Characterization of the two distinct subtypes of metabotropic glutamate receptors from honeybee, Apis mellifera

Funada, Masahiro; Yasuo, Shinobu; Yoshimura, Takashi; Ebihara, Shizufumi; Sasagawa, Hiromi; Kitagawa, Yasuo; Kadowaki, Tatsuhiko

doi:10.1016/j.neulet.2004.02.004

Cited by 26 publications

(20 citation statements)

References 21 publications

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“…Although other possibilities remain, this difference regarding STM could be explained by the contribution of distinct brain areas, because the manipulated NMDAR is weakly expressed throughout the brain with higher expression levels in cell bodies surrounding the calyces of the MBs. The discrepancy between the localization of the Drosophila NMDAR (around the calyces) and the effect obtained using uncaging of glutamate in the honeybee mushroom bodies suggest that other glutamate receptors re-ported to be expressed in the insect mushroom bodies (Volkner et al, 2000;Funada et al, 2004) may also participate in the glutamate function in memory formation in honeybees.…”

Section: Discussionmentioning

confidence: 93%

“…Glutamate-like immunoreactivity (Bicker et al, 1988;Schür-mann et al, 2000;Sinakevitch et al, 2001) and glutamateinduced ion currents (Cayre et al, 1999) were described in insect CNS neurons. Moreover, molecular studies identified the expression of glutamate transporters and glutamate receptors homologous to mammalian ones (Ultsch et al, 1993;Parmentier et al, 1996;Seal et al, 1998;Kucharski et al, 2000;Volkner et al, 2000;Funada et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

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Focal and Temporal Release of Glutamate in the Mushroom Bodies Improves Olfactory Memory inApis mellifera

Locatelli

Bundrock²,

Müller³

2005

J. Neurosci.

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In contrast to vertebrates, the role of the neurotransmitter glutamate in learning and memory in insects has hardly been investigated. The reason is that a pharmacological characterization of insect glutamate receptors is still missing; furthermore, it is difficult to locally restrict pharmacological interventions. In this study, we overcome these problems by using locally and temporally defined photo-uncaging of glutamate to study its role in olfactory learning and memory formation in the honeybee, Apis mellifera. Uncaging glutamate in the mushroom bodies immediately after a weak training protocol induced a higher memory rate 2 d after training, mimicking the effect of a strong training protocol. Glutamate release before training does not facilitate memory formation, suggesting that glutamate mediates processes triggered by training and required for memory formation. Uncaging glutamate in the antennal lobes shows no effect on memory formation. These results provide the first direct evidence for a temporally and locally restricted function of glutamate in memory formation in honeybees and insects.

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Section: Discussionmentioning

confidence: 93%

Section: Introductionmentioning

confidence: 99%

Focal and Temporal Release of Glutamate in the Mushroom Bodies Improves Olfactory Memory inApis mellifera

Locatelli

Bundrock²,

Müller³

2005

J. Neurosci.

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“…These are in the downgrowth lamina of the developing cockroach mushroom bodies (Sinakevitch et al, 2001, Brown and, in the core neuropil of the alpha and beta lobe of Drosophila melanogaster , and in basal ring neuropil of honey bees (Strausfeld et al, unpublished observations;Farris et al, 2004). Local release of glutamate in the honey bee mushroom body has been demonstrated to improve odor learning (Locatelli et al, 2005) and several different types of putative glutamate-receptors have been proposed to be present in the insect central nervous system (Funada et al, 2004;Xia et al, 2005;Völkner et al, 2000).…”

Section: Introductionmentioning

confidence: 99%

Global and local modulatory supply to the mushroom bodies of the moth Spodoptera littoralis

Sinakevitch¹,

Sjöholm

Hansson

et al. 2008

Arthropod Structure & Development

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The moth Spodoptera littoralis, is a major pest of agriculture whose olfactory system is tuned to odorants emitted by host plants and conspecifics. As in other insects, the paired mushroom bodies are thought to play pivotal roles in behaviors that are elicited by contextual and multisensory signals, amongst which those of specific odors dominate. Compared with species that have elaborate behavioral repertoires, such as the honey bee Apis mellifera or the cockroach Periplaneta americana, the mushroom bodies of S. littoralis were originally viewed as having a simple cellular organization. This has been since challenged by observations of putative transmitters and neuromodulators. As revealed by immunocytology, the spodopteran mushroom bodies like those of other taxa, are subdivided longitudinally into discrete neuropil domains. Such divisions are further supported by the present study, which also demonstrates discrete affinities to different mushroom body neuropils by antibodies raised against two putative transmitters, glutamate and γ-aminobutyric acid, and against three putative neuromodulatory substances: serotonin, A-type allatostatin, and tachykinin-related peptides. The results suggest that in addition to longitudinal divisions of the lobes, circuits in the calyces and lobes are likely to be independently modulated.

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“…In situ hybridization of honeybee (foragers) brain sections with digoxigenin-labeled riboprobes was carried out as described in Funada et al (2004). For the preparation of riboprobes, the partial honeybee Mahya cDNA (57-3580) with T7 and SP6 promoters was first PCR amplified, and then the sense and antisense riboprobes were made with either T7 or SP6 RNA polymerase and rNTPs containing digoxigenin-UTP.…”

Section: Methodsmentioning

confidence: 99%

Conservation of novel Mahya genes shows the existence of neural functions common between Hymenoptera and Deuterostome

et al. 2005

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Honeybees have been shown to exhibit cognitive performances that were thought to be specific to some vertebrates. However, the molecular and cellular mechanisms of such cognitive abilities of the bees have not been understood. We have identified a novel gene, Mahya, expressed in the brain of the honeybee, Apis mellifera, and other Hymenoptera. Mahya orthologues are present in Deuterostomes but are absent or highly diverged in nematodes and, intriguingly, in two dipteran insects (fruit fly and mosquito) and Lepidoptera (silk moth). Mahya genes encode novel secretory proteins with a follistatin-like domain (Kazal-type serine/threonine protease inhibitor domain and EF-hand calcium-binding domain), two immunoglobulin domains, and a C-terminal novel domain. Honeybee Mahya is expressed in the mushroom bodies and antennal lobes of the brain. Zebra fish Mahya orthologues are expressed in the olfactory bulb, telencephalon, habenula, optic tectum, and cerebellum of the brain. Mouse Mahya orthologues are expressed in the olfactory bulb, hippocampus, and cerebellum of the brain. These results suggest that Mahya may be involved in learning and memory and in processing of sensory information in Hymenoptera and vertebrates. Furthermore, the limited existence of Mahya in the genomes of Hymenoptera and Deuterostomes supports the hypothesis that the genes typically represented by Mahya were lost or highly diverged during the evolution of the central nervous system of specific Bilaterian branches under the specific selection and subsequent adaptation associated with different ecologies and life histories.

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Characterization of the two distinct subtypes of metabotropic glutamate receptors from honeybee, Apis mellifera

Cited by 26 publications

References 21 publications

Focal and Temporal Release of Glutamate in the Mushroom Bodies Improves Olfactory Memory inApis mellifera

Focal and Temporal Release of Glutamate in the Mushroom Bodies Improves Olfactory Memory inApis mellifera

Global and local modulatory supply to the mushroom bodies of the moth Spodoptera littoralis

Conservation of novel Mahya genes shows the existence of neural functions common between Hymenoptera and Deuterostome

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