ATP-sensitive voltage- and calcium-dependent chloride channels in sarcoplasmic reticulum vesicles from rabbit skeletal muscle |
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Authors: | J I Kourie |
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Institution: | (1) Muscle Research Group, Division of Neuroscience, John Curtin School of Medical Research, ANU, PO Box 334, Canberra City, ACT, 2601 Australia, AU |
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Abstract: | Chloride channels in the sarcoplasmic reticulum (SR) are thought to play an essential role in excitation-contraction (E-C)
coupling by balancing charge movement during calcium release and uptake. In this study the nucleotide-sensitivity of Cl− channels in the SR from rabbit skeletal muscle was investigated using the lipid bilayer technique. Two distinct ATP-sensitive
Cl− channels that differ in their conductance and kinetic properties and in the mechanism of ATP-induced channel inhibition were
observed. The first, a nonfrequent 150 pS channel was inhibited by trans (luminal) ATP, and the second, a common 75 pS small chloride (SCl) channel was inhibited by cis (cytoplasmic) ATP. In the case of the SCl channel the ATP-induced reversible decline in the values of current (maximal current
amplitude, I
max and integral current, I′) and kinetic parameters (frequency of opening F
O
, probability of the channel being open P
O
, mean open T
O
and closed T
c
times) show a nonspecific block of the voltage- and Ca2+-dependent SCl channel. ATP was a more potent blocker from the cytoplasmic side than from the luminal side of the channel.
The SCl channel block was not due to Ca2+ chelation by ATP, nor to phosphorylation of the channel protein. The inhibitory action of ATP was mimicked by the nonhydrolyzable
analogue adenylylimidodiphosphate (AMP-PNP) in the absence of Mg2+. The inhibitory potency of the adenine nucleotides was charge dependent in the following order ATP4− > ADP3− > > > AMP2−. The data suggest that ATP-induced effects are mediated via an open channel block mechanism. Modulation of the SCl channel
by ATP]
cis
and Ca2+]
cis
indicates that (i) this channel senses the bioenergetic state of the muscle fiber and (ii) it is linked to the ATP-dependent
cycling of the Ca2+ between the SR and the sarcoplasm.
Received: 4 September 1996/Revised: 6 December 1996 |
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Keywords: | : ATP-sensitive — Chloride channel — Sarcoplasmic reticulum — Skeletal muscle — Counter-ion channel |
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