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6 - The role of bacterial adhesion to epithelial cells in pathogenesis

from Part II - Bacterial cell biology and pathogenesis

Published online by Cambridge University Press:  12 August 2009

By
Christof R. Hauck
Edited by
Beth A. McCormick
Christof R. Hauck
Affiliation:
Department of Cell Biology, University of Konstanz, Konstanz, Germany
Beth A. McCormick
Affiliation:
Harvard University, Massachusetts
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Summary

INTRODUCTION

Colonizing host epithelia represents a formidable challenge to bacterial pathogens. To a large extent, epithelial surfaces are designed to shield the multicellular organism from the environment and to protect the body interior from potentially harmful microbes. Where epithelial surfaces permit exchange of molecular components with the external world, a multitude of innate and acquired host defence mechanisms keep microorganisms in check. In addition, invading pathogens either have to compete successfully with resident commensal bacteria for space and nutrients or have to reach and establish themselves in otherwise sterile parts of the body. As we will discuss in this chapter, the specific interaction with host surface components and the tight adhesion to epithelial cells form one of the common ways in which bacterial pathogens have evolved to successfully accomplish the colonization of their respective host organism. It is important to emphasize that in many cases, this initial host–microbe encounter at the epithelial barrier is not only a critical determinant of pathogen–host specificity and range but also, to a large extent, a decisive point for the infection process as a whole.

Adhesion of pathogenic bacteria to host cells had been observed at the beginning of the twentieth century in the early days of investigations into the microbiological origin of infectious diseases (Guyot, 1908). However, the concept that bacterial adhesion to host surfaces often represents an essential step in the development of infection matured only several decades later (Beachey, 1981; Duguid, 1959; Eden et al., 1976; McNeish et al. 1975; Punsalang and Sawyer, 1973).

Type
Chapter
Information
Bacterial-Epithelial Cell Cross-Talk
Molecular Mechanisms in Pathogenesis
 , pp. 158 - 183
Publisher: Cambridge University Press
Print publication year: 2006

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References

Agerer, F., Michel, A., Ohlsen, K., and Hauck, C. R. (2003). Integrin-mediated invasion of Staphylococcus aureus into human cells requires Src family protein tyrosine kinases. J. Biol. Chem. 278, 42 524–42 531.CrossRefGoogle ScholarPubMed
Agerer, F., Lux, S., Michel, A., et al. (2005). Cellular invasion by Staphylococcus aureus reveals a functional link between focal adhesion kinase and cortactin in integrin-mediated internalisation. J. Cell Sci. 118, 2189–2200.CrossRefGoogle ScholarPubMed
Apicella, M. A., Ketterer, M., Lee, F. K. N., et al. (1996). The pathogenesis of gonococcal urethritis in men: confocal and immunoelectron microscopic analysis of urethral exsudates from men infected with Neisseria gonorrhoeae. J. Infect. Dis. 173, 636–646.CrossRefGoogle Scholar
Ayala, B. P., Vasquez, B., Clary, S., et al. (2001). The pilus-induced Ca2+ flux triggers lysosome exocytosis and increases the amount of Lamp1 accessible to Neisseria IgA1 protease. Cell. Microbiol. 3, 265–275.CrossRefGoogle ScholarPubMed
Beachey, E. H. (1981). Bacterial adherence: adhesin–receptor interactions mediating the attachment of bacteria to mucosal surface. J. Infect. Dis. 143, 325–345.CrossRefGoogle ScholarPubMed
Benchimol, S., Fuks, A., Jothy, S., et al. (1989). Carcinoembryonic antigen, a human tumor marker, functions as an intercellular adhesion molecule. Cell 57, 327–334.CrossRefGoogle ScholarPubMed
Bhat, K. S., Gibbs, C. P., Barrera, O., et al. (1991). The opacity proteins of Neisseria gonorrhoeae strain MS11 are encoded by a family of 11 complete genes. Mol. Microbiol. 5, 1889–1901. [Published erratum appears in Mol. Microbiol. 1992, 6, 1073–1076.]CrossRefGoogle ScholarPubMed
Billker, O., Popp, A., Gray-Owen, S. D., and Meyer, T. F. (2000). The structural basis of CEACAM-receptor targeting by neisserial Opa proteins. Trends Microbiol. 8, 258–260.CrossRefGoogle ScholarPubMed
Billker, O., Popp, A., Brinkmann, V., et al. (2002). Distinct mechanisms of internalization of Neisseria gonorrhoeae by members of the CEACAM receptor family involving Rac1- and Cdc42- dependent and -independent pathways. EMBO J. 21, 560–571.CrossRefGoogle ScholarPubMed
Blau, D. M., Turbide, C., Tremblay, M., et al. (2001). Targeted disruption of the Ceacam1 (MHVR) gene leads to reduced susceptibility of mice to mouse hepatitis virus infection. J. Virol. 75, 8173–8186.CrossRefGoogle ScholarPubMed
Bos, M. P., Kao, D., Hogan, D. M., Grant, C. C., and 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.CrossRefGoogle ScholarPubMed
Bouckaert, J., Berglund, J., Schembri, M., et al. (2005). Receptor binding studies disclose a novel class of high-affinity inhibitors of the Escherichia coli FimH adhesin. Mol. Microbiol. 55, 441–455.CrossRefGoogle ScholarPubMed
Brouillette, E., Grondin, G., Shkreta, L., Lacasse, P., and Talbot, B. G. (2003). In vivo and in vitro demonstration that Staphylococcus aureus is an intracellular pathogen in the presence or absence of fibronectin-binding proteins. Microb. Pathog. 35, 159–168.CrossRefGoogle ScholarPubMed
Brummer, J., Ebrahimnejad, A., Flayeh, R., et al. (2001). cis Interaction of the cell adhesion molecule CEACAM1 with integrin beta(3). Am. J. Pathol. 159, 537–546.CrossRefGoogle Scholar
Chen, T., Belland, R. J., Wilson, J., and Swanson, J. (1995). Adherence of pilus- Opa+ gonococci to epithelial cells in vitro involves heparan sulfate. J. Exp. Med. 182, 511–517.CrossRefGoogle ScholarPubMed
Clark, M. A., Hirst, B. H., and Jepson, M. A. (1998). M-cell surface beta1 integrin expression and invasin-mediated targeting of Yersinia pseudotuberculosis to mouse Peyer's patch M cells. Infect. Immun. 66, 1237–1243.Google ScholarPubMed
Cohen, M. S. and Cannon, J. G. (1999). Human experimentation with Neisseria gonorrhoeae: progress and goals. J. Infect. Dis. 179 (Suppl 2), S375–379.CrossRefGoogle ScholarPubMed
Craig, L., Pique, M. E., and Tainer, J. A. (2004). Type IV pilus structure and bacterial pathogenicity. Nat. Rev. Microbiol. 2, 363–378.CrossRefGoogle ScholarPubMed
David, G. (1993). Integral membrane heparan sulfate proteoglycans. FASEB J. 7, 1023–1030.CrossRefGoogle ScholarPubMed
Deghmane, A. E., Giorgini, D., Larribe, M., Alonso, J. M., and Taha, M. K. (2002). Down-regulation of pili and capsule of Neisseria meningitidis upon contact with epithelial cells is mediated by CrgA regulatory protein. Mol. Microbiol. 43, 1555–1564.CrossRefGoogle ScholarPubMed
Dehio, M., Gomez-Duarte, O. G., Dehio, C., and Meyer, T. F. (1998). Vitronectin-dependent invasion of epithelial cells by Neisseria gonorrhoeae involves alpha(v) integrin receptors. FEBS Lett. 424, 84–88.CrossRefGoogle ScholarPubMed
Jonge, M. I., Bos, M. P., Hamstra, H. J., et al. (2002). Conformational analysis of opacity proteins from Neisseria meningitidis. Eur. J. Biochem. 269, 5215–5223.CrossRefGoogle ScholarPubMed
Dersch, P. and Isberg, R. R. (1999). A region of the Yersinia pseudotuberculosis invasin protein enhances integrin-mediated uptake into mammalian cells and promotes self-association. EMBO J. 18, 1199–1213.CrossRefGoogle ScholarPubMed
Duguid, J. P. (1959). Fimbriae and adhesive properties in Klebsiella strains. J. Gen. Microbiol. 21, 271–286.CrossRefGoogle ScholarPubMed
Dveksler, G. S., Dieffenbach, C. W., Cardellichio, C. B., et al. (1993). Several members of the mouse carcinoembryonic antigen-related glycoprotein family are functional receptors for the coronavirus mouse hepatitis virus-A59. J. Virol. 67, 1–8.Google ScholarPubMed
Eden, C. S., Hanson, L. A., Jodal, U., Lindberg, U., and Akerlund, A. S. (1976). Variable adherence to normal human urinary-tract epithelial cells of Escherichia coli strains associated with various forms of urinary-tract infection. Lancet 1, 490–492.Google ScholarPubMed
Edwards, N. J., Monteiro, M. A., Faller, G., et al. (2000). Lewis X structures in the O antigen side-chain promote adhesion of Helicobacter pylori to the gastric epithelium. Mol. Microbiol. 35, 1530–1539.CrossRefGoogle ScholarPubMed
Evans, B. A. (1977). Ultrastructural study of cervical gonorrhea. J. Infect. Dis. 136, 248–255.CrossRefGoogle ScholarPubMed
Foster, T. J. and Hook, M. (1998). Surface protein adhesins of Staphylococcus aureus. Trends Microbiol. 6, 484–488.CrossRefGoogle ScholarPubMed
Freissler, E., Meyer auf der Heyde, A., David, G., Meyer, T. F., and Dehio, C. (2000). Syndecan-1 and syndecan-4 can mediate the invasion of Opa HSPG-expressing Neisseria gonorrhoeae into epithelial cells. Cell. Microbiol. 2, 69–82.CrossRefGoogle Scholar
Gomez-Duarte, O. G., Dehio, M., Guzman, C. A., et al. (1997). Binding of vitronectin to Opa-expressing Neisseria gonorrhoeae mediates invasion of HeLa cells. Infect. Immun. 65, 3857–3866.Google ScholarPubMed
Guyot, G. (1908). Über die bakterielle Adhäsion. Zentralbl. Bakteriol. 46, 640–653.Google Scholar
Hammarstrom, S. (1999). The carcinoembryonic antigen (CEA) family: structures, suggested functions and expression in normal and malignant tissues. Semin. Cancer Biol. 9, 67–81.CrossRefGoogle ScholarPubMed
Helaine, S., Carbonnelle, E., Prouvensier, L., et al. (2005). PilX, a pilus-associated protein essential for bacterial aggregation, is a key to pilus-facilitated attachment of Neisseria meningitidis to human cells. Mol. Microbiol. 55, 65–77.CrossRefGoogle ScholarPubMed
Hill, D. J. and Virji, M. (2003). A novel cell-binding mechanism of Moraxella catarrhalis ubiquitous surface protein UspA: specific targeting of the N-domain of carcinoembryonic antigen-related cell adhesion molecules by UspA1. Mol. Microbiol. 48, 117–129.CrossRefGoogle ScholarPubMed
Hill, D. J., Toleman, M. A., Evans, D. J., et al. (2001). The variable P5 proteins of typeable and non-typeable Haemophilus influenzae target human CEACAM1. Mol. Microbiol. 39, 850–862.CrossRefGoogle ScholarPubMed
Hobbs, M. M., Seiler, A., Achtmann, M., and Cannon, J. G. (1994). Microevolution within a clonal population of pathogenic bacteria: recombination, gene duplication and horizontal genetic exchange in the opa gene family of Neisseria meningitidis. Mol. Microbiol. 12, 171–180.CrossRefGoogle ScholarPubMed
Hoffmann, I., Eugene, E., Nassif, X., Couraud, P. O., and Bourdoulous, S. (2001). Activation of ErbB2 receptor tyrosine kinase supports invasion of endothelial cells by Neisseria meningitidis. J. Cell Biol. 155, 133–143.CrossRefGoogle ScholarPubMed
Ilic, D., Kovacic, B., Johkura, K., et al. (2004). FAK promotes organization of fibronectin matrix and fibrillar adhesions. J. Cell Sci. 117, 177–187.CrossRefGoogle ScholarPubMed
Isberg, R. R. and Leong, J. M. (1990). Multiple b1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 60, 861–871.CrossRefGoogle Scholar
Isberg, R. R., Hamburger, Z., and Dersch, P. (2000). Signaling and invasin-promoted uptake via integrin receptors. Microbes Infect. 2, 793–801.CrossRefGoogle ScholarPubMed
Jerse, A. E., Cohen, M. S., Drown, P. M., et al. (1994). Multiple gonococcal opacity proteins are expressed during experimental urethral infection in the male. J. Exp. Med. 179, 911–920.CrossRefGoogle ScholarPubMed
Johansson, L., Rytkonen, A., Bergman, P., et al. (2003). CD46 in meningococcal disease. Science 301, 373–375.CrossRefGoogle ScholarPubMed
Jonson, A. B., Normark, S., and Rhen, M. (2005). Fimbriae, pili, flagella and bacterial virulence. Contrib. Microbiol. 12, 67–89.CrossRefGoogle ScholarPubMed
Kallstrom, H., Liszewski, M. K., Atkinson, J. P., and Jonsson, A. B. (1997). Membrane cofactor protein (MCP or CD46) is a cellular pilus receptor for pathogenic Neisseria. Mol. Microbiol. 25, 639–647.CrossRefGoogle ScholarPubMed
Kallstrom, H., Islam, M. S., Berggren, P.-O., and Jonsson, A.-B. (1998). Cell signaling by the type IV pili of pathogenic Neisseria. J. Biol. Chem. 273, 21 777–21 782.CrossRefGoogle ScholarPubMed
Kau, A. L., Hunstad, D. A., and Hultgren, S. J. (2005). Interaction of uropathogenic Escherichia coli with host uroepithelium. Curr. Opin. Microbiol. 8, 54–59.CrossRefGoogle ScholarPubMed
Kellogg, D. S., Peacock, W. L., Deacon, W. E., Brown, L., and Pirkle, C. I. (1963). Neisseria gonorrhoeae: I. Virulence linked to clonal variation. J. Bacteriol. 85, 1274–1279.Google ScholarPubMed
Kirchner, M. and Meyer, T. F. (2005). The PilC adhesin of the Neisseria type IV pilus: binding specificities and new insights into the nature of the host cell receptor. Mol. Microbiol. 56, 945–957.CrossRefGoogle ScholarPubMed
Kirchner, M., Heuer, D., and 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.CrossRefGoogle ScholarPubMed
Kuijpers, T. W., Hoogerwerf, M., Laan, L. J., et al. (1992). CD66 nonspecific cross-reacting antigens are involved in neutrophil adherence to cytokine-activated endothelial cells. J. Cell Biol. 118, 457–466.CrossRefGoogle ScholarPubMed
Kupsch, E. M., Knepper, B., Kuroki, T., Heuer, I., and Meyer, T. F. (1993). Variable opacity (Opa) outer membrane proteins account for the cell tropisms displayed by Neisseria gonorrhoeae for human leukocytes and epithelial cells. EMBO J. 12, 641–650.Google ScholarPubMed
Kuypers, J. M. and Proctor, R. A. (1989). Reduced adherence to traumatized rat heart valves by a low-fibronectin-binding mutant of Staphylococcus aureus. Infect. Immun. 57, 2306–2312.Google ScholarPubMed
Lecuit, M., Dramsi, S., Gottardi, C., et al. (1999). A single amino acid in E-cadherin responsible for host specificity towards the human pathogen Listeria monocytogenes. EMBO J. 18, 3956–3963.CrossRefGoogle ScholarPubMed
Lecuit, M., Vandormael-Pournin, S., Lefort, J., et al. (2001). A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. Science 292, 1722–1725.CrossRefGoogle ScholarPubMed
Lee, S. W., Bonnah, R. A., Higashi, D. L., et al. (2002). CD46 is phosphorylated at tyrosine 354 upon infection of epithelial cells by Neisseria gonorrhoeae. J. Cell Biol. 156, 951–957.CrossRefGoogle ScholarPubMed
Maier, B., Potter, L., So, M., et al. (2002). Single pilus motor forces exceed 100 pN. Proc. Natl. Acad. Sci. U. S. A. 99, 16 012–16 017.CrossRefGoogle ScholarPubMed
Malorny, B., Morelli, G., Kusecek, B., Kolberg, J., and Achtman, M. (1998). Sequence diversity, predicted two-dimensional protein structure, and epitope mapping of neisserial Opa proteins. J. Bacteriol. 180, 1323–1330.Google ScholarPubMed
Marra, A. and Isberg, R. R. (1997). Invasin-dependent and invasin-independent pathways for translocation of Yersinia pseudotuberculosis across the Peyer's patch intestinal epithelium. Infect. Immun. 65, 3412–3421.Google ScholarPubMed
McCaw, S. E., Liao, E. H., and 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.CrossRefGoogle ScholarPubMed
McCormick, B. A. (2003). The use of transepithelial models to examine host–pathogen interactions. Curr. Opin. Microbiol. 6, 77–81.CrossRefGoogle ScholarPubMed
McNeish, A. S., Turner, P., Fleming, J., and Evans, N. (1975). Mucosal adherence of human enteropathogenic Escherichia coli. Lancet 2, 946–948.CrossRefGoogle ScholarPubMed
McNiven, M. A., Kim, L., Krueger, E. W., et al. (2000). Regulated interactions between dynamin and the actin-binding protein cortactin modulate cell shape. J. Cell Biol. 151, 187–198.CrossRefGoogle ScholarPubMed
Melly, M. A., Gregg, C. R., and McGee, Z. A. (1981). Studies of toxicity of Neisseria gonorrhoeae for human fallopian tube mucosa. J. Infect. Dis. 143, 423–431.CrossRefGoogle ScholarPubMed
Mengaud, J., Ohayon, H., Gounon, P., Mege, R. M., and Cossart, P. (1996). E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 84, 923–932.CrossRefGoogle ScholarPubMed
Menzies, B. E. (2003). The role of fibronectin binding proteins in the pathogenesis of Staphylococcus aureus infections. Curr. Opin. Infect. Dis. 16, 225–229.CrossRefGoogle ScholarPubMed
Menzies, B. E., Kourteva, Y., Kaiser, A. B., and Kernodle, D. S. (2002). Inhibition of staphylococcal wound infection and potentiation of antibiotic prophylaxis by a recombinant fragment of the fibronectin-binding protein of Staphylococcus aureus. J. Infect. Dis. 185, 937–943.CrossRefGoogle ScholarPubMed
Merz, A. J., So, M., and Sheetz, M. P. (2000). Pilus retraction powers bacterial twitching motility. Nature 407, 98–102.Google ScholarPubMed
Meyer, T. F., Gibbs, C. P., and Haas, R. (1990). Variation and control of protein expression in Neisseria. Annu. Rev. Microbiol. 44, 451–477.CrossRefGoogle ScholarPubMed
Morand, P. C., Tattevin, P., Eugene, E., Beretti, J.-L., and Nassif, X. (2001). The adhesive property of the type IV pilus-associated component PilC1 of pathogenic Neisseria is supported by the conformational structure of the N-terminal part of the molecule. Mol. Microbiol. 40, 846–856.CrossRefGoogle ScholarPubMed
Morand, P. C., Bille, E., Morelle, S., et al. (2004). Type IV pilus retraction in pathogenic Neisseria is regulated by the PilC proteins. EMBO J. 23, 2009–2017.CrossRefGoogle ScholarPubMed
Mosleh, I. M., Boxberger, H. J., Sessler, M. J., and Meyer, T. F. (1997). Experimental infection of native human ureteral tissue with Neisseria gonorrhoeae: adhesion, invasion, intracellular fate, exocytosis, and passage through a stratified epithelium. Infect. Immun. 65, 3391–3398.Google ScholarPubMed
Muenzner, P., Naumann, M., Meyer, T. F., and 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, 24 331–24 340.CrossRefGoogle Scholar
Muenzner, P., Billker, O., Meyer, T. F., and Naumann, M. (2002). Nuclear factor-kB directs CEACAM1 receptor expression in Neisseria gonorrhoeae-infected epithelial cells. J. Biol. Chem. 277, 7438–7446.CrossRefGoogle Scholar
Muenzner, P., Rohde, M., Kneitz, S., and Hauck, C. R. (2005). CEACAM engagement by human pathogens enhances cell adhesion and counteracts bacteria-induced detachment of epithelial cells. J. Cell Biol. 170, 825–836.CrossRefGoogle ScholarPubMed
Obrink, B. (1997). CEA adhesion molecules: multifunctional proteins with signal-regulatory properties. Curr. Opin. Cell Biol. 9, 616–626.CrossRefGoogle ScholarPubMed
Ofek, I., Beachey, E. H., Jefferson, W., and Campbell, G. L. (1975). Cell membrane-binding properties of group A streptococcal lipoteichoic acid. J. Exp. Med. 141, 990–1003.CrossRefGoogle Scholar
Oikawa, S., Inuzuka, C., Kuroki, M., et al. (1991). A specific heterotypic cell adhesion activity between members of carcinoembryonic antigen family, W272 and NCA, is mediated by N-domains. J. Biol. Chem. 266, 7995–8001.Google ScholarPubMed
Old, D. C. (1972). Inhibition of the interaction between fimbrial haemagglutinins and erythrocytes by d-mannose and other carbohydrates. J. Gen. Microbiol. 71, 149–157.CrossRefGoogle ScholarPubMed
Ozeri, V., Rosenshine, I., Mosher, D. F., Fassler, R., and Hanski, E. (1998). Roles of integrins and fibronectin in the entry of Streptococcus pyogenes into cells via protein F1. Mol. Microbiol. 30, 625–637.CrossRefGoogle ScholarPubMed
Paradis, S. E., Dubreuil, J. D., Gottschalk, M., Archambault, M., and Jacques, M. (1999). Inhibition of adherence of Actinobacillus pleuropneumoniae to porcine respiratory tract cells by monoclonal antibodies directed against LPS and partial characterization of the LPS receptors. Curr. Microbiol. 39, 313–320.CrossRefGoogle ScholarPubMed
Patti, J. M., Allen, B. L., McGavin, M. J., and Hook, M. (1994). MSCRAMM-mediated adherence of microorganisms to host tissues. Annu. Rev. Microbiol. 48, 585–617.CrossRefGoogle ScholarPubMed
Pizarro-Cerda, J., Sousa, S., and Cossart, P. (2004). Exploitation of host cell cytoskeleton and signalling during Listeria monocytogenes entry into mammalian cells. C. R. Biol. 327, 115–123.CrossRefGoogle ScholarPubMed
Popp, A., Dehio, C., Grunert, F., Meyer, T. F., and Gray-Owen, S. D. (1999). Molecular analysis of neisserial Opa protein interactions with the CEA family of receptors: identification of determinants contributing to the differential specificities of binding. Cell. Microbiol. 1, 169–181.CrossRefGoogle Scholar
Poy, M. N., Ruch, R. J., Fernstrom, M. A., Okabayashi, Y., and Najjar, S. M. (2002). Shc and CEACAM1 interact to regulate the mitogenic action of insulin. J. Biol. Chem. 277, 1076–1084.CrossRefGoogle ScholarPubMed
Poy, M. N., Yang, Y., Rezaei, K., et al. (2002). CEACAM1 regulates insulin clearance in liver. Nat. Genet. 19, 19.Google Scholar
Pujol, C., Eugene, E., Saint Martin, L., and Nassif, X. (1997). Interaction of Neisseria meningitidis with a polarized monolayer of epithelial cells. Infect. Immun. 65, 4836–4842.Google ScholarPubMed
Punsalang, A. P. Jr and Sawyer, W. D. (1973). Role of pili in the virulence of Neisseria gonorrhoeae. Infect. Immun. 8, 255–263.Google ScholarPubMed
Rudel, T., Scheuerpflug, I., and Meyer, T. F. (1995). Neisseria PilC protein identified as type-4 pilus-tip located adhesin. Nature 373, 357–359.CrossRefGoogle ScholarPubMed
Ryll, R. R., Rudel, T., Scheuerpflug, I., Barten, R., and Meyer, T. F. (1997). PilC of Neisseria meningitidis is involved in class II pilus formation and restores pilus assembly, natural transformation competence and adherence to epithelial cells in PilC-deficient gonococci. Mol. Microbiol. 23, 879–892.CrossRefGoogle ScholarPubMed
Sadekova, S., Lamarche-Vane, N., Li, X., and Beauchemin, N. (2000). The CEACAM1-L glycoprotein associates with the actin cytoskeleton and localizes to cell–cell contact through activation of Rho-like GTPases. Mol. Biol. Cell 11, 65–77.CrossRefGoogle ScholarPubMed
Sauer, F. G., Remaut, H., Hultgren, S. J., and Waksman, G. (2004). Fiber assembly by the chaperone-usher pathway. Biochim. Biophys. Acta 1694, 259–267.CrossRefGoogle ScholarPubMed
Scheuerpflug, I., Rudel, T., Ryll, R., Pandit, J., and Meyer, T. F. (1999). Roles of PilC and PilE proteins in pilus-mediated adherence of Neisseria gonorrhoeae and Neisseria meningitidis to human erythrocytes and endothelial and epithelial cells. Infect. Immun. 67, 834–843.Google ScholarPubMed
Schmitter, T., Agerer, F., Peterson, L., Muenzner, P., and Hauck, C. R. (2004). Granulocyte CEACAM3 is a phagocytic receptor of the innate immune system that mediates recognition and elimination of human-specific pathogens. J. Exp. Med. 199, 35–46.CrossRefGoogle ScholarPubMed
Schubert, W.-D., Urbanke, C., Ziehm, T., et al. (2002). Structure of internalin, a major invasion protein of Listeria monocytogenes, in complex with its human receptor E-cadherin. Cell 111, 825.CrossRefGoogle Scholar
Schumann, D., Chen, C. J., Kaplan, B., and Shively, J. E. (2001). Carcinoembryonic antigen cell adhesion molecule 1 directly associates with cytoskeleton proteins actin and tropomyosin. J. Biol. Chem. 276, 47 421–47 433.CrossRefGoogle ScholarPubMed
Schwarzbauer, J. E. and Sechler, J. L. (1999). Fibronectin fibrillogenesis: a paradigm for extracellular matrix assembly. Curr. Opin. Cell Biol. 11, 622–627.CrossRefGoogle ScholarPubMed
Schwarz-Linek, U., Werner, J. M., Pickford, A. R., et al. (2003). Pathogenic bacteria attach to human fibronectin through a tandem beta-zipper. Nature 423, 177–181.CrossRefGoogle ScholarPubMed
Selbach, M. and Backert, S. (2005). Cortactin: an Achilles' heel of the actin cytoskeleton targeted by pathogens. Trends Microbiol. 13, 181–189.CrossRefGoogle ScholarPubMed
Simonet, M., Riot, B., Fortineau, N., and Berche, P. (1996). Invasin production by Yersinia pestis is abolished by insertion of an IS200-like element within the inv gene. Infect. Immun. 64, 375–379.Google ScholarPubMed
Sinha, B., Francois, P. P., Nusse, O., et al. (1999). Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin alpha5beta1. Cell. Microbiol. 1, 101–117.CrossRefGoogle ScholarPubMed
Stern, A. and Meyer, T. F. (1987). Common mechanism controlling phase and antigenic variation in pathogenic neisseriae. Mol. Microbiol. 1, 5–12.CrossRefGoogle ScholarPubMed
Stern, A., Brown, M., Nickel, P., and Meyer, T. F. (1986). Opacity genes in Neisseria gonorrhoeae: control of phase and antigenic variation. Cell 47, 61–71.CrossRefGoogle ScholarPubMed
Swanson, J., Barrera, O., Sola, J., and Boslego, J. (1988). Expression of outer membrane protein II by gonococci in experimental gonorrhea. J. Exp. Med. 168, 2121–2129.CrossRefGoogle ScholarPubMed
Tan, K., Zelus, B. D., Meijers, R., et al. (2002). Crystal structure of murine sCEACAM1a[1,4]: a coronavirus receptor in the CEA family. EMBO J. 21, 2076–2086.CrossRefGoogle ScholarPubMed
Tobiason, D. M. and Seifert, H. S. (2001). Inverse relationship between pilus-mediated gonococcal adherence and surface expression of the pilus receptor, CD46. Microbiology 147, 2333–2340.CrossRefGoogle ScholarPubMed
Ton-That, H. and Schneewind, O. (2004). Assembly of pili in Gram-positive bacteria. Trends Microbiol. 12, 228–234.CrossRefGoogle ScholarPubMed
Vandeputte-Rutten, L., Bos, M. P., Tommassen, J., and Gros, P. (2003). Crystal structure of neisserial surface protein A (NspA), a conserved outer membrane protein with vaccine potential. J. Biol. Chem. 278, 24 825–24 830.CrossRefGoogle Scholar
Putten, J. P. and Paul, S. M. (1995). Binding of syndecan-like cell surface proteoglycan receptors is required for Neisseria gonorrhoeae entry into human mucosal cells. EMBO J. 14, 2144–2154.Google ScholarPubMed
Putten, J. P., Duensing, T. D., and Cole, R. L. (1998). Entry of OpaA+ gonococci into HEp-2 cells requires concerted action of glycosaminoglycans, fibronectin and integrin receptors. Mol. Microbiol. 29, 369–379.CrossRefGoogle ScholarPubMed
Virji, M., Evans, D., Hadfield, A., et al. (1999). Critical determinants of host receptor targeting by Neisseria meningitidis and Neisseria gonorrhoeae: identification of Opa adhesiotopes on the N-domain of CD66 molecules. Mol. Microbiol. 34, 538–551.CrossRefGoogle ScholarPubMed
Virji, M., Evans, D., Griffith, J., et al. (2000). Carcinoembryonic antigens are targeted by diverse strains of typable and non-typable Haemophilus influenzae. Mol. Microbiol. 36, 784–795.CrossRefGoogle ScholarPubMed
Volberg, T., Romer, L., Zamir, E., and Geiger, B. (2001). pp60(c-src) and related tyrosine kinases: a role in the assembly and reorganization of matrix adhesions. J. Cell Sci. 114, 2279–2289.Google ScholarPubMed
Wang, J., Gray-Owen, S. D., Knorre, A., Meyer, T. F., and Dehio, C. (1998). Opa binding to cellular CD66 receptors mediates the transcellular traversal of Neisseria gonorrhoeae across polarized T84 epithelial cell monolayers. Mol. Microbiol. 30, 657–671.CrossRefGoogle ScholarPubMed
Ward, M. E., Watt, P. J., and Robertson, J. N. (1974). The human fallopian tube: a laboratory model for gonococcal infection. J. Infect. Dis. 129, 650–659.CrossRefGoogle ScholarPubMed
Weidenmaier, C., Kokai-Kun, J. F., Kristian, S. A., et al. (2004). Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat. Med. 10, 243–245.CrossRefGoogle Scholar
Zaidel-Bar, R., Cohen, M., Addadi, L., and Geiger, B. (2004). Hierarchical assembly of cell-matrix adhesion complexes. Biochem. Soc. Trans. 32, 416–420.CrossRefGoogle ScholarPubMed
Zamir, E. and Geiger, B. (2001). Molecular complexity and dynamics of cell-matrix adhesions. J. Cell Sci. 114, 3583–3590.Google ScholarPubMed
Zamir, E., Katz, M., Posen, Y., et al. (2000). Dynamics and segregation of cell-matrix adhesions in cultured fibroblasts. Nat. Cell Biol. 2, 191–196.CrossRefGoogle ScholarPubMed

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