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Ca²⁺ current-gated focal and local Ca²⁺ release in rat atrial myocytes: evidence from rapid 2-D confocal imaging

Sun-Hee Woo, Lars Cleemann and Martin Morad

In atrial myocytes immunocytochemistry has shown two groups of ryanodine receptors (RyRs): those at the periphery colocalized with dihydropyridine receptors (DHPRs) and those at the cell interior not associated with DHPRs. The extent to which the two sets of RyRs are controlled by Ca²⁺ current (I_Ca) or Ca²⁺ diffusion remains to be determined. Here, using rapid (240 Hz) two-dimensional confocal Ca²⁺ imaging in rat atrial myocytes, we examine directly the role of I_Ca on the two-dimensional patterns of local and focal Ca²⁺ releases. I_Ca evoked peripheral Ca²⁺ release within 1-4 ms, causing a rapid monophasic local rise of Ca²⁺, which then propagated into the cell interior along sarcomeric lines (~2 µm) with a velocity of ~230 µm s^-1, even though we found no evidence for organized t-tubules using di-8-ANEPPS staining. I_Ca-triggered Ca²⁺ release in the cell centre, on the other hand, had both a rapid (12 ms) and slower delayed components (12-50 ms). The voltage dependence of peripheral Ca²⁺ release and the two components of central release was bell shaped, and the magnitude of each release component was linearly related to I_Ca. Premature termination (2-10 ms) of I_Ca was equally effective in abbreviating both the peripheral and slow central Ca²⁺ release. High concentration of Ca²⁺ buffers (2-5 mM EGTA plus 1 mM fluo-3) completely abolished the I_Ca-gated propagation wave and the slow delayed component of Ca²⁺ release, but had little or no effect on the rapid component of central release. The efficacy of I_Ca to trigger Ca²⁺ release in periphery of the myocyte was ~5 times higher than in the centre, consistent with the smaller measured central Ca²⁺ release. The quantification of central Ca²⁺ release as a function of peripheral release suggests a cooperative gating mechanism(s) for central release. These findings indicate that both I_Ca and diffusion of Ca²⁺ from the peripheral sites contribute to the gating of Ca²⁺ release from central SR. How in fact the I_Ca-dependent fast component of central release is activated remains to be determined.

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