Adenosine inhibits voltage-dependent Ca2+ influx in cone photoreceptor terminals of the tiger salamander retina

Salvatore L. Stella, Wanda D. Hu, Alejandro Vila, Nicholas C. Brecha

Research output: Contribution to journalArticle

17 Citations (Scopus)

Abstract

Endogenous adenosine has already been shown to inhibit transmitter release from the rod synapse by suppressing Ca2+ influx through voltage-gated Ca2+ channels. However, it is not clear how adenosine modulates the cone synapse. Cone photoreceptors, like rod photoreceptors, also possess L-type Ca2+ channels that regulate the release of L-glutamate. To assess the impact of adenosine on Ca2+ influx though voltage-gated Ca 2+ channels in cone terminals, whole-cell perforated-patch clamp recording and Ca2+ imaging with fluo-4 were used on isolated cones and salamander retinal slices. Synaptic markers (VAMP and piccolo) and activity-dependent dye labeling revealed that tiger salamander cone terminals contain a broad, vesicle-filled cytoplasmic extension at the base of the somatic compartment, which is unlike rod terminals that contain one or more thin axons, each terminating in a large bulbous synaptic terminal. The spatiotemporal Ca2+ responses of the cone terminals do not differ significantly from the Ca2+ responses of the soma or inner segment like that observed in rods. Whole-cell recording of cone ICa and Ca2+ imaging of synaptic terminals in cones demonstrate that adenosine inhibited both I Ca and the depolarization-evoked Ca2+ increase in cone terminals in a dose-dependent manner from 1 to 50 μM, with an EC50 of 15.6 nM. These results indicate that, as in rods, adenosine's ability to suppress voltage-dependent Ca2+ channels at the cone synapse will limit the amount of L-glutamate released. Therefore, adenosine has an inhibitory effect on L-glutamate release at the first synapse, which likely favors elevated adenosine levels in the dark or during dark-adapted conditions.

Original languageEnglish (US)
Pages (from-to)1126-1137
Number of pages12
JournalJournal of Neuroscience Research
Volume85
Issue number5
DOIs
StatePublished - Apr 1 2007

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Ambystoma
Retinal Cone Photoreceptor Cells
Adenosine
Retina
Synapses
Glutamic Acid
Presynaptic Terminals
Cytoplasmic Vesicles
Retinal Rod Photoreceptor Cells
Urodela
Carisoprodol
Patch-Clamp Techniques
Axons
Coloring Agents

All Science Journal Classification (ASJC) codes

  • Cellular and Molecular Neuroscience

Cite this

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abstract = "Endogenous adenosine has already been shown to inhibit transmitter release from the rod synapse by suppressing Ca2+ influx through voltage-gated Ca2+ channels. However, it is not clear how adenosine modulates the cone synapse. Cone photoreceptors, like rod photoreceptors, also possess L-type Ca2+ channels that regulate the release of L-glutamate. To assess the impact of adenosine on Ca2+ influx though voltage-gated Ca 2+ channels in cone terminals, whole-cell perforated-patch clamp recording and Ca2+ imaging with fluo-4 were used on isolated cones and salamander retinal slices. Synaptic markers (VAMP and piccolo) and activity-dependent dye labeling revealed that tiger salamander cone terminals contain a broad, vesicle-filled cytoplasmic extension at the base of the somatic compartment, which is unlike rod terminals that contain one or more thin axons, each terminating in a large bulbous synaptic terminal. The spatiotemporal Ca2+ responses of the cone terminals do not differ significantly from the Ca2+ responses of the soma or inner segment like that observed in rods. Whole-cell recording of cone ICa and Ca2+ imaging of synaptic terminals in cones demonstrate that adenosine inhibited both I Ca and the depolarization-evoked Ca2+ increase in cone terminals in a dose-dependent manner from 1 to 50 μM, with an EC50 of 15.6 nM. These results indicate that, as in rods, adenosine's ability to suppress voltage-dependent Ca2+ channels at the cone synapse will limit the amount of L-glutamate released. Therefore, adenosine has an inhibitory effect on L-glutamate release at the first synapse, which likely favors elevated adenosine levels in the dark or during dark-adapted conditions.",
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Adenosine inhibits voltage-dependent Ca2+ influx in cone photoreceptor terminals of the tiger salamander retina. / Stella, Salvatore L.; Hu, Wanda D.; Vila, Alejandro; Brecha, Nicholas C.

In: Journal of Neuroscience Research, Vol. 85, No. 5, 01.04.2007, p. 1126-1137.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Adenosine inhibits voltage-dependent Ca2+ influx in cone photoreceptor terminals of the tiger salamander retina

AU - Stella, Salvatore L.

AU - Hu, Wanda D.

AU - Vila, Alejandro

AU - Brecha, Nicholas C.

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N2 - Endogenous adenosine has already been shown to inhibit transmitter release from the rod synapse by suppressing Ca2+ influx through voltage-gated Ca2+ channels. However, it is not clear how adenosine modulates the cone synapse. Cone photoreceptors, like rod photoreceptors, also possess L-type Ca2+ channels that regulate the release of L-glutamate. To assess the impact of adenosine on Ca2+ influx though voltage-gated Ca 2+ channels in cone terminals, whole-cell perforated-patch clamp recording and Ca2+ imaging with fluo-4 were used on isolated cones and salamander retinal slices. Synaptic markers (VAMP and piccolo) and activity-dependent dye labeling revealed that tiger salamander cone terminals contain a broad, vesicle-filled cytoplasmic extension at the base of the somatic compartment, which is unlike rod terminals that contain one or more thin axons, each terminating in a large bulbous synaptic terminal. The spatiotemporal Ca2+ responses of the cone terminals do not differ significantly from the Ca2+ responses of the soma or inner segment like that observed in rods. Whole-cell recording of cone ICa and Ca2+ imaging of synaptic terminals in cones demonstrate that adenosine inhibited both I Ca and the depolarization-evoked Ca2+ increase in cone terminals in a dose-dependent manner from 1 to 50 μM, with an EC50 of 15.6 nM. These results indicate that, as in rods, adenosine's ability to suppress voltage-dependent Ca2+ channels at the cone synapse will limit the amount of L-glutamate released. Therefore, adenosine has an inhibitory effect on L-glutamate release at the first synapse, which likely favors elevated adenosine levels in the dark or during dark-adapted conditions.

AB - Endogenous adenosine has already been shown to inhibit transmitter release from the rod synapse by suppressing Ca2+ influx through voltage-gated Ca2+ channels. However, it is not clear how adenosine modulates the cone synapse. Cone photoreceptors, like rod photoreceptors, also possess L-type Ca2+ channels that regulate the release of L-glutamate. To assess the impact of adenosine on Ca2+ influx though voltage-gated Ca 2+ channels in cone terminals, whole-cell perforated-patch clamp recording and Ca2+ imaging with fluo-4 were used on isolated cones and salamander retinal slices. Synaptic markers (VAMP and piccolo) and activity-dependent dye labeling revealed that tiger salamander cone terminals contain a broad, vesicle-filled cytoplasmic extension at the base of the somatic compartment, which is unlike rod terminals that contain one or more thin axons, each terminating in a large bulbous synaptic terminal. The spatiotemporal Ca2+ responses of the cone terminals do not differ significantly from the Ca2+ responses of the soma or inner segment like that observed in rods. Whole-cell recording of cone ICa and Ca2+ imaging of synaptic terminals in cones demonstrate that adenosine inhibited both I Ca and the depolarization-evoked Ca2+ increase in cone terminals in a dose-dependent manner from 1 to 50 μM, with an EC50 of 15.6 nM. These results indicate that, as in rods, adenosine's ability to suppress voltage-dependent Ca2+ channels at the cone synapse will limit the amount of L-glutamate released. Therefore, adenosine has an inhibitory effect on L-glutamate release at the first synapse, which likely favors elevated adenosine levels in the dark or during dark-adapted conditions.

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