Reduced expression of the vesicular acetylcholine transporter and neurotransmitter content affects synaptic vesicle distribution and shape in mouse neuromuscular junction

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Rodrigues, Hermann A ^a   Fonseca, Matheus De C ^a   Camargo, Wallace L ^a   Lima, Patrícia M A ^b   Martinelli, Patrícia M ^a   Naves, Lígia A ^a   Prado, Vânia F ^c   Prado, Marco A M ^c   Guatimosim, Cristina ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO JOÃO DEL REI   (Brazil)

^c ROBARTS RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; VESAMICOL; VESICULAR ACETYLCHOLINE TRANSPORTER;

ACETYLCHOLINE RELEASE; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL SHAPE; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ELECTROSTIMULATION; MOUSE; NERVE ENDING; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEUROMUSCULAR SYNAPSE; NEUROTRANSMITTER RELEASE; NEUROTRANSMITTER UPTAKE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN TRANSPORT; SYNAPSE VESICLE;

ACETYLCHOLINE; ANIMALS; ELECTRIC STIMULATION; MICE; MICE, KNOCKOUT; MOTOR ENDPLATE; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; VESICULAR ACETYLCHOLINE TRANSPORT PROTEINS;

EID: 84892507477     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078342     Document Type: Article

References (56)

1. Misgeld T, Burgess RW, Lewis RM, Cunningham JM, Lichtman JW, et al (2002) Roles of neurotransmitter in synapse formation: development of neuromuscular junctions lacking choline acetyltransferase. Neuron 36: 635-648.
2. Brandon EP, Lin W, D'amour KA, Pizzo DP, Dominguez B, et al. (2003) Aberrant patterning of neuromuscular synapses in choline acetyltransferasedeficient mice. J Neurosci 23: 539-549.
3. de Castro BM, De Jaeger X, Martins-Silva C, Lima RD, Amaral E, et al. (2009) The vesicular acetylcholine transporter is required for neuromuscular development and function. Mol Cell Biol, 29: 5238-5250.
4. Prado VF, Roy A, Kolisnyk B, Gros R, Prado MA (2013) Regulation of cholinergic activity by the vesicular acetylcholine transporter. Biochem J 450: 265-274.
5. Birks RI, MacIntosh FC (1961) Acetylcholine metabolism of a sympathetic ganglion. Can J Biochem Physiol 39: 787-827.
6. Katz B (1971) Quantal Mechanism of Neural Transmitter Release. Science 173: 123-126.
7. Parsons SM (2000) Transport mechanisms in acetylcholine and monoamine storage. FASEB J 14: 2423-2434.
8. Van der Kloot W, Molgó J, Cameron R, Colasante C (2002) Vesicle size and transmitter release at the frog neuromuscular junction when quantal acetylcholine content is increased or decreased. J Physiol 541: 385-393.
9. Prado VF, Martins-Silva C, de Castro BM, Lima RF, Barros DM, et al. (2006) Mice deficient for the vesicular acetylcholine transporter are myasthenic and have déficits in object and social recognition. Neuron 51: 601-612.
10. Lima RF, Prado VF, Prado MA, Kushmerick C (2010) Quantal Release of Acetylcholine in Mice with Reduced Levels of the Vesicular Acetylcholine Transporter. J Neurochem 113: 943-951.
11. Lara A, Damasceno DD, Pires R, Gros R, Gomes ER, et al. (2010) Dysautonomia due to reduced cholinergic neurotransmission causes cardiac remodeling and heart failure. Mol Cell Biol 30: 1746-1756.
12. Terry AVJr, Parikh V, Gearhart DA, Pillai A, Hohnadel E, et al. (2006) Timedependent effects of haloperidol and ziprasidone on nerve growth factor, cholinergic neurons, and spatial learning in rats. J Pharmacol Exp Ther 318: 709-724.
13. Terry JrAV, Gearhart DA, Warner S, Hohnadel EJ, Middlemore ML, et al. (2007) Protracted effects of chronic oral haloperidol and risperidone on on nerve growth factor, cholinergic neurons, and spatial reference learning in rats. Neuroscience 150: 413-424.
14. Smith R, Chung H, Rundquist S, Maat-Schieman ML, Colgan L, et al. (2006) Cholinergic neuronal defect without cell loss in Huntington's disease. Hum Mol Genet 15: 3119-3131.
15. Chen KH, Reese EA, Kim HW, Rapoport SI, Rao JS (2011) Disturbed neurotransmitter transporter expression in Alzheimer's disease brain. J Alzheimers Dis 26: 755-766.
16. Betz WJ, Mao F, Bewick GS (1992) Activity dependent fluorescent staining and destaining of living vertebrate motor nerve terminals. J Neurosci 12: 363-375.
17. Gaffield MA, Betz WJ (2006) Imaging synaptic vesicle exocytosis and endocytosis with FM dyes. Nat Protoc 1: 2916-2921.
18. Whitton PS, Marshall IG, Parsons SM (1986) Reduction of quantal size by vesamicol (AH 5183), an inhibitor of vesicular acetylcholine storage. Brain Res 385: 189-192.
19. Becherer U, Guatimosim C, Betz WJ (2001) Effects of staurosporine on exocytosis and endocytosis at frog motor nerve terminals. J Neurosci 21: 782- 787.
20. 2+ channel density and vesicle docking at the presynaptic active zone. Neuron 69: 304-316.
21. Croft BG, Fortin GD, Corera AT, Edwards RH, Beaudet A, et al. (2005) Normal biogenesis and cycling of empty synaptic vesicles in dopamine neurons of vesicular monoamine transporter 2 knockout mice. Mol Biol Cell 16: 306-315.
22. Rosenmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16: 1197-1207.
23. Fatt P, Katz B (1952) Spontaneous subthreshold activity at motor nerve endings. J Physiol 117: 109-128.
24. Hubbard JI, Jones SF, Landau EM (1968) An examination of the effects of osmotic pressure changes upon transmitter release from mammalian motor nerve terminals. J Physiol 197: 639-657.
25. Kita H, Van der Kloot W (1977) Time course and magnitude of effects of changes in tonicity on acetylcholine release at frog neuromuscular junction. J Neurophysiol 40: 212-224.
26. Cheng H, Miyamoto MD (1999) Effect of hypertonicity on augmentation and potentiation and on corresponding quantal parameters of transmitter release. J Neurophysiol 81: 1428-1431.
27. Sara Y, Mozhayeva MG, Liu X, Kavalali ET (2002) Fast vesicle recycling supports neurotransmission during sustained stimulation at hippocampal synapses. J Neurosci 22: 1608-1617.
28. Fremeau JrRT, Kam K, Qureshi T, Johnson J, Copenhagen DR, et al. (2004) Vesicular glutamate transporter 1 e 2 target to functionally distinct synaptic release sites. Science 304: 1815-1819.
29. Rizzoli SO, Betz WJ (2005) Synaptic vesicle pools. Nat Rev Neurosci 6: 57-69.
30. Daniels RW, Collins CA, Gelfand MV, Dant J, Brooks ES, et al. (2004) Increased expression of the Drosophila vesicular glutamate transporter leads to excess glutamate release and a compensatory decrease in quantal content. J Neurosci 24: 10466-10474.
31. Daniels RW, Collins CA, Chen K, Gelfand MV, Featherstone DE, et al. (2006) A Single Vesicular Glutamate Transporter Is Sufficient to Fill a Synaptic Vesicle. Neuron 49: 11-16.
32. Colliver TL, Pyott SJ, Achalabun M, Ewing AG (2000) VMAT-Mediated changes in quantal size and vesicular volume. J Neurosci 20: 5276-5282.
33. Pothos EN, Larsen KE, Krantz DE, Liu Y, Haycock JW, et al. (2000). Synaptic vesicle transporter expression regulates vesicle phenotype and quantal size. J Neurosci 20: 7297-7306.
34. Budzinski KL, Allen RW, Fujimoto BS, Kensel-Hammes P, Belnap DM, et al. (2009) Large structural change in isolated synaptic vesicles upon loading with neurotransmitter. Biophys J 97: 2577-2584.
35. Marshall IG (1970) Studies on the blocking actions of 2-(4-phenylpiperidino) cyclohexanol (AH5183). Br J Pharmacol 38: 503-516.
36. Anderson DC, King SC, Parsons S M (1983) Pharmacological characterization of the acetylcholine transport system in purified Torpedo electric organ synaptic vesicles. Mol Pharmacol 24: 48-54.
37. Prado MA, Gomez MV, Collier B (1993) Mobilization of a vesamicol-insensitive pool of acetylcholine from a sympathetic ganglion by ouabain. J Neurochem. 61: 45-56.
38. Witzemann V (2006) Development of the neuromuscular junction. Cell Tissue Res 326: 263-271.
39. Katz B (1969) The Release of Neural Transmitter Substances (Liverpool University Press, Liverpool, UK).
40. Alabi AA, Tsien RW (2012) Synaptic vesicle pools and dynamics. Cold Spring Harb Perspect Biol 4: 1-18.
41. Kamin D, Lauterbach MA, Westphal V, Keller J, Schönle A, et al. (2010) Highand low-mobility stages in the synaptic vesicle cycle. Biophys J 99: 675-684.
42. Südhof TC (2000) The synaptic vesicle cycle revisited. Neuron 28: 317-320.
43. Bogen IL, Haug KH, Roberg B, Fonnum F, Walaas SI (2009) The importance of synapsin I and II for neurotransmitter levels and vesicular storage in cholinergic, glutamatergic and GABAergic nerve terminals. Neurochem Int 55: 13-21.
44. Parsons RL, Calupca MA, Merriam LA, Prior C (1999) Empty synaptic vesicles recycle and undergo exocytosis at vesamicol-treated motor nerve terminals. J Neurophysiol 81: 2696-2700.
45. Nguyen ML, Cox GD, Parsons SM (1998) Kinetic parameters of the vesicular acetylcholine transporter: two protons are exchanged for one acetylcholine. Biochemistry 37: 13400-13410.
46. Prado VF, Prado MA (2002) Signals involved in targeting membrane proteins to synaptic vesicles. Cell Mol Neurobiol 22: 565-577.
47. Siksou L, Silm K, Biesemann C, Nehring RB, Wojcik SM, et al. (2013) A role for vesicular glutamate tranporter 1 in synaptic vesicle clustering and mobility. Eur J Neurosci. 37: 1631-1642.
48. Rodrigues HA, Lima RF, Fonseca MC, Amaral E, Martinelli PM, et al. (2013) Membrane cholesterol regulates different modes of synaptic vesicle release and retrieval at the frog neuromuscular junction. Eur J Neurosci "In press".
49. Zhang B, Koh YH, Beckstead RB, Budnik V, Ganetzky B, et al. (1998) Synaptic vesicle size and number are regulated by a clathrin adaptor protein required for endocytosis. Neuron 21: 1465-1475.
50. Nonet ML, Holgado AM, Brewer F, Serpe CJ, Norbeck BA, et al. (1999) UNC-11, a Caenorhabditis elegans AP180 homologue, regulates the size and protein composition of synaptic vesicles. Mol Biol Cell 10: 2343-2360.
51. Petralia RS, Wang YX, Indig FE, Bushlin I, Wu F, et al. (2013) Reduction of AP180 and CALM produces defects in synaptic vesicle size and density. NeuroMolecular Med 15: 49-60.
52. Barbosa JJr, Ferreira LT, Martins-Silva C, Santos MS, Torres GE, et al. (2002) Trafficking of the vesicular acetylcholine transporter in SN56 cells: a dynaminsensitive step and interaction with the AP-2 adaptor complex. J Neurochem 82: 1221-1228.
53. Ferreira LT, Santos MS, Kolmakova NG, Koenen J, Barbosa JJr, et al. (2005) Structural requirements for steady-state localization of the vesicular acetylcholine transporter. J Neurochem 94: 957-69.
54. Kim MH, Hersh LB (2004) The vesicular acetylcholine transporter interacts with clathrin-associated adaptor complexes AP-1 and AP-2. J Biol Chem 279: 12580-12587.
55. Guzman MS, De Jaeger X, Raulic S, Souza IA, Li AX, et al. (2011) Elimination of the vesicular acetylcholine transporter in the striatum reveals regulation of behaviour by cholinergic-glutamatergic co-transmission. PLoS Biol 9: e1001194. doi: 10.1371/journal.pbio.1001194. Epub 2011.
56. Martyn AC, De Jaeger X, Magalhães AC, Kesarwani R, Gonçalves DF, et al. (2012) 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: 17651-17656.