Ca2+ diffusion through endoplasmic reticulum supports elevated intraterminal Ca2+ levels needed to sustain synaptic release from rods in darkness

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Abstract

In addition to vesicle release at synaptic ribbons, rod photoreceptors are capable of substantial slow release at non-ribbon release sites triggered by Ca2+-induced Ca2+ release (CICR) from intracellular stores. To maintain CICR as rods remain depolarized in darkness, we hypothesized that Ca2+ released into the cytoplasm from terminal endoplasmic reticulum (ER) can be replenished continuously by ions diffusing within theERfrom the soma.Wemeasured [Ca2+] changes in cytoplasm andERof rods from Ambystoma tigrinum retina using various dyes. ER [Ca2+] changes were measured by loading ER with fluo-5N and then washing dye from the cytoplasm with a dye-free patch pipette solution. Small dye molecules diffused within ER between soma and terminal showing a single continuous ER compartment. Depolarization of rods to-40 mV depleted Ca2+ from terminal ER, followed by a decline in somatic ER [Ca2+]. Local activation of ryanodine receptors in terminals with a spatially confined puff of ryanodine caused a decline in terminal ER [Ca2+], followed by a secondary decrease in somatic ER. Localized photolytic uncaging of Ca2+ from o-nitrophenyl-EGTA in somatic ER caused an abrupt Ca2+ increase in somatic ER, followed by a slower Ca2+ increase in terminal ER. These data suggest that, during maintained depolarization, a soma-to-terminal [Ca2+] gradient develops within the ER that promotes diffusion of Ca2+ ions to resupply intraterminal ER Ca2+ stores and thus sustain CICR-mediated synaptic release. The ability of Ca2+ to move freely through the ER may also promote bidirectional communication of Ca2+ changes between soma and terminal.

Original languageEnglish (US)
Pages (from-to)11364-11373
Number of pages10
JournalJournal of Neuroscience
Volume35
Issue number32
DOIs
StatePublished - Aug 12 2015

Fingerprint

Darkness
Endoplasmic Reticulum
Carisoprodol
Coloring Agents
Cytoplasm
Ambystoma
Ions
Retinal Rod Photoreceptor Cells
Ryanodine
Ryanodine Receptor Calcium Release Channel
Aptitude
Retina

Keywords

  • Calcium imaging
  • Calcium-induced calcium release
  • Endoplasmic reticulum
  • Retina
  • Rod photoreceptors
  • Synaptic terminal

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

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title = "Ca2+ diffusion through endoplasmic reticulum supports elevated intraterminal Ca2+ levels needed to sustain synaptic release from rods in darkness",
abstract = "In addition to vesicle release at synaptic ribbons, rod photoreceptors are capable of substantial slow release at non-ribbon release sites triggered by Ca2+-induced Ca2+ release (CICR) from intracellular stores. To maintain CICR as rods remain depolarized in darkness, we hypothesized that Ca2+ released into the cytoplasm from terminal endoplasmic reticulum (ER) can be replenished continuously by ions diffusing within theERfrom the soma.Wemeasured [Ca2+] changes in cytoplasm andERof rods from Ambystoma tigrinum retina using various dyes. ER [Ca2+] changes were measured by loading ER with fluo-5N and then washing dye from the cytoplasm with a dye-free patch pipette solution. Small dye molecules diffused within ER between soma and terminal showing a single continuous ER compartment. Depolarization of rods to-40 mV depleted Ca2+ from terminal ER, followed by a decline in somatic ER [Ca2+]. Local activation of ryanodine receptors in terminals with a spatially confined puff of ryanodine caused a decline in terminal ER [Ca2+], followed by a secondary decrease in somatic ER. Localized photolytic uncaging of Ca2+ from o-nitrophenyl-EGTA in somatic ER caused an abrupt Ca2+ increase in somatic ER, followed by a slower Ca2+ increase in terminal ER. These data suggest that, during maintained depolarization, a soma-to-terminal [Ca2+] gradient develops within the ER that promotes diffusion of Ca2+ ions to resupply intraterminal ER Ca2+ stores and thus sustain CICR-mediated synaptic release. The ability of Ca2+ to move freely through the ER may also promote bidirectional communication of Ca2+ changes between soma and terminal.",
keywords = "Calcium imaging, Calcium-induced calcium release, Endoplasmic reticulum, Retina, Rod photoreceptors, Synaptic terminal",
author = "Minghui Chen and {Van Hook}, Matthew and Thoreson, {Wallace B}",
year = "2015",
month = "8",
day = "12",
doi = "10.1523/JNEUROSCI.0754-15.2015",
language = "English (US)",
volume = "35",
pages = "11364--11373",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "32",

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TY - JOUR

T1 - Ca2+ diffusion through endoplasmic reticulum supports elevated intraterminal Ca2+ levels needed to sustain synaptic release from rods in darkness

AU - Chen, Minghui

AU - Van Hook, Matthew

AU - Thoreson, Wallace B

PY - 2015/8/12

Y1 - 2015/8/12

N2 - In addition to vesicle release at synaptic ribbons, rod photoreceptors are capable of substantial slow release at non-ribbon release sites triggered by Ca2+-induced Ca2+ release (CICR) from intracellular stores. To maintain CICR as rods remain depolarized in darkness, we hypothesized that Ca2+ released into the cytoplasm from terminal endoplasmic reticulum (ER) can be replenished continuously by ions diffusing within theERfrom the soma.Wemeasured [Ca2+] changes in cytoplasm andERof rods from Ambystoma tigrinum retina using various dyes. ER [Ca2+] changes were measured by loading ER with fluo-5N and then washing dye from the cytoplasm with a dye-free patch pipette solution. Small dye molecules diffused within ER between soma and terminal showing a single continuous ER compartment. Depolarization of rods to-40 mV depleted Ca2+ from terminal ER, followed by a decline in somatic ER [Ca2+]. Local activation of ryanodine receptors in terminals with a spatially confined puff of ryanodine caused a decline in terminal ER [Ca2+], followed by a secondary decrease in somatic ER. Localized photolytic uncaging of Ca2+ from o-nitrophenyl-EGTA in somatic ER caused an abrupt Ca2+ increase in somatic ER, followed by a slower Ca2+ increase in terminal ER. These data suggest that, during maintained depolarization, a soma-to-terminal [Ca2+] gradient develops within the ER that promotes diffusion of Ca2+ ions to resupply intraterminal ER Ca2+ stores and thus sustain CICR-mediated synaptic release. The ability of Ca2+ to move freely through the ER may also promote bidirectional communication of Ca2+ changes between soma and terminal.

AB - In addition to vesicle release at synaptic ribbons, rod photoreceptors are capable of substantial slow release at non-ribbon release sites triggered by Ca2+-induced Ca2+ release (CICR) from intracellular stores. To maintain CICR as rods remain depolarized in darkness, we hypothesized that Ca2+ released into the cytoplasm from terminal endoplasmic reticulum (ER) can be replenished continuously by ions diffusing within theERfrom the soma.Wemeasured [Ca2+] changes in cytoplasm andERof rods from Ambystoma tigrinum retina using various dyes. ER [Ca2+] changes were measured by loading ER with fluo-5N and then washing dye from the cytoplasm with a dye-free patch pipette solution. Small dye molecules diffused within ER between soma and terminal showing a single continuous ER compartment. Depolarization of rods to-40 mV depleted Ca2+ from terminal ER, followed by a decline in somatic ER [Ca2+]. Local activation of ryanodine receptors in terminals with a spatially confined puff of ryanodine caused a decline in terminal ER [Ca2+], followed by a secondary decrease in somatic ER. Localized photolytic uncaging of Ca2+ from o-nitrophenyl-EGTA in somatic ER caused an abrupt Ca2+ increase in somatic ER, followed by a slower Ca2+ increase in terminal ER. These data suggest that, during maintained depolarization, a soma-to-terminal [Ca2+] gradient develops within the ER that promotes diffusion of Ca2+ ions to resupply intraterminal ER Ca2+ stores and thus sustain CICR-mediated synaptic release. The ability of Ca2+ to move freely through the ER may also promote bidirectional communication of Ca2+ changes between soma and terminal.

KW - Calcium imaging

KW - Calcium-induced calcium release

KW - Endoplasmic reticulum

KW - Retina

KW - Rod photoreceptors

KW - Synaptic terminal

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U2 - 10.1523/JNEUROSCI.0754-15.2015

DO - 10.1523/JNEUROSCI.0754-15.2015

M3 - Article

VL - 35

SP - 11364

EP - 11373

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 32

ER -