Transgenic overexpression of the presynaptic choline transporter elevates acetylcholine levels and augments motor endurance

Neurochemistry International

Volumn 73, Issue 1, 2014, Pages 217-228

  Holmstrand, Ericka C ^a   Lund, David ^a   Cherian, Ajeesh Koshy ^b,c   Wright, Jane ^a   Martin, Rolicia F ^a   Ennis, Elizabeth A ^a   Stanwood, Gregg D ^a   Sarter, Martin ^b,c   Blakely, Randy D ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Acetylcholine; Choline; Hemicholinium 3; Slc5a7; Transport

Indexed keywords

ACETYLCHOLINE; ACETYLCHOLINESTERASE; CHOLINE; CHOLINE ACETYLTRANSFERASE; HEMICHOLINIUM 3; CARRIER PROTEIN; CHOLINE TRANSPORTER; CHOLINERGIC RECEPTOR STIMULATING AGENT; PRESYNAPTIC RECEPTOR;

ACETYLCHOLINE BRAIN LEVEL; AGRICULTURE; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; CHOLINERGIC NERVE CELL; CHROMOSOME 17; CONTROLLED STUDY; CORPUS STRIATUM; ENDURANCE; FATIGUE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MOTOR PERFORMANCE; MOUSE; NERVE FIBER; NONHUMAN; OPEN FIELD TEST; PARASYMPATHETIC INNERVATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; TREADMILL TEST; WILD TYPE; ANIMAL; ANIMAL BEHAVIOR; BIOSYNTHESIS; C57BL MOUSE; DIAGNOSTIC USE; GENE DOSAGE; GENETICS; METABOLISM; PHYSIOLOGY; SYNAPTOSOME;

ANIMALIA; BACTERIA (MICROORGANISMS); MUS;

ACETYLCHOLINE; ANIMALS; BEHAVIOR, ANIMAL; CHOLINE; CHOLINERGIC AGENTS; CHROMOSOMES, ARTIFICIAL, BACTERIAL; GENE DOSAGE; HEMICHOLINIUM 3; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PHYSICAL ENDURANCE; RECEPTORS, PRESYNAPTIC; SYNAPTOSOMES;

EID: 84902465642     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2013.11.008     Document Type: Article

References (44)

1. T. Antonelli, L. Beani, C. Bianchi, F. Pedata, and G. Pepeu Changes in synaptosomal high affinity choline uptake following electrical stimulation of guinea-pig cortical slices: effect of atropine and physostigmine Br. J. Pharmacol. 74 1981 525 531
2. S. Apparsundaram, S.M. Ferguson, A.L. George Jr., and R.D. Blakely Molecular cloning of a human, hemicholinium-3-sensitive choline transporter Biochem. Biophys. Res. Commun. 276 2000 862 867
3. S. Apparsundaram, V. Martinez, V. Parikh, R. Kozak, and M. Sarter 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 2005 3851 3856
4. M.H. Bazalakova, J. Wright, E.J. Schneble, M.P. McDonald, C.J. Heilman, A.I. Levey, and R.D. Blakely Deficits in acetylcholine homeostasis, receptors and behaviors in choline transporter heterozygous mice Genes Brain Behav. 6 2007 411 424
5. J.R. Cooper, F.E. Bloom, and R.H. Roth Acetylcholine J.R. Cooper, F.E. Bloom, R.H. Roth, The Biochemical Basis of Neuropharmacology eighth ed. 2003 Oxford University Press New York 151 178
6. Y. Dong, J.A. Dani, and R.D. Blakely Choline transporter hemizygosity results in diminished basal extracellular dopamine levels in nucleus accumbens and blunts dopamine elevations following cocaine or nicotine Biochem. Pharmacol. 86 2013 1084 1088
7. B.A. English, M. Appalsamy, A. Diedrich, A.M. Ruggiero, D. Lund, J. Wright, N.R. Keller, K.M. Louderback, D. Robertson, and R.D. Blakely Tachycardia, reduced vagal capacity, and age-dependent ventricular dysfunction arising from diminished expression of the presynaptic choline transporter Am. J. Physiol. Heart Circ. Physiol. 299 2010 H799 H810
8. S. Ferguson, M. Bazalakova, V. Savchenko, J. Tapia, J. Wright, and R. Blakely Lethal impairment of cholinergic neurotransmission in hemicholinium-3-sensitive choline transporter knockout mice Proc. Natl. Acad. Sci. USA 101 2004 8762 8767
9. S.M. Ferguson, V. Savchenko, S. Apparsundaram, M. Zwick, J. Wright, C.J. Heilman, H. Yi, A.I. Levey, and R.D. Blakely Vesicular localization and activity-dependent trafficking of presynaptic choline transporters J. Neurosci. 23 2003 9697 9709
10. J.J. Freeman, J.W. Kosh, and J.S. Parrish Peripheral toxicity of hemicholinium-3 in mice Br. J. Pharmacol. 77 1982 239 244
11. C. Giuliano, V. Parikh, J.R. Ward, C. Chiamulera, and M. Sarter Increases in cholinergic neurotransmission measured by using choline-sensitive microelectrodes: enhanced detection by hydrolysis of acetylcholine on recording sites? Neurochem. Int. 52 2008 1343 1350
12. G. Guidry, B.D. Willison, R.D. Blakely, S.C. Landis, and B.A. Habecker Developmental expression of the high affinity choline transporter in cholinergic sympathetic neurons Auton. Neurosci. 123 2005 54 61
13. P. Guyenet, P. Lefresne, J. Rossier, J.C. Beaujouan, and J. Glowinski Effect of sodium, hemicholinium-3 and antiparkinson drugs on (14C)acetylcholine synthesis and (3H)choline uptake in rat striatal synaptosomes Brain Res. 62 1973 523 529
14. M. Guzman, X. De Jaeger, S. Raulic, I. Souza, A. Li, S. Schmid, R. Menon, R. Gainetdinov, M. Caron, R. Bartha, V. Prado, and M. Prado Elimination of the vesicular acetylcholine transporter in the striatum reveals regulation of behaviour by cholinergic-glutamatergic co-transmission PLoS Biol. 9 2011 e1001194
15. R.V. Haberberger, U. Pfeil, K.S. Lips, and W. Kummer Expression of the high-affinity choline transporter, CHT1, in the neuronal and non-neuronal cholinergic system of human and rat skin J. Invest. Dermatol. 119 2002 943 948
16. T. Haga, and H. Noda Choline uptake systems of rat brain synaptosomes Biochim. Biophys. Acta 291 1973 564 575
17. E.C. Holmstrand, J. Asafu-Adjei, A.R. Sampson, R.D. Blakely, and S.R. Sesack Ultrastructural localization of high-affinity choline transporter in the rat anteroventral thalamus and ventral tegmental area: differences in axon morphology and transporter distribution J. Comp. Neurol. 518 2010 1908 1924
18. W.M. Howe, A.S. Berry, J. Francois, G. Gilmour, J.M. Carp, M. Tricklebank, C. Lustig, and M. Sarter Prefrontal cholinergic mechanisms instigating shifts from monitoring for cues to cue-guided performance. Converging electrochemical and fMRI evidence from rats and humans J. Neurosci. 33 2013 8742 8752
19. R.N. Hughes The value of spontaneous alternation behavior (SAB) as a test of retention in pharmacological investigations of memory Neurosci. Biobehav. Rev. 28 2004 497 505
20. H. Iwamoto, R.D. Blakely, and L.J. De Felice Na+, Cl-, and pH dependence of the human choline transporter (hCHT) in Xenopus oocytes: the proton inactivation hypothesis of hCHT in synaptic vesicles J. Neurosci. 26 2006 9851 9859
21. J. Klein, R. Gonzalez, A. Koppen, and K. Loffelholz Free choline and choline metabolites in rat brain and body fluids: sensitive determination and implications for choline supply to the brain Neurochem. Int. 22 1993 293 300
22. J. Klein, A. Köppen, and K. Löffelholz Uptake and storage of choline by rat brain: influence of dietary choline supplementation J. Neurochem. 57 1991 370 375
23. A. Köppen, J. Klein, C. Erb, and K. Löffelholz Acetylcholine release and choline availability in rat hippocampus: effects of exogenous choline and nicotinamide J. Pharmacol. Exp. Ther. 282 1997 1139 1145
24. R. Lalonde The neurobiological basis of spontaneous alternation Neurosci. Biobehav. Rev. 26 2002 91 104
25. A. Lara, D.D. Damasceno, R. Pires, R. Gros, E.R. Gomes, M. Gavioli, R.F. Lima, D. Guimaraes, P. Lima, C.R. Bueno Jr., A. Vasconcelos, D. Roman-Campos, C.A. Menezes, R.A. Sirvente, V.M. Salemi, C. Mady, M.G. Caron, A.J. Ferreira, P.C. Brum, R.R. Resende, J.S. Cruz, M.V. Gomez, V.F. Prado, A.P. de Almeida, M.A. Prado, and S. Guatimosim Dysautonomia due to reduced cholinergic neurotransmission causes cardiac remodeling and heart failure Mol. Cell. Biol. 30 2010 1746 1756
26. K.S. Lips, U. Pfeil, K. Reiners, C. Rimasch, K. Kuchelmeister, R.C. Braun-Dullaeus, R.V. Haberberger, R. Schmidt, and W. Kummer Expression of the high-affinity choline transporter CHT1 in rat and human arteries J. Histochem. Cytochem. 51 2003 1645 1654
27. D. Lund, A.M. Ruggiero, S.M. Ferguson, J. Wright, B.A. English, P.A. Reisz, S.M. Whitaker, A.C. Peltier, and R.D. Blakely Motor neuron-specific overexpression of the presynaptic choline transporter: impact on motor endurance and evoked muscle activity Neuroscience 171 2010 1041 1053
28. C. Martins-Silva, X. De Jaeger, M.S. Guzman, R.D. Lima, M.S. Santos, C. Kushmerick, M.V. Gomez, M.G. Caron, M.A. Prado, and V.F. Prado Novel strains of mice deficient for the vesicular acetylcholine transporter: insights on transcriptional regulation and control of locomotor behavior PLoS One 6 2011 e17611
29. A.C. Martyn, X. De Jaeger, A.C. Magalhaes, R. Kesarwani, D.F. Goncalves, S. Raulic, M.S. Guzman, M.F. Jackson, I. Izquierdo, J.F. Macdonald, M.A. Prado, and V.F. Prado Elimination of the vesicular acetylcholine transporter in the forebrain causes hyperactivity and deficits in spatial memory and long-term potentiation Proc. Natl. Acad. Sci. USA 109 2012 17651 17656
30. I.W. McLean, and P.K. Nakane Periodate-lysine-paraformaldehyde fixative. A new fixation for immunoelectron microscopy J. Histochem. Cytochem. 22 1974 1077 1083
31. Y.S. Mineur, A. Obayemi, M.B. Wigestrand, G.M. Fote, C.A. Calarco, A.M. Li, and M.R. Picciotto Cholinergic signaling in the hippocampus regulates social stress resilience and anxiety- and depression-like behavior Proc. Natl. Acad. Sci. USA 110 2013 3573 3578
32. A.H. Mulder, H.I. Yamamura, M.J. Kuhar, and S.H. Snyder Release of acetylcholine from hippocampal slices by potassium depolarization: dependence on high affinity choline uptake Brain Res. 70 1974 372 376
33. P.M. Nagy, and I. Aubert B6eGFPChAT mice overexpressing the vesicular acetylcholine transporter exhibit spontaneous hypoactivity and enhanced exploration in novel environments Brain Behav. 3 2013 367 383
34. K. Nakata, T. Okuda, and H. Misawa Ultrastructural localization of high-affinity choline transporter in the rat neuromuscular junction: enrichment on synaptic vesicles Synapse 53 2004 53 56
35. T. Okuda, T. Haga, Y. Kanai, H. Endou, T. Ishihara, and I. Katsura Identification and characterization of the high-affinity choline transporter Nat. Neurosci. 3 2000 120 125
36. V. Parikh, M. St Peters, R.D. Blakely, and M. Sarter The presynaptic choline transporter imposes limits on sustained cortical acetylcholine release and attention J. Neurosci. 33 2013 2326 2337
37. A.M. Ruggiero, J. Wright, S.M. Ferguson, M. Lewis, K.S. Emerson, H. Iwamoto, M.T. Ivy, E.C. Holmstrand, E.A. Ennis, C.D. Weaver, and R.D. Blakely Nonisotopic assay for presynaptic choline transport reveals capacity for allosteric modulation of choline uptake ACS Chem. Neurosci. 3 2012 767 781
38. A. Salahpour, A.J. Ramsey, I.O. Medvedev, B. Kile, T.D. Sotnikova, E. Holmstrand, V. Ghisi, P.J. Nicholls, L. Wong, K. Murphy, S.R. Sesack, R.M. Wightman, R.R. Gainetdinov, and M.G. Caron Increased amphetamine-induced hyperactivity and reward in mice overexpressing the dopamine transporter Proc. Natl. Acad. Sci. USA 105 2008 4405 4410
39. K. Sandberg, P.R. Sanberg, and J.T. Coyle Effects of intrastriatal injections of the cholinergic neurotoxin AF64A on spontaneous nocturnal locomotor behavior in the rat Brain Res. 299 1984 339 343
40. M. Sarter, V. Parikh, and W.M. Howe Phasic acetylcholine release and the volume transmission hypothesis: time to move on Nat. Rev. Neurosci. 10 2009 383 390
41. H.E. Shannon, and S.C. Peters A comparison of the effects of cholinergic and dopaminergic agents on scopolamine-induced hyperactivity in mice J. Pharmacol. Exp. Ther. 255 1990 549 553
42. S. Threlfell, T. Lalic, N.J. Platt, K.A. Jennings, K. Deisseroth, and S.J. Cragg Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons Neuron 75 2012 58 64
43. S. Wonnacott Presynaptic nicotinic ACh receptors Trends Neurosci. 20 1997 92 98
44. N.J. Woolf Cholinergic systems in mammalian brain and spinal cord Prog. Neurobiol. 37 1991 475 524