Neuropilin-1 Mediates Collapsin-1/Semaphorin III Inhibition of Endothelial Cell Motility: Functional Competition of Collapsin-1 and Vascular Endothelial Growth Factor-165

doi:10.1083/jcb.146.1.233

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© The Rockefeller University Press, 0021-9525/1999//233 $5.00
The Journal of Cell Biology, Volume 146, Number 1, , 1999 233-242

Original Article

Neuropilin-1 Mediates Collapsin-1/Semaphorin III Inhibition of Endothelial Cell Motility

: Functional Competition of Collapsin-1 and Vascular Endothelial Growth Factor-165

Hua-Quan Miao^a, Shay Soker^a^,c, Leonard Feiner^d, José Luis Alonso^a, Jonathan A. Raper^d, and Michael Klagsbrun^a^,b

^a Department of Surgical Research, Children's Hospital and Harvard Medical School, Boston, Massachusetts 02115
^b Department of Pathology, Children's Hospital and Harvard Medical School, Boston, Massachusetts 02115
^c Department of Urology, Children's Hospital and Harvard Medical School, Boston, Massachusetts 02115
^d Department of Neuroscience, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104
Department of Surgical Research, Children's Hospital, 300 Longwood Avenue, Boston, MA 02115.(617) 355-7291(617) 355-7503

klagsbrun{at}a1.tch.harvard.edu

Neuropilin-1 (NRP1) is a receptor for two unrelated ligandswith disparate activities, vascular endothelial growth factor-165(VEGF₁₆₅), an angiogenesis factor, and semaphorin/collapsins,mediators of neuronal guidance. To determine whether semaphorin/collapsinscould interact with NRP1 in nonneuronal cells, the effects ofrecombinant collapsin-1 on endothelial cells (EC) were examined.Collapsin-1 inhibited the motility of porcine aortic EC (PAEC)expressing NRP1 alone; coexpressing KDR and NRP1 (PAEC/KDR/NRP1),but not parental PAEC; or PAEC expressing KDR alone. The motilityof PAEC expressing NRP1 was inhibited by 65–75% and thisinhibition was abrogated by anti-NRP1 antibody. In contrast,VEGF₁₆₅ stimulated the motility of PAEC/KDR/NRP1. When VEGF₁₆₅and collapsin-1 were added simultaneously to PAEC/KDR/NRP1,dorsal root ganglia (DRG), and COS-7/NRP1 cells, they competedwith each other in EC motility, DRG collapse, and NRP1-bindingassays, respectively, suggesting that the two ligands have overlappingNRP1 binding sites. Collapsin-1 rapidly disrupted the formationof lamellipodia and induced depolymerization of F-actin in anNRP1-dependent manner. In an in vitro angiogenesis assay, collapsin-1inhibited the capillary sprouting of EC from rat aortic ringsegments. These results suggest that collapsin-1 can inhibitEC motility as well as axon motility, that these inhibitoryeffects on motility are mediated by NRP1, and that VEGF₁₆₅ andcollapsin-1 compete for NRP1-binding sites.

Key Words: angiogenesis • chemotaxis • KDR • neuronal guidance • growth cones

1.used in this paper: AP, alkaline phosphatase; DAPI, 4',6-diamidino-2-phenylindole;DIC, differential interference contrast; DRG, dorsal root ganglia;EC, endothelial cells; NRP1, neuropilin-1; PAEC, porcine aorticEC; RAEC, rat aortic EC; VEGF, vascular endothelial growth factor

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