Defining membrane spanning domains and crucial membrane-localized acidic amino acid residues for K+ transport of a Kup/HAK/KT-type Escherichia coli potassium transporter

Journal of Biochemistry

Volumn 155, Issue 5, 2014, Pages 315-323

  Sato, Yoko ^a   Nanatani, Kei ^a   Hamamoto, Shin ^a   Shimizu, Makoto ^a   Takahashi, Miho ^a   Tabuchi Kobayashi, Mayumi ^a   Mizutani, Akifumi ^b   Schroeder, Julian I ^c   Souma, Satoshi ^a   Uozumi, Nobuyuki ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b OKAYAMA UNIVERSITY   (Japan)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

acidic amino acid residues; Escherichia coli; Kup; potassium; topology

Indexed keywords

AMINO ACID; BACTERIAL PROTEIN; CYSTEINE; KUP HAK KT PROTEIN; POTASSIUM; SERINE; UNCLASSIFIED DRUG; ESCHERICHIA COLI PROTEIN; HISTIDINE; KUP PROTEIN, E COLI;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; MEMBRANE STRUCTURE; NONHUMAN; PH; POTASSIUM TRANSPORT; PROTEIN ANALYSIS; PROTEIN DOMAIN; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CELL MEMBRANE; CHEMISTRY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; TRANSPORT AT THE CELLULAR LEVEL;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BIOLOGICAL TRANSPORT; CELL MEMBRANE; CYSTEINE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HISTIDINE; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; POTASSIUM; PROTEIN STRUCTURE, TERTIARY; SERINE;

EID: 84899834827     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvu007     Document Type: Article

References (53)

1. Epstein, W. and Kim, B.S. (1971) Potassium transport loci in Escherichia coli K-12. J. Bacteriol. 108, 639-644
2. Haupt, M., Bramkamp, M., Coles, M., Kessler, H., and Altendorf, K. (2005) Prokaryotic Kdp-ATPase: recent insights into the structure and function of KdpB. J. Mol. Microbiol. Biotechnol. 10, 120-131
3. Hu, G.B., Rice, W.J., Drose, S., Altendorf, K., and Stokes, D.L. (2008) Three-dimensional structure of the KdpFABC complex of Escherichia coli by electron tomography of two-dimensional crystals. J. Struct. Biol. 161, 411-418
4. Schleyer, M. and Bakker, E.P. (1993) Nucleotide sequence and 30-end deletion studies indicate that the K-uptake protein kup from Escherichia coli is composed of a hydrophobic core linked to a large and partially essential hydrophilic C terminus. J. Bacteriol. 175, 6925-6931
5. Banuelos, M.A., Klein, R.D., Alexander-Bowman, S.J., and Rodrguez-Navarro, A. (1995) A potassium transporter of the yeast Schwanniomyces occidentalis homologous to the Kup system of Escherichia coli has a high concentrative capacity. EMBO J. 14, 3021-3027
6. Quintero, F.J. and Blatt, M.R. (1997) A new family of K transporters from Arabidopsis that are conserved across phyla. FEBS Lett. 415, 206-211
7. Santa-Mara, G.E., Rubio, F., Dubcovsky, J., and Rodrguez-Navarro, A. (1997) The HAK1 gene of barley is a member of a large gene family and encodes a high-affinity potassium transporter. Plant Cell. 9, 2281-2289
8. Fu, H.H. and Luan, S. (1998) AtKuP1: a dual-affinity K transporter from Arabidopsis. Plant Cell. 10, 63-73
9. Kim, E.J., Kwak, J.M., Uozumi, N., and Schroeder, J.I. (1998) AtKUP1: an Arabidopsis gene encoding highaffinity potassium transport activity. Plant Cell 10, 51-62
10. Bossemeyer, D., Schlosser, A., and Bakker, E.P. (1989) Specific cesium transport via the Escherichia coli Kup (TrkD) K uptake system. J. Bacteriol. 171, 2219-2221
11. Qi, Z., Hampton, C.R., Shin, R., Barkla, B.J., White, P.J., and Schachtman, D.P. (2008) The high affinity K transporter AtHAK5 plays a physiological role in planta at very low K concentrations and provides a caesium uptake pathway in Arabidopsis. J. Exp. Bot. 59, 595-607
12. Kobayashi, D., Uozumi, N., Hisamatsu, S., and Yamagami, M. (2010) AtKUP/HAK/KT9, a K transporter from Arabidopsis thaliana, mediates Cs uptake in Escherichia coli. Biosci. Biotechnol. Biochem. 74, 203-205
13. Rigas, S., Debrosses, G., Haralampidis, K., Vicente- Agullo, F., Feldmann, K.A., Grabov, A., Dolan, L., and Hatzopoulos, P. (2001) TRH1 encodes a potassium transporter required for tip growth in Arabidopsis root hairs. Plant Cell 13, 139-151
14. Gierth, M., Maser, P., and Schroeder, J.I. (2005) The potassium transporter AtHAK5 functions in K deprivation- induced high-affinity K uptake and AKT1 K channel contribution to K uptake kinetics in Arabidopsis roots. Plant Physiol. 137, 1105-1114
15. Gierth, M. and Maser, P. (2007) Potassium transporters in plants-involvement in K acquisition, redistribution and homeostasis. FEBS Lett. 581, 2348-2356
16. Rubio, F., Nieves-Cordones, M., Aleman, F., and Martinez, V. (2008) Relative contribution of AtHAK5 and AtAKT1 to K uptake in the high-affinity range of concentrations. Physiol. Plant. 134, 598-608
17. Pyo, Y.J., Gierth, M., Schroeder, J.I., and Cho, M.H. (2010) High-affinity K transport in Arabidopsis: AtHAK5 and AKT1 are vital for seedling establishment and postgermination growth under low-potassium conditions. Plant Physiol. 153, 863-875
18. Rubio, F., Aleman, F., Nieves-Cordones, M., and Martinez, V. (2010) Studies on Arabidopsis athak5, atakt1 double mutants disclose the range of concentrations at which AtHAK5, AtAKT1 and unknown systems mediate K uptake. Physiol. Plant 139, 220-228
19. Ward, J.M., Maser, P., and Schroeder, J.I. (2009) Plant ion channels: gene families, physiology, and functional genomics analyses. Annu. Rev. Physiol. 71, 59-82
20. Aleman, F., Nieves-Cordones, M., Martinez, V., and Rubio, F. (2011) Root K acquisition in plants: the Arabidopsis thaliana model. Plant Cell Physiol. 52, 1603-1612
21. Ahn, S.J., Shin, R., and Schachtman, D.P. (2004) Expression of KT/KUP genes in Arabidopsis and the role of root hairs in K uptake. Plant Physiol. 134, 1135-1145
22. Gambale, F. and Uozumi, N. (2006) Properties of shaker-type potassium channels in higher plants. J. Membr. Biol. 210, 1-19
23. Kato, N., Akai, M., Zulkifli, L., Matsuda, N., Kato, Y., Goshima, S., Hazama, A., Yamagami, M., Guy, H.R., and Uozumi, N. (2007) Role of positively charged amino acids in the M2D transmembrane helix of Ktr/ Trk/HKT type cation transporters. Channels (Austin) 1, 161-171
24. Tholema, N., Vor der Bruggen, M., Maser, P., Nakamura, T., Schroeder, J.I., Kobayashi, H., Uozumi, N., and Bakker, E.P. (2005) 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. 280, 41146-41154
25. Durell, S.R., Bakker, E.P., and Guy, H.R. (2000) 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. 78, 188-199
26. Durell, S.R. and Guy, H.R. (1999) Structural models of the KtrB, TrkH, and Trk1,2 symporters based on the structure of the KcsA K channel. Biophys. J. 77, 789-807
27. Durell, S.R., Hao, Y., Nakamura, T., Bakker, E.P., and Guy, H.R. (1999) Evolutionary relationship between K channels and symporters. Biophys. J. 77, 775-788
28. Maser, P., Hosoo, Y., Goshima, S., Horie, T., Eckelman, B., Yamada, K., Yoshida, K., Bakker, E.P., Shinmyo, A., Oiki, S., Schroeder, J.I., and Uozumi, N. (2002) Glycine residues in potassium channel-like selectivity filters determine potassium selectivity in four-loop-persubunit HKT transporters from plants. Proc. Natl Acad. Sci. U. S. A. 99, 6428-6433
29. Uozumi, N., and Deryer, I. (2012) Structure-function correlates in plant ion channels in Comprehensive Biophysics-Channel Proteins (Egelman, E., ed.) Vol. 6, pp. 234-245, Elsevier BV, Amsterdam
30. Manoil, C. (1991) Analysis of membrane protein topology using alkaline phosphatase and beta-galactosidase gene fusions. Methods Cell. Biol. 34, 61-75
31. Henn, D.K., Baumann, A., and Kaupp, U.B. (1995) Probing the transmembrane topology of cyclic nucleotide- gated ion channels with a gene fusion approach. Proc. Natl Acad. Sci. U. S. A. 92, 7425-7429
32. Uozumi, N., Nakamura, T., Schroeder, J.I., and Muto, S. (1998) Determination of transmembrane topology of an inward-rectifying potassium channel from Arabidopsis thaliana based on functional expression in Escherichia coli. Proc. Natl Acad. Sci. U. S. A. 95, 9773-9778
33. Kato, Y., Sakaguchi, M., Mori, Y., Saito, K., Nakamura, T., Bakker, E.P., Sato, Y., Goshima, S., and 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
34. Grabov, A. (2007) Plant KT/KUP/HAK potassium transporters: single family-multiple functions. Ann. Bot. 99, 1035-1041
35. Trchounian, A. and Kobayashi, H. (1999) Kup is the major K uptake system in Escherichia coli upon hyperosmotic stress at a low pH. FEBS Lett. 447, 144-148
36. Rodriguez-Navarro, A. (2000) Potassium transport in fungi and plants. Biochim. Biophys. Acta. 1469, 1-30
37. Bibi, E., Gros, P., and Kaback, H.R. (1993) Functional expression of mouse mdr1 in Escherichia coli. Proc. Natl Acad. Sci. U. S. A. 90, 9209-9213
38. Enomoto, H., Unemoto, T., Nishibuchi, M., Padan, E., and Nakamura, T. (1998) Topological study of Vibrio alginolyticus NhaB Na/H antiporter using gene fusions in Escherichia coli cells. Biochim. Biophys. Acta. 1370, 77-86
39. Brickman, E. and Beckwith, J. (1975) Analysis of the regulation of Escherichia coli alkaline phosphatase synthesis using deletions and phi80 transducing phages. J. Mol. Biol. 96, 307-316
40. Stumpe, S. and Bakker, E.P. (1997) Requirement of a large K-uptake capacity and of extracytoplasmic protease activity for protamine resistance of Escherichia coli. Arch. Microbiol. 167, 126-136
41. Matsuda, N., Kobayashi, H., Katoh, H., Ogawa, T., Futatsugi, L., Nakamura, T., Bakker, E.P., and Uozumi, N. (2004) 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. 279, 54952-54962
42. Kyte, J. and Doolittle, R.F. (1982) A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105-132
43. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E.L. (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567-580
44. Manoil, C., Boyd, D., and Beckwith, J. (1988) Molecular genetic analysis of membrane protein topology. Trends Genet. 4, 223-226
45. Zimmann, P., Puppe, W., and Altendorf, K. (1995) Membrane topology analysis of the sensor kinase KdpD of Escherichia coli. J. Biol. Chem. 270, 28282-28288
46. Hoth, S., Dreyer, I., Dietrich, P., Becker, D., Muller- Rober, B., and Hedrich, R. (1997) Molecular basis of plant-specific acid activation of K uptake channels. Proc. Natl Acad. Sci. U. S. A. 94, 4806-4810
47. Zulkifli, L. and Uozumi, N. (2006) Mutation of His-157 in the second pore loop drastically reduces the activity of the Synechocystis Ktr-type transporter. J. Bacteriol. 188, 7985-7987
48. Zhang, X.H. and Wright, S.H. (2006) Alanine-scanning mutations of negatively charged amino acid residues of rabbit organic cation transporter 2 (rbOCT2) revealed an important residue (Glu284) for substrate recognition. Faseb J. 20, A1239-A1239
49. Edgar, R. and Bibi, E. (1999) A single membraneembedded negative charge is critical for recognizing positively charged drugs by the Escherichia coli multidrug resistance protein MdfA. EMBO J. 18, 822-832
50. Nakamura, T., Fujisaki, Y., Enomoto, H., Nakayama, Y., Takabe, T., Yamaguchi, N., and Uozumi, N. (2001) Residue aspartate-147 from the third transmembrane region of Na/H antiporter NhaB of Vibrio alginolyticus plays a role in its activity. J. Bacteriol. 183, 5762-5767
51. Ben-Yona, A. and Kanner, B.I. (2012) An acidic amino acid transmembrane helix 10 residue conserved in the neurotransmitter:sodium:symporters is essential for the formation of the extracellular gate of the gammaaminobutyric acid (GABA) transporter GAT-1. J. Biol. Chem. 287, 7159-7168
52. Buurman, E.T., Kim, K.T., and Epstein, W. (1995) Genetic evidence for two sequentially occupied K binding sites in the Kdp transport ATPase. J. Biol. Chem. 270, 6678-6685
53. Tholema, N., Bakker, E.P., Suzuki, A., and 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