Membrane topology of the high-affinity l-glutamate transporter (GLAST-1) of the central nervous system

Journal of Cell Biology

Volumn 135, Issue 6 II, 1996, Pages 1867-1877

  Wahle, Stephan ^a   Stoffel, Wilhelm ^a,b  

^a UNIVERSITY OF COLOGNE   (Germany)

^b NONE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CENTRAL NERVOUS SYSTEM; GLIA CELL; HYDROPHOBICITY; NEUROTRANSMITTER RELEASE; PREDICTION; PRIORITY JOURNAL; REPORTER GENE; RNA TRANSLATION;

AMINO ACID SEQUENCE; AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CELL MEMBRANE; CENTRAL NERVOUS SYSTEM; CONSERVED SEQUENCE; CYTOPLASM; FEMALE; GLYCOPROTEINS; GLYCOSYLATION; MOLECULAR SEQUENCE DATA; OOCYTES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; XENOPUS;

EID: 0030471958     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.135.6.1867     Document Type: Article

References (60)

1. Akabas, M.H., D.A. Stauffer, M. Xu, and A. Karlin. 1992. Acetylcholine receptor channel structure probed in cysteine-substitution mutants. Science (Wash. DC). 258:307-310.
2. Arriza, J.L., M.P. Kavanaugh, W.A. Fairman, Y.N. Wu, G.H. Murdoch, R.A. North, and S.G. Amara. 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.
3. Blachly-Dyson, E., S. Peng, M. Colombini, and M. Forte. 1990. Selectivity changes in site-directed mutants of the VDAC ion channel: structural implications. Science (Wash. DC) 247:1233-1236.
4. Blakely, R.D., H.E. Berson, R. Fremeau, Jr., M.G. Caron, M.M. Peek, H.K. Prince, and C.C. Bradley. 1991. Cloning and expression of a functional serotonin transporter from rat brain. Nature (Lond.). 354:66-70.
5. Blau, R., and W. Stoffel. 1995. Rat and human glutamate transporter GLAST1: stable heterologous expression, biochemical and functional characterization. Biol. Chem. Hoppe-Seyler. 376:511-514.
6. Blobel, G. 1980. Intracellular protein topogenesis. Proc. Natl. Acad. Sci. USA. 77:1496-1500.
7. Bouvier, M., M. Szatkowski, A. Amato, and D. Attwell. 1992. The glial cell glutamate uptake carrier countertransports pH-changing anions. Nature (Lond.). 360:471-474.
8. Boyd, D., and J. Beckwith. 1989. Positively charged amino acid residues can act as topogenic determinants in membrane proteins. Proc. Natl. Acad. Sci. USA. 86:9446-9450.
9. Casado, M., A. Bendahan, F. Zafra, N.C. Danbolt, C. Aragon, C. Gimenez, and B.I. Kanner. 1993. Phosphorylation and modulation of brain glutamate transporters by protein kinase C. J. Biol. Chem. 268:27313-27317.
10. Catty, D. 1988. Antibodies: A Practical Approach. IRL Press, Oxford. 121-137.
11. Colman, A. 1984. Translation of eukaryotic messenger RNA in Xenopus oocytes. In Transcription and Translation: A Practical Approach. B.D. Hames and S.J. Higgins, editors. IRL Press, Oxford. 271-302.
12. +-dependent glutamate transporter GLAST-1 by site-directed mutagenesis. J. Biol. Chem. 270:25207-25212.
13. Conradt, M., T. Storck, and W. Stoffel. 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.
14. Cowan, S.W., T. Schirmer, G. Rummel, M. Steiert, R. Ghosh, R.A. Pauptit, J.N. Jansonius, and J.P. Rosenbusch. 1992. Crystal structures explain functional properties of two E. coli porins. Nature (Lond.). 358:727-733.
15. Crowley, K.S., G.D. Reinhart, and A.E. Johnson. 1993. The signal sequence moves through a ribosomal tunnel into a noncytoplasmic aqueous environment at the ER membrane early in translocation. Cell. 73:1101-1115.
16. Crowley, K.S., S. Liao, V.E. Worrell, G D. Reinhart, and A.E. Johnson. 1994. Secretory proteins move through the endoplasmic reticulum membrane via an aqueous, gated pore. Cell. 78:461-471.
17. Engelke, T., D. Jording, D. Kapp, and A. Puhler. 1989. Identification and sequence analysis of the Rhizobium meliloti dctA gene encoding the C4-dicarboxylate carrier. J. Bacteriol. 171:5551-5560.
18. Fairman, W.A., R.J. Vandenberg, J.L. Arriza, M.P. Kavanaugh, and S.G. Amara. 1995. An excitatory amino-acid transporter with properties of a ligandgated chloride channel. Nature (Lond.). 375:599-603.
19. Flott, B., and W. Seifert. 1991. Characterization of glutamate uptake systems in astrocyte primary cultures from rat brain. Glia. 4:293-304.
20. Fremeau, R., M.G. Caron, and R.D. Blakely. 1992. Molecular cloning and expression of a high affinity L-proline transporter expressed in putative glutamatergic pathways of rat brain. Neuron. 8:915-926.
21. Fujiki, Y., A.L. Hubbard, S. Fowler, and P. Lazarow. 1982. Isolation of intracellular membranes by means of sodium carbonate treatment application to endoplasmic reticulum. J. Cell Biol. 93:97-102.
22. Goodfriend, T.L., L. Levine, and G. Fasman. 1964. Antibodies to bradykinin and angiotensin: a use of carbodiimide in immunology. Science (Wash. DC). 144:144-146.
23. Görlich, D., E. Hartmann, S. Prehn, and T.A. Rapoport. 1992a. A protein of the endoplasmic reticulum involved early in polypeptide translocation. Nature (Lond.). 357:47-52.
24. Görlich, D., S. Prehn, E. Hartmann, K.U. Kalies, and T.A. Rapoport. 1992b. A mammalian homolog of SEC61p and SECYp is associated with ribosomes and nascent polypeptides during translocation. Cell. 71:489-503.
25. Guastella, J., N. Nelson, H. Nelson, L. Czyzyk, S. Keynan, M.C. Miedel, N. Davidson, H.A. Lester, and B.I. Kanner. 1990. Cloning and expression of a rat brain GABA transporter. Science (Wash. DC). 249:1303-1306.
26. Hart, G.W., K. Brew, G.A. Grant, R.A. Bradshaw. and W.J. Lennarz. 1978. Primary structural requirements for the enzymatic formation of the N-glycosidic bond in glycoproteins. J. Biol. Chem. 254:9747-9753.
27. +/glucose co-transporter. Nature (Lond.). 330:379-381.
28. Higuchi, R., B. Krummel, and R.K. Saiki. 1988. Recombinant PCR. A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res. 16:7351-7361.
29. Kanai, Y., and M.A. Hediger. 1992. Primary structure and functional characterization of a high-affinity glutamate transporter. Nature (Lond.). 360:467-471.
30. Kanai, Y., S. Nussberger, M.F. Romero, W.F. Boron, S.C. Hebert, and M.A. Hediger. 1995. Electrogenic properties of the epithelial and neuronal high affinity glutamate transporter. J. Biol. Chem. 270:16561-16568.
31. Klöckner, U., T. Storck, M. Conradt, and W. Stoffel. 1993. Electrogenic L-glutamate uptake in Xenopus laevis oocytes expressing a cloned rat brain L-glutamate/L-aspartate transporter (GLAST-1). J. Biol. Chem. 268:14594-14596.
32. Klöckner, U., T. Storck, M. Conradt, and W. Stoffel. 1994. Functional properties and substrate specificity of the cloned L-glutamate/L-aspartate transporter GLAST-1 from rat brain expressed in Xenopus oocytes. J. Neurosci. 14:5759-5765.
33. Kreis, T.E. 1986. Microinjected antibodies against the cytoplasmic domain of vesicular stomatitis virus glycoprotein block its transport to the cell surface. Source. 5:931-941.
34. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond.). 227:680-685.
35. 14C in polyacrylamide gels by fluorography. Eur. J. Biochem. 56:335-341.
36. Lehre, K.P., L.M. Levy, O.P. Ottersen, J. Storm-Mathisen, and N.C. Danbolt. 1995. Differential expression of two glial glutamate transporters in the rat brain: quantitative and immunocytochemical observations. J. Neurosci. 15: 1835-1853.
37. Martoglio, B., M.W. Hofmann, J. Brunner, and B. Dobberstein. 1995. The protein-conducting channel in the membrane of the endoplasmic reticulum is open laterally toward the lipid bilayer. Cell. 81:207-214.
38. Mothes, W., S. Prehn, and T. A. Rapoport. 1994. Systematic probing of the environment of a translocating secretory protein during translocation through the ER membrane. EMBO (Eur. Mol. Biol. Organ.) J. 13:3973-3982.
39. Nilsson, I., P. Whitley, and G. von Heijne. 1994. The COOH-terminal ends of internal signal and signal-anchor sequences are positioned differently in the ER translocase. J. Cell Biol. 126:1127-1132.
40. Pacholczyk, T., R.D. Blakely, and S.G. Amara. 1991. Expression cloning of a cocaine- and antidepressant-sensitive human noradrenaline transporter. Nature (Lond). 350:350-354.
41. Pines, G., N.C. Danbolt, M. Bjoras, Y. Zhang, A. Bendahan, L. Eide, H. Koepsell, J. Storm-Mathisen, E. Seeberg, and B.I. Kanner. 1992. Cloning and expression of a rat brain L-glutamate transporter. Nature (Lond.). 360:464-467.
42. +)-coupled glutamate transporter from rat brain. J. Biol. Chem. 270:17093-17097.
43. + coupling mechanisms. J. Theor. Biol. 150:239-249.
44. Russel, M., and P. Model. 1982. Filamentous phage pre-coat is an integral membrane protein: analysis by a new method of membrane preparation. Cell. 28: 177-184.
45. Schirmer, T., and S.W. Cowan. 1993. Prediction of membrane-spanning β-strands and its application to maltoporin. Protein Sci. 2:1361-1363.
46. Schulte, S., and W. Stoffel. 1995. UDP-galactose: ceramide galactosyltransferase and glutamate/aspartate transporter. Copurification, separation and characterization of the two glycoproteins. Eur. J. Biochem. 233:947-953.
47. +/glutamate cotransporters. J. Biol. Chem. 268:15351-15355.
48. Shaw, A.S., P.J.M. Rottier, and J.K. Rose. 1988. Evidence for the loop model of signal sequence insertion into endoplasmic reticulum. Proc. Natl. Acad. Sci. USA. 85:7592-7596.
49. Shimada, S., S. Kitayama, C.L. Lin, A. Patel, E. Nanthakumar, P. Gregor, M. Kuhar, and G. Uhl. 1991. Cloning and expression of a cocaine-sensitive dopamine transporter complementary DNA. Science (Wash. DC). 254:576-578.
50. Singh, P., B.L. Tang, S.H. Wong, and W. Hong. 1993. Transmembrane topology of the mammalian KDEL receptor. Mol. Cell. Biol. 13:6435-6441.
51. Smith, K.E., L.A. Borden, P.R. Hartig, T. Branchek, and R.L. Weinshank. 1992. Cloning and expression of a glycine transporter reveal colocalization with NMDA receptors. Neuron. 8:927-935.
52. +-dependent glutamate/aspartate transporter from rat brain. Proc. Natl. Acad. Sci. USA. 89:10955-10959.
53. Tolner, B., B. Poolman, and W.N. Konings. 1992a. Characterization and functional expression in Escherichia coli of the sodium/proton/glutamate symport proteins of Bacillus stearothermophilus and Bacillus caldotenax. Mol. Microbiol. 6:2845-2856.
54. Tolner, B., B. Poolman, B. Wallace, and W.N. Konings 1992b. Revised nucleotide sequence of the gltP gene, which encodes the proton-glutamate-aspartate transport protein of Escherichia coli K-12. J. Bacterial. 174:2391-2393.
55. Uhl, G.R. 1992. Neurotransmitter transporters (plus): a promising new gene family. Trends Neurosci 15:265-268.
56. von Heijne, G. 1985. Signal sequences. The limits of variation. J. Mol. Biol. 184: 99-105.
57. von Heijne, G. 1986. Towards a comparative anatomy of N-terminal topogenic protein sequences. J. Mol. Biol. 189:239-242.
58. von Heijne, G. 1989. Control of topology and mode of assembly of a polytopic membrane protein by positively charged residues. Nature (Lond.). 341:456-458.
59. Weiss, M.S., U. Abele, J. Weckesser, W. Welte, E. Schiltz, and G.E. Schulz. 1991. Molecular architecture and electrostatic properties of a bacterial porin. Science (Wash. DC). 254:1627-1630.
60. Wessels, H.P., and M. Spiess. 1988. Insertion of a multispanning membrane protein occurs sequentially and requires only one signal sequence. Cell. 55: 61-70.