Disruption of IcsP, the major Shigella protease that cleaves IcsA, accelerates actin-based motility

Molecular Microbiology

Volumn 25, Issue 3, 1997, Pages 451-462

  Shere, Kalpana D ^a   Sallustio, Sandra ^a,b   Manessis, Anastasios ^a   D'Aversa, Teresa G ^a   Goldberg, Marcia B ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b MOUNT SINAI HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BACTERIAL ENZYME; PROTEINASE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL INFECTION; BACTERIAL VIRULENCE; DNA SEQUENCE; ENZYME ACTIVITY; ESCHERICHIA COLI; INTESTINE EPITHELIUM CELL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; SEROTYPE; SHIGELLA FLEXNERI; STRAIN DIFFERENCE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; SHIGELLA; SHIGELLA FLEXNERI;

EID: 0030875733     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1997.4681827.x     Document Type: Article

References (39)

1. Allaoui, A., Mounier, J., Prevost, M.-C., Sansonetti, P.J., and Parsot, C. (1992) icsB: a Shigella flexneri virulence gene necessary for the lysis of protrusions during intercellular spread. Mol Microbiol 6: 1605-1616.
2. Balasubramanian, V., Pavelka, Jr, M.S., Bardarov, S., Martin, J., Weisbrod, T., McAdam, R., Bloom, B., and Jacobs, Jr, W.R. (1996) Allelic exchange in Mycobacterium tuberculosis with long linear recombination substrates. J Bacteriol 178: 273-279.
3. 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 bacterial intra- and intercellular spread through interaction with F-actin. Proc Natl Acad Sci USA 86: 3867-3871.
4. 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 55: 2681-2688.
5. d'Hauteville, H., and Sansonetti, P.J. (1992) Phosphorylation of IcsA by cAMP-dependent protein kinase and its effect on intercellular spread of Shigella flexneri. Mol Microbiol 6: 833-841.
6. d'Hauteville, H., Lagelouse, R.D., Nato, F., and Sansonetti, P. (1996) Lack of cleavage of IcsA in Shigella flexneri causes aberrant movement and allows demonstration of a cross-reactive eukaryotic protein. Infect Immun 64: 511-517.
7. Delbaere, L., Hutcheon, W., James, M., and Thiessen, W. (1975) Tertiary structural differences between microbial serine proteases and pancreatic serine enzymes. Nature 257: 758-763.
8. Egile, C., d'Hauteville, H., Parsot, C., and Sansonetti, P.J. (1997) SopA, the outer membrane protease responsible for polar localization of IcsA in Shigella flexneri. Mol Microbiol 23: 1063-1073.
9. Fukuda, I., Suzuki, T., Munakata, H., Hayashi, N., Katayama, E., Yoshizawa, M., and Sasakawa, C. (1995) Cleavage of Shigella surface protein VirG occurs at a specific site, but the secretion is not essential for intracellular spreading. J Bacteriol 177: 1719-1726.
10. Goldberg, M.B. (1997) Shigella actin-based motility in the absence of vinculin. Cell Motil Cytoskeleton 37: 44-53.
11. Goldberg, M.B., and Theriot, J.A. (1995) Shigella flexneri surface protein IcsA is sufficient to direct actin-based motility. Proc Natl Acad Sci USA 92: 6572-6576.
12. Goldberg, M.B., Barzu, O., Parsot, C., and Sansonetti, P.J. (1993) Unipolar localization and ATPase activity of IcsA, a Shigella flexneri protein involved in intracellular movement. J Bacteriol 175: 2189-2196.
13. Goldberg, M.B., Theriot, J.A., and Sansonetti, P.J. (1994) Regulation of surface presentation of IcsA, a Shigella protein essential to intracellular movement and spread, is growth phase-dependent. Infect Immun 62: 5664-5668.
14. Grodberg, J., and Dunn, J. (1988) ompT encodes the Escherichia coli outer membrane protease that cleaves T7 RNA polymerase during purification. J Bacteriol 170: 1245-1253.
15. High, N., Mounier, J., Prevost, M., and Sansonetti, P. (1992) IpaB of Shigella flexneri causes entry into epithelial cells and escape from the phagocytic vacuole. EMBO J 11: 1991-1999.
16. Hollifield, W., Fiss, E., and Neilands, J. (1978) Modification of a ferric enterobactin receptor protein from the outer membrane of Escherichia coli. Biochem Biophys Res Commun 83: 739-746.
17. Hovde, C., Calderwood, S., Mekalanos, J., and Collier, R. (1988) Evidence that glutamic acid 167 is an active-site residue of Shiga-like toxin I. Proc Natl Acad Sci USA 85: 2568-2572.
18. Jacobs, W.R., Barletta, R., Udani, R., Chan, J., Kalkut, G., Sarkis, G., Hatfull, G.F., and Bloom, B.R. (1993) Rapid assessment of drug susceptibilities of Mycobacterium tuberculosis by means of luciferase reporter phages. Science 260: 819-822.
19. Kadurugamuwa, J.L., Rohde, M., Wehland, L., and Timmis, K.N. (1991) Intercellular spread of Shigella flexneri through a monolayer mediated by membranous protrusions and associated with reorganization of the cytoskeletal protein vinculin. Infect Immun 59: 3463-3471.
20. Kaufmann, A., Stierhof, Y.-D., and Henning, U. (1994) New outer membrane-associated protease of Escherichia coli K-12. J Bacteriol 176: 359-367.
21. Kocks, C., Marchand, J.-B., Gouin, E., d'Hauteville, H., Sansonetti, P.J., Carlier, M.-F., and Cossart, P. (1995) The unrelated surface proteins ActA of Listeria monocytogenes and IcsA of Shigella flexneri are sufficient to confer actin-based motility on Listeria innocua and Escherichia coli, respectively. Mol Microbiol 18: 413-423.
22. LaBrec, E., Schneider, H., Magnani, T., and Formal, S. (1964) Epithelial cell penetration as an essential step in the pathogenesis of bacillary dysentery. J Bacteriol 88: 1503-1518.
23. Lett, M.-C., Sasakawa, C., Okada, N., Sakai, T., Makino, S., Yamada, M., Komatsu, K., and Yoshikawa, M. (1989) virG, a plasmid-coded virulence gene of Shigella flexneri: identification of the virG protein and determination of the complete coding sequence. J Bacteriol 171: 353-359.
24. Makino, S., Sasakawa, C., Kamata, K., Kurata, T., and Yoshikawa, M. (1986) A genetic determinant required for continuous reinfection of adjacent cells on large plasmid in S. flexneri 2a. Cell 46: 551-555.
25. Maurelli, A.T., Baudry, B., d'Hauteville, H., Hale, T.L., and Sansonetti, P.J. (1985) Cloning of virulence plasmid DNA sequences involved in invasion of HeLa cells by Shigella flexneri. Infect Immun 49: 164-171.
26. Meissner, P.S., Sisk, W.P., and Berman, M.L. (1987) Bacteriophage lambda cloning system for the construction of directional cDNA libraries. Proc Natl Acad Sci USA 84: 4171-4175.
27. Mobley, H.L.T., Jarvis, K.G., Elwood, J.P., Whittle, D.I., Lockatell, C.V., Russell, R.G., Johnson, D.E., Donnenberg, M.S., and Warren, J.W. (1993) Isogenic P-fimbrial deletion mutants of pyelonephritogenic Escherichia coli: The role of αGal (1-4)βGal binding in virulence of a wildtype strain. Mol Microbiol 10: 143-155.
28. Nakata, N., Tobe, T., Fukuda, I., Suzuki, T., Komatsu, K., Yoshikawa, M., and Sasakawa, C. (1993) The absence of a surface protease, OmpT, determines the intercellular spreading ability of Shigella: the relationship between the ompT and kcpA loci. Mol Microbiol 9: 459-468.
29. Oaks, E.V., Wingfield, M.E., and Formal, S.B. (1985) Plaque formation by virulent Shigella flexneri. Infect Immun 48: 124-129.
30. Ogawa, H., Nakamura, A., and Nakaya, R. (1968) Cinemicrographic study of tissue cell cultures infected with Shigella flexneri. Jpn J Med Sci Biol 21: 259-273.
31. Pal, T., Newland, J.W., Tall, B.D., Formal, S.B., and Hale, T.L. (1989) Intracellular spread of Shigella flexneri associated with the kcpA locus and a 140-kilodalton protein. Infect Immun 57: 477-486.
32. Prevost, M.C., Lesourd, M., Arpin, M., Vernel, F., Mounier, J., Hellio, R., and Sansonetti, P.J. (1992) Unipolar reorganization of F-actin layer at bacterial division and bundling of actin filaments by plastin correlate with movement of Shigella flexneri within HeLa cells. Infect Immun 60: 4088-4099.
33. Rawlings, N., and Barrett, A. (1994) Families of serine peptidases. Methods Enzymol 244: 19-61.
34. Sambrook, J., Fritsch, E., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
35. Sansonetti, P.J., Ryter, A., Clerc, P., Maurelli, A.T., and Mounier, J. (1986) Multiplication of Shigella flexneri within HeLa cells: lysis of the phagocytic vacuole and plasmid-mediated contact haemolysis. Infect Immun 51: 461-469.
36. Sansonetti, P.J., Mounier, J., Prevost, M.C., and Mege, R.-M. (1994) Cadherin expression is required for the spread of Shigella flexneri between epithelial cells. Cell 76: 829-839.
37. Smith, G.A., Portnoy, D.A., and Theriot, J.A. (1995) Asymmetric distribution of the Listeria monocytogenes ActA protein is required and sufficient to direct actin-based motility. Mol Microbiol 17: 945-951.
38. Sugimura, K., and Nishihara, T. (1988) Purification, characterization, and primary structure of Escherichia coli protease VII and OmpT. J Bacteriol 170: 5625-5632.
39. Suzuki, T., Lett, M.-C., and Sasakawa, C. (1995) Extracellular transport of VirG protein in Shigella. J Biol Chem 270: 30874-30880.