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J Biol Chem, Vol. 274, Issue 50, 35343-35350, December 10, 1999

Sphingosine 1-Phosphate Stimulates Cell Migration through a Gi-coupled Cell Surface Receptor
POTENTIAL INVOLVEMENT IN ANGIOGENESIS*

Fang WangDagger , James R. Van Brocklyn§, John P. Hobson, Sharareh Movafagh, Zofia Zukowska-Grojec, Sheldon Milstien||, and Sarah Spiegel**

From the Department of Biochemistry and Molecular Biology and Department of  Physiology and Biophysics, Georgetown University Medical Center, Washington, D.C. 20007 and the || Laboratory of Cellular and Molecular Regulation, NIMH, National Institutes of Health, Bethesda, Maryland 20892

Sphingosine 1-phosphate (SPP) has been shown to inhibit chemotaxis of a variety of cells, in some cases through intracellular actions, while in others through receptor-mediated effects. Surprisingly, we found that low concentrations of SPP (10-100 nM) increased chemotaxis of HEK293 cells overexpressing the G protein-coupled SPP receptor EDG-1. In agreement with previous findings in human breast cancer cells (Wang, F., Nohara, K., Olivera, O., Thompson, E. W., and Spiegel, S. (1999) Exp. Cell Res. 247, 17-28), SPP, at micromolar concentrations, inhibited chemotaxis of both vector- and EDG-1-overexpressing HEK293 cells. Nanomolar concentrations of SPP also induced a marked increase in chemotaxis of human umbilical vein endothelial cells (HUVEC) and bovine aortic endothelial cells (BAEC), which express the SPP receptors EDG-1 and EDG-3, while higher concentrations of SPP were less effective. Treatment with pertussis toxin, which ADP-ribosylates and inactivates Gi-coupled receptors, blocked SPP-induced chemotaxis. Checkerboard analysis indicated that SPP stimulates both chemotaxis and chemokinesis. Taken together, these data suggest that SPP stimulates cell migration by binding to EDG-1. Similar to SPP, sphinganine 1-phosphate (dihydro-SPP), which also binds to this family of SPP receptors, enhanced chemotaxis; whereas, another structurally related lysophospholipid, lysophosphatidic acid, did not compete with SPP for binding nor did it have significant effects on chemotaxis of endothelial cells. Furthermore, SPP increased proliferation of HUVEC and BAEC in a pertussis toxin-sensitive manner. SPP and dihydro-SPP also stimulated tube formation of BAEC grown on collagen gels (in vitro angiogenesis), and potentiated tube formation induced by basic fibroblast growth factor. Pertussis toxin treatment blocked SPP-, but not bFGF-stimulated in vitro angiogenesis. Our results suggest that SPP may play a role in angiogenesis through binding to endothelial cell Gi-coupled SPP receptors.

* This work was supported in part by National Institutes of Health Research Grant CA61774 (to S. S.).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Dagger Supported by Predoctoral Fellowship BC961968 from the United States Army Medical Research and Material Command, Breast Cancer Research Program.

§ Supported by Postdoctoral Fellowship F32 GM19209 from the National Institutes of Health.

** To whom correspondence should be addressed: Dept. of Biochemistry and Molecular Biology, Georgetown University Medical Center, 353 Basic Science Bldg., 3900 Reservoir Rd. NW, Washington, D.C. 20007. Tel.: 202-687-1432; Fax: 202-687-0260.

Copyright © 1999 by The American Society for Biochemistry and Molecular Biology, Inc.


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L. Balazs, J. Okolicany, M. Ferrebee, B. Tolley, and G. Tigyi
Topical application of the phospholipid growth factor lysophosphatidic acid promotes wound healing in vivo
Am J Physiol Regulatory Inte