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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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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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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