Structure and function of prokaryotic glutamate transporters from Escherichia coli and Pyrococcus horikoshii

Biochemistry

Volumn 45, Issue 42, 2006, Pages 12796-12805

  Raunser, Stefan ^a   Appel, Matthias ^a   Ganea, Constanta ^a,b   Geldmacher Kaufer, Ulrike ^a   Fendler, Klaus ^a   Kühlbrandt, Werner ^a,b  

^a MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^b CAROL DAVILA UNIVERSITY OF MEDICINE AND PHARMACY   (Romania)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELL MEMBRANES; CRYSTALS; ELECTRON MICROSCOPY; ESCHERICHIA COLI; GELS; OLIGOMERS;

GLUTAMATE TRANSPORTERS; HALF-SATURATION CONCENTRATION; TRIMER; TWO-DIMENSIONAL CRYSTALS;

BIOCHEMISTRY;

ASPARTIC ACID; GLUTAMATE TRANSPORTER; GLUTAMIC ACID;

AMINO ACID TRANSPORT; ARTICLE; ELECTRON MICROSCOPY; ESCHERICHIA COLI; GEL ELECTROPHORESIS; GEL FILTRATION; IMAGE PROCESSING; MOLECULAR CLONING; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; PROTEOLIPOSOME; PYROCOCCUS HORIKOSHII;

ESCHERICHIA COLI; PROKARYOTA; PYROCOCCUS HORIKOSHII;

EID: 33750360302     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061008+     Document Type: Article

References (49)

1. Headley, P. M., and Grillner, S. (1990) Excitatory amino acids and synaptic transmission: The evidence for a physiological function, Trends Pharmacol. Sci. 11, 205-211.
2. +-dependent glutamate/aspartate transporter from rat brain, Proc. Natl. Acad. Sci. U.S.A. 89, 10955-10959.
3. Pines, G., Danbolt, N. C., Bjoras, M., Zhang, Y., Bendahan, A., Eide, L., Koepsell, H., Storm-Mathisen, J., Seeberg, E., and Kanner, B. I. (1992) Cloning and expression of a rat brain L-glutamate transporter, Nature 360, 464-467
4. [comment erratum, (1992) Nature 360 (6406), 768;
5. comment, (1992) Nature 360 (6403), 420-421].
6. Kanai, Y., and Hediger, M. A. (1992) Primary structure and functional characterization of a high-affinity glutamate transporter, Nature 360, 467-471.
7. Fairman, W. A., Vandenberg, R. J., Arriza, J. L., Kavanaugh, M. P., and Amara, S. G. (1995) An excitatory amino-acid transporter with properties of a ligand-gated chloride channel, Nature 375, 599-603.
8. Arriza, J. L., Eliasof, S., Kavanaugh, M. P., and Amara, S. G. (1997) Excitatory amino acid transporter 5, a retinal glutamate transporter coupled to a chloride conductance, Proc. Natl. Acad. Sci. U.S.A. 94, 4155-4160.
9. Kanner, B. I., and Bendahan, A. (1982) Binding order of substrates to the sodium and potassium ion coupled L-glutamic acid transporter from rat brain, Biochemistry 21, 6327-6330.
10. Pines, G., and Kanner, B. I. (1990) Counterflow of L-glutamate in plasma membrane vesicles and reconstituted preparations from rat brain, Biochemistry 29, 11209-11214.
11. Kavanaugh, M. P., Bendahan, A., Zerangue, N., Zhang, Y., and Kanner, B. I. (1997) Mutation of an amino acid residue influencing potassium coupling in the glutamate transporter GLT-1 induces obligate exchange, J. Biol. Chem. 272, 1703-1708.
12. Halpern, Y. S. M. L. (1965) Glutamate transport in wild-type and mutant strains of Escherichia coli, J. Bacteriol. 90, 1288-1295.
13. Casadaban, M. J., Chou, J., and Cohen, S. N. (1980) In vitro gene fusions that join an enzymatically active β-galactosidase segment to amino-terminal fragments of exogenous proteins: Escherichia coli plasmid vectors for the detection and cloning of translational initiation signals, J. Bacteriol. 143, 971-980.
14. Halpern, Y. S., Barash, H., Dover, S., and Druck, K. (1973) Sodium and potassium requirements for active transport of glutamate by Escherichia coli K-12, J. Bacteriol. 114, 53-58.
15. Halpern, Y. S., Barash, H., and Druck, K. (1973) Glutamate transport in Escherichia coli K-12: Nonidentity of carriers mediating entry and exit, J. Bacteriol. 113, 51-57.
16. Miner, K. M., and Frank, L. (1974) Sodium-stimulated glutamate transport in osmotically shocked cells and membrane vesicles of Escherichia coli, J. Bacteriol. 117, 1093-1098.
17. Schellenberg, G. D., and Furlong, C. E. (1977) Resolution of the multiplicity of the glutamate and aspartate transport systems of Escherichia coli, J. Biol. Chem. 252, 9055-9064.
18. Tolner, B., Ubbink-Kok, T., Poolman, B., and Konings, W. N. (1995) Cation-selectivity of the L-glutamate transporters of Escherichia coli, Bacillus stearothermophilus, and Bacillus caldotenax: Dependence on the environment in which the proteins are expressed, Mol. Microbiol. 18, 123-133.
19. Yernool, D., Boudker, O., Jin, Y., and Gouaux, E. (2004) Structure of a glutamate transporter homologue from Pyrococcus horikoshii, Nature 431, 811-818.
20. Yernool, D., Boudker, O., Folta-Stogniew, E., and Gouaux, E. (2003) Trimeric subunit stoichiometry of the glutamate transporters from Bacillus caldotenax and Bacillus stearothermophilus, Biochemistry 42, 12981-12988.
21. Raunser, S., Haase, W., Bostina, M., Parcej, D. N., and Kuhlbrandt, W. (2005) High-yield expression, reconstitution and structure of the recombinant, fully functional glutamate transporter GLT-1 from Rattus norvegicus, J. Mol. Biol. 351, 598-613.
22. Gendreau, S., Voswinkel, S., Torres-Salazar, D., Lang, N., Heidtmann, H., Detro-Dassen, S., Schmalzing, G., Hidalgo, P., and Fahlke, C. (2004) A trimeric quaternary structure is conserved in bacterial and human glutamate transporters, J. Biol. Chem. 279, 39505-39512.
23. Tolner, B., Poolman, B., Wallace, B., and Konings, W. N. (1992) Revised nucleotide sequence of the gltP gene, which encodes the proton-glutamate- aspartate transport protein of Escherichia coli K-12, J. Bacteriol. 174, 2391-2393.
24. Deguchi, Y., Yamato, I., and Anraku, Y. (1989) Molecular cloning of gltS and gltP, which encode glutamate carriers of Escherichia coli B, J. Bacteriol. 171, 1314-1319.
25. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning, A laboratory manual, 2nd ed., Cold Spring Harbor Laboratory Press, Plainview, NY.
26. +-ATPase investigated on solid supported membranes: Rapid solution exchange with a new technique, Biophys. J. 76, 814-826.
27. Ganea, C., Pourcher, T., Leblanc, G., and Fendler, K. (2001) Evidence for intraprotein charge transfer during the transport activity of the melibiose permease from Escherichia coli, Biochemistry 40, 13744-13752.
28. Bamberg, E., Alpes, H., Apell, H. J., Bradley, R., Harter, B., Quelle, M. J., and Urry, D. W. (1979) Formation of ionic channels in black lipid membranes by succinic derivatives of gramicidin A, J. Membr. Biol. 50, 257-270.
29. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem. 72, 248-254.
30. Schagger, H., Cramer, W. A., and von Jagow, G. (1994) Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis, Anal. Biochem. 217, 220-230.
31. Schagger, H., and von Jagow, G. (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form, Anal. Biochem. 199, 223-231.
32. Frank, J., Radermacher, M., Penczek, P., Zhu, J., Li, Y., Ladjadj, M., and Leith, A. (1996) SPIDER and WEB: Processing and visualization of images in 3D electron microscopy and related fields, J. Struct. Biol. 116, 190-199.
33. Radermacher, M., Wagenknecht, T., Verschoor, A., and Frank, J. (1987) Three-dimensional reconstruction from a single-exposure, random conical tilt series applied to the 50S ribosomal subunit of Escherichia coli, J. Microsc. 146 (Part 2), 113-136.
34. Marco, S., Chagoyen, M., de la Fraga, L. G., and Carazo, J. M. (1996) A variant to the radon approximation of the reference-free alignment algorithm, Ultramicroscopy 66, 5-10.
35. Radermacher, M. (1997) Radon Transform Techniques for Alignment and Three-dimensional Reconstruction from Random Projections, Scanning Microsc. 11, 171-177.
36. 1-ATPase determined by three-dimensional electron microscopy of single particles, J. Struct. Biol. 135, 26-37.
37. Marabini, R., and Carazo, J. M. (1994) Pattern recognition and classification of images of biological macromolecules using artificial neural networks, Biophys. J. 66, 1804-1814.
38. Marabini, R., Masegosa, I. M., San Martin, M. C., Marco, S., Fernandez, J. J., de la Fraga, L. G., Vaquerizo, C., and Carazo, J. M. (1996) Xmipp: An Image Processing Package for Electron Microscopy, J. Struct. Biol. 116, 237-240.
39. Crowther, R. A., Henderson, R., and Smith, J. M. (1996) MRC image processing programs, J. Struct. Biol. 116, 9-16.
40. Henderson, R., Jubb, J. S., and Rossmann, M. G. (1982) A contracted form of the trigonal purple membrane of Halobacterium halobium, J. Mol. Biol. 154, 501-514.
41. Vinothkumar, K. R., Raunser, S., Jung, H., and Kuhlbrandt, W. (2006) Oligomeric structure of the carnitine transporter CaiT from Escherichia coli, J. Biol. Chem. 281, 4795-4801.
42. Heuberger, E. H., Veenhoff, L. M., Duurkens, R. H., Friesen, R. H., and Poolman, B. (2002) Oligomeric state of membrane transport proteins analyzed with blue native electrophoresis and analytical ultracentrifugation, J. Mol. Biol. 317, 591-600.
43. Valpuesta, J. M., Carrascosa, J. L., and Henderson, R. (1994) Analysis of electron microscope images and electron diffraction patterns of thin crystals of φ29 connectors in ice, J. Mol. Biol. 240, 281-287.
44. Shimamoto, K., Lebrun, B., Yasuda-Kamatani, Y., Sakaitani, M., Shigeri, Y., Yumoto, N., and Nakajima, T. (1998) DL-threo-β-Benzyloxyaspartate, a potent blocker of excitatory amino acid transporters, Mol. Pharmacol. 53, 195-201.
45. 3H]D-aspartate release by 3-hydroxy-4,5,6,6a- tetrahydro-3aH-pyrrolo[3,4-d]isoxazole-4-carboxylic acid and 3-hydroxy-4,5,6,6a-tetrahydro-3aH-pyrrolo[3,4-d]isoxazole-6-carboxylic acid, two conformationally constrained aspartate and glutamate analogs, Mol. Pharmacol. 66, 522-529.
46. Grewer, C., Balani, P., Weidenfeller, C., Bartusel, T., Tao, Z., and Rauen, T. (2005) Individual subunits of the glutamate transporter EAAC1 homotrimer function independently of each other, Biochemistry 44, 11913-11923.
47. Bessonneau, P., Besson, V., Collinson, I., and Duong, F. (2002) The SecYEG preprotein translocation channel is a conformationally dynamic and dimeric structure, EMBO J. 21, 995-1003.
48. Meyer-Lipp, K., Ganea, C., Pourcher, T., Leblanc, G., and Fendler, K. (2004) Sugar binding induced charge translocation in the melibiose permease from Escherichia coli, Biochemistry 43, 12606-12613.
49. Larsson, H. P., Tzingounis, A. V., Koch, H. P., and Kavanaugh, M. P. (2004) Fluorometric measurements of conformational changes in glutamate transporters, Proc. Natl. Acad. Sci. U.S.A. 101, 3951-3956.