Delineation of an endogenous zinc-binding site in the human dopamine transporter

EMBO Journal

Volumn 17, Issue 15, 1998, Pages 4266-4273

  Norregaard, Lene ^a,b   Frederiksen, Dorte ^a   Nielsen, Elsebet Ø ^b   Gether, Ulrik ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b NEUROSEARCH A S   (Denmark)

Author keywords

Dopamine; Membrane protein structure; Metal ion site; Na+ Cl dependent transporters; Transmembrane transport

Indexed keywords

DOPAMINE TRANSPORTER; NEUROTRANSMITTER; NORADRENALIN; PROTEIN; SODIUM CHLORIDE; ZINC ION;

ANIMAL CELL; ARTICLE; CELL STRAIN COS1; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DOPAMINERGIC TRANSMISSION; GENETIC CONSERVATION; HUMAN; NONHUMAN; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CARRIER PROTEINS; COCAINE; CONSERVED SEQUENCE; COS CELLS; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; DOPAMINE UPTAKE INHIBITORS; HISTIDINE; HUMANS; MEMBRANE GLYCOPROTEINS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NERVE TISSUE PROTEINS; NOREPINEPHRINE; NOREPINEPHRINE PLASMA MEMBRANE TRANSPORT PROTEINS; SYMPORTERS; ZINC;

EID: 0032480011     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.15.4266     Document Type: Article

References (43)

1. Amara, S.G. and Kuhar, M.J. (1993) Neurotransmitter transporters: recent progress. Annu. Rev. Neurosci., 16, 73-93.
2. 2+ from brain tissue during activity. Nature, 308, 734-736.
3. Barker, E.L. and Blakely, R.D. (1996) Identification of a single amino acid, phenylalanine 586, that is responsible for high affinity interactions of tricyclic antidepressants with the human serotonin transporter. Mol. Pharmacol., 50, 957-965.
4. Barker, E.L., Kimmel, H.L. and Blakely, R.D. (1994) Chimeric human and rat serotonin transporters reveal domains involved in recognition of transporter ligands. Mol. Pharmacol., 46, 799-807.
5. Bismuth, Y., Kavanaugh, M.P. and Kanner, B.I. (1997) Tyrosine 140 of the gamma-aminobutyric acid transporter GAT-1 plays a critical role in neurotransmitter recognition. J. Biol. Chem., 272, 16096-16102.
6. 2+. Mol. Pharmacol., 46, 1156-1159.
7. 2+. Eur. J. Pharmacol., 266, 87-97.
8. Buck, K.J. and Amara, S.G. (1994) Chimeric dopamine-norepinephrine transporters delineate structural domains influencing selectivity for catecholamines and 1-methyl-4-phenylpyridinium. Proc. Natl Acad. Sci. USA, 91, 12584-12588.
9. Buck, K.J. and Amara, S.G. (1995) Structural domains of catecholamine transporter chimeras involved in selective inhibition by antidepressants and psychomotor stimulants. Mol. Pharmacol., 48, 1030-1037.
10. Chen, J.G., Liu-Chen, S. and Rudnick, G. (1997a) External cysteine residues in the serotonin transporter. Biochemistry, 36, 1479-1486.
11. Chen, J.G., Sachpatzidis, A. and Rudnick, G. (1997b) The third transmembrane domain of the serotonin transporter contains residues associated with substrate and cocaine binding. J. Biol. Chem., 272, 28321-28327.
12. Dexter, D.T., Wells, F.R., Lees, A.J., Agid, F., Agid, Y., Jenner, P. and Marsden, C.D. (1989) Increased nigral iron content and alterations in other metal ions occurring in brain in Parkinson's disease. J. Neurochem., 52, 1830-1836.
13. Elling, C.E. and Schwartz, T.W. (1996) Connectivity and orientation of the seven helical bundle in the tachykinin NK-1 receptor probed by zinc site engineering. EMBO J., 15, 6213-6219.
14. Elling, C.E., Nielsen, S.M. and Schwartz, T.W. (1995) Conversion of antagonist-binding site to metal-ion site in the tachykinin NK-1 receptor. Nature, 374, 74-77.
15. Frederickson, C.J. (1989) Neurobiology of zinc and zinc-containing neurons. Int. Rev. Neurobiol., 31, 145-238.
16. Frederickson, C.J., Howell, G.A. and Kaserskis, E.J. (1984) The neurobiology of zinc. In Neurology and Neurobiology. Alan R. Liss, Inc., New York.
17. Gether, U., Marray, T., Schwartz, T.W. and Johansen, T.E. (1992) Stable expression of high affinity NK1 (substance P) and NK2 (neurokinin A) receptors but low affinity NK3 (neurokinin B) receptors in transfected CHO cells. FEBS Lett., 296, 241-244.
18. Giros, B. and Caron, M.G. (1993) Molecular characterization of the dopamine transporter. Trends Pharmacol. Sci., 14, 43-49.
19. Giros, B., el Mestikawy, S., Godinot, N., Zheng, K., Han, H., Yang-Feng, T. and Caron, M.G. (1992) Cloning, pharmacological characterization and chromosome assignment of the human dopamine transporter. Mol. Pharmacol., 42, 383-390.
20. Giros, B., Wang, Y.M., Suter, S., McLeskey, S.B., Pifl, C. and Caron, M.G. (1994) Delineation of discrete domains for substrate, cocaine and tricyclic antidepressant interactions using chimeric dopamine-norepinephrine transporters. J. Biol. Chem., 269, 15985-15988.
21. Giros, B., Jaber, M., Jones, S.R., Wightman, R.M. and Caron, M.G. (1996) Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature, 379, 606-612.
22. Glusker, J.P. (1991) Structural aspects of metal liganding to functional groups in proteins. In Anfinsen, C.B., Richards, F.M. and Eisenberg, D.S. (eds), Advances in Protein Chemistry, Metalloproteins: Structural Aspects. Vol. 42. Academic Press, Inc., San Diego, CA, pp. 3-66.
23. He, M.M., Voss, J., Hubbell, W.L. and Kaback, H.R. (1995) Use of designed metal-binding sites to study helix proximity in the lactose permease of Escherichia coli. 2. Proximity of helix IX (Arg302) with helix X (His322 and Glu325). Biochemistry, 34, 15667-15670.
24. Hollmann, M., Boulter, J., Maron, C., Beasley, L., Sullivan, J., Pecht, G. and Heinemann, S. (1993) Zinc potentiates agonist-induced currents at certain splice variants of the NMDA receptor. Neuron, 10, 943-954.
25. A receptors. Mol. Pharmacol., 53, 870-877.
26. Horn, A.S. (1990) Dopamine uptake: a review of progress in the last decade. Prog. Neurobiol., 34, 387-400.
27. Huang, E.P. (1997) Metal ions and synaptic transmission: think zinc. Proc. Natl Acad. Sci. USA, 94, 13386-13387.
28. Johansen, T.E., Scholler, M.S., Tolstoy, S. and Schwartz, T.W. (1990) Biosynthesis of peptide precursors and protease inhibitors using new constitutive and inducible eukaryotic expression vectors. FEBS Lett., 267, 289-294.
29. Kitayama, S., Shimada, S., Xu, H., Markham, L., Donovan, D.M. and Uhl, G.R. (1992) Dopamine transporter site-directed mutations differentially alter substrate transport and cocaine binding. Proc. Natl Acad. Sci. USA, 89, 7782-7785.
30. Laube, B., Kuhse, J., Rundstrom, N., Kirsch, J., Schmieden, V. and Betz, H. (1995) Modulation by zinc ions of native rat and recombinant human inhibitory glycine receptors. J. Physiol. (Lond.), 483, 613-619.
31. Palmiter, R.D., Cole, T.B., Quaife, C.J. and Findley, S.D. (1996) ZnT-3, a putative transporter of zinc into synaptic vesicles. Proc. Natl Acad. Sci. USA, 93, 14934-14939.
32. Pantanowitz, S., Bendahan, A. and Kanner, B.I. (1993) Only one of the charged amino acids located in the transmembrane alpha-helices of the gamma-aminobutyric acid transporter (subtype A) is essential for its activity. J. Biol. Chem., 268, 3222-3225.
33. Peters, S., Koh, J. and Choi, D.W. (1987) Zinc selectively blocks the action of N-methyl-D-aspartate on cortical neurons. Science, 236, 589-593.
34. Pifl, C., Giros, B. and Caron, M.G. (1993) Dopamine transporter expression confers cytotoxicity to low doses of the parkinsonism-inducing neurotoxin 1-methyl-4-phenylpyridinium. J. Neurosci., 13, 4246-4253.
35. Richfield, E.K. (1993) Zinc modulation of drug binding, cocaine affinity states and dopamine uptake on the dopamine uptake complex. Mol. Pharmacol., 43, 100-108.
36. Schwabe, J.W. and Klug, A. (1994) Zinc mining for protein domains. Nature Struct. Biol., 1, 345-349.
37. Sheikh, S.P., Zvyaga, T.A., Lichtarge, O., Sakmar, T.P. and Bourne, H.R. (1996) Rhodopsin activation blocked by metal-ion-binding sites linking transmembrane helices C and F. Nature, 383, 347-350.
38. Stephan, M.M., Chen, M.A., Penado, K.M. and Rudnick, G. (1997) An extracellular loop region of the serotonin transporter may be involved in the translocation mechanism. Biochemistry, 36, 1322-1328.
39. Vallee, B.L. and Falchuk, K.H. (1993) The biochemical basis of zinc physiology. Physiol. Rev., 73, 79-118.
40. Wang, J.B., Moriwaki, A. and Uhl, G.R. (1995) Dopamine transporter cysteine mutants: second extracellular loop cysteines are required for transporter expression. J. Neurochem., 64, 1416-1419.
41. Wang, T.L., Hackam, A., Guggino, W.B. and Cutting, G.R. (1995) A single histidine residue is essential for zinc inhibition of GABA rho 1 receptors. J. Neurosci., 15, 7684-7691.
42. Wenzel, H.J., Cole, T.B., Born, D.E., Schwartzkroin, P.A. and Palmiter, R.D. (1997) Ultrastructural localization of zinc transporter-3 (ZnT-3) to synaptic vesicle membranes within mossy fiber boutons in the hippocampus of mouse and monkey. Proc. Natl Acad. Sci. USA, 94, 12676-12681.
43. 2+ antagonize NMDA and GABA responses of hippocampal neurons. Nature, 328, 640-643.