IcsB, secreted via the type III secretion system, is chaperoned by IpgA and required at the post-invasion stage of Shigella pathogenicity

Molecular Microbiology

Volumn 48, Issue 4, 2003, Pages 913-931

  Ogawa, Michinaga ^a   Suzuki, Toshihiko ^a,b   Tatsuno, Ichiro ^a   Abe, Hiroyuki ^a   Sasakawa, Chihiro ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CHAPERONE; CONGO RED; HYBRID PROTEIN; PROTEIN ICSB; PROTEIN IPGA; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BACTERIAL VIRULENCE; CONTROLLED STUDY; CYTOSOL; ESCHERICHIA COLI; GUINEA PIG; IN VITRO STUDY; IN VIVO STUDY; KERATOCONJUNCTIVITIS; MASS SPECTROMETRY; NONHUMAN; PATHOGENICITY; PLAQUE FORMING CELL; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN STABILITY; SHIGELLA FLEXNERI; SHIGELLOSIS;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; GUINEA PIGS; MOLECULAR CHAPERONES; OPERON; RECOMBINANT FUSION PROTEINS; SHIGELLA; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); CAVIA PORCELLUS; ESCHERICHIA COLI; NEGIBACTERIA; SHIGELLA; SHIGELLA FLEXNERI; SUS SCROFA;

EID: 0038354852     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2003.03489.x     Document Type: Article

References (83)

1. Abe, A., de Grado, M., Pfuetzner, R.A., Sánchez-Sanmartin, C., Devinney, R., Puente, J.L., et al. (1999) Enteropathogenic Escherichia coli translocated intimin receptor, Tir, requires a specific chaperone for stable secretion. Mol Microbiol 33: 1162-1175.
2. Allaoui, A., Mounier, J., Prévost, 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.
3. Allaoui, A., Ménard, R., Sansonetti, P.J., and Parsot, C. (1993) 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. Baudry, B., Kaczorek, M., and Sansonetti, P.J. (1988) Nucleotide sequence of the invasion plasmid antigen B and C genes (ipaB and ipaC) of Shigella flexneri. Microb Pathog 4: 345-357.
5. Bennett, J.C., and Hughes, C. (2000) From flagellum assembly to virulence: the extended family of type III export chaperones. Trends Microbiol 8: 202-204.
6. 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.
7. Björk, G.R. (1995) Biothynthesis and function of modified nucleotides in tRNA. In tRNA: Structure, Biosynthesis, and Function. Soll, D., and RajBhandary, U.L. (eds). Washington D.C.: American Society for Microbiology Press, pp. 165-205.
8. 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.
9. Blocker, A., Jouihri, N., Larquet, E., Gounon, P., Ebel, F., Parsot, C., Sansonetti, P., and Allaoui, A. (2001) Structure and composition of the Shigella flexneri 'needle complex', a part of its type III secretion. Mol Microbiol 39: 652-663.
10. Boyd, A.P., Lambermont, I., and Cornelis, G.R. (2000) Competition between the Yops of Yersinia enterocolitica for delivery into eukaryotic cells: role of the SycE chaperone binding domain of YopE. J Bacteriol 182: 4811-4821.
11. Braun, A., Hämmerle, S., Suda, K., Rothen-Rutishauser, B., Günthert, M., Krämer, S.D., and Wunderli-Allenspach, H. (2000) Cell cultures as tools in biopharmacy. Eur J Pharm Sci 11: S51-S60.
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. Casadaban, M.J., and Cohen, S.N. (1980) Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J Mol Biol 138: 179-207.
14. Cornelis, G.R., and Wolf-Watz, H. (1997) The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol Microbiol 23: 861-867.
15. Delahay, R.M., Shaw, R.K., Erriott, S.J., Kaper, J.B., Knutton, S., and Frankel, G. (2002) Functional analysis of the enteropathogenic Escherichia coli type III secretion system chaperone CesT identifies domains that mediate substrate interactions. Mol Microbiol 43: 61-73.
16. Durand, J.M., Okada, N., Tobe, T., Watarai, M., Fukuda, I., Suzuki, T., et al. (1994) vacC, a virulence-associated chromosomal locus of Shigella flexneri, is homologous to tgt, a gene encoding tRNA-guanine transglycosylase (Tgt) of Escherichia coli K-12. J Bacteriol 176: 4627-4634.
17. Durand, J.M., Dagberg, B., Uhlin, B.E., and Björk, G.R. (2000) Transfer RNA modification, temperature and DNA superhelicity have a common target in the regulatory network of the virulence of Shigella flexneri: the expression of the virF gene. Mol Microbiol 35: 924-935.
18. Elliott, S.J., Hutcheson, S.W., Dubois, M.S., Mellies, J.L., Wainwright, L.A., Batchelor, M., et al. (1999) Identification of CesT, a chaperone for the type III secretion of Tir in enteropathogenic Escherichia coli. Mol Microbiol 33: 1176-1189.
19. Francis, M.S., Aili, M., Wiklund, M.L., and Wolf-Watz, H. (2000) A study of the YopD-IcrH interaction from Yersinia pseudotuberculosis reveals a role for hydrophobic residues within the amphipathic domain of YopD. Mol Microbiol 38: 85-102.
20. Fu, Y., and Galán, J.E. (1998) Identification of a specific chaperone for SptP, a substrate of the centisome 63 type III secretion system of Salmonella typhimurium. J Bacteriol 180: 3393-3399.
21. Fujii, S., Akiyama, M., Aoki, K., Sugaya, Y., Higuchi, K., Hiraoka, M., et al. (1999) DNA replication errors produced by the replicative apparatus of Escherichia coli. J Mol Biol 289: 835-850.
22. Håkansson, S., Schesser, K., Persson, C., Galyov, E.E., Rosqvist, R., Homblé, F., and Wolf-Watz, H. (1996) The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target cell plasma membrane and displays a contact-dependent membrane disrupting activity. EMBO J 15: 5812-5823.
23. Iriarte, M., and Cornelis, G.R. (1998) YopT, a new Yersinia Yop effector protein, affects the cytoskeleton of host cells. Mol Microbiol 29: 915-929.
24. Irvine, J.D., Takahashi, L., Lockhart, K., Cheong, J., Tolan, J.W., Serick, H.E., and Grove, J.R. (1999) MDCK (Madin-Darby canine kidney) cells: a tool for membrane permeability screening. J Pharm Sci 88: 28-33.
25. Köhler, H., Rodrigues, S.P., and McCormick, B.A. (2002) Shigella flexneri interactions with the basolateral membrane domain of polarized model intestinal epithelium: role of lipopolysaccharide in cell invasion and in activation of the mitogen-activated protein kinase ERK. Infect Immun 70: 1150-1158.
26. Kopecko, D.J. (1994) Experimental keratoconjunctivitis (Sereny) assay. Methods Enzymol 235: 39-47.
27. Kuwae, A., Yoshida, S., Tamano, K., Mimuro, H., Suzuki, T., and Sasakawa, C. (2001) Shigella invasion of macrophage requires the insertion of IpaC into the host plasma membrane. Functional analysis of IpaC. J Biol Chem 276: 32230-32239.
28. Lloyd, S.A., Forsberg, A., Wolf-Watz, H., and Francis, M.S. (2001a) Targeting exported substrates to the Yersinia TTSS: different functions for different signals? Trends Microbiol 9: 367-371.
29. Lloyd, S.A., Norman, M., Rosqvist, R., and Wolf-Watz, H. (2001b) Yersinia YopE is targeted for type III secretion by N-terminal, not mRNA, signals. Mol Microbiol 39: 520-531.
30. Lloyd, S.A., Sjöström, M., Andersson, S., and Wolf-Watz, H. (2002) Molecular characterization of type III secretion signals via analysis of synthetic N-terminal amino acid sequences. Mol Microbiol 43: 51-59.
31. 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.
32. Martinéz, E., Bartolomé, B., and de la Cruz, F. (1988) pACYC184-derived cloning vectors containing the multiple cloning site and IacZ alpha reporter gene of pUC8/9 and pUC18/19 plasmids. Gene 68: 159-162.
33. van Meer, G., and van't Hof, W. (1993) Epithelial sphingolipid sorting is insensitive to reorganization of the Golgi by nocodazole, but is abolished by monensin in MDCK cells and by brefeldin A in Caco-2 cells. J Cell Sci 104: 833-842.
34. Ménard, R., and Sansonetti, P.J. (1994) Shigella flexneri: isolation of noninvasive mutants of gram-negative pathogens. Methods Enzymol 236: 493-509.
35. 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.
36. Ménard, R., Sansonetti, P., and Parsot, C. (1994) The secretion of the Shigella flexneri Ipa invasins is activated by epithelial cells and controlled by IpaB and IpaD. EMBO J 13: 5293-5302.
37. Monlauzeur, L., Breuza, L., and Le Bivic, A. (2000) Different functional recognition of basoratelal signals in Caco-2 and MDCK cells. Exp Cell Res 258: 195-203.
38. 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 Immun 60: 237-248.
39. Nakata, N., Sasakawa, C., Okada, N., Tobe, T., Fukuda, I., Suzuki, T., et al. (1992) Identification and characterization of virK, a virulence-associated large plasmid gene essential for intercellurar spreading of Shigella flexneri. Mol Microbiol 6: 2387-2395.
40. Neyt, C., and Cornelis, G.R. (1999) Insertion of a Yop translocation pore into the macrophage plasma membrane by Yersinia enterocolitica: requirement for translocators YopB and YopD, but not LcrG. Mol Microbiol 33: 971-981.
41. Niebuhr, K., Jouihri, N., Allaoui, A., Gounon, P., Sansonetti, P.J., 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.
42. Niebuhr, K., Giuriato, S., Pedron, T., Philpott, D.J., Gaits, F., Sable, J., et al. (2002) Conversion of Ptdlns (4,5) P (2) into Ptdlns (5) P by the S. flexneri effector IpgD reorganizes host cell morphology. EMBO J 21: 5069-5078.
43. Oaks, E.V., Wingfield, M.E., and Formal, S.B. (1985) Plaque formation by virulent Shigella flexneri. Infect Immun 48: 124-129.
44. Page, A.L., and Parsot, C. (2002) Chaperones of the type III secretion pathway: jacks of all trades. Mol Microbiol 46: 1-11.
45. Page, A.L., Ohayon, H., Sansonetti, P.J., and Parsot, C. (1999) The secreted IpaB and IpaC invasins and their cytoplasmic chaperone IpgC are required for intercellular dissemination of Shigella flexneri. Cell Microbiol 1: 183-193.
46. 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.
47. Papini, E., Satin, B., Norais, N., de Bernard, M., Telford, J.L., Rappuoli, R., and Montecucco, C. (1998) Selective increase of the permeability of polarized epithelial cell monolayers by Helicobacter pylori vacuolating toxin. J Clin Invest 102: 813-820.
48. 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.
49. Rathman, M., Jouirhi, N., Allaoui, A., Sansonetti, P., Parsot, C., and Tran Van Nhieu, G. (2000) The development of a FACS-based strategy for the isolation of Shigella flexneri mutants that are deficient in intercellular spread. Mol Microbiol 35: 974-990.
50. 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.
51. Sansonetti, P.J., Hale, T.L., Dammin, G.J., Kapfer, C., Collins, H.H., Jr, and Formal, S.B. (1983) Alterations in the pathogenicity of Escherichia coli K-12 after transfer of plasmid and chromosomal genes from Shigella flexneri. Infect Immun 39: 1392-1402.
52. 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.
53. Sansonetti, P.J., Arondel, J., Cantey, J.R., Prévost, M.C., and Huerre, M. (1996) Infection of rabbit Peyer's patches by Shigella flexneri: effect of adhesive or invasive bacterial phenotypes on follicle-associated epithelium. Infect Immun 64: 2752-2764.
54. Sansonetti, P.J., Tran Van Nhieu, G., and Egile, C. (1999) Rupture of the intestinal epithelial barrier and mucosal invasion by Shigella flexneri. Clin Infect Dis 28: 466-475.
55. Sasakawa, C., Kamata, K., Sakai, T., Murayama, S.Y., Makino, S., and Yoshikawa, M. (1986a) Molecular alteration of the 140-megadalton plasmid associated with loss of virulence and Congo red binding activity in Shigella flexneri. Infect Immun 51: 470-475.
56. Sasakawa, C., Makino, S., Kamata, K., and Yoshikawa, M. (1986b) Isolation, characterization, and mapping of Tn5 insertions into the 140- megadalton invasion plasmid defective in the mouse Sereny test in Shigella flexneri 2a. Infect Immun 54: 32-36.
57. Sasakawa, C., Adler, B., Tobe, T., Okada, N., Nagai, S., Komatsu, K., and Yoshikawa, M. (1989) Functional organization and nucleotide sequence of virulence Region-2 on the large virulence plasmid in Shigella flexneri 2a. Mol Microbiol 3: 1191-1201.
58. Sawada, K., Terada, T., Saito, H., and Inui, K. (2001) Distinct transport characteristics of basolateral peptide transporters between MDCK and Caco-2 cells. Pflugers Arch 443: 31-37.
59. Sereny, B. (1975) Experimental keratoconjunctivitis in Shigellosa. Acta Microbiol Acad Sci Hung 4: 367-376.
60. Sory, M.P., Boland, A., Lambermont, I., and Cornelis, G.R. (1995) Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach. Proc Natl Acad Sci USA 92: 11998-12002.
61. Suzuki, T., and Sasakawa, C. (2001) Molecular basis of the intracellular spreading of Shigella. Infect Immun 69: 5959-5966.
62. Takeuchi, J., and Toh-e., A. (2001) Genetic dissection of the yeast 26S proteasome: cell cycle defects caused by the Drpn9 mutation. Biochimie 83: 333-340.
63. Tamano, K., Aizawa, S., 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.
64. 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.
65. Tardy, F., Homblé, F., Neyt, C., Wattiez, R., Cornelis, G.R., Ruysschaert, J.M., and Cabiaux, V. (1999) Yersinia enterocolitica type III secretion-translocation system: channel formation by secreted Yops. EMBO J 18: 6793-6799.
66. Tobe, T., Nagai, S., Okada, N., Adler, B., Yoshikawa, M., and Sasakawa, C. (1991) Temperature-regulated expression of invasion genes in Shigella flexneri is controlled through the transcriptional activation of the virB gene on the large plasmid. Mol Microbiol 5: 887-893.
67. Tobe, T., Sasakawa, C., Okada, N., Honma, Y., and Yoshikawa, M. (1992) vacB, a novel chromosomal gene required for expression of virulence genes on the large plasmid of Shigella flexneri. J Bacteriol 174: 6359-6367.
68. Tran Van Nhieu, G., Ben-Ze'ev, A., and Sansonetti, P.J. (1997) Modulation of bacterial entry into epithelial cells by association between vinculin and the Shigella IpaA invasin. EMBO J 16: 2717-2729.
69. Tran Van Nhieu, G., Caron, E., Hall, A., and Sansonetti, P.J. (1999) IpaC induces actin polymerization and filopodia formation during Shigella entry into epithelial cells. EMBO J 18: 3249-3262.
70. Tran Van Nhieu, G., Bourdet-Sicard, R., Duménil, G., Blocker, A., and Sansonetti, P.J. (2000) Bacterial signals and cell responses during Shigella entry into epithelial cells. Cell Microbiol 2: 187-193.
71. Uchiya, K., Tobe, T., Komatsu, K., Suzuki, T., Watarai, M., Fukuda, I., et al. (1995) Identification of a novel virulence gene, virA, on the large plasmid of Shigella, involved in invasion and intercellular spreading. Mol Microbiol 17: 241-250.
72. Venkatesan, M.M., and Buysse, J.M. (1990) Nucleotide sequence of invasion plasmid antigen gene ipaA from Shigella flexneri 5. Nucleic Acids Res 18: 1648.
73. 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.
74. Venkatesan, M.M., Goldberg, M.B., Rose, D.J., Grotbeck, E.J., Burland, V., and Blattner, F.R. (2001) Complete DNA sequence and analysis of the large virulence plasmid of Shigella flexneri. Infect Immun 69: 3271-3285.
75. Wassef, J.S., Keren, D.F., and Mailloux, J.L. (1989) Role of M cells in initial antigen uptake and in ulcer formation in the rabbit intestinal loop model of shigellosis. Infect Immun 57: 858-863.
76. Watanabe, T., van Geldorp, G., Najrana, T., Yamamura, E., Nunoshiba, T., and Yamamoto, K. (2001) Miscoding and misincorporation of 8-oxo-guanine during leading and lagging strand synthesis in Escherichia coli. Mol Gen Genet 264: 836-841.
77. Wattiau, P., and Cornelis, G.R. (1993) SycE, a chaperone-like protein of Yersinia enterocolitica involved in the secretion of YopE. Mol Microbiol 8: 123-131.
78. Wattiau, P., Bernier, B., Deslée, P., Michiels, T., and Cornelis, G.R. (1994) Individual chaperones required for Yop secretion by Yersinia. Proc Natl Acad Sci USA 91: 10493-10497.
79. Wattiau, P., Woestyn, S., and Cornelis, G.R. (1996) Customized secretion chaperones in pathogenic bacteria. Mol Microbiol 20: 255-262.
80. Wenthzel, A.M., Stancek, M., and Isaksson, L.A. (1998) Growth phase dependent stop codon readthrough and shift of translation reading frame in Escherichia coli. FEBS Lett 421: 237-242.
81. Yoshida, S., Katayama, E., Kuwae, A., Mimuro, H., Suzuki, T., and Sasakawa, C. (2002) Shigella deliver an effector protein to trigger host microtubule destabilization, which promotes Rac1 activity and efficient bacterial internalization. EMBO J 21: 2923-2935.
82. Yu, J.R., Choi, S.D., and Kim, Y.W. (2000) In vitro infection of Cryptosporidium parvum to four different cell lines. Korean J Parasitol 38: 59-64.
83. Zychlinsky, A., Prévost, M.C., and Sansonetti, P.J. (1992) Shigella flexneri induces apoptosis in infected macrophages. Nature 358: 167-169.