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Chloride Channel Function in the Yeast TRK-Potassium Transporters

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Abstract

The TRK proteins—Trk1p and Trk2p— are the main agents responsible for “active” accumulation of potassium by the yeast Saccharomyces cerevisiae. In previous studies, inward currents measured through those proteins by whole-cell patch-clamping proved very unresponsive to changes of extracellular potassium concentration, although they did increase with extracellular proton concentration—qualitatively as expected for H+ coupling to K+ uptake. These puzzling observations have now been explored in greater detail, with the following major findings: a) the large inward TRK currents are not carried by influx of either K+ or H+, but rather by an efflux of chloride ions; b) with normal expression levels for Trk1p and Trk2p in potassium-replete cells, the inward TRK currents are contributed approximately half by Trk1p and half by Trk2p; but c) strain background strongly influences the absolute magnitude of these currents, which are nearly twice as large in W303-derived spheroplasts as in S288c-derived cells (same cell-size and identical recording conditions); d) incorporation of mutations that increase cell size (deletion of the Golgi calcium pump, Pmr1p) or that upregulate the TRK2 promoter, can further substantially increase the TRK currents; e) removal of intracellular chloride (e.g., replacement by sulfate or gluconate) reveals small inward currents that are K+-dependent and can be enhanced by K+ starvation; and f) finally, the latter currents display two saturating kinetic components, with preliminary estimates of K0.5 at 46 μM [K+]out and 6.8 mM [K+]out, and saturating fluxes of ∼5 mM/min and ∼10 mM/min (referred to intracellular water). These numbers are compatible with the normal K+-transport properties of Trk1p and Trk2p, respectively.

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Acknowledgements

For yeast strains, the authors are indebted to Drs. Bert Smith (formerly in the Department of Molecular, Cellular, and Developmental Biology at Yale; now at deCode Genetics, Reykjavik), Kyle Cunningham (Johns Hopkins University), Richard Gaber (Northwestern University), and Per Ljungdahl (Ludwig Institute, Stockholm, Sweden). We are also indebted to Drs. Michael Snyder and Beth Rockmill (Yale Department of Molecular, Cellular, and Developmental Biology), to Dr. Scott Erdman (Syracuse University), to Dr. Peter Novick (Yale Department of Cell Biology), and to Dr. Ge-Fei Zeng (this Department) for much helpful advice toward the construction of yeast mutants. Finally, we are especially indebted to Dr. Adam Bertl (Botanical Institute I, Karlsruhe, Germany) for inspiring these investigations, for pointing to the likely importance of strain background, and for a thorough and helpful critique of the manuscript. The research was supported by Grant # GM-60696 from the National Institute of General Medical Sciences (to C.L.S.), and by an Overseas Research Scholarship from the Japanese Ministry of Education, Culture, Sports, Science, and Technology (to T.K.).

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  1. Department of Cellular and Molecular Physiology, Yale School of Medicine, 333 Cedar Street, New Haven, CT, 06520, USA

    T. Kuroda, E. Bashi, C. L. Slayman & A. Rivetta

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

    T. Kuroda

  3. Botanisches Institute, Lehrstuhl I, Universität Karlsruhe, D-76128, Karlsruhe, Germany

    H. Bihler

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Correspondence to C. L. Slayman.

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Kuroda, T., Bihler, H., Bashi, E. et al. Chloride Channel Function in the Yeast TRK-Potassium Transporters. J Membrane Biol 198, 177–192 (2004). https://doi.org/10.1007/s00232-004-0671-1

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