Abstract
The adhesion of bacteria to mucosal surfaces has been the focus of study in several laboratories around the world during the past decade and the results have led to a better understanding of the interactions between animal hosts and microbes. The study of bacterial adhesion to animal cells has been stimulated, in part, by the recognition of the importance of these processes in the pathogenesis of diseases caused by bacteria. As such, most of the ensuing discussion will be based on the data obtained from studies of disease pathogenesis. In particular, I shall use as primary examples, results from studies on the pathogenesis of enterotoxigenic Escherichia coli diarrheal disease and E. coli-induced urinary tract infections as these provide the most extensively studied examples of bacterial adhesion to animal cells. The initiation of most bacterial infections of mucosal surfaces requires the bacterial species in question to colonize and maintain a stable population at the mucosal site. In the cases of pathogenic E. coli, colonization is facilitated by adhesion to the mucosa, the adhesion being mediated by bacterial structures called pili. The following discussion will describe in detail the molecular basis of pilus-mediated bacterial adhesion to mucosal surfaces (animal cells). Although the structure and function of pili will be emphasized, the recognition and specificity of receptors on the animal cells is critical and will also be described (see Chapter 4, Section 4).
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Acres, S. D., Isaacson, R. E., Babiuk, L. A., and Kapitany, R. A., 1979, Immunization of calves against enterotoxigenic colibacillosis by vaccinating dams with purified K99 antigen and whole cell bacterins, Infect.Immun. 25:121–126.
Arbuckle, J. B. R., 1970, The location of Escherichia coli in the pig intestine, J. Med. Microbiol. 3:333–340.
Bak, A. L., Christiansen, G., Christiansen, C., Stenderup, A., Ørskov, I., and Ørskov, F., 1972, Circular DNA molecules controlling synthesis and transfer of the surface antigen (K88) in Escherichia coli, J. Gen. Microbiol. 73:373–385.
Barnum, D. A., Glantz, P. J., and Moon, H. W., 1967, Colibacillosis, Ciba Veterninary Monograph Series 2, Ciba Pharmaceutical Company, Summit, N.J.
Bertschinger, H. V., Moon, H. U., and Whipp, S. C., 1972, Association of Escherichia coli with the small intestinal epithelium. I. Comparison of enteropathogenic and nonenteropathogenic porcine strains in pigs, Infect. Immun. 5:595–605.
Brinton, C. C., 1959, Non-flagellar appendages of bacteria, Nature (London) 183:782–786.
Brinton, C. C., 1965, The structure, function, synthesis and genetic control of bacterial pili and a molecular model for DNA and RNA transport in gram negative bacteria, Trans. N.Y. Acad. Sci. 27:1003–1054.
Brinton, C. C., 1971, The properties of sex pili, the viral nature of “conjugal” genetic transfer systems, and some possible approaches to the control of bacterial drug resistance, Crit. Rev. Microbiol. 1:105–160.
Brinton, C. C., Gemski, P., Falkow, S., and Baron, L. S., 1961, Location of the piliation factor on the chromosome of Escherichia coli, Biochem. Biophys. Res. Commun. 5:293–298.
Brinton, C. C., Bryan, J., Dillon, J. A., Guerina, N., and Jacobsen, J., 1978, Uses of pili in gonorrhoea control: Role of bacterial pili in disease, purification and properties of gonococcal pili, and progress in the development of a gonococcal pilus vaccine for gonorrhoea, in: Immunobiology of Neisseria gonorrhoeae (G. F. Brooks, E. C. Gotschlich, K. K. Holmes, W. D. Sawyer, and F. E. Young, eds.), American Society for Microbiology, Washington, D.C., pp. 155–178.
Buchanan, T. M., 1975, Antigenic heterogeneity of gonococcal pili, J. Exp. Med. 141:1470–1475.
Cheney, C. P., and Boedeker, E. C., 1984, Appearance of host intestinal receptors for pathogenic E. coli with age, in: Attachment of Organisms to the Gut Mucosa, Vol. II (E. C. Boedecker, ed.), CRC Press, Boca Raton, pp. 157–166.
Cisar, J. O., and Vatter, A. E., 1979, Surface fibrils (fimbriae) of Actinomyces viscosus T14V, Infect. Immun. 24:523–531.
Dean, E. A., and Isaacson, R. E., 1982, In vitro adhesion of piliated Escherichia coli to small intestinal villous epithelial cells from rabbits and the identification of a soluble 987P pilus receptor-containing fraction, Infect.Immun. 36:1192–1198.
Dean, E. A., and Isaacson, R. E., 1985, Purification and characterizaton of a receptor for the 987P pilus of Escherichia coli, Infect. Immun. 47:98–105.
deGraaf, F. K., and Roorda, I., 1982, Production, purification, and characterization of the fimbrial adhesive antigen F41 isolated from calf enteropathogenic Escherichia coli strain B41M, Infect. Immun. 36:751–753.
deGraaf, F. K., Boor, P. K., and vanHess, J. E., 1980, Biosynthesis of the K99 surface antigen is repressed by alanine, Infect. Immun. 30:125–128.
deGraaf, F. K., Klemm, P., and Gaastra, W., 1981, Purification, characterization, and partial covalent structure of Escherichia coli adhesive antigen K99, Infect. Immun. 33:877–883.
Dobson, W. J., and McCurdy, H. D., 1979, The function of fimbriae in Myxococcus xanthus. I. Purification and properties of M. xanthus fimbriae, Can. J. Microbiol. 25:1152–1160.
Dougan, G., David, G., and Kehoe, M., 1983, Organization of K88ac encoded polypeptides in the Escherichia coli cell envelope: Use of minicells and outer membrane protein mutants for studying assembly of pili, J. Bacteriol. 153:364–370.
Duguid, J. P., and Old, D. C., 1980, Adhesive properties of Enterobacteriaceae, in: Bacterial Adherence (E. H. Beachey, ed.), Chapman & Hall, London, pp. 185–217.
Duguid, J. P., Smith, I. W., Dempster, G., and Edmunds, P. N., 1955, Non-flagellar filamentous appendages (“fimbriae”) and haemagglutinating activity in Bacterium coli, J. Pathol. Bacteriol. 70:335–348.
Eisenstein, B. I., 1981, Phase variation of type 1 fimbriae in Escherichia coli is under transcriptional control, Science 214:337–339.
Eshdat, Y., Silverblatt, F. J., and Sharon, N., 1981, Dissociation and reassembly of Escherichia coli type 1 pili, J.Bacteriol. 148:308–314.
Fader, R. C., Duffy, L. K., Davis, C. P., and Kurosky, A., 1982, Purification and chemical characterization of type 1 pili isolated from Klebsiella pneumoniae, J. Biol. Chem. 257:3301–3305.
Freter, R., Allweiss, B., O’Brien, P. C. M., Halstead, S. A., and Macsai, M. S., 1981, Role of chemotaxis in the association of mobile bacteria with intestinal mucosae: In vitro studies, Infect. Immun. 34:241–249.
Froholm, L. O., and Sletten, K., 1977, Purification and N-terminal sequence of fimbrial protein from Moraxellanonliquifaciens, FEBS Lett. 73:29–32.
Gaastra, W., and deGraaf, F. K., 1982, Host-specific fimbrial adhesins of noninvasive enterotoxigenic Escherichiacoli strains, Microbiol. Rev. 46:129–161.
Gaastra, W., Klemm, P., Walker, J. M., and deGraaf, F. K., 1979, K88 fimbrial proteins: Amino and carboxyl terminal sequences of intact proteins and cyanogen bromide fragments, FEMS Microbiol. Lett. 6:15–18.
Gibbons, R. A., Jones, G. W., and Sellwood, R., 1975, An attempt to identify the intestinal receptor for the K88 adhesin by means of a haemagglutination inhibition test using glycoproteins and fractions from sow colostrum, J. Gen. Microbiol. 86:228–240.
Gorbach, S. L., Kean, B. H., Evans, S. G., Evans, D. J., andBessudo, D., 1975, Travelers’ diarrhea and toxigenic Escherichia coli, N. Engl. J. Med. 292:933–936.
Gubish, E. R., Chen, K. D. S., and Buchanan, T. M., 1982, Attachment of gonococcal lectin-resistant clones of Chinese hamster ovary cells, Infect. Immun. 37P:189–194.
Guinée, P. A. M., and Jansen, W. H., 1979, Behavior of Escherichia coli antigens K88ab, K88ac, and K88ad in immunoelectrophoresis, double diffusion and hemagglutination, Infect. Immun. 23:700–705.
Guinée, P. A. M., Veldkamp, J., and Hansen, W. H., 1977, Improved Minca medium for the dilution of K99 antigen in calf enterotoxigenic strains of Escherichia coli, Infect. Immun. 15:676–678.
Guinée, P. A. M., Mooi, F. R., and Jansen, W. H., 1980, Preparation of specific Escherichia coli K88 antisera by means of purified K88ab and K88ad antigens, Zentralbl. Bakteriol. Parasitenkd. Infektionskr. Hyg. Abt. 1Orig. Reihe A 248:182–189.
Heckels, J. E., 1982, Role of surface proteins in pathogenic adhesion, in: Microbiology 1982 (D. Schlessinger, ed.), American Society for Microbiology, Washington, D.C., pp. 301–304.
Hermodson, M. H., Chen, K. C. S., and Buchanan, T. M., 1978, Neisseria pili proteins: Aminoterminal amino acid sequences and identification of an unusual amino acid, Biochemistry 17:442–445.
Hull, R. A., Gill, R. E., Hsu, P., Minshew, B., and Falkow, S., 1981, Construction and expression of recombinant plasmids encoding type 1 or d-mannose-resistant pili from a urinary tract infection Escherichia coli isolate, Infect. Immun. 33:933–938.
Isaacson, R. E., 1977, K99 surface antigen of Escherichia coli: Purification and partial characterization, Infect.Immun. 15:272–279.
Isaacson, R. E., 1980a, Pili of enterotoxigenic Escherichia coli, In: Third International Symposium on NeonatalDiarrhea (S. Acres, ed.), Veterinary Infectious Disease Organization, Saskatoon, pp. 213–236.
Isaacson, R. E., 1980b, Factors affecting expression of the Escherichia coli pilus K99, Infect. Immun. 28:190–194.
Isaacson, R. E., 1983, Regulation of expression of the Escherichia coli pilus K99, Infect. Immun. 40:633–639.
Isaacson, R. E., and Richter, P., 1981, Escherichia coli 987P pilus: Purification and partial characterization, J.Bacteriol. 146:784–789.
Isaacson, R. E., Nagy, B., and Moon, H. W., 1977, Colonization of porcine small intestines by Escherichia coli: Colonization and adhesion factors of pig enteropathogens that lack K88, J. Infect. Dis. 135:531–539.
Isaacson, R. E., Moon, H. W., and Schneider, R. A., 1978a, Distribution and virulence of Escherichia coli in the small intestines of calves with and without diarrhea, Am. J. Vet. Res. 39:1750–1755.
Isaacson, R. E., Fusco, P. C., Brinton, C. C., and Moon, H. W., 1978b, In vitro adhesion of Escherichia coli to porcine small intestinal epithelial cells: Pili as adhesive factors, Infect. Immun. 21:392–397.
Isaacson, R. E., Dean, E. A., Morgan, R. L., and Moon, H. W., 1980, Immunization of suckling pigs against enterotoxigenic Escherichia C(?/z-induced diarrheal disease by vaccinating dams with purified K99 or 987P pili: Antibody production in response to vaccination, Infect. Immun. 29:824–826.
Isaacson, R. E., Colmenero, J., and Richter, P., 1981, Escherichia coli K99 pili are composed of one subunit species, FEMS Microbiol. Lett. 12:229–232.
Isaacson, R. E., Betzold, J. A., and Petre, J. O., 1984, Cloning, genetic organization, and expression of the Escherichia coli pilus K99, J. BacterioL, Submitted.
Jann, K., Jann, B., and Schmidt, G., 1981, SDS polyacrylamide gel electrophoresis and serological analysis of pili from Escherichia coli of different pathogenic origin, FEMS Microbiol. Lett. 11:21–25.
Jones, G. W., and Isaacson, R. E., 1983, Proteinaceous bacterial adhesins and their receptors, CRC Crit. Rev.Microbiol. 10:229–260.
Jones, G. W., and Rutter, J. M., 1972, Contribution of the K88 antigen of Escherichia coli to enteropathogenicity: In the pathogenesis of neonatal diarrhea caused by Escherichia coli in piglets, Am. J. Clin. Nutr. 278:1414–1419.
Jones, G. W., and Rutter, J. M., 1974, Role of the K88 antigen. Protection against disease by neutralizing the adhesive properties of K88 antigen, Infect. Immun. 6:918–927.
Kehoe, M., Sellwood, R., Shipley, P. L., and Dougan, G., 1981, Genetic analysis of K88-mediated adhesion of enterotoxigenic Escherichia coli, Nature (London) 291:122–126.
Klemm, P., 1979, Fimbrial colonization factor CFA/1 protein from human enteropathogenic Escherichia coli strains, FEBS Lett. 108:107–110.
Klemm, P., 1981, The complete amino acid sequence of the K88 antigen—A fimbrial protein from Escherichiacoli, Eur. J. Biochem. 117:617–627.
Klemm, P., Ørskov, I., and Ørskov, F., 1982, F7 and type 1-like fimbriae from three Escherichia coli strains isolated from urinary tract infections: Protein, chemical and immunological aspects, Infect. Immun. 36:462–468.
Korhonen, T., Nurmiaho, E.-L., Ranta, H., and Svanborg-Eden, C., 1980a, New method for isolation of immuno-logically pure pili from Escherichia coli, Infect. Immun. 27:569–575.
Korhonen, T. K., Lownatma, K., Ranta, H., and Kwasi, N., 1980b, Characterization of the type 1 pili of Salmonella typhimurium LT2, J. Bacteriol. 144:800–805.
Kumazawa, N., and Yanogawa, R., 1972, Chemical properties of the pili of Corynebacterium renale, Infect.Immun. 5:27–30.
Lambden, P. R., Robertson, J. N., and Watt, P. J., 1981, The preparation and properties of a and p pili from variants of Neisseria gonorrhoeae P9, J. Gen. Microbiol. 124:109–116.
Leffler, H., and Svanborg-Eden, C., 1980, Chemical identification of a glycosphingolipid receptor of Escherichiacoli attaching to human urinary tract epithelial cells and agglutinating human erythrocytes, FEMS Microbiol.Lett. 8:127–134.
Lindahl, M., Faris, A., Wastrom, T., and Hjerton, S., 1981, A new test based on “salting out” to measure relative surface hydrophobicity of bacterial cells, Biochim. Biophys. Acta 677:471–476.
Lomberg, H., Jodal, U., Svanborg-Eden, C., Leffler, H., and Samuelsson, B., 1981, P1 blood group and urinary tract infection, Lancet 1:551–552.
McConnell, M. M., Smith, H. R., Willshaw, G. A., Field, A. M., and Rowe, B., 1981, Plasmids coding for colonization factor antigen I and heat-stable enterotoxin production isolated from enterotoxigenic Escherichiacoli: Comparison of their properties, Infect. Immun. 32:927–936.
McGee, Z. A., Stephens, D. S., Melly, M. A., Gregg, C. R., Schlech, W. F., and Hoffman, L. H., 1982, Role of attachment in the pathogenesis of disease caused by Neisseria gonorrhoeae and Neisseria meningitis, in: Microbiology 1982 (D. Schlessinger, ed.), American Society for Microbiology, Washington, D.C., pp. 292–295.
McMichael, J. C., and Ou, J. T., 1979, Structure of common pili from Escherichia coli, J. Bacteriol. 138:969–975.
MacRae, T. H., Dobson, W. J., and McCurdy, H. D., 1977, Fimbriation in gliding bacteria, Can. J. Microbiol. 23:1096–1108.
Mayer, L. W., Holmes, K. K., and Falkow, S., 1974, Characterization of plasmid deoxyribonucleic acid from Neisseria gonorrhoeae, Infect. Immun. 10:712–717.
Meyer, T. F., Mlawer, N., and So, M., 1982, Pilus expression in Neisseria gonorrhoeae involves chromosomal rearrangement, Cell 30:45–52.
Mooi, F. R., and deGraaf, F. K., 1979, Isolation and characterization of K88 antigens, FEMS Microbiol. Lett. 5:17–20.
Mooi, F. R., deGraaf, F. K., and van Embden, J. D. A., 1979, Cloning, mapping and expression of the genetic determinant that encodes for the K88ab antigen, Nucleic Acids Res. 6:849–865.
Mooi, F. R., Harms, N., Bakker, D., and deGraaf, F. K., 1981, Organization and expression of genes involved in the production of the K88ab antigen, Infect. Immun. 32:1155–1163.
Mooi, F. R., Wyfjes, A., and deGraaf, F. K., 1983, Identification and characterization of precursors in the biosynthesis of the K88ab fimbria of Escherichia coli, J. Bacteriol. 154:41–49.
Moon, H. W., Nagy, B., and Isaacson, R. E., 1977, Intestinal colonization and adhesion by enterotoxigenic Escherichia coli: Some ultrastructural observations on adherence to ileal epithelium of the pig, J. Infect. Dis. 136:S124–S129.
Moon, H. W., Kohler, E. M., Schneider, R. A., and Whipp, S. C., 1980, Prevalence of pilus antigens, enterotoxin types and enteropathogenicity among K88-negative enterotoxigenic Escherichia coli from neonatal pigs, Infect. Immun. 27:222–230.
Morgan, R. L., Isaacson, R. E., Moon, H. W., Brinton, C. C., and To, C. C., 1978, Immunization of suckling pigs against enterotoxigenic Escherichiacoli-induced diarrheal disease by vaccinating dams with purified 987 or K99 pili: Protection correlates with pilus homology of vaccine and challenge, Infect. Immun. 22:771–777.
Nagy, B., Moon, H. W., and Isaacson, R. E., 1976, Colonization of porcine small intestines by Escherichia coli: Ileal colonization and adhesion by pig enteropathogens that lack K88 antigen and by some acapsular mutants, Infect. Immun. 13:1214–1220.
Nagy, B., Moon, H. W., and Isaacson, R. E., 1977, Colonization of porcine intestine by enterotoxigenic Escherichia coli: Selection of piliated forms in vivo, adhesion of piliated forms to epithelial cells in vitro, andincidence of a pilus antigen among porcine enteropathogenic E. coli, Infect. Immun. 16:344–352.
Nagy, B., Moon, H. W., Isaacson, R. E., To, C. C., and Brinton, C. C., 1978, Immunization of suckling pigs against enterotoxigenic Escherichia coli infection by vaccinating dams with purified pili, Infect. Immun. 21:269–274.
Nozaki, L., and Tanford, C., 1971, The solubility of amino acid and two glycine peptides in aqueous ethanol and dioxane solutions, J. Biol. Chem. 246:2211–2217.
Old, D. C., 1972, Inhibition of the interaction between fimbrial hemagglutinins and erythrocytes by d-mannose and other carbohydrates, J. Gen. Microbiol. 71:149–157.
Old, D. C., and Duguid, J. P., 1970, Selective outgrowth of fimbriate bacteria in static medium, J. Bacteriol. 103:447–456.
Old, D. C., Cornell, I., Gibson, L. F., Thomson, A. D., and Duguid, J. P., 1968, Fimbriation pellicle formation and the amount of growth of Salmonella in broth, J. Gen. Microbiol. 51:1–16.
Ørskov, I., Ørskov, F., and Birch-Andersen, A., 1980, Comparison of Escherichia coli fimbrial antigen F7 with type 1 fimbriae, Infect. Immun. 27:657–666.
Ottow, J. C. G., 1975, Ecology, physiology and genetics of fimbriae and pili, Annu. Rev. Microbiol. 29:79–108.
Paranchych, W., Frost, L. S., and Carpenter, M., 1978, N-terminal amino acid sequence of pilin isolated from Pseudomonas aeruginosa, J. Bacteriol. 134:1179–1180.
Paranchych, W., Sastry, P. A., Frost, L. S., Carpenter, M., Armstrong, G. D., and Watts, T. H., 1979, Biochemical studies on pili isolated from Pseudomonas aeruginosa strain PAO, Can. J. Microbiol. 25:1175–1181.
Pearce, W. A., and Buchanan, T. M., 1980, Structure and cell membrane-binding properties of bacterial fimbriae, in: Bacterial Adherence (E. H. Beachey, ed.), Chapman & Hall, London, pp. 289–343.
Pethica, B. A., 1980, Microbial and cell adhesion, in: Microbial Adhesion to surfaces (R. C. W. Berkeley, J. M. Lynch, J. Melling, P. R. Rutter, and B. Vincent, eds.), Horwood, Chichester, pp. 19–45.
Pierce, J., and Clegg, S., 1983, Identification of the genetic determinants coding for expression of mannose-resistant fimbriae of Escherichia coli, Abstr. Annu. Meet. Am. Soc. Microbiol. B46.
Robertson, J. N., Vincent, P., and Ward, M. E., 1977, The preparation and properties of gonococcal pili, J. Gen.Microbiol. 102:169–177.
Rutter, J. M., Burrows, M. R., Sellwood, R., and Gibbons, R. A., 1975, A genetic basis for resistance to enteric disease caused by E. coli, Nature (London) 257:135–136.
Rutter, P. R., and Vincent, B., 1980, The adhesion of microorganisms to surfaces: Physicochemical aspects, in: Microbial Adhesion to Surfaces (R. C. W. Berkeley, J. M. Lynch, J. Melling, P. R. Rutter, and B. Vincent, eds.), Horwood, Chichester, pp. 79–92.
Schoolnik, G. K., 1982, Mechanism of binding of gonococcal pili, in: Microbiology 1982 (D. Schlessinger, ed.), American Society for Microbiology, Washington, D.C., pp. 312–316.
Sellwood, R., 1980, The interaction of the K88 antigen with porcine intestinal epithelial cell brush-borders, Biochim. Biophys. Acta 632:326–335.
Sellwood, R., Gibbons, R. A., Jones, G. W., and Rutter, J. M., 1975, Adhesion of enteropathogenic Escherichiacoli to pig intestinal brush-borders: The existence of two pig phenotypes, J. Med. Microbiol. 8:405–411.
Shipley, P. L., Gyles, C. L., and Falkow, S., 1978, Characterization of plasmids that encode for the K88 colonization antigen, Infect. Immun. 20:559–566.
Shipley, P. L., Dougan, G., and Falkow, S., 1981, Identification and cloning of the genetic determinant that encodes for the K88ac adherence antigen, J. Bacteriol. 145:920–925.
Silverman, M., and Simon, M., 1980, Phase variation: Genetic analysis of switching mutants, Cell 19:845–854.
Smith, H. W., and Linggood, M. A., 1971a. Further observations on Escherichia coli enterotoxins with particular regard to those produced by atypical piglet strains and by calf and lamb strains: The transmissible nature of these enterotoxins and of a K antigen possessed by calf and lamb strains, J. Med. Microbiol. 5:243–250.
Smith, H. W., and Linggood, M. A., 1971b, Observations on the pathogenic properties of the K88, Hly, and Ent plasmids of Escherichia coli with particular reference to porcine diarrhea, J. Med. Microbiol. 4:467–485.
Smyth, C., Jonsson, P., Olsson, E., Söderlünd, O., Rosengren, J., Hjesten, S., and Wadstrom, T., 1978, Differences in hydrophobic surface characteristics of porcine enteropathogenic Escherichia coli with and without K88 antigen as revealed by hydrophobic interaction chromatography, Infect. Immun. 22:462–472.
So, M., and McCarthy, B. J., 1980, Nucleotide sequence of the bacterial transposon TN 1681 encoding a heat-stable (ST) toxin and its identification in enterotoxigenic Escherichia coli strains, Proc. Natl. Acad. Sci. USA 77:4011–4015.
Stirm, S., Ørskov, F., Ørskov, I., and Mansa, B., 1967, Episome-carried surface antigen K88 of Escherichia coli. II. Isolation and chemical analysis,J. Bacteriol. 93:731–739.
Svanborg-Eden, C., 1978, Attachment of Escherichia coli to human urinary tract epithelial cells, Scand. J. Infect.Dis. Suppl. 15:1–54.
Swaney, L. M., Liu, Y.-P., Ippen-Ihler, K., and Brinton, C. C., 1977, Genetic complementation analysis of Escherichia coli type 1 somatic pilus mutants, J. Bacteriol. 130:506–511.
Swanson, J., Sparks, E., Young, D., and King, G., 1975, Studies on gonococcus infection. X. Pili and leukocyte association factor as mediators of interactions between gonococci and eukaryotic cells in vitro, Infect. Immun. 11:1352–1361.
Tadros, T. F., 1980, Particle-surface adhesion, in: Microbial Adhesion to Surfaces (R. C. W. Berkeley, J. M. Lynch, J. Melling, P. R. Rutter, and B. Vincent, eds.), Horwood, Chichester, pp. 93–116.
Uhlman, D., and Jones, G. W., 1982, Chemotaxis as a factor in interactions between HeLa cells and Salmonellatyphimurium, J. Gen. Microbiol. 128:415–417.
van Embden, J. D. A., deGraaf, F. K., Schouls, L. M., and Teppema, J. S., 1980, Cloning and expression of a deoxyribonucleic acid fragment that encodes for the adhesive antigen K99, Infect. Immun. 29:1125–1133.
Wadstrom, T., Smyth, C. J., Faris, A., Jonsson, P., and Freer, J. H., 1978, Hydrophobic adsorptive and hemagglutinating properties of enterotoxigenic Escherichia coli with different colonizing factors: K88, K99, and colonization factor antigens and adherence factor, in: Second International Symposium on Neonatal Diarrhea (S. Acres, ed.), Veterinary Infectious Disease Organization, Saskatoon, pp. 29–45.
Weaver, P., Pikken, R., Schmidt, G., Jann, B., and Jann, K., 1980, Characterization of pili associated with Escherichia coli 018ac, Infect. Immun. 29:685–691.
Weiss, L., and Harlos, J. P., 1972, Short-term interactions between cell surfaces, Prog. Surf. Sci. 1:355–405.
Willetts, N. S., and Skurray, R., 1980, The conjugation system of F-like plasmids, Annu. Rev. Genet. 14:41–76.
Wilson, M. R., and Hohmann, A. W., 1974, Immunity to Escherichia coli in pigs: Adhesion of enteropathogenic Escherichia coli to isolated intestinal epithelial cells, Infect. Immun. 10:776–786.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1985 Plenum Press, New York
About this chapter
Cite this chapter
Isaacson, R.E. (1985). Pilus Adhesins. In: Savage, D.C., Fletcher, M. (eds) Bacterial Adhesion. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-6514-7_11
Download citation
DOI: https://doi.org/10.1007/978-1-4615-6514-7_11
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4615-6516-1
Online ISBN: 978-1-4615-6514-7
eBook Packages: Springer Book Archive