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

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Keywords

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

ASJC Scopus subject areas

  • Neuroscience(all)

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