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Neurotransmitter secretion along growing nerve processes: comparison with synaptic vesicle exocytosis.

Zakharenko S, Chang S, O'Donoghue M, Popov SV - J. Cell Biol. (1999)

Bottom Line: We found that the parameters of neurotransmitter secretion at the nerve terminal and at the middle axon were strikingly similar.These results lead us to conclude that, as in the case of the presynaptic nerve terminal, synaptic vesicles involved in neurotransmitter release along the axon contain a complement of proteins for vesicle docking and Ca2+-dependent fusion.Taken together, our results support the idea that, in developing axons, the rudimentary machinery for quantal neurotransmitter secretion is distributed throughout the whole axonal surface.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology and Biophysics M/C 901, University of Illinois, Chicago, Illinois 60612, USA.

ABSTRACT
In mature neurons, synaptic vesicles continuously recycle within the presynaptic nerve terminal. In developing axons which are free of contact with a postsynaptic target, constitutive membrane recycling is not localized to the nerve terminal; instead, plasma membrane components undergo cycles of exoendocytosis throughout the whole axonal surface (Matteoli et al., 1992; Kraszewski et al., 1995). Moreover, in growing Xenopus spinal cord neurons in culture, acetylcholine (ACh) is spontaneously secreted in the quantal fashion along the axonal shaft (Evers et al., 1989; Antonov et al., 1998). Here we demonstrate that in Xenopus neurons ACh secretion is mediated by vesicles which recycle locally within the axon. Similar to neurotransmitter release at the presynaptic nerve terminal, ACh secretion along the axon could be elicited by the action potential or by hypertonic solutions. We found that the parameters of neurotransmitter secretion at the nerve terminal and at the middle axon were strikingly similar. These results lead us to conclude that, as in the case of the presynaptic nerve terminal, synaptic vesicles involved in neurotransmitter release along the axon contain a complement of proteins for vesicle docking and Ca2+-dependent fusion. Taken together, our results support the idea that, in developing axons, the rudimentary machinery for quantal neurotransmitter secretion is distributed throughout the whole axonal surface. Maturation of this machinery in the process of synaptic development would improve the fidelity of synaptic transmission during high-frequency stimulation of the presynaptic cell.

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α-Latrotoxin elicits massive neurotransmitter release  from Xenopus neurons. (A and B). Representative examples of  membrane currents recorded from myocytes at a preformed synapse (A) and from the myocyte manipulated into contact with  the middle axon (B). α-Latrotoxin (1 nM, arrow) was applied ∼5  min after the onset of recording. SSC frequency increased with a  characteristic delay of ∼10 min. (C) Quantitative analysis of the  effect of α-latrotoxin on neurotransmitter secretion at the preformed synapses (circles) and at the middle axon (squares).  Changes in the frequency of the current events with time after  the onset of α-latrotoxin application, normalized to the values at  the beginning of the recording. Data from five recordings at preformed synapses and five recordings at the middle axon were  normalized for each cell before averaging.
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Figure 13: α-Latrotoxin elicits massive neurotransmitter release from Xenopus neurons. (A and B). Representative examples of membrane currents recorded from myocytes at a preformed synapse (A) and from the myocyte manipulated into contact with the middle axon (B). α-Latrotoxin (1 nM, arrow) was applied ∼5 min after the onset of recording. SSC frequency increased with a characteristic delay of ∼10 min. (C) Quantitative analysis of the effect of α-latrotoxin on neurotransmitter secretion at the preformed synapses (circles) and at the middle axon (squares). Changes in the frequency of the current events with time after the onset of α-latrotoxin application, normalized to the values at the beginning of the recording. Data from five recordings at preformed synapses and five recordings at the middle axon were normalized for each cell before averaging.

Mentions: α-Latrotoxin is a potent stimulator of neurosecretion. Its action is mediated by the binding of the toxin to high-affinity presynaptic receptors (Petrenko et al., 1991; Krasnoperov et al., 1997). An unidentified signaling cascade leads to massive release of neurotransmitter from neurons and neuroendocrine cells (Longenecker et al., 1970; Rosenthal and Meldolesi, 1989). To investigate whether α-latrotoxin elicits ACh release from Xenopus neurons, we recorded quantal ACh release from the presynaptic nerve terminal and from the middle axon. Fig. 13 illustrates the result of a typical experiment. At both axonal regions, bath application of α-latrotoxin resulted in a dramatic increase in the SSC frequency (Fig. 13, A and B). 20 min after the onset of α-latrotoxin treatment, the SSC frequency increased ∼12 fold as compared with the control level of secretion. Potentiation of ACh release followed a similar kinetics at the preformed synapses and at the middle axon (Fig. 13 C).


Neurotransmitter secretion along growing nerve processes: comparison with synaptic vesicle exocytosis.

Zakharenko S, Chang S, O'Donoghue M, Popov SV - J. Cell Biol. (1999)

α-Latrotoxin elicits massive neurotransmitter release  from Xenopus neurons. (A and B). Representative examples of  membrane currents recorded from myocytes at a preformed synapse (A) and from the myocyte manipulated into contact with  the middle axon (B). α-Latrotoxin (1 nM, arrow) was applied ∼5  min after the onset of recording. SSC frequency increased with a  characteristic delay of ∼10 min. (C) Quantitative analysis of the  effect of α-latrotoxin on neurotransmitter secretion at the preformed synapses (circles) and at the middle axon (squares).  Changes in the frequency of the current events with time after  the onset of α-latrotoxin application, normalized to the values at  the beginning of the recording. Data from five recordings at preformed synapses and five recordings at the middle axon were  normalized for each cell before averaging.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2132923&req=5

Figure 13: α-Latrotoxin elicits massive neurotransmitter release from Xenopus neurons. (A and B). Representative examples of membrane currents recorded from myocytes at a preformed synapse (A) and from the myocyte manipulated into contact with the middle axon (B). α-Latrotoxin (1 nM, arrow) was applied ∼5 min after the onset of recording. SSC frequency increased with a characteristic delay of ∼10 min. (C) Quantitative analysis of the effect of α-latrotoxin on neurotransmitter secretion at the preformed synapses (circles) and at the middle axon (squares). Changes in the frequency of the current events with time after the onset of α-latrotoxin application, normalized to the values at the beginning of the recording. Data from five recordings at preformed synapses and five recordings at the middle axon were normalized for each cell before averaging.
Mentions: α-Latrotoxin is a potent stimulator of neurosecretion. Its action is mediated by the binding of the toxin to high-affinity presynaptic receptors (Petrenko et al., 1991; Krasnoperov et al., 1997). An unidentified signaling cascade leads to massive release of neurotransmitter from neurons and neuroendocrine cells (Longenecker et al., 1970; Rosenthal and Meldolesi, 1989). To investigate whether α-latrotoxin elicits ACh release from Xenopus neurons, we recorded quantal ACh release from the presynaptic nerve terminal and from the middle axon. Fig. 13 illustrates the result of a typical experiment. At both axonal regions, bath application of α-latrotoxin resulted in a dramatic increase in the SSC frequency (Fig. 13, A and B). 20 min after the onset of α-latrotoxin treatment, the SSC frequency increased ∼12 fold as compared with the control level of secretion. Potentiation of ACh release followed a similar kinetics at the preformed synapses and at the middle axon (Fig. 13 C).

Bottom Line: We found that the parameters of neurotransmitter secretion at the nerve terminal and at the middle axon were strikingly similar.These results lead us to conclude that, as in the case of the presynaptic nerve terminal, synaptic vesicles involved in neurotransmitter release along the axon contain a complement of proteins for vesicle docking and Ca2+-dependent fusion.Taken together, our results support the idea that, in developing axons, the rudimentary machinery for quantal neurotransmitter secretion is distributed throughout the whole axonal surface.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology and Biophysics M/C 901, University of Illinois, Chicago, Illinois 60612, USA.

ABSTRACT
In mature neurons, synaptic vesicles continuously recycle within the presynaptic nerve terminal. In developing axons which are free of contact with a postsynaptic target, constitutive membrane recycling is not localized to the nerve terminal; instead, plasma membrane components undergo cycles of exoendocytosis throughout the whole axonal surface (Matteoli et al., 1992; Kraszewski et al., 1995). Moreover, in growing Xenopus spinal cord neurons in culture, acetylcholine (ACh) is spontaneously secreted in the quantal fashion along the axonal shaft (Evers et al., 1989; Antonov et al., 1998). Here we demonstrate that in Xenopus neurons ACh secretion is mediated by vesicles which recycle locally within the axon. Similar to neurotransmitter release at the presynaptic nerve terminal, ACh secretion along the axon could be elicited by the action potential or by hypertonic solutions. We found that the parameters of neurotransmitter secretion at the nerve terminal and at the middle axon were strikingly similar. These results lead us to conclude that, as in the case of the presynaptic nerve terminal, synaptic vesicles involved in neurotransmitter release along the axon contain a complement of proteins for vesicle docking and Ca2+-dependent fusion. Taken together, our results support the idea that, in developing axons, the rudimentary machinery for quantal neurotransmitter secretion is distributed throughout the whole axonal surface. Maturation of this machinery in the process of synaptic development would improve the fidelity of synaptic transmission during high-frequency stimulation of the presynaptic cell.

Show MeSH
Related in: MedlinePlus