Na+, Cl-, and pH dependence of the human choline transporter (hCHT) in Xenopus oocytes: The proton inactivation hypothesis of hCHT in synaptic vesicles

Journal of Neuroscience

Volumn 26, Issue 39, 2006, Pages 9851-9859

  Iwamoto, Hideki ^a   Blakely, Randy D ^a   De Felice, Louis J ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Choline transporter; Choline induced current; Cl ; Na+; pH; Xenopus oocyte

Indexed keywords

ACETYLCHOLINE; CARRIER PROTEIN; CHLORIDE ION; HEMICHOLINIUM 3; PROTEIN HUMAN CHOLINE TRANSPORTER; SODIUM ION; UNCLASSIFIED DRUG;

AMINE TRANSPORT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MEMBRANE; CHOLINE UPTAKE; CONTROLLED STUDY; ELECTRODE; FEMALE; NONHUMAN; OOCYTE; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SYNAPSE VESICLE; VOLTAGE CLAMP; XENOPUS LAEVIS;

ACETYLCHOLINE; ANIMALS; BIOLOGICAL TRANSPORT; CHLORIDES; CHOLINE; FEMALE; HEMICHOLINIUM 3; HUMANS; MEMBRANE POTENTIALS; MEMBRANE TRANSPORT PROTEINS; MODELS, NEUROLOGICAL; OOCYTES; PATCH-CLAMP TECHNIQUES; PROTONS; RECOMBINANT FUSION PROTEINS; SODIUM; SYMPORTERS; SYNAPTIC VESICLES; XENOPUS LAEVIS;

EID: 33749177731     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1862-06.2006     Document Type: Article

References (63)

1. Adams SV, DeFelice LJ (2003) Ionic currents in the human serotonin transporter reveal inconsistencies in the alternating access hypothesis. Biophys J 85:1548-1559.
2. Apparsundaram S, Ferguson SM, George Jr AL, Blakely RD (2000) Molecular cloning of a human, hemicholinium-3-sensitive choline transporter. Biochem Biophys Res Commun 276:862-867.
3. Apparsundaram S, Ferguson SM, Blakely RD (2001) Molecular cloning and characterization of a murine hemicholinium-3-sensitive choline transporter. Biochem Soc Trans 29:711-716.
4. Aubrey KR, Mitrovic AD, Vandenberg RJ (2000) Molecular basis for proton regulation of glycine transport by glycine transporter subtype 1b. Mol Pharmacol 58:129-135.
5. Bales KR, Tzavara ET, Wu S, Wade MR, Bymaster FP, Paul SM, Nomikos GG (2006) Cholinergic dysfunction in a mouse model of Alzheimer disease is reversed by an anti-Aβ antibody. J Clin Invest 116:825-832.
6. 5 muscarinic receptor knockout mice as novel tools to delineate the physiological roles of the muscarinic cholinergic system. Neurochem Res 28:437-442.
7. + permeation and pH regulation at a mammalian serotonin transporter. J Neurosci 17:2257-2266.
8. Cao Y, Li M, Mager S, Lester HA (1998) Amino acid residues that control pH modulation of transport-associated current in mammalian serotonin transporters. J Neurosci 18:7739-7749.
9. Carvelli L, McDonald PW, Blakely RD, DeFelice LJ (2004) Dopamine transporters depolarize neurons by a channel mechanism. Proc Natl Acad Sci USA 101:16046-16051.
10. Collier B, Kwok YN, Welner SA (1983) Increased acetylcholine synthesis and release following presynaptic activity in a sympathetic ganglion. J Neurochem 40:91-98.
11. Dani JA, DeBiasi M (2001) Cellular mechanisms of nicotine addiction. Pharmacol Biochem Behav 70:439-446.
12. +-to-sugar stoichiometry of SGLT3. Am J Physiol Renal Physiol 49:F278-F282.
13. Diez-Sampedro A, Hirayama BA, Osswald C, Gorboulev V, Baumgarten K, Volk C, Wright EM, Koepsell H (2003) A glucose sensor hiding in a family of transporters. Proc Natl Acad Sci USA 20:11753-11758.
14. Eiden LE (1998) The cholinergic gene locus. J Neurochem 70:2227-2240.
15. - symporter: mechanism, stoichiometry, and specificity. J Biol Chem 272:27230-27238.
16. Ferguson SM, Blakely RD (2004) The choline transporter resurfaces: new roles for synaptic vesicles? Mol Intervent 4:22-37.
17. Ferguson SM, Savchenko V, Apparsundaram S, Zwick M, Wright J, Heilman CJ, Yi H, Levey AI, Blakely RD (2003) Vesicular localization and activity-dependent trafficking of presynaptic choline transporters. J Neurosci 23:9697-9709.
18. Ferguson SM, Bazalakova M, Savchenko V, Tapia JC, Wright J, Blakely RD (2004) Lethal impairment of cholinergic neurotransmission in hemicholinium-3-sensitive choline transporter knockout mice. Proc Natl Acad Sci USA 101:8762-8767.
19. Galli A, DeFelice LJ, Duke BJ, Moore KR, Blakely RD (1995) Sodium-dependent norepinephrine-induced currents in norephinephrine-transporter- transfected HEK-293 cells blocked by cocaine and antidepressants. J Exp Biol 198:2197-2212.
20. Galli A, Petersen CI, deBlaquiere M, Blakely RD, DeFelice LJ (1997) Drosophila serotonin transporters have voltage-dependent uptake coupled to a serotonin-gated ion channel. J Neurosci 17:3401-3411.
21. Galli A, Blakely RD, DeFelice LJ (1998) Patch-clamp and amperometric recordings from norepinephrine transporters: channel activity and voltage-dependent uptake. Proc Natl Acad Sci USA 95:13260-13265.
22. Geerlings A, Nunez E, Lopez-Corcuera B, Aragon C (2001) Calcium- and syntaxin 1-mediated trafficking of the neuronal glycine transporter GLYT2. J Biol Chem 276:17584-17590.
23. 3H]choline high-affinity uptake in rat striatal synaptosomes. Mol Pharmacol 9:630-639.
24. Haga T, Noda H (1973) Choline uptake systems of rat brain synaptosomes. Biochim Biophys Acta 291:564-575.
25. +/glucose cotransporter (SGLT1). J Biol Chem 269:21407-21410.
26. Ingram SL, Prasad BM, Amara SG (2002) Dopamine transporter-mediated conductances increase excitability of midbrain dopamine neurons. Nat Neurosci 5:971-978.
27. Kahlig KM, Binda F, Khoshbouei H, Blakely RD, McMahon DG, Javitch JA, Galli A (2005) Amphetamine induces dopamine efflux through a dopamine transporter channel. Proc Natl Acad Sci USA 102:3495-3500.
28. Karakossian MH, Spencer SR, Gomez AQ, Padilla OR, Sacher A, Loo DDF, Nerson N, Eskandari S (2005) Novel properties of a mouse γ-aminobutyric acid transporter (GAT4). J Membr Biol 203:65-82.
29. Keller JE, Parsons SM (2000) A critical histidine in the vesicular acetylcholine transporter. Neurochem Int 36:113-117.
30. Kuhar MJ, Murrin LC (1978) Sodium-dependent, high affinity choline uptake. J Neurochem 30:15-21.
31. Kusano K, Miledi R, Sinnakre J (1982) Cholinergic and catecholaminergic receptors in the Xenopus oocyte membrane. J Physiol (Lond) 328:143-170.
32. +-coupled cotransporters GAT1 and SGLT1. J Biol Chem 275:37414-37422.
33. 3H] hemicholinium-3 binding sites in the rat brain. Brain Res 381:191-194.
34. +/glucose cotransporter (SGLT1) currents and fluxes. J Membr Biol 162:101-106.
35. Mager S, Min C, Henry DJ, Chavkin C, Hoffman BJ, Davidson N, Lester HA (1994) Conducting states of a mammalian serotonin transporter. Neuron 12:845-859.
36. Mager S, Kleinberger-Doron N, Keshet GI, Davidson N, Kanner BI, Lester HA (1996) Ion binding and permeation at the GABA transporter GAT1. J Neurosci 16:5405-5414.
37. Marchbanks RM, Wonnacott S (1979) Relationship of choline uptake to acetylcholine synthesis and release. Prog Brain Res 49:77-88.
38. Ming L, Farley RA, Lester HA (2002) Voltage-dependent transient currents of human and rat 5-HT transporters (SERT) are blocked by HEPES and ion channel ligands. FEBS Lett 513:247-252.
39. Nakata K, Okuda T, Misawa H (2004) Ultrastructural localization of high-affinity choline transporter in the rat neuromuscular junction: enrichment on synaptic vesicles. Synapse 53:53-56.
40. Nelson N, Sacher A, Nelson H (2002) The significance of molecular slips in transport systems. Nat Rev Mol Cell Biol 3:876-881.
41. Nguyen ML, Cox GD, Parsons SM (1998) Kinetic parameters for the vesicular acetylcholine transporter: two protons are exchanged for one acetylcholine. Biochemistry 37:13400-13410.
42. Okuda T, Haga T (2000) Functional characterization of the human high-affinity choline transporter. FEBS Lett 484:92-97.
43. Okuda T, Haga T (2003) High-affinity choline transporter. Neurochem Res 28:483-488.
44. Okuda T, Haga T, Kanai Y, Endou H, Ishihara T, Katsura I (2000) Identification and characterization of the high-affinity choline transporter. Nat Neurosci 3:120-125.
45. Parsons SM, Prior C, Marshall IG (1993) Acetylcholine transport, storage, and release. Int Rev Neurobiol 35:279-390.
46. Perrin DD (1972) Dissociation constants of organic bases in aqueous solution. London: Butterworths.
47. Petersen CI, DeFelice LJ (1999) Ionic interactions in the Drosophila serotonin transporter identify it as a serotonin channel. Nat Neurosci 2:605-610.
48. Prasad PD, Ganapathy V (2000) Structure and function of mammalian sodium-dependent multivitamin transporter. Curr Opin Clin Nutr Metab Care 3:263-266.
49. Quick MW (2003) Regulating the conducting states of a mammalian serotonin transporter. Neuron 40:537-549.
50. Ramsey IS, DeFelice LJ (2002) Serotonin transporter function and pharmacology are sensitive to expression level: evidence for an endogenous regulatory factor. J Biol Chem 277:14475-14482.
51. Renick SE, Kleven DT, Chan J, Stenius K, Milner TA, Pickel VM, Fremeau Jr RT (1999) The mammalian brain high-affinity L-proline transporter is enriched preferentially in synaptic vesicles in a subpopulation of excitatory nerve terminals in rat forebrain. J Neurosci 19:21-33.
52. Ribeiro FM, Black SAG, Cregan SP, Prado VF, Prado MAM, Rylett RJ, Ferguson SSG (2005) Constitutive high-affinity choline transporter endocytosis is determined by a carboxyl-terminal tail dileucine motif. J Neurochem 94:86-96.
53. Ribeiro FM, Black SAG, Prado VF, Rylett RJ, Ferguson SSG, Prado MAM (2006) The "ins" and "outs" of the high-affinity choline transporter CHT1. J Neurochem 97:1-12.
54. 3H] hemicholinium-3 binding associated with neuronal choline uptake sites in rat brain membranes. Brain Res 348:321-330.
55. Sarter M, Parikh V (2005) Choline transporters, cholinergic transmission and cognition. Nat Neurosci 6:48-56.
56. Simon JR, Kuhar MJ (1975) Impulse-flow regulation of high affinity choline uptake in brain cholinergic nerve terminals. Nature 255:162-163.
57. Simon JR, Kuhar MJ (1976) High affinity choline uptake: ionic and energy requirements. J Neurochem 27:93-99.
58. Sonders MS, Zhu S, Zahniser NR, Kavanaugh MP, Amara SG (1997) Multiple ionic conductances of the human dopamine transporter: the actions of dopamine and psychostimulants. J Neurosci 17:960-974.
59. Tan PK, Waites C, Liu Y, Krantz DE, Edwards RH (1998) A leucine-based motif mediates the endocytosis of vesicular monoamine and acetylcholine transporters. J Biol Chem 273:17351-17360.
60. Wadiche JI, Amara SG, Kavanaugh MP (1995) Ion fluxes associated with excitatory amino acid transport. Neuron 15:721-728.
61. Wright EM, Turk E (2004) The sodium/glucose cotransport family SLC5. Pflügers Arch 447:510-518.
62. +-glucose cotransporters: SLC5. Physiology (Bethesda) 19:370-376.
63. Yamamura HI, Snyder SH (1972) Choline: high-affinity uptake by rat brain synaptosomes. Science 178:626-628.