Coexpression of the β1 subunit with the α subunit (mSlo) of BK channels increases the apparent Ca2+ sensitivity of the channel. This study investigates whether the mechanism underlying the increased Ca2+ sensitivity requires Ca2+, by comparing the gating in 0 Ca2+i of BK channels composed of α subunits to those composed of α+β1 subunits. The β1 subunit increased burst duration ∼20-fold and the duration of gaps between bursts ∼3-fold, giving an ∼10-fold increase in open probability (Po) in 0 Ca2+i. The effect of the β1 subunit on increasing burst duration was little changed over a wide range of Po achieved by varying either Ca2+i or depolarization. The effect of the β1 subunit on increasing the durations of the gaps between bursts in 0 Ca2+i was preserved over a range of voltage, but was switched off as Ca2+i was increased into the activation range. The Ca2+-independent, β1 subunit-induced increase in burst duration accounted for 80% of the leftward shift in the Po vs. Ca2+i curve that reflects the increased Ca2+ sensitivity induced by the β1 subunit. The Ca2+-dependent effect of the β1 subunit on the gaps between bursts accounted for the remaining 20% of the leftward shift. Our observation that the major effects of the β1 subunit are independent of Ca2+i suggests that the β1 subunit mainly alters the energy barriers of Ca2+-independent transitions. The changes in gating induced by the β1 subunit differ from those induced by depolarization, as increasing Po by depolarization or by the β1 subunit gave different gating kinetics. The complex gating kinetics for both α and α+β1 channels in 0 Ca2+i arise from transitions among two to three open and three to five closed states and are inconsistent with Monod-Wyman-Changeux type models, which predict gating among only one open and one closed state in 0 Ca2+i.
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1 June 2000
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June 01 2000
Functional Coupling of the β1 Subunit to the Large Conductance Ca2+-Activated K+ Channel in the Absence of Ca2+ : Increased Ca2+ Sensitivity from a Ca2+-Independent Mechanism
Crina M. Nimigean,
Crina M. Nimigean
aDepartment of Physiology and Biophysics, University of Miami School of Medicine, Miami, Florida 33101-6430
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Karl L. Magleby
Karl L. Magleby
aDepartment of Physiology and Biophysics, University of Miami School of Medicine, Miami, Florida 33101-6430
Search for other works by this author on:
Crina M. Nimigean
aDepartment of Physiology and Biophysics, University of Miami School of Medicine, Miami, Florida 33101-6430
Karl L. Magleby
aDepartment of Physiology and Biophysics, University of Miami School of Medicine, Miami, Florida 33101-6430
Portions of this work were previously published in abstract form (Nimigean, C.M., and K.L. Magleby. 2000. Biophys. J. 78:91A; and Nimigean, C.M., B.L. Moss, and K.L. Magleby. 1999. Soc. Neurosci. Abstr. 25:985).
Abbreviations used in this paper: BK channel, large conductance Ca2+-activated K+ channel; GFP, green fluorescent protein; HEK cells, human embryonic kidney cells; MWC, Monod-Wyman-Changeux.
Received:
February 07 2000
Revision Requested:
April 12 2000
Accepted:
April 13 2000
Online ISSN: 1540-7748
Print ISSN: 0022-1295
© 2000 The Rockefeller University Press
2000
The Rockefeller University Press
J Gen Physiol (2000) 115 (6): 719–736.
Article history
Received:
February 07 2000
Revision Requested:
April 12 2000
Accepted:
April 13 2000
Citation
Crina M. Nimigean, Karl L. Magleby; Functional Coupling of the β1 Subunit to the Large Conductance Ca2+-Activated K+ Channel in the Absence of Ca2+ : Increased Ca2+ Sensitivity from a Ca2+-Independent Mechanism . J Gen Physiol 1 June 2000; 115 (6): 719–736. doi: https://doi.org/10.1085/jgp.115.6.719
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