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MBC in Press, published online ahead of print October 5, 2005
Mol. Biol. Cell 10.1091/mbc.E05-05-0413

A more recent version of this article appeared on December 1, 2005
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Submitted on May 10, 2005
Revised on September 20, 2005
Accepted on September 23, 2005

Dynamic Partitioning into Lipid Rafts Controls the Endo-Exocytic Cycle of the {alpha}L/{beta}2 Integrin (LFA-1) during Leukocyte Chemotaxis

Monica Fabbri,*{dagger} Silvia Di Meglio,*{dagger} Maria Cristina Gagliani,{ddagger} Elisa Consonni,* Raffaella Molteni,* Jeffrey R. Bender,{sect} Carlo Tacchetti,{ddagger} and Ruggero Pardi*

*Unit of Leukocyte Biology, Vita-Salute San Raffaele University School of Medicine, DIBIT-Scientific Institute San Raffaele, 20132 Milano, Italy; {ddagger}MicroSCoBiO Research Center and IFOM Center of Cell Oncology and Ultrastructure, Department of Experimental Medicine, University of Genova, 16132 Genova, Italy; {sect}Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Sections of Cardiovascular Medicine and Immunobiology, Yale University School of Medicine, New Haven, CT 06536

Monitoring Editor: Martin A. Schwartz

Cell migration entails the dynamic redistribution of adhesion receptors from the cell rear toward the cell front, where they form new protrusions and adhesions. This process may involve regulated endo-exocytosis of integrins. Here we show that in primary neutrophils unengaged {alpha}L/{beta}2 integrin (LFA-1) is internalized and rapidly recycled upon chemoattractant stimulation via a clathrin-independent, cholesterol-sensitive pathway involving dynamic partitioning into detergent-resistant membranes (DRMs). Persistent DRM association is required for recycling of the internalized receptor, as: 1) over 90% of endocytosed LFA-1 is associated with DRMs and a large fraction of the internalized receptor colocalizes intracellularly with markers of DRMs and the recycling endocytic compartment; 2) a recycling-defective mutant ({alpha}L/{beta}2Y735A) dissociates rapidly from DRM upon being endocytosed and is subsequently diverted into a late endosomal pathway; 3) a dominant negative Rab11 mutant (Rab11S25N) induces intracellular accumulation of endocytosed {alpha}L/{beta}2 and prevents its enrichment in chemoattractant-induced lamellipodia. Notably, chemokine-induced migration of neutrophils over immobilized ICAM-1 is abrogated by cholesterol-sequestering agents. We propose that DRM-associated endocytosis allows efficient retrieval of integrins, as they detach from their ligands, followed by polarized recycling to areas of the plasma membrane, such as lamellipodia, where they establish new adhesive interactions and promote outside-in signaling events.

{dagger}These authors contributed equally to this work.

Address correspondence to: Monica Fabbri (fabbri.monica{at}hsr.it)




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