Oligomer formation by Na+-Cl--coupled neurotransmitter transporters

European Journal of Pharmacology

Volumn 479, Issue 1-3, 2003, Pages 229-236

  Sitte, Harald H ^a,b   Freissmuth, Michael ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Dimer; FRET (fluorescence resonance energy transfer); Microscopy; Na+ Cl coupled neurotransmitter transporter; Neurotransmitter: Na+ symporter; Oligomer

Indexed keywords

CARRIER PROTEIN; COTRANSPORTER; GLYCOPHORIN; NEUROTRANSMITTER; OLIGOMER; SODIUM ION;

ALPHA HELIX; CELL SURFACE; ENDOPLASMIC RETICULUM; FLUORESCENCE RESONANCE ENERGY TRANSFER MICROSCOPY; GOLGI COMPLEX; HUMAN; MICROSCOPY; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REGULATORY MECHANISM; REVIEW;

EID: 0242469285     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2003.08.072     Document Type: Article

References (96)

1. Adams S.V., DeFelice L.J. Flux coupling in the human serotonin transporter. Biophys. J. 83:2002;3268-3282.
2. Amara S.G., Kuhar M.J. Neurotransmitter transporters: recent progress. Annu. Rev. Neurosci. 16:1993;73-93.
3. Androutsellis-Theotokis A., Goldberg N.R., Ueda K., Beppu T., Beckman M.L., Das S., Javitch J.A., Rudnick G. Characterization of a functional bacterial homologue of sodium-dependent neurotransmitter transporters. J. Biol. Chem. 278:2003;12703-12709.
4. Arkin I.T. Structural aspects of oligomerization taking place between the transmembrane alpha-helices of bitopic membrane proteins. Biochim. Biophys. Acta. 1565:2002;347-363.
5. Arkin I.T., Adams P.D., MacKenzie K.R., Lemmon M.A., Brunger A.T., Engelman D.M. Structural organization of the pentameric transmembrane alpha-helices of phospholamban, a cardiac ion channel. EMBO J. 13:1994;4757-4764.
6. Arkin I.T., Adams P.D., Brunger A.T., Smith S.O., Engelman D.M. Structural perspectives of phospholamban, a helical transmembrane pentamer. Annu. Rev. Biophys. Biomol. Struct. 26:1997;157-179.
7. 3H-Norepinephrine by tissues. Science. 133:1961;383-384.
8. Beliveau R., Demeule M., Jette M., Potier M. Molecular sizes of amino acid transporters in the luminal membrane from the kidney cortex, estimated by the radiation-inactivation method. Biochem. J. 268:1990;195-200.
9. Berger S.P., Farrell K., Conant D., Kempner E.S., Paul S.M. Radiation inactivation studies of the dopamine reuptake transporter protein. Mol. Pharmacol. 46:1994;726-731.
10. Bjerggaard C., Loland C.J., Hastrup H., Madsen K., Javitch J., Gether U. ER export and surface targeting of the dopamine transporter are dependent on the distal C-terminus but occurs independently of PDZ domain interactions. Society for Neuroscience Annual Meeting 2002:2002;. Program #547.13.
11. Burant C.F., Bell G.I. Mammalian facilitative glucose transporters: evidence for similar substrate recognition sites in functionally monomeric proteins. Biochemistry. 31:1992;10414-10420.
12. Busch W., Saier M.H. Jr. The transporter classification (TC) system. Crit. Rev. Biochem. Mol. Biol. 37:2002;287-337.
13. Carroll F.I., Howell L.L., Kuhar M.J. Pharmacotherapies for treatment of cocaine abuse: preclinical aspects. J. Med.Chem. 42:1999;2721-2736.
14. Cesura A.M., Muller K., Peyer M., Pletscher A. Solubilization of imipramine-binding protein from human blood platelets. Eur. J. Pharmacol. 96:1983;235-242.
15. Chen N.H., Reith M.E., Quick M.W. Synaptic uptake and beyond: the sodium- and chloride-dependent neurotransmitter transporter family SLC6. Pflugers Arch. 2003;. (10.1007/s00424-003-1064-5).
16. Choma C., Gratkowski H., Lear J.D., DeGrado W.F. Asparagine-mediated self-association of a model transmembrane helix. Nat. Struct. Biol. 7:2000;161-166.
17. 2+ pump of cardiac sarcoplasmic reticulum. J. Biol. Chem. 275:2000;41487-41494.
18. Cuppoletti J., Goldinger J., Kang B., Jo I., Berenski C., Jung C.Y. Anion carrier in the human erythrocyte exists as a dimer. J. Biol. Chem. 260:1985;15714-15717.
19. DeGrado W.F., Gratkowski H., Lear J.D. How do helix-helix interactions help determine the folds of membrane proteins? Perspectives from the study of homo-oligomeric helical bundles. Protein Sci. 12:2003;647-665.
20. Dehnes Y., Chaudhry F.A., Ullensvang K., Lehre K.P., Storm-Mathisen J., Danbolt N.C. The glutamate transporter EAAT4 in rat cerebellar Purkinje cells: a glutamate-gated chloride channel concentrated near the synapse in parts of the dendritic membrane facing astroglia. J. Neurosci. 18:1998;3606-3619.
21. Dieckmann G.R., DeGrado W.F. Modeling transmembrane helical oligomers. Curr. Opin. Struck. Biol. 7:1997;486-494.
22. Egan M.E., Glockner-Pagel J., Ambrose C., Cahill P.A., Pappoe L., Balamuth N., Cho E., Canny S., Wagner C.A., Geibel J., Caplan M.J. Calcium-pump inhibitors induce functional surface expression of Delta F508-CFTR protein in cystic fibrosis epithelial cells. Nat. Med. 8:2002;485-492.
23. Ellgaard L., Helenius A. Quality control in the endoplasmic reticulum. Nat. Rev., Mol. Cell Biol. 4:2003;181-191.
24. Eskandari S., Wright E.M., Kreman M., Starace D.M., Zampighi G.A. Structural analysis of cloned plasma membrane proteins by freeze-fracture electron microscopy. Proc. Natl. Acad. Sci. U. S. A. 95:1998;11235-11240.
25. Eskandari S., Kreman M., Kavanaugh M.P., Wright E.M., Zampighi G.A. Pentameric assembly of a neuronal glutamate transporter. Proc. Natl. Acad. Sci. U. S. A. 97:2000;8641-8646.
26. + exchanger isoforms NHE1 and NHE3 exist as stable dimers in membranes with a high degree of specificity for homodimers. J. Biol. Chem. 269:1994;2589-2596.
27. Förster T. Zwischenmolekulare Energiewanderung und Fluoreszenz. Ann. Phys. (Leipz.). 2:1948;57-75.
28. Garcia J., Nakai J., Imoto K., Beam K.G. Role of S4 segments and the leucine heptad motif in the activation of an L-type calcium channel. Biophys. J. 72:1997;2515-2523.
29. + antiporter of Escherichia coli in the membrane and its functional and structural consequences. Biochemistry. 40:2001;3403-3412.
30. Golemis E.A., Tew K.D., Dadke D. Protein interaction-targeted drug discovery: evaluating critical issues. Biotechniques. 32:2002;636-638.
31. Gurezka R., Laage R., Brosig B., Langosch D. A heptad motif of leucine residues found in membrane proteins can drive self-assembly of artificial transmembrane segments. J. Biol. Chem. 274:1999;9265-9270.
32. Habert E., Graham D., Langer S.Z. Solubilization and characterization of the 5-hydroxytryptamine transporter complex from rat cerebral cortical membranes. Eur. J. Pharmacol. 122:1986;197-204.
33. Hahn M.K., Robertson D., Blakely R.D. A mutation in the human norepinephrine transporter gene (SLC6A2) associated with Orthostatic Intolerance disrupts surface expression of mutant and wild-type transporters. J. Neurosci. 23:2003;4470-4478.
34. Hastrup H., Karlin A., Javitch J.A. 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. U. S. A. 98:2001;10055-10060.
35. Haugeto O., Ullensvang K., Levy L.M., Chaudhry F.A., Honore T., Nielsen M., Lehre K.P., Danbolt N.C. Brain glutamate transporter proteins form homomultimers. J. Biol. Chem. 271:1996;27715-27722.
36. Heldin C.H. Dimerization of cell surface receptors in signal transduction. Cell. 80:1995;213-223.
37. Horiuchi M., Nicke A., Gomeza J., Aschrafi A., Schmalzing G., Betz H. Surface-localized glycine transporters 1 and 2 function as monomeric proteins in Xenopus oocytes. Proc. Natl. Acad. Sci. U. S. A. 98:2001;1448-1453.
38. Iversen L. Neurotransmitter transporters: fruitful targets for CNS drug discovery. Mol. Psychiatry. 5:2000;357-362.
39. Jennings M.L., Smith J.S. Anion-proton cotransport through the human red blood cell band 3 protein. Role of glutamate 681. J. Biol. Chem. 267:1992;13964-13971.
40. Jentsch T.J. Chloride channels are different. Nature. 415:2002;276-277.
41. Jess U., Betz H., Schloss P. The membrane-bound rat serotonin transporter, SERT1, is an oligomeric protein. FEBS Lett. 394:1996;44-46.
42. Just H., Sitte H.H., Freissmuth M., Kudlacek O. The carboxy terminal half of the human serotonin transporter contains a second oligomerization domain. Naunyn-Schmiedeberg's Arch. Pharmacol. 367:2003;R5.
43. Kent J.M. SNaRIs, NaSSAs, and NaRIs: new agents for the treatment of depression. Lancet. 355:2000;911-918.
44. Kilic F., Rudnick G. Oligomerization of serotonin tranporter and its functional consequences. Proc. Natl. Acad. Sci. U. S. A. 97:2000;3106-3111.
45. Kitayama S., Ikeda T., Mitsuhata C., Sato T., Morita K., Dohi T. Dominant negative isoform of rat norepinephrine transporter produced by alternative RNA splicing. J. Biol. Chem. 274:1999;10731-10736.
46. Klingenberg M. Membrane protein oligomeric structure and transport function. Nature. 290:1981;449-454.
47. Kocabas A.M., Rudnick G., Kilic F. Functional consequences of homo- but not hetero-oligomerization between transporters for the biogenic amine neurotransmitters. J. Neurochem. 85:2003;1513-1520.
48. Köhler K., Forster I.C., Lambert G., Biber J., Murer H. The functional unit of the renal type IIa Na+/Pi cotransporter is a monomer. J. Biol. Chem. 275:2000;26113-26120.
49. Lee F.J., Pristupa Z.B., Ciliax B.J., Levey A.I., Niznik H.B. The dopamine transporter carboxyl-terminal tail. Truncation/substitution mutants selectively confer high affinity dopamine uptake while attenuating recognition of the ligand binding domain. J. Biol. Chem. 271:1996;20885-20894.
50. Lemmon M.A., Treutlein H.R., Adams P.D., Brunger A.T., Engelman D.M. A dimerization motif for transmembrane alpha-helices. Nat. Struct. Biol. 1:1994;157-163.
51. +-dependent phlorizin binding and Na+-dependent D-glucose transport. Biochim. Biophys. Acta. 777:1984;201-208.
52. Liu Y., Engelman D.M., Gerstein M. Genomic analysis of membrane protein families: abundance and conserved motifs. Genome Biol. 3(10):2002;. (research 0054.1-0054.12).
53. Lopez-Corcuera B., Alcantara R., Vazquez J., Aragon C. Hydrodynamic properties and immunological identification of the sodium- and chloride-coupled glycine transporter. J. Biol. Chem. 268:1993;2239-2243.
54. Macara I.G., Cantley L.C. Interactions between transport inhibitors at the anion binding sites of the band 3 dimer. Biochemistry. 20:1981;5095-5105.
55. MacKenzie K.R., Prestegard J.H., Engelman D.M. A transmembrane helix dimer: structure and implications. Science. 276:1997;131-133.
56. Masson J., Sagne C., Hamon M., el Mestikawy S. Neurotransmitter transporters in the central nervous system. Pharmacol. Rev. 51:1999;439-464.
57. McCormack K., Tanouye M.A., Iverson L.E., Lin J.W., Ramaswami M., McCormack T., Campanelli J.T., Mathew M.K., Rudy B. A role for hydrophobic residues in the voltage-dependent gating of Shaker K+ channels. Proc. Natl. Acad. Sci. U. S. A. 88:1991;2931-2935.
58. Milligan G., White J.H. Protein-protein interactions at G-protein-coupled receptors. Trends Pharmacol. Sci. 22:2001;513-518.
59. Milner H.E., Beliveau R., Jarvis S.M. The in situ size of the dopamine transporter is a tetramer as estimated by radiation inactivation. Biochim. Biophys. Acta. 1190:1994;185-187.
60. Murakami S., Nakashima R., Yamashita E., Yamaguchi A. Crystal structure of bacterial multidrug efflux transporter AcrB. Nature. 419:2002;587-593.
61. (2+) site engineering at the oligomeric interface of the dopamine transporter. FEBS Lett. 524:2002;87-91.
62. Pankevych H., Korkhov V., Freissmuth M., Nanoff C. Truncation of the A1-adenosine receptor reveals distinct roles of the membrane-proximal carboxy terminus in receptor folding and G protein coupling. J. Biol. Chem. 2003;. (10.1074/jbc.M212918200).
63. - channel is functional when retained in endoplasmic reticulum of mammalian cells. J. Biol. Chem. 270:1995;12347-12350.
64. Petäjä-Repo U.E., Hogue M., Laperriere A., Bhalla S., Walker P., Bouvier M. Newly synthesized human delta opioid receptors retained in the endoplasmic reticulum are retrotranslocated to the cytosol, deglycosylated, ubiquitinated, and degraded by the proteasome. J. Biol. Chem. 276:2001;4416-4423.
65. 3H]citalopram binding proteins. Eur. J. Pharmacol. 189:1990;129-134.
66. Pollok B.A., Heim R. Using GFP in FRET-based applications. Trends Cell Biol. 9:1999;57-60.
67. Popot J.L., Engelman D.M. Helical membrane protein folding, stability, and evolution. Annu. Rev. Biochem. 69:2000;881-922.
68. Ramamoorthy S., Bauman A.L., Moore K.R., Han H., Yang F.T., Chang A.S., Ganapathy V., Blakely R.D. Antidepressant- and cocaine-sensitive human serotonin transporter: molecular cloning, expression, and chromosomal localization. Proc. Natl. Acad. Sci. U. S. A. 90:1993;2542-2546.
69. Ramsey I.S., DeFelice L.J. Serotonin transporter function and pharmacology are sensitive to expression level: evidence for an endogenous regulatory factor. J. Biol. Chem. 277:2002;14475-14482.
70. Reggiori F., Pelham H.R. A transmembrane ubiquitin ligase required to sort membrane proteins into multivesicular bodies. Nat. Cell Biol. 4:2002;117-123.
71. Riven I., Kalmanzon E., Segev L., Reuveny E. Conformational rearrangements associated with the gating of the G protein-coupled potassium channel revealed by FRET Microscopy. Neuron. 38:2003;225-235.
72. Rosenmund C., Stern-Bach Y., Stevens C.F. The tetrameric structure of a glutamate receptor channel. Science. 280:1998;1596-1599.
73. Rudnick G., Clark J. From synapse to vesicle: the reuptake and storage of biogenic amine neurotransmitters. Biochim. Biophys. Acta. 1144:1993;249-263.
74. Schloss P., Williams D.C. The serotonin transporter: a primary target for antidepressant drugs. J. Psychopharmacol. 12:1998;115-121.
75. Schmid J.A., Sitte H.H. Fluorescence resonance energy transfer in the study of cancer pathways. Curr. Opin. Oncol. 15:2003;55-64.
76. Schmid J.A., Scholze P., Kudlacek O., Freissmuth M., Singer E.A., Sitte H.H. 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. 276:2001;3805-3810.
77. Scholze P., Zwach J., Kattinger A., Pifl C., Singer E.A., Sitte H.H. Transporter-mediated release: a superfusion study on human embryonic kidney cells stably expressing the human serotonin transporter. J. Pharmacol. Exp. Ther. 293:2000;870-878.
78. Scholze P., Norregaard L., Singer E.A., Freissmuth M., Gether U., Sitte H.H. The role of zinc ions in reverse transport mediated by monoamine transporters. J. Biol. Chem. 277:2002;21505-21513.
79. Scholze P., Freissmuth M., Sitte H.H. Mutations within an intramembrane leucine heptad repeat disrupt oligomer formation of the rat GABA transporter 1. J. Biol. Chem. 277:2002;43682-43690.
80. Seal R.P., Amara S.G. Excitatory amino acid transporters: a family in flux. Annu. Rev. Pharmacol. Toxicol. 39:1999;431-456.
81. Sonders M.S., Amara S.G. Channels in transporters. Curr. Opin. Neurobiol. 6:1996;294-302.
82. Sorkina T., Doolen S., Galperin E., Zahniser N.R., Sorkin A. Oligomerization of dopamine transporters visualized in living cells by FRET microscopy. J. Biol. Chem. 2003;. (10.1074/jbc.M210652200).
83. Soskine M., Steiner-Mordoch S., Schuldiner S. Crosslinking of membrane-embedded cysteines reveals contact points in the EmrE oligomer. Proc. Natl. Acad. Sci. U. S. A. 99:2002;12043-12048.
84. Stevens B.R., Fernandez A., Hirayama B., Wright E.M., Kempner E.S. Intestinal brush border membrane Na+/glucose cotransporter functions in situ as a homotetramer. Proc. Natl. Acad. Sci. U. S. A. 87:1990;1456-1460.
85. Torres G.E., Carneiro A., Seamans K., Fiorentini C., Sweeney A., Yao W.D., Caron M.G. Oligomerization and trafficking of the human dopamine transporter. Mutational analysis identifies critical domains important for the functional expression of the transporter. J. Biol. Chem. 278:2003;2731-2739.
86. Veenhoff L.M., Heuberger E.H., Poolman B. The lactose transport protein is a cooperative dimer with two sugar translocation pathways. EMBO J. 20:2001;3056-3062.
87. Veenhoff L.M., Heuberger E.H., Poolman B. Quaternary structure and function of transport proteins. Trends Biochem. Sci. 27:2002;242-249.
88. Veyhl M., Spangenberg J., Puschel B., Poppe R., Dekel C., Fritzsch G., Haase W., Koepsell H. Cloning of a membrane-associated protein which modifies activity and properties of the Na(+)-D-glucose cotransporter. J. Biol. Chem. 268:1993;25041-25053.
89. Weiner D.B., Liu J., Cohen J.A., Williams W.V., Greene M.I. A point mutation in the neu oncogene mimics ligand induction of receptor aggregation. Nature. 339:1989;230-231.
90. White S.H., Wimley W.C. Membrane protein folding and stability: physical principles. Annu. Rev. Biophys. Biomol. Struct. 28:1999;319-365.
91. Wigley W.C., Corboy M.J., Cutler T.D., Thibodeau P.H., Oldan J., Lee M.G., Rizo J., Hunt J.F., Thomas P.J. A protein sequence that can encode native structure by disfavoring alternate conformations. Nat. Struct. Biol. 9:2002;381-388.
92. Williams K.A. Three-dimensional structure of the ion-coupled transport protein NhaA. Nature. 403:2000;112-115.
93. Williams K.A., Geldmacher-Kaufer U., Padan E., Schuldiner S., Kuhlbrandt W. Projection structure of NhaA, a secondary transporter from Escherichia coli, at 4.0 A resolution. EMBO J. 18:1999;3558-3563.
94. Wouters F.S., Verveer P.J., Bastiaens P.I. Imaging biochemistry inside cells. Trends Cell Biol. 11:2001;203-211.
95. Zhou F.X., Cocco M.J., Russ W.P., Brunger A.T., Engelman D.M. Interhelical hydrogen bonding drives strong interactions in membrane proteins. Nat. Struct. Biol. 7:2000;154-160.
96. Zhou F.X., Merianos H.J., Brunger A.T., Engelman D.M. Polar residues drive association of polyleucine transmembrane helices. Proc. Natl. Acad. Sci. U. S. A. 98:2001;2250-2255.