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Infection and Immunity, September 2006, p. 5311-5318, Vol. 74, No. 9
0019-9567/06/$08.00+0     doi:10.1128/IAI.00614-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Roles of Cellular Activation and Sulfated Glycans in Haemophilus somnus Adherence to Bovine Brain Microvascular Endothelial Cells

E. Behling-Kelly,1 H. Vonderheid,1 Kwang Sik Kim,2 L. B. Corbeil,3 and C. J. Czuprynski1*

Department Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin—Madison, Madison, Wisconsin 53706,1 Department of Pediatrics, Johns Hopkins University, Baltimore, Maryland,2 Department of Pathology, University of California, San Diego, La Jolla, California3

Received 15 April 2006/ Returned for modification 15 May 2006/ Accepted 26 June 2006

Haemophilus somnus can cause a devastating fibrinopurulent meningitis with thrombotic vasculitis and encephalitis in cattle. The mechanisms used by H. somnus to migrate from the bloodstream into the central nervous system (CNS) are unknown. In this study, we demonstrate that H. somnus adheres to, but does not invade, bovine brain endothelial cells (BBEC) in vitro. The number of adherent H. somnus was significantly increased by prior activation of the BBEC with tumor necrosis factor alpha (TNF-{alpha}). Addition of exogenous glycosaminoglycans significantly reduced H. somnus adherence to resting and TNF-{alpha}-activated BBEC. Heparinase digestion of the endothelial cell's glycocalyx or sodium chlorate inhibition of endothelial cell sulfated glycan synthesis significantly reduced the number of adherent H. somnus. In contrast, addition of hyaluronic acid, a nonsulfated glycosaminoglycan, had no inhibitory effect. These findings suggest a critical role for both cellular activation and sulfated glycosaminoglycans in adherence of H. somnus to BBEC. Using heparin-labeled agarose beads, we demonstrated a high-molecular-weight heparin-binding protein expressed by H. somnus. Heparin was also shown to bind H. somnus in a 4°C binding assay. These data suggest that heparin-binding proteins on H. somnus could serve as initial adhesins to sulfated proteoglycans on the endothelial cell surface, thus contributing to the ability of H. somnus to infect the bovine CNS.

* Corresponding author. Mailing address: University of Wisconsin School of Veterinary Medicine, 2015 Linden Drive, Madison, WI 53706. Phone: (608) 262-8102. Fax: (608) 262-8102. E-mail: czuprync{at}svm.vetmed.wisc.edu.

Editor: J. T. Barbieri

Infection and Immunity, September 2006, p. 5311-5318, Vol. 74, No. 9
0019-9567/06/$08.00+0     doi:10.1128/IAI.00614-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



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