Biotinylation of single cysteine mutants of the glutamate transporter GLT-1 from rat brain reveals its unusual topology

Neuron

Volumn 21, Issue 3, 1998, Pages 623-632

  Grunewald, Myriam ^a   Bendahan, Annie ^a   Kanner, Baruch I ^a  

^a HEBREW UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; MUTANT PROTEIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BIOTINYLATION; BRAIN; HUMAN; HUMAN CELL; HYDROPHOBICITY; MOLECULAR CLONING; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MODIFICATION;

EID: 0032169137     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80572-3     Document Type: Article

References (48)

1. Arriza, J.L., Kavanaugh, M.P., Fairman, W.A., Wu, Y.N., Murdoch, G.H., North, R.A., and Amara, S.G. (1993). Cloning and expression of a human neutral amino acid transporter with structural similarity to the glutamate transporter gene family. J. Biol. Chem. 268, 15329-15332.
2. 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. USA 94, 4155-4160.
3. 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.
4. Conradt, M., and Stoffel, W. (1995). Functional analysis of the high affinity, Na(+)-dependent glutamate transporter GLAST-1 by site-directed mutagenesis. J. Biol. Chem. 270, 25207-25212.
5. Conradt, M., Storck, T., and Stoffel, W. (1995). Localization of N-glycosylation sites and functional role of the carbohydrate units of GLAST-1, a cloned rat brain L-glutamate/L-aspartate transporter. Eur. J. Biochem. 229, 682-687.
6. Danbolt, N.C., Pines, G., and Kanner, B.I. (1990). Purification and reconstitution of the sodium-and potassium-coupled glutamate transport glycoprotein from rat brain. Biochemistry 29, 6734-6740.
7. +]coupled L-glutamate transporter purified from rat brain is located in glial cell processes. Neuroscience 51, 295-310.
8. Diamond, J.S., and Jahr, C.E. (1997). Transporters buffer synaptically released glutamate on asubmillisecond timescale. J. Neurosci. 17, 4672-4687.
9. + conduction and selectivity. Science 280, 69-77.
10. Fairman, W.A., Vandenberg, RJ., 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.
11. Grunewald, M., and Kanner, B. (1995). Conformational changes monitored on the glutamate transporter GLT-1 indicate the existence of two neurotransmitter-bound states. J. Biol. Chem. 270, 17017-17024.
12. + channels. Science 251, 942-944.
13. + channel signature sequence. Biophys. J. 66, 1061-1067.
14. Holmgren, M., Liu, Y., Xu, Y., and Yellen, G. (1996). On the use of thiol-modifying agents to determine channel topology. Neuropharmacology 35, 797-804.
15. Kanai,Y.,and Hediger, M.A. (1992). Primary structure and functional characterization of a high-affinity glutamate transporter. Nature 360, 467-471.
16. 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.
17. Kanner, B.I., and Schuldiner, S. (1987). Mechanism of transport and storage of neurotransmitters. CRC Grit. Rev. Biochem. 22, 1-38.
18. Kanner, B.I., and Sharon, I. (1978). Active transport of L-glutamate by membrane vesicles isolated from rat brain. Biochemistry 17, 3949-3953.
19. 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.
20. Kekuda, R., Prasad, P.D., Fei, Y.J., Torres-Zamorano, V., Sinha, S., Yang-Feng, T.L., Leibach, F.H., and Ganapathy, V. (1996). Cloning of the sodium-dependent, broad-scope, neutral amino acid transporter Bo from a human placental choriocarcinoma cell line. J. Biol. Chem. 277, 18657-18661.
21. Keynan, S., Suh, Y.J., Kanner, B.I., and Rudnick, G. (1992). Expression of a cloned gamma-aminobutyric acid transporter in mammalian cells. Biochemistry 31, 1974-1979.
22. Krishnasastry, M., Walker, B., Braha, O., and Bayley, H. (1994). Surface labeling of key residues during assembly of the transmembrane pore formed by staphycococcal α-hemolysin. FEBS Lett. 356,66-71.
23. Kuner, T., Wollmuth, L.P., Karlin, A., Seeburg, P.H., and Sakmann, B. (1996). Structure of the NMDA receptor channel M2 segment inferred from the accessibility of substituted cysteines. Neuron 17, 343-352.
24. Kunkel, T.A., Roberts, J.D., and Zakour, R.A. (1987). Rapid and efficient site-specific mutagenesis without phenotypic selection. Meth. Enzymol. 154, 367-382.
25. Loo, T.W., and Clarke, D.M. (1995). Membrane topology of acysteineless mutant of human P-glycoprotein. J. Biol. Chem. 270, 843-848.
26. MacKinnon, R. (1995). Pore loops: an emerging theme in ion channel structure. Neuron 14, 889-892.
27. Mennerick, S., and Zorumski, C.F. (1994). Glial contributions to excitatory neurotransmission in cultured hippocampal cells. Nature 368, 59-62.
28. Nicholls, D., and Attwell, D. (1990). The release and uptake of excitatory amino acids. Trends Pharmacol. Sci. 11, 462-468.
29. + antiporter of Escherichia coli is exposed and faces the cell exterior. J. Biol. Chem. 272, 1761-1768.
30. Otis, T.S., Wu, Y.C., and Trussell, L.O. (1996). Delayed clearance of transmitter and the role of glutamate transporters at synapses with multiple release sites. J. Neurosci. 16, 1634-1644.
31. 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.
32. 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.
33. +)-coupled glutamate transporter from rat brain. J. Biol. Chem. 270, 17093-17097.
34. Rothstein, J.D., Dykes-Hoberg, M., Pardo, C.A., Bristol, L.A., Jin, L., Kuncl, R.W., Kanai, Y., Hediger, M.A., Wang, Y., Schielke, J.P., et al. (1996). Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16, 675-686.
35. +/glutamate cotransporters. J. Biol. Chem. 268, 15351-15355.
36. 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.
37. +-dependent glutamate/ aspartate transporter from rat brain. Proc. Natl. Acad. Sci. USA 89, 10955-10959.
38. Tanaka, K., Watase, K., Manabe, T., Yamada, K., Watanabe, M., Takahashi, K., Iwama, H., Nishikawa, T., Ichihara, N., Kikuchi, T., et al. (1997). Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276, 1699-1702.
39. Tolner, B., Ubbink-Kok, T., Poolman, B., and Konings, W.N. (1995). Characterization of the proton/glutamate symport protein of Bacillus subtilis and its functional expression in Escherichia coli. J. Bacteriol. 177, 2863-2869.
40. Tong, G., and Jahr, C.E. (1994). Block of glutamate transporters potentiates postsynaptic excitation. Neuron 13, 1195-1203.
41. +-dependent neutral amino acid transporter. J. Biol. Chem. 271, 14883-14890.
42. Vandenberg, R.J., Arriza, J.L., Amara, S.G., and Kavanaugh, M.P. (1995). Constitutive ion fluxes and substrate binding domains of human glutamate transporters. J. Biol. Chem. 270, 17668-17671.
43. Wadiche, J.I., Arriza, J.L., Amara, S.G., and Kavanaugh, M.P. (1995). Kinetics of a human glutamate transporter. Neuron 14, 1019-1027.
44. Wahle, S., and Stoffel, W. (1996). Membrane topology of the high-affinity L-glutamate transporter (GLAST-1) of the central nervous system. J. Cell Biol. 135, 1867-1877.
45. + channel. Science 251, 939-942.
46. Zarbiv, R., Grunewald, M., Kavanaugh, M.P., and Kanner, B.I. (1998). Cysteine scanning of the surroundings of an alkali-ion binding site of the glutamate transporter GLT-1 reveals a conformationally sensitive residue. J. Biol. Chem. 273, 14231-14237.
47. Zerangue, N., and Kavanaugh, M.P. (1996). Flux coupling in a neuronal glutamate transporter. Nature 383, 634-637.
48. +)-coupled rat brain glutamate transporter. Proc. Natl. Acad. Sci. USA 95, 751-755.