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Originally published In Press as doi:10.1074/jbc.M203952200 on May 14, 2002

J. Biol. Chem., Vol. 277, Issue 29, 26364-26371, July 19, 2002
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Calcium Oscillations Trigger Focal Adhesion Disassembly in Human U87 Astrocytoma Cells*

Gregory GiannoneDagger , Philippe Rondé§, Mireille Gaire, Jacques Haiech, and Kenneth Takeda

From the Laboratoire de Pharmacologie et Physicochimie des Interactions Cellulaires et Moléculaires, UMR CNRS 7034, Université Louis Pasteur de Strasbourg, 67401 Illkirch, France

Integrin-associated intracellular Ca2+ oscillations modulate cell migration, probably by controlling integrin-mediated release of the cell rear during migration. Focal adhesion kinase (FAK), via its tyrosine phosphorylation activity, plays a key role in integrin signaling. In human U87 astrocytoma cells, expression of the dominant negative FAK-related non-kinase domain (FRNK) inhibits the Ca2+-sensitive component of serum-dependent migration. We investigated how integrin-associated Ca2+ signaling might be coupled to focal adhesion (FA) dynamics by visualizing the effects of Ca2+ spikes on FAs using green fluorescent protein (GFP)-tagged FAK and FRNK. We report that Ca2+ spikes are temporally correlated with movement and disassembly of FAs, but not their formation. FRNK transfection did not affect generation of Ca2+ spikes, although cell morphology was altered, with fewer FAs of larger size and having a more peripheral localization being observed. Larger sized FAs in FRNK-transfected cells were not disassembled by Ca2+ spikes, providing a possible explanation for impaired Ca2+-dependent migration in these cells. Stress fiber end movements initiated by Ca2+ spikes were visualized using GFP-tagged myosin light chain kinase (MLCK). Ca2+-associated movements of stress fiber ends and FAs had similar kinetics, suggesting that stress fibers and FAs move in a coordinated fashion. This indicates that increases in Ca2+ likely trigger disassembly of adhesive structures that involves disruption of integrin-extracellular matrix interactions, supporting a key role for Ca2+-sensitive inside-out signaling in cell migration. A rapid increase in tyrosine phosphorylation of FAK was found in response to an elevation in Ca2+ induced by thapsigargin, and we propose that this represents the initial triggering event linking Ca2+ signaling and FA dynamics to cell motility.

* This work was supported in part by the Ligue Nationale Contre le Cancer (Comités du Haut Rhin et du Bas Rhin), the Fondation pour la Recherche Médicale, the Assocation pour la Recherche Contre le Cancer, and the Association Régionale pour l'Enseignement et la Recherche Scientifique en Champagne-Ardenne.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Dagger Present address: Columbia University, Dept. of Biological Sciences, P. O. Box 2408, Sherman Fairchild Center, 1212 Amsterdam Ave., New York, NY 10027.

§ Recipient of a Fellowship from the Ligue Nationale Contre le Cancer.

To whom correspondence should be addressed: Pharmacologie et Physicochimie, UMR CNRS 7034, Université Louis Pasteur, BP 24, 67401 Illkirch, France.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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