Ca2+ sparks are small, localized cytosolic Ca2+ transients due to Ca2+ release from sarcoplasmic reticulum through ryanodine receptors. In smooth muscle, Ca2+ sparks activate large conductance Ca2+-activated K+ channels (BK channels) in the spark microdomain, thus generating spontaneous transient outward currents (STOCs). The purpose of the present study is to determine experimentally the level of Ca2+ to which the BK channels are exposed during a spark. Using tight seal, whole-cell recording, we have analyzed the voltage-dependence of the STOC conductance (g(STOC)), and compared it to the voltage-dependence of BK channel activation in excised patches in the presence of different [Ca2+]s. The Ca2+ sparks did not change in amplitude over the range of potentials of interest. In contrast, the magnitude of g(STOC) remained roughly constant from 20 to −40 mV and then declined steeply at more negative potentials. From this and the voltage dependence of BK channel activation, we conclude that the BK channels underlying STOCs are exposed to a mean [Ca2+] on the order of 10 μM during a Ca2+ spark. The membrane area over which a concentration ≥10 μM is reached has an estimated radius of 150–300 nm, corresponding to an area which is a fraction of one square micron. Moreover, given the constraints imposed by the estimated channel density and the Ca2+ current during a spark, the BK channels do not appear to be uniformly distributed over the membrane but instead are found at higher density at the spark site.
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1 July 2002
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June 10 2002
Spontaneous Transient Outward Currents Arise from Microdomains Where BK Channels Are Exposed to a Mean Ca2+ Concentration on the Order of 10 μM during a Ca2+ Spark
Ronghua ZhuGe,
Ronghua ZhuGe
Biomedical Imaging Group, Department of Physiology, University of Massachusetts Medical School, Worcester, MA 01655
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Kevin E. Fogarty,
Kevin E. Fogarty
Biomedical Imaging Group, Department of Physiology, University of Massachusetts Medical School, Worcester, MA 01655
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Richard A. Tuft,
Richard A. Tuft
Biomedical Imaging Group, Department of Physiology, University of Massachusetts Medical School, Worcester, MA 01655
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John V. Walsh, Jr
John V. Walsh, Jr
Biomedical Imaging Group, Department of Physiology, University of Massachusetts Medical School, Worcester, MA 01655
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Ronghua ZhuGe
Biomedical Imaging Group, Department of Physiology, University of Massachusetts Medical School, Worcester, MA 01655
Kevin E. Fogarty
Biomedical Imaging Group, Department of Physiology, University of Massachusetts Medical School, Worcester, MA 01655
Richard A. Tuft
Biomedical Imaging Group, Department of Physiology, University of Massachusetts Medical School, Worcester, MA 01655
John V. Walsh, Jr
Biomedical Imaging Group, Department of Physiology, University of Massachusetts Medical School, Worcester, MA 01655
Address correspondence to John V. Walsh, Jr, Department of Physiology, University of Massachusetts Medical Center, Worcester, MA 01655. Fax: (508) 856-5997; E-mail: [email protected]
*
Abbreviations used in this paper: RyR, ryanodine receptor; SR, sarcoplasmic reticulum; STOC, spontaneous transient outward current.
Received:
January 31 2002
Revision Received:
April 12 2002
Accepted:
May 06 2002
Online ISSN: 1540-7748
Print ISSN: 0022-1295
The Rockefeller University Press
2002
J Gen Physiol (2002) 120 (1): 15–27.
Article history
Received:
January 31 2002
Revision Received:
April 12 2002
Accepted:
May 06 2002
Citation
Ronghua ZhuGe, Kevin E. Fogarty, Richard A. Tuft, John V. Walsh; Spontaneous Transient Outward Currents Arise from Microdomains Where BK Channels Are Exposed to a Mean Ca2+ Concentration on the Order of 10 μM during a Ca2+ Spark . J Gen Physiol 1 July 2002; 120 (1): 15–27. doi: https://doi.org/10.1085/jgp.20028571
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