MxiK and MxiN interact with the Spa47 ATPase and are required for transit of the needle components MxiH and MxiI, but not of Ipa proteins, through the type III secretion apparatus of Shigella flexneri

Molecular Microbiology

Volumn 49, Issue 3, 2003, Pages 755-767

  Jouihri, Noureddine ^a   Sory, Marie Paule ^a   Page, Anne Laure ^b   Gounon, Pierre ^b   Parsot, Claude ^b   Allaoui, Abdelmounaaïm ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CARRIER PROTEIN; CONGO RED; CYTOPLASM PROTEIN; IPA PROTEIN; PROTEIN MXIH; PROTEIN MXIK; PROTEIN MXIL; PROTEIN MXIN; PROTEIN SPA33; PROTEIN SPA47; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ARTICLE; BACTERIAL GENE; BACTERIAL MEMBRANE; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CELL SECRETION; CONTROLLED STUDY; EPITHELIUM CELL; GENE FUNCTION; GENE INACTIVATION; GRAM NEGATIVE BACTERIUM; IMMUNOPRECIPITATION; MXIH GENE; MXIK GENE; MXIL GENE; MXIN GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SHIGELLA FLEXNERI; TWO HYBRID SYSTEM; YEAST;

ADENOSINE TRIPHOSPHATASES; ADHESINS, BACTERIAL; BACTERIAL PROTEINS; CONGO RED; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, BACTERIAL; MACROMOLECULAR SUBSTANCES; PLASMIDS; PRECIPITIN TESTS; PROMOTER REGIONS (GENETICS); PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SHIGELLA FLEXNERI; TWO-HYBRID SYSTEM TECHNIQUES; VIRULENCE;

BACTERIA (MICROORGANISMS); EUKARYOTA; NEGIBACTERIA; SHIGELLA; SHIGELLA FLEXNERI;

EID: 0041663990     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2003.03590.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. Allaoui, A., Sansonetti, P.J., and Parsot, C. (1993a) MxiD, an outer membrane protein necessary for the secretion of the Shigella flexneri Ipa invasins. Mol Microbiol 7: 59-68.
3. Allaoui, A., Ménard, R., Sansonetti, P.J., and Parsot, C. (1993b) Characterization of the Shigella flexneri ipgD and ipgF genes, which are located in the proximal part of the mxi locus. Infect Immun 61: 1707-1714.
4. Allaoui, A., Sansonetti, P.J., Ménard, R., Barzu, S., Mounier, J., Phalipon, A., and Parsot, C. (1995) MxiG, a membrane protein required for secretion of Shigella spp. Ipa invasins: involvement in entry into epithelial cells and in intercellular dissemination. Mol Microbiol 17: 461-470.
5. Andrews, G.P., and Maurelli, A.T. (1992) mxiA of Shigella flexneri 2a, which facilitates export of invasion plasmid antigens, encodes a homolog of the low-calcium-response protein, LcrD, of Yersinia pestis. Infect Immun 60: 3287-3295.
6. Auvray, F., Thomas, J., Fraser, G.M., and Hughes, C. (2001) Flagellin polymerisation control by a cytosolic export chaperone. J Mol Biol 308: 221-229.
7. Bahrani, F.K., Sansonetti, P.J., and Parsot, C. (1997) Secretion of Ipa proteins by Shigella flexneri: inducer molecules and kinetics of activation. Infect Immun 65: 4005-4010.
8. Barzu, S., Nato, F., Rouyre, S., Mazie, J.C., Sansonetti, P., and Phalipon, A. (1993) Characterization of B-cell epitopes on IpaB, an invasion-associated antigen of Shigella flexneri: identification of an immunodominant domain recognized during natural infection. Infect Immun 61: 3825-3831.
9. Blocker, A., Gounon, P., Larquet, E., Niebuhr, K., Cabiaux, V., Parsot, C., and Sansonetti, P. (1999) The tripartite type III secreton of Shigella flexneri inserts IpaB and IpaC into host membranes. J Cell Biol 147: 683-693.
10. Blocker, A., Jouihri, N., Larquet, E., Gounon, P., Ebel, F., Parsot, C., et al. (2001) Structure and composition of the Shigella flexneri 'needle complex', a part of its type III secreton. Mol Microbiol 39: 652-663.
11. Bourdet-Sicard, R., Rudiger, M., Jockusch, B.M., Gounon, P., Sansonetti, P.J., and Tran Van Nhieu, G. (1999) Binding of the Shigella protein IpaA to vinculin induces F-actin depolymerization. EMBO J 18: 5853-5862.
12. Buchrieser, C., Glaser, P., Rusniok, C., Nedjari, H., D'Hauteville, H., Kunst, F., et al. (2000) The virulence plasmid pWR100 and the repertoire of proteins secreted by the type III secretion apparatus of Shigella flexneri. Mol Microbiol 38: 760-771.
13. Fraser, G.M., Bennett, J.C.-Q., and Hughes, C. (1999) Substrate-specific binding of hook-associated proteins by FIgN and FliT, putative chaperones for flagellum asembly. Mol Microbiol 32: 569-580.
14. Hueck, C.J. (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62: 379-433.
15. Jackson, M.W., and Plano, G.V. (2000) Interactions between type III secretion apparatus components from Yersinia pestis detected using the yeast two-hybrid system. FEMS Microbiol Lett 186: 85-90.
16. Kimbrough, T.G., and Miller, S.I. (2000) Contribution of Salmonella typhimurium type III secretion components to needle complex formation. Proc Natl Acad Sci USA 97: 11008-11013.
17. Klein, J.R., Fahlen, T.F., and Jones, B.D. (2000) Transcriptional organization and function of invasion genes within Salmonella enterica serovar Typhimurium pathogenicity island 1, including the prgH, prgI, prgJ, prgK, orgA, orgB, and orgC genes. Infect Immun 68: 3368-3376.
18. Macnab, R.M. (1999) The bacterial flagellum: reversible rotary propellor and type III export apparatus. J Bacteriol 181: 7149-7153.
19. Magdalena, J., Hachani, A., Chamekh, M., Jouihri, N., Gounon, P., Blocker, A., and Allaoui, A. (2002) Spa32 regulates a switch in substrate specificity of the typeIII secreton of Shigella flexneri from needle components to Ipa proteins. J Bacteriol 184: 3433-3441.
20. Mavris, M., Page, A.L., Tournebize, R., Demers, B., Sansonetti, P., and Parsot, C. (2002) Regulation of transcription by the activity of the Shigella flexneri type III secretion apparatus. Mol Microbiol 43: 1543-1553.
21. Ménard, R., Sansonetti, P.J., and Parsot, C. (1993) Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J Bacteriol 175: 5899-5906.
22. Ménard, R., Sansonetti, P., Parsot, C., and Vasselon, T. (1994) Extracellular association and cytoplasmic partitioning of the IpaB and IpaC invasins of Shigella flexneri. Cell 79: 515-525.
23. Miller, V.L., and Mekalanos, J.J. (1988) A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol 170: 2575-2583.30.
24. Niebuhr, K., Jouihri, N., Allaoui, A., Gounon, P., Sansonetti, P., and Parsot, C. (2000) IpgD, a protein secreted by the type III secretion machinery of Shigella flexneri, is chaperoned by IpgE and implicated in entry focus formation. Mol Microbiol 38: 8-19.
25. Page, A.L., Fromont-Racine, M., Sansonetti, P., Legrain, P., and Parsot, C. (2001) Characterization of the interaction partners of secreted proteins and chaperones of Shigella flexneri. Mol Microbiol 42: 1133-1145.
26. Page, A.L., Sansonetti, P., and Parsot, C. (2002) Spa15 of Shigella flexneri, a third type of chaperone in the type III secretion pathway. Mol Microbiol 43: 1533-1542.
27. Phalipon, A., Arondel, J., Nato, F., Rouyre, S., Mazie, J.C., and Sansonetti, P.J. (1992) Identification and characterization of B-cell epitopes of IpaC, an invasion-associated protein of Shigella flexneri. Infect Immun 60: 1919-1926.
28. Plano, G.V., Day, J.B., and Ferracci, F. (2001) Type III export: new uses for an old pathway. Mol Microbiol 40: 284-293.
29. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Harbor Laboratory Press.
30. Sansonetti, P.J. (2001) Rupture, invasion and inflammatory destruction of the intestinal barrier by Shigella, making sense of prokaryote-eukaryote cross-talks. FEMS Microbiol Rev 25: 3-14.
31. Sansonetti, P.J., Kopecko, D.J., and Formal, S.B. (1982) Involvement of a plasmid in the invasive ability of Shigella flexneri. Infect Immun 35: 852-860.
32. 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 hemolysis. Infect Immun 51: 461-469.
33. Sasakawa, C., Kamata, K., Tobe, T., Suzuki, T., and Yoshikawa, M. (1993) Eight genes in region 5 that form an operon are essential for invasion of epithelial cells by Shigella flexneri 2a. J Bacteriol 175: 2334-2346.
34. Schuch, R., and Maurelli, A.T. (2001a) MxiM and MxiJ, base elements of the Mxi-Spa type IIi secretion system of Shigella, interact with and stabilize the MxiD secretin in the cell envelope. J Bacteriol 183: 6991-6998.
35. Schuch, R., and Maurelli, A.T. (2001b) Spa33, a cell surface-associated subunit of the Mxi-Spa type III secretory pathway of Shigella flexneri, regulates Ipa protein traffic. Infec Immun 69: 2180-2189.
36. Sukhan, A., Kubori, T., Wilson, J., and Galan, J.E. (2001) Genetic analysis of assembly of the Salmonella enterica serovar Typhimurium type III secretion-associated needle complex. J Bacteriol 183: 1159-1167.
37. Tamano, K., Aizawa, S.-I., Katayama, E., Nonaka, T., Imajoh-Ohmi, S., Kuwae, A., et al. (2000) Supramolecular structure of the Shigella type III secretion machinery: the needle part is changeable in length and essential for delivery of effectors. EMBO J 19: 3876-3887.
38. Tamano, K., Katayama, E., Toyotome, T., and Sasakawa, C. (2002) Shigella Spa32 is an essential secretory protein for functional type III secretion machinery and uniformity of its needle length. J Bacteriol 184: 1244-1252.
39. Venkatesan, M.M., Buysse, J.M., and Oaks, E.V. (1992) Surface presentation of Shigella flexneri invasion plasmid antigens requires the products of the spa locus. J Bacteriol 174: 1990-2001.