A Trk/HKT-type K+ transporter from Trypanosoma brucei

Eukaryotic Cell

Volumn 9, Issue 4, 2010, Pages 539-546

  Mosimann, Marc ^a   Goshima, Shinobu ^b   Wenzler, Tanja ^c,d   Lüscher, Alexandra ^a   Uozumi, Nobuyuki ^b   Mäser, Pascal ^a,c,d  

^a UNIVERSITY OF BERN   (Switzerland)

^b TOHOKU UNIVERSITY   (Japan)

^c SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^d UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CATION TRANSPORT PROTEIN; HKT1 PROTEIN, TRYPANOSOMA BRUCEI; POTASSIUM; PROTOZOAL PROTEIN;

ANIMAL; ARTICLE; CELL LINE; CLASSIFICATION; CYTOLOGY; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; OOCYTE; PARASITOLOGY; PATCH CLAMP; PHENOTYPE; PHYLOGENY; PHYSIOLOGY; RNA INTERFERENCE; TRYPANOSOMA BRUCEI; TSETSE FLY; XENOPUS LAEVIS; GLOSSINIDAE; PATCH CLAMP TECHNIQUE; TRYPANOSOMA BRUCEI BRUCEI;

ANIMALS; CATION TRANSPORT PROTEINS; CELL LINE; HUMANS; MOLECULAR SEQUENCE DATA; OOCYTES; PATCH-CLAMP TECHNIQUES; PHENOTYPE; PHYLOGENY; POTASSIUM; PROTOZOAN PROTEINS; RNA INTERFERENCE; TRYPANOSOMA BRUCEI BRUCEI; TSETSE FLIES; XENOPUS LAEVIS;

ARCHAEA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA; FUNGI; GLOSSINA (GENUS); KINETOPLASTIDA; MAMMALIA; PROTOZOA; SACCHAROMYCES CEREVISIAE; TRYPANOSOMA; TRYPANOSOMA BRUCEI; TRYPANOSOMATIDAE; XENOPUS LAEVIS;

EID: 77950542177     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00314-09     Document Type: Article

References (56)

1. Allemann, N., and A. Schneider. 2000. ATP production in isolated mitochondria of procyclic Trypanosoma brucei. Mol. Biochem. Parasitol. 111: 87-94.
2. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
3. Barrett, M. P., D. W. Boykin, R. Brun, and R. R. Tidwell. 2007. Human African trypanosomiasis: pharmacological re-engagement with a neglected disease. Br. J. Pharmacol. 152:1155-1171.
4. Barrett, M. P., E. Tetaud, A. Seyfang, F. Bringaud, and T. Baltz. 1998. Trypanosome glucose transporters. Mol. Biochem. Parasitol. 91:195-205.
5. Benito, B., B. Garciadeblas, and A. Rodriguez-Navarro. 2002. Potassium- or sodium-efflux ATPase, a key enzyme in the evolution of fungi. Microbiology 148:933-941.
6. Berriman, M., E. Ghedin, C. Hertz-Fowler, G. Blandin, H. Renauld, D. C. Bartholomeu, N. J. Lennard, E. Caler, N. E. Hamlin, B. Haas, U. Bohme, L. Hannick, M. A. Aslett, J. Shallom, L. Marcello, L. Hou, B. Wickstead, U. C. Alsmark, C. Arrowsmith, R. J. Atkin, A. J. Barron, F. Bringaud, K. Brooks, M. Carrington, I. Cherevach, T. J. Chillingworth, C. Churcher, L. N. Clark, C. H. Corton, A. Cronin, R. M. Davies, J. Doggett, A. Djikeng, T. Feldblyum, M. C. Field, A. Fraser, I. Goodhead, Z. Hance, D. Harper, B. R. Harris, H. Hauser, J. Hostetler, A. Ivens, K. Jagels, D. Johnson, J. Johnson, K. Jones, A. X. Kerhornou, H. Koo, N. Larke, S. Landfear, C. Larkin, V. Leech, A. Line, A. Lord, A. Macleod, P. J. Mooney, S. Moule, D. M. Martin, G. W. Morgan, K. Mungall, H. Norbertczak, D. Ormond, G. Pai, C. S. Peacock, J. Peterson, M. A. Quail, E. Rabbinowitsch, M. A. Rajandream, C. Reitter, S. L. Salzberg, M. Sanders, S. Schobel, S. Sharp, M. Simmonds, A. J. Simpson, L. Tallon, C. M. Turner, A. Tait, A. R. Tivey, S. Van Aken, D. Walker, D. Wanless, S. Wang, B. White, O. White, S. Whitehead, J. Woodward, J. Wortman, M. D. Adams, T. M. Embley, K. Gull, E. Ullu, J. D. Barry, A. H. Fairlamb, F. Opperdoes, B. G. Barrell, J. E. Donelson, N. Hall, C. M. Fraser, S. E. Melville, and N. M. El-Sayed. 2005. The genome of the African trypanosome Trypanosoma brucei. Science 309:416-422.
7. Borst, P., and A. H. Fairlamb. 1998. Surface receptors and transporters of Trypanosoma brucei. Annu. Rev. Microbiol. 52:745-778.
8. Brun, R., J. Blum, F. Chappuis, and C. Burri. 2010. Human African trypanosomiasis. Lancet 375:148-159.
9. Brun, R., and M. Schönenberger. 1979. Cultivation and in vivo cloning of procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Acta Trop. 36:289-292.
10. Davenport, R. J., A. Munoz-Mayor, D. Jha, P. A. Essah, A. Rus, and M. Tester. 2007. The Na transporter AtHKT1;1 controls retrieval of Na from the xylem in Arabidopsis. Plant Cell Environ. 30:497-507.
11. Defrise-Quertain, F., C. Fraser-L'Hostis, D. Coral, and J. Deshusses. 1996. Kinetic study of the plasma-membrane potential in procyclic and bloodstream forms of Trypanosoma brucei brucei using the fluorescent probe bisoxonol. Biochem. J. 314:595-601.
12. de Koning, H. P., D. Bridges, and R. J. Burchmore. 2005. Purine and pyrimidine transport in pathogenic protozoa: from biology to therapy. FEMS Microbiol. Rev. 29:987-1020.
13. Doyle, D. A., J. Morais Cabral, R. A. Pfuetzner, A. Kuo, J. M. Gulbis, S. L. Cohen, B. T. Chait, and R. MacKinnon. 1998. The structure of the potassium channel: molecular basis of K conduction and selectivity. Science 280:69-77.
14. Durell, S. R., and H. R. Guy. 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.
15. Durell, S. R., Y. Hao, T. Nakamura, E. P. Bakker, and H. R. Guy. 1999. Evolutionary relationship between K() channels and symporters. Biophys. J. 77:775-788.
16. Eddy, S. R. 1995. Multiple alignment using hidden Markov models. Proc. Int. Conf. Intell. Syst. Mol. Biol. 3:114-120.
17. Eddy, S. R. 1998. Profile hidden Markov models. Bioinformatics 14:755-763.
18. Ellekvist, P., J. Maciel, G. Mlambo, C. H. Ricke, H. Colding, D. A. Klaerke, and N. Kumar. 2008. Critical role of a K channel in Plasmodium berghei transmission revealed by targeted gene disruption. Proc. Natl. Acad. Sci. U. S. A. 105:6398-6402.
19. Ellekvist, P., C. H. Ricke, T. Litman, A. Salanti, H. Colding, T. Zeuthen, and D. A. Klaerke. 2004. Molecular cloning of a K() channel from the malaria parasite Plasmodium falciparum. Biochem. Biophys. Res. Commun. 318: 477-484.
20. Gaber, R. F., C. A. Styles, and G. R. Fink. 1988. TRK1 encodes a plasma membrane protein required for high-affinity potassium transport in Saccharomyces cerevisiae. Mol. Cell. Biol. 8:2848-2859.
21. Gierth, M., and P. Mäser. 2007. Potassium transporters in plants-involvement in K acquisition, redistribution and homeostasis. FEBS Lett. 581: 2348-2356.
22. Hannaert, V., E. Saavedra, F. Duffieux, J. P. Szikora, D. J. Rigden, P. A. Michels, and F. R. Opperdoes. 2003. Plant-like traits associated with metabolism of Trypanosoma parasites. Proc. Natl. Acad. Sci. U. S. A. 100:1067-1071.
23. Harms, C., Y. Domoto, C. Celik, E. Rahe, S. Stumpe, R. Schmid, T. Nakamura, and E. P. Bakker. 2001. 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 147:2991-3003.
24. Hirumi, H., and K. Hirumi. 1989. Continuous cultivation of Trypanosoma brucei blood stream forms in a medium containing a low concentration of serum protein without feeder cell layers. J. Parasitol. 75:985-989.
25. Huson, D. H., D. C. Richter, C. Rausch, T. Dezulian, M. Franz, and R. Rupp. 2007. Dendroscope: an interactive viewer for large phylogenetic trees. BMC Bioinformatics 8:460.
26. Jackson, A. P. 2007. Origins of amino acid transporter loci in trypanosomatid parasites. BMC Evol. Biol. 7:26.
27. Kato, Y., M. Sakaguchi, Y. Mori, K. Saito, T. Nakamura, E. P. Bakker, Y. Sato, S. Goshima, and N. Uozumi. 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.
28. Kesteloot, H., and J. V. Joossens. 1988. Relationship of serum sodium, potassium, calcium, and phosphorus with blood pressure. Belgian Interuniv. Res. Nutr. Health Hypertens. 12:589-593.
29. Krogh, A., B. Larsson, G. von Heijne, and E. L. Sonnhammer. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305:567-580.
30. Landfear, S. M. 2008. Drugs and transporters in kinetoplastid protozoa. Adv. Exp. Med. Biol. 625:22-32.
31. Legros, D., G. Ollivier, M. Gastellu-Etchegorry, C. Paquet, C. Burri, J. Jannin, and P. Buscher. 2002. Treatment of human African trypanosomiasis-present situation and needs for research and development. Lancet Infect. Dis. 2:437-440.
32. Liu, W., D. J. Fairbairn, R. J. Reid, and D. P. Schachtman. 2001. Characterization of two HKT1 homologues from Eucalyptus camaldulensis that display intrinsic osmosensing capability. Plant Physiol. 127:283-294.
33. Mäser, P., B. Eckelman, R. Vaidyanathan, T. Horie, D. J. Fairbairn, M. Kubo, M. Yamagami, K. Yamaguchi, M. Nishimura, N. Uozumi, W. Robertson, M. R. Sussman, and J. I. Schroeder. 2002. Altered shoot/root Na distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na transporter AtHKT1. FEBS Lett. 531:157-161.
34. Mäser, P., Y. Hosoo, S. Goshima, T. Horie, B. Eckelman, K. Yamada, K. Yoshida, E. P. Bakker, A. Shinmyo, S. Oiki, J. I. Schroeder, and N. Uozumi. 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.
35. Mäser, P., A. Lüscher, and R. Kaminsky. 2003. Drug transport and drug resistance in African trypanosomes. Drug Resist. Updat. 6:281-290.
36. Nakamura, T., N. Yamamuro, S. Stumpe, T. Unemoto, and E. P. Bakker. 1998. Cloning of the trkAH gene cluster and characterization of the Trk K()-uptake system of Vibrio alginolyticus. Microbiology 144:2281-2289.
37. Nolan, D. P., and H. P. Voorheis. 2000. Factors that determine the plasmamembrane potential in bloodstream forms of Trypanosoma brucei. Eur. J. Biochem. 267:4615-4623.
38. Oberholzer, M., S. Morand, S. Kunz, and T. Seebeck. 2006. A vector series for rapid PCR-mediated C-terminal in situ tagging of Trypanosoma brucei genes. Mol. Biochem. Parasitol. 145:117-120.
39. Platten, J. D., O. Cotsaftis, P. Berthomieu, H. Bohnert, R. J. Davenport, D. J. Fairbairn, T. Horie, R. A. Leigh, H. X. Lin, S. Luan, P. Maser, O. Pantoja, A. Rodriguez-Navarro, D. P. Schachtman, J. I. Schroeder, H. Sentenac, N. Uozumi, A. A. Very, J. K. Zhu, E. S. Dennis, and M. Tester. 2006. Nomenclature for HKT transporters, key determinants of plant salinity tolerance. Trends Plant Sci. 11:372-374.
40. Räz, B., M. Iten, Y. Grether-Bühler, R. Kaminsky, and R. Brun. 1997. The Alamar Blue assay to determine drug sensitivity of African trypanosomes in vitro. Acta Trop. 68:139-147.
41. Rodriguez-Navarro, A., and J. Ramos. 1984. Dual system for potassium transport in Saccharomyces cerevisiae. J. Bacteriol. 159:940-945.
42. Rubio, F., W. Gassmann, and J. I. Schroeder. 1995. Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270:1660-1663.
43. Saier, M. H., Jr., C. V. Tran, and R. D. Barabote. 2006. TCDB: the Transporter Classification Database for membrane transport protein analyses and information. Nucleic Acids Res. 34:D181-D186.
44. Schachtman, D. P., and J. I. Schroeder. 1994. Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants. Nature 370:655-658.
45. Stiles, J. K., Z. Kucerova, B. Sarfo, C. A. Meade, W. Thompson, P. Shah, L. Xue, and J. C. Meade. 2003. Identification of surface-membrane P-type ATPases resembling fungal K()- and Na()-ATPases, in Trypanosoma brucei, Trypanosoma cruzi and Leishmania donovani. Ann. Trop. Med. Parasitol. 97:351-366.
46. Stumpe, S., and E. P. Bakker. 1997. Requirement of a large K -uptake capacity and of extracytoplasmic protease activity for protamine resistance of Escherichia coli. Arch. Microbiol. 167:126-136.
47. Sunarpi, T. Horie, J. Motoda, M. Kubo, H. Yang, K. Yoda, R. Horie, W. Y. Chan, H. Y. Leung, K. Hattori, M. Konomi, M. Osumi, M. Yamagami, J. I. Schroeder, and N. Uozumi. 2005. Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na unloading from xylem vessels to xylem parenchyma cells. Plant J. 44:928-938.
48. Tholema, N., E. P. Bakker, A. Suzuki, and T. Nakamura. 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.
49. Tholema, N., M. Vor der Bruggen, P. Maser, T. Nakamura, J. I. Schroeder, H. Kobayashi, N. Uozumi, and E. P. Bakker. 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.
50. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
51. Uozumi, N., E. J. Kim, F. Rubio, T. Yamaguchi, S. Muto, A. Tsuboi, E. P. Bakker, T. Nakamura, and J. I. Schroeder. 2000. The Arabidopsis HKT1 gene homolog mediates inward Na currents in Xenopus laevis oocytes and Na(+) uptake in Saccharomyces cerevisiae. Plant Physiol. 122:1249-1259.
52. Waller, K. L., S. M. McBride, K. Kim, and T. V. McDonald. 2008. Characterization of two putative potassium channels in Plasmodium falciparum. Malar. J. 7:19.
53. Ward, J. M., P. Maser, and J. I. Schroeder. 2009. Plant ion channels: gene families, physiology, and functional genomics analyses. Annu. Rev. Physiol. 71:59-82.
54. Wirtz, E., S. Leal, C. Ochatt, and G. A. Cross. 1999. A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol. Biochem. Parasitol. 99:89-101.
55. Zeng, G. F., M. Pypaert, and C. L. Slayman. 2004. Epitope tagging of the yeast K(+) carrier Trk2p demonstrates folding that is consistent with a channel-like structure. J. Biol. Chem. 279:3003-3013.
56. Zilberstein, D. 1993. Transport of nutrients and ions across membranes of trypanosomatid parasites. Adv. Parasitol. 32:261-291.