Intracellular calcium stores drive slow non-ribbon vesicle release from rod photoreceptors

Rods are capable of greater slow release than cones contributing to overall slower release kinetics. Slow release in rods involves Ca2+-induced Ca2+ release (CICR). By impairing release from ribbons, we found that unlike cones where release occurs entirely at ribbon-style active zones, slow release...

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Main Authors: Minghui eChen, David eKrizaj, Wallace B Thoreson
Format: Article
Language:English
Published: Frontiers Media S.A. 2014-02-01
Series:Frontiers in Cellular Neuroscience
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fncel.2014.00020/full
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author Minghui eChen
David eKrizaj
Wallace B Thoreson
author_facet Minghui eChen
David eKrizaj
Wallace B Thoreson
author_sort Minghui eChen
collection DOAJ
description Rods are capable of greater slow release than cones contributing to overall slower release kinetics. Slow release in rods involves Ca2+-induced Ca2+ release (CICR). By impairing release from ribbons, we found that unlike cones where release occurs entirely at ribbon-style active zones, slow release from rods occurs mostly at ectopic, non-ribbon sites. To investigate the role of CICR in ribbon and non-ribbon release from rods, we used total internal reflection fluorescence microscopy (TIRFM) as a tool for visualizing terminals of isolated rods loaded with fluorescent Ca2+ indicator dyes and synaptic vesicles loaded with dextran-conjugated pH-sensitive rhodamine (pHrodo). We found that rather than simply facilitating release, activation of CICR by ryanodine triggered release directly in rods, independent of plasma membrane Ca2+ channel activation. Ryanodine-evoked release occurred mostly at non-ribbon sites and release evoked by sustained depolarization at non-ribbon sites was mostly due to CICR. Unlike release at ribbon-style active zones, non-ribbon release did not occur at fixed locations. Fluorescence recovery after photobleaching of endoplasmic reticulum (ER)-tracker dye in rod terminals showed that ER extends continuously from synapse to soma. Release of Ca2+ from terminal ER by lengthy depolarization did not significantly deplete Ca2+ from ER in the perikaryon. Collectively, these results indicate that CICR-triggered release at non-ribbon sites is a major mechanism for maintaining vesicle release from rods and that CICR in terminals may be sustained by diffusion of Ca2+ through ER from other parts of the cell.
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spelling doaj.art-521cd0436b6d455c9b0436589f11e1272022-12-22T03:32:48ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022014-02-01810.3389/fncel.2014.0002076497Intracellular calcium stores drive slow non-ribbon vesicle release from rod photoreceptorsMinghui eChen0David eKrizaj1Wallace B Thoreson2University of Nebraska Medical CenterUniversity of UtahUniversity of Nebraska Medical CenterRods are capable of greater slow release than cones contributing to overall slower release kinetics. Slow release in rods involves Ca2+-induced Ca2+ release (CICR). By impairing release from ribbons, we found that unlike cones where release occurs entirely at ribbon-style active zones, slow release from rods occurs mostly at ectopic, non-ribbon sites. To investigate the role of CICR in ribbon and non-ribbon release from rods, we used total internal reflection fluorescence microscopy (TIRFM) as a tool for visualizing terminals of isolated rods loaded with fluorescent Ca2+ indicator dyes and synaptic vesicles loaded with dextran-conjugated pH-sensitive rhodamine (pHrodo). We found that rather than simply facilitating release, activation of CICR by ryanodine triggered release directly in rods, independent of plasma membrane Ca2+ channel activation. Ryanodine-evoked release occurred mostly at non-ribbon sites and release evoked by sustained depolarization at non-ribbon sites was mostly due to CICR. Unlike release at ribbon-style active zones, non-ribbon release did not occur at fixed locations. Fluorescence recovery after photobleaching of endoplasmic reticulum (ER)-tracker dye in rod terminals showed that ER extends continuously from synapse to soma. Release of Ca2+ from terminal ER by lengthy depolarization did not significantly deplete Ca2+ from ER in the perikaryon. Collectively, these results indicate that CICR-triggered release at non-ribbon sites is a major mechanism for maintaining vesicle release from rods and that CICR in terminals may be sustained by diffusion of Ca2+ through ER from other parts of the cell.http://journal.frontiersin.org/Journal/10.3389/fncel.2014.00020/fullExocytosisRetinaryanodine receptorsribbon synapsesynaptic vesicleTotal Internal Reflection Fluorescence microscopy
spellingShingle Minghui eChen
David eKrizaj
Wallace B Thoreson
Intracellular calcium stores drive slow non-ribbon vesicle release from rod photoreceptors
Frontiers in Cellular Neuroscience
Exocytosis
Retina
ryanodine receptors
ribbon synapse
synaptic vesicle
Total Internal Reflection Fluorescence microscopy
title Intracellular calcium stores drive slow non-ribbon vesicle release from rod photoreceptors
title_full Intracellular calcium stores drive slow non-ribbon vesicle release from rod photoreceptors
title_fullStr Intracellular calcium stores drive slow non-ribbon vesicle release from rod photoreceptors
title_full_unstemmed Intracellular calcium stores drive slow non-ribbon vesicle release from rod photoreceptors
title_short Intracellular calcium stores drive slow non-ribbon vesicle release from rod photoreceptors
title_sort intracellular calcium stores drive slow non ribbon vesicle release from rod photoreceptors
topic Exocytosis
Retina
ryanodine receptors
ribbon synapse
synaptic vesicle
Total Internal Reflection Fluorescence microscopy
url http://journal.frontiersin.org/Journal/10.3389/fncel.2014.00020/full
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AT davidekrizaj intracellularcalciumstoresdriveslownonribbonvesiclereleasefromrodphotoreceptors
AT wallacebthoreson intracellularcalciumstoresdriveslownonribbonvesiclereleasefromrodphotoreceptors