Anion currents in yeast K + transporters (TRK) characterize a structural homologue of ligand-gated ion channels

Alberto Rivetta, Teruo Kuroda, Clifford Slayman

Research output: Contribution to journalArticle

13 Citations (Scopus)

Abstract

Patch clamp studies of the potassium-transport proteins TRK1,2 in Saccharomyces cerevisiae have revealed large chloride efflux currents: at clamp voltages negative to -100 mV, and intracellular chloride concentrations >10 mM (J. Membr. Biol. 198:177, 2004). Stationary-state current-voltage analysis led to an in-series two-barrier model for chloride activation: the lower barrier (α) being 10-13 kcal/mol located ∼30% into the membrane from the cytoplasmic surface; and the higher one (β) being 12-16 kcal/mol located at the outer surface. Measurements carried out with lyotrophic anions and osmoprotective solutes have now demonstrated the following new properties: (1) selectivity for highly permeant anions changes with extracellular pH; at pH o=5.5: I -≈Br ->Cl ->SCN ->NO 3 -, and at pH o 7.5: I -≈Br ->SCN ->NO 3 - >Cl -. (2) NO 2 - acts like "superchoride", possibly enhancing the channel's intrinsic permeability to Cl -. (3) SCN - and NO 3 - block chloride permeability. (4) The order of selectivity for several slightly permeant anions (at pH o=5.5 only) is formate>gluconate>acetate>>phosphate -1. (5) All anion conductances are modulated (choked) by osmoprotective solutes. (6) The data and descriptive two-barrier model evoke a hypothetical structure (Biophys. J. 77:789, 1999) consisting of an intramembrane homotetramer of fungal TRK molecules, arrayed radially around a central cluster of four single helices (TM7) from each monomer. (7) That tetrameric cluster would resemble the hydrophobic core of (pentameric) ligand-gated ion channels, and would suggest voltage-modulated hydrophobic gating to underlie anion permeation.

Original languageEnglish
Pages (from-to)315-330
Number of pages16
JournalPflugers Archiv European Journal of Physiology
Volume462
Issue number2
DOIs
Publication statusPublished - Aug 2011

Fingerprint

Ligand-Gated Ion Channels
Yeast
Anions
Yeasts
Chlorides
formic acid
Clamping devices
Permeability
Electric potential
Permeation
Saccharomyces cerevisiae
Potassium
Carrier Proteins
Acetates
Monomers
Chemical activation
Phosphates
Cell Membrane
Membranes
Molecules

Keywords

  • Chaotropy
  • Chloride current
  • Eyring barriers
  • Facultative channels
  • Inward rectifier
  • Ligand-gated ion channels
  • Patch clamping
  • Saccharomyces cerevisiae
  • TRK proteins

ASJC Scopus subject areas

  • Physiology
  • Clinical Biochemistry
  • Physiology (medical)

Cite this

Anion currents in yeast K + transporters (TRK) characterize a structural homologue of ligand-gated ion channels. / Rivetta, Alberto; Kuroda, Teruo; Slayman, Clifford.

In: Pflugers Archiv European Journal of Physiology, Vol. 462, No. 2, 08.2011, p. 315-330.

Research output: Contribution to journalArticle

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abstract = "Patch clamp studies of the potassium-transport proteins TRK1,2 in Saccharomyces cerevisiae have revealed large chloride efflux currents: at clamp voltages negative to -100 mV, and intracellular chloride concentrations >10 mM (J. Membr. Biol. 198:177, 2004). Stationary-state current-voltage analysis led to an in-series two-barrier model for chloride activation: the lower barrier (α) being 10-13 kcal/mol located ∼30{\%} into the membrane from the cytoplasmic surface; and the higher one (β) being 12-16 kcal/mol located at the outer surface. Measurements carried out with lyotrophic anions and osmoprotective solutes have now demonstrated the following new properties: (1) selectivity for highly permeant anions changes with extracellular pH; at pH o=5.5: I -≈Br ->Cl ->SCN ->NO 3 -, and at pH o 7.5: I -≈Br ->SCN ->NO 3 - >Cl -. (2) NO 2 - acts like {"}superchoride{"}, possibly enhancing the channel's intrinsic permeability to Cl -. (3) SCN - and NO 3 - block chloride permeability. (4) The order of selectivity for several slightly permeant anions (at pH o=5.5 only) is formate>gluconate>acetate>>phosphate -1. (5) All anion conductances are modulated (choked) by osmoprotective solutes. (6) The data and descriptive two-barrier model evoke a hypothetical structure (Biophys. J. 77:789, 1999) consisting of an intramembrane homotetramer of fungal TRK molecules, arrayed radially around a central cluster of four single helices (TM7) from each monomer. (7) That tetrameric cluster would resemble the hydrophobic core of (pentameric) ligand-gated ion channels, and would suggest voltage-modulated hydrophobic gating to underlie anion permeation.",
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AU - Kuroda, Teruo

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N2 - Patch clamp studies of the potassium-transport proteins TRK1,2 in Saccharomyces cerevisiae have revealed large chloride efflux currents: at clamp voltages negative to -100 mV, and intracellular chloride concentrations >10 mM (J. Membr. Biol. 198:177, 2004). Stationary-state current-voltage analysis led to an in-series two-barrier model for chloride activation: the lower barrier (α) being 10-13 kcal/mol located ∼30% into the membrane from the cytoplasmic surface; and the higher one (β) being 12-16 kcal/mol located at the outer surface. Measurements carried out with lyotrophic anions and osmoprotective solutes have now demonstrated the following new properties: (1) selectivity for highly permeant anions changes with extracellular pH; at pH o=5.5: I -≈Br ->Cl ->SCN ->NO 3 -, and at pH o 7.5: I -≈Br ->SCN ->NO 3 - >Cl -. (2) NO 2 - acts like "superchoride", possibly enhancing the channel's intrinsic permeability to Cl -. (3) SCN - and NO 3 - block chloride permeability. (4) The order of selectivity for several slightly permeant anions (at pH o=5.5 only) is formate>gluconate>acetate>>phosphate -1. (5) All anion conductances are modulated (choked) by osmoprotective solutes. (6) The data and descriptive two-barrier model evoke a hypothetical structure (Biophys. J. 77:789, 1999) consisting of an intramembrane homotetramer of fungal TRK molecules, arrayed radially around a central cluster of four single helices (TM7) from each monomer. (7) That tetrameric cluster would resemble the hydrophobic core of (pentameric) ligand-gated ion channels, and would suggest voltage-modulated hydrophobic gating to underlie anion permeation.

AB - Patch clamp studies of the potassium-transport proteins TRK1,2 in Saccharomyces cerevisiae have revealed large chloride efflux currents: at clamp voltages negative to -100 mV, and intracellular chloride concentrations >10 mM (J. Membr. Biol. 198:177, 2004). Stationary-state current-voltage analysis led to an in-series two-barrier model for chloride activation: the lower barrier (α) being 10-13 kcal/mol located ∼30% into the membrane from the cytoplasmic surface; and the higher one (β) being 12-16 kcal/mol located at the outer surface. Measurements carried out with lyotrophic anions and osmoprotective solutes have now demonstrated the following new properties: (1) selectivity for highly permeant anions changes with extracellular pH; at pH o=5.5: I -≈Br ->Cl ->SCN ->NO 3 -, and at pH o 7.5: I -≈Br ->SCN ->NO 3 - >Cl -. (2) NO 2 - acts like "superchoride", possibly enhancing the channel's intrinsic permeability to Cl -. (3) SCN - and NO 3 - block chloride permeability. (4) The order of selectivity for several slightly permeant anions (at pH o=5.5 only) is formate>gluconate>acetate>>phosphate -1. (5) All anion conductances are modulated (choked) by osmoprotective solutes. (6) The data and descriptive two-barrier model evoke a hypothetical structure (Biophys. J. 77:789, 1999) consisting of an intramembrane homotetramer of fungal TRK molecules, arrayed radially around a central cluster of four single helices (TM7) from each monomer. (7) That tetrameric cluster would resemble the hydrophobic core of (pentameric) ligand-gated ion channels, and would suggest voltage-modulated hydrophobic gating to underlie anion permeation.

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KW - TRK proteins

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