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First published online 29 June 2004
doi: 10.1242/jcs.01208

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Annexin 2 is a phosphatidylinositol (4,5)-bisphosphate binding protein recruited to actin assembly sites at cellular membranes

Ursula Rescher^*, Daniela Ruhe^*, Carsten Ludwig^*, Nicole Zobiack^* and Volker Gerke

Institute for Medical Biochemistry, Center for Molecular Biology of Inflammation, von Esmarch-Str. 56, Münster, 48149, Germany

Author for correspondence (e-mail: gerke{at}uni-muenster.de)

Accepted 9 March 2004

Annexin 2 is a Ca²⁺-regulated membrane protein and an F-actin-binding protein enriched at actin assembly sites both, on the plasma membrane and on endosomal vesicles. Here, we identify annexin 2 as a phosphatidylinositol (4,5)-bisphosphate (PtdIns(4,5)P₂)-interacting protein, thereby explaining this specific membrane association. Using the pleckstrin-homology (PH) domain of phospholipase C1 fused to yellow fluorescent protein as a marker for PtdIns(4,5)P₂, we show that annexin 2 and its ligand p11 (S100A10) are targeted to sites of PtdIns(4,5)P₂ enrichment where F-actin accumulates. At the plasma membrane, adhesion of pedestal-forming enteropathogenic Escherichia coli induces a recruitment of 1-phosphatidylinositol-4-phosphate 5-kinase (PtdIns4P 5-kinase) and an enrichment of PtdIns(4,5)P₂ and annexin 2-p11 at sites of bacterial adhesion. Induction of PtdIns(4,5)P₂-enriched ruffles and PtdIns(4,5)P₂-positive, actin-coated vacuoles by Arf6-mediated activation of PtdIns4P 5-kinase also leads to a concomitant accumulation of the annexin 2-p11 complex and the PH domain. Binding studies with immobilized phosphoinositides and phosphoinositide-containing liposomes reveal that the purified annexin 2-p11 complex directly and specifically binds to PtdIns(4,5)P₂ with an affinity comparable to that of the PH domain of phospholipase C1. Experiments using individual subunits identify annexin 2 as the PtdIns(4,5)P₂-binding entity. Thus, the direct interaction of annexin 2 with PtdIns(4,5)P₂ is a means of specifically recruiting the annexin 2-p11 complex to sites of membrane-associated actin assembly.

Key words: Annexin 2-p11 complex, Actin dynamics, PtdIns(4,5)P₂-binding, Arf6

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