Recognition of a bacterial adhesin by an integrin: Macrophage CR3 (αMβ2,  ) binds filamentous hemagglutinin of Bordetella pertussis

Relman, David A.; Tuomanen, Elaine; Falkow, Stanley; Golenbock, Douglas T.; Saukkonen, Kirsi; Wright, Samuel D.

doi:10.1016/0092-8674(90)90701-f

Cited by 383 publications

(321 citation statements)

References 32 publications

Supporting

Mentioning

313

Contrasting

Unclassified

Order By: Relevance

“…In vitro studies suggest that FHA functions as an adhesin (14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28), and several binding domains have been identified. A heparin-binding domain promotes attachment to sulfated polysaccharides (29), a carbohydrate-recognition domain facilitates bacterial binding to ciliated respiratory epithelial cells and macrophages (30), and an arg-gly-asp (RGD) triplet interacts with the leukocyte-response integrin͞integrin-associated protein (LRI͞IAP) complex on monocytes͞macrophages, resulting in up-regulation of complement-receptor-3-binding activity (23) and, with very late antigen-5 on epithelial cells, stimulating the up-regulation of intercellular adhesion molecule-1 via an NF-B signaling pathway (19,31).…”

mentioning

confidence: 99%

Bordetellafilamentous hemagglutinin plays a critical role in immunomodulation, suggesting a mechanism for host specificity

Inatsuka

Julio

Cotter

2005

Proc. Natl. Acad. Sci. U.S.A.

120

View full text Add to dashboard Cite

Bordetella pertussis, the causative agent of the acute childhood respiratory disease whooping cough, is a human-adapted variant of Bordetella bronchiseptica, which displays a broad host range and typically causes chronic, asymptomatic infections. These pathogens express a similar but not identical surface-exposed and secreted protein called filamentous hemagglutinin (FHA) that has been proposed to function as both a primary adhesin and an immunomodulator. To test the hypothesis that FHA plays an important role in determining host specificity and͞or the propensity to cause acute versus chronic disease, we constructed a B. bronchiseptica strain expressing FHA from B. pertussis (FHA Bp) and compared it with wild-type B. bronchiseptica in several naturalhost infection models. FHA Bp was able to substitute for FHA from B. bronchiseptica (FHA Bb) with regard to its ability to mediate adherence to several epithelial and macrophage-like cell lines in vitro, but it was unable to substitute for FHA Bb in vivo. Specifically, FHA Bb, but not FHABp, allowed B. bronchiseptica to colonize the lower respiratory tracts of rats, to modulate the inflammatory response in the lungs of immunocompetent mice, resulting in decreased lung damage and increased bacterial persistence, to induce a robust anti-Bordetella antibody response in these immunocompetent mice, and to overcome innate immunity and cause a lethal infection in immunodeficient mice. These results indicate a critical role for FHA in B. bronchiseptica-mediated immunomodulation, and they suggest a role for FHA in host specificity.inflammation ͉ adhesin ͉ respiratory infection ͉ filamentous hemagglutinin D espite widespread vaccine coverage, whooping cough, or pertussis, remains a serious threat to human health, and its incidence has been increasing in recent years (1, 2). The causative agents, Bordetella pertussis and Bordetella parapertussis hu , are human-adapted pathogens that belong to a clade of very closely related Gram-negative bacteria that cause respiratory infections in mammals. Phylogenetic analyses indicate that Bordetella bronchiseptica, which displays a broad host range and typically colonizes its hosts chronically and asymptomatically, was the progenitor of this clade, with B. pertussis diverging relatively early and B. parapertussis hu diverging independently and much more recently than B. pertussis (3-6). Adaptation to humans and the propensity to cause acute disease (in which the infection is eventually cleared) rather than chronic disease (characterized by persistence of the bacteria, often for the lifetime of the host) has, therefore, evolved twice within this group of bacteria. Although a variety of Bordetella virulence factors have been characterized (4, 7-10), the mechanisms that determine host specificity and disease characteristics are not understood.Filamentous hemagglutinin (FHA), a primary component of acellular pertussis vaccines, is a large, ␤-helical, highly immunogenic protein that is both surface-associated and secreted (11)(12)(13). In vitro...

show abstract

mentioning

confidence: 99%

Bordetellafilamentous hemagglutinin plays a critical role in immunomodulation, suggesting a mechanism for host specificity

Inatsuka

Julio

Cotter

2005

Proc. Natl. Acad. Sci. U.S.A.

120

View full text Add to dashboard Cite

show abstract

“…It has been isolated from cases of endocarditis (1,2,21) and urinary tract infections (21) and from the intestinal tract (39). With the discovery of the RGD motifs on AsclO and Asal, the possiblity arises that these proteins could also act as adhesins for the E. faecalis cell by binding to eukaryotic cells via the integrin class of receptors (22,23,32). Interestingly, serum samples from patients with enterococcal endocarditis contain antibodies reactive with a 73-kDa enterococcal surface protein (1,2).…”

Section: Discussionmentioning

confidence: 99%

Role of the pheromone-inducible surface protein Asc10 in mating aggregate formation and conjugal transfer of the Enterococcus faecalis plasmid pCF10

et al. 1991

View full text Add to dashboard Cite

The high transfer frequency of pheromone-inducible conjugative plasmids of Enterococcusfaecalis in liquid culture is due in part to the formation of mating aggregates. These aggregates result from the interaction of two surface components, aggregation substance (AS), which is plasmid encoded, and the chromosomally encoded binding substance (BS). In the accompanying paper (S.-M. Kao, S. B. Olmsted, A. S. Viksnins, J. C. Gallo, G. M. Dunny, J. Bacteriol. 173:7650-7664, 1991), the sequence of the prgB gene encoding the AS molecule (Asc10) produced by pheromone-induced cells carrying plasmid pCF10 is presented. Here we report the results of genetic and immunological experiments which define the role of Ascl0 in aggregation and plasmid transfer. These data indicate expression of AS on the surface of an E. faecalis cell and its binding to BS expressed on a second cell are required for the formation of a mating pair and the efficient transfer of pCF10 in liquid matings. However, the orientation of the receptors was not critical for transfer; ie., AS expressed on recipient cells could facilitate plasmid transfer via binding to BS on the donor. Our results suggest that additional (as yet unidentified) products are involved in forming the channel that ultimately serves to transfer the DNA, with AS-BS binding serving primarily to generate the initial attachment between cells. The putative prgC gene product, identified by DNA sequencing (data presented in the accompanying paper), could be involved in transfer events occurring subsequent to aggregation.

show abstract

“…PT can function as one of the B. pertussis adhesins, which facilitate the first stage of infection by enabling attachment of the bacteria to the cilia of the respiratory tract (Relman et al, 1990;Saukkonen et al, 1992). In addition, several of the systemic disease effects which may result from infection, such as lymphocytosis, enhanced vascular permeability and stimulation of insulin secretion, can be reproduced by PT in experimental models (Ui, 1988).…”

Section: (Received November 2 1992) -Ejb 92 1550mentioning

confidence: 99%

Localisation of a receptor‐recognition domain on the S3 subunit of pertussis toxin by peptide mapping

Tallett

Seabrook

Irons

et al. 1993

European Journal of Biochemistry

View full text Add to dashboard Cite

Overlapping 1 O-amino-acid peptides, which consecutively span the amino acid sequence of the S3 subunit of pertussis toxin, were synthesised on polyethylene pins and screened for their ability to bind the glycoprotein fetuin. Fetuin binding was localised to a single peptide comprising amino acids 46-55. A free peptide, (E)S3c, of longer sequence (S3 amino acids 44-58) was also found to bind a-1 -acid glycoprotein, mixed brain gangliosides and fetuin. (E)S3c also recognised asialofetuin but with a lower apparent affinity relative to fetuin. The single tryptophan residue of the peptide yielded a fluorescence-emission maximum of 355 nm. In the presence of either ganglioside or the phospholipid L-a-lysolecithin, but not N-acetylneuramin-lactose or lactosylceramide, the emission intensity of (E)S3c was enhanced and the emission maximum blue-shifted to 340 nm by ganglioside, or to 345 nm by L-a-lysolecithin. Monosialogangliosides, disialogangliosides, and trisialogangliosides, when fluorescence-titrated, were each found to bind the peptide with a similar dissociation constant of 4.4 2 2.8 pM. These findings demonstrate that region 44-58 of the pertussis-toxin S3 subunit is likely to be involved in the recognition of both glycosylated and phospholipid constituents of target-cell membranes.

show abstract

Recognition of a bacterial adhesin by an integrin: Macrophage CR3 (αMβ2, ) binds filamentous hemagglutinin of Bordetella pertussis

Cited by 383 publications

References 32 publications

Bordetellafilamentous hemagglutinin plays a critical role in immunomodulation, suggesting a mechanism for host specificity

Bordetellafilamentous hemagglutinin plays a critical role in immunomodulation, suggesting a mechanism for host specificity

Role of the pheromone-inducible surface protein Asc10 in mating aggregate formation and conjugal transfer of the Enterococcus faecalis plasmid pCF10

Localisation of a receptor‐recognition domain on the S3 subunit of pertussis toxin by peptide mapping

Contact Info

Product

Resources

About