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MEMBRANE TRANSPORTERS, ION CHANNELS, AND PUMPS

Ca²⁺ spark sites in smooth muscle cells are numerous and differ in number of ryanodine receptors, large-conductance K⁺ channels, and coupling ratio between them

¹Biomedical Imaging Group, ²Department of Physiology, and ³Department of Information Services, University of Massachusetts Medical School, Worcester, Massachusetts 01655; and ⁴Neuroscience and Biomedical Systems, Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow G12 8QQ, United Kingdom

Submitted 19 March 2004 ; accepted in final form 27 July 2004

Ca²⁺ sparks are highly localized Ca²⁺ transients caused by Ca²⁺ release from sarcoplasmic reticulum through ryanodine receptors (RyR). In smooth muscle, Ca²⁺ sparks activate nearby large-conductance, Ca²⁺-sensitive K⁺ (BK) channels to generate spontaneous transient outward currents (STOC). The properties of individual sites that give rise to Ca²⁺ sparks have not been examined systematically. We have characterized individual sites in amphibian gastric smooth muscle cells with simultaneous high-speed imaging of Ca²⁺ sparks using wide-field digital microscopy and patch-clamp recording of STOC in whole cell mode. We used a signal mass approach to measure the total Ca²⁺ released at a site and to estimate the Ca²⁺ current flowing through RyR [I_Ca(spark)]. The variance between spark sites was significantly greater than the intrasite variance for the following parameters: Ca²⁺ signal mass, I_Ca(spark), STOC amplitude, and 5-ms isochronic STOC amplitude. Sites that failed to generate STOC did so consistently, while those at the remaining sites generated STOC without failure, allowing the sites to be divided into STOC-generating and STOC-less sites. We also determined the average number of spark sites, which was 42/cell at a minimum and more likely on the order of at least 400/cell. We conclude that 1) spark sites differ in the number of RyR, BK channels, and coupling ratio of RyR-BK channels, and 2) there are numerous Ca²⁺ spark-generating sites in smooth muscle cells. The implications of these findings for the organization of the spark microdomain are explored.

wide-field imaging; spontaneous transient outward current; microdomain

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