Development‐dependent and ‐independent ubiquitin expression in divisions of the cockroach mushroom body

Brown, Sheena; Strausfeld, Nicholas J.

doi:10.1002/cne.20943

Cited by 7 publications

(9 citation statements)

References 75 publications

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“…Disappearance of this signal could result from the release or intracellular metabolism of this amino acid. Similarly, it was observed in cockroach MBs that newborn KCs loose Glu immunoreactivity when they become mature and establish contacts with extrinsic neurons [77,81]. Here we also present the first evidence that Glu transiently accumulates at a high level in developing newborn KCs of Drosophila in late larva and during pupal stages.…”

Section: Discussionsupporting

confidence: 83%

Dynamics of glutamatergic signaling in the mushroom body of young adult Drosophila

et al. 2010

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BackgroundThe mushroom bodies (MBs) are paired brain centers located in the insect protocerebrum involved in olfactory learning and memory and other associative functions. Processes from the Kenyon cells (KCs), their intrinsic neurons, form the bulk of the MB's calyx, pedunculus and lobes. In young adult Drosophila, the last-born KCs extend their processes in the α/β lobes as a thin core (α/β cores) that is embedded in the surrounding matrix of other mature KC processes. A high level of L-glutamate (Glu) immunoreactivity is present in the α/β cores (α/βc) of recently eclosed adult flies. In a Drosophila model of fragile X syndrome, the main cause of inherited mental retardation, treatment with metabotropic Glu receptor (mGluR) antagonists can rescue memory deficits and MB structural defects.ResultsTo address the role of Glu signaling in the development and maturation of the MB, we have compared the time course of Glu immunoreactivity with the expression of various glutamatergic markers at various times, that is, 1 hour, 1 day and 10 days after adult eclosion. We observed that last-born α/βc KCs in young adult as well as developing KCs in late larva and at various pupal stages transiently express high level of Glu immunoreactivity in Drosophila. One day after eclosion, the Glu level was already markedly reduced in the α/βc neurons. Glial cell processes expressing glutamine synthetase and the Glu transporter dEAAT1 were found to surround the Glu-expressing KCs in very young adults, subsequently enwrapping the α/β lobes to become distributed equally over the entire MB neuropil. The vesicular Glu transporter DVGluT was detected by immunostaining in processes that project within the MB lobes and pedunculus, but this transporter is apparently never expressed by the KCs themselves. The NMDA receptor subunit dNR1 is widely expressed in the MB neuropil just after eclosion, but was not detected in the α/βc neurons. In contrast, we provide evidence that DmGluRA, the only Drosophila mGluR, is specifically expressed in Glu-accumulating cells of the MB α/βc immediately and for a short time after eclosion.ConclusionsThe distribution and dynamics of glutamatergic markers indicate that newborn KCs transiently accumulate Glu at a high level in late pupal and young eclosed Drosophila, and may locally release this amino acid by a mechanism that would not involve DVGluT. At this stage, Glu can bind to intrinsic mGluRs abundant in the α/βc KCs, and to NMDA receptors in the rest of the MB neuropil, before being captured and metabolized in surrounding glial cells. This suggests that Glu acts as an autocrine or paracrine agent that contributes to the structural and functional maturation of the MB during the first hours of Drosophila adult life.

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Section: Discussionsupporting

confidence: 83%

Dynamics of glutamatergic signaling in the mushroom body of young adult Drosophila

et al. 2010

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“…Enhanced cytoplasmic electron density either is found in sprouting neural and glial cells (this study; Salecker and Boeckh, 1995) or represents decaying degenerating material in these cell types (Schü rmann, 1987;Watts et al, 2003Watts et al, , 2004Brown and Strausfeld, 2006). The glial system has been demonstrated to be crucially involved in growth processes sorting the neuropil into subdivisions and to serve for intimate contact with nerve cells (Tolbert and Oland, 1990;Rössler et al, 1999;Tucker et al, 2004).…”

Section: Ultrastructural Characters Of Developing Kenyon Cellsmentioning

confidence: 89%

Sprouting interneurons in mushroom bodies of adult cricket brains

Mashaly¹,

Winkler²,

Frambach³

et al. 2008

J of Comparative Neurology

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In crickets, neurogenesis persists throughout adulthood for certain local brain interneurons, the Kenyon cells in the mushroom bodies, which represent a prominent compartment for sensory integration, learning, and memory. Several classes of these neurons originate from a perikaryal layer, which includes a cluster of neuroblasts, surrounded by somata that provide the mushroom body's columnar neuropil. We describe the form, distribution, and cytology of Kenyon cell groups in the process of generation and growth in comparison to developed parts of the mushroom bodies in adult crickets of the species Gryllus bimaculatus. A subset of growing Kenyon cells with sprouting processes has been distinguished from adjacent Kenyon cells by its prominent f-actin labelling. Growth cone-like elements are detected in the perikaryal layer and in their associated sprouting fiber bundles. Sprouting fibers distant from the perikarya contain ribosomes and rough endoplasmic reticulum not found in the dendritic processes of the calyx. A core of sprouting Kenyon cell processes is devoid of synapses and is not invaded by extrinsic neuronal elements. Measurements of fiber cross-sections and counts of synapses and organelles suggest a continuous gradient of growth and maturation leading from the core of added new processes out to the periphery of mature Kenyon cell fiber groups. Our results are discussed in the context of Kenyon cell classification, growth dynamics, axonal fiber maturation, and function.

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“…By analogy with studies that have related cell body location and cell birth date (Farris and Strausfeld, 2003), glutamateimmunoreactive KCs that extend into the pedunculus are the last to have been generated during postembryonic development: thus, the basal ring Kenyon cells in the honey bee mushroom body, and Kenyon cells supplying the core neuropil of the adult fruit fly (Farris et al, 2004;Strausfeld et al, 2003). And although the most recently generated Kenyon cells at any instar are glutamate immunoreactive, in adulthood this expression persists only within the core or downgrowth zone of the pedunculus and lobes Brown and Strausfeld, 2006). It is also conceivable that glutamate-positive neuron cell bodies observed in S. littoralis may include Kenyon cells generated in the adult, as is known to occur in the moth Agrotis ipsilon (Dufour and Gadenne, 2006).…”

Section: Discussionmentioning

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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Development‐dependent and ‐independent ubiquitin expression in divisions of the cockroach mushroom body

Cited by 7 publications

References 75 publications

Dynamics of glutamatergic signaling in the mushroom body of young adult Drosophila

Dynamics of glutamatergic signaling in the mushroom body of young adult Drosophila

Sprouting interneurons in mushroom bodies of adult cricket brains

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

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