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J. Biol. Chem., Vol. 278, Issue 39, 37987-37997, September 26, 2003

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Structurally Distinct Requirements for Binding of P-selectin Glycoprotein Ligand-1 and Sialyl Lewis x to Anaplasma phagocytophilum and P-selectin^*

Tadayuki Yago , Anne Leppänen , Jason A. Carlyon ¶, Mustafa Akkoyunlu ¶ ||, Sougata Karmakar , Erol Fikrig ¶, Richard D. Cummings  and Rodger P. McEver   **

From the Cardiovascular Biology Research Program, Oklahoma Medical Research Foundation and Department of Biochemistry and Molecular Biology and Oklahoma Center for Medical Glycobiology, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma 73104 and ^¶Section of Rheumatology, Department of Internal Medicine, Yale University School of Medicine, New Haven, Connecticut 06520

Colonization of neutrophils by the bacterium Anaplasma phagocytophilum causes the disease human granulocytic ehrlichiosis. The pathogen also infects mice, its natural host. Like binding of P-selectin, binding of A. phagocytophilum to human neutrophils requires expression of P-selectin glycoprotein ligand-1 (PSGL-1) and 1–3-fucosyltransferases that construct the glycan determinant sialyl Lewis x (sLe^x). Binding of A. phagocytophilum to murine neutrophils, however, requires expression of 1–3-fucosyltransferases but not PSGL-1. To further characterize the molecular features that A. phagocytophilum recognizes, we measured bacterial binding to microspheres bearing specific glycoconjugates or to cells expressing human PSGL-1 and particular glycosyltransferases. Like P-selectin, A. phagocytophilum bound to purified human PSGL-1 and to glycopeptides modeled after the N terminus of human PSGL-1 that presented sLe^x on an O-glycan. Unlike P-selectin, A. phagocytophilum bound to glycopeptides that contained sLe^x but lacked tyrosine sulfation or a specific core-2 orientation of sLe^x on the O-glycan. A. phagocytophilum bound only to glycopeptides that contained a short amino acid sequence found in the N-terminal region of human but not murine PSGL-1. Unlike P-selectin, A. phagocytophilum bound to cells expressing PSGL-1 in cooperation with sLe^x on both N-and O-glycans. Moreover, bacteria bound to microspheres coupled independently with glycopeptide lacking sLe^x and with sLe^x lacking peptide. These results demonstrate that, unlike P-selectin, A. phagocytophilum binds cooperatively to a nonsulfated N-terminal peptide in human PSGL-1 and to sLe^x expressed on PSGL-1 or other glycoproteins. Distinct bacterial adhesins may mediate these cooperative interactions.

Received for publication, June 2, 2003 , and in revised form, July 1, 2003.

^* This work was supported in part by National Institutes of Health Grants HL 65631 (to R. P. M.), AI 48075 (to R. D. C.), AI 041440 and AI 054630 (to E. F.), and AI 10554 (to J. A. C.) and by the Burroughs Welcome Fund (to E. F.). 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.

^|| Present address: Food and Drug Administration, Center for Biologics Evaluation and Research, Rockville, MD 20852.

^** To whom correspondence should be addressed: Cardiovascular Biology Research Program, Oklahoma Medical Research Foundation, 825 N. E. 13th St., Oklahoma City, OK 73104. Tel.: 405-271-6480; Fax: 405-271-3137; E-mail: rodger-mcever{at}omrf.ouhsc.edu.

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