Modulation of bacterial entry into epithelial cells by association between vinculin and the Shigella IpaA invasin

EMBO Journal

Volumn 16, Issue 10, 1997, Pages 2717-2729

  Tran Van Nhieu, G ^a   Ben Ze'ev, A ^b   Sansonetti, P J ^a  

^a INSERM   (France)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Actin polymerization; Bacterial invasion; IpaA; Shigella vinculin

Indexed keywords

ALPHA ACTININ; BACTERIAL PROTEIN; INVASIN; VINCULIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CELL INVASION; CELL MEMBRANE; CYTOSKELETON; DYSENTERY; EPITHELIUM CELL; HOST PARASITE INTERACTION; HUMAN; HUMAN CELL; NONHUMAN; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SHIGELLA FLEXNERI; SHIGELLOSIS; TARGET CELL;

ACTININ; ANTIGENS, BACTERIAL; BACTERIAL ADHESION; BACTERIAL PROTEINS; CYTOSKELETON; EPITHELIUM; HELA CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; PINOCYTOSIS; PROTEIN BINDING; SHIGELLA FLEXNERI; VINCULIN;

BACTERIA (MICROORGANISMS); SHIGELLA; SHIGELLA FLEXNERI;

EID: 0030994387     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.10.2717     Document Type: Article

References (43)

1. Adam, T., Arpin, M., Prévost, M.C., Gounon, P. and Sansonetti, P.J. (1995) Cytoskeletal rearrangements and the functional role of T-plastin during entry of Shigella flexneri into HeLa cells. J. Cell Biol., 129, 367-381.
2. Adam, T., Giry, M., Boquet, P. and Sansonetti, P.J. (1996) Rho-dependent membrane folding causes Shigella entry into epithelial cells. EMBO J., 15, 3315-3321.
3. Ben-Ze'ev, A., Reiss, R., Bendori, B. and Gorodecki, B. (1990) Transient induction of vinculin gene expression in 3T3 fibroblasts stimulated by serum growth factors. Cell Regular., 1, 621-636.
4. Bernardini, M.L., Mounier, J., d'Hauteville, H., Coquis-Rondon, M. and Sansonetti, P.J. (1989) Identification of icsA, a plasmid locus of Shigella flexneri that governs intra- and intercellular spread through interaction with F-actin. Proc. Natl Acad. Sci. USA. 86, 3867-3871.
5. Brasaemle, D.L. and Attie, A.D. (1988) Microelisa reader quantitation of fixed, stained, solubilized cells in microtitre dishes. BioTechniques, 6, 418-419.
6. Burridge, K., Fath, K., Kelly, G., Nuckolls, G. and Turner, C. (1988) Focal adhesions: transmembrane junctions between extracellular matrix and the cytoskeleton. Annu. Rev. Cell Biol., 4, 487-525.
7. Clark, E.A. and Brugge, J.S. (1995) Integrins and signal transduction pathways: the road taken. Science, 268, 233-239.
8. Clerc, P. and Sansonetti, P.J. (1987) Entry of Shigella flexneri into HeLa cells: evidence for directed phagocytosis involving actin polymerization and myosin accumulation. Infect. Immun., 57, 2681-2688.
9. Craig, S.W. and Johnson, R.P. (1996) Assembly of focal adhesions: progress, paradigms, and portents. Curr. Opin. Cell Biol., 8, 74-85.
10. c-src mediated signalling pathway. EMBO J., 14, 2471-2482.
11. Evans, R.R., Robson, R.M. and Stromer, M.H. (1984) Properties of smooth muscle vinculin. J. Biol. Chem., 259, 3916-3924.
12. Finlay, B.B. and Ruschkowski, S. (1991) Cytoskeletal rearrangements accompanying Salmonella entry into epithelial cells. J. Cell Sci., 99, 283-296.
13. Francis, C.L., Ryan, T.A., Jones, B.D., Smith, S.J. and Falkow, S. (1993) Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria. Nature, 364, 639-642.
14. Geiger, B. and Ginsberg, D. (1991) The cytoplasmic domain of adherens-type junctions. Cell Motil. Cytoskeleton, 20, 1-6.
15. Groisman, E.A. and Ochman, H. (1993) Cognate gene clusters govern invasion of host epithelial cells by Salmonella typhimurium and Shigella flexneri. EMBO J., 12, 3779-3787.
16. Hermant, D., Ménard, R., Arricau, N., Parsot, C. and Popoff, M.Y. (1995) Functional conservation of the Salmonella and Shigella effectors of entry into epithelial cells. Mol. Microbiol., 17, 781-789.
17. Isberg, R.R. (1991) Discrimination between intracellular uptake and surface adhesion of bacterial pathogens. Science, 252, 934-938.
18. Isberg, R.R. and Falkow, S. (1985) A single genetic lous encoded by Yersinia pseudotuberculosis permits invasion of cultured animal cells by Escherichia coli K-12. Nature, 317, 262-264.
19. Isberg, R.R. and Tran Van Nhieu, G. (1994) Two mammalian cell internalization strategies used by pathogenic bacteria. Annu. Rev. Genet., 27, 395-422.
20. Johnson, R.P. and Craig, S.W. (1995) F-actin binding site masked by the intramolecular association of vinculin head and tail domains. Nature, 373, 261-264.
21. Kaniga, K., Trollinger, D. and Galan, J.E. (1995) Identification of two targets of the type III protein secretion system encoded by the inv and spa loci of Salmonella typhimurium that have homology to the Shigella IpaD and IpaA proteins. J. Bacteriol., 177, 7078-7085.
22. Kadurugamuwa, J.L., Rohde, M. Wehland, J. and Timmis, K.N. (1991) Intercellular spread of Shigella flexneri through a monolayer medriated by membranous protrusions and associated with reorganization of the cytoskeletal protein vinculin. Infect. Immun., 59, 3463-3471.
23. Labigne-Roussel, A.F., Lark, L., Schoolnik, G. and Falkow, S. (1984) Cloning and expression of an afimbrial adhesin (AFA) responsible for P blood group-independent mannose-resistant hemagglutination from a pyelonephritic E. coli strain. Infect. Immun., 46, 251-259.
24. Laemmli, U.K. (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature, 227, 680-685.
25. Lee, C., Levin, A. and Branton, D. (1987) Copper staining: a five-minute protein staining for sodium-dodecyl sulfate polyacrylamide gels. Anal. Biochem., 166, 308-312.
26. Maurelli, A.T., Baudry, B., d'Hauteville, H., Hale, T.L. and Sansonetti, P.J. (1985) Cloning of plasmid DNA sequences involved in invasion of HeLa cells by Shigella flexneri. Infect. Immun., 49, 164-171.
27. Ménard, R., Sansonetti, P.J. and Parsot, C. (1993) Non polar mutagenesis of the ipa gene defines IpaB, IpaC and IpaD as effectors of Shigella flexneri entry into epithelial cells. J. Bacteriol., 175, 5899-5906.
28. Ménard, R., Sansonetti, P.J. and Parsot, C. (1994) The secretion of the Shigella flexneri Ipa invasins is induced by the epithelial cell and controlled by IpaB and IpaD. EMBO J., 13, 5293-5302.
29. Ménard, R., Prévost, M.-C., Gounon, P. Sansonetti, P. and Dehio, C. (1996) The secreted Ipa complex of Shigella flexneri promotes entry into mammalian cells. Proc. Natl Acad. Sci. USA. 93, 1254-1258.
30. Mengaud, J., Ohayon, H., Gounon, P. Mège, R.-M. and Cossart, P. (1996) E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell, 84, 923-933.
31. Menkel, A.R., Kroemker, M., Bubeck, P. Ronsiek, M., Nikolai, G. and Jockusch, B.M. (1994) Characterization of an F-actin-binding domain in the cytoskeletal protein vinculin. J. Cell Biol., 126, 1231-1240.
32. Nobes, C.D. and Hall, A. (1995) Rho, Rac, and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell, 81, 53-62.
33. 125I-vinculin gel overlay technique. J. Cell Biol., 97, 1283-1287.
34. Parsons, T.J. (1996) Integrin-mediated signalling: regulation by protein tyrosine kinases and small GTP-binding proteins. Curr. Opin. Cell Biol., 8, 146-152.
35. Parsot, C., Ménard, R., Gounon, P. and Sansonetti, P.J. (1995) Enhanced secretion through the Shigella flexneri Mxi-Spa translocon leads to assembly of extracellular proteins into macromolecular structures. Mol. Microbiol., 16, 291-300.
36. Rodriguez-Fernandez, J.L., Geiger, B., Salomon, D., Sabanay, I., Zöller, M. and Ben-Ze'ev, A. (1992) Suppression of tumorigenicity in transformed cells after transfection with vinculin cDNA. J. Cell Biol., 119, 427-438.
37. Rosqvist, R., Magnusson, K.E. and Wolf-Watz, H. (1994) Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J., 13, 964-972.
38. Rosqvist, R., Hakansson, S., Forsberg, A. and Wolf-Watz, H. (1995) Functional conservation of the secretion and translocation machinery for virulence proteins of yersiniae, salmonellae and shigellae. EMBO J., 14, 4187-4195.
39. Sasakawa, C., Kamata, K., Sakai, T., Makino, S., Yamada, M., Okada, N. and Yoshikawa, M. (1988) Virulence-associated genetic regions comprising 31 kilobases of the 230-kilobase plasmid in Shigella flexneri 2a. J. Bacteriol., 170, 2480-2484.
40. Suzuki, T., Saga, S. and Sasakawa, C. (1996) Functional analysis of VirG domains esential for interaction with vinculin and actin-based motility. J. Biol. Chem., 271, 21878-21885.
41. Tran Van Nhieu, G. and Isberg, R.R. (1993) Bacterial internalization mediated by β1 chain integrins is determined by ligands affinity and receptor density. EMBO J., 12, 1887-1895.
42. Varnum-Finney, B. and Reichardt, L. (1994) Vinculin-deficient PC12 cell lines extend unstable lamellipodia and filopodia and have a reduced rate of neurite outgrowth. J. Cell Biol., 127, 1071-1084.
43. Watarai, M., Funato, S. and Sasakawa, C. (1996) Interaction of Ipa proteins of Shigella flexneri with α5β1 integrin promotes entry of the bacteria into mammalian cells. J. Exp. Med., 183, 991-999.