Bacterial Adhesion to Animal Cells and Tissues
Authors: Itzhak Ofek, David L. Hasty, Ron J. DoyleCategory: Bacterial Pathogenesis
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The adhesion of bacteria to host cells is a critical event in the development of bacterial infections. Knowledge of the molecular mechanisms of this process is key to understanding an essential step in pathogenesis and to identifying potential targets for antimicrobial therapy.
This authoritative volume covers historical perspectives, general principles, methodologies, specific host cell and bacterial components associated with the process, including post-adhesion consequences, regulation of adhesion expression, and anti-adhesion therapy. The final chapter compiles, primarily in tabular format, a list of all the pathogenic bacterial species that were tested over the past ten years for their ability to adhere, the test substrata that were used, as well as the adhesions involved in the cases where they are known.
Bacterial Adhesion to Animal Cells and Tissues is an essential reference for students and investigators interested in host-pathogen interactions.
Electronic Only, 416 pages, illustrations, index.
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Chapter 1 : Basic Concepts in Bacterial Adhesion
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During the first several decades of intensified investigation of bacterial adhesion mechanisms, several fundamental principles were established. The contribution of hydrophobicity to bacterial adhesion to mucosal surfaces is probably underestimated because it is often responsible for the initial, weak and reversible interaction that is so difficult to measure. A key feature of bacterial adhesins is that they are associated with surface structures. It has recently been found that mannose derivatives can also be used to detect even intraspecies differences, such as differences among Escherichia coli isolates. Until recently, only lectins expressed on the surface of macrophages had been found to interact with complementary carbohydrates on bacterial surfaces. In all of these cases, the carbohydrate structures recognized by the macrophage lectins were contained in either the capsular polysaccharides or the lipopolysaccharides (LPS) of the outer membrane of gram-negative bacteria. The protein-protein type of interaction in bacterial adhesion is probably best exemplified by the interaction of fibronectin binding proteins and fibronectin on the animal cell surface. One of the fibronectin binding proteins, protein F1, binds fibronectin via domains that are 37 amino acids in length and repeated two to six times. The adhesin on Streptococcus aureus is a fibronectin binding protein, whereas one of the fibronectin-specific adhesins of S. pyogenes is lipoteichoic acid (LTA).
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Chapter 2 : Methodological Approaches to Analysis of Adhesins and Adhesion
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The study of mechanisms of adhesion vary from simple methods providing limited information to more complex methods that are difficult to perform and analyze but provide more meaningful information. This chapter discusses some of the most important methods and emphasizes the types of knowledge gained from the use of a specific method. Bacteria that exhibit increased hydrophobicity, as determined by the contact angle technique, are more readily engulfed by phagocytes, consistent with the notion that hydrophobicity is important in adhesion. Adhesion to microspheres can be determined by light microscopy, among many other techniques (enzyme-linked immunosorbent assay (ELISA) and use of radiolabeled bacteria). Hemagglutination reactions have been responsible for the initial identification of many lectin adhesins and were important in the characterization of adhesin-saccharide specificities, through the use of carbohydrate inhibitors of the reactions. In approaching important subjects such as affinity, the chapter mentions two basic types of experiments that can be performed. The usefulness of the kinetic approach is extended when experimental variables are manipulated. Methods have been developed to easily differentiate between extracellularly bound and internalized bacteria. One of simplest tests to determine whether an adhesin is expressed in vivo during a natural infection is to assay for antibodies against the adhesin in patient sera. Another relatively easy assay is to screen isolates from an infection for mRNA for an adhesin by reverse transcription-PCR.
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Chapter 3 : Target Tissues for Bacterial Adhesion
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A thorough understanding of cell and tissue biology is critical to the identification of the mechanisms of bacterial adhesion that operate within the host, especially in order to develop methods to selectively prevent pathogen adhesion. This chapter discusses some basic elements of cell biology that are relevant to bacterial adhesion. The distinction between membrane constituents as integral, peripheral, or belonging to the cell coat or extracellular matrix is based to some extent on the method required to dissociate the constituent in question from the cell membrane. The extracellular domains of integrins are located preferentially, but not exclusively, on basolateral surfaces of epithelial cells, where they bind to basal lamina components and other extracellular matrix macromolecules, while the cytoplasmic domains interact with cytoskeletal components and other cytoplasmic signaling partners. The peripheral membrane proteins and glycoproteins are anchored to the surface of the membrane by weak ionic interactions or by hydrogen bonding with integral constituents of the cell membranes, e.g., glycoproteins, glycolipids, or polar head groups of phospholipids. Some key examples of peripheral and extracellular components important for bacterial adhesion are discussed in the chapter. Changes are also bound to occur in cells exposed to the actions of drugs, some of which may affect the biosynthesis and expression of cell membrane constituents. Such changes have been best documented in carbohydrate residues of glycoproteins and glycolipids, largely due to the availability of specific lectin and gycosidase probes.
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Chapter 4 : Adhesins as Bacterial Cell Surface Structures: General Concepts of Structure, Biogenesis, and Regulation
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This chapter presents concise reviews of the general architectural plan of gram-positive and gram-negative cell surfaces. Within this context, a few specific examples are used to present basic concepts of the genetics of adhesin expression and adhesive organelle biogenesis. The adhesins of the gram-positive bacteria are anchored on the surface by four different mechanisms that include cell wall-anchoring mechanism, transmembrane mechanism, association of adhesins with surface proteins and the association of adhesins with surface glycolipids. The best described and probably the most prominent mechanism for anchoring adhesins is the cell wall-anchoring mechanism. The adhesins of the gram-negative bacteria are anchored on the outer membrane surface by four different mechanisms. The most widely used mechanism for fimbrial biogenesis appears to be the chaperone-usher pathway. This pathway is shared by many enterobacteria as well as some respiratory pathogens. Expression of type 1 fimbriae, as well as several other virulence factors, can also be affected in certain strains of E. coli by the excision of pathogenicity islands. Short peptides that inhibit quorumsensing mechanisms were found to inhibit S. aureus adhesion to epithelial cells as well as biofilm formation on medical device plastics. This is an interesting and promising new direction in the efforts to develop antiadhesion therapies for infectious diseases.
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Chapter 5 : Emerging Concepts in Bacterial Adhesion and Its Consequences
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It is becoming more and more evident that adhesins can exhibit biological functions other than bacterial adhesion but that may nevertheless play a crucial role in the infectious process. The concept that adhesins can have pathogenic activities other than in bacterial adhesion are illustrated by the proinflammatory properties of lipoteichoic acid (LTA). Because some of the additional biological functions are postulated to be directly related to the development of disease, it is expected that therapies based on neutralizing these functions would protect at multiple levels. Inhibition of adhesion by oligosaccharides and simple sugars continues to be a major method of identifying lectin adhesins and characterizing receptor specificities. The interaction of bacteria with phagocytic cells has been extensively studied, and the role of this interaction in host defense has been well documented. In the last decade, increased interest has been focused on mast cells, immune cells that are best known for their role in allergy and that have never previously been implicated in interactions with bacterial targets. The concept that bacterial clones are capable of producing multiple adhesins was established a number of years ago. Recent studies have not only confirmed this concept but have also shown that it is even more extensive than previously thought.
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Chapter 6 : Diversification of Receptor Specificities and Its Biological Consequences
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This chapter discusses concept and presents examples of the various mechanisms for receptor specificity diversification. The best-known examples of this type of variation are the pathogenicity islands (PAIs), which carry genes that encode adhesins with distinct receptor specificity, as well as genes that confer other specific aspects of pathogenicity. The changes in receptor specificity emerging from either acquisition or deletion of PAIs are usually much more pronounced than with allelic variation. The organisms express at least two families of adhesins, each of which can vary in its receptor specificity. The mechanism that controls the variation of the pilus shaft is gene rearrangement. Genomic DNA encodes one complete pilin gene and multiple copies of incomplete pilin genes. To better understand the biological consequences of the rapid change in receptor specificity, the chapter addresses how changes in two major adhesins expressed by E. coli, type 1 and P fimbrial bacterial adhesins, affect host and tissue tropism of the organism. The intraspecies diversities in the receptor specificities of FimH and PapG are due to allelic variations in the fimH and papG genes. In conclusion, the remarkable diversity in the fine sugar specificity of the type 1 and P fimbrial lectins clearly illustrates the concept that functional diversity of fimbrial lectins plays an important role in host tropism, tissue tropism, and infectivity.
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Chapter 7 : Entry of Bacteria into Nonphagocytic Cells
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Entry of bacteria into nonphagocytic cells (NPCs) has, perhaps more than any other postadhesion event, captured the interest of investigators within the field of host-pathogen interactions. There are three categories of bacterial growth in the presence of NPCs: obligate intracellular, facultative intracellular, and extracellular. The zipper mechanism of bacterial uptake is exemplified by Listeria monocytogenes and Yersinia spp. Proteins encoded by the mxi/spa locus appear to make up the secretion system, while the proteins encoded by the ipa operon are effectors. Internalin binds to E-cadherin, and invasin binds to β1-integrins. Currently, it appears that Shigella is example of the pathogenic organisms that utilize M cells to gain access to the subepithelial compartment. The invasome mechanism of entry has been described for Bartonella species, which are able to penetrate and multiply within both nucleated and nonnucleated cells. The fact that a large bacterial aggregate is an apparent requisite for triggering of internalization via this mechanism suggests that expression of the effector molecules may require a quorum-sensing signaling cascade. There is little clear-cut evidence to date that the entry of predominantly extracellular pathogens into NPCs in vitro truly reflects a process that is important in the pathophysiology of infections. However, the fact that this phenomenon has been described for such a large and growing list of pathogens suggests that it must play an important role in the overall survival of the species in a susceptible host.
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Chapter 8 : Postadhesion Events Induced in Nonphagocytic Cells
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This chapter focuses on contact-induced signaling of nonphagocytic cells (NPCs) as an immediate postadhesion event, and discusses two major events, one involving an immediate activation of cytoskeletal responses and the other involving activation of transcriptional responses. The former is needed for completion of internalization, while the latter results in the production of inflammatory mediators that can have a great systemic influence on the course of infection. While the cytoskeletal response is associated mainly with actual or abortive entry of bacteria into the cell, the transcriptional response may result either from adherent or from internalized bacteria. An adherent bacterium can transmit a transcriptional signal to nonphagocytic cells (NPCs) in two ways. One way is by using a specific secretory system to create a channel through which effector molecules can be passed into the host cell cytosol, and the second is by secreting effector molecules into the space between the bacterium and the cell, resulting in a relatively high concentration at the cell surface. In summary, considering the four types of activation mechanisms that include the high concentration mechanism, the association mechanism, the adhesin-dependent mechanism and the cooperativity mechanism, and the vast number of modulins produced by pathogenic bacteria, it appears that adhesion per se is only one prerequisite for a wide variety of potential subsequent reactions between the bacterium and target cell that influence the infectious process.
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Chapter 9 : Adhesion-Dependent Upregulation of Bacterial Genes
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There are many studies showing upregulation of genes in vivo. Whether adhesion is required for the activation of many these genes is not known. In a few cases, however, it has been shown that adhesion itself activates gene expression. The PilC1-mediated contact then activates the contact regulatory element of Neisseria (CREN) site within the promoter, which induces expression of bacterial genes for a second stage of the process. In this step, more PilC1 adhesin molecules are expressed, eventually leading to the presentation of PilC1 adhesin at the pilus tip. This step is followed by upregulation of the machinery for intimate attachment associated with attaching/effacing lesions and concomitant downregulation of pilus expression. A CREN-like element also participates in the intimate-adhesion step of the process. It appears that the Opc and Opa proteins may also be involved in some aspects of the adhesion process. The target cell receptor involved in PilC1-mediated adhesion is the CD46 glycoprotein. That the outer membrane form of PilC1 could mediate adhesion in vitro was shown by centrifuging nonpiliated bacteria onto epithelial cells. The few examples provided in this chapter show that this phenomenon does occur, but the true extent to which the process of adhesion activates bacterial gene expression remains to be more fully explored.
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Chapter 10 : Role of Adhesion in Biofilm Formation
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As bacterial adhesion is an indispensable component of biofilm formation, the factors involved in bacterium-substratum interactions are an important basis for understanding biofilm physiology. In fact, biofilm formation may be regarded as one of the most important sequelae of bacterial adhesion. This chapter discusses the advantages gained by bacteria from participation in a biofilm community, the mechanisms of biofilm formation, and attempts to block biofilm development in an effort to prevent infections. The chapter focuses on two types of medically important biofilms which have been extensively studied: hard tissue biofilms on tooth surfaces (i.e., dental plaque) and biomedical implant-associated biofilms. It is likely that there is an inverse relationship between the initial number of adherent bacteria required for biofilm formation and the avidity of the adhesion. The presence of this polysaccharide seems to be required for biofilm formation by strains of these organisms. This material appears to be the major constituent of the so-called slime, previously shown to be essential for biofilm formation by Staphylococcus epidermidis. The organisms produce another polysaccharide rich in galactose, which also contributes to biofilm formation. A type of quorum sensing used by many gram-negative bacterial species is the system involving acyl homoserine lactones. The dental biofilm is based on many bacterium-bacterium interactions, especially metal ion-requiring lectin-carbohydrate interactions. Infectious diseases associated with indwelling medical devices are now considered a major problem in health care. Some bacteria bind best to uncoated biomedical devices, and coating with various compounds can prevent bacterial adhesion.
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Chapter 11 : Antiadhesion Therapy
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This chapter provides a review of the various traditional approaches of antiadhesion therapy and immunity, including the usef of adhesin-based vaccines, receptor and adhesin analogs, sub-lethal concentrations of antibiotics, dietary constituents, and innate host-derived antiadhesion factors. The adhesin analog strategy is based on the assumption that the isolated adhesin molecule or its synthetic or recombinant fragment binds to the receptor and thereby competitively blocks adhesion of the bacteria. It has so far been impractical to use adhesin analogs in antiadhesion therapy because they are almost always macromolecules that must be employed in relatively high molar concentrations and they are available only in limited supply. In addition, careful consideration must be given to their toxicity and immunogenicity. Nevertheless, modern proteomics and recombinant biotechnology have permitted the development of unique types of relatively small peptides for antiadhesion therapy. The chapter talks about the studies performed to investigate the antiadhesion activities of cranberry materials. In a study it was found that cranberry extract inhibited the coaggregation between pairs of gram-negative oral bacteria more often than it did those between pairs of gram-positive bacteria. The target of the antiadhesive activity is the bacterial adhesin, not the animal cell receptors or human mucus. The most important host-derived components which potentially may provide innate immunity by inhibiting adhesion are those found associated with mucus on mucosal surfaces. The secretor or nonsecretor status of individuals is of particular interest in relation to their susceptibility to infection and the possible role of soluble adhesin receptors.
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Chapter 12 : Adhesins, Receptors, and Target Substrata Involved in the Adhesion of Pathogenic Bacteria to Host Cells and Tissues
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The study of adhesion during the 1960s, 1970s, and 1980s focused in large part on establishing the importance of this field of biological research. The molecules involved in adhesion have become clearly linked to infections, and information regarding their structure and molecular function is constantly growing. A section contains a tabulation of all of the studies of adhesion between January 1992 and December 2002 in which adhesins, receptors, and target substrata involved in the adhesion of pathogenic bacteria to host cells and tissues were performed. The species studied number almost 300, but it remains true that studies of the adhesion of Escherichia coli outnumber those of many of the other species combined. It is interesting that the number of adhesion studies performed for some of the pathogens does not reflect the clinical significance of the infections in each case. For many of those organisms which are being studied extensively, the numbers of putative adhesins and receptors identified have increased dramatically over the last 10 years compared to the previous decade. The studies cited here were essentially limited to those which involved adhesion tests of host cells or tissue components, materials of prosthetic devices, or other indwelling medical equipment. One table in this chapter includes only a very few studies of adhesion to foods (e.g., lettuce leaves) and essentially no studies of adhesion to food processing components (e.g., stainless steel tables) or to environmental materials (e.g., pipes in water-processing plants).
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