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Am J Physiol Cell Physiol 287: C1577-C1588, 2004. First published August 11, 2004; doi:10.1152/ajpcell.00153.2004
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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

Ronghua ZhuGe,1,2 Kevin E. Fogarty,1,2 Stephen P. Baker,3 John G. McCarron,4 Richard A. Tuft,1,2 Lawrence M. Lifshitz,1,2 and John V. Walsh, Jr.2

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 [ICa(spark)]. The variance between spark sites was significantly greater than the intrasite variance for the following parameters: Ca2+ signal mass, ICa(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


Address for reprint requests and other correspondence: J. V. Walsh, Jr., Dept. of Physiology, Univ. of Massachusetts Medical Center, 55 Lake Ave. North, Worcester, MA 01655 (E-mail: john.walsh{at}umassmed.edu)




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