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Abstract:

The effects of adenosine on neurotransmission have been widely studied by monitoring transmitter release. However, the effects of adenosine on vesicle recycling are still unknown. We used fluorescence microscopy of FM2-10-labeled synaptic vesicles in combination with intracellular recordings to examine whether adenosine regulates vesicle recycling during high-frequency stimulation at mouse neuromuscular junctions. The A1 adenosine receptor antagonist (8-cyclopentyl-1,3-dipropylxanthine) increased the quantal content released during the first endplate potential, suggesting that vesicle exocytosis can be restricted by endogenous adenosine, which accordingly decreases the size of the recycling vesicle pool. Staining protocols designed to label specific vesicle pools that differ in their kinetics of release showed that all vesicles retrieved in the presence of 8-cyclopentyl-1,3-dipropylxanthine were recycled towards the fast-release pool, favoring its loading with FM2-10 and suggesting that endogenous adenosine promotes vesicle recycling towards the slow-release pool. In accordance with this effect, exogenous applied adenosine prevented the replenishment of the fast-release vesicle pool and, thus, hindered its loading with the dye. We had found that, during high-frequency stimulation, Ca 2+ influx through L-type channels directs newly formed vesicles to a fast-release pool (Perissinotti et al., 2008). We demonstrated that adenosine did not prevent the effect of the L-type blocker on transmitter release. Therefore, activation of the A1 receptor promotes vesicle recycling towards the slow-release pool without a direct effect on the L-type channel. Further studies are necessary to elucidate the molecular mechanisms involved in the regulation of vesicle recycling by adenosine. © 2010 Federation of European Neuroscience Societies and Blackwell Publishing Ltd.

Registro:

Documento: Artículo
Título:Adenosine drives recycled vesicles to a slow-release pool at the mouse neuromuscular junction
Autor:Perissinotti, P.P.; Uchitel, O.D.
Filiación:Departamento de Fisiología Biología Molecular y Celular, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón 2, piso 2, Buenos Aires 1428, Argentina
Palabras clave:FM2-10; levator auris longus; neuromodulator; vesicle pools; vesicle recycling; 8 cyclopentyl 1,3 dipropylxanthine; adenosine; animal experiment; animal tissue; article; calcium transport; cell vacuole; exocytosis; fluorescence microscopy; male; mouse; neuromuscular synapse; neurotransmitter release; nonhuman; priority journal; staining; synapse vesicle; Adenosine; Animals; Male; Mice; Motor Endplate; Neuromuscular Junction; Presynaptic Terminals; Receptors, Purinergic P1; Synaptic Vesicles; Time Factors; Xanthines
Año:2010
Volumen:32
Número:6
Página de inicio:985
Página de fin:996
DOI: http://dx.doi.org/10.1111/j.1460-9568.2010.07332.x
Título revista:European Journal of Neuroscience
Título revista abreviado:Eur. J. Neurosci.
ISSN:0953816X
CODEN:EJONE
CAS:8 cyclopentyl 1,3 dipropylxanthine, 102146-07-6; adenosine, 58-61-7; 1,3-dipropyl-8-cyclopentylxanthine, 102146-07-6; Adenosine, 58-61-7; Receptors, Purinergic P1; Xanthines
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_0953816X_v32_n6_p985_Perissinotti

Referencias:

  • Baxter, R.L., Vega-Riveroll, L.J., Deuchars, J., Parson, S.H., A2A adenosine receptors are located on presynaptic motor nerve terminals in the mouse (2005) Synapse, 57, pp. 229-234
  • Bennett, M.R., Karunanithi, S., Lavidis, N.A., Probabilistic secretion of quanta from nerve terminals in toad (Bufo marinus) muscle modulated by adenosine (1991) J. Physiol., 433, pp. 421-434
  • Betz, W.J., Depression of transmitter release at the neuromuscular junction of the frog (1970) J. Physiol., 206, pp. 629-644
  • Catterall, W.A., Structure and regulation of voltage-gated Ca2+ channels (2000) Annu. Rev. Cell Dev. Biol., 16, pp. 521-555
  • Ceccarelli, B., Hurlbut, W.P., Ca2+-dependent recycling of synaptic vesicles at the frog neuromuscular junction (1980) J. Cell Biol., 87, pp. 297-303
  • Ceccarelli, B., Hurlbut, W.P., Mauro, A., Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction (1973) J. Cell Biol., 57, pp. 499-524
  • Chen, Y., Deng, L., Maeno-Hikichi, Y., Lai, M., Chang, S., Chen, G., Zhang, J.F., Formation of an endophilin-Ca2+ channel complex is critical for clathrin-mediated synaptic vesicle endocytosis (2003) Cell, 115, pp. 37-48
  • Christensen, B.N., Martin, A.R., Estimates of probability of transmitter release at the mammalian neuromuscular junction (1970) J. Physiol., 210, pp. 933-945
  • Chung, C., Barylko, B., Leitz, J., Liu, X., Kavalali, E.T., Acute dynamin inhibition dissects synaptic vesicle recycling pathways that drive spontaneous and evoked neurotransmission (2010) J. Neurosci., 30, pp. 1363-1376
  • De Lorenzo, S., Veggetti, M., Muchnik, S., Losavio, A., Presynaptic inhibition of spontaneous acetylcholine release induced by adenosine at the mouse neuromuscular junction (2004) Br. J. Pharmacol., 142, pp. 113-124
  • Deák, F., Schoch, S., Liu, X., Südhof, T.C., Kavalali, E.T., Synaptobrevin is essential for fast synaptic-vesicle endocytosis (2004) Nat. Cell Biol., 6, pp. 1102-1108
  • Dowdall, M.J., Boyne, A.F., Whittaker, V.P., Adenosine triphosphate. A constituent of cholinergic synaptic vesicles (1974) Biochem. J., 140, pp. 1-12
  • Flink, M.T., Atchison, W.D., Ca2+ channels as targets of neurological disease: Lambert-Eaton syndrome and other Ca2+ channelopathies (2003) J. Bioenerg. Biomembr., 35, pp. 697-718
  • Galli, T., Haucke, V., (2004) Cycling of Synaptic Vesicles: How Far? How Fast!, , Science's STKE [electronic resource]: signal transduction knowledge environment
  • Von Gersdorff, H., Matthews, G., Inhibition of endocytosis by elevated internal calcium in a synaptic terminal (1994) Nature, 370, pp. 652-655
  • Hamilton, B.R., Smith, D.O., Autoreceptor-mediated purinergic and cholinergic inhibition of motor nerve terminal calcium currents in the rat (1991) J. Physiol., 432, pp. 327-341
  • Heuser, J.E., Reese, T.S., Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction (1973) J. Cell Biol., 57, pp. 315-344
  • Hirsh, J.K., Silinsky, E.M., Inhibition of spontaneous acetylcholine secretion by 2-chloroadenosine as revealed by a protein kinase inhibitor at the mouse neuromuscular junction (2002) Br. J. Pharmacol., 135, pp. 1897-1902
  • Hirsh, J.K., Searl, T.J., Silinsky, E.M., Regulation of Rab3A of an endogeneous modulator of neurotransmitter release at mouse motor nerve endings (2002) J. Physiol., 545, pp. 337-343
  • Kalandakanond, S., Coffield, J.A., Cleavage of SNAP-25 by botulinum toxin type A requires receptor-mediated endocytosis, pH-dependent translocation, and zinc (2001) J. Pharmacol. Exp. Ther., 296, pp. 980-986
  • Kuromi, H., Kidokoro, Y., Selective replenishment of two vesicle pools depends on the source of Ca2+ at the Drosophila synapse (2002) Neuron, 35, pp. 333-343
  • Liu, G.J., Werry, E.L., Bennett, M.R., Secretion of ATP from Schwann cells in response to uridine triphosphate (2005) Eur. J. Neurosci., 21, pp. 151-160
  • McLachlan, E.M., Martin, A.R., Non-linear summation of end-plate potentials in the frog and mouse (1981) J. Physiol., 311, pp. 307-324
  • Meriney, S.D., Grinnell, A.D., Endogenous adenosine modulates stimulation-induced depression at the frog neuromuscular junction (1991) J. Physiol., 443, pp. 441-455
  • Morgan, J.R., Augustine, G.J., Lafer, E.M., Synaptic vesicle endocytosis: The races, places, and molecular faces (2002) Neuromolecular Med., 2, pp. 101-114
  • Moulder, K.L., Mennerick, S., Reluctant vesicles contribute to the total readily releasable pool in glutamatergic hippocampal neurons (2005) J. Neurosci., 25, pp. 3842-3850
  • Nagano, O., Foldes, F.F., Nakatsuka, H., Reich, D., Ohta, Y., Sperlagh, B., Vizi, E.S., Presynaptic A1-purinoceptor-mediated inhibitory effects of adenosine and its stable analogues on the mouse hemidiaphragm preparation (1992) Naunyn Schmiedebergs Arch. Pharmacol., 346, pp. 197-202
  • Nagy, A., Baker, R.R., Morris, S.J., Whittaker, V.P., The preparation and characterization of synaptic vesicles of high purity (1976) Brain Res., 109, pp. 285-309
  • Neher, E., Zucker, R.S., Multiple calcium-dependent processes related to secretion in bovine chromaffin cells (1993) Neuron, 10, pp. 21-30
  • Nicholson-Tomishima, K., Ryan, T.A., Kinetic efficiency of endocytosis at mammalian CNS synapses requires synaptotagmin i (2004) Proc. Natl Acad. Sci. USA, 101, pp. 16648-16652
  • Novick, P., Brennwald, P., Friends and family: The role of the Rab GTPases in vesicular traffic (1993) Cell, 75, pp. 597-601
  • Perissinotti, P.P., Tropper, B.G., Uchitel, O.D., L-type calcium channels are involved in fast endocytosis at the mouse neuromuscular junction (2008) Eur. J. Neurosci., 27, pp. 1333-1344
  • Pfeffer, S.R., Rab GTPases: Master regulators of membrane trafficking (1994) Curr. Opin. Cell Biol., 6, pp. 522-526
  • Polo-Parada, L., Bose, C.M., Landmesser, L.T., Alterations in transmission, vesicle dynamics, and transmitter release machinery at NCAM-deficient neuromuscular junctions (2001) Neuron, 32, pp. 815-828
  • Poskanzer, K.E., Marek, K.W., Sweeney, S.T., Davis, G.W., Synaptotagmin i is necessary for compensatory synaptic vesicle endocytosis in vivo (2003) Nature, 426, pp. 559-563
  • Protti, D.A., Uchitel, O.D., Transmitter release and presynaptic Ca2+ currents blocked by the spider toxin ω-Aga-IVA (1993) Neuroreport, 5, pp. 333-336
  • Pyle, J.L., Kavalali, E.T., Piedras-Rentería, E.S., Tsien, R.W., Rapid reuse of readily releasable pool vesicles at hippocampal synapses (2000) Neuron, 28, pp. 221-231
  • Redman, R.S., Silinsky, E.M., ATP released together with acetylcholine as the mediator of neuromuscular depression at frog motor nerve endings (1994) J. Physiol., 477, pp. 117-127
  • Ribeiro, J.A., Sebastiao, A.M., On the role, inactivation and origin of endogenous adenosine at the frog neuromuscular junction (1987) J. Physiol., 384, pp. 571-585
  • Ribeiro, J.A., Walker, J., The effects of adenosine triphosphate and adenosine diphosphate on transmission at the rat and frog neuromuscular junctions (1975) Br. J. Pharmacol., 54, pp. 213-218
  • Richards, D.A., Guatimosim, C., Betz, W.J., Two endocytic recycling routes selectively fill two vesicle pools in frog motor nerve terminals (2000) Neuron, 27, pp. 551-559
  • Richards, D.A., Guatimosim, C., Rizzoli, S.O., Betz, W.J., Synaptic vesicle pools at the frog neuromuscular junction (2003) Neuron, 39, pp. 529-541
  • Rizzoli, S.O., Betz, W.J., Synaptic vesicle pools (2005) Nat. Rev. Neurosci., 6, pp. 57-69
  • Rosenmund, C., Stevens, C.F., Definition of the readily releasable pool of vesicles at hippocampal synapses (1996) Neuron, 16, pp. 1197-1207
  • Schikorski, T., Stevens, C.F., Morphological correlates of functionally defined synaptic vesicle populations (2001) Nat. Neurosci., 4, pp. 391-395
  • Sheng, Z.H., Rettig, J., Cook, T., Catterall, W.A., Calcium-dependent interaction of N-type calcium channels with the synaptic core complex (1996) Nature, 379, pp. 451-454
  • Silinsky, E.M., On the mechanism by which adenosine receptor activation inhibits the release of acetylcholine from motor nerve endings (1984) J. Physiol., 346, pp. 243-256
  • Silinsky, E.M., Adenosine decreases both presynaptic calcium currents and neurotransmitter release at the mouse neuromuscular junction (2004) J. Physiol., 558, pp. 389-401
  • Silinsky, E.M., Modulation of calcium currents is eliminated after cleavage of a strategic component of the mammalian secretory apparatus (2005) J. Physiol., 566, pp. 681-688
  • Silinsky, E.M., Selective disruption of the mammalian secretory apparatus enhances or eliminates calcium current modulation in nerve endings (2008) Proc. Natl Acad. Sci. USA, 105, pp. 6427-6432
  • Simons, K., Zerial, M., Rab proteins and the road maps for intracellular transport (1993) Neuron, 11, pp. 789-799
  • Smith, D.O., Sources of adenosine released during neuromuscular transmission in the rat (1991) J. Physiol., 432, pp. 343-354
  • Stevens, C.F., Tsujimoto, T., Estimates for the pool size of releasable quanta at a single central synapse and for the time required to refill the pool (1995) Proc. Natl Acad. Sci. USA, 92, pp. 846-849
  • Südhof, T.C., The synaptic vesicle cycle revisited (2000) Neuron, 28, pp. 317-320
  • Takahashi, T., Momiyama, A., Different types of calcium channels mediate central synaptic transmission (1993) Nature, 366, pp. 156-158
  • Uchitel, O.D., Protti, D.A., Sanchez, V., Cherksey, B.D., Sugimori, M., Llinas, R., P-type voltage-dependent calcium channel mediates presynaptic calcium influx and transmitter release in mammalian synapses (1992) Proc. Natl Acad. Sci. USA, 89, pp. 3330-3333
  • Urbano, F.J., Depetris, R.S., Uchitel, O.D., Coupling of L-type calcium channels to neurotransmitter release at mouse motor nerve terminals (2001) Pflugers Arch., 441, pp. 824-831
  • Veggetti, M., Muchnik, S., Losavio, A., Effect of purines on calcium-independent acetylcholine release at the mouse neuromuscular junction (2008) Neuroscience, 154, pp. 1324-1336
  • Voglmaier, S.M., Kam, K., Yang, H., Fortin, D.L., Hua, Z., Nicoll, R.A., Edwards, R.H., Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recycling (2006) Neuron, 51, pp. 71-84
  • Wang, C., Zucker, R.S., Regulation of synaptic vesicle recycling by calcium and serotonin (1998) Neuron, 21, pp. 155-167
  • Watanabe, H., Yamashita, T., Saitoh, N., Kiyonaka, S., Iwamatsu, A., Campbell, K.P., Mori, Y., Takahashi, T., Involvement of Ca2+ channel synprint site in synaptic vesicle endocytosis (2010) J. Neurosci., 30, pp. 655-660

Citas:

---------- APA ----------
Perissinotti, P.P. & Uchitel, O.D. (2010) . Adenosine drives recycled vesicles to a slow-release pool at the mouse neuromuscular junction. European Journal of Neuroscience, 32(6), 985-996.
http://dx.doi.org/10.1111/j.1460-9568.2010.07332.x
---------- CHICAGO ----------
Perissinotti, P.P., Uchitel, O.D. "Adenosine drives recycled vesicles to a slow-release pool at the mouse neuromuscular junction" . European Journal of Neuroscience 32, no. 6 (2010) : 985-996.
http://dx.doi.org/10.1111/j.1460-9568.2010.07332.x
---------- MLA ----------
Perissinotti, P.P., Uchitel, O.D. "Adenosine drives recycled vesicles to a slow-release pool at the mouse neuromuscular junction" . European Journal of Neuroscience, vol. 32, no. 6, 2010, pp. 985-996.
http://dx.doi.org/10.1111/j.1460-9568.2010.07332.x
---------- VANCOUVER ----------
Perissinotti, P.P., Uchitel, O.D. Adenosine drives recycled vesicles to a slow-release pool at the mouse neuromuscular junction. Eur. J. Neurosci. 2010;32(6):985-996.
http://dx.doi.org/10.1111/j.1460-9568.2010.07332.x