Ca2+-induced Ca2+ Release in Chromaffin Cells Seen from inside the ER with Targeted Aequorin

doi:10.1083/jcb.144.2.241

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© The Rockefeller University Press, 0021-9525/1999//241 $5.00
The Journal of Cell Biology, Volume 144, Number 2, , 1999 241-254

Regular Articles

Ca²⁺-induced Ca²⁺ Release in Chromaffin Cells Seen from inside the ER with Targeted Aequorin

Maria Teresa Alonso^*, Maria José Barrero^*, Pedro Michelena, Estela Carnicero^*, Inmaculada Cuchillo, Antonio G. García, Javier García-Sancho^*, Mayte Montero^*, and Javier Alvarez^*

^* Instituto de Biología y Genética Molecular, Departamento de Bioquímica y Biología Molecular y Fisiología, Facultad de Medicina, Universidad de Valladolid y Consejo Superior de Investigaciones Científicas, E-47005 Valladolid, Spain; and Instituto de Farmacología Teófilo Hernando, Departamento de Farmacología y Terapéutica, Facultad de Medicina, Universidad Autónoma de Madrid, E-28029 Madrid, Spain

The presence and physiological role of Ca²⁺-induced Ca²⁺ release(CICR) in nonmuscle excitable cells has been investigated onlyindirectly through measurements of cytosolic [Ca²⁺] ([Ca²⁺]_c).Using targeted aequorin, we have directly monitored [Ca²⁺]changes inside the ER ([Ca²⁺]_ER) in bovine adrenal chromaffin cells. Ca²⁺ entry induced by cell depolarization triggereda transient Ca²⁺ release from the ER that was highly dependenton [Ca²⁺]_ER and sensitized by low concentrations of caffeine.Caffeine-induced Ca²⁺ release was quantal in nature due to modulationby [Ca²⁺]_ER. Whereas caffeine released essentially all the Ca²⁺ from the ER, inositol 1,4,5-trisphosphate (InsP₃)- producingagonists released only 60–80%. Both InsP₃ and caffeineemptied completely the ER in digitonin-permeabilized cells whereascyclic ADP-ribose had no effect. Ryanodine induced permanentemptying of the Ca²⁺ stores in a use-dependent manner afteractivation by caffeine. Fast confocal [Ca²⁺]_c measurements showed that the wave of [Ca²⁺]_c induced by 100-ms depolarizingpulses in voltage-clamped cells was delayed and reduced inintensity in ryanodine-treated cells. Our results indicatethat the ER of chromaffin cells behaves mostly as a singlehomogeneous thapsigargin-sensitive Ca²⁺ pool that can releaseCa²⁺ both via InsP₃ receptors or CICR.

Key Words: endoplasmic reticulum • aequorin • chromaffin cells • calcium • ryanodine

Abbreviations used in this paper: [Ca²⁺]_c, cytosolic [Ca²⁺]; [Ca²⁺]_ER, ER [Ca²⁺]; BAPTA, 1,2-bis(2-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid; cADPR, cyclic adenosine diphosphate ribose; CICR, Ca²⁺-induced Ca²⁺ release; CPA, ciclopiazonic acid; DMPP, 1,1-dimethyl-4-phenyl- piperazinium iodide; HSV-1, herpes simplex virus type 1; InsP₃R, InsP₃ receptor; InsP₃, inositol 1,4,5-trisphosphate; ivu, infectious virus units; RyR, ryanodine receptor.

M.J. Barrero was supported by a predoctoral fellowship fromthe University of Valladolid and I. Cuchillo is a fellow fromthe Fundación Teófilo Hernando. Financial supportfrom Fondo de Investigaciones Sanitarias to J. Alvarez (96/0456)and to M.T. Alonso (96/1443), Junta de Castilla y Leónto J. García-Sancho (VA 87/96), Dirección Generalde Enseñanza Superior (PB97/0474) to J. García-Sanchoand Dirección General de Investigación Científicay Técnica (PB94/0150) to A.G. García is gratefully acknowledged.

M.T. Alonso and M.J. Barrero contributed equally to this work.

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