Journal of Neuroscience, Vol 11, 553-562, Copyright © 1991 by Society for Neuroscience
Stimulation of somatostatin expression in developing ciliary ganglion neurons by cells of the choroid layer
JN Coulombe and R Nishi
Department of Cell Biology and Anatomy, Oregon Health Sciences University, Portland 97201.
An important component of neuronal development is the matching of
neurotransmitter expression with the appropriate target cell. We have
examined how peptide transmitter expression is controlled in a simple model
system, the avian ciliary ganglion (CG). This parasympathetic ganglion
contains 2 distinct types of neurons: choroid neurons, which project to
vasculature in the eye's choroid layer and use somatostatin as a
co-transmitter with ACh, and ciliary neurons, which innervate the ciliary
body and iris and use ACh but no known peptide co-transmitter. We have
found that the earliest developmental stage in which neurons with
somatostatinlike immunoreactivity (SOM-IR) are consistently found in vivo
is stage 30 (embryonic day 6.5), a time shortly after the extension of
neurites to targets in the eye's choroid layer. In cell culture, CG neurons
expressed SOM-IR in co-culture with choroid cells, but not when cultured
with striated muscle myotubes or with ganglion non-neuronal cells. No
significant differences in neuronal survival or in ChAT activity were
observed under these different co-culture conditions, which suggests that
somatostatin expression is independently regulated. The stimulation of
somatostatin expression was also specific in that other neuropeptides
commonly found in autonomic neurons [neuropeptide Y (NPY), substance P
(SP), vasoactive intestinal polypeptide (VIP)] were not induced in the
presence of choroid cells. The ability to stimulate SOM-IR was not contact
dependent because a macromolecule of greater than or equal to 10 kDa in
choroid-conditioned medium (ChCM) was found to stimulate somatostatin
expression in a dosage-dependent fashion. The somatostatin-stimulating
activity induced SOM-IR in more than 90% of CG neurons, as well as in
retrogradely labeled ciliary neurons, which would not normally express
SOM-IR. Thus, the expression of somatostatin in cultured CG neurons is
regulated by a macromolecule produced by cells in the choroid layer, a
target normally innervated in vivo by CG neurons expressing somatostatin.