Intercellular Ca(2+) waves induce temporally and spatially distinct intracellular Ca(2+) oscillations in glia.
Mechanically induced intercellular Ca(2+) waves propagated for approximately 300 microm in primary glial cultures. Following the wave propagation, 34% of the cells displayed Ca(2+) oscillations in a zone 60-120 microm from the stimulated cell. The initiation, frequency, and duration of these Ca(2+) oscillations were dependent on the cells' distance from the wave origin but were not dependent on the cell type nor on the magnitude of the Ca(2+) wave. When an individual cell propagated two sequential intercellular Ca(2+) waves originating from different sites, the characteristics of the Ca(2+) oscillations initiated by each wave were determined by the distance of the cell from the origin of each wave. Each Ca(2+) oscillation commonly occurred as an intracellular Ca(2+) wave that was initiated from a specific site within the cell. The position of the initiation site and the direction of the intracellular Ca(2+) wave were independent of the orientation of the initial intercellular Ca(2+) wave. Because initiation and frequency of Ca(2+) oscillations are dependent on the intracellular inositol trisphosphate concentration ([IP(3)](i)), we propose that the zone of cells displaying Ca(2+) oscillations is determined by an intercellular gradient of [IP(3)](i), established by the diffusion of IP(3) through gap junctions during the propagation of the intercellular Ca(2+) wave. Exposure to acetylcholine, a muscarinic agonist that initiates IP(3) production, shifted the zone of oscillating cells about 45 microm farther away from the origin of the mechanically induced wave. These findings indicate that a glial syncytium can resolve information provided by a local Ca(2+) wave into a distinct spatial and temporal pattern of Ca(2+) oscillations.
Strahonja-Packard
A
A
Department of Physiology, University of Massachusetts Medical School, Worcester, Massachusetts 01655, USA.
Sanderson
M J
MJ
D000109:Acetylcholine / Q000494:pharmacology / Q000502:physiology; D000818:Animals; D002118:Calcium / Q000378:metabolism*; D020013:Calcium Signaling / Q000187:drug effects / Q000502:physiology*; D018929:Cell Culture Techniques; D005110:Extracellular Space / Q000378:metabolism* / Q000502:physiology*; D016257:Fura-2; D005696:Galactosidases / Q000032:analysis; D017629:Gap Junctions / Q000502:physiology; D005904:Glial Fibrillary Acidic Protein / Q000032:analysis; D007150:Immunohistochemistry; D015544:Inositol 1,4,5-Trisphosphate / Q000378:metabolism*; D009457:Neuroglia / Q000187:drug effects / Q000378:metabolism*; D010812:Physical Stimulation; D051381:Rats; D011976:Receptors, Muscarinic / Q000737:chemistry / Q000502:physiology; D013997:Time Factors
D005904:Glial Fibrillary Acidic Protein; D011976:Receptors, Muscarinic; D015544:Inositol 1,4,5-Trisphosphate; D005696:Galactosidases; D000109:Acetylcholine; D002118:Calcium; D016257:Fura-2