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The Journal of Neuroscience, June 15, 2002, 22(12):4850-4859

Control and Plasticity of Intercellular Calcium Waves in Astrocytes: A Modeling Approach

Thomas Höfer¹, Laurent Venance², and Christian Giaume²

¹ Theoretische Biophysik, Institut für Biologie, Humboldt-Universität Berlin, 10115 Berlin, Germany, and ² Institut National de la Santé et de la Recherche Médicale U114, Collège de France, 75231 Paris Cedex 05, France

Intercellular Ca²⁺ waves in astrocytes are thought to serve as a pathway of long-range signaling. The waves can propagate by the diffusion of molecules through gap junctions and across the extracellular space. In rat striatal astrocytes, the gap-junctional route was shown to be dominant. To analyze the interplay of the processes involved in wave propagation, a mathematical model of this system has been developed. The kinetic description of Ca²⁺ signaling within a single cell accounts for inositol 1,4,5-trisphosphate (IP₃) generation, including its activation by cytoplasmic Ca²⁺, IP₃-induced Ca²⁺ liberation from intracellular stores and various other Ca²⁺ transports, and cytoplasmic diffusion of IP₃ and Ca²⁺. When cells are coupled by gap junction channels in a two-dimensional array, IP₃ generation in one cell triggers Ca²⁺ waves propagating across some tens of cells. The spatial range of wave propagation is limited, yet depends sensitively on the Ca²⁺-mediated regeneration of the IP₃ signal. Accordingly, the term "limited regenerative signaling" is proposed. The gap-junctional permeability for IP₃ is the crucial permissive factor for wave propagation, and heterogeneity of gap-junctional coupling yields preferential pathways of wave propagation. Processes involved in both signal initiation (activation of IP₃ production caused by receptor agonist) and regeneration (activation of IP₃ production by Ca²⁺, loading of the Ca²⁺ stores) are found to exert the main control on the wave range. The refractory period of signaling strongly depends on the refilling kinetics of the Ca²⁺ stores. Thus the model identifies multiple steps that may be involved in the regulation of this intercellular signaling pathway.

Key words: intercellular calcium waves; glial cells; inositol 1,4,5-trisphosphate; phospholipase C; gap junctions; mathematical model

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Copyright © 2002 Society for Neuroscience  0270-6474/02/22124850-10$05.00/0

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