Programmed Cell Death in the Apical Ganglion During Larval Metamorphosis of the Marine Mollusc<i>Ilyanassa obsoleta</i>

Gifondorwa, David J.; Leise, Esther M.

doi:10.2307/4134600

Cited by 59 publications

(72 citation statements)

References 95 publications

(120 reference statements)

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“…To first confirm that the AG is indeed lost by a form of PCD, we examined it within 24 hours of metamorphic initiation. Induction by either 5HT or 7-NI yielded signs of cellular degeneration, condensation and loss of nuclei, and evidence of phagocytic activity in histological sections [16]. In the early stages of PCD, endonucleases cleave nuclear DNA into fragments that are multiples of 180-200 base pairs in length [40].…”

Section: Nitric Oxide Inhibition Of Metamorphosismentioning

confidence: 99%

Induction of Metamorphosis in the Marine GastropodIlyanassa obsoleta: 5HT, NO and Programmed Cell Death

Leise

Kempf

Durham

et al. 2004

Acta Biologica Hungarica

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Abstract:The central nervous system (CNS) of a metamorphically competent larva of the caenogastropod Ilyanassa obsoleta contains a medial, unpaired apical ganglion (AG) of approximately 25 neurons that lies above the commissure connecting the paired cerebral ganglia. The AG, also known as the cephalic or apical sensory organ (ASO), contains numerous sensory neurons and innervates the ciliated velar lobes, the larval swimming and feeding structures. Before metamorphosis, the AG contains 5 serotonergic neurons and exogenous serotonin can induce metamorphosis in competent larvae. The AG appears to be a purely larval structure as it disappears within 3 days of metamorphic induction. In competent larvae, most neurons of the AG display nitric oxide synthase (NOS)-like immunoreactivity and inhibition of NOS activity can induce larval metamorphose. Because nitric oxide (NO) can prevent cells from undergoing apoptosis, a form of programmed cell death (PCD), we hypothesize that inhibition of NOS activity triggers the loss of the AG at the beginning of the metamorphic process. Within 24 hours of metamorphic induction, cellular changes that are typical of the early stages of PCD are visible in histological sections and results of a terminal deoxynucleotidyl transferase dUTP nick end labeling (TUNEL) assay in metamorphosing larvae show AG nuclei containing fragmented DNA, supporting our hypothesis. Keywords: Apoptosis -caenogastropod -mollusc -nitric oxide -serotonin Article: INTRODUCTION Larval Ilyanassa obsoleta, like most marine molluscs, undergo a series of physiological and anatomical transformations at metamorphosis which allow them to begin their juvenile life history phase. The most obvious external change is the loss of the ciliated larval feeding organ or velum [39], which, in the laboratory, occurs with a delay of some 12-36 hours after exposure to an inducing substance. In addition to loss of the velum, within 48 hours of metamorphic induction, internal transformations include rearrangements within the digestive tract and nervous system [13,14,27]. However, until recently, few changes in larval physiology or morphology during the 12-36 hour delay period in I. obsoleta had been described. In this species, by about 83% of larval development [27,42], the CNS contains rudiments of all of the adult ganglia along with a medial, unpaired apical ganglion (AG). Typically, the larval AG innervates the muscular and ciliary components of the velar lobes [20, 29-31, 34, 35]. The AG is an outgrowth of the trochophore apical tuft and has long been postulated to have a sensory function [6,34,35,38]. Recent experiments on a nudibranch provide evidence that the AG can detect a metamorphic cue [17], but a review of literature about molluscan AGs suggests that they are sensorimotor, coordinating the functions of the velar lobes [34,35] and sensing inductive and other stimuli [34]. Currently, the AG appears to be the only part of the larval CNS that is lost at metamorphosis. Some evidence from I. obsoleta and other species suggests t...

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Section: Nitric Oxide Inhibition Of Metamorphosismentioning

confidence: 99%

Induction of Metamorphosis in the Marine GastropodIlyanassa obsoleta: 5HT, NO and Programmed Cell Death

Leise

Kempf

Durham

et al. 2004

Acta Biologica Hungarica

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“…The organ degenerates before or at the time of settling (Dickinson and Croll, 2003), and the cells may undergo apoptosis (Gifondorwa and Leise, 2006). In the gastropod Crepidula, the four apical cells degenerate at an early developmental stage, long before the larva hatches from the egg mass (Conklin, 1897).…”

Section: Protostomiamentioning

confidence: 99%

Larval nervous systems: true larval and precocious adult

Nielsen

2015

Journal of Experimental Biology

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The apical organ of ciliated larvae of cnidarians and bilaterians is a true larval organ that disappears before or at metamorphosis. It appears to be sensory, probably involved in metamorphosis, but knowledge is scant. The ciliated protostome larvae show ganglia/nerve cords that are retained as the adult central nervous system (CNS). Two structures can be recognized, viz. a pair of cerebral ganglia, which form the major part of the adult brain, and a blastoporal (circumblastoporal) nerve cord, which becomes differentiated into a perioral loop, paired or secondarily fused ventral nerve cords and a small perianal loop. The anterior loop becomes part of the brain. This has been well documented through cell-lineage studies in a number of spiralians, and homologies with similar structures in the ecdysozoans are strongly indicated. The deuterostomes are generally difficult to interpret, and the nervous systems of echinoderms and enteropneusts appear completely enigmatic. The ontogeny of the chordate CNS can perhaps be interpreted as a variation of the ontogeny of the blastoporal nerve cord of the protostomes, and this is strongly supported by patterns of gene expression. The presence of 'deuterostomian' blastopore fates both in an annelid and in a mollusk, which are both placed in families with the 'normal' spiralian gastrulation type, and in the chaetognaths demonstrates that the chordate type of gastrulation could easily have evolved from the spiralian type. This indicates that the latest common ancestor of the deuterostomes was very similar to the latest common pelago-benthic ancestor of the protostomes as described by the trochaea theory, and that the neural tube of the chordates is morphologically ventral. KEY WORDS: Deuterostomy, Metamorphosis, Nervous systems, Dorsal-ventral orientation IntroductionStudies on ontogeny are very important for our understanding of nervous system evolution and diversification, and new methods have made important contributions to knowledge of the structure and development of larval nervous systems and their relationships to adult nervous systems.The nervous system has for a long time been considered one of the most conservative animal organ systems and has therefore been given high importance in studies of animal evolution. More than a century ago, Hatschek (Hatschek, 1888) introduced the names Zygoneura (now Protostomia), Ambulacraria and Chordonia (now Chordata) for three major groups of the Bilateria, based on the structure and position of the central nervous system (CNS). The Zygoneura were characterized by a paired longitudinal ventral nerve cord [a cluster of nervous cells including their cell bodies, as opposed to a nerve, which is a bundle of axons (Richter et al., 2010); the ventral nerve cord may REVIEWThe Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark.*Author for correspondence (cnielsen@snm.ku.dk) be specialized into rows of ganglia connected by connectives] and the Chordonia by an unpaired dorsal n...

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“…Averages ranged from 540 to 657 μm. Bath experiments have also been described previously (Couper and Leise, 1996;Froggett and Leise, 1999;Gifondorwa and Leise, 2006). Briefly, competent larvae were tested in untreated 24-well Falcon® tissue culture plates at 10 larvae in 2 ml of experimental solution per well, at ambient light and temperature (~22°C).…”

Section: Methodsmentioning

confidence: 99%

“…And, although the response to 5-HT is high, it may be artificially elevated by the high levels of spontaneous metamorphosis observed in FIO. We speculate that late in the competence period, larvae may lose responsiveness because of degeneration of sensory neurons (Gifondorwa and Leise, 2006) or the lack of particular functional receptor molecules, but that they retain an ability to undergo a complete metamorphosis.…”

Section: Potential Inhibition Of Spontaneous Metamorphosismentioning

confidence: 99%

“…When larval metamorphosis is initiated by the reception of an appropriate pharmacological stimulus in the laboratory, the ensuing morphological and physiological transformations include a decrease in the expression of the gene coding for nitric oxide synthase, the enzyme that produces NO (Froggett and Leise, 1999;Leise et al, 2001Leise et al, , 2004Gifondorwa and Leise, 2006;Hens et al, 2006). Leise and colleagues also confirmed Levantine and Bonar's (1986) discovery that the classical neurotransmitter serotonin (5-HT) can induce metamorphosis in competent larvae, and they provided pharmacological data supporting the idea that exogenously applied 5-HT mimics the action of serotonergic neurons in the larval nervous system (Couper and Leise, 1996;Leise et al, 2001Leise et al, , 2004.…”

Section: Introductionmentioning

confidence: 99%

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Diatom cultures exhibit differential effects on larval metamorphosis in the marine gastropod Ilyanassa obsoleta (Say)

Leise

Froggett

Nearhoof

et al. 2009

Journal of Experimental Marine Biology and Ecology

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Abstract:Adult Ilyanassa obsoleta recruit from the plankton to surface sediments of intertidal mudflats along the U.S. East Coast as a result of metamorphic induction of planktonic larvae by environmental cues. A previous researcher discovered that seawater extracts of mud from juvenile habitats could induce metamorphosis and provided evidence that the inductive agent was of biological origin. Because juvenile I. obsoleta are herbivorous and grow when fed diets of benthic diatoms, we hypothesized that benthic diatoms or their associated microflora might be responsible for producing a metamorphic stimulus. We tested extracts of a culture of mixed diatoms and extracts of cultures of 6 diatom species isolated from mudflat sediments along the coast of North Carolina in which sexually mature and immature adult (juvenile) I. obsoleta commonly co-occur. We also tested extracts of one diatom culture isolated at the Friday Harbor Laboratories (Friday Harbor, WA). We found differential effects among the diatom species tested. One centric diatom, Coscino-discus sp., induced metamorphosis at levels close to those triggered by a known neuroactive compound, serotonin. Several species of benthic diatoms displayed neutral effects, showing little or no inductive capability. In one experiment, an unidentified pennate diatom species appeared to inhibit spontaneous metamorphosis that occurred in some competent larvae. We hypothesize that Coscinodiscus sp. or its associated microflora, is part of a suite of benthic species that is either indicative of a favorable juvenile environment or is itself part of the postmetamorphic diet. Our results also indicate that larval Ilyanassa demonstrated positive, neutral, and perhaps even negative responses to potential metamorphic cues.

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Programmed Cell Death in the Apical Ganglion During Larval Metamorphosis of the Marine MolluscIlyanassa obsoleta

Cited by 59 publications

References 95 publications

Induction of Metamorphosis in the Marine GastropodIlyanassa obsoleta: 5HT, NO and Programmed Cell Death

Induction of Metamorphosis in the Marine GastropodIlyanassa obsoleta: 5HT, NO and Programmed Cell Death

Larval nervous systems: true larval and precocious adult

Diatom cultures exhibit differential effects on larval metamorphosis in the marine gastropod Ilyanassa obsoleta (Say)

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