Exploitation of microfilament proteins by Listeria monocytogenes: Microvillus-like composition of the comet tails and vectorial spreading in polarized epithelial sheets

Journal of Cell Science

Volumn 107, Issue 10, 1994, Pages 2951-2960

  Temm Grove, Constance J ^a,d   Jockusch, Brigitte M ^a   Ronde, Manfred ^b   Niebuhr, Kirsten ^b   Chakraborty, Trinad ^c   Wehland, Jürgen ^b  

^a TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

^d Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

Actin filament; Cytoskeleton; Intracellular motility; Intracellular parasite; Polarized epithelia

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; ALPHA ACTININ; EZRIN; RADIXIN; VILLIN;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL POLARITY; CELL SPREADING; CELL SURFACE; CYTOSKELETON; EPITHELIUM CELL; HOST PARASITE INTERACTION; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOREACTIVITY; KIDNEY TUBULE EPITHELIUM; LISTERIA MONOCYTOGENES; LISTERIOSIS; MICROFILAMENT; MICROVILLUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN LOCALIZATION;

ACTINS; ANIMALS; BACTERIAL PROTEINS; CELL POLARITY; CELLS, CULTURED; DISEASE VECTORS; EPITHELIUM; LISTERIA MONOCYTOGENES; MICROVILLI;

ANIMALIA; BACTERIA (MICROORGANISMS); LISTERIA; LISTERIA MONOCYTOGENES;

EID: 0028092177     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (37)

1. Algrain, M., Turunen, Ossi, Vaheri, A., Louvard, D. and Arpin, M. (1993). Ezrin contains cytoskeleton and membrane binding domains accounting for ils proposed role as a membrane-cytoskeletal linker. J. Cell Biol. 120, 129-139.
2. Arpin, M., Algrain, M. and Louvard, D. (1994). Membrane-actin microfilament connections: an increasing diversity of players related to band 4.1. Curr. Opin. Cell Biol. 6, 136-141.
3. Birgbauer, E. and Solomon, F. (1989). A marginal band-associated protein has properties of both microtubule- and microlilament-associated proteins. J. Cell Biol. 109, 1609-1620.
4. Bretscher, A. (1983). Purification of an 80,000-dalton protein that is a component of the isolated microvillus cytoskeleton, and its localization in nonmuscle cells. J. Cell Biol. 97, 425-432.
5. Bretscher, A. (1991). Microfilament structure and function in the cortical cytoskeleton. Annu. Rev. Cell Biol. 7, 337-374.
6. Bye, W. A., Allan C. H. and Trier J. S. (1984). Structure, distribution and origin of M cells in Peyer's patches of mouse ileum. Gastroenterology 86, 789-801.
7. Cossart, P. and Mengaud, J. (1989). Listeria monocytogenes: a model system for the molecular study of intracellular parasitism. Mol. Biol. Med. 6, 463-474.
8. Dabiri, G. A., Sanger, J. M., Portnoy and Southwick, F. S. (1990). Listeria monocytogenes moves rapidly through the host-cell cytoplasm by inducing directional actin assembly. Proc. Nat. Acad. Sci. USA 87, 6068-6072.
9. Domann, E., Wehland, J., Rohde, M., Pistor, S., Hartl, M., Goebel, W., Leimeister-Wächter, M., Wünscher, M. and Chakraborty, T. (1992). A novel bacterial virulence gene in Listeria monocytogenes required for host cell microfilament interaction with homology to the proline-rich region of vinculin. EMBO J. 11, 1981-1990.
10. Finlay, B. B. and Falkow S. (1990). Salmonella interaction with polarized human intestinal Caco-2 epithelial cells. J. Infect. Dis. 162, 1096-1106.
11. Gaillard, J.-L., Berche, P., Mounier, J., Richard, S. and Sansonetti, P. (1987). In vitro model of penetration and intracellular growth of Listeria monocytogenes in the human enterocyte cell line Caco-2. Infect. Immunol. 55, 2822-2829.
12. Gellin, B. G. and Broome, C. V. (1989). Listeriosis. J. Am. Med. Assoc. 261, 1313-1320.
13. Gould, K. L., Bretscher, A., Esch, F. S. and Hunter, T. (1989). cDNA cloning and sequencing of the protein tyrosine kinase substrate, ezrin, reveals homology to band 4. 1. EMBO J. 8, 4133-4142.
14. Kocks, C., Gouin, E., Tabouret, M., Berche, P., Ohayon, H. and Cossart, P. (1992). Listeria monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell 68, 521-531.
15. Kocks, C. and Cossart, P. (1993). Directional actin assembly by Listeria monocytogenes at the site of polar surface expression of the actA gene product involving the actin-bundling protein plastin (fimbrin). Infect. Agents Dis. 2, 207-209.
16. Kocks, C., Hellio, R., Gounon, P., Ohayon, H. and Cossart, P. (1993). Polarized distribution of Listeria monocytogenes surface protein ActA at the site of directional actin assembly. J. Cell Sci. 105, 699-710.
17. Louvard, D. (1989). The function of the major cytoskeletal components of the brush border. Curr. Opin. Cell Biol. 1, 51-57.
18. Mounier, J., Ryter, A., Coquis-Rondon, M. and Sansonetti, P. J. (1990). Intracellular and cell-to-cell spread of Listeria monocytogenes involves interaction with F-actin in the enterocytelike cell line Caco-2. Infect. Immunol. 58, 1048-1058.
19. Mounier, J., Vasselon, T., Hellio, R., Lesourd, M. and Sansonetti, P. J. (1992). Shigella flexneri enters human colonic Caco-2 epithelial cells through the basolateral pole. Infect. Immunol. 60, 237-248.
20. Niebuhr, K., Chakraborty, T., Rohde, M., Gazlig, T., Jansen, B., Köllner, P. and Wehland, J. (1993). Localization of the ActA polypeptide of Listeria monocytogenes in infected tissue culture cell lines: ActA is not associated with actin 'comets'. Infect. Immunol. 61, 2793-2802.
21. Pistor, S., Chakraborty, T., Niebuhr, K., Domann, E. and Wehland, J. (1994). The ActA protein of Listeria monocytogenes acts as a nucleator inducing reorganization of the actin cytoskeleton. EMBO J. 13, 758-763.
22. Racz, P., Tenner, K. and Szivessy, K. (1970). Electron microscopic studies in experimental keratoconjunctivitis listeriosa. I. Penetration of Listeria monocytogenes into corneal epithelial cells. Acta Microbiol. Acad. Sci. Hung. 17, 221-236.
23. Racz, P., Tenner, K. and Mero, E. (1972). Experimental Listeria enteritis. I. An electron microscopic study of the epithelial phase in experimental Listeria infection. Lab. Invest. 26, 694-700.
24. Robine, M., Huet, C., Mall, R., Sahuquillo-Merino, C., Coudrier, E., Zweibaum, A. and Louvard, D. (1985). Can villin be used to identify malignant and undifferentiated normal digestive epithelial cells? Proc. Nat. Acad. Sci. USA 82, 8488-8495.
25. Sanger, J. M., Sanger, J. W. and Southwick, F. S. (1992). Host cell actin assembly is necessary and likely to provide the propulsive force for intracellular movement of Listeria monocytogenes. Infect. Immunol. 60, 3609-3619.
26. Schrader, M., Temm-Grove, C. J., Lessard, J. L. and Jockusch, B. M. (1994). Chicken antibodies to rabbit muscle actin with a restricted repertoire of F-actin recognition. Eur. J. Cell Biol. 63, 326-335.
27. Temm-Grove, C. J., Helbing, D. Wiegand, C., Höner, B. and Jockusch, B. M. (1992). The upright position of brush border-type microvilli depends on myosin filaments. J. Cell Sci. 101, 599-610.
28. Theriot, J. A., Mitchison, T. J., Tilney, L. G. and Portnoy, D. A. (1992). The rate of actin-based motility of intracellular Listeria monocytogenes equals the rate of actin polymerization. Nature 357, 257-260.
29. Theriot, J. A., Rosenblatt, J., Portnoy, D. A., Goldschmidt-Clermont, P. J. and Mitchison, T. J. (1994). Involvement of profilin in the actin-based motility of L. monocytogenes in cells and in cell-free extracts. Cell 76, 505-517.
30. Tilney, L. G. and Portnoy, D. A. (1989). Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J. Cell Biol. 109, 1597-1608.
31. Tilney, L. G., DeRosier, D. J. and Tilney, M. S. (1992a). How Listeria exploits host cell actin to form its own cytoskeleton. I. Formation of a tail and how that tail might be involved in movement. J. Cell. Biol. 118, 71-81.
32. Tilney, L. G., DeRosier, D., Weber, A. and Tilney, M. S. (1992b) How Listeria exploits host cell actin to form its own cytoskeleton. II. Nucleation, actin filament polarity, filament assembly, and evidence for a pointed end capper. J. Cell Biol. 118, 83-93.
33. Tilney, L. G. and Tilney, M. S. (1993). The wily ways of a parasite: induction of actin assembly by Listeria. Trends Microbiol. 1, 25-31.
34. Vasselon, T., Mounier, J., Hellio, R. and Sansonetti, P. J. (1992). Movement along actin filaments of the perijunctional area and de novo polymerization of cellular actin are required for Shigella flexneri colonization of epithelial Caco-2 cell monolayers. Infect. Immunol. 60, 1031-1040.
35. Wassef, J. S., Keren D. F. and Mailloux, J. L. (1989). Role of M cells in initial bacterial uptake and in ulcer formation in the rabbit intestinal loop model in shigellosis. Infect. Immunol. 57, 858-863.
36. Wilgenbus, K. K., Milatovich, A., Francke, U. and Furthmayer, H. (1993). Molecular cloning, cDNA sequence, and chromosomal assignment of the human radixin gene and two dispersed pseudogenes. Genomics 16, 199-206.
37. Winckler, B. Gonzalez-Agosti, C. Magendantz, M. and Solomon, F. (1994). Analysis of a differentiated cytoskeleton: The role of ezrin-radixin-moesin (ERM-proteins) in the marginal band of chicken erythrocytes. J. Cell Sci. 107 (in press).