Permeant Anions Control Gating of Calcium-dependent Chloride Channels

Permeant Anions Control Gating of Calcium-dependent Chloride Channels The effects of external anions (SCN−, NO 3 − , I−, Br−, F−, glutamate, and aspartate) on gating of Ca2+-dependent Cl− channels from rat parotid acinar cells were studied using the whole-cell configuration of the patch-clamp technique. Shifts in the reversal potential of the current induced by replacement of external Cl− with foreign anions, gave the following selectivity sequence based on permeability ratios (P x/P Cl): SCN−>I−>NO 3 − >Br−>Cl−>F−>aspartate>glutamate. Using a continuum electrostatic model we calculated that this lyotropic sequence resulted from the interaction between anions and a polarizable tunnel with an effective dielectric constant of ∼23. Our data revealed that anions with P x/PCl > 1 accelerated activation kinetics in a voltage-independent manner and slowed deactivation kinetics. Moreover, permeant anions enhanced whole-cell conductance (g, an index of the apparent open probability) in a voltage-dependent manner, and shifted leftward the membrane potential-g curves. All of these effects were produced by the anions with an effectiveness that followed the selectivity sequence. To explain the effects of permeant anions on activation kinetics and g Cl we propose that there are 2 different anion-binding sites in the channel. One site is located outside the electrical field and controls channel activation kinetics, while a second site is located within the pore and controls whole-cell conductance. Thus, interactions of permeant anions with these two sites hinder the closing mechanism and stabilize the channel in the open state. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png The Journal of Membrane Biology Springer Journals

Permeant Anions Control Gating of Calcium-dependent Chloride Channels

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Publisher
Springer Journals
Copyright
Copyright © 2004 by Springer-Verlag
Subject
Life Sciences; Human Physiology; Biochemistry, general
ISSN
0022-2631
eISSN
1432-1424
DOI
10.1007/s00232-004-0659-x
pmid
15216414
Publisher site
See Article on Publisher Site

Abstract

The effects of external anions (SCN−, NO 3 − , I−, Br−, F−, glutamate, and aspartate) on gating of Ca2+-dependent Cl− channels from rat parotid acinar cells were studied using the whole-cell configuration of the patch-clamp technique. Shifts in the reversal potential of the current induced by replacement of external Cl− with foreign anions, gave the following selectivity sequence based on permeability ratios (P x/P Cl): SCN−>I−>NO 3 − >Br−>Cl−>F−>aspartate>glutamate. Using a continuum electrostatic model we calculated that this lyotropic sequence resulted from the interaction between anions and a polarizable tunnel with an effective dielectric constant of ∼23. Our data revealed that anions with P x/PCl > 1 accelerated activation kinetics in a voltage-independent manner and slowed deactivation kinetics. Moreover, permeant anions enhanced whole-cell conductance (g, an index of the apparent open probability) in a voltage-dependent manner, and shifted leftward the membrane potential-g curves. All of these effects were produced by the anions with an effectiveness that followed the selectivity sequence. To explain the effects of permeant anions on activation kinetics and g Cl we propose that there are 2 different anion-binding sites in the channel. One site is located outside the electrical field and controls channel activation kinetics, while a second site is located within the pore and controls whole-cell conductance. Thus, interactions of permeant anions with these two sites hinder the closing mechanism and stabilize the channel in the open state.

Journal

The Journal of Membrane Biology – Springer Journals

Published: Jan 1, 2004

References

  • Interaction of tetraethylammonium ion derivatives with the potassium channels of giant axons
    Armstrong, C.
  • Volume-activated chloride channels in rat parotid acinar cells
    Arreola, J.; Melvin, J.E.; Begenisich, T.
  • Activation of calcium-dependent chloride channels in rat parotid acinar cells
    Arreola, J.; Melvin, J.E.; Begenisich, T.
  • Three distinct chloride channels control anion movement in rat parotid acinar cells
    Arreola, J.; Melvin, J.E.; Begenisich, T.
  • Regulation of chloride channels in secretory epithelia
    Begenisich, T.; Melvin, J.E.
  • Mechanism of anion permeation through channels gated by glycine and γ-aminobutyric acid in mouse cultured spinal neurones
    Bormann, J.; Hamill, O.P.; Sakmann, B.
  • Nonequilibrium gating and voltage dependence of the ClC-0 Cl− channel
    Chen, T.Y.; Miller, C.
  • Physiology of the Gastrointestinal Tract
    Cook, D.I.; Van Lennep, E.W.; Roberts, M.L.; Young, J.A.
  • Na+ and Cl− conductances are controlled by cytosolic Cl− concentration in the intralobular duct cells of mouse mandibular glands
    Dinudom, A.; Young, J.A.; Cook, D.I.
  • CFTR: Mechanism of anion conduction
    Dawson, D.C.; Smith, S.S.; Mansoura, M.K.
  • Gating the selectivity filter in ClC chloride channels
    Dutzler, R.; Campbell, E.B.; MacKinnon, R.
  • Calcium-activated chloride currents in isolated cells from rat lachrymal gland
    Evans, M.G.; Marty, A.
  • Mechanism of ion permeation in skeletal muscle chloride channels
    Fahlke, C.; Dürr, C.; George, A.L.
  • [Ca2+]i modulation of Cl− content controls cell volume in single salivary acinar cells during fluid secretion
    Foskett, J.K.
  • Activation of salivary secretion: coupling of cell volume and [Ca2+]i in single cells
    Foskett, J.K.; Melvin, J.E.
  • Modulation of decay of Ca2+-activated Cl− currents in rabbit portal vein smooth muscle cells by external anions
    Greenwood, I.A.; Large, W.A.
  • Anion permeation in an apical membrane chloride channel of a secretory epithelial cell
    Halm, D.R.; Frizzell, R.A.
  • Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches
    Hamill, O.P.; Marty, A.; Neher, E.; Sakmann, B.; Sigworth, F.J.
  • Properties of cAMP-dependent and Ca2+-dependent whole-cell Cl− conductances in rat epididymal cells
    Huang, S.J.; Fu, W.O.; Chung, Y.W.; Zhou, T.S.; Wong, P.Y.D.
  • A calcium- and voltage-dependent chloride current in developing chick skeletal muscle
    Hume, R.I.; Thomas, S.A.
  • A Ca2+-activated Cl− current in sheep parotid secretory cells
    Ishikawa, T.; Cook, D.I.
  • Intracellular Ca2+ and Cl− channel activation in secretory cells
    Kidd, J.F.; Thorn, P.
  • A calcium-dependent chloride current in insulin-secreting bTC-3 cells
    Kozak, J.A.; Logothetis, D.E.
  • Ion Properties
    Marcus, Y.
  • Correction for liquid junction potentials in patch clamp experiments
    Neher, E.
  • α-Adrenergic stimulation activates a calcium-sensitive chloride current in brown fat cells
    Pappone, P.; Lee, S.C.
  • Gating of the voltage-dependent chloride channel ClC-0 by the permeant anion
    Pusch, M.; Ludewig, U.; Rehfeldt, A.; Jentsch, T.J.
  • Chloride dependence of hyperpolarization-activated chloride channel gates
    Pusch, M.; Jordt, S.E.; Stein, V.; Jentsch, T.J.
  • Anion permeation in Ca2+-activated Cl− Channels
    Qu, Z.; Hartzell, H.
  • Concentration and pH dependence of skeletal muscle chloride channel ClC-1
    Rychkov, G.Y.; Pusch, M.; Astill, D.S.; Roberts, M.L.; Jentsch, T.J.; Bretag, A.H.
  • Permeation and block of the skeletal muscle chloride channel ClC-1 by foreign anions
    Rychkov, G.Y.; Pusch, M.; Roberts, M.L.; Jentsch, T.J.; Bretag, A.H.
  • Cystic fibrosis transmembrane conductance regulator: physical basis for lyotropic anion selectivity patterns
    Smith, S.S.; Steinle, E.D.; Meyerhoff, M.E.; Dawson, D.C.
  • Halide permeation in wild-type and mutant cystic fibrosis transmembrane conductance regulator chloride channels
    Tabcharani, J.A.; Linsdell, P.; Hanrahan, J.W.
  • High density of Ca2+-dependent K+ and Cl− channels on the luminal membrane of lacrimal acinar cells
    Tan, Y.P.; Marty, A.; Trautmann, A.
  • Gating competence of constitutively open ClC-0 mutants revealed by the interaction with a small organic inhibitor
    Traverso, S.; Elia, L.; Pusch, M.
  • Measurements of cytosolic free Ca2+ with Quin 2
    Tsien, R.; Pozzan, T.
  • Biology of Salivary Glands
    Turner, R.J.
  • Modulation of voltage-dependent properties of a swelling-activated Cl− current
    Voets, T.; Droogmans, G.; Nilius, B.

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