Differential distribution ofShaker-like andShab-like K+-channel subunits in goldfish retina and retinal bipolar cells

Yazulla, Stephen; Studholme, Keith M.

doi:10.1002/(sici)1096-9861(19980622)396:1<131::aid-cne10>3.0.co;2-s

Cited by 36 publications

(23 citation statements)

References 43 publications

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“…Ozaita et al (2004) have provided evidence for potassium channels on amacrine cell dendrites in the mouse. K + channel subunits (Kv1.1, 1.2, 2.1) that account for the delayed rectifier have been localized to all Mb bipolar cells in goldfish retina (Yazulla and Studholme 1998). Immunoreactivity in the region of Mb bipolar terminals is punctate and does not have the extended features of the intrusions.…”

Section: Sodium Channels On Invaginating Dendritessupporting

confidence: 75%

Novel processes invaginate the pre-synaptic terminal of retinal bipolar cells

Zimov

Yazulla

2008

Cell Tissue Res

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Mixed-rod cone bipolar (Mb) cells of goldfish retina have large synaptic terminals (10 microm in diameter) that make 60-90 ribbon synapses mostly onto amacrine cells and rarely onto ganglion cells and, in return, receive 300-400 synapses from gamma-aminobutyric acid (GABA)-ergic amacrine cells. Tissue viewed by electron microscopy revealed the presence of double-membrane-bound processes deep within Mb terminals. No membrane specializations were apparent on these invaginating processes, although rare vesicular fusion was observed. These invaginating dendrites were termed "InDents". Mb bipolar cells were identified by their immunoreactivity for protein kinase C. Double-label immunofluorescence with other cell-type-specific labels eliminated Müller cells, efferent fibers, other Mb bipolar cells, dopaminergic interplexiform cells, and somatostatin amacrine cells as a source of the InDents. Confocal analysis of double-labeled tissue clearly showed dendrites of GABA amacrine cells, backfilled ganglion cells, and dendrites containing PanNa immunoreactivity extending into and passing through Mb terminals. Nearly all Mb terminals showed evidence for the presence of InDents, indicating their common presence in goldfish retina. No PanNa immunoreactivity was found on GABA or ganglion cell InDents, suggesting that a subtype of glycine amacrine cell contained voltage-gated Na channels. Thus, potassium and calcium voltage-gated channels might be present on the InDents and on the Mb terminal membrane opposed to the InDents. In addition to synaptic signaling at ribbon and conventional synapses, Mb bipolar cells may exchange information with InDents by an alternative signaling mechanism.

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Section: Sodium Channels On Invaginating Dendritessupporting

confidence: 75%

Novel processes invaginate the pre-synaptic terminal of retinal bipolar cells

Zimov

Yazulla

2008

Cell Tissue Res

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“…Similarly, the identical perisynaptic localization pattern of SAP102 and NR2B subunit also suggests a preferential interaction that is consistent with previous evidence in rat retina showing similar colocalization at the LM level in the IPL (Koulen et al, 1998b) and coimmunoprecipitation results in rat brain (Müller et al, 1996; Sans et al, 2000). The MAGUKs examined here also may underlie targeting of AMPARs (e.g., Roche et al, 1999; Elias et al, 2006), or potassium channels (Kim et al, 1995; Kim and Sheng, 1996; Yazulla and Studholme, 1998). In addition, it remains to be investigated whether other proteins that interact with NMDAR subunits – e.g., interactor collapsin receptor mediator protein 2 (GRMP2), which interacts with NR2B (Al-Hallaq et al, 2007) – affect synaptic signaling in RGCs.…”

Section: Discussionmentioning

confidence: 99%

Subunit- and Pathway-Specific Localization of NMDA Receptors and Scaffolding Proteins at Ganglion Cell Synapses in Rat Retina

Zhang¹,

Diamond²

2009

J. Neurosci.

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Retinal ganglion cells (RGCs) receive excitatory glutamatergic input from ON and OFF bipolar cells in distinct sublaminae of the inner plexiform layer (IPL). AMPA and NMDA receptors (AMPARs and NMDARs) mediate excitatory inputs in both synaptic layers, but specific roles for NMDARs at RGC synapses remain unclear. NMDARs comprise NR1 and NR2 subunits and are anchored by membrane associated guanylate kinases (MAGUKs), but it is unknown whether particular NR2 subunits associate preferentially with particular NR1 splice variants and MAGUKs. Here, we used postembedding immunogold electron microscopy (EM) techniques to examine the subsynaptic localization of NMDAR subunits and MAGUKs at ON and OFF synapses onto rat RGCs. We found that the NR2A subunit, the NR1C2‘ splice variant and MAGUKs PSD-95 and PSD-93 are localized to the postsynaptic density (PSD), preferentially at OFF synapses, whereas the NR2B subunit, the NR1C2 splice variant and the MAGUK SAP102 are localized perisynaptically, with NR2B exhibiting a preference for ON synapses. Consistent with these anatomical data, spontaneous EPSCs (sEPSCs) recorded from OFF cells exhibited an NMDAR component that was insensitive to the NR2B antagonist Ro 25-6981. In ON cells, sEPSCs expressed an NMDAR component, partially sensitive to Ro 25-6981, only when glutamate transport was inhibited, indicating perisynaptic expression of NR2B NMDARs. These results provide the first evidence for preferential association of particular NR1 splice variants, NR2 subunits and MAGUKs at central synapses and suggest that different NMDAR subtypes may play specific roles at functionally distinct synapses in the retinal circuitry.

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“…5C). The former was shown to be expressed in photoreceptors (56) and the latter is known to be a part of the interphotoreceptor matrix (57). However the highly restricted localization patterns observed in Fig.…”

Section: Averaging Protein Distribution Profiles Between Twomentioning

confidence: 99%

Proteomic Profiling of a Layered Tissue Reveals Unique Glycolytic Specializations of Photoreceptor Cells

Reidel

Thompson

Farsiu

et al. 2011

Molecular & Cellular Proteomics

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The retina is a highly ordered tissue whose outermost layers are formed by subcellular compartments of photoreceptors generating light-evoked electrical responses. We studied protein distributions among individual photoreceptor compartments by separating the entire photoreceptor layer of a flat-mounted frozen retina into a series of thin tangential cryosections and analyzing protein compositions of each section by label-free quantitative mass spectrometry. Based on 5038 confidently identified peptides assigned to 896 protein database entries, we generated a quantitative proteomic database (a "map") correlating the distribution profiles of identified proteins with the profiles of marker proteins representing individual compartments of photoreceptors and adjacent cells. We evaluated the applicability of several common peptide-toprotein quantification algorithms in the context of our database and found that the highest reliability was obtained by summing the intensities of all peptides representing a given protein, using at least the 5-6 most intense peptides when applicable. We used this proteome map to investigate the distribution of glycolytic enzymes, critical in fulfilling the extremely high metabolic demands of photoreceptor cells, and obtained two major findings. First, unlike the majority of neurons rich in hexokinase I, but similar to other highly metabolically active cells, photoreceptors express hexokinase II. Hexokinase II has a very high catalytic activity when associated with mitochondria, and indeed we found it colocalized with mitochondria in photoreceptors. Second, photoreceptors contain very little triosephosphate isomerase, an enzyme converting dihydroxyacetone phosphate into glyceraldehyde-3-phosphate. This may serve as a functional adaptation because dihydroxyacetone phosphate is a major precursor in phospholipid biosynthesis, a process particularly active in photoreceptors because of the constant renewal of their lightsensitive membrane disc stacks. Overall, our approach for proteomic profiling of very small tissue amounts at a resolution of a few microns, combining cryosectioning and liquid chromatography-tandem MS, can be applied for quantitative investigation of proteomes where spatial resolution is paramount.

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Differential distribution ofShaker-like andShab-like K+-channel subunits in goldfish retina and retinal bipolar cells

Cited by 36 publications

References 43 publications

Novel processes invaginate the pre-synaptic terminal of retinal bipolar cells

Novel processes invaginate the pre-synaptic terminal of retinal bipolar cells

Subunit- and Pathway-Specific Localization of NMDA Receptors and Scaffolding Proteins at Ganglion Cell Synapses in Rat Retina

Proteomic Profiling of a Layered Tissue Reveals Unique Glycolytic Specializations of Photoreceptor Cells

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