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Regulation of junctional and non-junctional sarcoplasmic reticulum calcium release in excitation-contraction coupling in cat atrial myocytes

Katherine A. Sheehan and Lothar A. Blatter

We have characterized the dependence on membrane potential (V_m) and calcium current (I_Ca) of calcium-induced calcium release (CICR) from the junctional-SR (j-SR, in the subsarcolemmal (SS) space) and non-junctional-SR (nj-SR, in the central (CT) region of the cell) of cat atrial myocytes using whole-cell voltage-clamp together with spatially resolved laser-scanning confocal microscopy. Subsarcolemmal and central [Ca²⁺]_i transient amplitudes and I_Ca had a bell-shaped dependence on V_m, but [Ca²⁺]_i reached a maximum at more negative V_m (-10 to 0 mV) than I_Ca (+10 mV). Termination of I_Ca after a brief depolarization (2.5 to 22.5 ms) immediately interrupted only the SS [Ca²⁺]_i transient, leaving the development of the CT [Ca²⁺]_i transient unaffected. Block of SR function with 20 µM ryanodine and 2 µM thapsigargin, revealed that > 90 % of the control [Ca²⁺]_i transient amplitude was attributable to active SR Ca²⁺ release through ryanodine receptors (RyRs). The gain of SR Ca²⁺ release was highest in the SS space at negative test potentials and was less pronounced in the CT region. Inhibition of Na⁺-Ca²⁺ exchange resulted in prolonged and higher amplitude [Ca²⁺]_i transients, elevated resting [Ca²⁺]_i, accelerated propagation of CICR, decreased extrusion of Ca²⁺ and an increase in j-SR Ca²⁺ load. Increasing the cytosolic Ca²⁺ buffer capacity by internal perfusion with 1 mM EGTA limited SR Ca²⁺ release to the SS region, indicating that Ca²⁺ release from nj-SR is initiated by diffusion of Ca²⁺ from the cell periphery and propagating CICR. Junctional-SR Ca²⁺ release occurred at discrete sites whose order of activation and amplitude of release varied from beat to beat. In conclusion, during normal excitation-contraction coupling in cat atrial myocytes, only Ca²⁺ release from the j-SR is directly activated by Ca²⁺ entering via I_Ca. Elevation of SS [Ca²⁺]_i is required to provide the cytosolic Ca²⁺ gradient needed to initiate regenerative and propagating CICR from nj-SR.

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