Regeneration of ciliary comb plates in the ctenophore Mnemiopsis leidyi. i. morphology

Abstract

Regeneration of missing body parts in model organisms provides information on the mechanisms underlying the regeneration process. The aim here is to use ctenophores to investigate regeneration of their giant ciliary swimming plates. When part of a row of comb plates on Mnemiopsis is excised, the wound closes and heals, greatly increasing the distance between comb plates near the former cut edges. Video differential interference contrast (DIC) microscopy of the regeneration of new comb plates between widely separated plates shows localized widenings of the interplate ciliated groove (ICG) first, followed by growth of two opposing groups of comb plate cilia on either side. The split parts of a new plate elongate as their bases extend laterally away from the ICG widening and continue ciliogenesis at both ends. The split parts of a new plate grow longer and move closer together into the ICG widening until they merge into a single plate that interrupts the ICG in a normal manner. Video DIC snapshots of dissected gap preparations 1.5-3-day postoperation show that ICG widenings and/or new plates do not all appear at the same time or with uniform spacing within a gap: the lengths and distances between young plates in a gap are quite variable. Video stereo microscopy of intact animals 3-4 days after the operation show that all the new plates that will form in a gap are present, fairly evenly spaced and similar in length, but smaller and closer together than normal. Normal development of comb plates in embryos and growing animals is compared to the pattern of comb plate regeneration in adults. Comb plate regeneration differs in the cydippid Pleurobrachia that lacks ICGs and has a firmer mesoglea than Mnemiopsis. This study provides a morphological foundation for histological, cellular, and molecular analysis of ciliary regeneration in ctenophores.

Evidence for Involvement of Wnt Signalling in Body Polarities, Cell Proliferation, and the Neuro-Sensory System in an Adult Ctenophore

“…A parallel example among bilaterians is the complete loss of Wnt function in setting up the antero-posterior axis in flies, a derived lineage of insects in which early development does not rely anymore on cell-cell communications [2], [13]. On the contrary, regulative processes are prevalent in the adult body of ctenophores, as indicated by their high regenerative capacities [57], and by intense cell turnover taking place continuously in all regions of the body [32], [34]. Positional cues are thus probably required to maintain tissue homeostasis and body shape, as it is the case in adult cnidarians [26].…”

“…The basal cushion represents a particularly promising system to address PCP in ctenophores, because it is a specialised portion of epithelium displaying marked polarity reflected at the level of individual cells as well as of the whole structure, and because its formation can be followed experimentally both under normal conditions (addition of new combs at both extremities of comb rows, [32]) and under regeneration after ablation [57].…”

Regeneration in the absence of a blastema requires cell division but is not tied to wound healing in the ctenophoreMnemiopsis leidyi

“…Comb plate formation did not follow a consistent pattern initially. The correct orientation of comp plates and coordination of their beating was accomplished after a number of comb plates were formed (Figure 2D surface, down), as has been described previously (Tamm, 2012).…”

“…Although the regenerative response has been studied previously in M. leidyi (Coonfield, 1936;Martindale, 1986;Martindale and Henry, 1996;Henry and Martindale, 2000;Tamm, 2012) we first characterized the sequence of morphogenic events during cydippid regeneration to provide a baseline for further experimental investigations. For this, two types of surgeries -covering all the structures of the cydippid's body (apical organ, comb rows, tentacle bulbs and tentacles)were performed (Figure 1).…”

“…It has been known for well over 50 years that ctenophores have the capacity to replace missing body parts (Coonfield, 1936;Martindale, 1986;Martindale and Henry, 1996;Henry and Martindale, 2000;Tamm, 2012) but the cellular and molecular mechanisms underlying this ability are poorly understood. Is cell proliferation required for ctenophore regeneration?…”