Role of the conserved glutamine 291 in the rat γ-aminobutyric acid transporter rGAT-1

Cellular and Molecular Life Sciences

Volumn 63, Issue 1, 2006, Pages 100-111

  Mari, S A ^a   Soragna, A ^b   Castagna, M ^a   Santacroce, M ^a   Perego, C ^a   Bossi, E ^b   Peres, A ^b   Sacchi, V F ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF INSUBRIA   (Italy)

Author keywords

Electrophysiology; GAT 1; Neurotransmitter transporter; Site directed mutagenesis; Structure function relationship; Xenopus laevis oocyte

Indexed keywords

4 AMINOBUTYRIC ACID; CYSTEINE; GLUTAMINE DERIVATIVE;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CHEMICAL MODIFICATION; CONTROLLED STUDY; NONHUMAN; OLIGOMERIZATION; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; RAT; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; CONSERVED SEQUENCE; CYSTEINE; ELECTROPHYSIOLOGY; GABA PLASMA MEMBRANE TRANSPORT PROTEINS; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION; GLUTAMINE; HUMANS; LITHIUM; MOLECULAR SEQUENCE DATA; MUTATION; PATCH-CLAMP TECHNIQUES; RATS; SEQUENCE ALIGNMENT;

ANIMALIA; XENOPUS LAEVIS;

EID: 30744442989     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-005-5512-6     Document Type: Article

References (58)

1. Guastella J., Nelson N., Nelson H., Czyzyk L., Keynan S., Miedel M. C. et al. (1990) Cloning and expression of a rat brain GABA transporter. Science 249: 1303-1306
2. Palacìn M., Estévez R., Bertran J. and Zorzano A. (1998) Molecular biology of mammalian plasma membrane amino acid transporters. Physiol. Rev. 78: 969-1054
3. Chen J. G., Liu-Chen S. and Rudnick G. (1998) Determination of external loop topology in the serotonin transporter by site-directed chemical labeling. J.Biol.Chem. 273: 12675-12681
4. Mager S., Naeve J., Quick M., Labarca C., Davidson N. and Lester H.A. (1993) Steady states, charge movements, and rates for a cloned GABA transporter expressed in Xenopus oocytes. Neuron 10: 177-188
5. -) cotransport function. Database reconstruction with an alternating access model. J. Gen. Physiol. 114: 459-475
6. -) cotransport function. Kinetic studies in giant Xenopus oocytes membrane patches. J. Gen. Physiol. 114: 445-457
7. -) cotransport function. Steady state studies in giant Xenopus oocyte membrane patches. J. Gen. Physiol. 114: 429-444
8. --dependent GABA cotransporters rGAT1. J. Physiol. 541: 343-350
9. Fesce R., Giovannardi S., Binda F., Bossi E. and Peres A. (2002) The relation between charge movement and transport-associated currents in the GABA cotransporter rGAT1. J. Physiol. 545: 739-750
10. DeFelice L. J., Adams S. V. and Ypey D. L. (2001) Single-file diffusion and neurotransmitter transporters: Hodgkin and Keynes model revisited. BioSystems 62: 57-66
11. +-coupled cotransporters GAT1 and SGLT1. J. Biol. Chem. 275: 37414-37422
12. +-induced leak current in the rat α-aminobutyric acid (GABA) trasporter-1. J. Physiol. 544: 447-458
13. Golovanevsky V. and Kanner B. I. (1999) The reactivity of the γ-aminobutyric acid transporter GAT-1 toward sulfhydryl reagents is conformationally sensitive: identification of a major target residue. J. Biol. Chem. 274: 23020-23026
14. Kanner B. I. (2003) Transmembrane domain I of the γ-aminobutyric acid transporter plays a crucial role in the transition between cation leak and transport modes. J. Biol. Chem. 278: 3705-3712
15. Zomot E. and Kanner B. I. (2003) The interaction of the γ-aminobutyric acid transporter GAT-1 with the neurotransmitter is selectively impaired by sulphydryl modification of a conformationally sensitive cysteine residue engineered in extracellular loop IV. J. Biol. Chem. 278: 42950-12958
16. Pantanowitz S., Bendahan A. and Kanner B. I. (1993) Only one of the charged amino acids located in the transmembrane α-helices of the γ-aminobutyric acid transporter (subtype A) is essential for its activity. J. Biol. Chem. 268: 3222-3225
17. Keshet G. I., Bendahan A., Su H., Mager S., Lester H. A. and Kanner B. I. (1995) Glutamate-101 is critical for the function of the sodium and chloride-coupled GABA transporter GAT-1. FEBS Lett. 371: 39-42
18. Sussman J. L., Harel M., Frolow F., Oefner C., Goldman A., Toker L. et al. (1991) Atomic structure of acetylcholinesterase from Torpedo californica: a prototypic acetylcholine-binding protein. Science 253: 872-879
19. Gallivan J. P. and Dougherty D. A. (1999) Cation-pi interactions in structural biology. Proc. Natl. Acad. Sci. USA 96: 9459-9464
20. Kavanaugh M. P., Hurst R. S., Yakel J., Varnum M. D., Adelman J. P. and North R. A. (1992) Multiple subunits of a voltage-dependent potassium channel contribute to the binding site for tetraethylammonium. Neuron 8: 493-497
21. Kleinberger-Doron N. and Kanner B. I. (1994) Identification of tryptophan residues critical for the function and targeting of the g-aminobutyric acid transporter (subtype A). J. Biol. Chem. 269: 3063-3067
22. Mager S., Kleinberger-Doron N., Keshet G. I., Davidson N., Kanner B. I. and Lester H. A. (1996) Ion binding and permeation at the GABA transporter GAT1. J. Neurosci. 16: 5405-5414
23. Zomot E., Zhou Y. and Kanner B. I. (2005) Proximity of transmembrane domains 1 and 3 of the GABA transporter GAT-1 inferred from paired cysteine mutagenesis. J.Biol.Chem. 280: 25512-25516
24. Bismuth Y., Kavanaugh M. P. and Kanner B. I. (1997) Tyrosine 140 of the g-aminobutyric acid transporter GAT-1 plays a critical role in neurotransmitter recognition. J. Biol. Chem. 272: 16096-16102
25. Zhou F. X., Merianos H. J., Brunger A. T. and Engelman D. M. (2001) Polar residues drive association of polyleucine transmembrane helices. Proc. Natl. Acad. Sci. USA 98: 2250-2255
26. --dependent neurotransmitter transporters. Nature 437: 215-223
27. Mari S. A., Soragna A., Castagna M., Bossi E., Peres A. and Sacchi V. F. (2004) Aspartate 338 contributes to the cationic specificity and to driver-amino acid coupling in the insect cotransporter KAAT1. Cell. Mol. Life Sci. 61: 243-256
28. -)-coupled g-aminobutyric acid transporter from rat brain. J. Biol. Chem. 272: 1203-1210
29. Veenhoff L. M., Heuberger E. H. M. L. and Poolman B. (2002) Quaternary structure and function of transport proteins. Trends Biol. Sci. 27: 242-249
30. Horiuchi M., Nicke A., Gomeza J., Ashrafi A., Schmalzing G. and Betz H. (2001) Surface-localized glycine transporters 1 and 2 function as monomeric proteins in Xenopus oocytes. Proc. Natl. Acad. Sci. USA 98: 1448-1453
31. Schmid J. A., Scholze P., Kudlacek O., Freissmuth M., Singer E. A. and Sitte H. H. (2001) Oligomerization of the human serotonin transporter and of the rat GABA transporter 1 visualized by fluorescence resonance energy transfer microscopy in living cells. J. Biol. Chem. 276: 3805-3810
32. Scholze P., Freissmuth M. and Sitte H. H. (2002) Mutations within an intramembrane leucine heptad repeat disrupt oligomer formation of the rat GABA transporter 1. J. Biol. Chem. 277: 43682-43690
33. Hastrup H., Karlin A. and Javitch J. A. (2001) Symmetrical dimer of the human dopamine transporter revealed by cross-linking Cys-306 at the extracellular end of the sixth transmembrane segment. Proc. Natl. Acad. Sci. USA 98: 10055-10060
34. Korkhov V. M., Farhan H., Freissmuth M. and Sitte H. H. (2004) Oligomerization of the g-aminobutyric acid transporter-1 is driven by an interplay of polar and hydrophobic interactions in transmembrane helix II. J. Biol. Chem. 279: 55728-55736
35. Hastrup H., Sen N. and Javitch J. A. (2003) The human dopamine transporter forms a tetramer in the plasma membrane: cross-linking of a cysteine in the fourth transmembrane segment is sensitive to cocaine analogs. J. Biol. Chem. 278: 45045-45048
36. Just H., Sitte H. H., Schmid J. A., Freissmuth M. and Kudlacek O. (2004) Identification of an additional interaction domain in transmembrane domains 11 and 12 that supports oligomer formation in human serotonin transporter. J. Biol. Chem. 279: 6650-6657
37. Yu N., Cao Y., Mager S. and Lester H. A. (1998) Topological localization of cysteine 74 in the GABA transporter, GAT1, and its importance in ion binding and permeation. FEBS Lett. 426: 174-178
38. Zhou Y., Bennet E. R. and Kanner B. I. (2004) The aqueous accessibility in the external half of transmembrane domain I of the GABA transporter GAT-1 is modulated by its ligands. J. Biol. Chem. 279: 13800-13808
39. Hirokawa T., Boon-Chieng S. and Mitaku S. (1998) SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14: 378-379
40. Forlani G., Bossi E., Ghirardelli R., Giovannardi S., Binda F., Bonadiman L. et al. (2001) Mutation K448E in the external loop 5 of rat GABA transporters rGAT1 induces pH sensitivity and alters substrate interactions. J. Physiol. 536: 479-494
41. Soragna A., Bossi E., Giovannardi S., Pisani R. and Peres A. (2005) Relations between substrate affinities and charge equilibration rates in the rat GABA cotransporter GAT1. J. Physiol. 562: 333-345
42. Grossman T. R. and Nelson N. (2003) Effect of sodium lithium and proton concentrations on the electrophysiological properties of the four mouse GABA transporters expressed in Xenopus oocytes. Neurochem. Int. 43: 431-443
43. Kilic F. and Rudnick G. (2000) Oligomerization of serotonin transporter and its functional consequences. Proc. Natl. Acad. Sci. USA 97: 3106-3111
44. Farhan H., Korkhov V. M., Paulitschke V., Dorostkar M. M., Scholze P., Kudlacek O. et al. (2004) Two discontinuous segments in the carboxyl terminal are required for membrane targeting of the rat g-aminobutyric acid transporter-1 (GAT-1). J. Biol. Chem. 279: 28553-28563
45. --coupled neurotransmitter transporters. Eur. J. Pharmacol. 479: 229-236
46. Soragna A., Bossi E., Giovannardi S., Pisani R. and Peres A. (2005) Functionally independent subunits in the oligomeric structure of the GABA cotransporter rGAT 1. Cell. Mol. Life Sci. 23: 2862-2870
47. Torres G. E., Carneiro A., Seamans K., Fiorentini C., Sweeney A., Yao W.-D. et al. (2003) Oligomerization and trafficking of the human dopamine transporter: mutational analysis identifies critical domains important for the functional expression of the transporter. J. Biol. Chem. 278: 2731-2739
48. Seidel S., Singer E. A., Just H., Farhan H., Scholze P., Kudlacek O. et al. (2005) Amphetamines take two to tango: an oligomerbased counter-transport model on neurotransmitter transport explores the amphetamine action. Mol. Pharmacol. 67: 140-151
49. Peres A., Giovannardi S., Bossi E. and Fesce R. (2004) Electrophysiological insights into the mechanism of ion-coupled cotransporters. News Physiol. Sci. 19: 80-84
50. Kaplan R. S., Mayor J. A., Brauer D., Kotaria R., Walters D. E. and Dean A. M. (2000) The yeast mitochondrial citrate transport protein: probing the secondary structure of transmembrane domain IV and identification of residues that likely comprise a portion of the citrate translocation pathway. J. Biol. Chem. 275: 12009-12016
51. Kanner B. I. (2005) Molecular physiology: intimate contact enables transport. Nature 437: 203-205
52. Persson B. and Argos P. (1994) Prediction of transmembrane segments in proteins utilising multiple sequence alignments. J. Mol. Biol. 237: 182-192
53. Krogh A., Larsson B., Heijne G. von and Sonnhammer E. L. (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305: 567-580
54. Tusnady G. E. and Simon I. (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics. 17: 849-850
55. Cserzo M., Wallin E., Simon I., Heijne G. von and Elofsson A. (1997) Prediction of transmembrane alpha-helices in prokaryotic membrane proteins: the dense alignment surface method. Protein Eng. 10: 673-676
56. Hofmann K. and Stoffel W. (1993) TMbase - a database of membrane spanning protein segments. Biol. Chem. Hoppe-Seyler 374: 166-168
57. Jones D. T., Taylor W. R. and Thornton J. M. (1994) A model recognition approach to the prediction of all-helical membrane protein structure and topology. Biochemistry 33: 3038-3049
58. Pasquier C. and Hamodrakas S. J. (1999) An hierarchical artificial neural network system for the classification of transmembrane proteins. Protein Eng. 12: 631-634