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 J.
AU - Thoreson, Wallace B.
N1 - Publisher Copyright:
© 2015 the authors.
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
C2 - 26269643
AN - SCOPUS:84939176326
SN - 0270-6474
VL - 35
SP - 11364
EP - 11373
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 32
ER -