Chapter 8 : Bacterial Adherence and Tropism in the Human Respiratory Tract

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This chapter presents a comparative overview of several major adhesins and invasins of four human-tropic respiratory bacteria and includes examples of frequent to rare colonizers, namely, , , , and , and their extensively studied host tissue-targeting mechanisms. It considers one's current understanding of the bacterial adhesion factors that determine their tropism in the human respiratory tract, although it has to be noted that other factors important for bacterial survival also constitute determinants of host and tissue tropism. Several ligands of the organisms described in this chapter target extracellular matrix (ECM) proteins and directly or indirectly target the RGD-binding integrins. In addition, heparan sulfate proteoglycans (HSPGs) and members of Ig superfamily, especially the carcinoembryonic antigenrelated cell adhesion molecules (CEACAMs), are targeted by multiple mucosal bacteria and are specifically discussed. The adhesins that form layers above the bacterial outer membrane due to their extended morphology are categorized in this section and include polymeric as well as monomeric or small multimeric filamentous or protruding structures visible by electron microscopy (EM). Pili are generally regarded as the most important adhesins in capsulate phenotypes of and are thought to determine host and tissue tropism mediating primary interactions with human epithelial and endothelial cells. Pili thus allow the bacteria to make an initial contact with a host cell surface, leading to more intimate interactions via nonfilamentous adhesins. It is therefore also credible that the primary adhesins such as pili in general determine host and tissue tropism.

Citation: Virji M. 2005. Bacterial Adherence and Tropism in the Human Respiratory Tract, p 97-118. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch8

Key Concept Ranking

Bacterial Proteins
Lower Respiratory Tract Infections
Tumor Necrosis Factor alpha
Outer Membrane Protein C
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Image of Figure 1
Figure 1

Observations of the modes of interaction of and with human nasopharyngeal organ cultures ( ). Both bacteria attach to nonciliated cells; whereas enters cells, appears to transmigrate between cells. Both bacteria were found beneath epithelial cells. had a much greater tendency to bind to mucus than did Adapted from reference with permission from the publisher.

Citation: Virji M. 2005. Bacterial Adherence and Tropism in the Human Respiratory Tract, p 97-118. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch8
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Image of Figure 2
Figure 2

Pilus morphology, structure, and function in species. (A to D) Negative-stain transmission electron micrographs of a class II piliated isolate (A) and a class I piliated isolate (B), showing long filamentous pili forming rope-like bundles, which occur in both classes of pili. Pili were labeled with antibody against pilin conjugated to gold. In and pilin structural variants within a single strain may produce morphologically distinct pili. For example, in class I piliated strain C311, variant 3 (C) elaborates individual pili, whereas variant 16 (D) produces laterally aggregated bundles. Pilus aggregation in this case is not related to glycosylation status since removal of glycans does not affect aggregation ( ). (E) A three-dimensional molecular model of a pilin of strain C311 was based on that of MS11 pilin, which was determined by X-ray crystallography ( ). The model was built with the help of structural databases and minimized using the program X-plor. Positions a, b, and c mark the positions of sequence differences between the pilins of variants 3 and 16. In a fiber model of the variant 16 pilus (constructed using transformations suggested by Forest and Tainer [ ], pilin n of one helical turn and n+5of the next are so juxtapositioned as to bring loops a and b of pilin n very close to loop c of pilin n+5 (only pilins n and n+5 of a variant 16 pilus model are shown). Therefore, the three loops may present a single epitope on the surface of the fiber, which is repeated many times along its length. Single amino acid changes introduced into any one of the sites affect both the lateral aggregation and adherence properties of the pili (L. Serino, A. Hadfield, and M. Virji, unpublished studies). Asterisks show the positions of glycans. (F) Adherence of distinct piliated isolates to human cells and cells of animal origin: human umbilical vein endothelial cells (H), human conjunctiva epithelial cell line (C), human polymorphonuclear phagocytes and monocytes (P), bovine endothelial cells (B), and Madin-Darby canine kidney cells (M). In general, piliated organisms adhere specifically to human endothelial and epithelial cells with greater variation observed in binding of variant pili to human epithelial cell types ( ). C311 and MC58 are class I piliated strains; C114 and C319 are class II piliated strains.

Citation: Virji M. 2005. Bacterial Adherence and Tropism in the Human Respiratory Tract, p 97-118. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch8
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Image of Figure 3
Figure 3

Adherence of MX1 to CEACAMs. (A) Relative adherence of bacteria (determined by a viable-count assay) to Chinese hamster ovary cell transfectants expressing CEACAM1 (black columns) without or with anti-CEACAM-specific polyclonal (P) or monoclonal (M) blocking antibodies. The CHO column shows adherence to sham-transfected CHO cells. Blank columns show quantification of the binding of MX1 to A549 cells and inhibition in the presence of the antibodies, demonstrating that CEACAMs are the primary targets of the adhesins of this isolate on A549 cells. (B to D) Immunofluorescence analysis showing the tropism of MX1 for human epithelial cell lines. (B) A549; (C) HEp-2; (D) Chang. Adherent bacteria were labeled using rhodamine-conjugated antibacterial antibodies. Based on published information, the lack of adherence to Chang and HEp-2 cells suggests that MX1 does not express adhesins previously implicated in binding to these cell lines ( Table 2 ) ( ).

Citation: Virji M. 2005. Bacterial Adherence and Tropism in the Human Respiratory Tract, p 97-118. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch8
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Figure 4

(A) Van der Waals’ surface representation of the model (front views) of the N domain of CEACAM1, showing the critical common residues that are required for the interactions of and with the receptor. The amino acids exerting the greatest influence on binding of and are Ile 91 and Tyr 34. Ile 91 lies in close proximity to Tyr 34, which lies in the center of the illustrated face of the N-terminal domain, which is devoid of carbohydrate. The other amino acids shown, which appear to affect the binding of distinct strains and variants to variable extents, also lie in close proximity. The binding regions are overlapping, such that and may compete for binding to the receptor ( ). (B) Domain structure of several CEA family members of the Ig superfamily (adapted from the CEA website, http://cea.klinikum.uni-muenchen.de/). The family characteristically contains a single N-terminal 1gV-like domain, and in addition, most members contain several 1gC2-like domains (A1, B1, etc.). CEA (a) is anchored via a glycosylphosphatidylinositol extension, whereas CEACAM1 (b) and CEACAM3 (c) are transmembrane molecules. (C) Competition between and strains in targeting CEACAM1 receptors on CHO transfectants. Adhesion of (Hi) (blank columns) and (Nm) (black columns) after 3 h of incubation in the absence of (c) and when the strain was added at = 0 (a) or at 2 h (b) after inoculation with Within 1 h, inhibited the binding of that had been inoculated 2 h prior to addition (b). In each case, the number of bacteria adhering per cell is shown ( ).

Citation: Virji M. 2005. Bacterial Adherence and Tropism in the Human Respiratory Tract, p 97-118. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch8
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1. Aebi, C.,, E. R. Lafontaine,, L. D. Cope,, J. L. Latimer,, S. L. Lumbley,, G. H. McCracken, Jr., and E. J. Hansen. 1998. Phenotypic effect of isogenic uspA1 and uspA2 mutations on Moraxella catarrhalis O35E. Infect. Immun. 66:31133119.
2. Ahmed, K.,, K. Matsumoto,, N. Rikitomi,, and T. Nagatake. 1996. Attachment of Moraxella catarrhalis to pharyngeal epithelial cells is mediated by a glycosphingolipid receptor. FEMS Microbiol. Lett. 135:305309.
3. Ahmed, K.,, T. Nakagawa,, Y. Nakano,, G. Martinez,, A. Ichinose,, C. H. Zheng,, M. Akaki,, M. Aikawa,, and T. Nagatake. 2000. Attachment of Moraxella catarrhalis occurs to the positively charged domains of pharyngeal epithelial cells. Microb. Pathog. 28:203209.
4. Ahren, I. L.,, H. Janson,, A. Forsgren,, and K. Riesbeck. 2001. Protein D expression promotes the adherence and internalization of non-typeable Haemophilus influenzae into human monocytic cells. Microb. Pathog. 31:151158.
5. Anderson, P. W.,, M. E. Pichichero,, and E. M. Connor. 1985. Enhanced nasopharyngeal colonization of rats by piliated Haemophilus influenzae type b. Infect. Immun. 48:565568.
6. Barsum, W.,, R. Wilson,, R. C. Read,, A. Rutman,, H. C. Todd,, N. Houdret,, P. Roussel,, and P. J. Cole. 1995. Interaction of fimbriated and nonfimbriated strains of unencapsulated Haemophilus influenzae with Human respiratory-tract mucus in vitro. Eur. Respir. J. 8:709714.
7. Berggard, K.,, E. Johnsson,, F. R. Mooi,, and G. Lindahl. 1997. Bordetella pertussis binds the human complement regulator C4BP: role of filamentous hemagglutinin. Infect. Immun. 65:36383643.
8. Bernstein, J. M.,, and M. Reddy. 2000. Bacteria-mucin interaction in the upper aerodigestive tract shows striking heterogeneity: implications in otitis media, rhinosinusitis, and pneumonia. Otolaryngol. Head Neck Surg. 122:514520.
9. Blom, A. M.,, A. Rytkonen,, P. Vasquez,, G. Lindahl,, B. Dahlback,, and A. B. Jonsson. 2001. A novel interaction between type IV pili of Neisseria gonorrhoeae and the human complement regulator C4B-binding protein. J. Immunol. 166:67646770.
10. Bordessoule, D.,, M. Jones,, K. C. Gatter,, and D. Y. Mason. 1993. Immunohistological patterns of myeloid antigens: tissue distribution of CD13, CD14, CD16, CD31, CD36, CD65, CD66 and CD67. Br. J. Haematol. 83:370383.
11. Bos, M. P.,, F. Grunert,, and R. J. Belland. 1997. Differential recognition of members of the carcinoembryonic antigen family by Opa variants of Neisseria gonorrhoeae. Infect. Immun. 65:23532361.
12. Cartwright, K., 1995. Meningococcal carriage and disease, p. 115146. In K. Cartwright (ed.), Meningococcal Disease. John Wiley & Sons, Chichester, United Kingdom.
13. Chance, D. L.,, T. J. Reilly,, and A. L. Smith. 1999. Acid phosphatase activity as a measure of Haemophilus influenzae adherence to mucin. J. Microbiol. Methods 39:4958.
14. Chen, T.,, R. J. Belland,, J. Wilson,, and J. Swanson. 1995. Adherence of pilus− Opa+ gonococci to epithelial cells in vitro involves heparan sulfate. J. Exp. Med. 182:511517.
15. Chen, T.,, and E. C. Gotschlich. 1996. CGM1a antigen of neutrophils, a receptor of gonococcal opacity proteins. Proc. Natl. Acad. Sci. USA 93:1485114856.
16. Clemans, D. L.,, C. F. Marrs,, M. Patel,, M. Duncan,, and J. R. Gilsdorf. 1998. Comparative analysis of Haemophilus influenzae hifA (pilin) genes. Infect. Immun. 66:656663.
17. Coutte, L.,, S. Alonso,, N. Reveneau,, E. Willery,, B. Quatannens,, C. Locht,, and F. Jacob-Dubisson. 2003. Role of adhesin release for mucosal colonization by a bacterial pathogen. J. Exp. Med. 197:735742.
18. Cue, D.,, P. E. Dombek,, H. Lam,, and P. P. Cleary. 1998. Streptococcus pyogenes serotype M1 encodes multiple pathways for entry into human epithelial cells. Infect. Immun. 66:45934601.
19. Cywes, C.,, and M. R. Wessels. 2001. Group A Streptococcus tissue invasion by CD44-mediated cell signalling. Nature 414:648652.
20. Dansky-Ullmann, C.,, M. Salgaller,, S. Adams,, J. Schlom,, and J. W. Greiner. 1995. Synergistic effects of IL-6 and IFNgamma on carcinoembryonic antigen (CEA) and HLA expression by human colorectal carcinoma cells: role for endogenous IFN-beta. Cytokine 7:118129.
21. Dawid, S.,, S. J. Barenkamp,, and J. W. St. Geme. 3rd. 1999. Variation in expression of the Haemophilus influenzae HMW adhesins: a prokaryotic system reminiscent of eukaryotes. Proc. Natl. Acad. Sci. USA 96:10771082.
22. de Vries, F. P.,, R. Cole,, J. Dankert,, M. Frosch,, and J. P. van Putten. 1998. Neisseria meningitidis producing the Opc adhesin binds epithelial cell proteoglycan receptors. Mol. Microbiol. 27:12031212.
23. deVries, F. P.,, A. vanderEnde,, J. P. van Putten,, and J. Dankert. 1996. Invasion of primary nasopharyngeal epithelial cells by Neisseria meningitidis is controlled by phase variation of multiple surface antigens. Infect. Immun. 64:29983006.
24. Diaz, J.-L.,, M. Virji,, and J. E. Heckels. 1984. Structural and antigenic differences between two types of meningococcal pili. FEMS Microbiol. Lett. 21:181184.
25. Duensing, T. D.,, and J. P. M. van Putten. 1998. Vitronectin binds to the gonococcal adhesin OpaA through a glycosaminoglycan molecular bridge. Biochem. J. 334:133139.
26. Eberhard, T.,, G. Kronvall,, and M. Ullberg. 1999. Surface bound plasmin promotes migration of Streptococcus pneumoniae through reconstituted basement membranes. Microb. Pathog. 26:175181.
27. Edwards, J. L.,, E. J. Brown,, S. Uk-Nham,, J. G. Cannon,, M. S. Blake,, and M. A. Apicella. 2002. A co-operative interaction between Neisseria gonorrhoeae and complement receptor 3 mediates infection of primary cervical epithelial cells. Cell. Microbiol. 4:571584.
28. Fink, D. L.,, B. A. Green,, and J.W. St Geme III. 2002. The Haemophilus influenzae Hap autotransporter binds to fibronectin, laminin, and collagen IV. Infect. Immun. 70:49024907.
29. Forest, K. T.,, and J. A. Tainer. 1997. Type-4 pilus-structure: outside to inside and top to bottom—a minireview. Gene 192:165169.
30. Forsgren, A.,, M. Brant,, M. Karamehmedovic,, and K. Riesbeck. 2003. The immunoglobulin D-binding protein MID from Moraxella catarrhalis is also an adhesin. Infect. Immun. 71:33023309.
31. Geuijen, C. A. W.,, R. J. L. Willems,, P. Hoogerhout,, W. C. Puijk,, R. H. Meloen,, and F. R. Mooi. 1998. Identification and characterization of heparin binding regions of the Fim2 subunit of Bordetella pertussis. Infect. Immun. 66:22562263.
32. Gill, D. B.,, M. Koomey,, K. G. Cannon,, and J. P. Atkinson. 2003. Down-regulation of CD46 by piliated Neisseria gonorrhoeae. J. Exp. Med. 198:13131322.
33. Gilsdorf, J. R., 2002. Role of pili in Haemophilus influenzae adherence, colonisation and diseases, p. 139161. In M. Wilson (ed.), Bacterial Adhesion to Host Tissues: Mechanisms and Consequences. Cambridge University Press, Cambridge, United Kingdom.
34. Gilsdorf, J. R.,, K. W. McCrea,, and C. F. Marrs. 1997. Role of pili in Haemophilus influenzae adherence and colonization. Infect. Immun. 65:29973002.
35. Gorter, A. D.,, P. S. Hiemstra,, S. de Bentzmann,, S. van Wetering,, J. Dankert,, and L. van Alphen. 2000. Stimulation of bacterial adherence by neutrophil defensins varies among bacterial species but not among host cell types. FEMS Immunol. Med. Microbiol. 28:105111.
36. Grant, C. C.,, and J. D. Cherry. 2002. Keeping pace with the elusive Bordetella pertussis. J. Infect. 44:712.
37. Grass, S.,, A. Z. Buscher,, W. E. Swords,, M. A. Apicella,, S. J. Barenkamp,, N. Ozchlewski,, and J. W. St Geme III. 2003. The Haemophilus influenzae HMW1 adhesin is glycosylated in a process that requires HMW1C and phosphoglucomutase, an enzyme involved in lipooligosaccharide biosynthesis. Mol. Microbiol. 48:737751.
38. Gray-Owen, S. D.,, D. R. Lorenzen,, A. Haude,, T. F. Meyer,, and C. Dehio. 1997. Differential Opa specificities for CD66 receptors influence tissue interactions and cellular response to Neisseria gonorrhoeae. Mol. Microbiol. 26:971980.
39. Gubish, E. R. J.,, K. C. Chen,, and T. M. Buchanan. 1982. Attachment of gonococcal pili to lectin-resistant clones of Chinese hamster ovary cells. Infect. Immun. 37:189194.
40. Hahn, H. P. 1997. The type-4 pilus is the major virulenceassociated adhesin of Pseudomonas aeruginosa: a review. Gene 192:99108.
41. Hammarstrom, S. 1999. The carcinoembryonic antigen (CEA) family: structures, suggested functions and expression in normal and malignant tissues. Semin. Cancer Biol. 9:6781.
42. Harvey, H. A.,, M. P. Jennings,, C. A. Campbell,, R. Williams,, and M. A. Apicella. 2001. Receptor-mediated endocytosis of Neisseria gonorrhoeae into primary human urethral epithelial cells: the role of the asialoglycoprotein receptor. Mol. Microbiol. 42:659672.
43. Hauck, C. R.,, and T. F. Meyer. 2003. ‘Small’ talk: Opa proteins as mediators of Neisseria-host-cell communication. Curr. Opin. Microbiol. 6:4349.
44. Henderson, I. R.,, and J. P. Nataro. 2001. Virulence functions of autotransporter proteins. Infect. Immun. 69:12311243.
45. Henderson, I. R.,, P. Owen,, and J. P. Nataro. 1999. Molecular switches—the ON and OFF of bacterial phase variation. Mol. Microbiol. 33:919932.
46. Hers, J. F. P.,, and J. Mulder. 1953. The mucosal epithelium of the respiratory tract in muco-purulent bronchitis caused by Haemophilus influenzae. J. Pathol. Bacteriol. 66:103108.
47. Hill, D. J.,, M. A. Toleman,, D. J. Evans,, S. Villullas,, L. Van Alphen,, and M. Virji. 2001. The variable P5 proteins of typeable and non-typeable Haemophilus influenzae target human CEACAM1. Mol. Microbiol. 39:850862.
48. Hill, D. J.,, and M. Virji. 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. 48:117129.
49. Hitchcock, P. J. 1989. Unified nomenclature for pathogenic Neisseria species. Clin. Microbiol. Rev. 2:S64S65.
50. Hoiczyk, E.,, A. Roggenkamp,, M. Reichenbecher,, A. Lupas,, and J. Heesemann. 2000. Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins. EMBO J. 19:59895999.
51. Holm, M. M.,, S. L. Vanlerberg,, I. M. Foley,, D. D. Sledjeski,, and E. R. Lafontaine. 2004. The Moraxella catarrhalis porinlike outer membrane protein CD is an adhesin for human lung cells. Infect. Immun. 72:19061913.
52. Holm, M. M.,, S. L. Vanlerberg,, D. D. Sledjeski,, and E. R. Lafontaine. 2003. The hag protein of Moraxella catarrhalis strain O35E is associated with adherence to human lung and middle ear cells. Infect. Immun. 71:49774984.
53. Hu, W. G.,, J. Chen,, J. C. McMichael,, and X. X. Gu. 2001. Functional characteristics of a protective monoclonal antibody against serotype A and C lipooligosaccharides from Moraxella catarrhalis. Infect. Immun. 69:13581363.
54. Hultgren, S. J.,, S. Abraham,, M. Caparon,, P. Falk,, J. W. St. Geme III, and S. Normark. 1993. Pilus and nonpilus bacterial adhesins: assembly and function in cell recognition. Cell 73:887901.
55. Ishibashi, Y.,, and A. Nishikawa. 2003. Role of nuclear factor- kappa B in the regulation of intercellular adhesion molecule 1 after infection of human bronchial epithelial cells by Bordetella pertussis. Microb. Pathog. 35:169177.
56. Janson, H.,, B. Carlen,, A. Cervin,, A. Forsgren,, A. B. Magnusdottir,, S. Lindberg,, and T. Runer. 1999. Effects on the ciliated epithelium of protein D-producing and -nonproducing nontypeable Haemophilus influenzae in nasopharyngeal tissue cultures. J. Infect. Dis. 180:737746.
57. Jiang, Z.,, N. Nagata,, E. Molina,, L. O. Bakaletz,, H. Hawkins,, and J. A. Patel. 1999. Fimbria-mediated enhanced attachment of nontypeable Haemophilus influenzae to respiratory syncytial virus-infected respiratory epithelial cells. Infect. Immun. 67:187192.
58. Johansson, L.,, A. Rytkonen,, P. Bergman,, B. Albiger,, H. Kallstrom,, T. Hokfelt,, B. Agerberth,, R. Cattaneo,, and A. B. Jonsson. 2003. CD46 in meningococcal disease. Science 301:373375.
59. Johnsson, E.,, A. Thern,, B. Dahlback,, L. O. Heden,, M. Wikstrom,, and G. Lindahl. 1996. A highly variable region in members of the streptococcal M protein family binds the human complement regulator C4BP. J. Immunol. 157:30213029.
60. Jones, C.,, M. Virji,, and P. R. Crocker. 2003. Recognition of sialylated meningococcal lipopolysaccharide by siglecs expressed on myeloid cells leads to enhanced bacterial uptake. Mol. Microbiol. 49:12131225.
61. Jonsson, A. B.,, D. Ilver,, P. Falk,, J. Pepose,, and S. Normark. 1994. Sequence changes in the pilus subunit lead to tropism variation of Neisseria gonorrhoeae to human tissue. Mol. Microbiol. 13:403416.
62. Kahler, C. M.,, L. E. Martin,, Y. L. Tzeng,, Y. K. Miller,, K. Sharkey,, D. S. Stephens,, and J. K. Davies. 2001. Polymorphisms in pilin glycosylation locus of Neisseria meningitidis expressing class II pili. Infect. Immun. 69:35973604.
63. Kajava, A. V.,, N. Cheng,, R. Cleaver,, M. Kessel,, M. N. Simon,, E. Willery,, F. Jacob-Dubuisson,, C. Locht,, and A. C. Steven. 2001. Beta-helix model for the filamentous haemagglutinin adhesin of Bordetella pertussis and related bacterial secretory proteins. Mol. Microbiol. 42:279292.
64. Kallstrom, H.,, D. Blackmer Gill,, B. Albiger,, M. K. Liszewski,, J. P. Atkinson,, and A. B. Jonsson. 2001. Attachment of Neisseria gonorrhoeae to the cellular pilus receptor CD46: identification of domains important for bacterial adherence. Cell. Microbiol. 3:133143.
65. Kallstrom, H.,, M. K. Liszewski,, J. P. Atkinson,, and A. B. Jonsson. 1997. Membrane cofactor protein (MCP or CD46) is a cellular pilus receptor for pathogenic Neisseria. Mol. Microbiol. 25:639647.
66. Kazmierczak, B. I.,, K. Mostov,, and J. N. Engel. 2001. Interaction of bacterial pathogens with polarized epithelium. Annu. Rev. Microbiol. 55:407435.
67. Kerr, J. R.,, and R. C. Matthews. 2000. Bordetella pertussis infection: pathogenesis, diagnosis, management, and the role of protective immunity. Eur. J. Clin. Microbiol. Infect. Dis. 19:7788.
68. Knepper, B.,, I. Heuer,, T. F. Meyer,, and J. P. van Putten. 1997. Differential response of human monocytes to Neisseria gonorrhoeae variants expressing pili and opacity proteins. Infect. Immun. 65:41224129.
69. Kubiet, M.,, R. Ramphal,, A. Weber,, and A. Smith. 2000. Pilus-mediated adherence of Haemophilus influenzae to human respiratory mucins. Infect. Immun. 68:33623367.
70. Lafontaine, E. R.,, L. D. Cope,, C. Aebi,, J. L. Latimer,, G. H. McCracken, Jr., and E. J. Hansen. 2000. The UspA1 protein and a second type of UspA2 protein mediate adherence of Moraxella catarrhalis to human epithelial cells in vitro. J. Bacteriol. 182:13641373.
71. Lafontaine, E. R.,, N. J. Wagner,, and E. J. Hansen. 2001. Expression of the Moraxella catarrhalis UspA1 protein undergoes phase variation and is regulated at the transcriptional level. J. Bacteriol. 183:15401551.
72. Leininger, E.,, C. A. Ewanowich,, A. Bhargava,, M. S. Peppler,, J. G. Kenimer,, and M. J. Brennan. 1992. Comparative roles of the Arg-Gly-Asp sequence present in the Bordetella pertussis adhesins pertactin and filamentous hemagglutinin. Infect. Immun. 60:23802385.
73. Leusch, H. G.,, Z. Drzeniek,, Z. Markos-Pusztai,, and C. Wagener. 1991. Binding of Escherichia coli and Salmonella strains to members of the carcinoembryonic antigen family: differential binding inhibition by aromatic alpha-glycosides of mannose. Infect. Immun. 59:20512057.
74. Locht, C.,, P. Bertin,, F. D. Menozzi,, and G. Renauld. 1993. The filamentous haemagglutinin, a multifaceted adhesion produced by virulent Bordetella spp. Mol. Microbiol. 9:653660.
75. Lopez-Vidriero, M. T. 1981. Airway mucus; production and composition. Chest 80:799804.
76. Makhov, A. M.,, J. H. Hannah,, M. J. Brennan,, B. L. Trus,, E. Kocsis,, J. F. Conway,, P. T. Wingfield,, M. N. Simon,, and A. C. Steven. 1994. Filamentous hemagglutinin of Bordetella pertussis—a bacterial adhesin formed as a 50-nm monomeric rigid-rod based on a 19-residue repeat motif rich in betastrands and beta-turns. J. Mol. Biol. 241:110124.
77. Malorny, B.,, G. Morelli,, B. Kusecek,, J. Kolberg,, and M. Achtman. 1998. Sequence diversity, predicted two-dimensional protein structure, and epitope mapping of neisserial Opa proteins. J. Bacteriol. 180:13231330.
78. Marceau, M.,, J. L. Beretti,, and X. Nassif. 1995. High adhesiveness of encapsulated Neisseria meningitidis to epithelial cells is associated with the formation of bundles of pili. Mol. Microbiol. 17:855863.
79. Marrs, C. F.,, and S. Weir. 1990. Pili (fimbriae) of Branhamella species. Am. J. Med. 88:36S40S.
80. McCrea, K. W.,, W. J. Watson,, J. R. Gilsdorf,, and C. F. Marrs. 1997. Identification of two minor subunits in the pilus of Haemophilus influenzae. J. Bacteriol. 179:42274231.
81. McMichael, J. C. 2000. Progress toward the development of a vaccine to prevent Moraxella (Branhamella) catarrhalis infections. Microb. Infect. 2:561568.
82. McMichael, J. C.,, M. J. Fiske,, R. A. Fredenburg,, D. N. Chakravarti,, K. R. van der Meid,, V. Barniak,, J. Caplan,, E. Bortell,, S. Baker,, R. Arumugham,, and D. Chen. 1998. Isolation and characterization of two proteins from Moraxella catarrhalis that bear a common epitope. Infect. Immun. 66:43744381.
83. McNeil, G.,, and M. Virji. 1997. Phenotypic variants of meningococci and their potential in phagocytic interactions: the influence of opacity proteins, pili, PilC and surface sialic acids. Microb. Pathog. 22:295304.
84. McNeil, G.,, M. Virji,, and E. R. Moxon. 1994. Interactions of Neisseria meningitidis with human monocytes. Microb. Pathog. 16:153163.
85. Menozzi, F. D.,, K. Pethe,, P. Bifani,, F. Soncin,, M. J. Brennan,, and C. Locht. 2002. Enhanced bacterial virulence through exploitation of host glycosaminoglycans. Mol. Microbiol. 43:13791386.
86. Merz, A. J.,, and M. So. 2000. Interactions of pathogenic neisseriae with epithelial cell membranes. Annu. Rev. Cell Dev. Biol. 16:423457.
87. Muenzner, P.,, M. Naumann,, T. F. Meyer,, and S. D. Gray- Owen. 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-kappaB. J. Biol. Chem. 276:2433124340.
88. Nassif, X.,, J. Lowy,, P. Stenberg,, P. O’Gaora,, A. Ganji,, and M. So. 1993. Antigenic variation of pilin regulates adhesion of Neisseria meningitidis to human epithelial cells. Mol. Microbiol. 8:719725.
89. Nassif, X.,, M. Marceau,, C. Pujol,, B. Pron,, J. L. Beretti,, and M. K. Taha. 1997. Type-4 pili and meningococcal adhesiveness. Gene 192:149153.
90. Noel, G. J.,, D. C. Love,, and D. M. Mosser. 1994. Highmolecular- weight proteins of nontypeable Haemophilus influenzae mediate bacterial adhesion to cellular proteoglycans. Infect. Immun. 62:40284033.
91. Obrink, B. 1997. CEA adhesion molecules: multifunctional proteins with signal-regulatory properties. Curr. Opin. Cell Biol. 9:616626.
92. Olyhoek, A. J.,, J. Sarkari,, M. Bopp,, G. Morelli,, and M. Achtman. 1991. Cloning and expression in Escherichia coli of opc, the gene for an unusual class 5 outer membrane protein from Neisseria meningitidis (meningococci/surface antigen). Microb. Pathog. 11:249257.
93. Pancholi, V.,, P. Fontan,, and H. Jin. 2003. Plasminogenmediated group A streptococcal adherence to and pericellular invasion of human pharyngeal cells. Microb. Pathog. 35:293303.
94. Parge, H. E.,, K. T. Forest,, M. J. Hickey,, D. A. Christensen,, E. D. Getzoff,, and J. A. Tainer. 1995. Structure of the fibreforming protein pilin at 2.6 A resolution. Nature 378:3238.
95. Park, H. S. M.,, M. Wolfgang,, J. P. M. van Putten,, D. Dorward,, S. F. Hayes,, and M. Koomey. 2001. Structural alterations in a type IV pilus subunit protein result in concurrent defects in multicellular behaviour and adherence to host tissue. Mol. Microbiol. 42:293307.
96. Patti, J. M.,, B. L. Allen,, M. J. McGavin,, and M. Hook. 1994. MSCRAMM-mediated adherence of microorganisms to host tissues. Annu. Rev. Microbiol. 48:585617.
97. Pearson, M. M.,, E. R. Lafontaine,, N. J. Wagner,, J. W. St. Geme III, and E. J. Hansen. 2002. A hag mutant of Moraxella catarrhalis strain O35E is deficient in hemagglutination, autoagglutination, and immunoglobulin D-binding activities. Infect. Immun. 70:45234533.
98. Pinner, R. W.,, P. A. Spellman,, and D. S. Stephens. 1991. Evidence for functionally distinct pili expressed by Neisseria meningitidis. Infect. Immun. 59:31693175.
99. Poolman, J. T.,, L. Bakaletz,, A. Cripps,, P. A. Denoel,, A. Forsgren,, J. Kyd,, and Y. Lobet. 2000. Developing a nontypeable Haemophilus influenzae (NTHi) vaccine. Vaccine 19:S108S115.
100. Prall, F.,, P. Nollau,, M. Neumaier,, H. D. Haubeck,, Z. Drzeniek,, U. Helmchen,, T. Loning,, and C. Wagener. 1996. CD66a (BGP), an adhesion molecule of the carcinoembryonic antigen family, is expressed in epithelium, endothelium, and myeloid cells in a wide range of normal human tissues. J. Histochem. Cytochem. 44:3541.
101. Prasadarao, N. V.,, E. Lysenko,, C. A. Wass,, K. S. Kim,, and J. N. Weiser. 1999. Opacity-associated protein A contributes to the binding of Haemophilus influenzae to chang epithelial cells. Infect. Immun. 67:41534160.
102. Prince, S. M.,, M. Achtman,, and J. P. Derrick. 2002. Crystal structure of the OpcA integral membrane adhesin from Neisseria meningitidis. Proc. Natl. Acad. Sci. USA 99:34173421.
103. Rahman, M.,, H. Kallstrom,, S. Normark,, and A. B. Jonsson. 1997. PiIC of pathogenic Neisseria is associated with the bacterial cell surface. Mol. Microbiol. 25:1125.
104. Read, R. C.,, R. Wilson,, A. Rutman,, V. Lund,, H. C. Todd,, A. P. R. Brain,, P. K. Jeffery,, and P. J. Cole. 1991. Interaction of nontypable Haemophilus influenzae with human respiratory mucosa in vitro. J. Infect. Dis. 163:549558.
105. Reddy, M. S. 1992. Human tracheobronchial mucin— purification and binding to Pseudomonas aeruginosa. Infect. Immun. 60:15301535.
106. Reddy, M. S.,, J. M. Bernstein,, T. F. Murphy,, and H. S. Faden. 1996. Binding between outer membrane proteins of nontypeable Haemophilus influenzae and human nasopharyngeal mucin. Infect. Immun. 64:14771479.
107. Reddy, M. S.,, T. F. Murphy,, H. S. Faden,, and J. M. Bernstein. 1997. Middle ear mucin glycoprotein: purification and interaction with nontypable Haemophilus influenzae and Moraxella catarrhalis. Otolaryngol. Head Neck Surg. 116:175180.
108. Rest, R. F.,, and W. M. Shafer. 1989. Interactions of Neisseria gonorrhoeae with human neutrophils. Clin. Microbiol. Rev. 2(Suppl.):S83S91.
109. Rikitomi, N.,, K. Ahmed,, and T. Nagatake. 1997. Moraxella (Branhamella) catarrhalis adherence to human bronchial and oropharyngeal cells: the role of adherence in lower respiratory tract infections. Microbiol. Immunol. 41:487494.
110. Rodriguez, C. A.,, V. Avadhanula,, A. Buscher,, A. L. Smith,, J. W. St Geme III,, and E. E. Adderson. 2003. Prevalence and distribution of adhesins in invasive non-type b encapsulated Haemophilus influenzae. Infect. Immun. 71:16351642.
111. Rostand, K. S.,, and J. D. Esko. 1997. Microbial adherence to and invasion through proteoglycans. Infect. Immun. 65:18.
112. Rudel, T.,, I. Scheurerpflug,, and T. F. Meyer. 1995. Neisseria PilC protein identified as type-4 pilus tip-located adhesin. Nature 373:357359.
113. Rytkonen, A.,, L. Johansson,, V. Asp,, B. Albiger,, and A. B. Jonsson. 2001. Soluble pilin of Neisseria gonorrhoeae interacts with human target cells and tissue. Infect. Immun. 69:64196426.
114. Sandros, J.,, and E. Tuomanen. 1993. Attachment factors of Bordetella pertussis: mimicry of eukaryotic cell recognition molecules. Trends Microbiol. 1:192196.
115. Sarkari, J.,, N. Pandit,, E. R. Moxon,, and M. Achtman. 1994. Variable expression of the Opc outer membrane protein in Neisseria meningitidis is caused by size variation of a promoter containing poly-cytidine. Mol. Microbiol. 13:207217.
116. Saukkonen, K.,, W. N. Burnette,, V. L. Mar,, H. R. Masure,, and E. I. Tuomanen. 1992. Pertussis toxin has eukaryoticlike carbohydrate recognition domains. Proc. Natl. Acad. Sci. USA 89:118122.
117. Sauter, S. L.,, S. M. Rutherfurd,, C. Wagener,, J. E. Shively,, and S. A. Hefta. 1991. Binding of nonspecific cross-reacting antigen, a granulocyte membrane glycoprotein, to Escherichia coli expressing type 1 fimbriae. Infect. Immun. 59:24852493.
118. Sauter, S. L.,, S. M. Rutherfurd,, C. Wagener,, J. E. Shively,, and S. A. Hefta. 1993. Identification of the specific oligosaccharide sites recognized by type 1 fimbriae from Escherichia coli on nonspecific cross-reacting antigen, a CD66 cluster granulocyte glycoprotein. J. Biol. Chem. 268:1551015516.
119. Scheuerpflug, I.,, T. Rudel,, R. Ryll,, J. Pandit,, and T. F. Meyer. 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. 67:834843.
120. Serruto, D.,, J. Adu-Bobie,, M. Scarselli,, D. Veggi,, M. Pizza,, R. Rappuoli,, and B. Arico. 2003. Neisseria meningitidis App, a new adhesin with autocatalytic serine protease activity. Mol. Microbiol. 48:323334.
121. Sirakova, T.,, P. E. Kolattukudy,, D. Murwin,, J. Billy,, E. Leake,, D. Lim,, T. DeMaria,, and L. Bakaletz. 1994. Role of fimbriae expressed by nontypeable Haemophilus influenzae in pathogenesis of and protection against otitis media and relatedness of the fimbrin subunit to outer membrane protein A. Infect. Immun. 62:2002ndash;2020.
122. Stephens, D. S.,, and M. M. Farley. 1991. Pathogenic events during infection of the human nasopharynx with Neisseria meningitidis and Haemophilus influenzae. Rev. Infect. Dis.13:2233.
123. Sterk, L. M. T.,, L. vanAlphen,, L. Geelen-vandenBroek,, H. J. Houthoff,, and J. Dankert. 1991. Differential binding of Haemophilus influenzae to human tissues by fimbriae. J. Med. Microbiol. 35:129138.
124.St. Geme, J. W., III. 2002. Molecular and cellular determinants of non-typeable Haemophilus influenzae adherence and invasion. Cell. Microbiol. 4:191200.
125.St. Geme, J. W., III. 1996. Molecular determinants of the interaction between Haemophilus influenzae and human cells. Am. J. Respir. Crit. Care Med. 154:S192S196.
126.St. Geme, J. W., III. 2000. The pathogenesis of nontypable Haemophilus influenzae otitis media. Vaccine 19:S41S50.
127.St. Geme, J. W., III, and D. Cutter. 1996. Influence of pili, fibrils, and capsule on in vitro adherence by Haemophilus influenzae type b. Mol. Microbiol. 21:2131.
128.St. Geme, J. W., III, A. Takala, E. Esko, and S. Falkow. 1994. Evidence for capsule gene sequences among pharyngeal isolates of nontypeable Haemophilus influenzae. J. Infect. Dis. 169:337342.
129. Stimson, E.,, M. Virji,, S. Barker,, M. Panico,, I. Blench,, J. Saunders,, G. Payne,, E. R. Moxon,, A. Dell,, and H. R. Morris. 1996. Discovery of a novel protein modification: alphaglycerophosphate is a substituent of meningococcal pilin. Biochem. J. 316:2933.
130. Stimson, E.,, M. Virji,, K. Makepeace,, A. Dell,, H. R. Morris,, G. Payne,, J. R. Saunders,, M. P. Jennings,, S. Barker,, and M. Panico. 1995. Meningococcal pilin: a glycoprotein substituted with digalactosyl-2,4- diacetamido-2,4,6-trideoxyhexose. Mol. Microbiol. 17:12011214.
131. Swanson, J.,, E. Sparks,, D. Young,, and G. King. 1975. Studies on gonococcus infection. X. Pili and leukocyte association factor as mediators of interactions between gonococci and eukaryotic cells in vitro. Infect. Immun. 11:13521361.
132. Swords, W. E.,, B. A. Buscher,, K. V. S. Li,, A. Preston,, W. A. Nichols,, J. N. Weiser,, B. W. Gibson,, and M. A. Apicella. 2000. Non-typeable Haemophilus influenzae adhere to and invade human bronchial epithelial cells via an interaction of lipooligosaccharide with the PAF receptor. Mol. Microbiol. 37:1327.
133. Taha, M. K., 2002. Transcription regulation of meningococcal gene expression upon adhesion to target cells, p. 165182. In M. Wilson (ed.), Bacterial Adhesion to Host Tissues: Mechanisms and Consequences. Cambridge University Press, Cambridge, United Kingdom.
134. Timpe, J. M.,, M. M. Holm,, S. L. Vanlerberg,, V. Basrur,, and E. R. Lafontaine. 2003. Identification of a Moraxella catarrhalis outer membrane protein exhibiting both adhesin and lipolytic activities. Infect. Immun. 71:43414350.
135. Tobiason, D. M.,, and H. S. Seifert. 2001. Inverse relationship between pilus-mediated gonococcal adherence and surface expression of the pilus receptor, CD46. Microbiology 147:23332340.
136. Toleman, M.,, E. Aho,, and M. Virji. 2001. Expression of pathogen-like Opa adhesins in commensal Neisseria: genetic and functional analysis. Cell. Microbiol. 3:3344.
137. Tosi, M. F.,, J. M. Stark,, A. Hamedani,, C. W. Smith,, D. C. Gruenert,, and Y. T. Huang. 1992. Intercellular-adhesion molecule-1 (ICAM-1)-dependent and ICAM-1-independent adhesive interactions between polymorphonuclear leukocytes and human airway epithelial cells infected with parainfluenza virus type-2. J. Immunol. 149:33453349.
138. Tran Van Nhieu, G.,, and R. R. Isberg. 1993. Bacterial internalization mediated by beta 1 chain integrins is determined by ligand affinity and receptor density. EMBO J. 12:18871895.
139. Tsutsumi, Y.,, N. Onoda,, M. Misawa,, M. Kuroki,, and Y. Matsuoka. 1990. Immunohistochemical demonstration of nonspecific cross-reacting antigen in normal and neoplastic human tissues using a monoclonal-antibody: comparison with carcinoembryonic antigen localization. Acta Pathol. Jpn. 40:8597.
140. Unkmeir, A.,, K. Latsch,, G. Dietrich,, E. Wintermeyer,, B. Schinke,, S. Schwender,, K. S. Kim,, M. Eigenthaler,, and M. Frosch. 2002. Fibronectin mediates Opc-dependent internalization of Neisseria meningitidis in human brain microvascular endothelial cells. Mol. Microbiol. 46:933946.
141. van Alphen, L.,, L. Geelen-van den Broek,, L. Blaas,, M. van Ham,, and J. Dankert. 1991. Blocking of fimbria-mediated adherence of Haemophilus influenzae by sialyl gangliosides. Infect. Immun. 59:44734477.
142. van Alphen, L.,, and S. M. van Ham. 1994. Adherence and invasion of Haemophilus influenzae. Rev. Med. Microbiol. 5:245.
143. van den Berg, B. M.,, H. Beekhuizen,, R. J. L. Willems,, F. R. Mooi,, and R. van Furth. 1999. Role of Bordetella pertussis virulence factors in adherence to epithelial cell lines derived from the human respiratory tract. Infect. Immun. 67:10561062.
144. van der Flier, A.,, and A. Sonnenberg. 2001. Function and interactions of integrins. Cell Tissue Res. 305:285298.
145. van Putten, J. P.,, and S. M. Paul. 1995. Binding of syndecanlike cell surface proteoglycan receptors is required for Neisseria gonorrhoeae entry into human mucosal cells. EMBO J. 14:21442154.
146. van Schilfgaarde, M.,, L. van Alphen,, P. Eijk,, V. Everts,, and J. Dankert. 1995. Paracytosis of Haemophilus influenzae through cell layers of Nci-H292 lung epithelial-cells. Infect. Immun. 63:47294737.
147. Verduin, C. M.,, C. Hol,, A. Fleer,, H. van Dijk,, and A. van Belkum. 2002. Moraxella catarrhalis: from emerging to established pathogen. Clin. Microbiol. Rev. 15:125144.
148. Virji, M. 2001. CEA and innate immunity. Trends Microbiol. 9:258259.
149. Virji, M.,, C. Alexandrescu,, D. J. Ferguson,, J. R. Saunders,, and E. R. Moxon. 1992. Variations in the expression of pili: the effect on adherence of Neisseria meningitidis to human epithelial and endothelial cells. Mol. Microbiol. 6:12711279.
150. Virji, M.,, D. Evans,, J. Griffith,, D. Hill,, L. Serino,, A. Hadfield,, and S. M. Watt. 2000. Carcinoembryonic antigens are targeted by diverse strains of typable and non-typable Haemophilus influenzae. Mol. Microbiol. 36:784795.
151. Virji, M.,, D. Evans,, A. Hadfield,, F. Grunert,, A. M. Teixeira,, and S. M. Watt. 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. 34:538551.
152. Virji, M.,, K. Makepeace,, D. J. Ferguson,, M. Achtman,, and E. R. Moxon. 1993. Meningococcal Opa and Opc proteins: their role in colonization and invasion of human epithelial and endothelial cells. Mol. Microbiol. 10:499510.
153. Virji, M.,, K. Makepeace,, D. J. Ferguson,, and S. M. Watt. 1996. Carcinoembryonic antigens (CD66) on epithelial cells and neutrophils are receptors for Opa proteins of pathogenic Neisseriae. Mol. Microbiol. 22:941950.
154. Virji, M.,, K. Makepeace,, and E. R. Moxon. 1994. Distinct mechanisms of interactions of Opc-expressing meningococci at apical and basolateral surfaces of human endothelial cells: the role of integrins in apical interactions. Mol. Microbiol. 14:173184.
155. Virji, M.,, K. Makepeace,, I. R. Peak,, D. J. Ferguson,, M. P. Jennings,, and E. R. Moxon. 1995. Opc- and pilus-dependent interactions of meningococci with human endothelial cells: molecular mechanisms and modulation by surface polysaccharides. Mol. Microbiol. 18:741754.
156. Virji, M.,, J. R. Saunders,, G. Sims,, K. Makepeace,, D. Maskell,, and D. J. Ferguson. 1993. Pilus-facilitated adherence of Neisseria meningitidis to human epithelial and endothelial cells: modulation of adherence phenotype occurs concurrently with changes in primary amino acid sequence and the glycosylation status of pilin. Mol. Microbiol. 10:10131028.
157. Virji, M.,, S. M. Watt,, S. Barker,, K. Makepeace,, and R. Doyonnas. 1996. The N-domain of the human CD66a adhesion molecule is a target for Opa proteins of Neisseria meningitidis and Neisseria gonorrhoeae. Mol. Microbiol. 22:929939.
158. Virkola, R.,, M. Brummer,, H. Rauvala,, L. van Alphen,, and T. K. Korhonen. 2000. Interaction of fimbriae of Haemophilus influenzae type B with heparin-binding extracellular matrix proteins. Infect. Immun. 68:56965701.
159. Virkola, R.,, K. Lahteenmaki,, T. Eberhard,, P. Kuusela,, L. Van Alphen,, M. Ullberg,, and T. K. Korhonen. 1996. Interaction of Haemophilus influenzae with the mammalian extracellular matrix. J. Infect. Dis. 173:11371147.
160. Wadstrom, T.,, and A. Ljungh. 1999. Glycosaminoglycanbinding microbial proteins in tissue adhesion and invasion: key events in microbial pathogenicity. J. Med. Microbiol. 48:223233.
161. Webb, D. C.,, and A. W. Cripps. 1999. A method for the purification and refolding of a recombinant form of the nontypeable Haemophilus influenzae P5 outer membrane protein fused to polyhistidine. Protein Expression Purif. 15:17.
162. Webb, D. C.,, and A. W. Cripps. 1998. Secondary structure and molecular analysis of interstrain variability in the P5 outer-membrane protein of non-typable Haemophilus influenzae isolated from diverse anatomical sites. J. Med. Microbiol. 47:10591067.
163. Weber, A.,, K. Harris,, S. Lohrke,, L. Forney,, and A. L. Smith. 1991. Inability to express fimbriae results in impaired ability of Haemophilus influenzae B to colonize the nasopharynx. Infect. Immun. 59:47244728.
164. Weiser, J. N.,, D. Bae,, C. Fasching,, R. W. Scamurra,, A. J. Ratner,, and E. N. Janoff. 2003. Antibody-enhanced pneumococcal adherence requires IgA1 protease. Proc. Natl. Acad. Sci. USA 100:42154220.
165. Weiser, J. N.,, S. T. Chong,, D. Greenberg,, and W. Fong. 1995. Identification and characterization of a cell envelope protein of Haemophilus influenzae contributing to phase variation in colony opacity and nasopharyngeal colonization. Mol. Microbiol. 17:555564.
166. Weiser, J. N.,, J. B. Goldberg,, N. Pan,, L. Wilson,, and M. Virji. 1998. The phosphorylcholine epitope undergoes phase variation on a 43-kilodalton protein in Pseudomonas aeruginosa and on pili of pathogenic neisseriae. Infect. Immun. 66:42634267.
167. Widdicombe, J. 1995. Relationships among the composition of mucus, epithelial lining liquid, and adhesion of microorganisms. Am. J. Respir. Crit. Care Med. 151:20882093.
168. Widdicombe, J. H. 2002. Regulation of the depth and composition of airway surface liquid. J. Anat. 201:313318.
169. Willems, R.,, A. Paul,, H. G. J. van der Heide,, A. R. Teravest,, and F. R. Mooi. 1990. Fimbrial phase variation in Bordetella pertussis—a novel mechanism for transcriptional regulation. EMBO J. 9:28032809.
170. Willems, R. J.,, C. Geuijen,, H. G. vanderHeide,, M. Matheson,, A. Robinson,, L. F. Versluis,, R. Ebberink,, J. Theelen,, and F. R. Mooi. 1993. Isolation of a putative fimbrial adhesin from Bordetella pertussis and the identification of its gene. Mol. Microbiol. 9:623634.
171. Winther-Larsen, H. C.,, F. T. Hegge,, M. Wolfgang,, S. F. Hayes,, J. P. van Putten,, and M. Koomey. 2001. Neisseria gonorrhoeae PilV, a type IV pilus-associated protein essential to human epithelial cell adherence. Proc. Natl. Acad. Sci. USA 98:1527615281.
172. Zaleski, A.,, N. K. Scheffler,, P. Densen,, F. K. Lee,, A. A. Campagnari,, B. W. Gibson,, and M. A. Apicella. 2000. Lipooligosaccharide P(k) (Galα1-4Galβ1-4Glc) epitope of Moraxella catarrhalis is a factor in resistance to bactericidal activity mediated by normal human serum. Infect. Immun. 68:52615268.
173. Zhang, J. R.,, K. E. Mostov,, M. E. Lamm,, M. Nanno,, S. Shimida,, M. Ohwaki,, and E. Tuomanen. 2000. The polymeric immunoglobulin receptor translocates pneumococci across human nasopharyngeal epithelial cells. Cell 102:827837.


Generic image for table
Table 1

Adhesins of

Citation: Virji M. 2005. Bacterial Adherence and Tropism in the Human Respiratory Tract, p 97-118. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch8
Generic image for table
Table 2

Adhesins of

Citation: Virji M. 2005. Bacterial Adherence and Tropism in the Human Respiratory Tract, p 97-118. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch8

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