Differential expression of ionotropic glutamate receptor subunits in the outer retina

Morigiwa, Katsuko; Vardi, Noga

doi:10.1002/(sici)1096-9861(19990308)405:2<173::aid-cne3>3.0.co;2-l

Cited by 122 publications

(119 citation statements)

References 68 publications

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“…Recent studies on the localization of the various known glutamate receptors in the OPL revealed an unexpectedly high degree of complexity. The effects of glutamate released by the photoreceptors are mediated and modulated by glutamate receptors, which are present post-and presynaptically and extrasynaptically at the photoreceptor synapses (9,14,19,(32)(33)(34)(35).…”

Section: Discussionmentioning

confidence: 99%

An alternative pathway for rod signals in the rodent retina: Rod photoreceptors, cone bipolar cells, and the localization of glutamate receptors

Hack

Peichl

Brandstätter

1999

Proc. Natl. Acad. Sci. U.S.A.

165

157

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In the mammalian retina, extensive processing of spatiotemporal and chromatic information occurs. One key principle in signal transfer through the retina is parallel processing. Two of these parallel pathways are the ON-and OFF-channels transmitting light and dark signals. This dual system is created in the outer plexiform layer, the first relay station in retinal signal transfer. Photoreceptors release glutamate onto ON-and OFF-type bipolar cells, which are functionally distinguished by their postsynaptic expression of different types of glutamate receptors, namely ionotropic and metabotropic glutamate receptors. In the current concept, rod photoreceptors connect only to rod bipolar cells (ON-type) and cone photoreceptors connect only to cone bipolar cells (ON-and OFF-type). We have studied the distribution of (RS)-␣-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) glutamate receptor subunits at the synapses in the outer plexiform layer of the rodent retina by immunoelectron microscopy and serial section reconstruction. We report a non-classical synaptic contact and an alternative pathway for rod signals in the retina. Rod photoreceptors made synaptic contact with putative OFF-cone bipolar cells that expressed the AMPA glutamate receptor subunits GluR1 and GluR2 on their dendrites. Thus, in the retina of mouse and rat, an alternative pathway for rod signals exists, where rod photoreceptors bypass the rod bipolar cell and directly excite OFF-cone bipolar cells through an ionotropic sign-conserving AMPA glutamate receptor.

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Section: Discussionmentioning

confidence: 99%

An alternative pathway for rod signals in the rodent retina: Rod photoreceptors, cone bipolar cells, and the localization of glutamate receptors

Hack

Peichl

Brandstätter

1999

Proc. Natl. Acad. Sci. U.S.A.

165

157

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“…For example, it has been shown to play a role in insulin secretion from pancreatic islet beta-cells~Spurlin et al & Vardi, 1999;Qin & Pourcho, 1999a, 1999bHack et al, 2001;Pan & Massey, 2007!, although …”

Section: Pre-or Postsynaptic Function?mentioning

confidence: 99%

Robust syntaxin-4 immunoreactivity in mammalian horizontal cell processes

et al. 2007

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Horizontal cells mediate inhibitory feed-forward and feedback communication in the outer retina; however, mechanisms that underlie transmitter release from mammalian horizontal cells are poorly understood. Toward determining whether the molecular machinery for exocytosis is present in horizontal cells, we investigated the localization of syntaxin-4, a SNARE protein involved in targeting vesicles to the plasma membrane, in mouse, rat, and rabbit retinae using immunocytochemistry. We report robust expression of syntaxin-4 in the outer plexiform layer of all three species. Syntaxin-4 occurred in processes and tips of horizontal cells, with regularly spaced, thicker sandwich-like structures along the processes. Double labeling with syntaxin-4 and calbindin antibodies, a horizontal cell marker, demonstrated syntaxin-4 localization to horizontal cell processes; whereas, double labeling with PKC antibodies, a rod bipolar cell~RBC! marker, showed a lack of co-localization, with syntaxin-4 immunolabeling occurring just distal to RBC dendritic tips. Syntaxin-4 immunolabeling occurred within VGLUT-1-immunoreactive photoreceptor terminals and underneath synaptic ribbons, labeled by CtBP20RIBEYE antibodies, consistent with localization in invaginating horizontal cell tips at photoreceptor triad synapses. Vertical sections of retina immunostained for syntaxin-4 and peanut agglutinin~PNA! established that the prominent patches of syntaxin-4 immunoreactivity were adjacent to the base of cone pedicles. Horizontal sections through the OPL indicate a one-to-one co-localization of syntaxin-4 densities at likely all cone pedicles, with syntaxin-4 immunoreactivity interdigitating with PNA labeling. Pre-embedding immuno-electron microscopy confirmed the subcellular localization of syntaxin-4 labeling to lateral elements at both rod and cone triad synapses. Finally, co-localization with SNAP-25, a possible binding partner of syntaxin-4, indicated co-expression of these SNARE proteins in the same subcellular compartment of the horizontal cell. Taken together, the strong expression of these two SNARE proteins in the processes and endings of horizontal cells at rod and cone terminals suggests that horizontal cell axons and dendrites are likely sites of exocytotic activity.

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“…At ribbon-type synapses of the auditory, vestibular, and visual systems, vesicles are first thought to be captured or ''docked'' to a ''synaptic ribbon,'' before undergoing exocytosis. Synaptic ribbons are specifically located opposite postsynaptic receptors (2)(3)(4)(5) and tethered to each synaptic ribbon is a dense array of synaptic vesicles (6)(7)(8). Given this localization and the fact that these structures are specific to nonspiking tonic synapses that release large amounts of neurotransmitter, it has long been suggested that vesicles tethered to the ribbon are recruited to release neurotransmitter in these synapses (9)(10)(11).…”

mentioning

confidence: 98%

Vesicle association and exocytosis at ribbon and extraribbon sites in retinal bipolar cell presynaptic terminals

Zenisek

2008

Proc. Natl. Acad. Sci. U.S.A.

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Synaptic vesicles release neurotransmitter by following a process of vesicle docking and exocytosis. Although these steps are well established, it has been difficult to observe and measure these rates directly in living synapses. Here, by combining the direct imaging of single synaptic vesicles and synaptic ribbons, I measure the properties of vesicle docking and evoked and spontaneous release from ribbon and extraribbon locations in a ribbon-type synaptic terminal, the goldfish retinal bipolar cell. In the absence of a stimulus, captured vesicles near ribbons associate tightly and only rarely undock or undergo spontaneous exocytosis. By contrast, vesicle capture at outlier sites is less stable and spontaneous exocytosis occurs at a higher rate. In response to a stimulus, exocytic events cluster near ribbons, but show no evidence of clustering away from ribbon sites. Together, the results here indicate that, although vesicles can associate and fuse both near and away from synaptic sites, vesicles at synaptic ribbons associate more stably and fusion is more tightly linked to stimuli.imaging ͉ neurotransmitter release ͉ retina ͉ synapse ͉ synaptic vesicle

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Differential expression of ionotropic glutamate receptor subunits in the outer retina

Cited by 122 publications

References 68 publications

An alternative pathway for rod signals in the rodent retina: Rod photoreceptors, cone bipolar cells, and the localization of glutamate receptors

An alternative pathway for rod signals in the rodent retina: Rod photoreceptors, cone bipolar cells, and the localization of glutamate receptors

Robust syntaxin-4 immunoreactivity in mammalian horizontal cell processes

Vesicle association and exocytosis at ribbon and extraribbon sites in retinal bipolar cell presynaptic terminals

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