Disulfide cross-linking of transport and trimerization domains of a neuronal glutamate transporter restricts the role of the substrate to the gating of the anion conductance

Journal of Biological Chemistry

Volumn 289, Issue 16, 2014, Pages 11175-11182

  Shabaneh, Mustafa ^a   Rosental, Noa ^a   Kanner, Baruch I ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ION EXCHANGE;

DISULFIDE CROSS-LINKING; GLUTAMATE TRANSPORTERS; ION-CONDUCTING; TRIMERIZATION;

IONS;

1,10 PHENANTHROLINE COPPER; ANION; CADMIUM CHLORIDE; CHLORIDE; CYSTEINE; DITHIOTHREITOL; EXCITATORY AMINO ACID TRANSPORTER 3;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CELL TRANSPORT; CHANNEL GATING; CHLORIDE CURRENT; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CROSS LINKING; DISULFIDE BOND; FEMALE; ION CONDUCTANCE; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN TRANSPORT; TRIMERIZATION; WILD TYPE; XENOPUS LAEVIS;

GATING; GLUTAMATE; MEMBRANE BIOPHYSICS; MEMBRANE ENERGETICS; MEMBRANE TRANSPORT; NEUROTRANSMITTER TRANSPORT;

AMINO ACID SUBSTITUTION; ANIMALS; DITHIOTHREITOL; EXCITATORY AMINO ACID TRANSPORTER 3; HELA CELLS; HUMANS; ION CHANNEL GATING; ION TRANSPORT; MUTATION, MISSENSE; ORGANOMETALLIC COMPOUNDS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RABBITS; XENOPUS LAEVIS;

EID: 84899011312     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.550277     Document Type: Article

References (52)

1. Kanner, B. I., and Sharon, I. (1978) Active transport of L-glutamate by membrane vesicles isolated from rat brain. Biochemistry 17, 3949-3953
2. Brew, H., and Attwell, D. (1987) Electrogenic glutamate uptake is a major current carrier in the membrane of axolotl retinal glial cells. Nature 327, 707-709
3. Zerangue, N., and Kavanaugh, M. P. (1996) Flux coupling in a neuronal glutamate transporter. Nature 383, 634-637
4. Levy, L. M., Warr, O., and Attwell, D. (1998) Stoichiometry of the glial glutamate transporter GLT-1 expressed inducibly in a Chinese hamster ovary cell line selected for low endogenous Na+-dependent glutamate uptake. J. Neurosci. 18, 9620-9628
5. 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
6. 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
7. 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
8. 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
9. Wadiche, J. I., Amara, S. G., and Kavanaugh, M. P. (1995) Ion fluxes associated with excitatory amino acid transport. Neuron 15, 721-728
10. 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
11. Picaud, S., Larsson, H. P., Wellis, D. P., Lecar, H., and Werblin, F. (1995) Cone photoreceptors respond to their own glutamate release in the tiger salamander. Proc. Natl. Acad. Sci. U.S.A. 92, 9417-9421
12. Yernool, D., Boudker, O., Jin, Y., and Gouaux, E. (2004) Structure of a glutamate transporter homologue from Pyrococcus horikoshii. Nature 431, 811-818
13. Boudker, O., Ryan, R. M., Yernool, D., Shimamoto, K., and Gouaux, E. (2007) Coupling substrate and ion binding to extracellular gate of a sodium-dependent aspartate transporter. Nature 445, 387-393
14. Reyes, N., Ginter, C., and Boudker, O. (2009) Transport mechanism of a bacterial homologue of glutamate transporters. Nature 462, 880-885
15. Verdon, G., and Boudker, O. (2012) Crystal structure of an asymmetric trimer of a bacterial glutamate transporter homolog. Nat. Struct. Mol. Biol. 19, 355-357
16. Koch, H. P., and Larsson, H. P. (2005) Small-scale molecular motions accomplish glutamate uptake in human glutamate transporters. J. Neurosci. 25, 1730-1736
17. 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
18. Leary, G. P., Stone, E. F., Holley, D. C., and Kavanaugh, M. P. (2007) The glutamate and chloride permeation pathways are colocalized in individual neuronal glutamate transporter subunits. J. Neurosci. 27, 2938-2942
19. Koch, H. P., Brown, R. L., and Larsson, H. P. (2007) The glutamate-activated anion conductance in excitatory amino acid transporters is gated independently by the individual subunits. J. Neurosci. 27, 2943-2947
20. 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
21. Grunewald, M., and Kanner, B. I. (2000) The accessibility of a novel reentrant loop of the glutamate transporter GLT-1 is restricted by its substrate. J. Biol. Chem. 275, 9684-9689
22. 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
23. Zhang, Y., and Kanner, B. I. (1999) Two serine residues of the glutamate transporter GLT-1 are crucial for coupling the fluxes of sodium and the neurotransmitter. Proc. Natl. Acad. Sci. U.S.A. 96, 1710-1715
24. Borre, L., and Kanner, B. I. (2001) Coupled, but not uncoupled, fluxes in a neuronal glutamate transporter can be activated by lithium ions. J. Biol. Chem. 276, 40396-40401
25. Zhang, Y., Bendahan, A., Zarbiv, R., Kavanaugh, M. P., and Kanner, B. I. (1998) Molecular determinant of ion selectivity of a (Na+ + K+)-coupled rat brain glutamate transporter. Proc. Natl. Acad. Sci. U.S.A. 95, 751-755
26. 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
27. Teichman, S., and Kanner, B. I. (2007) Aspartate 444 is essential for productive substrate interactions in a neuronal glutamate transporter. J. Gen. Physiol. 129, 527-539
28. Crisman, T. J., Qu, S., Kanner, B. I., and Forrest, L. R. (2009) Inward-facing conformation of glutamate transporters as revealed by their inverted-topology structural repeats. Proc. Natl. Acad. Sci. U.S.A. 106, 20752-20757
29. Groeneveld, M., and Slotboom, D. J. (2007) Rigidity of the subunit interfaces of the trimeric glutamate transporter GltT during translocation. J. Mol. Biol. 372, 565-570
30. Ryan, R. M., and Mindell, J. A. (2007) The uncoupled chloride conductance of a bacterial glutamate transporter homolog. Nat. Struct. Mol. Biol. 14, 365-371
31. Kanai, Y., and Hediger, M. A. (1992) Primary structure and functional characterization of a high-affinity glutamate transporter. Nature 360, 467-471
32. Borre, L., and Kanner, B. I. (2004) Arginine 445 controls the coupling between glutamate and cations in the neuronal transporter EAAC-1. J. Biol. Chem. 279, 2513-2519
33. Pines, G., Zhang, Y., and Kanner, B. I. (1995) Glutamate 404 is involved in the substrate discrimination of GLT-1, a (Na+ + K+)-coupled glutamate transporter from rat brain. J. Biol. Chem. 270, 17093-17097
34. Kunkel, T. A., Roberts, J. D., and Zakour, R. A. (1987) Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154, 367-382
35. Keynan, S., Suh, Y. J., Kanner, B. I., and Rudnick, G. (1992) Expression of a cloned γ-aminobutyric acid transporter in mammalian cells. Biochemistry 31, 1974-1979
36. Fuerst, T. R., Niles, E. G., Studier, F. W., and Moss, B. (1986) Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc. Natl. Acad. Sci. U.S.A. 83, 8122-8126
37. Pérez-Garcia, M. T., Chiamvimonvat, N., Marban, E., and Tomaselli, G. F. (1996) Structure of the sodium channel pore revealed by serial cysteine mutagenesis. Proc. Natl. Acad. Sci. U.S.A. 93, 300-304
38. Glusker, J. P. (1991) Structural aspects of metal liganding to functional groups in proteins. Adv. Protein Chem. 42, 1-76
39. Bénitah, J. P., Tomaselli, G. F., and Marban, E. (1996) Adjacent pore-lining residues within sodium channels identified by paired cysteine mutagenesis. Proc. Natl. Acad. Sci. U.S.A. 93, 7392-7396
40. Wadiche, J. I., and Kavanaugh, M. P. (1998) Macroscopic and microscopic properties of a cloned glutamate transporter/chloride channel. J. Neurosci. 18, 7650-7661
41. Seal, R. P., Shigeri, Y., Eliasof, S., Leighton, B. H., and Amara, S. G. (2001) Sulfhydryl modification of V449C in the glutamate transporter EAAT1 abolishes substrate transport but not the substrate-gated anion conductance. Proc. Natl. Acad. Sci. U.S.A. 98, 15324-15329
42. Borre, L., Kavanaugh, M. P., and Kanner, B. I. (2002) Dynamic equilibrium between coupled and uncoupled modes of a neuronal glutamate transporter. J. Biol. Chem. 277, 13501-13507
43. Ryan, R. M., and Vandenberg, R. J. (2002) Distinct conformational states mediate the transport and anion channel properties of the glutamate transporter EAAT-1. J. Biol. Chem. 277, 13494-13500
44. Shachnai, L., Shimamoto, K., and Kanner, B. I. (2005) Sulfhydryl modification of cysteine mutants of a neuronal glutamate transporter reveals an inverse relationship between sodium-dependent conformational changes and the glutamate-gated anion conductance. Neuropharmacology 49, 862-871
45. 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
46. Focke, P. J., Moenne-Loccoz, P., and Larsson, H. P. (2011) Opposite movement of the external gate of a glutamate transporter homolog upon binding cotransported sodium compared with substrate. J. Neurosci. 31, 6255-6262
47. 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
48. Otis, T. S., and Kavanaugh, M. P. (2000) Isolation of current components and partial reaction cycles in the glial glutamate transporter EAAT2. J. Neurosci. 20, 2749-2757
49. Auger, C., and Attwell, D. (2000) Fast removal of synaptic glutamate by postsynaptic transporters. Neuron 28, 547-558
50. Schicker, K., Uzelac, Z., Gesmonde, J., Bulling, S., Stockner, T., Freissmuth, M., Boehm, S., Rudnick, G., Sitte, H. H., and Sandtner, W. (2012) Unifying concept of serotonin transporter-associated currents. J. Biol. Chem. 287, 438-445
51. Felts, B., Pramod, A. B., Sandtner, W., Burbach, N., Bulling, S., Sitte, H. H., and Henry, L. K. (2014) The two Na+ sites in the human serotonin transporter play distinct roles in the ion coupling and electrogenicity of transport. J. Biol. Chem. 289, 1825-1840
52. Li, J., Shaikh, S. A., Enkavi, G., Wen, P. C., Huang, Z., and Tajkhorshid, E. (2013) Transient formation of water-conducting states in membrane transporters. Proc. Natl. Acad. Sci. U.S.A. 110, 7696-7701