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K_Ca channel insensitivity to Ca²⁺ sparks underlies fractional uncoupling in newborn cerebral artery smooth muscle cells

Department of Physiology, University of Tennessee Health Science Center, Memphis, Tennessee

Submitted 13 December 2005 ; accepted in final form 29 March 2006

In smooth muscle cells, localized intracellular Ca²⁺ transients, termed "Ca²⁺ sparks," activate several large-conductance Ca²⁺-activated K⁺ (K_Ca) channels, resulting in a transient K_Ca current. In some smooth muscle cell types, a significant proportion of Ca²⁺ sparks do not activate K_Ca channels. The goal of this study was to explore mechanisms that underlie fractional Ca²⁺ spark-K_Ca channel coupling. We investigated whether membrane depolarization or ryanodine-sensitive Ca²⁺ release (RyR) channel activation modulates coupling in newborn (1- to 3-day-old) porcine cerebral artery myocytes. At steady membrane potentials of –40, 0, and +40 mV, mean transient K_Ca current frequency was 0.18, 0.43, and 0.26 Hz and K_Ca channel activity [number of K_Ca channels activated by Ca²⁺ sparks x open probability of K_Ca channels at peak of Ca²⁺ sparks (NP_o)] at the transient K_Ca current peak was 4, 12, and 24, respectively. Depolarization between –40 and +40 mV increased K_Ca channel sensitivity to Ca²⁺ sparks and elevated the percentage of Ca²⁺ sparks that activated a transient K_Ca current from 59 to 86%. In a Ca²⁺-free bath solution or in diltiazem, a voltage-dependent Ca²⁺ channel blocker, steady membrane depolarization between –40 and +40 mV increased transient K_Ca current frequency up to 1.6-fold. In contrast, caffeine (10 µM), an RyR channel activator, increased mean transient K_Ca current frequency but did not alter Ca²⁺ spark-K_Ca channel coupling. These data indicate that coupling is increased by mechanisms that elevate K_Ca channel sensitivity to Ca²⁺ sparks, but not by RyR channel activation. Overall, K_Ca channel insensitivity to Ca²⁺ sparks is a prominent factor underlying fractional Ca²⁺ spark uncoupling in newborn cerebral artery myocytes.

ryanodine-sensitive calcium release channel; calcium-activated potassium channel; membrane potential

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