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Pflügers Archiv - European Journal of Physiology

, Volume 467, Issue 12, pp 2447–2460 | Cite as

A structural model for facultative anion channels in an oligomeric membrane protein: the yeast TRK (K+) system

  • Juan Pablo Pardo
  • Martin González-Andrade
  • Kenneth Allen
  • Teruo Kuroda
  • Clifford L. SlaymanEmail author
  • Alberto Rivetta
Ion channels, receptors and transporters

Abstract

TRK transporters, a class of proteins which generally carry out the bulk of K+ accumulation in plants, fungi, and bacteria, mediate ion currents driven by the large membrane voltages (−150 to −250 mV) common to non-animal cells. Bacterial TRK proteins resemble K+ channels in their primary sequence, crystallize as membrane dimers having intramolecular K+-channel-like folding, and complex with a cytoplasmic collar formed of four RCK domains (Nature 471:336, 2011; Ibid 496:324, 2013). Fungal TRK proteins appear simpler in form than the bacterial members, but do possess two special features: a large built-in regulatory domain, and a highly conserved pair of transmembrane helices (TM7 and TM8, ahead of the C-terminus), which were postulated to facilitate intramembranal oligomerization (Biophys. J. 77:789, 1999; FEMS Yeast Res. 9:278, 2009). A surprising associated functional process in the fungal proteins which have been explored (Saccharomyces, Candida, and Neurospora) is facilitation of channel-like chloride efflux. That process is suppressed by osmoprotective agents, appears to involve hydrophobic gating, and strongly resembles conduction by Cys-loop ligand-gated anion channels. And it leads to a rather general hypothesis: that the thermodynamic tendency for hydrophobic or amphipathic transmembrane helices to self-organize into oligomers can create novel ionic pathways through biological membranes: fundamental hydrophobic nanopores, pathways of low selectivity governed by the chaotropic behavior of individual ionic species and under the strong influence of membrane voltage.

Keywords

Chaotropic anions TRK-potassium transporters Ligand-gated channels Compatible solutes Microbial chloride efflux 

Notes

Acknowledgments

The authors are indebted to Dr. Esther Bashi for technical assistance throughout these experiments, especially in the construction and maintenance of yeast strains, to Dr. Fred Sigworth for the key suggestion to characterize very high-voltage effects, and to Dr. Carolyn Slayman for essential advice and encouragement. We are also indebted to Dr. Ming Zhou (Baylor College of Medicine) and Dr. Jost Ludwig (Czech Academy of Sciences, and University of Bonn) for critical thoughts on the structures of TRK proteins, and to Dr. Ludwig for the structural coordinates in Fig. 7a. The work was supported in part by Research Grant R01-GM60696 (to CLS) from the U.S. National Institute of General Medical Sciences, by funds from the Yale Department of Cellular and Molecular Physiology, by grant IN209614 from Programa de Apoyo a Proyectos de Investigacion e Innovacion Tecnologica, UNAM (to JPP and MG-A), and by an Overseas Research Scholarship from the Japanese Ministry of Education, Culture, Sports, Science, and Technology (to TK).

Compliance with ethical standards

This manuscript has approval for submission by all six authors, is not under consideration by any other journal, represents no conflicts of interest for any of the authors, and does not involve human nor animal subjects.

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Authors and Affiliations

  1. 1.Departamento de Bioquimica, Facultad de MedicinaUniversidad Nacional Autonoma de MexicoMexico, D.F.Mexico
  2. 2.Department of GeneticsYale School of MedicineNew HavenUSA
  3. 3.Department of Microbiology, Graduate School of Medicine, Dentistry, and Pharmaceutical SciencesOkayama UniversityOkayamaJapan
  4. 4.Department of Cellular and Molecular PhysiologyYale School of MedicineNew HavenUSA

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