The high-affinity choline transporter: A critical protein for sustaining cholinergic signaling as revealed in studies of genetically altered mice

Handbook of Experimental Pharmacology

Volumn 175, Issue , 2006, Pages 525-544

  Bazalakova, M H ^a   Blakely, R D ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Choline; Hemicholinium 3; Heterozygote; Knockout; Transgenic; Transporter

Indexed keywords

ACETYLCHOLINESTERASE; CARRIER PROTEIN; CHOLINE; CHOLINE ACETYLTRANSFERASE; CHOLINE TRANSPORTER; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR SUBUNIT ALPHA3;

ANIMAL; GENETICS; METABOLISM; MOUSE; MOUSE MUTANT; NERVE CELL PLASTICITY; PHYSIOLOGY; REVIEW; SYNAPTIC TRANSMISSION; SYNAPTOSOME;

ACETYLCHOLINESTERASE; ANIMALS; CHOLINE; CHOLINE O-ACETYLTRANSFERASE; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, KNOCKOUT; NEURONAL PLASTICITY; PRESYNAPTIC TERMINALS; RECEPTORS, NICOTINIC; SYNAPTIC TRANSMISSION;

EID: 34347387212     PISSN: 01712004     EISSN: 18650325     Source Type: Book Series    
DOI: 10.1007/3-540-29784-7_21     Document Type: Article

References (78)

1. Apparsundaram S, Ferguson SM, George AL Jr, Blakely RD (2000) Molecular cloning of a human, hemicholinium-3-sensitive choline transporter. Biochem Biophys Res Commun 276:862-867
2. Apparsundaram S, Ferguson SM, Blakely RD (2001a) Molecular cloning and characterization of a murine hemicholinium-3-sensitive choline transporter. Biochem Soc Trans 29:711-716
3. Apparsundaram S, Sung U, Price RD, Blakely RD (2001b) Trafficking-dependent and -independent pathways of neurotransmitter transporter regulation differentially involving p38 mitogen-activated protein kinase revealed in studies of insulin modulation of norepinephrine transport in SK-N-SH cells. J Pharmacol Exp Ther 299:666-677
4. Apparsundaram S, Martinez V, Parikh V, Kozak R, Sarter M (2005) Increased capacity and density of choline transporters situated in synaptic membranes of the right medial prefrontal cortex of attentional task-performing rats. J Neurosci 25:3851-3856
5. Arnold HM, Burk JA, Hodgson EM, Sarter M, Bruno JP (2002) Differential cortical acetylcholine release in rats performing a sustained attention task versus behavioral control tasks that do not explicitly tax attention. Neuroscience 114:451-460
6. Bazalakova MH, Ferguson SM,Wright J,McDonald MP, Blakely RD (2004)Modeling presynaptic cholinergic hypofunction: pharmacological and behavioral studies in choline transporter heterozygous mice. Soc Neurosci Abstr 142.1
7. Beeri R, Andres C, Lev-Lehman E, Timberg R, Huberman T, Shani M, Soreq H (1995) Transgenic expression of human acetylcholinesterase induces progressive cognitive deterioration in mice. Curr Biol 5:1063-1071
8. Beeri R, Le Novere N, Mervis R, Huberman T, Grauer E, Changeux JP, Soreq H (1997) Enhanced hemicholinium binding and attenuated dendrite branching in cognitively impaired acetylcholinesterase-transgenic mice. J Neurochem 69:2441-2451
9. Birks R, McIntosh FC (1961) Acetylcholine metabolism of a sympathetic ganglion. Can J Biochem Physiol 39:787-825
10. Blusztajn JK (1998) Choline, a vital amine. Science 281:794-795
11. Brandon EP, Lin W, DAmour KA, Pizzo DP, Dominguez B, Sugiura Y, Thode S, Ko CP, Thal LJ, Gage FH, Lee KF (2003) Aberrant patterning of neuromuscular synapses in choline acetyltransferase-deficient mice. J Neurosci 23:539-549
12. Brandon EP, Mellott T, Pizzo DP, Coufal N, DAmour KA, Gobeske K, Lortie M, Lopez- Coviella I, Berse B, Thal LJ, Gage FH, Blusztajn JK (2004) Choline transporter 1maintains cholinergic function in choline acetyltransferase haploinsufficiency. JNeurosci 24:5459-5466
13. Burgel P, Rommelspacher H (1978) Changes in high affinity choline uptake in behavioral experiments. Life Sci 23:2423-2427
14. Bussiere M, Vance JE, Campenot RB, Vance DE (2001) Compartmentalization of choline and acetylcholine metabolism in cultured sympathetic neurons. J Biochem (Tokyo) 130:561-568
15. Chatterjee TK, Bhatnagar RK (1990) Ca2(+)-dependent, ATP-induced conversion of the [3H]hemicholinium-3 binding sites from high- to low-affinity states in rat striatum: effect of protein kinase inhibitors on this affinity conversion and synaptosomal choline transport. J Neurochem 54:1500-1508
16. Dani JA (2001)Overview of nicotinic receptors and their roles in the central nervous system. Biol Psychiatry 49:166-174
17. Duysen EG, Stribley JA, Fry DL, Hinrichs SH, Lockridge O (2002) Rescue of the acetylcholinesterase knockout mouse by feeding a liquid diet; phenotype of the adult acetylcholinesterase deficient mouse. Brain Res Dev Brain Res 137:43-54
18. Erb C, Troost J, Kopf S, Schmitt U, Loffelholz K, Soreq H, Klein J (2001) Compensatory mechanisms enhance hippocampal acetylcholine release in transgenic mice expressing human acetylcholinesterase. J Neurochem 77:638-646
19. Ferguson SM, Blakely RD (2004) The choline transporter resurfaces: new roles for synaptic vesicles? Mol Interv 4:22-37
20. 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
21. Ferguson SM, BazalakovaM, 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 U S A 101:8762-8767
22. Fink-Jensen A, Fedorova I,Wortwein G,Woldbye DP, Rasmussen T, ThomsenM, Bolwig TG, Knitowski KM,McKinzie DL, Yamada M,Wess J, Basile A (2003) Role forM5muscarinic acetylcholine receptors in cocaine addiction. J Neurosci Res 74:91-96
23. Fujii T, Okuda T, Haga T, Kawashima K (2003) Detection of the high-affinity choline transporter in the MOLT-3 human leukemic T-cell line. Life Sci 72:2131-2134
24. Gates J Jr, Ferguson SM, Blakely RD, Apparsundaram S (2004) Regulation of choline transporter surface expression and phosphorylation by protein kinase C and protein phosphatase 1/2A. J Pharmacol Exp Ther 310:536-545
25. Gerber DJ, Sotnikova TD, Gainetdinov RR, Huang SY, Caron MG, Tonegawa S (2001) Hyperactivity, elevated dopaminergic transmission, and response to amphetamine in M1 muscarinic acetylcholine receptor-deficient mice. Proc Natl Acad Sci U S A 98:15312-15317
26. Goldman ME, EricksonCK(1983) Effects of acute and chronic administration of antidepressant drugs on the central cholinergic nervous system. Comparison with anticholinergic drugs. Neuropharmacology 22:1215-1222
27. Guyenet P, Lefresne P, Rossier J, Beaujouan JC, Glowinski J (1973) Inhibition by hemicholinium- 3 of (14C)acetylcholine synthesis and (3H)choline high-affinity uptake in rat striatal synaptosomes. Mol Pharmacol 9:630-639
28. Haga T, NodaH(1973) Choline uptake systems of rat brain synaptosomes. Biochim Biophys Acta 291:564-575
29. Holden JT, Rossier J, Beaujouan JC, Guyenet P, Glowinski J (1975) Inhibition of highaffinity choline transport in rat striatal synaptosomes by alkyl bisquaternaryammonium compounds. Mol Pharmacol 11:19-27
30. Jope RS (1979) High affinity choline transport and acetylCoA production in brain and their roles in the regulation of acetylcholine synthesis. Brain Res 180:313-344
31. Kawashima K, FujiiT(2003) The lymphocytic cholinergic systemand its biological function. Life Sci 72:2101-2109
32. Kitabatake Y, Hikida T, Watanabe D, Pastan I, Nakanishi S (2003) Impairment of rewardrelated learning by cholinergic cell ablation in the striatum. Proc Natl Acad Sci U S A 100:7965-7970
33. Kuhar MJ,Murrin LC (1978) Sodium-dependent, high affinity choline uptake. J Neurochem 30:15-21
34. Kuhar MJ, Sethy VH, Roth RH, Aghajanian GK (1973) Choline: selective accumulation by central cholinergic neurons. J Neurochem 20:581-593
35. Kus L, Borys E, PingChu Y, Ferguson SM, Blakely RD, EmborgME, Kordower JH, Levey AI, Mufson EJ (2003) Distribution of high affinity choline transporter immunoreactivity in the primate central nervous system. J Comp Neurol 463:341-357
36. Li B, Stribley JA, Ticu A, Xie W, Schopfer LM, Hammond P, Brimijoin S, Hinrichs SH, Lockridge O (2000) Abundant tissue butyrylcholinesterase and its possible function in the acetylcholinesterase knockout mouse. J Neurochem 75:1320-1331
37. Li B, Duysen EG, Volpicelli-Daley LA, Levey AI, Lockridge O (2003) Regulation of muscarinic acetylcholine receptor function in acetylcholinesterase knockout mice. Pharmacol Biochem Behav 74:977-986
38. Lips KS, PfeilU,HaberbergerRV,KummerW(2002) Localisation of the high-affinity choline transporter-1 in the rat skeletal motor unit. Cell Tissue Res 307:275-280
39. Lowenstein PR, Coyle JT (1986) Rapid regulation of [3H]hemicholinium-3 binding sites in the rat brain. Brain Res 381:191-194
40. Macintosh FC, Birks RI, Sastry PB (1956) Pharmacological inhibition of acetylcholine synthesis. Nature 4543:1181
41. Maire JC,Wurtman RJ (1985) Effects of electrical stimulation and choline availability on the release and contents of acetylcholine and choline in superfused slices fromrat striatum. J Physiol (Paris) 80:189-195
42. McGaughy J, Kaiser T, Sarter M (1996) Behavioral vigilance following infusions of 192 IgGsaporin into the basal forebrain: selectivity of the behavioral impairment and relation to cortical AChE-positive fiber density. Behav Neurosci 110:247-265
43. Mesulam MM, Guillozet A, Shaw P, Levey A, Duysen EG, Lockridge O (2002) Acetylcholinesterase knockouts establish central cholinergic pathways and can use butyrylcholinesterase to hydrolyze acetylcholine. Neuroscience 110:627-639
44. Misawa H, Nakata K, Matsuura J, Nagao M, Okuda T, Haga T (2001) Distribution of the high-affinity choline transporter in the central nervous system of the rat. Neuroscience 105:87-98
45. Misgeld T, Burgess RW, Lewis RM, Cunningham JM, Lichtman JW, Sanes JR (2002) Roles of neurotransmitter in synapse formation: development of neuromuscular junctions lacking choline acetyltransferase. Neuron 36:635-648
46. Murrin LC, Kuhar MJ (1976) Activation of high-affinity choline uptake in vitro by depolarizing agents. Mol Pharmacol 12:1082-1090
47. Murrin LC, DeHaven RN, Kuhar MJ (1977) On the relationship between (3H)choline uptake activation and (3H)acetylcholine release. J Neurochem 29:681-687
48. 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
49. ORegan S, Traiffort E, Ruat M, Cha N, Compaore D, Meunier FM (2000) An electric lobe suppressor for a yeast choline transportmutation belongs to a new family of transporterlike proteins. Proc Natl Acad Sci U S A 97:1835-1840
50. Okuda T, Haga T (2000) Functional characterization of the human high-affinity choline transporter. FEBS Lett 484:92-97
51. 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
52. Perry E, Walker M, Grace J, Perry R (1999) Acetylcholine in mind: a neurotransmitter correlate of consciousness? Trends Neurosci 22:273-280
53. Pfeil U, Haberberger RV, Lips KS, Eberling L, Grau V, KummerW(2003a) Expression of the high-affinity choline transporter CHT1 in epithelia. Life Sci 72:2087-2090
54. Pfeil U, Lips KS, Eberling L, Grau V, Haberberger RV, KummerW(2003b) Expression of the high-affinity choline transporter, CHT1, in the rat trachea. Am J Respir Cell Mol Biol 28:473-477
55. Proskocil BJ, Sekhon HS, Jia Y, Savchenko V, Blakely RD, Lindstrom J, Spindel ER (2004) Acetylcholine is an autocrine or paracrine hormone synthesized and secreted by airway bronchial epithelial cells. Endocrinology 145:2498-2506
56. Rassadi S,KrishnaswamyA, Pie B,McConnellR, Jacob MH,Cooper E (2005)Anullmutation for the alpha3 nicotinic acetylcholine (ACh) receptor gene abolishes fast synaptic activity in sympathetic ganglia and reveals that ACh output from developing preganglionic terminals is regulated in an activity-dependent retrograde manner. J Neurosci 25:8555-8566
57. RibeiroFM,Alves-Silva J,VolknandtW,Martins-Silva C,MahmudH,Wilhelm A,GomezMV, Rylett RJ, Ferguson SS, Prado VF, Prado MA (2003) The hemicholinium-3 sensitive high affinity choline transporter is internalized by clathrin-mediated endocytosis and is present in endosomes and synaptic vesicles. J Neurochem 87:136-146
58. Ribeiro FM, Black SA, Cregan SP, Prado VF, Prado MA, Rylett RJ, Ferguson SS (2005) Constitutive high-affinity choline transporter endocytosis is determined by a carboxylterminal tail dileucine motif. J Neurochem 94:86-96
59. SaltarelliMD, Yamada K, Coyle JT (1990) Phospholipase A2 and 3H-hemicholinium-3 binding sites in rat brain: a potential second-messenger role for fatty acids in the regulation of high-affinity choline uptake. J Neurosci 10:62-72
60. Sandberg K, Coyle JT (1985) Characterization of [3H]hemicholinium-3 binding associated with neuronal choline uptake sites in rat brain membranes. Brain Res 348:321-330
61. Sarter M, Bruno JP (1997) Cognitive functions of cortical acetylcholine: toward a unifying hypothesis. Brain Res Brain Res Rev 23:28-46
62. Schueler FW (1955) A new group of respiratory paralyzants. I. The hemicholiniums. J Pharmacol Exp Ther 115:127-143
63. Simon JR, KuharMG(1975) Impulse-flow regulation of high affinity choline uptake in brain cholinergic nerve terminals. Nature 255:162-163
64. Simon JR, Kuhar MJ (1976) High affinity choline uptake: ionic and energy requirements. J Neurochem 27:93-99
65. Svedberg MM, Svensson AL, Bednar I, Nordberg A (2003) Neuronal nicotinic and muscarinic receptor subtypes at different ages of transgenic mice overexpressing human acetylcholinesterase. Neurosci Lett 340:148-152
66. Thomsen M, Woldbye DP, Wortwein G, Fink-Jensen A, Wess J, Caine SB (2005) Reduced cocaine self-administration in muscarinic M5 acetylcholine receptor-deficient mice. J Neurosci 25:8141-8149
67. Tucek S (1985) Regulation of acetylcholine synthesis in the brain. J Neurochem 44:11-24
68. Vickroy TW, Roeske WR, Yamamura HI (1984) Sodium-dependent high-affinity binding of [3H]hemicholinium-3 in the rat brain: a potentially selective marker for presynaptic cholinergic sites. Life Sci 35:2335-2343
69. Vickroy TW, Roeske WR, Gehlert DR,Wamsley JK, Yamamura HI (1985) Quantitative light microscopic autoradiography of [3H]hemicholinium-3 binding sites in the rat central nervous system: a novel biochemical marker for mapping the distribution of cholinergic nerve terminals. Brain Res 329:368-373
70. Volpicelli-Daley LA, Duysen EG, Lockridge O, Levey AI (2003a) Altered hippocampal muscarinic receptors in acetylcholinesterase-deficient mice. Ann Neurol 53:788-796
71. Volpicelli-Daley LA, Hrabovska A, Duysen EG, Ferguson SM, Blakely RD, Lockridge O, LeveyAI (2003b) Altered striatal function andmuscarinic cholinergic receptors in acetylcholinesterase knockout mice. Mol Pharmacol 64:1309-1316
72. Wenk G, Hepler D, Olton D (1984) Behavior alters the uptake of [3H]choline into acetylcholinergic neurons of the nucleus basalis magnocellularis and medial septal area. Behav Brain Res 13:129-138
73. Wess J (2004) Muscarinic acetylcholine receptor knockout mice: novel phenotypes and clinical implications. Annu Rev Pharmacol Toxicol 44:423-450
74. Winkler J, Suhr ST, Gage FH, Thal LJ, Fisher LJ (1995) Essential role of neocortical acetylcholine in spatial memory. Nature 375:484-487
75. XieW, Stribley JA, Chatonnet A,Wilder PJ, Rizzino A, McComb RD, Taylor P, Hinrichs SH, Lockridge O (2000) Postnatal developmental delay and supersensitivity to organophosphate in gene-targeted mice lacking acetylcholinesterase. J Pharmacol Exp Ther 293:896-902
76. Yamamura HI, Snyder SH (1972) Choline: high-affinity uptake by rat brain synaptosomes. Science 178:626-628
77. Yamamura HI, Snyder SH (1973) High affinity transport of choline into synaptosomes of rat brain. J Neurochem 21:1355-1374
78. ZhuCB,HewlettWA, Feoktistov I,Biaggioni I,BlakelyRD(2004)Adenosine receptor,protein kinase G, and p38 mitogen-activated protein kinase-dependent up-regulation of serotonin transporters involves both transporter trafficking and activation. Mol Pharmacol 65:1462-1474