Cloning and characterisation of NMDA receptors in the Pacific oyster, Crassostrea gigas (Thunberg, 1793) in relation to metamorphosis and catecholamine synthesis

Vogeler, Susanne; Carboni, Stefano; Li, Xiaoxu; Ireland, J.; Miller-Ezzy, Penny; Joyce, Alyssa

doi:10.1016/j.ydbio.2020.10.008

Cited by 6 publications

(14 citation statements)

References 119 publications

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“…The inducing effect of these NO pathway inhibitors, however, varies between larval cohorts, thus con rming that the internal NO concentration is not the only factor regulating metamorphosis. In addition to batch-related variability, which has also been observed previously for other inducers of Paci c oysters (3,5) and other bivalve species (2), reported differences in effectiveness of the NOS inhibitors might also be caused by the binding speci city of each compound to different NOS isozymes. SMIS is a relatively speci c inhibitor of vertebrate inducible NOS (NOS II), while AGH is an inhibitor of NOS II as well as vertebrate neuronal NOS (NOS I), and 7-NI is advertised to inhibit NOS I, although its binding selectivity has been questioned (54).…”

Section: Discussionsupporting

confidence: 61%

“…The foot glands C together with foot glands D are presumed to be involved in the production and secretion of the adhesive that oysters produce to cement to the surface during settlement (47)(48)(49). CgNOS expression, however, with its speci c localisation near the foot base differs from CgNR1, the gene that expresses NMDA receptor subunit 1 CgNR1 and which is expressed in the nerve network penetrating the whole foot starting from the base of the foot towards the ciliated tip ( Figure 5B & D) (5). Furthermore, CgNOS is not expressed in or near the apical/cerebral ganglia, as it has been shown previously for CgNR1 (5).…”

Section: Localisation No Nos Nmda Receptor and Cgmpmentioning

confidence: 99%

“…CgNOS expression, however, with its speci c localisation near the foot base differs from CgNR1, the gene that expresses NMDA receptor subunit 1 CgNR1 and which is expressed in the nerve network penetrating the whole foot starting from the base of the foot towards the ciliated tip ( Figure 5B & D) (5). Furthermore, CgNOS is not expressed in or near the apical/cerebral ganglia, as it has been shown previously for CgNR1 (5). Instead, CgNOS expression is located in the velum membrane ( Figure 5 E & F), which after unfolding, forms the velum including a cilia band.…”

Section: Localisation No Nos Nmda Receptor and Cgmpmentioning

confidence: 99%

“…Complex neuroendocrine pathways and neurotransmitters have been proposed as regulators for metamorphosis in bivalves (reviewed in (2)), but there are many unknown factors regulating this process. Recently, we provided evidence for a previously unexplored regulatory pathway involved in bivalve metamorphosis involving the transmembrane N-Methyl-D-aspartate (NMDA) receptor (3)(4)(5). As ligand-gated and voltage-dependent ion channels, NMDA receptors are located in synaptic cell membranes and are activated by agonists, predominantly glutamate, co-agonists (e.g.…”

Section: Introductionmentioning

confidence: 99%

“…Cloning and characterisation of NMDA receptors in the Paci c oyster Crassostrea gigas as well as localisation of NMDA receptor subunit 1, CgNR1, in key structures of competent larvae such as the apical sensory organ (ASO), the underlying apical/cerebral ganglia and the nerve network of the foot (5), established the existence of functional NMDA receptors in bivalve nervous systems. Both the ASO and the foot are structures speci c to larval stages, that disappear after metamorphosis, which are assumed to be involved in sensing the environment for settlement cues (7)(8)(9).…”

Section: Introductionmentioning

confidence: 99%

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Bivalves are NO different: nitric oxide as negative regulator of metamorphosis in the Pacific oyster, Crassostrea gigas.

Vogeler

Carboni

et al. 2020

Preprint

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Background: Nitric oxide (NO) is presumed to be a regulator of metamorphosis in many invertebrate species, and although NO pathways have been comparatively well-investigated in gastropods, annelids and crustaceans, there has been very limited research on the effects of NO on metamorphosis in bivalve shellfish.Results: In this paper, we investigate the effects of NO pathway inhibitors and NO donors on metamorphosis induction in larvae of the Pacific oyster, Crassostrea gigas. The nitric oxides synthase (NOS) inhibitors s-methylisothiourea hemisulfate salt (SMIS), aminoguanidine hemisulfate salt (AGH) and 7-nitroindazole (7-NI) induced metamorphosis ranging from 75%, 76% to 83% respectively, and operating in a concentration-dependent manner. Additional induction of up to 54% resulted from exposures to 1H-[1,2,4]Oxadiazole[4,3-a]quinoxalin-1-one (ODQ), an inhibitor of soluble guanylyl cyclase, with which NO interacts to catalyse the synthesis of cyclic guanosine monophosphate (cGMP). Conversely, high concentrations of the NO donor sodium nitroprusside dihydrate in combination with metamorphosis inducers epinephrine, MK-801 or SMIS, significantly decreased metamorphosis, although a potential harmful effect of excessive NO unrelated to metamorphosis pathway cannot be excluded. Expression of CgNOS also decreased in larvae after metamorphosis regardless of the inducers used, but intensified again post-metamorphosis in spat. Fluorescent detection of NO in competent larvae with DAF-FM diacetate and localisation of the oyster nitric oxide synthase CgNOS expression by in-situ hybridisation showed that NO occurs primarily in two key larval structures, the velum and foot. cGMP was also detected in the foot using immunofluorescent assays, and is potentially involved in the foot’s smooth muscle relaxation.Conclusion: Together, these results suggest that the NO pathway acts as negative regulator of metamorphosis in Pacific oyster larvae, and that NO reduction induces metamorphosis by inhibiting swimming or crawling behaviour, in conjunction with a cascade of additional neuroendocrine downstream responses.

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Section: Discussionsupporting

confidence: 61%

Section: Localisation No Nos Nmda Receptor and Cgmpmentioning

confidence: 99%

Section: Localisation No Nos Nmda Receptor and Cgmpmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Bivalves are NO different: nitric oxide as negative regulator of metamorphosis in the Pacific oyster, Crassostrea gigas.

Vogeler

Carboni

et al. 2020

Preprint

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Transcriptional regulation analysis reveals the complexity of metamorphosis in the Pacific oyster (Crassostrea gigas)

Xu,

Deng,

Gavriouchkina

et al. 2023

Mar Life Sci Technol

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A whole nervous system atlas of glutamate receptors reveals distinct receptor roles in sensorimotor circuits

Borba

Kourakis

Miao

et al. 2023

Preprint

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A goal of connectomics is to reveal the links between neural circuits and behavior. Larvae of the primitive chordate Ciona are well-suited to make contributions in this area. The small size of the Ciona larval nervous system (~180 neurons) has facilitated the full characterization of a connectome. In addition, the larvae display a range of behaviors that are readily quantified in both normal and manipulated larvae. Moreover, the small number of neurons allows for a neuron-by-neuron characterization of attributes such as neurotransmitter use. We present here a nervous system-wide atlas of glutamate receptor expression. Included in the atlas are both ionotropic receptors (AMPA, NMDA, and Kainate), and metabotropic receptors. The expression of these receptors is presented in the context of known circuits driving behaviors such as phototaxis, mechanosensation, and looming shadow response. The expression of AMPA and NMDA receptors, in particular, helps to resolve the apparently paradoxical coproduction of GABA and glutamate by some photoreceptors. We find that the targets of these photoreceptors, midbrain relay neurons, primarily express NMDA receptors in the absence of AMPA receptors. This is in agreement with previous results indicating that GABA is the primary neurotransmitter from the photoreceptors evoking a behavioral response (swimming) through a disinhibition mechanism. We hypothesize that NMDA receptors have a modulatory effect in the relay neurons. Other findings reported here are more unexpected. For example, the targets of glutamatergic epidermal sensory neurons (ESNs) do not express any of the ionotropic receptors, yet the ESNs themselves express metabotropic receptors. Thus, we speculate that their production of glutamate may be for communication with neighboring ESNs, rather than to their interneuron targets.

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Cloning and characterisation of NMDA receptors in the Pacific oyster, Crassostrea gigas (Thunberg, 1793) in relation to metamorphosis and catecholamine synthesis

Cited by 6 publications

References 119 publications

Bivalves are NO different: nitric oxide as negative regulator of metamorphosis in the Pacific oyster, Crassostrea gigas.

Bivalves are NO different: nitric oxide as negative regulator of metamorphosis in the Pacific oyster, Crassostrea gigas.

Transcriptional regulation analysis reveals the complexity of metamorphosis in the Pacific oyster (Crassostrea gigas)

A whole nervous system atlas of glutamate receptors reveals distinct receptor roles in sensorimotor circuits

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