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Single channel properties of Ca(2+)-activated K(+) (BK or Maxi-K) channels have been investigated in presynaptic membranes in Xenopus motoneurone-muscle cell cultures. The occurrence and density of BK channels increased with maturation/synaptogenesis and was not uniform: highest at the release face of bouton-like synaptic varicosities in contact with muscle cells, and lowest in varicosities that did not contact muscle cells. The Ca(2+) affinity of the channel (K(d)= 7.7 microM at a membrane potential of +20 mV) was lower than those of BK channels that have been characterized in other terminals. Hill coefficients varied between 1.5 and 2.8 at different potentials and open probability increased e-fold per 16 mV change in membrane potential over a range of [Ca(2+)](i) from 1 microM to 1 mM. The maximal activation rate of ensembled single BK channel currents was in the submillisecond range at > or =+20 mV. The activation rate increased approximately 10-fold in response to a [Ca(2+)](i) increase from 1 to 100 microM, but increased only approximately 2-fold with a voltage change from +20 to +130 mV. The fastest activation kinetics of BK channels in cell-attached patches resembled that in inside-out patches with [Ca(2+)](i) of 100 microM or more, suggesting that many BK channels are located very close to calcium channels. Given the low Ca(2+) affinity and rapid Ca(2+) binding/unbinding properties, we conclude that BK channels in this preparation are adapted to play an important role in regulation of neurotransmitter release, and they are ideal reporters of local [Ca(2+)] at the inner membrane surface.
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