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Bacterial Adhesion to Cells and Tissues Bacterial Adhesion to Cells and Tissues J. ITZHAK OFEK AND RONALD DOYLE CHAPMAN & HALL New York· London First published in 1994 by Chapman & Hall One Penn Plaza New York, NY 10119 Published in Great Britain by Chapman & Hall 2-6 Boundary Row London SEI 8HN © 1994 Chapman & Hall, Inc. Softcover reprint of the hardcover 1st edition 1994 All rights reserved. No part of this book may be reprinted.or reproduced or utilized in any form or by any electronic, mechanical or other means, now known or hereafter invented, including photocopying and recording, or by an information storage or retrieval system, without permission in writing from the publishers. Library of Congress Cataloging in Publication Data Ofek, Itzhak Bacterial adhesion to cells & tissues 1 Itzhak Ofek and Ronald J. Doyle. p. cm. Includes bibliographical references and index. ISBN-13: 978-1-4684-6437-5 e-ISBN-13: 978-1-4684-6435-1 DOl: 10.1007/978-1-4684-6435-1 1. Bacteria-Adhesion. I. Doyle, Ronald J. II. Title. III. Title: Bacterial adhesion to cells and tissues. [DNLM: 1. Bacterial Adhesion. 2. Cell Adhesion. QW 52 D754b 1993] QR96.8.D68 1993 589.9'087'5-dc20 DNLM/DLC for Library of Congress 93-7370 CIP British Library Cataloguing in Publication Data Please send your order for this or any Chapman & Hall book to Chapman & Hall, 29 West 35th Street, New York, NY 10001, Attn: Customer Service Department. You may also call our Order Department at 1-212-244-3336 or fax your purchase order to 1-800-248-4 724. For a complete listing of Chapman & Hall's titles, send your requests to Chapman & Hall, Dept. BC, One Penn Plaza, New York, NY 10119. Dedication In Memory of a Friend: Edwin H. Beachey, M.D. We dedicate this book to the memory of our friend, Ed Beachey. It seems almost impossible that we live in a world without Ed, who was a victim of cancer in 1989 at a relatively young age. Our dedication of this book to Ed attests to our personal respect for and friendship with him. When Ed was a medical student at Northwestern University, he became ill with rheumatic fever, a sequellae to a streptococcal infection. His attending physician, Gene Stollerman, proved to be such an influence on Ed that he dedicated his career to the study of streptococcal diseases. Most individuals who study this book will immediately recognize the contributions Ed made to streptococcal adhesion. They will also recognize the name of Ed as a leader in microbial adhesion mechanisms of other bacterial pathogens. In fact, in a review article he wrote in the early 1980s for the Journal of Infectious Diseases, Ed captured the most important principles of bacterial adhesion to soft and hard tissues, including the role of adhesion in pathogenesis. The article was especially important in its presentation of basic molecular methodology to study bacterial adhesion. It is not surprising that this review became a Citation Classic and continues to be well-cited. Ed Beachey grew in stature in the scientific world from the early 1970s to the late 1980s, and his remarkable abilities seemed to emerge more and more from year to year. Young scientists from around the world found a way to visit Ed in Memphis. In spite of demands for teaching, clinical rounds, grants, paper writing, writing of reviews, refereeing, scientific study sections and other respon sibilities, Ed always was a gracious host. We do not know of other individuals who have so assiduously devoted themselves to the course of science. Although Ed has been gone for more than three years, we retain a fond and respectful memory of him. His fundamental work on bacterial adhesion will continue to inspire us and others for generations to come. Long live the legacy of Ed Beachey. v Contents Dedication v Preface ix Chapter 1. Principles of Bacterial Adhesion Chapter 2. Methods, Models, and Analysis of Bacterial Adhesion 16 Chapter 3. Animal Cell Membranes as Substrata for Bacteria Adhesion 41 Chapter 4. Relationship Between Bacterial Cell Surfaces and Adhesins 54 Chapter 5. Bacterial Lectins as Adhesins 94 Chapter 6. Gram-Positive Pyogenic Cocci 136 Chapter 7. Interaction of Bacteria with Phagocytic Cells 171 Chapter 8. Adhesion of Bacteria to Oral Tissues 195 Chapter 9. Regulation and Expression of Bacterial Adhesins 239 Chapter 10. Recent Developments in Bacterial Adhesion to Animal Cells 321 Chapter 11. Common Themes in Bacterial Adhesion 513 Index 563 vii Preface Systematic studies on bacterial adhesion began about three decades ago. By the mid 1980s, there were approximately 500 publications per year on adhesion and its relationship to pathogenesis, a level that has been sustained. The emer gence of recombinant DNA technology, gene cloning, and rapid DNA sequencing methods and the development of reliable assays for bacterial adhesion have resulted in a shift of research eff0rts aimed toward an understanding of the molecular mechanisms of adhesin regulation. Concomitantly, new techniques have been developed to identify and isolate adhesin receptors. This volume emphasizes three general areas of adhesion of pathogenic bacteria: (1) A review of the most extensively studied bacteria, especially Escherichia coli, describing the molecular mechanisms of adhesion. Chapters dealing with pyogenic Gram-positive cocci and oral bacteria as well as detailed chapters on the biogenesis and regulation of adhesins are also included. (2) The recognition of common themes in adhesion is made clear at several locations in the text. One chapter devotes considerable space to the common themes of bacterial adhesion. (3) The final area is concerned with data treatment, methods in adhe sion, principles of adhesion, and composition of surfaces of bacteria and eucary otic cell receptors. Additional chapters deal with lectins as adhesins and with adhesion in nonopsonic phagocytosis. In general, we have attempted to present views dealing with mechanisms of bacterial adhesion and its regulation, focusing on bacteria that have been studied in detail at the molecular level. We wish to express our gratitude to the late Ed Beachey for stimulating discussions and for support and encouragement in convincing us to write this book. We also thank the numerous granting agencies that have supported our research, including the NIDR-NIH, March of Dimes (Ohio Valley), US-Israel Bi-Nat Science Foundation, the US Army R&D Command, and the V A hospital system. Finally, much credit is due to Administra tive Assistant Atha Carter and typist Kim Hayes. I. Ofek, Tel-Aviv R.I. Doyle, Louisville, KY ix Bacterial Adhesion to Cells and Tissues 1 Principles of Bacterial Adhesion Certain fundamental aspects of bacterial adhesion have been known for years (reviewed in Marshall, 1976; Ellwood et aI., 1979; Beachey, 1980a, b; Berkeley et aI., 1980; Bitton and Marshall, 1980; Beachey et aI., 1982; Schlessinger, 1982; Jones and Isaacson, 1984; Marshall, 1984; Mergenhagen and Rosan, 1985; Savage and Fletcher, 1985; Lark et aI., 1986). More discussions on various fundamental aspects can also be found in other selected books (Boedeker, 1984; Mirelman, 1986; Switalski et aI., 1989; Doyle and Rosenberg, 1990; Hook and Switalski, 1992). During the first decade of intense research on the adhesion of microorganisms to various substrata a number of points had become clear. One, there is little doubt that the survival of microorganisms in various niches is dependent on their ability to adhere to surfaces or substrata. Second, the adhesion process involves an interaction between complementary molecules on the respec tive surfaces of the microbe and the substratum. Third, the expression by the organisms of the macromolecules that participate in the adhesion process is under a number of regulatory control mechanisms. During the second decade of research most of the efforts have been focused on molecular mechanisms (fine specificity and genetic control) and consequences of the adhesion phenomenon, with the premise that the process of microbial adhesion may be specifically manipulated. In this first chapter the fundamental principles that have emerged from studies performed during the last two decades are reviewed, with an emphasis on how bacteria adhere to biological substrata, the importance of adhesion in infectious processes, and the basic genetic and phenotypic variables affecting adhesion. A summary of common terms that are now widely used and have become prominent in the concepts developed in the study of bacterial adhesion is given in Table 1-1. The chapters that follow provide more in-depth discussion of the molecular nature of adhesins and their receptors. In addition, thorough reviews of the genetic regulation of adhesins are presented, along with an appraisal of the 1 Table 1-1. Explanation of terms in bacterial adhesion Adhesion The measurable union between a bacterium and a substratum. A bacterium is (or adherence) said to have adhered to a substratum when energy is required to separate the bacterium from the substratum. Adhesin A surface molecule of a bacterium capable of binding to a receptor on a substratum. Most bacterial species express more than one type of adhesin. An adhesin site is a region of the adhesin molecule engaged in stereospecific interaction with a receptor. In some cases, an adhesin may possess two or more distinct adhesin sites specific for two distinct receptors. Amorphin Amorphous appearing materials observed on the surfaces of some bacteria. Amorphin does not appear to possess regular repeating structures and may be composed of protein and/or polysaccharide. Association An encounter between a bacterium and a substratum that may lead to adhesion of the bacterium without specification of mechanism. Capsule Secreted polymers, usually acidic polysaccharide, that have a tendency to remain cell associated and may participate in adhesive events. Capsule-like proteins have been implicated as adhesins in a few bacteria. Colonization Bacterial growth at a site following adhesion of bacteria on the site. Cryptitope Latent receptor for a bacterial adhesin. The cryptitope may be made available as a receptor by proteolysis, heat, or other treatments. Deposition Bacteria adhering to a substratum during fluid movement. Fibrillae Appendages, consisting of protein subunits, emanating from the wall or membrane compartments of Gram-positive or Gram-negative bacteria. The fibrillae are usually shorter than fimbriae and are usually of an indeterminant diameter. Fibrillae carry adhesins in a not well understood manner. Fimbriae Appendages, consisting of protein subunits that are anchored in the outer or pili membrane of Gram-negative bacteria or the cytoplasmic membrane or cell wall of Gram-positive bacteria. Fimbriae may be tubular (rigid) or flexible. Rigid fimbriae are usually 6-10 nm in diameter and carry adhesins at their tips and in some cases along their sides as well. Flexible fimbriae are thin (usually < 5 mm in diamater) and usually carry adhesins along their entire length. Glycocalyx The outer coating of polysaccharide possessed by some bacteria. Some refer to capsule or cell-associated slime as a glycocalyx. Hydrophobic A name given for the tendency of apolar molecules to adhere or bind to each effect other. A hydrophobic molecule has a greater tendency to adhere to another apolar molecule than to water. Hydrophobins Apolar molecules on bacterial surfaces involved in adhesion. Isolectins Proteins with identical function and specificity but differing slightly in amino acid composition. Isoreceptor A form of an adhesin receptor that differs in composition from another receptor with similar function and stereochemical arrangements. Lectin A carbohydrate binding protein of nonimmune origin. Many bacteria employ surface lectins as adhesins. continued 2 Principles of Bacterial Adhesion / 3 Table 1-1. continued Ligand Molecules complementary to adhesin or receptor. MATH Acronym for microbial adhesion to hydrocarbons Microbioadh Association between microorganisms leading to aggregation or cohesion. Small cocci adhering with rod-shaped bacteria form aggregating pairs referred to as "com cobs," a term also employed for other interacting bacteria. Microbioadh is a replacement for com cobs and includes all coaggregating microorganisms. Nonspecific An association between the bacterium and a substatum that does not require a adhesion precise stereochemical fit. The same forces involved in the specific adhesion are also involved in nonspecific adhesion. Pellicle A coated surface. Salivary pellicles consist of saliva-coated surfaces. The term "conditioned" surface is a synonym for pellicle that is most often used in environmental adhesion. RGD An amino acid sequence, arginine-glycine-aspartic acid, found in the primary structure of proteins or glycoproteins of host (e.g., fibronectin) or bacterial origin and recognized by integrin molecules on many types of animal cell surfaces. Some bacteria (invasin-bearing Yersinia) adhere to animal cells via an RGD-dependent interaction. Receptor A substratum molecule that is complementary to an adhesin. In some cases the distinction between "receptor" and "adhesin" cannot be made and the terms may be used interchangeably. A receptor site (attachment site) is a defined region of the substratum molecule engaged in stereospecific interaction with the adhesin. In some cases a receptor may have two distinct receptor sites for two distinct adhesins. Slimectin Soluble secreted polymers, usually acidic polysaccharide, involved in adhesion; to be distinguished from "slime," a name reserved for noncapsular secreted polymers of similar structures not involved in adhesion phenomena. Specific adhesion An association between a bacterium and a substratum that requires rigid stereochemical constraints. Specific adhesion may require hydrogen bond formation, ion-ion pairing, or the hydrophobic effect. Substratum A surface bearing receptors for bacterial adhesins. Tropism The apparent tendency of bacterium to colonize a specific tissue. Some bacteria are found in high numbers in buccal mucosal cells, so the bacteria are said to have a tropism for those cells. Tropism is a result of many host and bacterial factors, one of which is adhesion. biological significance of the adhesion process. Finally, recent advances on adhesion of the most widely studied pathogens are provided. How Bacteria Adhere Bacteria adhere only to complementary substrata. They adhere by ionic or Cou lombic interactions, by hydrogen bonding (Pimental and McClellan, 1990), by the hydrophobic effect (Duncan-Hewitt, 1990), and by coordination complexes
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