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Ca²⁺ images and K⁺ current during depolarization in smooth muscle cells of the guinea-pig vas deferens and urinary bladder

Yuji Imaizumi, Yuichi Torii *, Yoshiaki Ohi, Norihiro Nagano *, Kaoru Atsuki *, Hisao Yamamura, Katsuhiko Muraki *, Minoru Watanabe * and Thomas B. Bolton ¹

1. Electrical events and intracellular calcium concentration ([Ca²⁺]) imaged using fluo-3 and laser scanning confocal microscopy were simultaneously monitored in single smooth muscle cells freshly isolated from guinea-pig vas deferens or urinary bladder.

2. Images obtained every 8 ms, during stepping from -60 to 0 or +10 mV for 50 ms under voltage clamp, showed that a rise in [Ca²⁺] could be detected within 20 ms of depolarization in five to twenty small (< 2 µm diameter) 'hot spots', over 95 % of which were located within 1·5 µm of the cell membrane. Depolarization at 30 s intervals activated hot spots at the same places.

3. Cd²⁺ or verapamil abolished both hot spots and Ca²⁺-activated K⁺ current (I_K,Ca). Caffeine almost abolished hot spots and markedly reduced I_K,Ca. Cyclopiazonic acid, which raised basal global [Ca²⁺], decreased the rise in hot spot [Ca²⁺] and I_K,Ca amplitude during depolarization. These results suggest that Ca²⁺ entry caused Ca²⁺-induced Ca²⁺ release (CICR).

4. Under voltage clamp, hot spot [Ca²⁺] closely paralleled the rise in I_K,Ca and reached a peak within 20 ms of the start of depolarization, but the rise in global [Ca²⁺] over the whole cell area was much slower. Step depolarization to potentials positive to -20 mV caused hot spots to grow in size and coalesce, leading to a rise in global [Ca²⁺] and contraction. Ca²⁺ hot spots also occurred during the up-stroke of an evoked action potential under current clamp.

5. It is concluded that the entry of Ca²⁺ in the early stages of an action potential evokes CICR from discrete subplasmalemma Ca²⁺ storage sites and generates hot spots that spread to initiate a contraction. The activation of Ca²⁺-dependent K⁺ channels in the plasmalemma over hot spots initiates I_K,Ca and action potential repolarization.

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