Synchronous Ca2+ oscillation emerges from voltage fluctuations of Ca2+ stores


M. Yamashita, Department of Physiology I, Nara Medical University, Shijo-cho 840, Kashihara 634-8521, Japan
Fax: +81 744 29 0306
Tel: +81 744 29 8827


Synchronous Ca2+ oscillation occurs in various cell types to regulate cellular functions. However, the mechanism for synchronization of Ca2+ increases between cells remains unclear. Recently, synchronous oscillatory changes in the membrane potential of internal Ca2+ stores were recorded using an organelle-specific voltage-sensitive dye [Yamashita et al. (2006) FEBS J273, 3585–3597], and an electrical coupling model of the synchronization of store potentials and Ca2+ releases has been proposed [Yamashita (2006) FEBS Lett580, 4979–4983]. This model is based on capacitative coupling, by which transient voltage changes can be synchronized, but oscillatory slow potentials cannot be communicated. Another candidate mechanism is synchronization of action potentials and ensuing Ca2+ influx through voltage-dependent Ca channels. The present study addresses the question of whether Ca2+ increases are synchronized by action potentials, and how oscillatory store potentials are synchronized across the cells. Electrophysiological and Ca2+-sensitive fluorescence measurements in early embryonic chick retina showed that synchronous Ca2+ oscillation was caused by releases of Ca2+ from Ca2+ stores without any evidence of action potentials in retinal neuroepithelial cells or newborn neurons. High-speed fluorescence measurement of store membrane potential surprisingly revealed that the synchronous oscillatory changes in the store potential were periodic repeats of a burst of high-frequency voltage fluctuations. The burst coincided with a Ca2+ increase. The present study suggests that synchronization of Ca2+ release is mediated by the high-frequency fluctuation in the store potential. Close apposition of the store membrane and plasma membrane in an epithelial structure would allow capacitative coupling across the cells.