NADPH-Diaphorase activity changes during gangliogenesis and metamorphosis in the gastropod molluscIlyanassa obsoleta

Lin, Miao-Fang; Leise, Esther M.

doi:10.1002/(sici)1096-9861(19961014)374:2<194::aid-cne3>3.0.co;2-y

Cited by 58 publications

(34 citation statements)

References 60 publications

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“…At this stage, identifiable cells of the cerebral and pedal ganglia were not observed and, therefore, innervation of the foot most likely originates from cells of the apical organ. Similarly, axons were suggested to project from apical cells to the foot in some opisthobranchs (Kempf et al 1991(Kempf et al , 1997Lin and Leise 1996a;Marois and Carew 1997a-c) and the Prosobranchia I. obsoleta (Lin and Leise 1996a, b). Such innervation may control the pedal ciliary band reported to be involved with feeding (D'Asaro 1969) and locomotion (Diefenbach et al 1991).…”

Section: Innervation In the Footmentioning

confidence: 98%

Histochemical localization of FMRFamide, serotonin and catecholamines in embryonic Crepidula fornicata (Gastropoda, Prosobranchia)

Dickinson¹,

Nason

Croll³

1999

Zoomorphology

132

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Recent reports indicate that neuronal elements develop in early larval stages of some Gastropoda from the Pulmonata and Opisthobranchia prior to the appearance of any ganglia of the future adult central nervous system (CNS). The present study describes similar early neuronal elements in Crepidula fornicata. A posterior FMRFamide-like immunoreactive (LIR) cell with anteriorly projected fibers was observed in the trochophore stage. Additional FMRFamide-LIR and serotonin-LIR cells and fibers were found in the apical organ in the trochophore and early veliger stages. FMRFamide-LIR and serotonin-LIR projections to the velum and foot were also detected at this time. As the veliger developed, peripheral FMRFamide-LIR and later catecholaminergic cells were located in the foot region. Also during this stage, catecholaminergic cells and processes were observed near the mouth. In addition, this study tentatively identified the first serotonin-and FMRFamide-LIR cells and fibers within the developing ganglia of the adult CNS, which appeared in close proximity to the earlier developing elements. These observations are consistent with the hypothesis that, in addition to its presumed role in the control of larval behaviors, the larval nervous system guides the development of the adult CNS. Larvae from the class Bivalvia and other invertebrate phyla also have neuronal elements marked by the presence of FMRFamide, serotonin, and catecholamines, and, therefore, this study may provide additional insights into phylogenetic relationships of the Gastropoda with other representatives of the Mollusca and different invertebrate phyla.& b d y :

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Section: Innervation In the Footmentioning

confidence: 98%

Histochemical localization of FMRFamide, serotonin and catecholamines in embryonic Crepidula fornicata (Gastropoda, Prosobranchia)

Dickinson¹,

Nason

Croll³

1999

Zoomorphology

132

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“…We stained no epithelial neurons, but discovered NADPHd activity in all ganglionic neuropils. Staining intensity increased throughout larval development, with the neuropil of the AG displaying the strongest NADPHd activity in competent larvae [28]. Once metamorphosis was initiated, staining intensity dropped dramatically [28].…”

Section: Nitric Oxide Inhibition Of Metamorphosismentioning

confidence: 99%

“…Staining intensity increased throughout larval development, with the neuropil of the AG displaying the strongest NADPHd activity in competent larvae [28]. Once metamorphosis was initiated, staining intensity dropped dramatically [28]. With immunocytochemical methods that incorporated the use of mammalian anti-neuronal NOS antibodies, we determined that the majority of neurons in the AG of competent larvae displayed NOS-like immunoreactivity (NOS-IR) [42].…”

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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“…Although the localization of putative NOS-containing cells has been adequately demonstrated by NADPH-d histochemistry (Elofsson et al 1993;Martinez 1995;Moroz et al 1996) and biochemical assays (Elphick et al 1993) in the adult central nervous system (CNS) of various invertebrates, little information is available regarding the distribution of NOS during embryogenesis (Lin and Leise 1996;Truman et al 1996). Therefore, our aim has been to follow the ontogenetic distribution of NOS in the pond snail Lymnaea stagnalis, with special reference to the nervous system.…”

Section: Introductionmentioning

confidence: 99%

NADPH-diaphorase activity in the nervous system of the embryonic and juvenile pond snail, Lymnaea stagnalis

Serfözö

Elekes²,

Varga

1998

Cell and Tissue Research

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Nicotinamide-adenine-dinucleotide-phosphate-diaphorase (NADPH-d) histochemistry has been applied in the present study to determine the distribution of putative nitric oxide (nitric oxide synthase)-producing cells during embryonic and early postembryonic development in the pond snail, Lymnaea stagnalis L., with special reference to the nervous system. The first NADPH-d-positive structures appear as early as 18% of development (E18, trochophore stage) and correspond to the pair of protonephridia. These structures later show disintegration, although after metamorphosis (E26=75%) staining of their individually spreading cells can be observed until hatching. Peripheral sensory neurons in the foot, mantle edge and lips, and their afferents projecting to the central nervous system reveal NADPH-d activity in the postmetamorphosis period (E25-E27=E60%-E80%) of embryogenesis. After hatching (P1-P3), a number of stained sensory cells appear in the pharynx and esophagus. Some NADPH-d positive neuronal perikarya occur in the pedal and pleural ganglia, and a few weakly stained cells in the cerebral and buccal ganglia of juvenile snails. At the same time, a continuous bundle of reactive fibers is formed in the neuropil both through and through around the circumesophageal ganglion ring. The localization of NADPH-d activity in the developing nervous system of Lymnaea suggests that nitric oxide participates mainly in sensory processes. However, its role in specific intraganglionic integrative events cannot be excluded following embryonic metamorphosis.

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NADPH-Diaphorase activity changes during gangliogenesis and metamorphosis in the gastropod molluscIlyanassa obsoleta

Cited by 58 publications

References 60 publications

Histochemical localization of FMRFamide, serotonin and catecholamines in embryonic Crepidula fornicata (Gastropoda, Prosobranchia)

Histochemical localization of FMRFamide, serotonin and catecholamines in embryonic Crepidula fornicata (Gastropoda, Prosobranchia)

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

NADPH-diaphorase activity in the nervous system of the embryonic and juvenile pond snail, Lymnaea stagnalis

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