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J. Biol. Chem., Vol. 280, Issue 29, 26965-26973, July 22, 2005

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Identification of L-selectin Binding Heparan Sulfates Attached to Collagen Type XVIII^*

Johanna W. A. M. Celie, Eelco D. Keuning, Robert H. J. Beelen, Angelika M. Dräger¶, Sonja Zweegman¶, Floortje L. Kessler¶, Raija Soininen||, and Jacob van den Born

From the Departments of Molecular Cell Biology and Immunology and ^¶Hematology, VU University Medical Center, 1007 MB, Amsterdam, the Netherlands and the ^||Medical Biochemistry and Molecular Biology, Biocenter Oulu, University of Oulu, FIN-90014, Oulu, Finland

L-selectin is a C-type lectin expressed on leukocytes that is involved in both lymphocyte homing to the lymph node and leukocyte extravasation during inflammation. Known L-selectin ligands include sulfated Lewis-type carbohydrates, glycolipids, and proteoglycans. Previously, we have shown that in situ detection of different types of L-selectin ligands is highly dependent on the tissue fixation protocol used. Here we use this knowledge to specifically examine the expression of L-selectin binding proteoglycans in normal mouse tissues. We show that L-selectin binding chondroitin/dermatan sulfate proteoglycans are present in cartilage, whereas L-selectin binding heparan sulfate proteoglycans are present in spleen and kidney. Furthermore, we show that L-selectin only binds a subset of renal heparan sulfates, attached to a collagen type XVIII protein backbone and predominantly present in medullary tubular and vascular basement membranes. As L-selectin does not bind other renal heparan sulfate proteoglycans such as perlecan, agrin, and syndecan-4, and not all collagen type XVIII expressed in the kidney binds L-selectin, this indicates that there is a specific L-selectin binding domain on heparan sulfate glycosaminoglycan chains. Using an in vitro L-selectin binding assay, we studied the contribution of N-sulfation, O-sulfation, C5-epimerization, unsubstituted glucosamine residues, and chain length in L-selectin binding to heparan sulfate/heparin glycosaminoglycan chains. Based on our results and the accepted model of heparan sulfate domain organization, we propose a model for the interaction of L-selectin with heparan sulfate glycosaminoglycan chains. Interestingly, this opens the possibility of active regulation of L-selectin binding to heparan sulfate proteoglycans, e.g. under inflammatory conditions.

Received for publication, February 25, 2005 , and in revised form, April 29, 2005.

^* The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

To whom correspondence should be addressed: Dept. Molecular Cell Biology and Immunology, VU University Medical Center, P. O. Box 7057, 1007 MB, Amsterdam, the Netherlands. Tel.: 31-204448083; Fax: 31-204448081; E-mail: p.celie{at}vumc.nl.

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