Synaptic uptake and beyond: The sodium- and chloride-dependent neurotransmitter transporter family SLC6

Pflugers Archiv European Journal of Physiology

Volumn 447, Issue 5, 2004, Pages 519-531

  Chen, Nian Hang ^b   Reith, Maarten E A ^b   Quick, Michael W ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF ILLINOIS   (United States)

Author keywords

Amine; Amino acid; Neurotransmitter; Osmolyte balance; Synaptic transmission; Uptake

Indexed keywords

1 (4,4 DIPHENYL 3 BUTENYL)GUVACINE; 1 (4,4 DIPHENYL 3 BUTENYL)NIPECOTIC ACID; 1 [2 (BENZHYDRYLIDENEAMINOOXY)ETHYL] 1,2,5,6 TETRAHYDRO 3 PYRIDINECARBOXYLIC ACID; 4 AMINOBUTYRIC ACID TRANSPORTER 1; 4 AMINOBUTYRIC ACID TRANSPORTER 2; 4 AMINOBUTYRIC ACID TRANSPORTER 3; 4 AMINOBUTYRIC ACID TRANSPORTER 4; [N [3 (4' FLUOROPHENYL) 3 (4' PHENYLPHENOXY)PROPYL]]SARCOSINE; ALX 5407; AMINO ACID TRANSPORTER; ANTICONVULSIVE AGENT; ANTIDEPRESSANT AGENT; BETAINE TRANSPORTER 1; CARRIER PROTEIN; CHLORIDE; CREATINE TRANSPORTER 1; CREATINE TRANSPORTER 2; DOPAMINE TRANSPORTER; DOPAMINE UPTAKE INHIBITOR; GLYCINE TRANSPORTER 1; GLYCINE TRANSPORTER 2; NEUROTRANSMITTER; NORADRENALIN TRANSPORTER; NORADRENALIN UPTAKE INHIBITOR; PROLINE TRANSPORTER; SARCOSINE; SEROTONIN TRANSPORTER; SEROTONIN UPTAKE INHIBITOR; SODIUM; TAURINE TRANSPORTER; UNCLASSIFIED DRUG; UNINDEXED DRUG;

AMINO ACID COMPOSITION; AMINO TERMINAL SEQUENCE; ANXIETY DISORDER; AUTISM; BEHAVIOR DISORDER; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE TRANSPORT; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; CHLORIDE TRANSPORT; CYTOPLASM; DEPRESSION; DOPAMINERGIC TRANSMISSION; DRUG ABUSE; DRUG TARGETING; ELECTROCHEMISTRY; GABAERGIC SYSTEM; GASTROINTESTINAL DISEASE; GENE; GENE MUTATION; GENETIC POLYMORPHISM; HUMAN; INTESTINE; KIDNEY; MENTAL DISEASE; NERVE CELL; NEUROLOGIC DISEASE; NEUROMODULATION; NEUROTRANSMITTER UPTAKE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; PERIPHERAL NERVOUS SYSTEM; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; REVIEW; SCHIZOPHRENIA; SIGNAL TRANSDUCTION; SLC6 GENE; SLC6A1 GENE; SLCA11 GENE; SLCA13 GENE; SODIUM TRANSPORT; SOLUTE; SUBSTANCE ABUSE; SUICIDE; SYNAPTIC TRANSMISSION; TESTIS; TISSUE DISTRIBUTION; TRANSGENIC ANIMAL;

BIOLOGICAL TRANSPORT; CHLORIDES; HUMANS; MEMBRANE TRANSPORT PROTEINS; MULTIGENE FAMILY; NEUROTRANSMITTER AGENTS; SODIUM; SYNAPSES;

EID: 1242295211     PISSN: 00316768     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00424-003-1064-5     Document Type: Review

References (83)

1. Adkins EM, Barker EL, Blakely RD (2001) Interactions of tryptamine derivatives with serotonin transporter species variants implicate transmembrane domain 1 in substrate recognition. Mol Pharmacol 59:514-523
2. Androutsellis-Theotokis A, Goldberg NR, Ueda K, Beppu T, Beckman ML, Das S, Javitch JA Rudnick G (2003) Characterization of a functional bacterial homologue of sodium-dependent neurotransmitter transporters. J Biol Chem 278:12703-12709
3. Atkinson BN, Bell SC, De Vivo M, Kowalski LR, Lechner SM, Ognyanov VI, Tham CS, Tsai C, Jia J, Ashton D, Klitenick MA (2001) ALX 5407: a potent, selective inhibitor of the hGlyT1 glycine transporter. Mol Pharmacol 60:1414-1420
4. Aubrey KR, Mitrovic AD, Vandenberg RJ (2000) Molecular basis for proton regulation of glycine transport by glycine transporter subtype 1b. Mol Pharmacol 58:129-35
5. Bauman AL, Apparsundaram S, Ramamoorthy S, Wadzinski BE, Vaughan RA, Blakely RD (2000) Cocaine and antidepressant-sensitive biogenic amine transporters exist in regulated complexes with protein phosphatase 2A. J Neurosci 20:7571-7578
6. Bauman PA, Blakely RD (2002) Determinants within the C-terminus of the human norepinephrine transporter dictate transporter trafficking, stability, and activity. Arch Biochem Biophys 404:80-91
7. Beckman ML, Quick MW (1998) Neurotransmitter transporters: regulators of function and functional regulation. J Membr Biol 164:1-10
8. --coupled gamma-aminobutyric acid transporter from rat brain, impairs net flux but not exchange. J Biol Chem 275:34106-34113
9. Blakely RD, Bauman AL (2000) Biogenic amine transporters: regulation in flux. Curr Opin Neurobiol 10:328-336
10. Borden LA, Smith KE, Hartig PR, Branchek TA, Weinshank RL (1992) Molecular heterogeneity of the gamma-aminobutyric acid (GABA) transporter system. Cloning of two novel high affinity GABA transporters from rat brain. J Biol Chem 267:21098-21104
11. --dependent GABA cotransporter rGAT1. J Physiol (Lond) 541:343-350
12. Carneiro AM, Ingram SL, Beaulieu J-M, Sweeney A, Amara SG, Thomas SM, Caron MG, Torres GE (2002) The multiple LIM domain-containing adaptor protein Hic-5 synaptically colocalizes and interacts with the dopamine transporter. J Neurosci 22:7045-7054
13. Chang AS, Starnes DM, Chang SM (1998) Possible existence of quaternary structure in the high-affinity serotonin transport complex. Biochem Biophys Res Commun 249:416-412
14. Chen J-G, Rudnick G (2000) Permeation and gating residues in serotonin transporter. Proc Natl Acad Sci USA 97:1044-1049
15. Chen N, Vaughan RA, Reith MEA (2001) The role of conserved tryptophan and acidic residues in the human dopamine transporter as characterized by site-directed mutagenesis. J Neurochem 77:1116-1127
16. Chiu C-S, Jensen K, Sokolova I, Wang D, Li M, Deshpande P, Davidson N, Mody I, Quick MW, Quake SR, Lester HA (2002) Counting GABA transporters at presynaptic terminals of knock-in mice carrying GAT1-GFP fusions. J Neurosci 22:10251-10266
17. Deken SL, Beckman M, Boos L, Quick MW (2000) Permeation through GABA transporters is regulated by syntaxin 1A. Nat Neurosci 3:998-1003
18. Deken SL, Wang D, Quick MW (2003) Plasma membrane GABA transporters undergo rapid recycling and reside on distinct synaptic-like vesicles. J Neurosci 23:1563-1568
19. Evans J, Herdon H, Cairns W, O'Brien E, Chapman C, Terrett J, Gloger I (1999) Cloning, functional characterisation and population analysis of a variant form of the human glycine type 2 transporter. FEBS Lett 463:301-306
20. Falkenburger BH, Barstow KL, Mintz IM (2001) Dendrodendritic inhibition through reversal of dopamine transport. Science 293:2465-2470
21. --dependent neurotransmitter transporter gene family. Genomics 70:241-252
22. Foster JD, Pananusorn B, Vaughan RA (2002) Dopamine transporters are phosphorylated on N-terminal serines in rat striatum. J Biol Chem 277:25178-25186
23. Gainetdinov RR, Sotnikova TD, Caron MG (2002) Monoamine transporter pharmacology and mutant mice. Trends Pharmacol Sci 23:367-373
24. Geerlings A, Lopez-Corcuera B, Aragon C (2000) Characterization of the interactions between the glycine transporters GLYT1 and GLYT2 and the SNARE protein syntaxin 1A. FEBS Lett 470:51-54
25. Giros B, el Mestikawy S, Godinot N, Zheng K, Han H, Yang-Feng T, Caron MG (1992) Cloning, pharmacological characterization, and chromosome assignment of the human dopamine transporter. Mol Pharmacol 42:383-390
26. Grånäs C, Ferrer J, Loland CJ, Javitch JA, Gether U (2003) N-terminal truncation of the dopamine transporter abolishes phorbol ester-and substance P receptor-stimulated phosphorylation without impairing transporter internalization. J Biol Chem 278:4990-5000
27. 2-terminus of norepinephrine transporter contains a basolateral localization signal for epithelial cells. Mol Biol Cell 12:3797-807
28. Guastella J, Nelson N, Nelson H, Czyzyk L, Keynan S, Miedel MC, Davidson N, Lester HA, Kanner BI (1990) Cloning and expression of a rat brain GABA transporter. Science 249:1303-1306
29. Hanley JG, Jones EM, Moss SJ (2000) GABA receptor rho1 subunit interacts with a novel splice variant of the glycine transporter, GLYT-1. J Biol Chem 275:840-846
30. Hastrup H, Karlin A, Javitich JA (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
31. Iyer GS, Krahe R, Goodwin LA, Doggett NA, Siciliano MJ, Funanage VL, Proujansky R (1996) Identification of a testis-expressed creatine transporter gene at 16p11.2 and confirmation of the X-linked locus to Xq28. Genomics 34:143-146
32. Jayanthi LD, Wilson JJ, Montalvo J, DeFelice LJ (2000) Differential regulation of mammalian brain-specific proline transporter by calcium and calcium-dependent protein kinases. Br J Pharmacol 129:465-470
33. Jess U, Far OEI, Kirsch J, Betz H (2002) Interaction of the C-terminal region of the rat serotonin transporter with MacMAR-CKS modulates 5-HT uptake regulation by protein kinase C. Biochem Biophys Res Commun 294:272-279
34. Kamdar G, Penado KMY, Rudnick G, Stephan MM (2001) Functional role of critical strip residues in transmembrane span 7 of the serotonin transporter. J Biol Chem 276:4038-4045
35. Kang YS, Ohtsuki S, Takanaga H, Tomi M, Hosoya K, Terasaki T (2002) Regulation of taurine transport at the bloodbrain barrier by tumor necrosis factor-alpha, taurine, and hypertonicity. J Neurochem 83:1188-1195
36. +-dependent mechanism. J Biol Chem 278:12070-12077
37. Kilic F, Rudnick G (2000) Oligomerization of the serotonin transporter and its functional consequences. Proc Natl Acad Sci USA 97:3106-3111
38. Kitayama S, Shimada S, Xu H, Markham L, Donovan DM, Uhl GR (1992) Dopamine transporter site-directed mutations differentially alter substrate transport and cocaine binding. Proc Natl Acad Sci USA 89:7782-7785
39. Kwon HM (1996) Transcriptional regulation of the betaine/ gamma-aminobutyric acid transporter by hypertonicity. Biochem Soc Trans 24:853-856
40. Lee FJS, Liu F, Pristupa ZB, Niznik HB (2001) Direct binding and functional coupling of α-synuclein to the dopamine transporters accelerate dopamine-induced apoptosis. FASEB J 15:916-926
41. Lesch KP, Mossner R (1998) Genetically driven variation in serotonin uptake: is there a link to affective spectrum, neurodevelopmental, and neurodegenerative disorders? Biol Psychiatry 44:179-192
42. Lin Z, Wang W, Uhl GR (2000) Dopamine transporter tryptophan mutants highlight candidate dopamine-and cocaine-selective domains. Mol Pharmacol 58:1581-1592
43. Little KY, Elmer LW, Zhong H, Scheys JO, Zhang L (2002) Cocaine induction of dopamine transporter trafficking to the plasma membrane. Mol Pharmaocl 61:436-445
44. 2+ switch in the dopamine transporter: mutation of an intracellular tyrosine constitutively alters the conformational equilibrium of the transport cycle. Proc Natl Acad Sci USA 99:1683-1688
45. +-coupled cotransporters GAT1 and SGLT1. J Biol Chem 275:37414-37422
46. Maiya R, Buck KJ, Harris RA, Mayfield RD (2002) Ethanol-sensitive sites on the human dopamine transporter. J Biol Chem 277:30724-30729
47. Morrow JA, Collie IT, Dunbar DR, Walker GB, Shahid M, Hill DR (1998) Molecular cloning and functional expression of the human glycine transporter GlyT2 and chromosomal localisation of the gene in the human genome. FEBS Lett 439:334-340
48. Nash SR, Giros B, Kingsmore SF, Rochelle JM, Suter ST, Gregor P, Seldin MF, Caron MG (1994) Cloning, pharmacological characterization, and genomic localization of the human creatine transporter. Receptors Channels 2:165-174
49. - neurotransmitter transporters. J Neurochem 71:1785-1803
50. Nelson H, Mandiyan S, Nelson N (1990) Cloning of the human brain GABA transporter. FEBS Lett 269:181-184
51. Olivier B, Soudijn W, Wijngaarden I van (2000) Serotonin, dopamine and norepinephrine transporters in the central nervous system and their inhibitors. Prog Drug Res 54:59-119
52. Pacholczyk T, Blakely RD, Amara SG (1991) Expression cloning of a cocaine-and antidepressant-sensitive human noradrenaline transporter. Nature 350:350-354
53. Patrylo PR, Spencer DD, Williamson A (2001) GABA uptake and heterotransport are impaired in the dentate gyrus of epileptic rats and humans with temporal lobe sclerosis. J Neurophysiol 85:1533-1542
54. Poyotos I, Ruberti F, Martinez-Maza R, Gimenez C, Dotti CG, Zafra F (2000) Polarized distribution of glycine transporter isoforms in epithelial and neuronal cells. Mol Cell Neurosci 15:99-111
55. Ramamoorthy S, Bauman AL, Moore KR, Han H, Yang-Feng T, Chang AS, Ganapathy V, Blakely RD (1993) Antidepressant-and cocaine-sensitive human serotonin transporters: molecular cloning, expression, and chromosomal localization. Proc Natl Acad Sci USA 90:2542-2546
56. Ramamoorthy S, Leibach FH, Mahesh VB, Han H, Yang-Feng T, Blakely RD, Ganapathy V (1994) Functional characterization and chromosomal localization of a cloned taurine transporter from human placenta. Biochem J 300:893-900
57. Rasola A, Galietta LJ, Barone V, Romeo G, Bagnasco S (1995) Molecular cloning and functional characterization of a GABA/ betaine transporter from human kidney. FEBS Lett 373:229-233
58. Roubert C, Cox PJ, Bruss M, Hamon M, Bonisch H, Giros B (2001) Determination of residues in the norepinephrine transporter that are critical for tricyclic antidepressant affinity. J Biol Chem 276:8254-8260
59. Rudnick G, Clark J (1993) From synapse to vesicle: the reuptake and storage of biogenic amine neurotransmitters. Biochim Biophys Acta 1144:249-263
60. Saier MH Jr (1999) A functional-phylogenetic system for the classification of transport proteins. J Cell Biochem 32-33:84-94
61. Salomons GS, Dooren SJ van, Verhoeven NM, Cecil KM, Ball WS, Degrauw TJ, Jakobs C (2001) X-linked creatine-transporter gene (SLC6A8) defect: a new creatine-deficiency syndrome. Am J Hum Genet 68:1497-1500
62. Saransaari P, Oja SS (1999) Taurine release modified by nitric oxide-generating compounds in the developing and adult mouse hippocampus. Neuroscience 89:1103-1111
63. Saunders C, Ferrer JV, Shi L, Chen J, Merrill G, lamb M E, Leeb-Lundberg LMF, Carvelli L, Javitch JA, Galli A (2000) Amphetamine-induced loss of human dopamine transporter activity: an internalization-dependent and cocaine-sensitive mechanism. Proc Natl Acad Sci USA 97:6850-6855
64. Schmid JA, Scholze P, Kudlacek O, Freissmuth M, Singer E, Sitte HH (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
65. Schroeter S, Apparsundaram S, Wiley RG, Miner LH, Sesack SR, Blakely RD (2000) Immunolocalization of the cocaine-and antidepressant-sensitive 1-norepinephrine transporter. J Comp Neurol 420:211-232
66. Schwartz EA (1987) Depolarization without calcium can release γ-aminobutyric acid from a retinal neuron. Science 238:350-355
67. Shafqat S, Velaz-Faircloth M, Henzi VA, Whitney KD, Yang-Feng TL, Seldin MF, Fremeau RT (1995) Human brain-specific L-proline transporter: molecular cloning, functional expression, and chromosomal localization of the gene in the human and mouse genomes. Mol Pharmacol 48:219-229
68. Shannon JR, Flattem NL, Jordan J, Jacob G, Black BK, Biaggioni I, Blakely RD, Robertson D (2000) Orthostatic intolerance and tachycardia associated with norepinephrine-transporter deficiency. N Engl J Med 342:541-549
69. 0+. J Biol Chem 274:23740-23745
70. 0+ in lung: possible role in luminal protein removal. Am J Physiol 284:L39-L49
71. Soudijn W, Wijngaarden I van (2000) The GABA transporter and its inhibitors. Curr Med Chem 7:1063-1079
72. Sturman JA (1990) Taurine deficiency. Prog Clin Biol Res 351:385-395
73. 3H]tiagahine binding to GAT-1 in the cingulate cortex in schizophrenia. Neuropsychobiology 45:7-11
74. Sung U, Apparsundaram S, Galli A, Kahlig KM, Savchenko V, Schroeter S, Quick MW, Blakely RD (2003) A regulated interaction of syntaxin 1A with the antidepressant-sensitive norepinephrine transporter establishes catecholamine clearance capacity. J Neurosci 23:1697-709
75. Supplisson S, Roux MJ (2002) Why glycine transporters have different stoichiometries. FEBS Lett 529:93-101
76. --dependent high affinity taurine transporter. Biochim Biophys Acta 1464:219-230
77. Torres GE, Yao W-D, Mohn AR, Quan H, Kim K-M, Levey AI, Staudinger J, Caron MG (2001) Functional interaction between monoamine plasma membrane transporters and synaptic PDZ domain-containing protein PICK1. Neuron 30:121-134
78. Torres GE, Carneiro A, Seamans K, Fiorentini C, Sweeney A, Yao W-D, Caron MG (2003) Oligomerization and trafficking of the human dopamine transporter. J Biol Chem 278:2731-2739
79. Uhl GR, Hall FS, Sora I (2002) Cocaine, reward, movement and monoamine transporters. Mol Psychiatry 7:21-26
80. Van Winkle LJ (2001) Amino acid transport regulation and early embryo development. Biol Reprod 1:1-12
81. Whitworth TL, Quick MW (2001) Substrate-induced regulation of γ-aminobutyric acid (GABA) transporter trafficking requires tyrosine phosphorylation. J Biol Chem 276:42932-42937
82. Xu F, Gainetdinov RR, Wetsel WC, Jones SR, Bohn LM, Miller GW, Wang YM, Caron MG (2000) Mice lacking the norepinephrine transporter are supersensitive to psychostimulants. Nat Neurosci 3:465-471
83. --dependent neurotransmitter transporters: drugs, substrates, presynaptic receptors, and signaling systems. Pharmacol Ther 92:21-55