Adherence of pilus- Opa+ gonococci to epithelial cells in vitro involves heparan sulfate

doi:10.1084/jem.182.2.511

This Article

	Full Text (PDF)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JEM
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Chen, T.
	Articles by Swanson, J.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Chen, T.
	Articles by Swanson, J.


Social Bookmarking

	What's this?

ARTICLES

Adherence of pilus- Opa+ gonococci to epithelial cells in vitro involves heparan sulfate

T Chen, RJ Belland, J Wilson and J Swanson
Laboratory of Microbial Structure and Function, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana 59840, USA.

Neisseria gonorrhoeae attaches to host epithelial cells via pili and opacity-associated (Opa) outer membrane proteins. Pilus- gonococci (Gc) of strain MS11 adhere to both human and nonhuman cells, but only when particular Opa proteins are expressed; OpaA+ variants adhere best, OpaC+ variants are next best, and the seven other Opa+ variants adhere poorly or not at all. The adherence of OpaA+ Gc to Chinese hamster ovary (CHO) cells is inhibited by heparin or heparan sulfate (HS), but not by chondroitin sulfate. OpaA+ Gc do not adhere to CHO cells devoid of HS proteoglycans; low concentrations of heparin restore OpaA+ Gc adherence to these HS-deficient CHO cells and high concentrations inhibit it. 3H-heparin binding to whole Gc parallels their adherence abilities (OpaA+ > OpaC+ > OpaH+ >> Opas B, D, E, F, G, I = Opa- = 0). Opa proteins separated by SDS-PAGE also bind 3H-heparin. These data suggest that adherence of pilus-, Opa+ Gc involves HS-proteoglycan of eukaryotic cells.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Add to Reddit Reddit Add to Technorati Technorati What's this?

This article has been cited by other articles:

Lee, H. S. W., Ostrowski, M. A., Gray-Owen, S. D. (2008). CEACAM1 Dynamics during Neisseria gonorrhoeae Suppression of CD4+ T Lymphocyte Activation. J. Immunol. 180: 6827-6835 [Abstract] [Full Text]
Zhang, P., Skurnik, M., Zhang, S.-S., Schwartz, O., Kalyanasundaram, R., Bulgheresi, S., He, J. J., Klena, J. D., Hinnebusch, B. J., Chen, T. (2008). Human Dendritic Cell-Specific Intercellular Adhesion Molecule-Grabbing Nonintegrin (CD209) Is a Receptor for Yersinia pestis That Promotes Phagocytosis by Dendritic Cells. Infect. Immun. 76: 2070-2079 [Abstract] [Full Text]
Lewis, L. A., Ram, S., Prasad, A., Gulati, S., Getzlaff, S., Blom, A. M., Vogel, U., Rice, P. A. (2008). Defining Targets for Complement Components C4b and C3b on the Pathogenic Neisseriae. Infect. Immun. 76: 339-350 [Abstract] [Full Text]
Schmitter, T., Pils, S., Weibel, S., Agerer, F., Peterson, L., Buntru, A., Kopp, K., Hauck, C. R. (2007). Opa Proteins of Pathogenic Neisseriae Initiate Src Kinase-Dependent or Lipid Raft-Mediated Uptake via Distinct Human Carcinoembryonic Antigen-Related Cell Adhesion Molecule Isoforms. Infect. Immun. 75: 4116-4126 [Abstract] [Full Text]
Patrone, J. B., Bish, S. E., Stein, D. C. (2006). TNF-{alpha}-Independent IL-8 Expression: Alterations in Bacterial Challenge Dose Cause Differential Human Monocytic Cytokine Response. J. Immunol. 177: 1314-1322 [Abstract] [Full Text]
Kuhlewein, C., Rechner, C., Meyer, T. F., Rudel, T. (2006). Low-Phosphate-Dependent Invasion Resembles a General Way for Neisseria gonorrhoeae To Enter Host Cells. Infect. Immun. 74: 4266-4273 [Abstract] [Full Text]
Simms, A. N., Jerse, A. E. (2006). In Vivo Selection for Neisseria gonorrhoeae Opacity Protein Expression in the Absence of Human Carcinoembryonic Antigen Cell Adhesion Molecules.. Infect. Immun. 74: 2965-2974 [Abstract] [Full Text]
Geraats-Peters, C. W. M., Brouwers, M., Schneeberger, P. M., van der Zanden, A. G. M., Bruisten, S. M., Weers-Pothoff, G., Boel, C. H. E., van den Brule, A. J. C., Harmsen, H. G., Hermans, M. H. A. (2005). Specific and Sensitive Detection of Neisseria gonorrhoeae in Clinical Specimens by Real-Time PCR. J. Clin. Microbiol. 43: 5653-5659 [Abstract] [Full Text]
Moore, J., Bailey, S. E. S., Benmechernene, Z., Tzitzilonis, C., Griffiths, N. J. E., Virji, M., Derrick, J. P. (2005). Recognition of Saccharides by the OpcA, OpaD, and OpaB Outer Membrane Proteins from Neisseria meningitidis. J. Biol. Chem. 280: 31489-31497 [Abstract] [Full Text]
Kirchner, M., Heuer, D., Meyer, T. F. (2005). CD46-Independent Binding of Neisserial Type IV Pili and the Major Pilus Adhesin, PilC, to Human Epithelial Cells. Infect. Immun. 73: 3072-3082 [Abstract] [Full Text]
McCaw, S. E., Liao, E. H., Gray-Owen, S. D. (2004). Engulfment of Neisseria gonorrhoeae: Revealing Distinct Processes of Bacterial Entry by Individual Carcinoembryonic Antigen-Related Cellular Adhesion Molecule Family Receptors. Infect. Immun. 72: 2742-2752 [Abstract] [Full Text]
Fischer, J. R., Parveen, N., Magoun, L., Leong, J. M. (2003). Decorin-binding proteins A and B confer distinct mammalian cell type-specific attachment by Borrelia burgdorferi, the Lyme disease spirochete. Proc. Natl. Acad. Sci. USA 100: 7307-7312 [Abstract] [Full Text]
Bos, M. P., Kao, D., Hogan, D. M., Grant, C. C. R., Belland, R. J. (2002). Carcinoembryonic Antigen Family Receptor Recognition by Gonococcal Opa Proteins Requires Distinct Combinations of Hypervariable Opa Protein Domains. Infect. Immun. 70: 1715-1723 [Abstract] [Full Text]
Fleckenstein, J. M., Holland, J. T., Hasty, D. L. (2002). Interaction of an Outer Membrane Protein of Enterotoxigenic Escherichia coli with Cell Surface Heparan Sulfate Proteoglycans. Infect. Immun. 70: 1530-1537 [Abstract] [Full Text]
Muenzner, P., Billker, O., Meyer, T. F., Naumann, M. (2002). Nuclear Factor-kappa B Directs Carcinoembryonic Antigen-related Cellular Adhesion Molecule 1 Receptor Expression in Neisseria gonorrhoeae-infected Epithelial Cells. J. Biol. Chem. 277: 7438-7446 [Abstract] [Full Text]
Rytkonen, A., Johansson, L., Asp, V., Albiger, B., Jonsson, A.-B. (2001). Soluble Pilin of Neisseria gonorrhoeae Interacts with Human Target Cells and Tissue. Infect. Immun. 69: 6419-6426 [Abstract] [Full Text]
Tobiason, D. M., Seifert, H. S. (2001). Inverse relationship between pilus-mediated gonococcal adherence and surface expression of the pilus receptor, CD46. Microbiology 147: 2333-2340 [Abstract] [Full Text]
Minor, S. Y., Banerjee, A., Gotschlich, E. C. (2000). Effect of alpha -Oligosaccharide Phenotype of Neisseria gonorrhoeae Strain MS11 on Invasion of Chang Conjunctival, HEC-1-B Endometrial, and ME-180 Cervical Cells. Infect. Immun. 68: 6526-6534 [Abstract] [Full Text]
McCormick, C. J., Newbold, C. I., Berendt, A. R. (2000). Sulfated glycoconjugates enhance CD36-dependent adhesion of Plasmodium falciparum-infected erythrocytes to human microvascular endothelial cells. Blood 96: 327-333 [Abstract] [Full Text]
Muenzner, P., Dehio, C., Fujiwara, T., Achtman, M., Meyer, T. F., Gray-Owen, S. D. (2000). Carcinoembryonic Antigen Family Receptor Specificity of Neisseria meningitidis Opa Variants Influences Adherence to and Invasion of Proinflammatory Cytokine-Activated Endothelial Cells. Infect. Immun. 68: 3601-3607 [Abstract] [Full Text]
Pethe, K., Aumercier, M., Fort, E., Gatot, C., Locht, C., Menozzi, F. D. (2000). Characterization of the Heparin-binding Site of the Mycobacterial Heparin-binding Hemagglutinin Adhesin. J. Biol. Chem. 275: 14273-14280 [Abstract] [Full Text]
Hopper, S., Wilbur, J. S., Vasquez, B. L., Larson, J., Clary, S., Mehr, I. J., Seifert, H. S., So, M. (2000). Isolation of Neisseria gonorrhoeae Mutants That Show Enhanced Trafficking across Polarized T84 Epithelial Monolayers. Infect. Immun. 68: 896-905 [Abstract] [Full Text]
Duensing, T. D., Wing, J. S., van Putten, J. P. M. (1999). Sulfated Polysaccharide-Directed Recruitment of Mammalian Host Proteins: a Novel Strategy in Microbial Pathogenesis. Infect. Immun. 67: 4463-4468 [Abstract] [Full Text]
Bos, M. P., Hogan, D., Belland, R. J. (1999). Homologue Scanning Mutagenesis Reveals CD66 Receptor Residues Required for Neisserial Opa Protein Binding. J. Exp. Med. 190: 331-340 [Abstract] [Full Text]
McLeod Griffiss, J., Lammel, C. J., Wang, J., Dekker, N. P., Brooks, G. F. (1999). Neisseria gonorrhoeae Coordinately Uses Pili and Opa To Activate HEC-1-B Cell Microvilli, Which Causes Engulfment of the Gonococci. Infect. Immun. 67: 3469-3480 [Abstract] [Full Text]
van Putten, J. P.M., Duensing, T. D., Carlson, J. (1998). Gonococcal Invasion of Epithelial Cells Driven by P.IA, a Bacterial Ion Channel with GTP Binding Properties. J. Exp. Med. 188: 941-952 [Abstract] [Full Text]
Kallstrom, H., Islam, Md. S., Berggren, P.-O., Jonsson, A.-B. (1998). Cell Signaling by the Type IV Pili of Pathogenic Neisseria. J. Biol. Chem. 273: 21777-21782 [Abstract] [Full Text]
Bos, M. P., Kuroki, M., Krop-Watorek, A., Hogan, D., Belland, R. J. (1998). CD66 receptor specificity exhibited by neisserial Opa variants is controlled by protein determinants in CD66 N-domains. Proc. Natl. Acad. Sci. USA 95: 9584-9589 [Abstract] [Full Text]
Su, H., Caldwell, H. D. (1998). Sulfated Polysaccharides and a Synthetic Sulfated Polymer Are Potent Inhibitors of Chlamydia trachomatis Infectivity In Vitro but Lack Protective Efficacy in an In Vivo Murine Model of Chlamydial Genital Tract Infection. Infect. Immun. 66: 1258-1260 [Abstract] [Full Text]
Malorny, B., Morelli, G., Kusecek, B., Kolberg, J., Achtman, M. (1998). Sequence Diversity, Predicted Two-Dimensional Protein Structure, and Epitope Mapping of Neisserial Opa Proteins. J. Bacteriol. 180: 1323-1330 [Abstract] [Full Text]
Chen, T., Grunert, F., Medina-Marino, A., Gotschlich, E. C. (1997). Several Carcinoembryonic Antigens (CD66) Serve as Receptors for Gonococcal Opacity Proteins. J. Exp. Med. 185: 1557-1564 [Abstract] [Full Text]
Chen, T., Gotschlich, E.�C. (1996). CGM1a antigen of neutrophils, a receptor of gonococcal opacity�proteins. Proc. Natl. Acad. Sci. USA 93: 14851-14856 [Abstract] [Full Text]
Muenzner, P., Naumann, M., Meyer, T. F., Gray-Owen, S. D. (2001). Pathogenic Neisseria Trigger Expression of Their Carcinoembryonic Antigen-related Cellular Adhesion Molecule 1 (CEACAM1; Previously CD66a) Receptor on Primary Endothelial Cells by Activating the Immediate Early Response Transcription Factor, Nuclear Factor-kappa B. J. Biol. Chem. 276: 24331-24340 [Abstract] [Full Text]