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Swelling‐activated calcium signalling in cultured mouse primary sensory neurons
Author(s) -
Viana Félix,
De La Peña Elvira,
Pecson Brian,
Schmidt Robert F.,
Belmonte Carlos
Publication year - 2001
Publication title -
european journal of neuroscience
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.346
H-Index - 206
eISSN - 1460-9568
pISSN - 0953-816X
DOI - 10.1046/j.0953-816x.2000.01441.x
Subject(s) - biophysics , sensory neuron , stimulation , extracellular , chemistry , trigeminal ganglion , depolarization , calcium , tonicity , thapsigargin , membrane potential , electrophysiology , neuron , calcium in biology , intracellular , neuroscience , endocrinology , medicine , biochemistry , biology , sensory system , organic chemistry
Abstract The effects of hypo‐osmotic membrane stretch on intracellular calcium concentration ([Ca 2+ ] i ), cell volume and cellular excitability were investigated in cultured mouse primary sensory trigeminal neurons. Hypotonic solutions (15–45%) led to rapid cell swelling in all neurons. Swelling was accompanied by dose‐dependent elevations in [Ca 2+ ] i in a large fraction of neurons. Responses could be classified into three categories. (i) In 57% of the neurons [Ca 2+ ] i responses had a slow rise time and were generally of small amplitude. (ii) In 21% of the neurons, responses had a faster rise and were larger in amplitude. (iii) The remaining cells (22%) did not show [Ca 2+ ] i responses to hypo‐osmotic stretch. Slow and fast [Ca 2+ ] i changes were observed in trigeminal neurons of different sizes with variable responses to capsaicin (0.5 µ m ). The swelling‐induced [Ca 2+ ] i responses were not abolished after depletion of intracellular Ca 2+ stores with cyclopiazonic acid or preincubation in thapsigargin, but were suppressed in the absence of external Ca 2+ . They were strongly attenuated by extracellular nickel and gadolinium. Hypotonic stimulation led to a decrease in input resistance and to membrane potential depolarization. Under voltage‐clamp, the [Ca 2+ ] i elevation produced by hypotonic stimulation was accompanied by the development of an inward current and a conductance increase. The time course and amplitude of the [Ca 2+ ] i response to hypo‐osmotic stimulation showed a close correlation with electrophysiological properties of the neurons. Fast [Ca 2+ ] i responses were characteristic of trigeminal neurons with short duration action potentials and marked inward rectification. These findings suggest that hypo‐osmotic stimulation activates several Ca 2+ ‐influx pathways, including Gd 3+ ‐sensitive stretch‐activated ion channels, in a large fraction of trigeminal ganglion neurons. Opening of voltage‐gated Ca 2+ channels also contributes to the response. The pattern and rate of Ca 2+ influx may be correlated with functional subtypes of sensory neurons.