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

Minghui Chen, David Križaj, Wallace B Thoreson

Research output: Contribution to journalArticle

16 Citations (Scopus)

Abstract

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 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. 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.

Original languageEnglish (US)
Article number20
JournalFrontiers in Cellular Neuroscience
Volume8
Issue numberFEB
DOIs
StatePublished - Feb 3 2014

Fingerprint

Retinal Rod Photoreceptor Cells
Endoplasmic Reticulum
Calcium
Ryanodine
Coloring Agents
Fluorescence Recovery After Photobleaching
Rhodamines
Synaptic Vesicles
Carisoprodol
Dextrans
Ion Channels
Fluorescence Microscopy
Synapses
Cell Membrane

Keywords

  • Calcium-induced calcium release
  • Exocytosis
  • Retina
  • Ribbon synapse
  • Ryanodine receptors
  • Synaptic vesicle
  • Total internal reflection fluorescence microscopy

ASJC Scopus subject areas

  • Cellular and Molecular Neuroscience

Cite this

Intracellular calcium stores drive slow non-ribbon vesicle release from rod photoreceptors. / Chen, Minghui; Križaj, David; Thoreson, Wallace B.

In: Frontiers in Cellular Neuroscience, Vol. 8, No. FEB, 20, 03.02.2014.

Research output: Contribution to journalArticle

@article{0ad8edf0b67e45469c7dca70cf0d3321,
title = "Intracellular calcium stores drive slow non-ribbon vesicle release from rod photoreceptors",
abstract = "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 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. 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.",
keywords = "Calcium-induced calcium release, Exocytosis, Retina, Ribbon synapse, Ryanodine receptors, Synaptic vesicle, Total internal reflection fluorescence microscopy",
author = "Minghui Chen and David Križaj and Thoreson, {Wallace B}",
year = "2014",
month = "2",
day = "3",
doi = "10.3389/fncel.2014.00020",
language = "English (US)",
volume = "8",
journal = "Frontiers in Cellular Neuroscience",
issn = "1662-5102",
publisher = "Frontiers Research Foundation",
number = "FEB",

}

TY - JOUR

T1 - Intracellular calcium stores drive slow non-ribbon vesicle release from rod photoreceptors

AU - Chen, Minghui

AU - Križaj, David

AU - Thoreson, Wallace B

PY - 2014/2/3

Y1 - 2014/2/3

N2 - 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 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. 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.

AB - 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 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. 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.

KW - Calcium-induced calcium release

KW - Exocytosis

KW - Retina

KW - Ribbon synapse

KW - Ryanodine receptors

KW - Synaptic vesicle

KW - Total internal reflection fluorescence microscopy

UR - http://www.scopus.com/inward/record.url?scp=84893218450&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84893218450&partnerID=8YFLogxK

U2 - 10.3389/fncel.2014.00020

DO - 10.3389/fncel.2014.00020

M3 - Article

C2 - 24550779

AN - SCOPUS:84893218450

VL - 8

JO - Frontiers in Cellular Neuroscience

JF - Frontiers in Cellular Neuroscience

SN - 1662-5102

IS - FEB

M1 - 20

ER -