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

  • Ion Channels, Receptors and Transporters
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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 pHo = 5.5: I− ≈ Br− > Cl− > SCN− > NO −3 , and at pHo 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 pHo = 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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Acknowledgments

The authors are indebted to Dr. Esther Bashi for technical assistance throughout these experiments and especially for the construction of the EB series of strains, and to Mr. Kenneth Allen for always ready advice and assistance in the management of yeast cultures. We are also grateful to Dr. Albert Smith and to Dr. Kyle Cunningham (Johns Hopkins University) for provision of starting strains; and to Dr. Ming Zhou (Columbia University) for prepublication review of his manuscript on the structure of VpTrkH. Finally, Drs. Fred Sigworth, Edward Moczdlowski (Clarkson University), and Bertl Hille (University of Washington) provided much creative and helpful criticism of the manuscript. The work was supported by Research Grant R01-GM60696 (to CLS) from the US National Institute of General Medical Sciences and by an Overseas Research Scholarship from the Japanese Ministry of Education, Culture, Sports, Science, and Technology (to TK).

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  1. Department of Cellular and Molecular Physiology, Yale School of Medicine, 333 Cedar Street, New Haven, CT, 06510, USA

    Alberto Rivetta, Teruo Kuroda & Clifford Slayman

  2. Department of Microbiology, Faculty of Pharmaceutical Sciences, Okayama University, 1-1-1 Tsushimanaka, Okayama, 700-8530, Japan

    Teruo Kuroda

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Rivetta, A., Kuroda, T. & Slayman, C. Anion currents in yeast K+ transporters (TRK) characterize a structural homologue of ligand-gated ion channels. Pflugers Arch - Eur J Physiol 462, 315–330 (2011). https://doi.org/10.1007/s00424-011-0959-9

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