The uncoupled chloride conductance of a bacterial glutamate transporter homolog

Nature Structural and Molecular Biology

Volumn 14, Issue 5, 2007, Pages 365-371

  Ryan, Renae M ^a   Mindell, Joseph A ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; GLUTAMATE TRANSPORTER; MUTANT PROTEIN;

AMINO ACID TRANSPORT; ARTICLE; BACTERIUM; CHLORIDE CONDUCTANCE; MOLECULAR DYNAMICS; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; STRUCTURE ANALYSIS;

ASPARTIC ACID; BACTERIAL PROTEINS; CHLORINE; EVOLUTION, MOLECULAR; GLUTAMATE PLASMA MEMBRANE TRANSPORT PROTEINS; ION TRANSPORT; KINETICS; MUTATION; PERMEABILITY;

BACTERIA (MICROORGANISMS); MAMMALIA;

EID: 34247648737     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb1230     Document Type: Article

References (50)

1. Danbolt, N.C. Glutamate uptake. Prog. Neurobiol. 65, 1-105 (2001).
2. Slotboom, D.J., Konings, W.N. & Lolkema, J.S. Structural features of the glutamate transporter family. Microbiol. Mol. Biol. Rev. 63, 293-307 (1999).
3. Zerangue, N. & Kavanaugh, M.P. Flux coupling in a neuronal glutamate transporter. Nature 383, 634-637 (1996).
4. Veruki, M.L., Morkve, S.H. & Hartveit, E. Activation of a presynaptic glutamate transporter regulates synaptic transmission through electrical signaling. Nat. Neurosci. 9, 1388-1396 (2006).
5. Grant, G.B. & Dowling, J.E. On bipolar cell responses in the teleost retina are generated by two distinct mechanisms. J. Neurophysiol. 76, 3842-3849 (1996).
6. Otis, T.S., Kavanaugh, M.P. & Jahr, C.E. Postsynaptic glutamate transport at the climbing fiber-Purkinje cell synapse. Science 277, 1515-1518 (1997).
7. Billups, B., Rossi, D. & Attwell, D. Anion conductance behavior of the glutamate uptake carrier in salamander retinal glial cells. J. Neurosci. 16, 6722-6731 (1996).
8. Eliasof, S. & Jahr, C.E. Retinal glial cell glutamate transporter is coupled to an anionic conductance. Proc. Natl. Acad. Sci. USA 93, 4153-4158 (1996).
9. Fairman, W.A., Vandenberg, R.J., Arriza, J.L., Kavanaugh, M.P. & Amara, S.G. An excitatory amino-acid transporter with properties of a ligand-gated chloride channel. Nature 375, 599-603 (1995).
10. Wadiche, J.I., Amara, S.G. & Kavanaugh, M.P. Ion fluxes associated with excitatory amino acid transport. Neuron 15, 721-728 (1995).
11. Wadiche, J.I., Arriza, J.L., Amara, S.G. & Kavanaugh, M.P. Kinetics of a human glutamate transporter. Neuron 14, 1019-1027 (1995).
12. Wadiche, J.I. & Kavanaugh, M.P. Macroscopic and microscopic properties of a cloned glutamate transporter/chloride channel. J. Neurosci. 18, 7650-7661 (1998).
13. Vandenberg, R.J., Arriza, J.L., Amara, S.G. & Kavanaugh, M.P. Constitutive ion fluxes and substrate binding domains of human glutamate transporters. J. Biol. Chem. 270, 17668-17671 (1995).
14. Tolner, B., Ubbink-kok, T., Poolman, B. & Konings, W.N. Cation-selectivity of the L-glutamate transporters of E. coli, B. stearothermophillus and B. caldotenax: dependence on the environment in which the proteins are expressed. Mol. Microbiol. 18, 123-133 (1995a).
15. Yernool, D., Boudker, O., Jin, Y. & Gouaux, E. Structure of a glutamate transporter homologue from Pyrococcus horikoshii. Nature 431, 811-818 (2004).
16. Yernool, D., Boudker, O., Folta-Stogniew, E. & Gouaux, E. Trimeric subunit stoichiometry of the glutamate transporters from Bacillus caldotenax and Bacillus stearothermophilus. Biochemistry 42, 12981-12988 (2003).
17. Bendahan, A., Armon, A., Madani, N., Kavanaugh, M.P. & Kanner, B.I. Arginine 447 plays a pivotal role in substrate interactions in a neuronal glutamate transporter. J. Biol. Chem. 275, 37436-37442 (2000).
18. Kavanaugh, M.P., Bendahan, A., Zerangue, N., Zhang, Y. & Kanner, B.I. Mutation of an amino acid residue influencing potassium coupling in the glutamate transporter GLT-1 induces obligate exchange. J. Biol. Chem. 272, 1703-1708 (1997).
19. Ryan, R.M., Mitrovic, A.D. & Vandenberg, R.J. The chloride permeation pathway of a glutamate transporter and its proximity to the glutamate translocation pathway. J. Biol. Chem. 279, 20742-20751 (2004).
20. Slotboom, D.J., Konings, W.N. & Lolkema, J.S. Cysteine-scanning mutagenesis reveals a highly amphipathic, pore-lining membrane-spanning helix in the glutamate transporter GltT. J. Biol. Chem. 276, 10775-10781 (2001).
21. Slotboom, D.J., Sobczak, I., Konings, W.N. & Lolkema, J.S. A conserved serine-rich stretch in the glutamate transporter family forms a substrate-sensitive reentrant loop. Proc. Natl. Acad. Sci. USA 96, 14282-14287 (1999).
22. Grunewald, M., Bendahan, A. & Kanner, B.I. Biotinylation of single cysteine mutants of the glutamate transporter GLT-1 from rat brain reveals its unusual topology. Neuron 21, 623-632 (1998).
23. Grunewald, M. & Kanner, B.I. The accessibility of a novel reentrant loop of the glutamate transporter GLT-1 is restricted by its substrate. J. Biol. Chem. 275, 9684-9689 (2000).
24. Seal, R.P. & Amara, S.G. A reentrant loop domain in the glutamate carrier EAAT1 participates in substrate binding and translocation. Neuron 21, 1487-1498 (1998).
25. Grunewald, M., Menaker, D. & Kanner, B.I. Cysteine-scanning mutagenesis reveals a conformationally sensitive reentrant pore-loop in the glutamate transporter GLT-1. J. Biol. Chem. 277, 26074-26080 (2002).
26. Borre, L., Kavanaugh, M.P. & Kanner, B.I. Dynamic equilibrium between coupled and uncoupled modes of a neuronal glutamate transporter. J. Biol. Chem. 277, 13501-13507 (2002).
27. Leighton, B.H., Seal, R.P., Shimamoto, K. & Amara, S.G. A hydrophobic domain in glutamate transporters forms an extracellular helix associated with the permeation pathway for substrates. J. Biol. Chem. 277, 29847-29855 (2002).
28. Ryan, R.M. & Vandenberg, R.J. Distinct conformational states mediate the transport and anion channel properties of the glutamate transporter EAAT-1. J. Biol. Chem. 277, 13494-13500 (2002).
29. Arriza, J.L. et al. Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. J. Neurosci. 14, 5559-5569 (1994).
30. Boudker, O., Ryan, R.M., Yernool, D., Shimamoto, K. & Gouaux, E. Coupling substrate and ion binding to extracellular gate of a sodium-dependent aspartate transporter. Nature 445, 387-393 (2007).
31. Grewer, C. et al. Individual subunits of the glutamate transporter EAAC1 homotrimer function independently of each other. Biochemistry 44, 11913-11923 (2005).
32. Eskandari, S., Kreman, M., Kavanaugh, M.P., Wright, E.M. & Zampighi, G.A. Pentameric assembly of a neuronal glutamate transporter. Proc. Natl. Acad. Sci. USA 97, 8641-8646 (2000).
33. Torres-Salazar, D. & Fahlke, C. Intersubunit interactions in EAAT4 glutamate transporters. J. Neurosci. 26, 7513-7522 (2006).
34. Gaillard, I., Slotboom, D., Knol, J., Lolkema, J.S. & Konings, W.N. Purification and reconstitution of the glutamate carrier GltT of the thermophilic bacterium Bacillus stearothermophilus. Biochemistry 35, 6150-6156 (1996).
35. Nicholls, D.G. Bioenergetics: An Introduction to the Chemiosmotic Theory (Academic Press, London; New York, 1982).
36. Verkman, A.S. Development and biological applications of chloride-sensitive fluorescent indicators. Am. J. Physiol. 259, C375-C388 (1990).
37. + exchange transporter. J. Gen. Physiol. 129, 317-329 (2007).
38. --dependent neurotransmitter transporters. Nature 437, 215-223 (2005).
39. Galli, A., Blakely, R.D. & DeFelice, L.J. Norepinephrine transporters have channel modes of conduction. Proc. Natl. Acad. Sci. USA 93, 8671-8676 (1996).
40. Galli, A., Petersen, C.I., deBlaquiere, M., Blakely, R.D. & DeFelice, L.J. Drosophila serotonin transporters have voltage-dependent uptake coupled to a serotonin-gated ion channel. J. Neurosci. 17, 3401-3411 (1997).
41. Ingram, S.L., Prasad, B.M. & Amara, S.G. Dopamine transporter-mediated conductances increase excitability of midbrain dopamine neurons. Nat. Neurosci. 5, 971-978 (2002).
42. Mager, S. et al. Conducting states of a mammalian serotonin transporter. Neuron 12, 845-859 (1994).
43. Mager, S. et al. Steady states, charge movements, and rates for a cloned GABA transporter expressed in Xenopus oocytes. Neuron 10, 177-188 (1993).
44. Risso, S., DeFelice, L.J. & Blakely, R.D. Sodium-dependent GABA-induced currents in GAT1-transfected HeLa cells. J. Physiol. (Lond.) 490, 691-702 (1996).
45. Carvelli, L., McDonald, P.W., Blakely, R.D. & Defelice, L.J. Dopamine transporters depolarize neurons by a channel mechanism. Proc. Natl. Acad. Sci. USA 101, 16046-16051 (2004).
46. Quick, M. et al. State-dependent conformations of the translocation pathway in the tyrosine transporter Tyt1, a novel neurotransmitter:sodium symporter from Fusobacterium nucleatum. J. Biol. Chem. 281, 26444-26454 (2006).
47. Koch, H.P. & Larsson, H.P. Small-scale molecular motions accomplish glutamate uptake in human glutamate transporters. J. Neurosci. 25, 1730-1736 (2005).
48. Dutzler, R., Campbell, E.B., Cadene, M., Chait, B.T. & MacKinnon, R. X-ray structure of a ClC chloride channel at 3.0 Å reveals the molecular basis of anion selectivity. Nature [comment] 415, 287-294 (2002).
49. Roux, M.J. & Supplisson, S. Neuronal and glial glycine transporters have different stoichiometries. Neuron 25, 373-383 (2000).
50. DeLano, W.L. The PyMOL Molecular Graphics System (DeLano Scientific, San Carlos, California, USA, 2002).