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Journal of Neuroscience, Vol 8, 3208-3220, Copyright © 1988 by Society for Neuroscience
Capsaicin-induced ion fluxes in dorsal root ganglion cells in culture
JN Wood, J Winter, IF James, HP Rang, J Yeats and S Bevan
Sandoz Institute for Medical Research, London, England.
Capsaicin is a pungent pain-producing compound found in plants of the
capsicum family; it exerts excitatory, desensitizing, and toxic effects on
a subset of sensory neurons, including the polymodal nociceptor population.
We have carried out a quantitative study of capsaicin- induced fluxes of
sodium, guanidine, calcium, rubidium, and chloride ions in cultures of
neonatal and adult rat DRG neurons, in conjunction with the use of a
histochemical stain that identifies capsaicin- sensitive neurons by means
of cobalt uptake. Those cells that take up cobalt in a capsaicin-dependent
manner (EC50 = 0.2 microM) represent about 50% of the total neuronal
population derived from neonatal DRGs on short-term culture. Overnight
treatment of cultures with 2 microM capsaicin leads to the loss of the
cobalt-staining subpopulation. The capsaicin-insensitive neurons contain
immunoreactive neurofilament epitopes that are present in fewer than 10% of
capsaicin-sensitive neurons. This observation provides indirect evidence
that the sensitive cells correspond to the small, dark B-type neurons,
which are negative for neurofilament immunoreactivity in vivo. A
capsaicin-dependent calcium uptake (EC50 = 0.2 microM), as measured by 45Ca
incorporation, is shown by a DRG neuronal subpopulation that, like the
cobalt-staining population of DRG neurons, is lost after overnight
capsaicin treatment (2 microM). Capsaicin application leads to the
accumulation of millimolar levels of calcium within a few minutes. Cadmium
and other divalent cations block capsaicin-induced calcium uptake, but
little or no inhibition is seen with organic calcium channel antagonists.
Mitochondria, rather than the endoplasmic reticulum, are the probable
destination of the internalized calcium, because ruthenium red inhibits
calcium uptake (IC50 = 0.05 microM), whereas methylxanthines are inactive.
The subset of sensory neurons that takes up calcium also releases 86Rb when
exposed to capsaicin (EC50 = 0.06 microM). No efflux of 36Cl ions could be
induced by capsaicin. These cells also show a capsaicin-induced uptake of
22Na or 14C guanidine (EC50 = 0.06 microM). In contrast, chick DRG cells in
culture showed no capsaicin-induced calcium or cobalt uptake. Primary
cultures of rat superior cervical ganglion neurons and Schwann cells, and a
number of neuronal cell lines, also failed to respond to capsaicin, as
judged by the calcium, cobalt, or guanidine uptake assays.
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