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Vol. 15, Issue 10, 4695-4709, October 2004

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NrCAM Coupling to the Cytoskeleton Depends on Multiple Protein Domains and Partitioning into Lipid Rafts

Julien Falk ^*, Olivier Thoumine , Caroline Dequidt , Daniel Choquet , and Catherine Faivre-Sarrailh  

^* Neurogenèse et Morphogenèse du Développement à l'Adulte, UMR 6156 CNRS, Institut de Biologie du Développement de Marseille, Marseille, France; Physiologie Cellulaire de la Synapse, UMR 5091 CNRS, Institut François Magendie, Université Bordeaux 2, France; and Neurobiologie des Interactions Cellulaires et Neurophysiopathologie, UMR 6184 CNRS, Institut Jean-Roche, Marseille, France

Submitted March 2, 2004; Revised July 5, 2004; Accepted July 6, 2004
Monitoring Editor: Richard Hynes

NrCAM is a cell adhesion molecule of the L1 family that is implicated in the control of axonal growth. Adhesive contacts may promote advance of the growth cone by triggering the coupling of membrane receptors with the F-actin retrograde flow. We sought to understand the mechanisms leading to clutching the F-actin at the site of ligand-mediated clustering of NrCAM. Using optical tweezers and single particle tracking of beads coated with the ligand TAG-1, we analyzed the mobility of NrCAM-deletion mutants transfected in a neuroblastoma cell line. Deletion of the cytoplasmic tail did not prevent the coupling of NrCAM to the actin flow. An additional deletion of the FNIII domains to remove cis-interactions, was necessary to abolish the rearward movement of TAG-1 beads, which instead switched to a stationary behavior. Next, we showed that the actin-dependent retrograde movement of NrCAM required partitioning into lipid rafts as indicated by cholesterol depletion experiments using methyl--cyclodextrin. Recruitment of the raft component caveolin-1 was induced at the adhesive contact between the cell surface and TAG-1 beads, indicating that enlarged rafts were generated. Photobleaching experiments showed that the lateral mobility of NrCAM increased with raft dispersion in these contact areas, further suggesting that TAG-1–coated beads induced the coalescence of lipid rafts. In conclusion, we propose that anchoring of NrCAM with the retrograde actin flow can be triggered by adhesive contacts via cooperative processes including interactions with the cytoplasmic tail, formation of cis-complex via the FNIII repeats, and lipid raft aggregation.

Corresponding author. E-mail address: sarrailh.c{at}jean-roche.univ-mrs.fr.

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