Individual subunits of the glutamate transporter EAAC1 homotrimer function independently of each other

Biochemistry

Volumn 44, Issue 35, 2005, Pages 11913-11923

  Grewer, Christof ^a   Balani, Poonam ^b   Weidenfeller, Christian ^b   Bartusel, Thorsten ^b   Tao, Zhen ^a   Rauen, Thomas ^c  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; NEGATIVE IONS; PH EFFECTS;

ANION PERMEATION; HOMOTRIMER;

MECHANICAL PERMEABILITY;

ALANINE; AMINO ACID; CYSTEINE; EXCITATORY AMINO ACID TRANSPORTER; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; GLUTAMINE;

AMINO ACID TRANSPORT; ARTICLE; CATALYSIS; CELL STRAIN HEK293; CONCENTRATION RESPONSE; CROSS LINKING; EMBRYO; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MEMBRANE POTENTIAL; MEMBRANE VESICLE; NEUROTRANSMISSION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; WESTERN BLOTTING;

ALANINE; AMINO ACID SUBSTITUTION; ANIMALS; ASPARTIC ACID; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID TRANSPORTER 3; GLUTAMIC ACID; GLUTAMINE; HUMANS; MUTAGENESIS, SITE-DIRECTED; PROTEIN SUBUNITS; RATS;

EID: 24344507684     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi050987n     Document Type: Article

References (41)

1. 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.
2. Zerangue, N., and Kavanaugh, M. P. (1996) Flux coupling in a neuronal glutamate transporter. Nature 383, 634-637.
3. Wadiche, J. I., Amara, S. G., and Kavanaugh, M. P. (1995) Ion fluxes associated with excitatory amino acid transport, Neuron 15, 721-728.
4. Ryan, R. M., Mitrovic, A. D., and Vandenberg, R. J. (2004) The chloride permeation pathway of a glutamate transporter and its proximity to the glutamate translocation pathway, J. Biol. Chem. 24, 24.
5. Slotboom, D. J., Konings, W. N., and Lolkema, J. S. (2001) Glutamate transporters combine transporter- and channel-like features, Trends Biochem. Sci. 26, 534-539.
6. Broer, A., Brookes, N., Ganapathy, V., Dimmer, K. S., Wagner, C. A., Lang, F., and Broer, S. (1999) The astroglial ASCT2 amino acid transporter as a mediator of glutamine efflux, J. Neurochem. 73, 2184-2194.
7. Zerangue, N., and Kavanaugh, M. P. (1996) ASCT-1 is a neutral amino acid exchanger with chloride channel activity, J. Biol. Chem. 271, 27991-27994.
8. Finan, T. M., Oresnik, I., and Bottacin, A. (1988) Mutants of Rhizobium meliloti defective in succinate metabolism, J. Bacteriol. 170, 3396-3403.
9. Finan, T. M., Wood, J. M., and Jordan, D. C. (1981) Succinate transport in Rhizobium leguminosarum, J. Bacteriol. 148, 193-202.
10. Brocke, L., Bendahan, A., Grunewald, M., and Kanner, B. I. (2002) Proximity of two oppositely oriented reentrant loops in the glutamate transporter GLT-1 identified by paired cysteine mutagenesis, J. Biol. Chem. 277, 3985-3992.
11. Grunewald, M., Bendahan, A., and Kanner, B. I. (1998) Biotinylation of single cysteine mutants of the glutamate transporter GLT-1 from rat brain reveals its unusual topology, Neuron 21, 623-632.
12. Slotboom, D. J., Lolkema, J. S., and Konings, W. N. (1996) Membrane topology of the C-terminal half of the neuronal, glial, and bacterial glutamate transporter family, J. Biol. Chem. 271, 31317-31321.
13. Slotboom, D. J., Sobczak, I., Konings, W. N., and Lolkema, J. S. (1999) A conserved serine-rich stretch in the glutamate transporter family forms a substrate-sensitive reentrant loop, Proc. Natl. Acad. Sci. U.S.A. 96, 14282-14287.
14. Yernool, D., Boudker, O., Jin, Y., and Gouaux, E. (2004) Structure of a glutamate transporter homologue from Pyrococcus horikoshii, Nature 431, 811-818.
15. Haugeto, O., Ullensvang, K., Levy, L. M., Chaudhry, F. A., Honore, T., Nielsen, M., Lehre, K. P., and Danbolt, N. C. (1996) Brain glutamate transporter proteins form homomultimers, J. Biol. Chem. 271, 27715-27722.
16. Eskandari, S., Kreman, M., Kavanaugh, M. P., Wright, E. M., and Zampighi, G. A. (2000) Pentameric assembly of a neuronal glutamate transporter, Proc. Natl. Acad. Sci. U.S.A. 97, 8641-8646.
17. Gendreau, S., Voswinkel, S., Torres-Salazar, D., Lang, N., Heidtmann, H., Detro-Dassen, S., Schmalzing, G., Hidalgo, P., and Fahlke, C. (2004) A trimeric quatemary structure is conserved in bacterial and human glutamate transporters, J. Biol. Chem. 279, 39505-39512.
18. Bendahan, A., Armon, A., Madani, N., Kavanaugh, M. P., and Kanner, B. I. (2000) Arginine 447 plays a pivotal role in substrate interactions in a neuronal glutamate transporter, J. Biol. Chem. 275, 37436-37442.
19. Grewer, C., Watzke, N., Wiessner, M., and Rauen, T. (2000) Glutamate translocation of the neuronal glutamate transporter EAAC1 occurs within milliseconds, Proc. Natl. Acad. Sci. U.S.A. 97, 9706-9711.
20. Chen, C., and Okayama, H. (1987) High-efficiency transformation of mammalian cells by plasmid DNA, Mol. Cell. Biol. 7, 2745-2752.
21. Grewer, C., Watzke, N., Rauen, T., and Bicho, A. (2003) Is the glutamate residue Glu-373 the proton acceptor of the excitatory amino acid carrier 1? J. Biol. Chem. 278, 2585-2592.
22. Rauen, T., Rothstein, J. D., and Wassle, H. (1996) Differential expression of three glutamate transporter subtypes in the rat retina, Cell Tissue Res. 286, 325-336.
23. Hamill, O. P., Marty, A., Neher, E., Sakmann, B., and Sigworth, F. J. (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches, Pflugers Arch. Eur. J. Physiol. 391, 85-100.
24. Watzke, N., Bamberg, E., and Grewer, C. (2001) Early intermediates in the transport cycle of the neuronal excitatory amino acid carrier EAAC1, J. Gen. Physiol. 117, 547-562.
25. Bergles, D. E., and Jahr, C. E. (1997) Synaptic activation of glutamate transporters in hippocampal astrocytes, Neuron 19, 1297-1308.
26. Watzke, N., Rauen, T., Bamberg, E., and Grewer, C. (2000) On the mechanism of proton transport by the neuronal excitatory amino acid carrier 1, J. Gen. Physiol. 116, 609-622.
27. Bergles, D. E., Tzingounis, A. V., and Jahr, C. E. (2002) Comparison of coupled and uncoupled currents during glutamate uptake by GLT-1 transporters, J. Neurosci. 22, 10153-10162.
28. Otis, T. S., and Jahr, C. E. (1998) Anion currents and predicted glutamate flux through a neuronal glutamate transporter, J. Neurosci. 18, 7099-7110.
29. Wadiche, J. I., and Kavanaugh, M. P. (1998) Macroscopic and microscopic properties of a cloned glutamate transporter/chloride channel, J. Neurosci. 18, 7650-7661.
30. 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. Pharm. 53, 195-201.
31. Campiani, G., De Angelis, M., Armaroli, S., Fattorusso, C., Catalanotti, B., Ramunno, A., Nacci, V., Novellino, E., Grewer, C., Ionescu, D., Rauen, T., Griffiths, R., Sinclair, C., Fumagalli, E., and Mennini, T. (2001) A rational approach to the design of selective substrates and potent nontransportable inhibitors of the excitatory amino acid transporter EAAC1 (EAAT3). New glutamate and aspartate analogues as potential neuroprotective agents, J. Med. Chem. 44, 2507-2510.
32. +-dependent anion leak, J. Physiol. 557, 747-759.
33. Tao, Z., and Grewer, C. (2005) The conserved histidine 295 does not contribute to proton cotransport by the glutamate transporter EAAC1, Biochemistry 44, 3466-3476.
34. +)-coupled glutamate transporter from rat brain, J. Biol. Chem. 270, 17093-17097.
35. 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.
36. Schwartz, E. A., and Tachibana, M. (1990) Electrophysiology of glutamate and sodium co-transport in a glial cell of the salamander retina, J. Physiol. 426, 43-80.
37. +-dependent glutamate transporter GLAST-1 by site-directed mutagenesis, J. Biol. Chem. 270, 25207-25212.
38. Kanai, Y., Nussberger, S., Romero, M. F., Boron, W. F., Hebert, S. C., and Hediger, M. A. (1995) Electrogenic properties of the epithelial and neuronal high affinity glutamate transporter, J. Biol. Chem. 270, 16561-16568.
39. Billups, B., and Attwell, D. (1996) Modulation of non-vesicular glutamate release by pH, Nature 379, 171-174.
40. Grewer, C., and Rauen, T. (2005) Electrogenic glutamate transport in the CNS: Molecular mechanism, pre-steady-state kinetics, and their impact on synaptic signaling, J. Membr. Biol. 203, 1-20.
41. Koch, H. P., and Larsson, H. P. (2005) Small-scale molecular motions accomplish glutamate uptake in human glutamate transporters, J. Neurosci. 25, 1730-1736.