Semaphorin3A Enhances Endocytosis at Sites of Receptor-F-actin Colocalization during Growth Cone Collapse

doi:10.1083/jcb.149.2.411

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© The Rockefeller University Press, 0021-9525/2000/4/411/ $5.00
The Journal of Cell Biology, Volume 149, Number 2, April 17, 2000 411-422

Original Article

Semaphorin3A Enhances Endocytosis at Sites of Receptor–F-actin Colocalization during Growth Cone Collapse

Alyson E. Fournier^a,b, Fumio Nakamura^a,b, Susumu Kawamoto^d, Yoshio Goshima^e, Robert G. Kalb^a,c, and Stephen M. Strittmatter^a,b
^a Department of Neurology, Yale University School of Medicine, New Haven, Connecticut 06520
^b Department of Neurobiology, Yale University School of Medicine, New Haven, Connecticut 06520
^c Department of Pharmacology, Yale University School of Medicine, New Haven, Connecticut 06520
^d Department of Bacteriology, Yokohama City University School of Medicine, Yokohama 236, Japan
^e Department of Pharmacology, Yokohama City University School of Medicine, Yokohama 236, Japan

Correspondence to: Stephen M. Strittmatter, Department of Neurology, Yale University School of Medicine, 333 Cedar Street, P.O. Box 208018, New Haven, CT 06520. Tel:(203) 785-4878 Fax:(203) 785-5098 E-mail:stephen.strittmatter{at}yale.edu.

Axonal growth cone collapse is accompanied by a reduction infilopodial F-actin. We demonstrate here that semaphorin 3A (Sema3A)induces a coordinated rearrangement of Sema3A receptors andF-actin during growth cone collapse. Differential interferencecontrast microscopy reveals that some sites of Sema3A-inducedF-actin reorganization correlate with discrete vacuoles, structuresinvolved in endocytosis. Endocytosis of FITC-dextran by thegrowth cone is enhanced during Sema3A treatment, and sites ofdextran accumulation colocalize with actin-rich vacuoles andridges of membrane. Furthermore, the Sema3A receptor proteins,neuropilin-1 and plexin, and the Sema3A signaling molecule,rac1, also reorganize to vacuoles and membrane ridges afterSema3A treatment. These data support a model whereby Sema3Astimulates endocytosis by focal and coordinated rearrangementof receptor and cytoskeletal elements. Dextran accumulationis also increased in retinal ganglion cell (RGC) growth cones,in response to ephrin A5, and in RGC and DRG growth cones, inresponse to myelin and phorbol-ester. Therefore, enhanced endocytosismay be a general principle of physiologic growth cone collapse.We suggest that growth cone collapse is mediated by both actinfilament rearrangements and alterations in membrane dynamics.

Key Words: membrane dynamics, ephrins, dextran uptake, axon guidance, axonrepulsion

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