Cloning and characterization of an ionotropic glutamate receptor subunit expressed in the squid nervous system

Battaglia, Anna; Nardi, G.; Steinhardt, Alicia; Novakovic, Ana; Gentile, S.; Idelson, Paola Iaccarino; Gilly, William F.; Santis, A. De

doi:10.1046/j.1460-9568.2003.02680.x

Cited by 13 publications

(15 citation statements)

References 56 publications

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“…Complementary results have been obtained by Battaglia et al [5] on the squid Loligo. Having cloned a glutamate receptor subunit, SqGluR (see above) they also showed by in situ hybridisation that SqGluR mRNA occurs in the secondorder "giant" visual cells in the inner and outer granular layers, and in what appears to be the subvertical lobe.…”

Section: The Brainsupporting

confidence: 85%

“…Recently Battaglia et al [5] cloned a putative glutamate receptor subunit, SqGluR, from the stellate ganglion of the squid Loligo opalescens. They showed that its primary structure was homologous to mammalian AMPA-subunits GluR1-GluR4 (44-46% amino-acid identity) and also that intracellular injection of the C-terminal 15-amino-acid peptide of SqGluR into the post-synaptic region of the third-order fibre inhibited synaptic transmission at the giant synapse (Fig.…”

Section: The Squid Giant Synapsementioning

confidence: 99%

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L-Glutamate and its Ionotropic Receptors in the Nervous System of Cephalopods

Cosmo

Cristo²,

Messenger³

2006

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Abstract:In several species of cephalopod molluscs there is good evidence for the presence of L-glutamate in the central and peripheral nervous system and evidence for both classes of ionotropic receptor, AMPA/kainate and NMDA.The best evidence for glutamate being a transmitter in cephalopods comes from pharmacological, immunohistochemical and molecular investigations on the giant fibre system in the squid stellate ganglion. These studies confirm there are AMPA/kainate-like receptors on the third-order giant axon. In the (glial) Schwann cells associated with the giant axons both classes of glutamate receptor occur.Glutamate is an excitatory transmitter in the chromatophores and in certain somatic muscles and its action is mediated primarily via AMPA/kainate-like receptors, but at some chromatophores there are NMDA-like receptors.In the statocysts the afferent crista fibres are also glutamatergic, acting at non-NMDA receptors.In the brain (of Sepia) a neuronal NOS is activated by glutamate with subsequent production of nitric oxide and elevation of cGMP levels. This signal transduction pathway is blocked by D-AP-5, a specific antagonist of the NMDA receptor.Recently immunohistochemical analysis has demonstrated (in Sepia and Octopus) the presence of NMDAR2A /B -like receptors in motor centres, in the visual and olfactory systems and in the learning system. Physiological experiments have shown that glutamatergic transmission is involved in long term potentation (LTP) in the vertical lobe of Octopus, a brain area involved in learning. This effect seems to be mediated by non-NMDA receptors. Finally in the CNS of Sepia NMDA-mediated nitration of tyrosine residues of cytoskeletal protein such as -tubulin, has been demonstrated.

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Section: The Brainsupporting

confidence: 85%

Section: The Squid Giant Synapsementioning

confidence: 99%

L-Glutamate and its Ionotropic Receptors in the Nervous System of Cephalopods

Cosmo

Cristo²,

Messenger³

2006

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“…The potentiation of glutamate currents by CTZ suggests that SqGluR, with a 44%-46% amino acid identity to the mammalian AMPA-subunits GluR1-GluR4, is the subunit making up the native glutamate receptors (Battaglia et al, 2003).…”

Section: Discussionmentioning

confidence: 99%

“…Evidence indicates that glutamate is an excitatory neurotransmitter (Miledi, 1967;DeSantis et al, 1978;Eusebi et al, 1985;Corrie et al, 1993) that activates alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)-type receptors in postsynaptic terminals of the squid synapses (Messenger, 1996;Di Cosmo et al, 2006). The cloning of the glutamate receptor subunit SqGluR from the stellate ganglion of Loligo opalescens provides further support for the excitatory role of glutamate in squid (Battaglia et al, 2003). Conversely, the inhibitory neurotransmission in squid and other cephalopods is largely unexplored.…”

Section: Introductionmentioning

confidence: 99%

Microtransplantation of Cellular Membranes From Squid Stellate Ganglion Reveals Ionotropic GABA Receptors

Conti

Limón

Palma

et al. 2013

The Biological Bulletin

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Abstract. The squid has been the most studied cephalopod, and it has served as a very useful model for investigating the events associated with nerve impulse generation and synaptic transmission. While the physiology of squid giant axons has been extensively studied, very little is known about the distribution and function of the neurotransmitters and receptors that mediate inhibitory transmission at the synapses. In this study we investigated whether ␥-aminobutyric acid (GABA) activates neurotransmitter receptors in stellate ganglia membranes. To overcome the low abundance of GABA-like mRNAs in invertebrates and the low expression of GABA in cephalopods, we used a two-electrode voltage clamp technique to determine if Xenopus laevis oocytes injected with cell membranes from squid stellate ganglia responded to GABA. Using this method, membrane patches containing proteins and ion channels from the squid's stellate ganglion were incorporated into the surface of oocytes. We demonstrated that GABA activates membrane receptors in cellular membranes isolated from squid stellate ganglia. Using the same approach, we were able to record native glutamate-evoked currents. The squid's GABA receptors showed an EC 50 of 98 mol l -1 to GABA and were inhibited by zinc (IC 50 ϭ 356 mol l -1 ). Interestingly, GABA receptors from the squid were only partially blocked by bicuculline. These results indicate that the microtransplantation of native cell membranes is useful to identify and characterize scarce membrane proteins. Moreover, our data also support the role of GABA as an ionotropic neurotransmitter in cephalopods, acting through chloride-permeable membrane receptors.

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“…For example, 2-amino-5-phosphonovalerate (APV) was not a blocker of Lymnaea's NMDA receptors, and NMDA-induced currents were not affected by Mg 2ϩ . Finally, although other types of ionotropic glutamate receptors were cloned from selected gastropods and cephalopods (Hutton et al, 1991;Yung et al, 2002;Battaglia et al, 2003), genes for NMDA receptors have not been identified in any molluscan species.…”

Section: Introductionmentioning

confidence: 99%

Molecular Characterization of NMDA-Like Receptors inAplysiaandLymnaea:Relevance to Memory Mechanisms

Kohn

Bobkova

et al. 2006

The Biological Bulletin

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Abstract. The N-methyl-D-aspartate (NMDA) receptor belongs to the group of ionotropic glutamate receptors and has been implicated in synaptic plasticity, memory acquisition, and learning in both vertebrates and invertebrates, including molluscs. However, the molecular identity of NMDA-type receptors in molluscs remains unknown. Here, we cloned two NMDA-type receptors from the sea slug Aplysia californica, AcNR1-1 and AcNR1-2, as well as their homologs from the freshwater pulmonate snail Lymnaea stagnalis, LsNR1-1 and LsNR1-2. The cloned receptors contain a signal peptide, two extracellular segments with predicted binding sites for glycine and glutamate, three recognized transmembrane regions, and a fourth hydrophobic domain that makes a hairpin turn to form a pore-like structure. Phylogenetic analysis suggests that both the AcNR1s and LsNR1s belong to the NR1 subgroup of ionotrophic glutamate receptors. Our in situ hybridization data indicate highly abundant, but predominantly neuron-specific expression of molluscan NR1-type receptors in all central ganglia, including identified motor neurons in the buccal and abdominal ganglia as well as groups of mechanosensory cells. AcNR1 transcripts were detected extrasynaptically in the neurites of metacerebral cells of Aplysia. The widespread distribution of AcNR1 and LsNR1 transcripts also implies diverse functions, including their involvement in the organization of feeding, locomotory, and defensive behaviors.

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Cloning and characterization of an ionotropic glutamate receptor subunit expressed in the squid nervous system

Cited by 13 publications

References 56 publications

L-Glutamate and its Ionotropic Receptors in the Nervous System of Cephalopods

L-Glutamate and its Ionotropic Receptors in the Nervous System of Cephalopods

Microtransplantation of Cellular Membranes From Squid Stellate Ganglion Reveals Ionotropic GABA Receptors

Molecular Characterization of NMDA-Like Receptors inAplysiaandLymnaea:Relevance to Memory Mechanisms

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