Selective synaptic distribution of AMPA and kainate receptor subunits in the outer plexiform layer of the carp retina

Schultz, Konrad; Janssen‐Bienhold, Ulrike; Weiler, Reto

doi:10.1002/cne.1042

Cited by 26 publications

(30 citation statements)

References 60 publications

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“…The patterns described in the present study are in good agreement with earlier reports (Hughes et al, 1992;Mü ller et al, 1992). At the protein level, the localization of AMPA-type GluRs in the retina has been described for cat Morigiwa and Vardi, 1999;Qin and Pourcho, 1999a,b), rat (Peng et al, 1995;Vardi et al, 1998;Hack et al, 1999;Qin and Pourcho, 1999a), goldfish (Peng et al, 1995;Schultz et al, 1997;Vardi et al, 1998;Yazulla and Studholme, 1999;Qin and Pourcho, 1999a,b;Vandenbranden et al, 2000), and carp (Schultz et al, 2001). We will, therefore, restrict the discussion mainly to the localization of AMPA-type GluR subunits in the outer retina with respect to their localization in bipolar cells.…”

Section: Discussionsupporting

confidence: 93%

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Expression of AMPA‐type glutamate receptor subunit (GluR2) in ON‐bipolar neurons in the rat retina

Kamphuis

Klooster

Dijk

2002

J of Comparative Neurology

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The role of glutamate receptors (GluR) in the signal pathways of the retina is widely recognized. Photoreceptors make synaptic contact with functionally different classes of bipolar cells. The OFF-type bipolar cells mediate light offset-evoked responses and use ionotropic alpha-amino-3-hydroxy-5-methyl-isoxazole-4-propionate (AMPA)- or kainate-type GluRs, whereas bipolars involved in the ON-pathway use the metabotropic GluR6. This dichotomy predicts a defined expression pattern of AMPA-type GluRs and mGluR6 in bipolar cell classes. This hypothesis was tested by performing immunocytochemical double labeling studies combining GluR-specific antibodies with markers specific for the diverse bipolar cell populations in the rat retina. AMPA-type receptors are composed of combinations of four types of subunits, GluR1-4. GluR1 is expressed by a few somata in the outer part of the inner nuclear layer (INL). Sparse colocalization with any of the bipolar markers used could be established. In contrast, GluR2 is expressed by many of the somata in the outer zone of the INL. At the transcript level, in situ hybridizations demonstrated abundant GluR2 expression over the complete width of the INL. In contrast to our expectations, approximately 70% of the somata labeled by the rod ON-bipolar markers protein kinase C (PKC) or Goalpha, colocalized with GluR2. Approximately 90% of the OFF-type bipolar cells, identified as recoverin-positive, showed GluR2 immunoreactivity. At least 40% of the somata that were mGluR6-immunoreactive, a both rod and cone ON-type bipolar marker, were GluR2-immunopositive. Ultrastructurally, examples were observed of GluR2 localization in bipolar processes with labeling outside the actual compartment associated with the synaptic complex of the rod terminal. No specific antibody was available against GluR3, but 74% of the PKC-positive cells were GluR2/3-positive. GluR4 did not show a somatic localization making double labeling impossible. On the basis of these results, we conclude that ionotropic GluRs are expressed by rod ON-type bipolar cells (PKC- or Goalpha-immunoreactive), and by cone ON- and OFF-type bipolars based on a colocalization with nearly all of the present recoverin-positive somata. Our observations show that the functional dichotomy in ON- and OFF-type bipolars is not reflected in a matching expression pattern of ionotropic and metabotropic GluRs. This finding raises the intriguing possibility that the AMPA-type GluRs are, in an as yet unclear manner, involved in the ON signaling pathways of rods and cones.

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Section: Discussionsupporting

confidence: 93%

“…The GluR2/3 immunoreactivity was depicted as being concentrated at the site of the invagination of the dendrite into the rod spherule, and appears to differ from the localization of GluR2 at noninvaginating dendrites (Hack et al, 1999). In the carp, ON-and OFF-bipolar processes contacting red cones were GluR2/3-IR (Schultz et al, 2001). …”

Section: Glur2mentioning

confidence: 99%

Expression of AMPA‐type glutamate receptor subunit (GluR2) in ON‐bipolar neurons in the rat retina

Kamphuis

Klooster

Dijk

2002

J of Comparative Neurology

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“…Also, our fixation was from 30 min to 60 min, a condition that reduced GluRl-IR in goldfish (VandenBranden et al, 2000a). Recently, Schultz et al (2001) used an antiserum against GluRl from PharMingen at 1: 500 in carp retina. They also report weak somatic labeling and no labeling in either plexiform layer.…”

Section: Glycinergic Systemmentioning

confidence: 99%

Neurochemical anatomy of the zebrafish retina as determined by immunocytochemistry

Yazulla¹,

Studholme²

2002

Chemical Anatomy of the Zebrafish Retina

117

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The zebrafish retina is rapidly becoming a major preparation for the study of molecular genetic mechanisms underlying neural development and visual behavior. Studies utilizing retinal mutants would benefit by the availability of a data base on the distribution of neurotransmitter systems in the wild-type fish. To this end, the neurochemical anatomy of the zebrafish retina was surveyed by light microscopic immunocytochemistry. An extensive series of 60 separate antibodies were used to describe the distribution of major transmitter systems and a variety of neuron-associated membrane channels and proteins.These include markers (i.e., antibodies against enzymes, receptors, transporters) for transmitters: GABA, glycine, glutamate, biogenic amines, acetylcholine, cannabinoids and neuropeptides; as well as a sample of voltage-gated channels and synapse associated membrane proteins. Discussion of the comparative localization of these antibodies is restricted to other teleost fishes, particularly goldfish. Overall, there was great similarity in the distribution of the various markers, as might be expected. However, there were some notable differences, including several antibodies that did not label zebrafish at all, even though goldfish retinas that were processed in parallel, labeled beautifully. This survey is extensive, but not exhaustive, and hopefully will serve as a valuable resource for future studies of the zebrafish retina.

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“…3A). Fret43 is an antiserum that marks the pedicles of red-and green-sensitive cones in carp retina (Schultz et al, 2001), and double-labeling experiments confirmed the presence of Caldendrin in cone pedicles (Fig. 3B).…”

Section: Synaptic Localization Of Caldendrinmentioning

confidence: 68%

“…In cone pedicles, label was typically concentrated in elements lateral to the synaptic ribbons (Fig. 4A,B), which were identified as horizontal cell terminals on the basis of their shape and location (Stell, 1975;Schultz et al, 2001). Label was confined to the membrane and a narrow band of cytoplasm in close proximity to the membrane and was most prominent at the tips of spinules and along the membranes facing the releasing site of neurotransmitter of the cones.…”

Section: Synaptic Localization Of Caldendrinmentioning

confidence: 97%

Calcium‐binding protein Caldendrin and CaMKII are localized in spinules of the carp retina

Schultz

Janssen‐Bienhold

Gundelfinger

et al. 2004

J of Comparative Neurology

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Calcium-binding proteins translate the influx of Ca(2+) at excitatory synapses into spatiotemporal signals that regulate a variety of processes underlying synaptic plasticity. In the fish retina, the synaptic connectivity between photoreceptors and horizontal cells undergoes a remarkable plasticity, triggered by the ambient light conditions. With increasing light, the synaptic dendrites of horizontal cells form numerous spinules that are dissolved during dark adaptation. The dynamic regulation of this process is calcium-dependent and involves the Ca(2+)/calmodulin-dependent protein kinase II (CaMKII), but astonishingly its principal regulator Calmodulin (CaM) could not be localized to spinules. Here, we show that antibodies directed against Caldendrin (CaBP1), a member of the EF-hand calcium-binding protein family, strongly label the terminal dendrites of horizontal cells invaginating cone pedicles. Double-labeling experiments revealed that this label is closely associated with label for CaMKII. This association was confirmed at the ultrastructural level. Caldendrin immunoreactivity and CaMKII immunoreactivity are both present in horizontal cell dendrites flanking the synaptic ribbon within the cone pedicle and in particular in spinules formed by these terminals. Comparison of light- and dark-adapted retinas revealed a shift of the membrane-associated label for Caldendrin from the terminal dendrites into the spinules during light adaptation. These results suggest that Caldendrin is involved in the dynamic regulation of spinules and confirms the assumed potential of Caldendrin as a neural calcium sensor for synaptic plasticity.

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Selective synaptic distribution of AMPA and kainate receptor subunits in the outer plexiform layer of the carp retina

Cited by 26 publications

References 60 publications

Expression of AMPA‐type glutamate receptor subunit (GluR2) in ON‐bipolar neurons in the rat retina

Expression of AMPA‐type glutamate receptor subunit (GluR2) in ON‐bipolar neurons in the rat retina

Neurochemical anatomy of the zebrafish retina as determined by immunocytochemistry

Calcium‐binding protein Caldendrin and CaMKII are localized in spinules of the carp retina

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