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Journal of Neuroscience, Vol 13, 4229-4245, Copyright © 1993 by Society for Neuroscience
Calcium signaling of glial cells along mammalian axons
S Kriegler and SY Chiu
Biophysics Training Program, University of Wisconsin, Madison 53706.
Glial [Ca2+]i signaling was examined in a mammalian white matter lacking
neuronal cell bodies and synapses. Rat optic nerves (postnatal days 2 and
7) were stained with calcium indicator dyes and confocal images of [Ca2+bdi
were recorded at approximately 25 degrees C or approximately 37 degrees C.
Glial cell bodies showed spiking or sustained [Ca2+], response to
bath-applied glutamate (50-500 microM). The metabotropic glutamate agonist
trans-ACPD elicited transient, sometimes spiking, [Ca2+], responses,
whereas ionotropic agonists kainate and AMPA elicited a
6,7-dinitroquinoxaline-2,3-dione-sensitive, mostly sustained [Ca2+]i
response. Transient and spiking glial [Ca2+]i responses also were elicited
by adenosine and ATP (0.1-100 microM). Repetitive nerve stimulation (10-20
Hz) elicited [Ca2+bdi spiking in 15- 25% of glial cells in postnatal day 7
nerves, with spiking typically occurring 15-60 sec after onset of nerve
stimulation. At 37 degrees C, the frequency of glial [Ca2+]i spikes
increased from approximately 0.06 Hz to approximately 0.11 Hz when axonal
stimulation was increased from 10 to 20 Hz. This activity-dependent glial
spiking was inhibited by TTX, could not be mimicked by increasing the bath
K+ by 20 mM, and occurred when nerves were stimulated in the absence of
bath calcium. Activity-dependent and glutamate-induced glial spiking could
be mimicked by altering ionic gradients known to favor release of glutamate
via glutamate transporters, including elevation of intracellular Na+ by
veratridine concurrent with external K+ elevation. We suggest that glial
[Ca2+]i spiking observed during electrical activity resulted from
activation of glial receptors (e.g., metabotropic glutamate receptor,
adenosine receptor) by substances (e.g., glutamate, adenosine) released
from the optic nerve in a nonvesicular fashion, possibly through a reversal
of sodium-coupled transporters when Na+ and K+ gradients are altered by
prolonged nerve activity.
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