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Journal of Neuroscience, Vol 6, 803-813, Copyright © 1986 by Society for Neuroscience
The bag cells of Aplysia as a multitransmitter system: identification of alpha bag cell peptide as a second neurotransmitter
KA Sigvardt, BS Rothman, RO Brown and E Mayeri
The bag cell neurons of the marine mollusk, Aplysia, are a putative
multitransmitter system that utilizes two or more peptide transmitters
derived from a common precursor protein. Two putative transmitters are
egg-laying hormone (ELH), a 36 amino acid peptide that induces egg laying
and mediates bag cell-induced excitatory effects on certain abdominal
ganglion neurons, and alpha-bag cell peptide (alpha BCP), which mimics bag
cell-induced inhibition of the left upper quadrant (LUQ) neurons and the
depolarization of the bag cells that occurs during the bag cell burst
discharge. Alpha BCP was previously purified from bag cell extracts in
three neuroactive forms: alpha BCP(1-9), a nine amino acid peptide encoded
on the ELH/BCP precursor protein, and two NH2-terminal fragments, alpha
BCP(1-8) and alpha BCP(1-7). Analyzing bag cell-induced inhibition of LUQ
neurons, we report here that alpha BCP fulfills the main criteria for
transmitter identification: stimulation of individual bag cells produces
inhibition of the neurons; inhibitory activity is present in releasate
collected following an elicited bag cell burst discharge in the presence of
protease inhibitors; alpha BCP(1-9) and alpha BCP(1-8) are detected in the
releasate in the presence of protease inhibitors; alpha BCP is rapidly
inactivated after release, as indicated by the lack of detectable alpha BCP
or inhibitory activity in the releasate in the absence of protease
inhibitors, and by the increase in potency of the arterially perfused
peptide in the presence of protease inhibitors; alpha BCP and the
endogenously released transmitter produce apparently identical changes in
membrane conductance; bag cell-induced inhibition is reduced or abolished
following desensitization of the inhibitory response by long-term
application of high concentrations of alpha BCP. The results provide
additional evidence that the bag cells are a multitransmitter system and
also suggest that many of the physiological properties of alpha
BCP-mediated neurotransmission differ from those of ELH. First, unlike ELH,
alpha BCP is rapidly inactivated after release. Second, alpha BCP(1-9) may
be activated by carboxypeptidase cleavage since alpha BCP(1-8) and alpha
BCP(1-7) are 30 and 10X as potent, respectively, as alpha BCP(1-9). Third,
the inhibitory action of alpha BCP on its targets has a more rapid onset
and a shorter time course than the excitatory actions of ELH. Thus, alpha
BCP may diffuse to less distant targets than ELH and serve to regulate the
more rapidly occurring neural events underlying egg-laying behavior.
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