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Journal of Neuroscience, Vol 7, 2153-2162, Copyright © 1987 by Society for Neuroscience
Ultrastructural distribution of 125I-toxin F binding sites on chick ciliary neurons: synaptic localization of a toxin that blocks ganglionic nicotinic receptors
RH Loring and RE Zigmond
Although alpha-bungarotoxin (BGT), a common probe for nicotinic ACh
receptors from vertebrate skeletal muscle, binds tightly to many autonomic
ganglia, it fails to block nicotinic transmission in most of these ganglia.
Recently, we have isolated a second toxin, toxin F, that blocks
transmission in several autonomic ganglia, including the chick ciliary
ganglion. 125I-Toxin F binds to 2 sites in the ciliary ganglion: one site
that is also recognized by BGT and one site that is not. Since the presence
of BGT fails to prevent the blocking effect of toxin F, the toxin F site
not recognized by BGT most likely represents the neuronal nicotinic
receptor. Accordingly, we have localized the binding of 125I-toxin F to
both sites, using electron-microscopic autoradiography. After a 45 min
incubation, 125I-toxin F binding sensitive to BGT was primarily localized
extrasynaptically on the neuronal plasma membranes; however, by 4 hr, much
of this site had been internalized. In contrast, the 125I-toxin F binding
site not recognized by BGT was highly concentrated near synaptic membranes
at both times. Pretreatment of ganglia with the classic nicotinic
antagonists dihydro- beta-erythroidine (DHBE) and d-tubocurarine (DTC)
significantly reduced 125I-toxin F binding to the toxin F-specific site.
The average density of these sites on synaptic membranes was approximately
600 sites/micron 2. We conclude that toxin F binds to 2 pharmacologically
distinct sites in the ciliary ganglion and that these sites are distributed
differently over the plasma membrane of ciliary neurons. On the basis of
the density of the toxin F-specific binding sites at synaptic membranes, we
infer that the density of synaptic nicotinic receptors on these neurons is
at least 20-fold lower than the density of nicotinic receptors at the
vertebrate neuromuscular junction, as determined by BGT binding. These
findings are consistent with those of electrophysiological studies, which
also suggest low nicotinic receptor densities on ganglionic neurons.
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