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Adhesin–Receptor Interactions in Pasteurellaceae1 FEMS Microbiology Reviews 22 (1998) 45^59 Adhesin^receptor interactions in Pasteurellaceae Mario Jacques *, Sonia-Eè laine Paradis Groupe de Recherche sur les Maladies Infectieuses du Porc and Deèpartement de Pathologie et Microbiologie, Faculteè de Meèdecine Veèteèrinaire, Downloaded from https://academic.oup.com/femsre/article/22/1/45/512698 by guest on 01 October 2021 Universiteè de Montreèal, C.P. 5000, St-Hyacinthe, Queèbec J2S 7C6, Canada Received 7 August 1997; revised 3 March 1998; accepted 23 March 1998 Abstract The ability of bacteria to adhere to mucosal epithelium is dependent on the expression of adhesive molecules or structures, called adhesins, that allow attachment of the organisms to complementary molecules on mucosal surfaces, the receptors. Important human and animal pathogens are found among the Pasteurellaceae family which includes Haemophilus, Actinobacillus, and Pasteurella organisms. The purpose of this paper is to review the adhesin-receptor systems found in Pasteurellaceae, with an emphasis on recent developments in this specific area. Most of these organisms can employ multiple molecular mechanisms of adherence (or multiple adhesins) to initiate infection. Indeed, a wide variety of adhesins are expressed by members of the Pasteurellaceae, and different proteins (e.g. fimbriae, fibrils, outer membrane proteins) as well as polysaccharides (lipooligosaccharides, lipopolysaccharides, capsular polysaccharides) were clearly shown to play an important role in adherence. In many instances, these adhesins have proved to represent good vaccine candidates. Surprisingly, the receptors on host mucosal surfaces have yet been identified in very few cases. z 1998 Federation of European Micro- biological Societies. Published by Elsevier Science B.V. Keywords: Adherence; Adhesin; Receptor; Actinobacillus; Haemophilus; Pasteurella Contents 1. Introduction . ....................................................................... 46 2. Haemophilus . ....................................................................... 46 2.1. Haemophilus ducreyi ................................................................. 46 2.2. Haemophilus in£uenzae . ............................................................. 47 2.2.1. Capsule . .................................................................. 47 2.2.2. Fimbriae (pili) . ............................................................. 47 2.2.3. Surface ¢brils ................................................................. 48 2.2.4. High molecular mass adhesion proteins .............................................. 49 2.2.5. Other putative adhesins . ........................................................ 49 2.2.6. Binding to mucus . ............................................................. 50 * Corresponding author. Tel.: +1 (514) 773-8521, ext. 8348; Fax: +1 (514) 778-8108; E-mail: [email protected] This paper was presented at the Haemophilus, Actinobacillus, Pasteurella International Conference (HAP'96) held in Acapulco, Mexico, October 13^17, 1996. 0168-6445 / 98 / $19.00 ß 1998 Federation of European Microbiological Societies. Published by Elsevier Science B.V. PII S0168-6445(98)00007-2 FEMSRE 608 29-5-98 46 M. Jacques, S.-E. Paradis / FEMS Microbiology Reviews 22 (1998) 45^59 2.2.7. Binding to extracellular matrix components . ......................................... 50 2.2.8. Cell invasion .................................................................. 50 3. Actinobacillus . ....................................................................... 51 3.1. Actinobacillus actinomycetemcomitans . ................................................... 51 3.2. Actinobacillus pleuropneumoniae . ........................................................ 52 4. Pasteurella ........................................................................... 53 4.1. Pasteurella haemolytica . ............................................................. 53 4.2. Pasteurella multocida . ............................................................. 53 5. Conclusion ........................................................................... 54 Acknowledgements. ....................................................................... 55 References . ............................................................................. 55 1. Introduction found in Pasteurellaceae, i.e. organisms of the Hae- Downloaded from https://academic.oup.com/femsre/article/22/1/45/512698 by guest on 01 October 2021 mophilus, Actinobacillus, and Pasteurella (HAP) The initial event in bacterial colonization of their group, with an emphasis on recent developments in host organisms is the adherence of microorganisms this speci¢c area. The literature review for this article to the epithelial cells and/or mucus layer of the mu- ended in May 1997. cosal surfaces, which involves speci¢c interactions between bacterial adhesins and host receptors [1]. Bacterial adherence endows the pathogen with the 2. Haemophilus ability to withstand normal host defense cleansing mechanisms on mucosal surfaces. Adherence also 2.1. Haemophilus ducreyi confers a number of advantages on the bacterium, including enhanced toxicity to the host and increased H. ducreyi is the etiological agent of chancroid, a resistance to deleterious agents. The fact that bacte- sexually transmitted disease that is common in devel- rial colonization and infection can be prevented by oping countries and that has characteristic genital blocking adherence has stimulated research on the mucocutaneous ulcerative lesions (for a recent review identi¢cation of adhesins, their molecular biology, see [3]). The disease has received renewed attention and their binding speci¢cities. after reports that genital ulcers facilitate the trans- Members of the Pasteurellaceae are small Gram- mission of the human immunode¢ciency virus in en- negative rods that can colonize the mucosal surface demic populations. It has been proposed [3,4] that of the respiratory and genital tracts. Important hu- bacterial adherence to epithelial cells is the ¢rst step man and animal pathogens are found among this in the pathogenesis of H. ducreyi infection. Adher- bacterial family (Table 1) [2]. The purpose of this ence is followed by the growth of bacteria on the paper is to review the adhesin-receptor systems epithelial cells and the secretion of cytotoxin which Table 1 Members of the Pasteurellaceae family described in the present review and the diseases they cause in their respective host Organism Host Disease Haemophilus H. ducreyi human chancroid H. in£uenzae capsular type b (Hib) human meningitis, septicemia, epiglottitis H. in£uenzae non-typable (NTHi) human otitis media, sinusitis, conjunctivitis, acute lower respiratory tract infection Actinobacillus A. actinomycetemcomitans human juvenile and adult periodontitis A. pleuropneumoniae swine pleuropneumonia Pasteurella P. haemolytica bovine and sheep pneumonia P. multocida swine pneumonia, atrophic rhinitis FEMSRE 608 29-5-98 M. Jacques, S.-E. Paradis / FEMS Microbiology Reviews 22 (1998) 45^59 47 result in cell damage that may be responsible for the H. ducreyi to foreskin ¢broblasts in a dose-depend- development of ulcers. ent manner. In addition, proteinase K treatment of H. ducreyi adheres strongly to many cultured cell H. ducreyi signi¢cantly reduced attachment suggest- lines including HEp-2 (human laryngeal epidermoid ing protein involvement. It appeared that H. ducreyi carcinoma), CHO (Chinese hamster ovary), MRC-C binds to ¢bronectin in the extracellular matrix of (human embryo lung), C16 (clone of MRC-C), HeLa human foreskin ¢broblasts since ¢bronectin was (human cervical carcinoma), HEC-1-B (endometrial able to signi¢cantly reduce attachment. These au- adenocarcinoma), and A549 (human lung carcino- thors hypothesized that the attachment of H. ducreyi ma), to human foreskin cells, foreskin ¢broblasts, involves both a protein mediator (likely pili) as well and keratinocytes [4^10]. Cell invasion has been ob- as LOS and that one or both of these bacterial sur- served with some of these cell lines [3]. In vitro, all face components interacts with ¢bronectin to medi- the strains tested could survive and multiply on cell ate attachment to human foreskin ¢broblasts. monolayers, and a small fraction of bacteria could Downloaded from https://academic.oup.com/femsre/article/22/1/45/512698 by guest on 01 October 2021 also survive inside eukaryotic cells. However, be- 2.2. Haemophilus in£uenzae cause many cells, including epithelial cells, can phag- ocytose foreign particles, cell invasion may re£ect the H. in£uenzae is an important human pathogen phagocytic activity of the epithelial cells rather than worldwide. Non-encapsulated isolates, known as the invasive properties of the bacteria. H. ducreyi non-typable H. in£uenzae (NTHi), are a common adheres also to extracellular matrix proteins such cause of otitis media, sinusitis, conjunctivitis and as ¢brinogen, ¢bronectin, collagen, gelatin and lam- acute lower respiratory tract infections. Capsular inin [11]. type b isolates (Hib) cause invasive, bacteremic in- This microorganism expresses surface structures fections such as meningitis, septicemia, and epiglot- that resemble pili or ¢mbriae [12]. Although their titis, particularly in infants. H. in£uenzae is a typical role in adherence to host cells has not been demon- example of microorganisms expressing multiple ad- strated they seemed to be involved in binding to hesins [18,19]. laminin [11]. These ¢ne tangled pili are composed predominantly
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