Calcium homeostasis and cone signaling are regulated by interactions between calcium stores and plasma membrane ion channels.

Calcium is a messenger ion that controls all aspects of cone photoreceptor function, including synaptic release. The dynamic range of the cone output extends beyond the activation threshold for voltage-operated calcium entry, suggesting another calcium influx mechanism operates in cones hyperpolariz...

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Main Authors: Tamas Szikra, Peter Barabas, Theodore M Bartoletti, Wei Huang, Abram Akopian, Wallace B Thoreson, David Krizaj
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2009-08-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC2725299?pdf=render
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author Tamas Szikra
Peter Barabas
Theodore M Bartoletti
Wei Huang
Abram Akopian
Wallace B Thoreson
David Krizaj
author_facet Tamas Szikra
Peter Barabas
Theodore M Bartoletti
Wei Huang
Abram Akopian
Wallace B Thoreson
David Krizaj
author_sort Tamas Szikra
collection DOAJ
description Calcium is a messenger ion that controls all aspects of cone photoreceptor function, including synaptic release. The dynamic range of the cone output extends beyond the activation threshold for voltage-operated calcium entry, suggesting another calcium influx mechanism operates in cones hyperpolarized by light. We have used optical imaging and whole-cell voltage clamp to measure the contribution of store-operated Ca(2+) entry (SOCE) to Ca(2+) homeostasis and its role in regulation of neurotransmission at cone synapses. Mn(2+) quenching of Fura-2 revealed sustained divalent cation entry in hyperpolarized cones. Ca(2+) influx into cone inner segments was potentiated by hyperpolarization, facilitated by depletion of intracellular Ca(2+) stores, unaffected by pharmacological manipulation of voltage-operated or cyclic nucleotide-gated Ca(2+) channels and suppressed by lanthanides, 2-APB, MRS 1845 and SKF 96365. However, cation influx through store-operated channels crossed the threshold for activation of voltage-operated Ca(2+) entry in a subset of cones, indicating that the operating range of inner segment signals is set by interactions between store- and voltage-operated Ca(2+) channels. Exposure to MRS 1845 resulted in approximately 40% reduction of light-evoked postsynaptic currents in photopic horizontal cells without affecting the light responses or voltage-operated Ca(2+) currents in simultaneously recorded cones. The spatial pattern of store-operated calcium entry in cones matched immunolocalization of the store-operated sensor STIM1. These findings show that store-operated channels regulate spatial and temporal properties of Ca(2+) homeostasis in vertebrate cones and demonstrate their role in generation of sustained excitatory signals across the first retinal synapse.
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spelling doaj.art-ebbf04a5f5ac461893d482d8a6fdb5f22022-12-22T02:43:12ZengPublic Library of Science (PLoS)PLoS ONE1932-62032009-08-0148e672310.1371/journal.pone.0006723Calcium homeostasis and cone signaling are regulated by interactions between calcium stores and plasma membrane ion channels.Tamas SzikraPeter BarabasTheodore M BartolettiWei HuangAbram AkopianWallace B ThoresonDavid KrizajCalcium is a messenger ion that controls all aspects of cone photoreceptor function, including synaptic release. The dynamic range of the cone output extends beyond the activation threshold for voltage-operated calcium entry, suggesting another calcium influx mechanism operates in cones hyperpolarized by light. We have used optical imaging and whole-cell voltage clamp to measure the contribution of store-operated Ca(2+) entry (SOCE) to Ca(2+) homeostasis and its role in regulation of neurotransmission at cone synapses. Mn(2+) quenching of Fura-2 revealed sustained divalent cation entry in hyperpolarized cones. Ca(2+) influx into cone inner segments was potentiated by hyperpolarization, facilitated by depletion of intracellular Ca(2+) stores, unaffected by pharmacological manipulation of voltage-operated or cyclic nucleotide-gated Ca(2+) channels and suppressed by lanthanides, 2-APB, MRS 1845 and SKF 96365. However, cation influx through store-operated channels crossed the threshold for activation of voltage-operated Ca(2+) entry in a subset of cones, indicating that the operating range of inner segment signals is set by interactions between store- and voltage-operated Ca(2+) channels. Exposure to MRS 1845 resulted in approximately 40% reduction of light-evoked postsynaptic currents in photopic horizontal cells without affecting the light responses or voltage-operated Ca(2+) currents in simultaneously recorded cones. The spatial pattern of store-operated calcium entry in cones matched immunolocalization of the store-operated sensor STIM1. These findings show that store-operated channels regulate spatial and temporal properties of Ca(2+) homeostasis in vertebrate cones and demonstrate their role in generation of sustained excitatory signals across the first retinal synapse.http://europepmc.org/articles/PMC2725299?pdf=render
spellingShingle Tamas Szikra
Peter Barabas
Theodore M Bartoletti
Wei Huang
Abram Akopian
Wallace B Thoreson
David Krizaj
Calcium homeostasis and cone signaling are regulated by interactions between calcium stores and plasma membrane ion channels.
PLoS ONE
title Calcium homeostasis and cone signaling are regulated by interactions between calcium stores and plasma membrane ion channels.
title_full Calcium homeostasis and cone signaling are regulated by interactions between calcium stores and plasma membrane ion channels.
title_fullStr Calcium homeostasis and cone signaling are regulated by interactions between calcium stores and plasma membrane ion channels.
title_full_unstemmed Calcium homeostasis and cone signaling are regulated by interactions between calcium stores and plasma membrane ion channels.
title_short Calcium homeostasis and cone signaling are regulated by interactions between calcium stores and plasma membrane ion channels.
title_sort calcium homeostasis and cone signaling are regulated by interactions between calcium stores and plasma membrane ion channels
url http://europepmc.org/articles/PMC2725299?pdf=render
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