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Article

The Vesicular Acetylcholine Transporter Is Required for Neuromuscular Development and Function

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Pages 5238-5250 | Received 24 Feb 2009, Accepted 08 Jul 2009, Published online: 21 Mar 2023

REFERENCES

  • Alfonso, A., K. Grundahl, J. S. Duerr, H. P. Han, and J. B. Rand. 1993. The Caenorhabditis elegans unc-17 gene: a putative vesicular acetylcholine transporter. Science 261:617–619.
  • Barbosa, J., Jr., A. D. Clarizia, M. V. Gomez, M. A. Romano-Silva, V. F. Prado, and M. A. Prado. 1997. Effect of protein kinase C activation on the release of [3H]acetylcholine in the presence of vesamicol. J. Neurochem. 69:2608–2611.
  • Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248–254.
  • Brandon, E. P., W. Lin, K. A. D'Amour, D. P. Pizzo, B. Dominguez, Y. Sugiura, S. Thode, C. P. Ko, L. J. Thal, F. H. Gage, and K. F. Lee. 2003. Aberrant patterning of neuromuscular synapses in choline acetyltransferase-deficient mice. J. Neurosci. 23:539–549.
  • Brittain, R. T., G. P. Levy, and M. B. Tyers. 1969. The neuromuscular blocking action of 2-(4-phenylpiperidino)cyclohexanol (AH 5183). Eur. J. Pharmacol. 8:93–99.
  • Buss, R. R., T. W. Gould, J. Ma, S. Vinsant, D. Prevette, A. Winseck, K. A. Toops, J. A. Hammarback, T. L. Smith, and R. W. Oppenheim. 2006. Neuromuscular development in the absence of programmed cell death: phenotypic alteration of motoneurons and muscle. J. Neurosci. 26:13413–13427.
  • Cabeza, R., and B. Collier. 1988. Acetylcholine mobilization in a sympathetic ganglion in the presence and absence of 2-(4-phenylpiperidino)cyclohexanol (AH5183). J. Neurochem. 50:112–121.
  • Carpenter, R. S., R. Koenigsberger, and S. M. Parsons. 1980. Passive uptake of acetylcholine and other organic cations by synaptic vesicles from Torpedo electric organ. Biochemistry 19:4373–4379.
  • Ceccarelli, B., and W. P. Hurlbut. 1975. The effects of prolonged repetitive stimulation in hemicholinium on the frog neuromuscular junction. J. Physiol. 247:163–188.
  • Clarizia, A. D., M. V. Gomez, M. A. Romano-Silva, S. M. Parsons, V. F. Prado, and M. A. Prado. 1999. Control of the binding of a vesamicol analog to the vesicular acetylcholine transporter. Neuroreport 10:2783–2787.
  • Clarizia, A. D., M. A. Romano-Silva, V. F. Prado, M. V. Gomez, and M. A. M. Prado. 1998. Role of protein kinase C in the release of [H-3]acetylcholine from myenteric plexus treated with vesamicol. Neurosci. Lett. 244:115–117.
  • Clarke, P. G., and R. W. Oppenheim. 1995. Neuron death in vertebrate development: in vitro methods. Methods Cell Biol. 46:277–321.
  • Collier, B., S. A. Welner, J. Ricny, and D. M. Araujo. 1986. Acetylcholine synthesis and release by a sympathetic ganglion in the presence of 2-(4-phenylpiperidino)cyclohexanol (AH5183). J. Neurochem. 46:822–830.
  • Dan, Y., and M. M. Poo. 1992. Quantal transmitter secretion from myocytes loaded with acetylcholine. Nature 359:733–736.
  • de Castro, B. M., G. S. Pereira, V. Magalhães, J. I. Rossato, X. De Jaeger, C. Martins-Silva, B. Leles, P. Lima, M. V. Gomez, R. R. Gainetdinov, M. G. Caron, I. Izquierdo, M. Cammarota, V. F. Prado, and M. A. Prado. 2009. Reduced expression of the vesicular acetylcholine transporter causes learning deficits in mice. Genes Brain Behav. 8:23–35.
  • Dobransky, T., and R. J. Rylett. 2005. A model for dynamic regulation of choline acetyltransferase by phosphorylation. J. Neurochem. 95:305–313.
  • Dragatsis, I., and S. Zeitlin. 2000. CaMKIIalpha-Cre transgene expression and recombination patterns in the mouse brain. Genesis 26:133–135.
  • Edwards, R. H. 2007. The neurotransmitter cycle and quantal size. Neuron 55:835–858.
  • Estrella, D., K. L. Green, C. Prior, J. Dempster, R. F. Halliwell, R. S. Jacobs, S. M. Parsons, R. L. Parsons, and I. G. Marshall. 1988. A further study of the neuromuscular effects of vesamicol (AH5183) and of its enantiomer specificity. Br. J. Pharmacol. 93:759–768.
  • Falk-Vairant, J., P. Correges, L. Eder-Colli, N. Salem, E. Roulet, A. Bloc, F. Meunier, B. Lesbats, F. Loctin, M. Synguelakis, M. Israel, and Y. Dunant. 1996. Quantal acetylcholine release induced by mediatophore transfection. Proc. Natl. Acad. Sci. USA 93:5203–5207.
  • Ferguson, S. M., M. Bazalakova, V. Savchenko, J. C. Tapia, J. Wright, and R. D. Blakely. 2004. Lethal impairment of cholinergic neurotransmission in hemicholinium-3-sensitive choline transporter knockout mice. Proc. Natl. Acad. Sci. USA 101:8762–8767.
  • Ferguson, S. M., V. Savchenko, S. Apparsundaram, M. Zwick, J. Wright, C. J. Heilman, H. Yi, A. I. Levey, and R. D. Blakely. 2003. Vesicular localization and activity-dependent trafficking of presynaptic choline transporters. J. Neurosci. 23:9697–9709.
  • Ferguson, S. S., and M. G. Caron. 2004. Green fluorescent protein-tagged beta-arrestin translocation as a measure of G protein-coupled receptor activation. Methods Mol. Biol. 237:121–126.
  • Girod, R., S. Popov, J. Alder, J. Q. Zheng, A. Lohof, and M. M. Poo. 1995. Spontaneous quantal transmitter secretion from myocytes and fibroblasts: comparison with neuronal secretion. J. Neurosci. 15:2826–2838.
  • Glover, V. A., and L. T. Potter. 1971. Purification and properties of choline acetyltransferase from ox brain striate nuclei. J. Neurochem. 18:571–580.
  • Gomez, R. S., M. V. Gomez, and M. A. Prado. 1996. Inhibition of Na+, K+-ATPase by ouabain opens calcium channels coupled to acetylcholine release in guinea pig myenteric plexus. J. Neurochem. 66:1440–1447.
  • Gomez, R. S., M. A. Prado, F. Carazza, and M. V. Gomez. 1999. Halothane enhances exocytosis of [3H]-acetylcholine without increasing calcium influx in rat brain cortical slices. Br. J. Pharmacol. 127:679–684.
  • Heeroma, J. H., J. J. Plomp, E. W. Roubos, and M. Verhage. 2003. Development of the mouse neuromuscular junction in the absence of regulated secretion. Neuroscience 120:733–744.
  • Hosono, R., T. Sassa, and S. Kuno. 1987. Mutations affecting acetylcholine levels in the nematode Caenorhabditis elegans. J. Neurochem. 49:1820–1823.
  • Iwamoto, H., R. D. Blakely, and L. J. De Felice. 2006. 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. 26:9851–9859.
  • Kitamoto, T., X. Xie, C. F. Wu, and P. M. Salvaterra. 2000. Isolation and characterization of mutants for the vesicular acetylcholine transporter gene in Drosophila melanogaster. J. Neurobiol. 42:161–171.
  • Leao, R. M., M. V. Gomez, B. Collier, and M. A. Prado. 1995. Inhibition of potassium-stimulated acetylcholine release from rat brain cortical slices by two high-affinity analogs of vesamicol. Brain Res. 703:86–92.
  • Marchbanks, R. M., S. Wonnacott, and M. A. Rubio. 1981. The effect of acetylcholine release on choline fluxes in isolated synaptic terminals. J. Neurochem. 36:379–393.
  • Matteoli, M., K. Takei, M. S. Perin, T. C. Sudhof, and P. De Camilli. 1992. Exo-endocytotic recycling of synaptic vesicles in developing processes of cultured hippocampal neurons. J. Cell Biol. 117:849–861.
  • Misgeld, T., R. W. Burgess, R. M. Lewis, J. M. Cunningham, J. W. Lichtman, and J. R. Sanes. 2002. Roles of neurotransmitter in synapse formation: development of neuromuscular junctions lacking choline acetyltransferase. Neuron 36:635–648.
  • Nakata, K., T. Okuda, and H. Misawa. 2004. Ultrastructural localization of high-affinity choline transporter in the rat neuromuscular junction: enrichment on synaptic vesicles. Synapse 53:53–56.
  • Nguyen, M. L., G. D. Cox, and S. M. Parsons. 1998. Kinetic parameters for the vesicular acetylcholine transporter: two protons are exchanged for one acetylcholine. Biochemistry 37:13400–13410.
  • Oppenheim, R. W., J. Caldero, D. Cuitat, J. Esquerda, J. J. McArdle, B. M. Olivera, D. Prevette, and R. W. Teichert. 2008. The rescue of developing avian motoneurons from programmed cell death by a selective inhibitor of the fetal muscle-specific nicotinic acetylcholine receptor. Dev. Neurobiol. 68:972–980.
  • Oppenheim, R. W., D. Prevette, A. D'Costa, S. Wang, L. J. Houenou, and J. M. McIntosh. 2000. Reduction of neuromuscular activity is required for the rescue of motoneurons from naturally occurring cell death by nicotinic-blocking agents. J. Neurosci. 20:6117–6124.
  • Parsons, R. L., M. A. Calupca, L. A. Merriam, and C. Prior. 1999. Empty synaptic vesicles recycle and undergo exocytosis at vesamicol-treated motor nerve terminals. J. Neurophysiol. 81:2696–2700.
  • Parsons, S. M. 2000. Transport mechanisms in acetylcholine and monoamine storage. FASEB J. 14:2423–2434.
  • Pittman, R., and R. W. Oppenheim. 1979. Cell death of motoneurons in the chick embryo spinal cord. IV. Evidence that a functional neuromuscular interaction is involved in the regulation of naturally occurring cell death and the stabilization of synapses. J. Comp. Neurol. 187:425–446.
  • Pittman, R. H., and R. W. Oppenheim. 1978. Neuromuscular blockade increases motoneurone survival during normal cell death in the chick embryo. Nature 271:364–366.
  • Prado, M. A., T. Moraes-Santos, R. N. Freitas, M. A. Silva, and M. V. Gomez. 1990. Choline oxidase chemiluminescent assay, after removal of eserine from medium, of acetylcholine released in vitro from brain slices. J. Neurosci. Methods 31:193–196.
  • Prado, M. A. M., M. V. Gomez, and B. Collier. 1992. Mobilization of the readily releasable pool of acetylcholine from a sympathetic-ganglion by tityustoxin in the presence of vesamicol. J. Neurochem. 59:544–552.
  • Prado, M. A. M., M. V. Gomez, and B. Collier. 1993. Mobilization of a vesamicol-insensitive pool of acetylcholine from a sympathetic-ganglion by ouabain. J. Neurochem. 61:45–56.
  • Prado, V. F., C. Martins-Silva, B. M. de Castro, R. F. Lima, D. M. Barros, E. Amaral, A. J. Ramsey, T. D. Sotnikova, M. R. Ramirez, H. G. Kim, J. I. Rossato, J. Koenen, H. Quan, V. R. Cota, M. F. Moraes, M. V. Gomez, C. Guatimosim, W. C. Wetsel, C. Kushmerick, G. S. Pereira, R. R. Gainetdinov, I. Izquierdo, M. G. Caron, and M. A. Prado. 2006. Mice deficient for the vesicular acetylcholine transporter are myasthenic and have deficits in object and social recognition. Neuron 51:601–612.
  • Prado, V. F., M. A. M. Prado, and S. M. Parsons. 2008. VAChT. UCSD-Nature Molecule Pages. doi:10.1038/mp.a002796.01.
  • Rempe, D., G. Vangeison, J. Hamilton, Y. Li, M. Jepson, and H. J. Federoff. 2006. Synapsin I Cre transgene expression in male mice produces germline recombination in progeny. Genesis 44:44–49.
  • Ribeiro, F. M., J. Alves-Silva, W. Volknandt, C. Martins-Silva, H. Mahmud, A. Wilhelm, M. V. Gomez, R. J. Rylett, S. S. Ferguson, V. F. Prado, and M. A. Prado. 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.
  • Ribeiro, F. M., S. A. Black, S. P. Cregan, V. F. Prado, M. A. Prado, R. J. Rylett, and S. S. Ferguson. 2005. Constitutive high-affinity choline transporter endocytosis is determined by a carboxyl-terminal tail dileucine motif. J. Neurochem. 94:86–96.
  • Ribeiro, F. M., S. A. Black, V. F. Prado, R. J. Rylett, S. S. Ferguson, and M. A. Prado. 2006. The “ins” and “outs” of the high-affinity choline transporter CHT1. J. Neurochem. 97:1–12.
  • Richards, D. A., C. Guatimosim, S. O. Rizzoli, and W. J. Betz. 2003. Synaptic vesicle pools at the frog neuromuscular junction. Neuron 39:529–541.
  • Song, H., G. Ming, E. Fon, E. Bellocchio, R. H. Edwards, and M. Poo. 1997. Expression of a putative vesicular acetylcholine transporter facilitates quantal transmitter packaging. Neuron 18:815–826.
  • Sudhof, T. C. 2004. The synaptic vesicle cycle. Annu. Rev. Neurosci. 27:509–547.
  • Sun, Y. A., and M. M. Poo. 1985. Non-quantal release of acetylcholine at a developing neuromuscular synapse in culture. J. Neurosci. 5:634–642.
  • Tucek, S. 1985. Regulation of acetylcholine synthesis in the brain. J. Neurochem. 44:11–24.
  • Vaca, K., and G. Pilar. 1979. Mechanisms controlling choline transport and acetylcholine synthesis in motor nerve terminals during electrical stimulation. J. Gen. Physiol. 73:605–628.
  • Van der Kloot, W. 1986. 2-(4-Phenylpiperidino)cyclohexanol (AH5183) decreases quantal size at the frog neuromuscular junction. Pflugers Arch. 406:83–85.
  • Van der Kloot, W. 2003. Loading and recycling of synaptic vesicles in the Torpedo electric organ and the vertebrate neuromuscular junction. Prog. Neurobiol. 71:269–303.
  • Vyskocil, F., and P. Illes. 1977. Non-quantal release of transmitter at mouse neuromuscular junction and its dependence on the activity of Na+-K+ ATP-ase. Pflugers Arch. 370:295–297.
  • Wang, Y. M., R. R. Gainetdinov, F. Fumagalli, F. Xu, S. R. Jones, C. B. Bock, G. W. Miller, R. M. Wightman, and M. G. Caron. 1997. Knockout of the vesicular monoamine transporter 2 gene results in neonatal death and supersensitivity to cocaine and amphetamine. Neuron 19:1285–1296.
  • Whitton, P. S., I. G. Marshall, and S. M. Parsons. 1986. Reduction of quantal size by vesamicol (AH5183), an inhibitor of vesicular acetylcholine storage. Brain Res. 385:189–192.
  • Yang, H., and S. Kunes. 2004. Nonvesicular release of acetylcholine is required for axon targeting in the Drosophila visual system. Proc. Natl. Acad. Sci. USA 101:15213–15218.
  • Zhu, H., J. S. Duerr, H. Varoqui, J. R. McManus, J. B. Rand, and J. D. Erickson. 2001. Analysis of point mutants in the Caenorhabditis elegans vesicular acetylcholine transporter reveals domains involved in substrate translocation. J. Biol. Chem. 276:41580–41587.

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