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Science 299 (5605): 405-408

Copyright © 2003 by the American Association for the Advancement of Science

Trophoblast L-Selectin-Mediated Adhesion at the Maternal-Fetal Interface

Olga D. Genbacev,1 Akraporn Prakobphol,1 Russell A. Foulk,4 Ana R. Krtolica,5 Dusko Ilic,1 Mark S. Singer,2 Zhi-Qiang Yang,6 Laura L. Kiessling,6 Steven D. Rosen,2 Susan J. Fisher123*

Trophoblast adhesion to the uterine wall is the requisite first step of implantation and, subsequently, placentation. At the maternal-fetal interface, we investigated the expression of selectin adhesion systems that enable leukocyte capture from the bloodstream. On the maternal side, human uterine epithelial cells up-regulated selectin oligosaccharide-based ligands during the window of receptivity. On the fetal side, human trophoblasts expressed L-selectin. This ligand-receptor system was functional, because beads coated with the selectin ligand 6-sulfo sLex bound to trophoblasts, and trophoblasts bound to ligand-expressing uterine luminal epithelium in tissue sections. These results suggest that trophoblast L-selectin mediates interactions with the uterus and that this adhesion mechanism may be critical to establishing human pregnancy.

Departments of 1 Stomatology, 2 Anatomy, and 3 Pharmaceutical Chemistry, University of California, San Francisco, CA 94143, USA. 4 Nevada Center for Reproductive Medicine, Reno, NV 89509, USA. 5 Life Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA. 6 Departments of Chemistry and Biochemistry, University of Wisconsin, Madison, WI 53706, USA.
*   To whom correspondence should be addressed. E-mail: sfisher{at}cgl.ucsf.edu



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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Full Text »    PDF »
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