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Infection and Immunity, June 2000, p. 3601-3607, Vol. 68, No. 6
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Carcinoembryonic Antigen Family Receptor Specificity of Neisseria meningitidis Opa Variants Influences Adherence to and Invasion of Proinflammatory Cytokine-Activated Endothelial Cells

Petra Muenzner,1,2 Christoph Dehio,1 Taku Fujiwara,1 Mark Achtman,3 Thomas F. Meyer,1,2,* and Scott D. Gray-Owen1,dagger

Abteilung, Infektionsbiologie, Max-Planck-Institut für Biologie, 72076 Tübingen,1 Max-Planck-Institut für Molekulare Genetik, 14195 Berlin,3 and Max-Planck-Institut für Infektionsbiologie, 10117 Berlin,2 Germany

Received 20 October 1999/Returned for modification 31 January 2000/Accepted 16 February 2000

The carcinoembryonic antigen (CEA) family member CEACAM1 (previously called biliary glycoprotein or CD66a) was previously shown to function as a receptor that can mediate the binding of Opa protein-expressing Neisseria meningitidis to both neutrophils and epithelial cells. Since neutrophils and polarized epithelia have both been shown to coexpress multiple CEACAM receptors, we have now extended this work to characterize the binding specificity of meningococcal Opa proteins with other CEA family members. To do so, we used recombinant Escherichia coli expressing nine different Opa variants from three meningococcal strains and stably transfected cell lines expressing single members of the CEACAM family. These infection studies demonstrated that seven of the nine Opa variants bound to at least one CEACAM receptor and that binding to each of these receptors is sufficient to trigger the Opa-dependent bacterial uptake by these cell lines. The other two Opa variants do not appear to bind to either CEACAM receptors or heparan sulfate proteoglycan receptors, which are bound by some gonococcal Opa variants, thus implying a novel class of Opa proteins. We have also extended previous studies by demonstrating induction of CEACAM1 expression after stimulation of human umbilical vein endothelial cells with the proinflammatory cytokine tumor necrosis factor alpha, which is present in high concentrations during meningococcal disease. This induced expression of CEACAM1 leads to an increased Opa-dependent bacterial binding and invasion into the primary endothelia, implying that these interactions may play an important role in the pathogenesis of invasive meningococcal disease.

* Corresponding author. Mailing address: Max-Planck-Institut für Infektionsbiologie, Abteilung Molekulare Biologie, Monbijoustrasse 2, 10117 Berlin, Germany. Phone: 49 (0) 30 28 46 04 02. Fax: 49 (0) 30 28 46 04 01. E-mail: meyer{at}mpiib-berlin.mpg.de.

dagger Present address: Department of Medical Genetics and Microbiology, University of Toronto, M5S 1A8 Toronto, Canada.

Infection and Immunity, June 2000, p. 3601-3607, Vol. 68, No. 6
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


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