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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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Evoked ACh secretion is inhibited by ω−conotoxin  GVIA. Traces are representative examples of the membrane currents recorded from myocytes at the preformed synapses (A) and  the middle axonal segment (B). Evoked synaptic currents (small  arrows) were elicited by electrical stimulation of the cell body to  generate action potentials. Bath application of ω−conotoxin  GVIA (1 μM, large arrow) rapidly inhibited ESCs both at the  preformed synapses and at the middle axon. Samples of ESCs before and after ω−conotoxin GVIA application are shown below  at a higher resolution.
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Figure 7: Evoked ACh secretion is inhibited by ω−conotoxin GVIA. Traces are representative examples of the membrane currents recorded from myocytes at the preformed synapses (A) and the middle axonal segment (B). Evoked synaptic currents (small arrows) were elicited by electrical stimulation of the cell body to generate action potentials. Bath application of ω−conotoxin GVIA (1 μM, large arrow) rapidly inhibited ESCs both at the preformed synapses and at the middle axon. Samples of ESCs before and after ω−conotoxin GVIA application are shown below at a higher resolution.

Mentions: The action potential-induced neurotransmitter release is triggered by the rapid elevation of the cytoplasmic Ca2+ due to the opening of Ca2+ channels (Bennett, 1997). In Xenopus spinal cord neurons, evoked neurotransmitter release is mediated primarily by N-type Ca2+ channels (Yazejian et al., 1997). Application of a specific blocker of N-type Ca2+ channels, ω−conotoxin GVIA, dramatically inhibited evoked neurotransmitter secretion both at the presynaptic nerve terminal and at the middle axonal segment (Fig. 7). Hence, as seen in the presynaptic nerve terminal, the evoked ACh release at the middle axon is mediated largely by N-type Ca2+ channels.


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

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

Evoked ACh secretion is inhibited by ω−conotoxin  GVIA. Traces are representative examples of the membrane currents recorded from myocytes at the preformed synapses (A) and  the middle axonal segment (B). Evoked synaptic currents (small  arrows) were elicited by electrical stimulation of the cell body to  generate action potentials. Bath application of ω−conotoxin  GVIA (1 μM, large arrow) rapidly inhibited ESCs both at the  preformed synapses and at the middle axon. Samples of ESCs before and after ω−conotoxin GVIA application are shown below  at a higher resolution.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2132923&req=5

Figure 7: Evoked ACh secretion is inhibited by ω−conotoxin GVIA. Traces are representative examples of the membrane currents recorded from myocytes at the preformed synapses (A) and the middle axonal segment (B). Evoked synaptic currents (small arrows) were elicited by electrical stimulation of the cell body to generate action potentials. Bath application of ω−conotoxin GVIA (1 μM, large arrow) rapidly inhibited ESCs both at the preformed synapses and at the middle axon. Samples of ESCs before and after ω−conotoxin GVIA application are shown below at a higher resolution.
Mentions: The action potential-induced neurotransmitter release is triggered by the rapid elevation of the cytoplasmic Ca2+ due to the opening of Ca2+ channels (Bennett, 1997). In Xenopus spinal cord neurons, evoked neurotransmitter release is mediated primarily by N-type Ca2+ channels (Yazejian et al., 1997). Application of a specific blocker of N-type Ca2+ channels, ω−conotoxin GVIA, dramatically inhibited evoked neurotransmitter secretion both at the presynaptic nerve terminal and at the middle axonal segment (Fig. 7). Hence, as seen in the presynaptic nerve terminal, the evoked ACh release at the middle axon is mediated largely by N-type Ca2+ channels.

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