Cellular localisation of metabotropic glutamate receptors in the mammalian optic nerve: a mechanism for axon-glia communication

Jeffery, Glen; Sharp, C.; Malitschek, Barbara; Salt, Thomas E.; Kühn, Rainer; Knöpfel, Thomas

doi:10.1016/s0006-8993(96)00919-5

Cited by 21 publications

(16 citation statements)

References 24 publications

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“…In our material, mGluR5 immunoreactivity was also present in astrocytic cell bodies, in line with the previous studies ( Van den Pol et al, 1994Romano et al, 1995;Liu et al, 1998). mGluR2/3 immunostaining was confined to the neuropil, in line with ultrastructural studies on VP and other brain regions (Liu et al, 1998) that showed immunoreactivity in glial processes and occasionally in axon terminals (Petralia et al, 1996;Jeffery et al, 1996). In the youngest animals examined, mGluR1␣ and mGluR2/3 immunostaining was transiently found in fibers of the descending trigeminal tract, and mGluR2/3 also appeared in fiber bundles within brainstem trigeminal nuclei, the internal capsule and cortical white matter.…”

Section: Discussionsupporting

confidence: 92%

Development of metabotropic glutamate receptors from trigeminal nuclei to barrel cortex in postnatal mouse

1999

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Expression patterns of group I (mGluR1α and mGluR5) and group II (mGluR2/3) metabotropic glutamate receptor subtypes were examined immunocytochemically in the trigeminal system of mice during the first 3 weeks of postnatal development, when somatotopic whisker representations are sequentially established from brainstem through thalamus to cerebral cortex. Immunostaining for all three epitopes formed whisker‐related patterns in the trigeminal nuclei from postnatal day (P) 0, in the ventral posterior thalamic nucleus from P2, and in the posteromedial barrel subfield of somatosensory cortex (SI) from P4. The appearance of whisker‐related patterns was preceded by increased levels of immunostaining of the neuropil, which subsequently declined from the trigeminal nuclei upward. In SI, mGluR1α‐positive neurons were observed in all cortical layers from P2. mGluR5 was localized in neurons, glial cells, and neuropil from P2. mGluR2/3 immunostaining was distributed only in the neuropil at all ages. The three receptor subtypes showed moderate to high expression in deep layer V throughout development. Transient expression peaked in the hollows of layer IV barrels from P4 to P9, and then fell off as expression increased in supragranular layers from P14 to P21. The deep aspect of the cortical subplate (layer VIb) showed dense mGluR5 and less dense mGluR1α immunostaining throughout development. Up‐regulation of expression of group I and II mGluRs is correlated with the growth and refinement of connectivity and the establishment of somatotopic patterns in the three main relay stations of the trigeminal system. This finding suggests roles for mGluRs in the early processing of sensory information and in developmental plasticity. J. Comp. Neurol. 409:549–566, 1999. © 1999 Wiley‐Liss, Inc.

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Section: Discussionsupporting

confidence: 92%

Development of metabotropic glutamate receptors from trigeminal nuclei to barrel cortex in postnatal mouse

1999

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“…It is likely that the cells that provide information to developing fibres are immature astrocytes, because, at the time of chiasm formation, oligodendrocytes are not yet present (Skoff et al, 1976(Skoff et al, , 1980. Furthermore, it is clear from studies in the mature optic nerve that neurotransmitter signalling can occur between optic axons and glia (Kriegler and Chiu, 1993) and that this is mediated by one of the metabotropic glutamate receptors, mGluR3, between axons and astrocytes (Jeffery et al, 1996). Whether any of these receptors play a role in signalling at the developing chiasm remains to be revealed.…”

Section: Discussionmentioning

confidence: 99%

First evidence of diversity in eutherian chiasmatic architecture: Tree shrews, like marsupials, have spatially segregated crossed and uncrossed chiasmatic pathways

1998

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In the optic chiasm of mammals, axons either cross the midline to the opposite side of the brain or remain uncrossed. In the eutherian species studied to date, uncrossed axons in the caudal nerve are found in all regions. In the chiasm, they are dispersed through the hemichiasm, with many axons approaching the midline and then turning back to enter the same side of the brain as the originating eye. In marsupials, by contrast, uncrossed axons never approach the midline; instead, they remain grouped in the lateral nerve and chiasm. The impression gained from these data is that there is a major difference in chiasmatic architecture between eutherian and marsupial mammals. Therefore, the mechanisms by which axons choose their route through the chiasm was also thought to differ between the two major groups of mammals. However, the present study shows that the chiasm of a highly visual eutherian mammal, the tree shrew, is similar to that found in marsupials, with uncrossed axons confined to lateral regions and not approaching the midline. However, unlike marsupials, in the tree shrew, optic fascicles in the chiasm are often separated by thick collagen bundles. It is probable that the chiasmatic structure described to date for eutherian mammals is not ubiquitous, as was previously thought, and theories explaining the mechanisms by which axons chose their route through the chiasm during development will have to be expanded.

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“…These cells may represent oligodendrocytes such as those identified in the rat optic nerve (Butt and Ransom, 1989). Interestingly, oligodendrocytes in vitro and astrocytes in the rat optic nerve as well as uncharacterized glia throughout the brain have been reported to contain non-NMDA ionotropic and metabotropic glutamate receptors (Jeffery et al, 1996;Petralia et al, 1996;Steinhauser and Gallo, 1996). The role of glial glutamate receptors is the subject of increasing research interest.…”

Section: Discussionmentioning

confidence: 99%

Immunolabeling reveals cellular localization of the N-methyl-D-aspartate receptor subunit NR2B in neurosecretory cells but not astrocytes of the rat magnocellular nuclei

et al. 2000

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Previous studies suggest that activation of N-methyl-D-aspartate (NMDA) receptors facilitates phasic firing and spike clustering displayed by magnocellular neuroendocrine cells (MNCs) of the supraoptic (SON) and paraventricular nucleus of the hypothalamus (PVN). Osmotic stimulation produces similar activity patterns which, in turn, can lead to enhanced release of vasopressin and oxytocin from MNCs. Our laboratory has shown that dehydration regulates the expression of the NMDA receptor subunits, NR1 and NR2B, in the SON and PVN, suggesting their involvement in osmoregulation. In the present study, we examined the cellular localization of NR2B, one of the glutamate-binding subunits of the NMDA receptor, with an NR2B-specific antibody. Using double-label immunohistochemistry and three different detection methods with metallic, peroxidase, and fluorescence markers, it was found that both vasopressin and oxytocin-producing MNC populations synthesize NR2B. The incidence of NR2B colocalization with vasopressin-neurophysin in the SON and lateral magnocellular PVN (PVL) was 0.95 and 0.91, respectively. For oxytocin-neurophysin, the corresponding values were 0.97 and 0.95, respectively. Furthermore, the extent of colocalization in MNCs of the SON, PVL, retrochiasmatic SON, and accessory neurosecretory nuclei was similar. Astrocytes associated with the SON, and identified with antibodies targeting glial fibrillary acidic protein (GFAP) or vimentin, were not colabeled with NR2B. Our results demonstrate that NR2B protein is expressed by almost all MNCs and that it is equally prevalent in vasopressinergic and oxytocinergic populations of various magnocellular neuroendocrine nuclei supporting a role of NMDA receptors in MNC-mediated neurosecretory processes. Although NR2B may form part of functional NMDA receptors on MNCs, it is probably not present on astrocytes associated with nearby MNCs.

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Cellular localisation of metabotropic glutamate receptors in the mammalian optic nerve: a mechanism for axon-glia communication

Cited by 21 publications

References 24 publications

Development of metabotropic glutamate receptors from trigeminal nuclei to barrel cortex in postnatal mouse

Development of metabotropic glutamate receptors from trigeminal nuclei to barrel cortex in postnatal mouse

First evidence of diversity in eutherian chiasmatic architecture: Tree shrews, like marsupials, have spatially segregated crossed and uncrossed chiasmatic pathways

Immunolabeling reveals cellular localization of the N-methyl-D-aspartate receptor subunit NR2B in neurosecretory cells but not astrocytes of the rat magnocellular nuclei

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