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J. Biol. Chem., Vol. 279, Issue 27, 28715-28723, July 2, 2004

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Calcium Rises Locally Trigger Focal Adhesion Disassembly and Enhance Residency of Focal Adhesion Kinase at Focal Adhesions^*

Grégory Giannone, Philippe Rondé¶, Mireille Gaire, Joël Beaudouin||, Jacques Haiech, Jan Ellenberg||, and Kenneth Takeda**

From the Laboratoire de Pharmacologie et Physicochimie des Interactions Cellulaires et Moléculaires, Unité Mixte de Recherche CNRS 7034, Université Louis Pasteur de Strasbourg, 67401 Illkirch, France and ^||Gene Expression and Cell Biology/Biophysics Programmes, European Molecular Biology Laboratory, 69117 Heidelberg, Germany

Focal adhesion kinase (FAK) activity and Ca²⁺ signaling led to a turnover of focal adhesions (FAs) required for cell spreading and migration. We used yellow Cameleon-2 (Ycam), a fluorescent protein-based Ca²⁺ sensor fused to FAK or to a FAK-related non-kinase domain, to measure simultaneously local Ca²⁺ variations at FA sites and FA dynamics. Discrete subcellular Ca²⁺ oscillators initiate both propagating and abortive Ca²⁺ waves in migrating U87 astrocytoma cells. Ca²⁺-dependent FA disassembly occurs when the Ca²⁺ wave reaches individual FAs, indicating that local but not global Ca²⁺ increases trigger FA disassembly. An unexpectedly rapid flux of FAK between cytosolic and FA compartments was revealed by fluorescence recovery after photobleaching studies. The FAK-Ycam recovery half-time (17 s) at FAs was slowed (to 29 s) by Ca²⁺ elevation. FAK-related non-kinase domain-Ycam had a faster, Ca²⁺-insensitive recovery half-time (11 s), which is consistent with the effect of Ca²⁺ on FAK-Ycam dynamics not being due to a general modification of the dynamics of FA components. Because FAK association at FAs was prolonged by Ca²⁺ and FAK autophosphorylation was correlated to intracellular Ca²⁺ levels, we propose that local Ca²⁺ elevations increase the residency of FAK at FAs, possibly by means of tyrosine phosphorylation of FAK, thereby leading to increased activation of its effectors involved in FA disassembly.

Received for publication, April 12, 2004

^* 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 Association pour la Recherche Contre le Cancer, and the Association Régionale pour l'Enseignement et la Recherche Scientifique et Technologique. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains one figure.

Recipient of fellowships from the Ministère de la Recherche and the European Advanced Light Microscopy Facility. 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 60024, 67401 Illkirch, France. Tel.: 33-3-9024-4111; Fax: 33-3-9024-4313; E-mail: kt{at}pharma.u-strasbg.fr.

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