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Vol. 14, Issue 10, 4207-4220, October 2003

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Cross Talk between Tetanus Neurotoxin-insensitive Vesicle-associated Membrane Protein-mediated Transport and L1-mediated Adhesion

Philipp Alberts ^*, Rachel Rudge ^*, Ina Hinners , Aude Muzerelle , Sonia Martinez-Arca ^*, Theano Irinopoulou ^*, Véronique Marthiens , Sharon Tooze , Fritz Rathjen ^||, Patricia Gaspar , and Thierry Galli ^* ¶

^* Membrane Traffic and Neuronal Plasticity, Institut National de la Santé et de la Recherche Médicale U536, F-75005 Paris, France; Secretory Pathways Laboratory, Cancer Research UK, London Research Institute, London WC2A 3PX, United Kingdom; Institut National de la Santé et de la Recherche Médicale U106, Hôpital Salpêtrière, F-75651, Paris, France; Institut National de la Santé et de la Recherche Médicale U440, F-75005 Paris, France; and ^|| Max-Delbrueck-Centrum fuer Molekulare Medizin, D-13092 Berlin, Germany

Submitted March 14, 2003; Revised June 2, 2003; Accepted June 4, 2003
Monitoring Editor: Jennifer Lippincott-Schwartz

The membrane-trafficking pathway mediated by tetanus neurotoxin-insensitive vesicle-associated membrane protein (TI-VAMP) in neurons is still unknown. We show herein that TI-VAMP expression is necessary for neurite outgrowth in PC12 cells and hippocampal neurons in culture. TI-VAMP interacts with plasma membrane and endosomal target soluble N-ethylmaleimide-sensitive factor attachment protein receptors, suggesting that TI-VAMP mediates a recycling pathway. L1, a cell-cell adhesion molecule involved in axonal outgrowth, colocalized with TI-VAMP in the developing brain, neurons in culture, and PC12 cells. Plasma membrane L1 was internalized into the TI-VAMP–containing compartment. Silencing of TI-VAMP resulted in reduced expression of L1 at the plasma membrane. Finally, using the extracellular domain of L1 and N-cadherin immobilized on beads, we found that the silencing of TI-VAMP led to impaired L1- but not N-cadherin–mediated adhesion. Furthermore, TI-VAMP- but not synaptobrevin 2-containing vesicles accumulated at the site of the L1 bead-cell junction. We conclude that TI-VAMP mediates the intracellular transport of L1 and that L1-mediated adhesion controls this membrane trafficking, thereby suggesting an important cross talk between membrane trafficking and cell-cell adhesion.

Abbreviations used: CAM, cell adhesion molecule; IgCAM, cell adhesion molecule of the immunoglobulin superfamily; Stx, syntaxin; siRNA, small interfering double-stranded RNA; TI-VAMP, tetanus neurotoxin-insensitive vesicle-associated membrane protein.

Online version of this article contains both videos and supplementary figure material for some figures. Online version is available at www.molbiolcell.org.

^¶ Corresponding author. E-mail address: galli{at}ifm.inserm.fr.

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