1887

Abstract

Previous observations on the highly infectious LG V strain 434 of and the guinea pig inclusion conjunctivitis (GPIC) strain of (which requires centrifugation of inocula with host cell monolayers for maximum infectivity) indicated that infectivity differences were expressed, not at entry, but at an intracellular stage affecting multiplication. Centrifugation increased the potential of internalized chlamydiae to undergo productive infection. Here, analysis of the intracellular fate of chlamydiae by ultrastructural methods indicates that strain GPIC exhibits two patterns of behaviour depending on the mode of inoculation. Strain GPIC showed limited entry, with 47 % of intracellular organisms becoming associated with thorotrast-labelled lysosomes, following static incubation with monolayers. In contrast, with centrifugation, entry was not limited and association with lysosomes was reduced to 12 %; strain 434 behaved similarly but independently of the mode of inoculation. The different results for strain GPIC correlated with distinct entry mechanisms. Entry during static incubation was unimpaired either by treatment with cytochalasin D or by temperature reduction to 20 °C, suggesting that it was pinocytic. Entry during centrifugation was markedly impaired by both treatments, suggesting that it was phagocytic. The data lead to two novel conclusions: first, that chlamydiae can apparently enter cells by both pinocytic and phagocytic mechanisms; second, that the entry mechanism influences intracellular fate. It is suggested that entry mechanism is linked to selection of the vesicle membrane forming around the internalizing chlamydiae. This, in turn, may influence both intracellular translocation and subsequent inhibition or promotion of multiplication of the internalized parasite.

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/content/journal/micro/10.1099/00221287-135-7-2107
1989-07-01
2021-08-02
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References

  1. Aggeler J., Werb Z. 1982; Initial events during phagocytosis by macrophages viewed from outside and inside the cell: membrane-particle interactions and clathrin.. Journal of Cell Biology 94:613–623
    [Google Scholar]
  2. Albrecht-Buehler G., Lancaster R.M. 1976; A quantitative description of the extension and retraction of surface protrusions in spreading 3T3 mouse fibroblasts.. Journal of Cell Biology 71:370–382
    [Google Scholar]
  3. Allan I., Pearce J.H. 1983; Amino acid requirements of strains of Chlamydia trachomatis and C. psittaci growing in McCoy cells: relationship with clinical syndrome and host origin.. Journal of General Microbiology 129:2001–2007
    [Google Scholar]
  4. Allan I., Spragg S.P., Pearce J.H. 1977; A pressure component in centrifuge-assisted chlamydial infection of cell cultures.. FEMS Microbiology letters 2:79–82
    [Google Scholar]
  5. Axline S.G., Reaven E.P. 1974; inhibition of phagocytosis and plasma membrane mobility of the cultivated macrophage by cytochalasin B. Role of sub-plasmalemmal microfilaments.. Journal of Cell Biology 62:647–659
    [Google Scholar]
  6. Barron A.L. 1982; Contributions of animal models to the study of human chlamydial infections.. In Chlamydial Infections, pp 357–366 Mardh P. A., Holmes K. K., Oriel J. D., Piot P., Schachter J. Edited by Amsterdam, New York, Oxford: Elsevier Biomedical Press;
    [Google Scholar]
  7. Besterman J.M., Low R.B. 1983; Endocytosis: a review of mechanisms and plasma membrane dynamics.. Biochemical Journal 210:1–13
    [Google Scholar]
  8. Bukholm G., Berg M., Degre M. 1987; Interferon-induced protein synthesis inhibits endocytosis of bacteria in epithelial cells.. Journal of Interferon Research 7:409–417
    [Google Scholar]
  9. Cooper J.A. 1987; Effects of cytochalasin and phalloidin on actin.. Journal of Cell Biology 105:1473–1478
    [Google Scholar]
  10. Dean R., Jessup W., Roberts C. 1984; Effects of exogenous amines on mammalian cells, with particular reference to membrane flow.. Biochemical Journal 217:27–40
    [Google Scholar]
  11. Friis R.R. 1972; Interaction of L cells and Chlamydia psittaci: entry of the parasite and host responses to its development.. Journal of Bacteriology 110:706–721
    [Google Scholar]
  12. Gregory W., Byrne G., Gardener M., Moulder J. 1979; Cytochalasin B does not inhibit ingestion of Chlamydia psittaci by mouse fibroblasts (L cells) and mouse peritoneal macrophages.. Infection and Immunity 25:463–466
    [Google Scholar]
  13. Griffin F.M., Mullinax P.J. 1981; Augmentation of macrophage complement receptor function in vitro. III. C3b receptors that promote phagocytosis migrate within the plane of the macrophage plasma membrane.. Journal of Experimental Medicine 154:291–305
    [Google Scholar]
  14. Griffin F.M., Griffin J.A., Leider J.E., Silverstein S.C. 1975; Studies on the mechanism of phagocytosis. I. Requirements for circumferential attachment of particle-bound ligands to specific receptors on the macrophage plasma membrane.. Journal of Experimental Medicine 142:1263–1282
    [Google Scholar]
  15. Griffiths M.S., Ainsworth S., Pearce J.H. 1976; Infectivity titration of guinea pig conjunctivitis agent in irradiated McCoy cells.. Journal of General Microbiology 95:249–256
    [Google Scholar]
  16. Hart P., D’Arcy Young, Gordon A.H., Sullivan K.H. 1987; Inhibition of phagosome- lysosome fusion in macrophages by certain mycobacteria can be explained by inhibition of lysosomal movements observed after phagocytosis.. Journal of Experimental Medicine 166:933–946
    [Google Scholar]
  17. Hodinka R., Wyrick P.B. 1986; Ultrastructural study of mode of entry of Chlamydia psittaci into l- 929 cells.. Infection and Immunity 54:855–863
    [Google Scholar]
  18. Hodinka R., Davis C.H., Choong J., Wyrick P.B. 1988; Ultrastructural study of endocytosis of Chlamydia trachomatis by McCoy cells.. Infection and Immunity 56:1456–1463
    [Google Scholar]
  19. Hoff S.F., Huang Y.O., Wisnieski B., Fox C.F. 1976; Temperature dependent events during phagocytosis of latex beads by cultured mouse LM cells.. Journal of Cell Biology 70:127a
    [Google Scholar]
  20. Kuo C.C., Wang S.P., Grayston J.T. 1977; Growth of trachoma organisms in HeLa-229 cell cultures.. In Nongonococcal Urethritis and Related Infections, pp 328–336 Holmes K. K., Hobson D. Edited by Washington: American Society for Microbiology;
    [Google Scholar]
  21. Lawn A.M., Blyth W.A., Taverne J. 1973; Interactions of TRIC agents with macrophages and BHK-21 cells observed by electron microscopy.. Journal of Hygiene 71:515–528
    [Google Scholar]
  22. Lee C. 1981; Interaction between a trachoma strain of Chlamydia trachomatis and mouse fibroblasts (McCoy cells) in the absence of centrifugation.. Infection and Immunity 31:584–591
    [Google Scholar]
  23. Marsh M., Helenius A. 1980; Adsorptive endocytosis of Semliki Forest virus.. Journal of Molecular Biology 142:439–454
    [Google Scholar]
  24. Mellman I., Fuchs R., Helenius A. 1986; Acidification of the endocytic and exocytic pathways.. Annual Review of Biochemistry 55:663–700
    [Google Scholar]
  25. Nicholson G.L. 1976; Transmembrane control of the receptors on normal and tumor cells. 1. Cytoplasmic influence over cell surface components.. Biochimica et biophysica acta 457:57–108
    [Google Scholar]
  26. Niesel D.W., Hess C.B., Cho Y.J., Klimpel K.D., Klimpel G.R. 1986; Natural and recombinant interferons inhibit epithelial invasion by Shigellaspp.. Infection and Immunity 52:828–833
    [Google Scholar]
  27. Painter R., Whisenand J., McIntosh A. 1981; Effects of cytochalasin B on actin and myosin association with particle binding sites in mouse macrophages: implication with regard to the mechanism of action of cytochalasins.. Journal of Cell Biology 91:373–384
    [Google Scholar]
  28. Patterson S.OXFORD, Dourmashkin R.R. 1979; Studies on the mechanism of influenza virus entry into cells.. Journal of General Virology 43:223–229
    [Google Scholar]
  29. Pearce J.H. 1988; Chlamydial invasion mechanisms: implications for parasite growth and host restraint.. Proceedings of the European Society for Chlamydia Research 1:109–112
    [Google Scholar]
  30. Pearce J.H., Allan I., Ainsworth S. 1981; Interaction of chlamydiae with host cells and mucous surfaces.. In Adhesion and Micro-organism Pathogenicity, Ciba Foundation Symposium 80: pp 234–249 Elliott K., O'Connor M., Whelan J. Edited by London: Pitman Medical;
    [Google Scholar]
  31. Prain C.J., Pearce J.H. 1985; Endocytosis of chlamydiae by McCoy cells: measurement and effects of centrifugation.. FEMS Microbiology Letters 26:233–237
    [Google Scholar]
  32. Rabinovitch M. 1976; The dissociation attachment and ingestion phases of phagocytosis by macrophages:. Experimental Cell Research 46:19–28
    [Google Scholar]
  33. Schliwa M. 1982; Action of cytochalasin D on cytoskeletal network.. Journal of Cell Biology 92:79–81
    [Google Scholar]
  34. Sllverstein S.C., Steinman R.M., Cohn Z.A. 1977; Endocytosis.. Annual Review of Biochemistry 46:669–722
    [Google Scholar]
  35. Soderlund G., Kihlström E. 1983; Effect of methylamine and monodansylcadaverine on the susceptibility of McCoy cells to Chlamydia trachomatis infections.. Infection and Immunity 40:534–541
    [Google Scholar]
  36. Stossel T.P., Hartwig J.H. 1976; Interactions of actin, myosin and a new actin binding protein of rabbit pulmonary macrophages. II. Role in cytoplasmic movement and phagocytosis.. Journal of Cell Biology 68:602–619
    [Google Scholar]
  37. Ukkonen P., Lewis V., Marsh M., Helenius A., Mellman I. 1986; Transport of macrophage Fc receptors and Fc receptor-bound ligands to lyso- somes.. Journal of Experimental Medicine 163:952–971
    [Google Scholar]
  38. Wang E., Michl J., Pfeffer L.M., Silverstein S.C., Tamm I. 1984; Interferon suppresses pinocytosis but stimulates phagocytosis in mouse peritoneal macrophages: related changes in cytoskeletal organisation.. Journal of Cell Biology 98:1328–1341
    [Google Scholar]
  39. Ward M.E. 1983; Chlamydial classification, development and structure.. British Medical Bulletin 39:109–115
    [Google Scholar]
  40. Ward M.E., Murray A. 1984; Control mechanisms governing the infectivity of Chlamydia trachomatis for HeLa cells: mechanisms of endocytosis.. Journal of General Microbiology 130:1765–1780
    [Google Scholar]
  41. Ward M.E., Salari H. 1982; Control mechanisms governing the infectivity of Chlamydia trachomatis for HeLa cells: modulation by cyclic nucleotides, prostaglandins and calcium.. Journal of General Microbiology 128:639–650
    [Google Scholar]
  42. Wyrick P.B., Brownridge E. 1978; Growth of Chlamydia psittaci in macrophages.. Infection and Immunity 19:1054–1060
    [Google Scholar]
  43. Young S.P., Bomford A., Williams R. 1983; Dual pathways for the uptake of rat asialotransferrin by rat hepatocytes.. Journal of Biological Chemistry 258:4972–4976
    [Google Scholar]
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