An intermediate state of the γ-aminobutyric acid transporter GAT1 revealed by simultaneous voltage clamp and fluorescence

Journal of General Physiology

Volumn 115, Issue 4, 2000, Pages 491-508

  Li, Ming ^a   Farley, Robert A ^a   Lester, Henry A ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Conformational change; Tetramethylrhodamine; Voltage clamp; Xenopus oocyte

Indexed keywords

4 AMINOBUTYRIC ACID; RHODAMINE; SODIUM CHLORIDE;

ARTICLE; CELL TRANSPORT; CONFORMATIONAL TRANSITION; FLUORESCENCE ANALYSIS; HYPERPOLARIZATION; MEMBRANE POTENTIAL; NEUROTRANSMISSION; NONHUMAN; VOLTAGE CLAMP; XENOPUS;

ANIMALS; CARRIER PROTEINS; ELECTROPHYSIOLOGY; FLUORESCENT DYES; GABA PLASMA MEMBRANE TRANSPORT PROTEINS; GAMMA-AMINOBUTYRIC ACID; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MICROSCOPY, FLUORESCENCE; MUTATION; OOCYTES; ORGANIC ANION TRANSPORTERS; PATCH-CLAMP TECHNIQUES; PROTEIN CONFORMATION; QUATERNARY AMMONIUM COMPOUNDS; RATS; RHODAMINES; SODIUM; XENOPUS LAEVIS;

EID: 0034031645     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.115.4.491     Document Type: Article

References (52)

1. Amara, S.G., and M. Kuhar. 1993. Neurotransmitter transporters: recent progress. Annu. Rev. Neurosci. 16:73-93.
2. + channel gating. Neuron. 20:1283-1294.
3. Bendahan, A., and B.I. Kanner. 1993. Identification of domains of a cloned rat-brain GABA transporter which are not required for its functional expression. FEBS Lett. 318:41-44.
4. -)-coupled γ-aminobutyric acid transporter from rat brain. J. Biol. Chem. 272:1203-1210.
5. Blakely, R.D., H.E. Berson, J.R.T. Fremeau, 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. 354:66-70.
6. Cammack, J.N., S.V. Rakhilin, and E.A. Schwartz. 1994. A GABA transporter operates asymmetrically and with variable stoichiometry. Neuron. 13:949-960.
7. Cammack, J.N., and E.A. Schwartz. 1996. Channel behavior in a GABA transporter. Proc. Natl. Acad. Sci. USA. 93:723-727.
8. + channel with fluorescence. Neuron. 19:1127-1140.
9. + channel. J. Gen. Physiol. 112: 391-408.
10. Eskandari, S., E.M. Wright, M. Kreman, D.M. Starace, and G.A. Zampighi. 1998. Structural analysis of cloned plasma membrane proteins by freeze-fracture electron microscopy. Proc. Natl. Acad. Sci. USA. 95:11235-11240.
11. Galli, A., R.D. Blakely, and L.J. DeFelice. 1998. Patch-clamp and amperometric recordings from norepinephrine transporters: channel activity and voltage-dependent uptake. Proc. Natl. Acad. Sci. USA. 95:13260-13265.
12. Golovanevsky, V., and B.I. Kanner. 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.
13. Guastella, J.G., N. Nelson, H. Nelson, L. Czyzyk, S. Keynan, M.C. Midel, N. Davidson, H.A. Lester, and B. Kanner. 1990. Cloning and expression of a rat brain GABA transporter. Science. 249: 1303-1306.
14. -) cotransport function. Database reconstruction with an alternating access model. J. Gen. Physiol. 114:459-476.
15. Hoffman, B.J., E. Mezey, and M.J. Brownstein. 1991. Cloning of a serotonin transporter affected by antidepressants. Science. 254: 579-580.
16. Kanner, B.I. 1978. Solubilization and reconstitution of the γ-aminobutyric acid transporter from rat brain. FEBS Lett. 89:47-50.
17. Kanner, B.I., and A. Bendahan. 1982. Binding order of substrates to the sodium and potassium ion coupled L-glutamic acid transporter from rat brain. Biochemistry. 21:6327-6330.
18. Kleinberger-Doron, N., and B.I. Kanner. 1994. Identification of tryptophan residues critical for the function and targeting of the γ-aminobutyric acid transporter (subtype A). J. Biol. Chem. 269: 3063-3067.
19. Kluger, R., and W.C. Tsui. 1980. Amino group reactions of the sulfhydryl reagent methyl methanesulfonothioate. Inactivation of D-3-hydroxybutyrate dehydrogenase and reaction with amines in water. Can. J. Biochem. 58:629-632.
20. Kuhar, M.J., M.C. Ritz, and J.W. Boja. 1991. The dopamine hypothesis of the reinforcing properties of cocaine. Trends Neurosci. 144: 299-302.
21. Lester, H.A., Y. Cao, and S. Mager. 1996. Listening to neurotransmitter transporters. Neuron. 17:807-810.
22. + and glucose transport. Proc. Natl. Acad. Sci. USA. 95:7789-7794.
23. + channel. J. Gen. Physiol. 112: 377-389.
24. -) cotransport function. Kinetic studies in giant Xenopus oocyte membrane patches. J. Gen. Physiol. 114:445-458.
25. -) cotransport function. Steady state studies in giant Xenopus oocyte membrane patches. J. Gen. Physiol. 114:429-444.
26. Lu, C.-C., A. Kabakov, V.S. Markin, S. Mager, A. Frazier, and D.W. Hilgemann. 1996. Membrane transport mechanisms probed by capacitance measurements with megahertz voltage clamp. Proc. Natl. Acad. Sci.USA. 92:11220-11224.
27. Mabjeesh, N.J., and B.I. Kanner. 1992. Neither amino nor carboxyl termini are required for function of the sodium- and chloride-coupled γ-aminobutyric acid transporter from rat brain. J. Biol. Chem. 267:2563-2568.
28. Mager, S., Y. Cao, and H.A. Lester. 1998. Measurement of transient currents from neurotransmitter transporters expressed in Xenopus oocytes. Methods Enzymol. 296:551-566.
29. Mager, S., N. Kleinberger-Doron, G.I. Keshet, N. Davidson, B.I. Kanner, and H.A. Lester. 1996. Ion binding and permeation at the GABA transporter GAT1. J. Neurosci. 16:5405-5414.
30. Mager, S., C. Min, D.J. Henry, C. Chavkin, B.J. Hoffman, N. Davidson, and H.A. Lester. 1994. Conducting states of a mammalian serotonin transporter. Neuron. 12:845-859.
31. Mager, S., J. Naeve, M. Quick, J. Guastella, N. Davidson, and H.A. Lester. 1993. Steady states, charge movements, and rates for a cloned GABA transporter expressed in Xenopus oocytes. Neuron. 10:177-188.
32. Mannuzzu, L.M., M.M. Moronne, and E.Y. Isacoff. 1996. Direct physical measure of conformational rearrangement underlying potassium channel gating. Science. 271:213-216.
33. Means, G., and R.E. Feeney. 1971. Chemical Modification of Proteins. Holden-Day, Inc., San Francisco, CA. 105-114.
34. Pacholczyk, T., R.D. Blakely, and S.G. Amara. 1991. Expression cloning of a cocaine-sensitive and antidepressant-sensitive human noradrenaline transporter. Nature. 350:350-354.
35. Pantanowitz, S., A. Bandahan, and B.I. Kanner. 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. 286:3222-3225.
36. Pastuszko, A., D.F. Wilson, and M. Erecinska. 1982. Energetics of γ-aminobutyrate transport in rat brain synaptosomes. J. Biol. Chem. 257:7514-7519.
37. Penado, K.M., G. Rudnick, and M.M. Stephan. 1998. Critical amino acid residues in transmembrane span 7 of the serotonin transporter identified by random mutagenesis. J. Biol. Chem. 273: 28098-28106.
38. Petersen, C.I., and L.J. DeFelice. 1999. Ionic interactions in the Drosophila serotonin transporter identify it as a serotonin channel. Nat. Neurosci. 2:605-610.
39. Quick, M.W., and H.A. Lester. 1994. Methods for expression of excitability proteins in Xenopus oocytes. Methods Neurosci. 19:261-279.
40. Radian, R., and B.I. Kanner. 1983. Stoichiometry of sodium- and chloride-coupled γ-aminobutyric acid transport by synaptic plasma membrane vesicles isolated from rat brain. Biochemistry. 22:142-168.
41. Radian, R., and B.I. Kanner. 1985. Reconstitution and purification of the sodium- and chloride-coupled g-aminobutyric acid transporter from rat brain. J. Biol. Chem. 260:11859-11865.
42. Risso, S., L.J. DeFelice, and R.D. Blakely. 1996. Sodium-dependent GABA-induced currents in GAT1-transfected HeLa cells. J. Physiol. 490:691-702.
43. Rudnick, G. 1977. Active transport of 5-hydroxytryptamine in plasma membrane vesicles isolated from human blood platelets. J. Biol. Chem. 252:2170-2174.
44. Rudnick, G., and P.J. Nelson. 1978. Plalelet 5-hydroxytryptamine transport, an electroneutral mechanism coupled to potassium. Biochemistry. 17:4739-4742.
45. Shimada, S., S. Kitayama, C.L. Lin, A. Patel, E. Nanthakumar, M. Kuhar, and G. Uhl. 1991. Cloning and expression of a cocaine-sensitive dopainine transporter complementary-DNA. Science. 254:576-578.
46. Siegel, M.S., and E.V. Isacoff. 1997. A genetically encoded optical probe of membrane voltage. Neuron. 19:735-741.
47. Sonders, M., S.-J. Zhu, N. Zahniser, M. Kavanaugh, and S. Amara. 1997. Multiple ionic conductances of the human dopamine transporter: the actions of dopamine and psychostimulants. J. Neurosci. 17:960-974.
48. +, and methansulfonate reagents. Soc. Neurosci. Abstr. 25:1699.
49. Su, A., S. Mager, S.L. Mayo, and H.A. Lester. 1996. A multi-substrate single-file model for ion-coupled transporters. Biophys. J. 70:762-777.
50. Tamura, S., H. Nelson, A. Tamura, and N. Nelson. 1995. Short external loops as potential substrate binding site of γ-aminobutyric acid transporters. J. Biol. Chem. 270:28712-28715.
51. Usdin, T.B., E. Mezey, C. Chen, M.J. Brownstein, and B.J. Hoffman. 1991. Cloning of the cocaine-sensitive bovine dopamine transporter. Proc. Natl. Acad. Sci. USA. 88:11168-11171.
52. Yu, N., Y. Cao, S. Mager, and H.A. Lester. 1998. Topological localization of cysteine 74 in the GABA transporter, GAT1, and its importance in ion binding and permeation. FEBS Lett. 426:174-178.