1887

Abstract

Bacterial entry into intestinal host cells is the result of a fairly sophisticated manipulation of host cell machinery by the pathogens. To study further the potential cell target of spp., the in-vitro entry of strains into intestinal cells was examined in relation to the metabolism, proliferation and differentiation of the cells by the alamarBlue assay, [H] thymidine incorporation, and brush border-associated enzyme activities, respectively. The study showed that cell metabolism was not involved in the entry of in three cell models (two human and one porcine). On the other hand, entry was closely related to the proliferation process and poorly related to the differentiation state of the cells. The use of mutants lacking invasion proteins showed that InIA and InIB acted in synergy to mediate the entry of into proliferative cells, whereas InIA alone seemed to be involved in the entry into non-proliferative cells. These two entry pathways could correspond to the two cellular processes used by to enter proliferative and non-proliferative cells, as suggested by the use of cytochalasin D, nocodazole, chloroquine and monodansylcadaverine. Taken together, we propose a hypothesis in which the entry of is mediated by interaction between randomly distributed E-cadherin on the surface of proliferative cells. In contrast, the entry into non-proliferative cells may involve pp60, a proto-oncogenic tyrosine kinase signal that modifies E-cadherin localisation. In conclusion, these results suggest that may preferentially enter crypt cells by a microfilament-dependent process, whereas the few bacteria that infect villus cells enter by an E-cadherin-internalin interaction that mediates microtubule-dependent endocytosis.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/00222615-46-8-681
1997-08-01
2024-12-12
Loading full text...

Full text loading...

/deliver/fulltext/jmm/46/8/medmicro-46-8-681.html?itemId=/content/journal/jmm/10.1099/00222615-46-8-681&mimeType=html&fmt=ahah

References

  1. Salyers A. A., Whitt D. D. Listeria monocytogenes. In Bacterial pathogenesis. A molecular approach Washington, DC: ASM Press; 1994182–189
    [Google Scholar]
  2. Schlech W. F. New perspectives on the gastrointestinal mode of transmission in invasive Listeria monocytogenes infection. Clin Invest Med 1984; 7:321–324
    [Google Scholar]
  3. MacDonald T. T., Carter P. B. Cell-mediated immunity to intestinal infection. Infect Immun 1980; 28:516–523
    [Google Scholar]
  4. Racz P., Tenner K., Mẻrӧ E. Experimental Listeria enteritis. I. An electron microscopic study of the epithelial phase in experimental Listeria infection. Lab Invest 1972; 26:694–700
    [Google Scholar]
  5. 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; 55:2822–2829
    [Google Scholar]
  6. Meyer D. H., Bunduki M., Beliveau C. M., Donnelly C. W. Differences in invasion and adherence of Listeria monocytogenes with mammalian gut cells. Food Microbiol 1992; 9:115–126
    [Google Scholar]
  7. Velge P., Bottreau E., Kaeffer B., Pardon P. Cell immortalization enhances Listeria monocytogenes invasion. Med Microbiol Immunol 1994; 183:145–158
    [Google Scholar]
  8. Portnoy D. A., Chakraborty T., Goebel W., Cossart P. Molecular determinants of Listeria monocytogenes pathogenesis. Infect Immun 1992; 60:1263–1267
    [Google Scholar]
  9. Sheehan B., Kocks C., Dramsi S. Molecular and genetic determinants of the Listeria monocytogenes infectious process. Curr Top Microbiol Immunol 1994; 192:187–216
    [Google Scholar]
  10. Gaillard J.-L., Berche P., Frehel C., Gouin E., Cossart P. Entry of L. monocytogenes into cells is mediated by intemalin, a repeat protein reminiscent of surface antigens from gram-positive cocci. Cell 1991; 65:1127–1141
    [Google Scholar]
  11. Kuhn M., Goebel W. Identification of an extracellular protein of Listeria monocytogenes possibly involved in intracellular uptake by mammalian cells. Infect Immun 1989; 57:55–61
    [Google Scholar]
  12. Dramsi S., Biswas I., Maguin E., Braun L., Mastroeni P., Cossart P. Entry of Listeria monocytogenes into hepatocytes requires expression of InlB, a surface protein of the intemalin multigene family. Mol Microbiol 1995; 16:251–261
    [Google Scholar]
  13. Mengaud J., Ohayon H., Gounon P., Mẻge R. M., Cossart P. E-cadherin is the receptor for intemalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 1996; 84:923–932
    [Google Scholar]
  14. Mounier J., Ryter A., Coquis-Rondon M., Sansonetti P. J. Intracellular and cell-to-cell spread of Listeria monocytogenes involves interaction with F-actin in the enterocytelike cell line Caco-2. Infect Immun 1990; 58:1048–1058
    [Google Scholar]
  15. Gaillard J.-L., Finlay B. B. Effect of cell polarization and differentiation on entry of Listeria monocytogenes into the enterocyte-like Caco-2 cell line. Infect Immun 1996; 64:1299–1308
    [Google Scholar]
  16. Velge P., Bottreau E., Kaeffer B., Van Langendonck N. The loss of contact inhibition and anchorage-dependent growth are key steps in the acquisition of Listeria monocytogenes susceptibility phenotype by non-phagocytic cells. Biol Cell 1995; 85:55–66
    [Google Scholar]
  17. Demuth A., Chakraborty T., Krohne G., Goebel W. Mammalian cells transfected with the listeriolysin gene exhibit enhanced proliferation and focus formation. Infect Immun 1994; 62:5102–5111
    [Google Scholar]
  18. Pinto M., Appay M. D., Simon-Assman P. Enterocytic differentiation of cultured human colon cancer cells by replacement of glucose in the medium. Biol Cell 1982; 44:193–196
    [Google Scholar]
  19. Zweibaum A., Pinto M., Chevalier G. Enterocytic differentiation of a subpopulation of the human colon tumor cell line HT-29 selected for growth in sugar-free medium and its inhibition by glucose. J Cell Physiol 1985; 122:21–29
    [Google Scholar]
  20. Zweibaum A., Laburthe M., Grasset E., Louvard D. Use of cultured cell lines in studies of intestinal cell differentiation and function. In Field M., Frizzell R. A. (eds) Handbook of physiology. Intestinal transport of the gastrointestinal system American Physiology Society; 1991223–255
    [Google Scholar]
  21. Galan J. E. Interactions of bacteria with non-phagocytic cells. Curr Opin Immunol 1994; 6:590–595
    [Google Scholar]
  22. Kemẻis S., Gabastou J.-M., Bemet-Camard M.-F., Coconnier M. H., Nowicki B. J., Servin A. L. Human cultured intestinal cells express attachment sites for uropathogenic Escherichia coli bearing adhesins of the Dr adhesin family. FEMS Microbiol Lett 1994; 119:27–32
    [Google Scholar]
  23. Kaeffer B., Bottreau E., Velge P., Pardon P. Epithelioid and fibroblastic cell lines derived from the ileum of an adult histocompatible miniature boar (d/d haplotype) and immortalized by SV40 plasmid. Eur J Cell Biol 1993; 62:152–162
    [Google Scholar]
  24. Chen T. R. In situ detection of Mycoplasma contamination in cell cultures by fluorescent Hoechst 33258 stain. Exp Cell Res 1977; 104:255–262
    [Google Scholar]
  25. Messer M., Dahlqvist A. A one-step ultramicro method for the assay of intestinal disaccharidases. Anal Biochem 1966; 14:376–392
    [Google Scholar]
  26. Garen A., Levinthal C. A fine-structure genetic and chemical study of the enzyme alkaline phosphatase of E. coli. I. Purification and characterization of alkaline phosphatase. Biochim Biophys Acta 1960; 38:470–483
    [Google Scholar]
  27. Nagatsu T., Hino M., Fuyamada H. New chromogenic substrates for X-prolyl dipeptidyl-aminopeptidase. Anal Biochem 1976; 74:466–476
    [Google Scholar]
  28. Fields R. D., Lancaster M. V. Dual-attribute continuous monitoring of cell proliferation/cytotoxicity. Am Biotechnol Lab 1993; 11:48–50
    [Google Scholar]
  29. MacPherson I., Montagnier L. Agar suspension culture for the selective assay of cells transformed by polyoma virus. Virology 1964; 23:291–294
    [Google Scholar]
  30. Gopalakrishnan S., Quinlan M. P. Modulation of E-cadherin localization in cells expressing wild-type Ela 12S or hypertransforming mutants. Cell Growth Differ 1995; 6:985–998
    [Google Scholar]
  31. Tabouret M., De Rycke J., Audurier A., Poutrel B. Pathogenicity of Listeria monocytogenes isolates in immunocompromised mice in relation to listeriolysin production. J Med Microbiol 1991; 34:13–18
    [Google Scholar]
  32. Velge P., Bottreau E., Kaeffer B., Yurdusev N., Pardon P., Van Langendonck N. Protein tyrosine kinase inhibitors block the entries of Listeria monocytogenes and Listeria ivanovii into epithelial cells. Microb Pathog 1994; 17:37–50
    [Google Scholar]
  33. Russell R. G., Blake D. C. Cell association and invasion of Caco-2 cells by Campylobacter jejuni . Infect Immun 1994; 62:3773–3779
    [Google Scholar]
  34. Schroy P. C., Rustgi A. K., Ikonomu E. Growth and intestinal differentiation are independently regulated in HT29 colon cancer cells. J Cell Physiol 1994; 161:111–123
    [Google Scholar]
  35. Drevets D. A., Sawyer R. T., Potter T. A., Campbell P. A. Listeria monocytogenes infects human endothelial cells by two distinct mechanisms. Infect Immun 1995; 63:4268–4276
    [Google Scholar]
  36. Lingnau A., Domann E., Hudel M. Expression of the Listeria monocytogenes EGD inlA and inlB genes, whose products mediate bacterial entry into tissue culture cell lines, by prfa-dependent and -independent mechanisms. Infect Immun 1995; 63:3896–3903
    [Google Scholar]
  37. Levitzki A., Willingham M., Pastan I. Evidence for participation of transglutaminase in receptor-mediated endocytosis. Proc Natl Acad Sci USA 1980; 77:2706–2710
    [Google Scholar]
  38. Oelschlaeger T. A., Guerry P., Kopecko D. J. Unusual microtubuledependent endocytosis mechanisms triggered by Campylobacter jejuni and Citrobacter freundii . Proc Natl Acad Sci USA 1993; 90:6884–6888
    [Google Scholar]
  39. Guzman C. A., Rohde M., Chakraborty T. Interaction of Listeria monocytogenes with mouse dendritic cells. Infect Immun 1995; 63:3665–3673
    [Google Scholar]
  40. Nӓthke I. S., Hinck L. E., Nelson W. J. Epithelial cell adhesion and development of cell surface polarity: possible mechanisms for modulation of cadherin function, organization and distribution. J Cell Sci 1993 Suppl 17:139–145
    [Google Scholar]
  41. Mareel M., Bracke M., Van Roy F. Invasion promoter versus invasion suppressor molecules the paradigm of E-cadherin. Mol Biol Rep 1994; 19:45–67
    [Google Scholar]
  42. Drubin D. G., Nelson W. J. Origins of cell polarity. Cell 1996; 84:335–344
    [Google Scholar]
  43. Louvard D., Kedinger M., Hauri H. P. The differentiating intestinal epithelial cell: establishment and maintenance of functions through interactions between cellular structures. Annu Rev Cell Biol 1992; 8:157–195
    [Google Scholar]
  44. Gordon J. I. Understanding gastrointestinal epithelial cell biology: lessons from mice with help from worms and flies. Gastroenterology 1993; 105:315–324
    [Google Scholar]
/content/journal/jmm/10.1099/00222615-46-8-681
Loading
/content/journal/jmm/10.1099/00222615-46-8-681
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error