KtrB, a member of the superfamily of K + transporters

European Journal of Cell Biology

Volumn 90, Issue 9, 2011, Pages 696-704

  Hänelt, Inga ^a   Tholema, Nancy ^a   Kröning, Nadine ^a   Vor der Brüggen, Marc ^a   Wunnicke, Dorith ^a   Bakker, Evert P ^a  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

HKT; K + channel KcsA; K + transport; K + selectivity filter; Kdp system; Kef system; KTN domain; RCK domain; SKT proteins; Trk system

Indexed keywords

BACTERIAL PROTEIN; POTASSIUM CHANNEL; POTASSIUM ION; PROTEIN KTRB; UNCLASSIFIED DRUG;

CYTOPLASM; MEMBRANE PERMEABILITY; NONHUMAN; POTASSIUM TRANSPORT; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; SHORT SURVEY; VIBRIO ALGINOLYTICUS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CATION TRANSPORT PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POTASSIUM; PROTEIN STRUCTURE, SECONDARY; PROTEIN TRANSPORT; VIBRIO ALGINOLYTICUS;

BACTERIA (MICROORGANISMS); FUNGI; VIBRIO ALGINOLYTICUS;

EID: 79960556806     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2011.04.010     Document Type: Short Survey

References (65)

1. Albright R.A., Ibar J.L., Kim C.U., Gruner S.M., Morais-Cabral J.H. The RCK domain of the KtrAB K+ transporter: multiple conformations of an octameric ring. Cell 2006, 126:1147-1159.
2. Albright R.A., Joh K., Morais-Cabral J.H. Probing the structure of the dimeric KtrB membrane protein. J. Biol. Chem. 2007, 282:35046-35055.
3. Ariño J., Ramos J., Sychrová H. Alkali metal cation transport and homeostasis in yeasts. Microbiol. Mol. Biol. Rev. 2010, 74:95-120.
4. Bakker E.P. Cell K+ and K+Transport systems in prokaryotes. Alkali Cation Transport Systems in Prokaryotes 1993, CRC Press, pp. 205-224 (Chapter IIA). E.P. Bakker (Ed.).
5. Bateman A., Birney E., Durbin R., Eddy S.R., Howe K.L., Sonnhammer E.L. The Pfam protein families database. Nucleic Acids Res. 2000, 28:263-266.
6. Bertrand J., Altendorf K., Bramkamp M. Amino acid substitutions in putative selectivity filter regions III and IV in KdpA alter ion selectivity of the KdpFABC complex from Escherichia coli. J. Bacteriol. 2004, 186:5519-5522.
7. Booth I.R. Regulation of cytoplasmic pH in bacteria. Microbiol. Rev. 1985, 49:359-378.
8. Bult C.J., White O., Olsen G.J., Zhou L., Fleischmann R.D., Sutton G.G., Blake J.A., FitzGerald L.M., Clayton R.A., Gocayne J.D., Kerlavage A.R., Dougherty B.A., Tomb J.F., Adams M.D., Reich C.I., Overbeek R., Kirkness E.F., Weinstock K.G., Merrick J.M., Glodek A., Scott J.L., Geoghagen N.S., Venter J.C. Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 1996, 273:1058-1073.
9. Buurman E.T., Kim K.T., Epstein W. Genetic evidence for two sequentially occupied K+ binding sites in the Kdp transporter ATPase. J. Biol. Chem. 1995, 270:6678-6685.
10. Cao Y., Jin X., Huang H., Derebe M.G., Levin E.J., Kabaleeswaran V., Pan Y., Punta M., Love J., Weng J., Quick M., Ye S., Kloss B., Bruni R., Martinez-Hackert E., Hendrickson W.A., Rost B., Javitch J.A., Rajashankar K.R., Jiang Y., Zhou M. Crystal structure of a potassium ion transporter, TrkH. Nature 2011, 471:336-340.
11. Corratgé-Faillie C., Jabnoune M., Zimmermann S., Véry A.A., Fizames C., Sentenac H. Potassium and sodium transport in non-animal cells: the Trk/Ktr/HKT transporter family. Cell Mol. Life Sci. 2010, 67:2511-2532.
12. Cuello L.G., Jogini V., Cortes D.M., Perozo E. Structural mechanism of C-type inactivation in K(+) channels. Nature 2010, 466:203-208.
13. Dorus S., Mimura H., Epstein W. Substrate-binding clusters of the K+-transporting Kdp ATPase of Escherichia coli investigated by amber suppression scanning mutagenesis. J. Biol. Chem. 2001, 276:9590-9598.
14. Doyle D.A., Morais Cabral J., Pfuetzner R.A., Kuo A., Gulbis J.M., Cohen S.L., Chait B.T., MacKinnon R. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 1998, 280:69-77.
15. Durell S.R., Guy H.R. Structural models of the KtrB, TrkH, and Trk1,2 symporters based on the structure of the KcsA K(+) channel. Biophys. J. 1999, 77:789-807.
16. Durell S.R., Hao Y., Nakamura T., Bakker E.P., Guy H.R. Evolutionary relationship between K(+) channels and symporters. Biophys. J. 1999, 77:775-788.
17. Durell S.R., Bakker E.P., Guy H.R. Does the KdpA subunit from the high affinity K(+)-translocating P-type KDP-ATPase have a structure similar to that of K(+) channels?. Biophys. J. 2000, 78:188-199.
18. Epstein W. The roles and regulation of potassium in bacteria. Prog. Nucleic Acid Res. Mol. Biol. 2003, 75:293-320.
19. Gaber R.F., Styles C.A., Fink G.R. TRK1 encodes a plasma membrane protein required for high-affinity potassium transport in Saccharomyces cerevisiae. Mol. Cell Biol. 1988, 8:2848-2859.
20. Gadsby D.C. Ion transport: spot the difference. Nature 2004, 427:795-797.
21. Gadsby D.C. Ion channels versus ion pumps: the principal difference, in principle. Nat. Rev. Mol. Cell Biol. 2009, 10:344-352.
22. Hänelt I., Löchte S., Sundermann L., Elbers K., Vor der Brüggen M., Bakker E.P. Gain of function mutations in membrane region M2C2 of KtrB open a gate controlling K+ transport by the KtrAB system from Vibrio alginolyticus. J. Biol. Chem. 2010, 285:10318-10327.
23. Hänelt I., Wunnicke D., Müller-Trimbusch M., Vor der Brüggen M., Kraus I., Bakker E.P., Steinhoff H.J. Membrane region M2C2 in subunit KtrB of the K+ uptake system KtrAB from Vibrio alginolyticus forms a flexible gate controlling K+ flux: an electron paramagnetic resonance study. J. Biol. Chem. 2010, 285:28210-28219.
24. Harms C., Domoto Y., Celik C., Rahe E., Stumpe S., Schmid R., Nakamura T., Bakker E.P. Identification of the ABC protein SapD as the subunit that confers ATP dependence to the K+-uptake systems Trk(H) and Trk(G) from Escherichia coli K-12. Microbiology 2001, 147:2991-3003.
25. Heginbotham L., Lu Z., Abramson T., MacKinnon R. Mutations in the K+ channel signature sequence. Biophys. J. 1994, 66:1061-1067.
26. Hesse J.E., Wieczorek L., Altendorf K., Reicin A.S., Dorus E., Epstein W. Sequence homology between two membrane transport ATPases, the Kdp-ATPase of Escherichia coli and the Ca2+-ATPase of sarcoplasmic reticulum. Proc. Natl. Acad. Sci. U.S.A. 1984, 81:4746-4750.
27. Holtmann G., Bakker E.P., Uozumi N., Bremer E. KtrAB and KtrCD: two K+ uptake systems in Bacillus subtilis and their role in adaptation to hypertonicity. J. Bacteriol. 2003, 185:1289-1298.
28. Horie T., Yoshida K., Nakayama H., Yamada K., Oiki S., Shinmyo A. Two types of HKT transporters with different properties of Na+ and K+ transport in Oryza sativa. Plant J. 2001, 27:129-138.
29. Jiang Y., Pico A., Cadene M., Chait B.T., MacKinnon R. Structure of the RCK domain from the E. coli K+ channel and demonstration of its presence in the human BK channel. Neuron 2001, 29:593-601.
30. Jiang Y., Lee A., Chen J., Cadene M., Chait B.T., MacKinnon R. Crystal structure and mechanism of a calcium-gated potassium channel. Nature 2002, 417:515-522.
31. Kato Y., Sakaguchi M., Mori Y., Saito K., Nakamura T., Bakker E.P., Sato Y., Goshima S., Uozumi N. 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. 2001, 98:6488-6493.
32. Ko C.H., Gaber R.F. TRK1 and TRK2 encode structurally related K+ transporters in Saccharomyces cerevisiae. Mol. Cell Biol. 1991, 11:4266-4273.
33. Kröning N., Willenborg M., Tholema N., Hänelt I., Schmid R., Bakker E.P. ATP binding to the KTN/RCK subunit KtrA from the K+-uptake system KtrAB of Vibrio alginolyticus: its role in the formation of the KtrAB complex and its requirement in vivo. J. Biol. Chem. 2007, 282:14018-14027.
34. Kuo A., Gulbis J.M., Antcliff J.F., Rahman T., Lowe E.D., Zimmer J., Cuthbertson J., Ashcroft F.M., Ezaki T., Doyle D.A. Crystal structure of the potassium channel KirBac1.1 in the closed state. Science 2003, 300:1922-1926.
35. Kuo M.M., Haynes W.J., Loukin S.H., Kung C., Saimi Y. Prokaryotic K(+) channels: from crystal structures to diversity. FEMS Microbiol. Rev. 2005, 29:961-985.
36. van der Laan M., Gassel M., Altendorf K. Characterization of amino acid substitutions in KdpA, the K+-binding and -translocating subunit of the KdpFABC complex of Escherichia coli. J. Bacteriol. 2002, 184:5491-5494.
37. Lü Q., Miller C. Silver as a probe of pore-forming residues in a potassium channel. Science 1995, 268:304-307.
38. Mäser P., Hosoo Y., Goshima S., Horie T., Eckelman B., Yamada K., Yoshida K., Bakker E.P., Shinmyo A., Oiki S., Schroeder J.I., Uozumi N. 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. 2002, 99:6428-6433.
39. Manoil C., Beckwith J. A genetic approach to analyzing membrane protein topology. Science 1986, 233:1403-1408.
40. Matsuda N., Kobayashi H., Katoh H., Ogawa T., Futatsugi L., Nakamura T., Bakker E.P., Uozumi N. Na+-dependent K+ uptake Ktr system from the cyanobacterium Synechocystis sp. PCC 6803 and its role in the early phases of cell adaptation to hyperosmotic shock. J. Biol. Chem. 2004, 279:54952-54962.
41. Mosimann M., Goshima S., Wenzler T., Lüscher A., Uozumi N., Mäser P. A Trk/HKT-type K+ transporter from Trypanosoma brucei. Eukaryot. Cell 2010, 9:539-546.
42. Munro A.W., Ritchie G.Y., Lamb A.J., Douglas R.M., Booth I.R. The cloning and DNA sequence of the gene for the glutathione-regulated potassium-efflux system KefC of Escherichia coli. Mol. Microbiol. 1991, 5:516-607.
43. Nakamura T., Yuda R., Unemoto T., Bakker E.P. KtrAB, a new type of bacterial K(+)-uptake system from Vibrio alginolyticus. J. Bacteriol. 1998, 180:3491-3494.
44. Nissen P., Hansen J., Ban N., Moore P.B., Steitz T.A. The structural basis of ribosome activity in peptide bond synthesis. Science 2000, 289:920-930.
45. Parfenova L.V., Abarca-Heidemann K., Crane B.M., Rothberg B.S. Molecular architecture and divalent cation activation of TvoK, a prokaryotic potassium channel. J. Biol. Chem. 2007, 282:24302-24309.
46. Rhoads D.B., Waters F.B., Epstein W. Cation transport in Escherichia coli. VIII. Potassium transport mutants. J. Gen. Physiol. 1976, 67:325-341.
47. Roosild T.P., Miller S., Booth I.R., Choe S. A mechanism of regulating transmembrane potassium flux through a ligand-mediated conformational switch. Cell 2002, 109:781-791.
48. Roosild T.P., Castronovo S., Miller S., Li C., Rasmussen T., Bartlett W., Gunasekera B., Choe S., Booth I.R. KTN (RCK) domains regulate K+ channels and transporters by controlling the dimer-hinge conformation. Structure 2009, 17:893-903.
49. Rubio F., Gassmann W., Schroeder J.I. Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 1995, 270:1660-1663.
50. Schachtman D.P., Schroeder J.I. Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants. Nature 1994, 370:655-658.
51. Schlösser A., Kluttig S., Hamann A., Bakker E.P. Subcloning, nucleotide sequence, and expression of trkG, a gene that encodes an integral membrane protein involved in potassium uptake via the Trk system of Escherichia coli. J. Bacteriol. 1991, 173:3170-3176.
52. Schlösser A., Hamann A., Bossemeyer D., Schneider E., Bakker E.P. NAD+ binding to the Escherichia coli K(+)-uptake protein TrkA and sequence similarity between TrkA and domains of a family of dehydrogenases suggest a role for NAD+ in bacterial transport. Mol. Microbiol. 1993, 9:533-543.
53. Schlösser A., Meldorf M., Stumpe S., Bakker E.P., Epstein W. TrkH and its homolog, TrkG, determine the specificity and kinetics of cation transport by the Trk system of Escherichia coli. J. Bacteriol. 1995, 177:1908-1910.
54. Schrempf H., Schmidt O., Kümmerlen R., Hinnah S., Müller D., Betzler M., Steinkamp T., Wagner R. A prokaryotic potassium ion channel with two predicted transmembrane segments from Streptomyces lividans. EMBO J. 1995, 14:5170-5178.
55. Strahl H., Greie J.C. The extremely halophilic archaeon Halobacterium salinarum R1 responds to potassium limitation by expression of the K+-transporting KdpFABC P-type ATPase and by a decrease in intracellular K+. Extremophiles 2008, 12:741-752.
56. Stumpe S., Schlösser A., Schleyer M., Bakker E.P. K+ circulation across the prokaryotic cell membrane: K+-uptake systems. Handbook of Biological Physics: Transport Processes In Eukaryotic and Prokaryotic Organisms 1996, Elsevier Science B.V., Amsterdam. W.N. Konings, H.R. Kaback, J.S. Lolkema (Eds.).
57. Takase K., Kakinuma S., Yamato I., Konishi K., Igarashi K., Kakinuma Y. Sequencing and characterization of the ntp gene cluster for vacuolar-type Na(+)-translocating ATPase of Enterococcus hirae. J. Biol. Chem. 1994, 269:11037-11044.
58. Tholema, N., 2002. Ph.D. Thesis. University of Osnabrück.
59. Tholema N., Bakker E.P., Suzuki A., Nakamura T. 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. 1999, 450:217-220.
60. Tholema N., Vor der Brüggen M., Mäser P., Nakamura T., Schroeder J.I., Kobayashi H., Uozumi N., Bakker E.P. All four putative selectivity filter glycine residues in KtrB are essential for high affinity and selective K+ uptake by the KtrAB system from Vibrio alginolyticus. J. Biol. Chem. 2005, 280:41146-41154.
61. Uozumi N., Kim E.J., Rubio F., Yamaguchi T., Muto S., Tsuboi A., Bakker E.P., Nakamura T., Schroeder J.I. The Arabidopsis HKT1 gene homolog mediates inward Na(+) currents in Xenopus laevis oocytes and Na(+) uptake in Saccharomyces cerevisiae. Plant Physiol. 2000, 122:1249-1259.
62. Wierenga R.K., Terpstra P., Hol W.G. Prediction of the occurrence of the ADP-binding beta alpha beta-fold in proteins, using an amino acid sequence fingerprint. J. Mol. Biol. 1986, 187:101-107.
63. Zeng G.F., Pypaert M., Slayman C.L. Epitope tagging of the yeast K(+) carrier Trk2p demonstrates folding that is consistent with a channel-like structure. J. Biol. Chem. 2004, 279:3003-3010.
64. Zhou Y., Morais-Cabral J.H., Kaufman A., MacKinnon R. Chemistry of ion coordination and hydration revealed by a K+ channel-Fab complex at 2.0A resolution. Nature 2001, 414:43-48.
65. Zulkifli L., Akai M., Yoshikawa A., Shimojima M., Ohta H., Guy H.R., Uozumi N. The KtrA and KtrE subunits are required for Na+-dependent K+ uptake by KtrB across the plasma membrane in Synechocystis sp. strain PCC 6803. J. Bacteriol. 2010, 192:5063-5070.