (Reproduced with permission 1. Copyright 2019, The Royal Society).…”