Abstract
The interaction of Aeromonas salmonicida with the murine macrophage (M phi) cell line P388D1 was used as a convenient model to study the involvement of the bacterial crystalline surface array (or A-layer) in the association with M phi s. A-layer-positive (A+) cells readily associated with M phi s in phosphate-buffered saline, whereas A- mutants were unable to do so, even when the bacterium-M phi interaction was forced by centrifugation. M phi s selectively interacted with A+ cells when challenged with mixtures of A+ and excess A- cells. Electron microscopy indicated that in phosphate-buffered saline only A+ bacteria were readily internalized, although by a nonconventional mechanism, suggesting that efficient phagocytosis in the absence of opsonins was A-layer mediated. Latex beads coated with a partially assembled A-layer were more efficiently taken up than uncoated or A-protein-coated beads, indicating that an organized A-layer was essential for M phi uptake. The reduced ability of M phi s plated on a substratum coated with the A-layer to bind A+ bacteria also suggested that association was both A-layer and receptor mediated. In the presence of tissue culture medium, competent M phi s interacted efficiently with A- bacteria and internalized them through conventional phagocytosis. A+ cells were markedly cytotoxic to M phi s, whereas the A-protein or A-layer was not. A- cells were cytotoxic to a lesser extent, suggesting that cytotoxicity was targeted.
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- Baumeister W., Wildhaber I., Phipps B. M. Principles of organization in eubacterial and archaebacterial surface proteins. Can J Microbiol. 1989 Jan;35(1):215–227. doi: 10.1139/m89-034. [DOI] [PubMed] [Google Scholar]
- Belland R. J., Trust T. J. Synthesis, export, and assembly of Aeromonas salmonicida A-layer analyzed by transposon mutagenesis. J Bacteriol. 1985 Sep;163(3):877–881. doi: 10.1128/jb.163.3.877-881.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chu S., Cavaignac S., Feutrier J., Phipps B. M., Kostrzynska M., Kay W. W., Trust T. J. Structure of the tetragonal surface virulence array protein and gene of Aeromonas salmonicida. J Biol Chem. 1991 Aug 15;266(23):15258–15265. [PubMed] [Google Scholar]
- Clerc P. L., Ryter A., Mounier J., Sansonetti P. J. Plasmid-mediated early killing of eucaryotic cells by Shigella flexneri as studied by infection of J774 macrophages. Infect Immun. 1987 Mar;55(3):521–527. doi: 10.1128/iai.55.3.521-527.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cluff C. W., Garcia M., Ziegler H. K. Intracellular hemolysin-producing Listeria monocytogenes strains inhibit macrophage-mediated antigen processing. Infect Immun. 1990 Nov;58(11):3601–3612. doi: 10.1128/iai.58.11.3601-3612.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Daskaleros P. A., Payne S. M. Congo red binding phenotype is associated with hemin binding and increased infectivity of Shigella flexneri in the HeLa cell model. Infect Immun. 1987 Jun;55(6):1393–1398. doi: 10.1128/iai.55.6.1393-1398.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Doig P., Emödy L., Trust T. J. Binding of laminin and fibronectin by the trypsin-resistant major structural domain of the crystalline virulence surface array protein of Aeromonas salmonicida. J Biol Chem. 1992 Jan 5;267(1):43–49. [PubMed] [Google Scholar]
- Dooley J. S., Engelhardt H., Baumeister W., Kay W. W., Trust T. J. Three-dimensional structure of an open form of the surface layer from the fish pathogen Aeromonas salmonicida. J Bacteriol. 1989 Jan;171(1):190–197. doi: 10.1128/jb.171.1.190-197.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Evenberg D., Van Boxtel R., Lugtenberg B., Schurer F., Blommaert J., Bootsma R. Cell surface of the fish pathogenic bacterium Aeromonas salmonicida. I. Relationship between autoagglutination and the presence of a major cell envelope protein. Biochim Biophys Acta. 1982 Jan 22;684(2):241–248. doi: 10.1016/0005-2736(82)90012-8. [DOI] [PubMed] [Google Scholar]
- Falkow S. Bacterial entry into eukaryotic cells. Cell. 1991 Jun 28;65(7):1099–1102. doi: 10.1016/0092-8674(91)90003-h. [DOI] [PubMed] [Google Scholar]
- Finlay B. B., Falkow S. Salmonella as an intracellular parasite. Mol Microbiol. 1989 Dec;3(12):1833–1841. doi: 10.1111/j.1365-2958.1989.tb00170.x. [DOI] [PubMed] [Google Scholar]
- Gaillard J. L., Berche P., Frehel C., Gouin E., Cossart P. Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci. Cell. 1991 Jun 28;65(7):1127–1141. doi: 10.1016/0092-8674(91)90009-n. [DOI] [PubMed] [Google Scholar]
- Gaillard J. L., Berche P., Mounier J., Richard S., Sansonetti P. In vitro model of penetration and intracellular growth of Listeria monocytogenes in the human enterocyte-like cell line Caco-2. Infect Immun. 1987 Nov;55(11):2822–2829. doi: 10.1128/iai.55.11.2822-2829.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ginis I., Tauber A. I. Activation mechanisms of adherent human neutrophils. Blood. 1990 Sep 15;76(6):1233–1239. [PubMed] [Google Scholar]
- Halablab M. A., Richards L., Bazin M. J. Phagocytosis of Legionella pneumophila. J Med Microbiol. 1990 Oct;33(2):75–83. doi: 10.1099/00222615-33-2-75. [DOI] [PubMed] [Google Scholar]
- Isberg R. R. Discrimination between intracellular uptake and surface adhesion of bacterial pathogens. Science. 1991 May 17;252(5008):934–938. doi: 10.1126/science.1674624. [DOI] [PubMed] [Google Scholar]
- Ishiguro E. E., Ainsworth T., Trust T. J., Kay W. W. Congo red agar, a differential medium for Aeromonas salmonicida, detects the presence of the cell surface protein array involved in virulence. J Bacteriol. 1985 Dec;164(3):1233–1237. doi: 10.1128/jb.164.3.1233-1237.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ishiguro E. E., Kay W. W., Ainsworth T., Chamberlain J. B., Austen R. A., Buckley J. T., Trust T. J. Loss of virulence during culture of Aeromonas salmonicida at high temperature. J Bacteriol. 1981 Oct;148(1):333–340. doi: 10.1128/jb.148.1.333-340.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kay W. W., Buckley J. T., Ishiguro E. E., Phipps B. M., Monette J. P., Trust T. J. Purification and disposition of a surface protein associated with virulence of Aeromonas salmonicida. J Bacteriol. 1981 Sep;147(3):1077–1084. doi: 10.1128/jb.147.3.1077-1084.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kay W. W., Phipps B. M., Ishiguro E. E., Trust T. J. Porphyrin binding by the surface array virulence protein of Aeromonas salmonicida. J Bacteriol. 1985 Dec;164(3):1332–1336. doi: 10.1128/jb.164.3.1332-1336.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kay W. W., Trust T. J. Form and functions of the regular surface array (S-layer) of Aeromonas salmonicida. Experientia. 1991 May 15;47(5):412–414. [PubMed] [Google Scholar]
- Kluftinger J. L., Kelly N. M., Hancock R. E. Stimulation by fibronectin of macrophage-mediated phagocytosis of Pseudomonas aeruginosa. Infect Immun. 1989 Mar;57(3):817–822. doi: 10.1128/iai.57.3.817-822.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Koval S. F., Hynes S. H. Effect of paracrystalline protein surface layers on predation by Bdellovibrio bacteriovorus. J Bacteriol. 1991 Apr;173(7):2244–2249. doi: 10.1128/jb.173.7.2244-2249.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kuhn M., Kathariou S., Goebel W. Hemolysin supports survival but not entry of the intracellular bacterium Listeria monocytogenes. Infect Immun. 1988 Jan;56(1):79–82. doi: 10.1128/iai.56.1.79-82.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Laurent F., Benoliel A. M., Capo C., Bongrand P. Oxidative metabolism of polymorphonuclear leukocytes: modulation by adhesive stimuli. J Leukoc Biol. 1991 Mar;49(3):217–226. doi: 10.1002/jlb.49.3.217. [DOI] [PubMed] [Google Scholar]
- Lee K. K., Ellis A. E. Glycerophospholipid:cholesterol acyltransferase complexed with lipopolysaccharide (LPS) is a major lethal exotoxin and cytolysin of Aeromonas salmonicida: LPS stabilizes and enhances toxicity of the enzyme. J Bacteriol. 1990 Sep;172(9):5382–5393. doi: 10.1128/jb.172.9.5382-5393.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McGee Z. A., Gorby G. L., Wyrick P. B., Hodinka R., Hoffman L. H. Parasite-directed endocytosis. Rev Infect Dis. 1988 Jul-Aug;10 (Suppl 2):S311–S316. doi: 10.1093/cid/10.supplement_2.s311. [DOI] [PubMed] [Google Scholar]
- Michl J., Pieczonka M. M., Unkeless J. C., Silverstein S. C. Effects of immobilized immune complexes on Fc- and complement-receptor function in resident and thioglycollate-elicited mouse peritoneal macrophages. J Exp Med. 1979 Sep 19;150(3):607–621. doi: 10.1084/jem.150.3.607. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mouallem M., Farfel Z., Hanski E. Bordetella pertussis adenylate cyclase toxin: intoxication of host cells by bacterial invasion. Infect Immun. 1990 Nov;58(11):3759–3764. doi: 10.1128/iai.58.11.3759-3764.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Munn C. B., Ishiguro E. E., Kay W. W., Trust T. J. Role of surface components in serum resistance of virulent Aeromonas salmonicida. Infect Immun. 1982 Jun;36(3):1069–1075. doi: 10.1128/iai.36.3.1069-1075.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Newman S. L., Tucci M. A. Regulation of human monocyte/macrophage function by extracellular matrix. Adherence of monocytes to collagen matrices enhances phagocytosis of opsonized bacteria by activation of complement receptors and enhancement of Fc receptor function. J Clin Invest. 1990 Sep;86(3):703–714. doi: 10.1172/JCI114766. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ofek I., Sharon N. Lectinophagocytosis: a molecular mechanism of recognition between cell surface sugars and lectins in the phagocytosis of bacteria. Infect Immun. 1988 Mar;56(3):539–547. doi: 10.1128/iai.56.3.539-547.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ofek I., Zafriri D., Goldhar J., Eisenstein B. I. Inability of toxin inhibitors to neutralize enhanced toxicity caused by bacteria adherent to tissue culture cells. Infect Immun. 1990 Nov;58(11):3737–3742. doi: 10.1128/iai.58.11.3737-3742.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Olivier G., Eaton C. A., Campbell N. Interaction between Aeromonas salmonicida and peritoneal macrophages of brook trout (Salvelinus fontinalis). Vet Immunol Immunopathol. 1986 Jun;12(1-4):223–234. doi: 10.1016/0165-2427(86)90126-1. [DOI] [PubMed] [Google Scholar]
- Pei Z., Blaser M. J. Pathogenesis of Campylobacter fetus infections. Role of surface array proteins in virulence in a mouse model. J Clin Invest. 1990 Apr;85(4):1036–1043. doi: 10.1172/JCI114533. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Phipps B. M., Kay W. W. Immunoglobulin binding by the regular surface array of Aeromonas salmonicida. J Biol Chem. 1988 Jul 5;263(19):9298–9303. [PubMed] [Google Scholar]
- Phipps B. M., Trust T. J., Ishiguro E. E., Kay W. W. Purification and characterization of the cell surface virulent A protein from Aeromonas salmonicida. Biochemistry. 1983 Jun 7;22(12):2934–2939. doi: 10.1021/bi00281a023. [DOI] [PubMed] [Google Scholar]
- Rosqvist R., Forsberg A., Rimpiläinen M., Bergman T., Wolf-Watz H. The cytotoxic protein YopE of Yersinia obstructs the primary host defence. Mol Microbiol. 1990 Apr;4(4):657–667. doi: 10.1111/j.1365-2958.1990.tb00635.x. [DOI] [PubMed] [Google Scholar]
- Rosqvist R., Forsberg A., Wolf-Watz H. Intracellular targeting of the Yersinia YopE cytotoxin in mammalian cells induces actin microfilament disruption. Infect Immun. 1991 Dec;59(12):4562–4569. doi: 10.1128/iai.59.12.4562-4569.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sakai D. K. Adhesion of Aeromonas salmonicida strains associated with net electrostatic charges of host tissue cells. Infect Immun. 1987 Mar;55(3):704–710. doi: 10.1128/iai.55.3.704-710.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sansonetti P. J. Genetic and molecular basis of epithelial cell invasion by Shigella species. Rev Infect Dis. 1991 Mar-Apr;13 (Suppl 4):S285–S292. doi: 10.1093/clinids/13.supplement_4.s285. [DOI] [PubMed] [Google Scholar]
- Silverstein S. C., Steinman R. M., Cohn Z. A. Endocytosis. Annu Rev Biochem. 1977;46:669–722. doi: 10.1146/annurev.bi.46.070177.003321. [DOI] [PubMed] [Google Scholar]
- Sleytr U. B., Messner P. Crystalline surface layers in procaryotes. J Bacteriol. 1988 Jul;170(7):2891–2897. doi: 10.1128/jb.170.7.2891-2897.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Speert D. P., Wright S. D., Silverstein S. C., Mah B. Functional characterization of macrophage receptors for in vitro phagocytosis of unopsonized Pseudomonas aeruginosa. J Clin Invest. 1988 Sep;82(3):872–879. doi: 10.1172/JCI113692. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Van Alstine J. M., Trust T. J., Brooks D. E. Differential partition of virulent Aeromonas salmonicida and attenuated derivatives possessing specific cell surface alterations in polymer aqueous-phase systems. Appl Environ Microbiol. 1986 Jun;51(6):1309–1313. doi: 10.1128/aem.51.6.1309-1313.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weel J. F., Hopman C. T., van Putten J. P. In situ expression and localization of Neisseria gonorrhoeae opacity proteins in infected epithelial cells: apparent role of Opa proteins in cellular invasion. J Exp Med. 1991 Jun 1;173(6):1395–1405. doi: 10.1084/jem.173.6.1395. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Williams P. Role of the cell envelope in bacterial adaptation to growth in vivo in infections. Biochimie. 1988 Aug;70(8):987–1011. doi: 10.1016/0300-9084(88)90263-5. [DOI] [PubMed] [Google Scholar]





