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

  • Ion channels, receptors and transporters
  • Published:
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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.

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Notes

  1. Stationary-state analysis is imposed by the yeast data: TRK-Cl− currents measured in response to voltage steps (Fig. 1a) always rise (or fall) faster than the patch-clamp amplifier can follow.

  2. Replacement of LHL by a 16-residue random coil was found to inactivate the whole protein [86], but that observation has been disputed (J. Ludwig, Pers. Comm).

References

  1. Albright RA, Ibar J-LV, Kim C-U, Gruner SM, Morais-Cabral JH (2006) The RCK domain of the KtrAB K+ transporter: multiple conformations of an octameric ring. Cell 126:147–1159

    Article  Google Scholar 

  2. Alvarez O, Gonzalez C, Latorre R (2002) Counting channels: a tutorial guide on ion channel fluctuation analysis. Adv Physiol Educ 26:327–341

  3. Amiri S, Tai K, Beckstein O, Biggin PC, Sansom MSP (2005) The α7 acetylcholine receptor: molecular modelling, electrostatics, and energetics. Mol Membr Biol 22:151–162

  4. Anishkin A, Sukharev S (2004) Water dynamics and dewetting transitions in the small mechanosensitive channel MscS. Biophys J 86:2883–2895

  5. Baev D, Rivetta A, Vylkova S, Sun JN, Zeng G-F, Slayman CL, Edgerton M (2004) The TRK1 potassium transporter is the critical effector for killing of Candida albicans by the cationic protein, Histatin 5. J Biol Chem 279:55060–55072

    Article  CAS  PubMed  Google Scholar 

  6. Bakker EP, Kroll RG, Booth IR (1984) Potassium transport in Escherichia coli: sodium is not a substrate of the potassium uptake system TrkA. FEMS Microbiol Lett 23:293–297

    Article  CAS  Google Scholar 

  7. Beckstein O, Biggin PC, Sansom MSP (2001) A hydrophobic gating mechanism for nanopores. J Phys Chem B 105:12902–12905

  8. Beckstein O, Sansom MSP (2003) Liquid–vapor oscillations of water in hydrophobic nanopores. Proc Natl Acad Sci U S A 100:7063–7068

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  9. Beckstein O, Sansom MSP (2005) A hydrophobic gate in an ion channel: the closed state of the nicotinic acetylcholine receptor. Phys Biol 3:147–159

    Article  Google Scholar 

  10. Bertl A, Bihler H, Kettner C, Slayman CL (1998) Electrophysiology in the eukaryotic model cell Saccharomyces cerevisiae. Pflügers Arch Eur J Physiol 436:999–1013

    Article  CAS  Google Scholar 

  11. Bielby MJ (1986) Potassium channels and different states of Chara plasmalemma. J Membr Biol 89:241–249

    Article  Google Scholar 

  12. Bihler H, Gaber RF, Slayman CL, Bertl A (1999) The presumed potassium carrier Trk2p in Saccharomyces cerevisiae determines an H+-dependent, K+-independent current. FEBS Lett 447:115–120

    Article  CAS  PubMed  Google Scholar 

  13. Black JF, Oakenful D, Smith MB (1979) Increased thermal stability of proteins in the presence of sugars and polyols. Biochemistry 18:5191–5196

  14. Blatt MR, Rodriguez-Navarro A, Slayman CL (1987) Potassium-proton symport in Neurospora: kinetic control by pH and membrane potential. J Membr Biol 98:169–189

    Article  CAS  PubMed  Google Scholar 

  15. Bocquet N, de Carvalho LP, Cartaud J, Neyton J, Le Poupon C, Taly A, Grutter T, Changeux J-P, Corringer P-J (2007) A prokaryotic proton-gated ion channel from the nicotinic acetylcholine receptor family. Nature 445:116–119

    Article  CAS  PubMed  Google Scholar 

  16. Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1111

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Boström M, Williams DRM, Ninham BW (2003) Specific ion effects: why the properties of lysozme in salt solutions follow a Hofmeister series. Biophys J 85:686–694

    Article  PubMed Central  PubMed  Google Scholar 

  18. Caldas T, Demont-Caulet N, Ghazi A, Richarme G (1999) Thermoprotection by glycine betaine and choline. Microbiology 145:2543–2548

    Article  CAS  PubMed  Google Scholar 

  19. Cao Y, Jin X, Huang H, Derebe MG, Levin EJ, Kabaleeswaran V, Pan Y, Punta M, Love J, Weng J, Quick M, Ye S, Kloss B, Bruni R, Martinez-Hackert E, Hendrickson WA, Rost B, Javitch JA, Rajashankar KR, Jiang Y, Zhou M (2011) Crystal structure of a potassium ion transporter, TrkH. Nature 471:336–341

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  20. Cao Y, Pan Y, Huang H, Jin X, Levin EJ, Kloss B, Zhou M (2013) Gating of the TrkH ion channel by its associated RCK protein TrkA. Nature 496:317–323

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. Chaplin M (2014) Water structure and science: kosmotropes and chaotropes. http://www1.Isbu.ac.uk/water/kosmos.html

  22. Collins KD, Washabaugh MW (1985) The Hofmeister effect and the behaviour of water at interfaces. Q Rev Biophys 18:323–422

    Article  CAS  PubMed  Google Scholar 

  23. Coster HGL (1968) The role of pH in the punch-through effect in the electrical characteristics of Chara australis. Aust J Biol Sci 22:365–374

    Google Scholar 

  24. DeLano WL (2000) PyMol open source molecular viewer. www.pymol.org; DNL v. 1.5.0.4 from Schrödinger LLC: www.schrodinger.com/pymol

  25. dos Santos AP, Diehl A, Levin Y (2010) Surface tensions, surface potentials and the Hofmeister series of electrolyte solutions. Langmuir 26:10778–10783

    Article  PubMed  Google Scholar 

  26. Durell SR, Guy HR (1999) Structural models of the KtrB, TrkH, and Trk1,2 symporters, based on the crystal strucure of the KcsA K+ channel. Biophys J 77:789–807

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Durell SR, Hao Y, Nakamura T, Bakker EP, Guy HR (1999) Evolutionary relationship between K+ channels and symporters. Biophys J 77:775–788

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  28. Dzubiella J, Hansen J-P (2005) Electric-field controlled water and ion permeation of a hydrophobic nanopore. J Chem Phys 122:234706-1/14

    Google Scholar 

  29. Felle H, Porter JS, Slayman CL, Kaback HR (1980) Quantitative measurements of membrane potential in Escherichia coli. Biochemistry 19:3585–3590

    Article  CAS  PubMed  Google Scholar 

  30. Fiser A, Do RK, Sali A (2000) Modeling of loops in protein structures. Protein Sci 9:1753–1773

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Gradmann D, Boyd CM (1999) Electrophysiology of the marine diatom Coscinodiscus wailesii IV: types of non-linear current–voltage-time relationships recorded with single saw-tooth voltage-clamp experiments. Eur Biophys J 28:591–599

    Article  CAS  PubMed  Google Scholar 

  32. Gray PT (1994) Analysis of whole cell currents to estimate the kinetics and amplitude of underlying unitary events: relaxation and ‘noise’ analysis. In: Ogden D (ed) Microelectrode techniques. Company of Biologists, Ltd, Cambridge, pp 189–207

    Google Scholar 

  33. Guo W, Tian Y, Jiang L (2013) Asymmetric ion transport through ion-channel-mimetic solid-state nanopores. Acc Chem Res 46:2834–2846

    Article  CAS  PubMed  Google Scholar 

  34. Hachez C, Chaumont F (2010) Aquaporins: a family of highly regulated multifunctional channels. Adv Exp Med Biol 679:1–17

  35. Haghighi AP, Cooper E (1998) Neuronal nicotinic acetylcholine receptors are blocked by intracellular spermine in a voltage-dependent manner. J Neurosci 18:4050–4062

    CAS  PubMed  Google Scholar 

  36. Herrera M, Garvin J (2011) Aquaporins as gas channels. Pflügers Arch Eur J Physiol 462:623–630

    Article  CAS  Google Scholar 

  37. Hibbs RE, Gouaux E (2011) Principles of activation and permeation in an anion-selective Cys-loop receptor. Nature 474:54–60

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Hilf RJC, Dutzler R (2009) Structure of a potentially open state of a proton-activated pentameric ligand-gated ion channel. Nature 457:115–119

    Article  CAS  PubMed  Google Scholar 

  39. Hille B (1975) Ionic selectivity, saturation, and block in sodium channels. A four-barrier model. J Gen Physiol 65:535–560

    Article  Google Scholar 

  40. Hornak V, Abel R, Okur A, Stockbine B, Roitberg A, Simmerling C (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65:712–725

    Article  CAS  PubMed  Google Scholar 

  41. Hottiger T, Boller T, Wiemken A (1987) Rapid changes of heat and desiccation tolerance correlated with changes of trehalose content in Saccharomyces cerevisiae cells subjected to temperature shifts. FEBS Lett 220:113–115

    Article  CAS  PubMed  Google Scholar 

  42. Hummer G, Rasalah JC, Noworyta JP (2001) Water conduction through the hydrophobic channel of a carbon nanotube. Nature 414:18–190

    Article  Google Scholar 

  43. Ivanov I, Cheng X-L, Sine SM, McCammon JA (2007) Barriers to ion translocation in cationic and anionic receptors from the Cys-loop family. J Am Chem Soc 129:8217–8224

    Article  CAS  PubMed  Google Scholar 

  44. Jan LY, Jan YN (1997) Cloned potassium channels from eukaryotes and prokaryotes. Annu Rev Neurosci 20:91–123

    Article  CAS  PubMed  Google Scholar 

  45. Jensen MO, Borhani DW, Lindorff-Larsen K, Maragakis P, Jogini V, Eastwood MP, Dror RO, Shaw DE (2010) Principles of conduction and hydrophobic gating in K+ channels. Proc Natl Acad Sci U S A 107:5833–5838

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  46. Kato Y, Sakaguchi M, Mori Y, Saito K, Nakamura T, Bakker EP, Sato Y, Goshima S, Uozumi N (2001) Evidence in support of a four transmembrane-pore-transmembrane topology model for the Arabidopsis thaliana Na+/K+ translocating AtHKT1 protein, a member of the superfamily of K+ transporters. Proc Natl Acad Sci U S A 98:6488–6493

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  47. Klotz K-H, Benz R (1993) Kinetics of the iodine- and bromine-mediated transport of halide ions: demonstration of an interfacial complexation mechanism. Biophys J 65:2661–2672

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  48. Kropf DL (1986) Elecrophysiological properties of Achlya hyphae: ionic currents studied by intracellular potential recording. J Cell Biol 102:1209–1216

    Article  CAS  PubMed  Google Scholar 

  49. Kruse E, Uehlein N, Kaldenhoff R (2006) The aquaporins. Genome Biol 7:206–215

    Article  PubMed Central  PubMed  Google Scholar 

  50. Kuroda T, Bihler H, Bashi E, Slayman CL, Rivetta A (2004) Chloride channel function in the yeast TRK-potassium transporters. J Membr Biol 198:177–192

    Article  CAS  PubMed  Google Scholar 

  51. Lages F, Silva-Graça M, Lucas C (1999) Active glycerol uptake is a mechanism underlying halotolerance in yeasts: a study of 42 species. Microbiology 145:2577–2585

    Article  CAS  PubMed  Google Scholar 

  52. Läuger P (1973) Ion transport through pores: a rate-theory analysis. Biochim Biophys Acta 311:423–441

    Article  PubMed  Google Scholar 

  53. Lo Nostro P, Ninham BW (2012) Hofmeister phenomena: an update on ion specificity in biology. Chem Rev 112:2286–2322

    Article  CAS  PubMed  Google Scholar 

  54. Machtens J-P, Kortzak D, Lansche C, Leinenweber A, Kilian P, Begemann B, Zachariae U, Ewers D, de Groot BL, Briones R, Fahlke C (2015) Mechanisms of anion conduction by coupled glutamate transporters. Cell 260:542–553

    Article  Google Scholar 

  55. Mäser P, Hosoo Y, Goshima S, Horie T, Eckelman B, Yamada K, Yoshida K, Bakker EP, Shinmyo A, Oiki S, Schroeder JI, Uozumi N (2002) Glycine residues in potassium channel-like selectivity filters determine potassium selectivity in four-loop-per subunit HKT transporters from plants. Proc Natl Acad Sci U S A 99:6428–6433

    Article  PubMed Central  PubMed  Google Scholar 

  56. McLaughlin S, Bruder A, Chen S, Moser C (1975) Chaotropic anions and the surface potential of bilayer membranes. Biochim Biophys Acta 394:304–313

    Article  CAS  PubMed  Google Scholar 

  57. Miranda M, Bashi E, Vylkova S, Edgerton M, Slayman CL, Rivetta A (2009) Conservation and dispersion of sequence and function in fungal TRK potassium transporters: Focus on Candida albicans. FEMS Yeast Res 9:278–292

    Article  CAS  PubMed  Google Scholar 

  58. Nicholls P, Miller N (1974) Chloride diffusion from liposomes. Biochim Biophys Acta 356:184–198

    Article  CAS  PubMed  Google Scholar 

  59. Nilius B, Eggemont J, Voets T, Buyse G, Manolopoulos V, Droogmans G (1997) Properties of volume-regulated anion channels in mammalian cells. Prog Biophys Mol Biol 68:69–119

    Article  CAS  PubMed  Google Scholar 

  60. Olejníková P, Hudecová D, Burgstaller W, Krystofová S, Varecka L (2011) Transient excretion of succinate from Trichoderma atroviride submerged mycelia reveals the complex movements and metabolism of carboxylates. Antonie Van Leeuwenhoek 100:55–66

    Article  PubMed  Google Scholar 

  61. Paula S, Volkov AG, Deamer DW (1998) Permeation of halide anions through phospholipid bilayers occurs by the solubility-diffusion mechanism. Biophys J 74:319–327

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  62. Powell MR, Cleary L, Davenport M, Shea KJ, Siwy ZS (2011) Electric-field-induced wetting and dewetting in single hydrophobic nanopores. Nat Nanotechnol 6:798–802

  63. Qiu A, Dubin AE, Mathur J, Tu B, Reddy K, Miraglia LJ, Reinhardt J, Orth AP, Patapoutian A (2014) SWELL1, a plasma membrane protein, is an essential component of volume-regulated anion channel. Cell 157:447–458

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  64. Rivetta A, Kuroda T, Slayman CL (2011) Anion currents in yeast K+ transporters (TRK) characterize a structural homologue of ligand-gated ion channels. Pflügers Arch Eur J Physiol 462:315–330

    Article  CAS  Google Scholar 

  65. Rivetta A, Slayman CL, Kuroda T (2005) Quantitative modeling of chloride conductance in yeast TRK potassium transporters. Biophys J 89:2412–2426

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  66. Rodriguez-Navarro A (2000) Potassium transport in fungi and plants. Biochim Biophys Acta 1469:1–30

    Article  CAS  PubMed  Google Scholar 

  67. Ryckaert JP, Ciccotti G, Berendsen HJC (1977) Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comput Phys 23:327–341

    Article  CAS  Google Scholar 

  68. Sachs F, Qin F (1993) Gated, ion-selective channels observed with patch pipettes in the absence of membranes: novel properties of a gigaseal. Biophys J 65:1101–1107

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  69. Sali A, Blundell TL (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234:779–815

    Article  CAS  PubMed  Google Scholar 

  70. Sigler K, Kotyk A, Knotková A, Operkarová M (1981) Processes involved in the creation of buffering capacity and in substrate-induced proton extrusion in the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 643:583–592

    Article  CAS  PubMed  Google Scholar 

  71. Slayman CL, Kaminski P, Stetson D (1990) Structure and function of fungal plasma-membrane ATPases. In: Kuhn PJ, Trinci AP, Jung MJ, Goosey MW, Coppng LG (eds) Biochemistry of cell walls and membranes of fungi. Springer, Berlin, pp 295–312

    Google Scholar 

  72. Slayman CL, Long WS, Lu CY-H (1973) The relationship between ATP and an electrogenic pump in the plasma membrane of Neurospora crassa. J Membr Biol 14:305–338

    Article  CAS  PubMed  Google Scholar 

  73. Smirnov SN, Vassiouk IV, Lavrik NV (2011) Voltage-gated hydrophobic nanopores. ACS Nano 5:7453–7461

    Article  CAS  PubMed  Google Scholar 

  74. Spronk SA, Elmore DE, Dougherty DA (2006) Voltage-dependent hydration and conduction properties of the hydrophobic pore of the mechanosensitive channel of small conductance. Biophys J 90:3555–3569

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  75. Stumpe S, Schlösser A, Schleyer M, Bakker EP (1996) K+ circulation across the prokaryotic cell membrane: K+-uptake systems. In: Konings WN, Kaback HR, Lolkema JS (eds) Transport processes in eukaryotic and prokaryotic organisms. Elsevier, Amsterdam, pp 473–500

    Chapter  Google Scholar 

  76. Sukharev S, Blount P, Martinac B, Kung C (1997) Mechanosensitive channels of Escherichia coli: MscL gene, protein, and activities. Annu Rev Physiol 59:633–657

    Article  CAS  PubMed  Google Scholar 

  77. Tholema N, Bakker EP, Suzuki A, Nakamura T (1999) Change to alanine of one out of four selectivity filter glycines in KtrB causes a two orders-of-magnitude decrease in the affinities for both K+ and Na+ of the Na+-dependent K+-uptake system KtrAB from Vibrio alginolyticus. FEBS Lett 450:217–220

    Article  CAS  PubMed  Google Scholar 

  78. Verveen VV, DeFelice LJ (1974) Membrane noise. Prog Biophys Mol Biol 28:189–265

    Article  CAS  PubMed  Google Scholar 

  79. Vieira-Pires RS, Szollosi A, Morais-Cabral JH (2013) The structure of the KtrAB potassium transporter. Nature 496:323–329

    Article  CAS  PubMed  Google Scholar 

  80. Volkov V, Boscari A, Clement M, Miller AJ, Amtmann A, Fricke W (2009) Electrophysiological characterization of pathways for K+ uptake into growing and non-growing leaf cells of barley. Plant Cell Environ 32:1778–1790

    Article  CAS  PubMed  Google Scholar 

  81. Voss FK, Ullrich F, Munch J, Lazarow K, Lutter D, Mah N, Andrade-Navarro MA, von Kries JP, Stauber T, Jentsch TJ (2014) Identification of LRRC8 heteromers as an essential component of the volume-regulated anion channel VRAC. Science 344:634–638

    Article  CAS  PubMed  Google Scholar 

  82. Vrabl P, Mutschlechner W, Burgstaller W (2008) Characteristics of glucose uptake by glucose- and NH4-limited grown Penicillium ochrochloron at low, medium and high glucose concentration. Fungal Genet Biol 45:1380–1392

    Article  CAS  PubMed  Google Scholar 

  83. Wang J, Wang W, Kollman PA, Case DA (2006) Automatic atom type and bond type perception in molecular mechanical calculations. J Mol Graph Model 25:247–260

    Article  PubMed  Google Scholar 

  84. Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cryoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819–2830

    Article  CAS  PubMed  Google Scholar 

  85. Zayats V, Stockner T, Pandey SK, Wörz K, Ettrich R, Ludwig J (2015) A refined atomic scale model of Saccharomyces cerevisiae K+-translocation protein Trk1p combined with experimental evidence confirms the role of selectifity filter glycines and other key residues. Biohim Biophys Acta 1848:1183–1195

    Article  CAS  Google Scholar 

  86. Zeng G-F, Pypaert M, Slayman CL (2004) Epitope tagging of the yeast K+ carrier, TRK2, demonstrates folding which is consistent with a channel-like structure. J Biol Chem 270:3003–3013

    Article  Google Scholar 

  87. Zhao L, Kuo Y-P, George AA, Peng J-H, Purandare MS, Schroeder KM, Lukas RJ, Wu J (2003) Functional properties of homomeric, human α7-nicotinic acetylcholine receptors heterologously expressed in the SH-EP1 human epithelial cell line. J Pharmacol Exp Ther 305:1132–1141

  88. Zilberstein D, Agmon V, Schuldner S, Padan E (1984) Escherichia coli intracellular pH, membrane potential, and cell growth. J Bacteriol 158:246–252

    PubMed Central  CAS  PubMed  Google Scholar 

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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).

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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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  1. Departamento de Bioquimica, Facultad de Medicina, Universidad Nacional Autonoma de Mexico, Ciudad Universitaria, Coyoacan, 04510, Mexico, D.F., Mexico

    Juan Pablo Pardo & Martin González-Andrade

  2. Department of Genetics, Yale School of Medicine, 333 Cedar Street, New Haven, CT, 06520, USA

    Kenneth Allen

  3. Department of Microbiology, Graduate School of Medicine, Dentistry, and Pharmaceutical Sciences, Okayama University, 1-1-1 Tsushima-Naka, Kita-ku, Okayama, 700-8530, Japan

    Teruo Kuroda

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

    Clifford L. Slayman & Alberto Rivetta

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  1. Juan Pablo Pardo
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Correspondence to Clifford L. Slayman.

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Pardo, J.P., González-Andrade, M., Allen, K. et al. A structural model for facultative anion channels in an oligomeric membrane protein: the yeast TRK (K+) system. Pflugers Arch - Eur J Physiol 467, 2447–2460 (2015). https://doi.org/10.1007/s00424-015-1712-6

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