The Journal of Cell Biology, Vol 124, 463-474, Copyright © 1994 by The Rockefeller University Press

ARTICLES

Intracellular calcium and cAMP regulate directional pigment movements in teleost erythrophores

KJ Kotz and MA McNiven
Department of Molecular Neuroscience, Mayo Clinic, Rochester, Minnesota 55905.

Teleost pigment cells (erythrophores and melanophores) are useful models for studying the regulation of rapid, microtubule-dependent organelle transport. Previous studies suggest that melanophores regulate the direction of pigment movements via changes in intracellular cAMP (Rozdzial and Haimo, 1986a; Sammak et al., 1992), whereas erythrophores may use calcium- (Ca(2+)-) based regulation (Luby- Phelps and Porter, 1982; McNiven and Ward, 1988). Despite these observations, there have been no direct measurements in intact erythrophores or any cell type correlating changes of intracellular free Ca2+ ([Ca2+]i) with organelle movements. Here we demonstrate that extracellular Ca2+ is necessary and that a Ca2+ influx via microinjection is sufficient to induce pigment aggregation in erythrophores, but not melanophores of squirrel fish. Using the Ca(2+)- sensitive indicator, Fura-2, we demonstrate that [Ca2+]i rises dramatically concomitant with aggregation of pigment granules in erythrophores, but not melanophores. In addition, we find that an erythrophore stimulated to aggregate pigment will immediately transmit a rise in [Ca2+]i to neighboring cells, suggesting that these cells are electrically coupled. Surprisingly, we find that a fall in [Ca2+]i is not sufficient to induce pigment dispersion in erythrophores, contrary to the findings obtained with the ionophore and lysed-cell models (Luby- Phelps and Porter, 1982; McNiven and Ward, 1988). We find that a rise in intracellular cAMP ([cAMP]i) induces pigment dispersion, and that this dispersive stimulus can be overridden by an aggregation stimulus, suggesting that both high [cAMP]i and low [Ca2+]i are necessary to produce pigment dispersion in erythrophores.
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