Supramolecular structure of the Shigella type III secretion machinery: The needle part is changeable in length and essential for delivery of effectors

EMBO Journal

Volumn 19, Issue 15, 2000, Pages 3876-3887

  Tamano, Koichi ^a   Aizawa, Shin Ichi ^b   Katayama, Eisaku ^a   Nonaka, Takashi ^a   Imajoh Ohmi, Shinobu ^a   Kuwae, Asaomi ^a   Nagai, Shinya ^c   Sasakawa, Chihiro ^a,d  

^a UNIVERSITY OF TOKYO   (Japan)

^b TEIKYO UNIVERSITY   (Japan)

^c NIPPON INSTITUTE FOR BIOLOGICAL SCIENCE   (Japan)

^d OSAKA UNIVERSITY   (Japan)

Author keywords

MxiH; Shigella invasion; Supramolecular structure; Type III secretion system

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; MEMBRANE PROTEIN;

ARTICLE; BACTERIAL INFECTION; CELL INVASION; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN STRUCTURE; SHIGELLA;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; SHIGELLA;

EID: 0034254475     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.15.3876     Document Type: Article

References (45)

1. Aizawa, S.-I. and Kubori, T. (1998) Bacterial flagellation and cell division. Genes Cells, 3, 625-634.
2. Allaoui, A., Mounier, J., Prevost, M.C., Sansonetti, P.J. and Parsot, C. (1992a) icsB: a Shigella flexneri virulence gene necessary for the lysis of protrusions during intercellular spread. Mol. Microbiol., 6, 1605-1616.
3. Allaoui, A., Sansonetti, P.J. and Parsot, C. (1992b) MxiJ, a lipoprotein involved in secretion of Shigella Ipa invasins, is homologous to YscJ, a secretion factor of the Yersinia Yop proteins. J. Bacteriol., 174, 7661-7669.
4. Allaoui, A., Ménard, R., Sansonetti, P.J. and Parsot, C. (1993a) 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.
5. Allaoui, A., Sansonetti, P.J. and Parsot, C. (1993b) MxiD, an outer membrane protein necessary for the secretion of the Shigella flexneri Ipa invasins. Mol. Microbiol., 7, 59-68.
6. 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.
7. 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.
8. Bourdet-Sicard, R., Rüdiger, 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.
9. Butler, P.J.G. (1984) The current picture of the structure and assembly of tobacco mosaic virus. J. Gen Virol., 65, 253-279.
10. Cornelis, G.R. (1998) The Yersinia deadly kiss. J. Bacteriol., 180, 5495-5504.
11. Cornelis, G.R. and Wolf-Watz, H. (1997) The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol. Microbiol., 23, 861-867.
12. Demers, B., Sansonetti, P.J. and Parsot, C. (1998) Induction of type III secretion in Shigella flexneri is associated with differential control of transcription of genes encoding secreted proteins. EMBO J., 17, 2894-2903.
13. 1 ATPase and to virulence proteins of mammalian and plant pathogens. J. Bacteriol., 175, 3131-3138.
14. Fan, F. and Macnab, R.M. (1996) Enzymatic characterization of FliI. J. Biol. Chem., 271, 31981-31988.
15. Galán, J.E. ( 1996) Molecular genetic bases of Salmonella entry into host cells. Mol. Microbiol., 20, 263-271.
16. Galán, J.E. and Collmer, A. (1999) Type III secretion machines: bacterial devices for protein delivery into host cells. Science, 284, 1322-1328.
17. Håkansson, S., Schesser, K., Persson, C., Galyov, E.E., Rosqvist, R., Homble, 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.
18. Hirano, T., Yamaguchi, S., Oosawa, K. and Aizawa, S.-I. (1994) Roles of FliK and FlhB in determination of flagellar hook length in Salmonella typhimurium. J. Bacteriol., 176, 5439-5449.
19. Hueck, C.J. (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev., 62, 379-433.
20. Kaniga, K., Tucker, S., Trollinger, D. and Galán, J.E. (1995) Homologs of the Shigella IpaB and IpaC invasins are required for Salmonella typhimurium entry into cultured epithelial cells. J. Bacteriol., 177, 3965-3971.
21. Katayama, E., Shiraishi, T., Oosawa, K., Baba, N. and Aizawa, S.-I. (1996) Geometry of the flagellar motor in the cytoplasmic membrane of Salmonella typhimurium as determined by stereo-photogrammetry of quick-freeze deep-etch replica images. J. Mol. Biol., 255, 458-475.
22. Koroyasu, S., Yamazato, M., Hirano, T. and Aizawa, S.-I. (1998) Kinetic analysis of the growth rate of the flagellar hook in Salmonella typhimurium by the population balance method. Biophys. J., 74, 436-443.
23. Kubori, T., Shimamoto, N., Yamaguchi, S., Namba, K. and Aizawa, S.-I. (1992) Morphological pathway of flagellar assembly in Salmonella typhimurium. J. Mol. Biol., 226, 433-446.
24. Kubori, T., Matsushima, Y., Nakamura, D., Uralil, J., Lara-Tejero, M., Sukhan, A., Galán, J.E. and Aizawa, S.-I. (1998) Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science, 280, 602-605.
25. Lee, C.A. (1997) Type III secretion systems: machines to deliver bacterial proteins into eukaryotic cells? Trends Microbiol., 5, 148-156.
26. Macnab, R.M. (1992) Genetics and biogenesis of bacterial flagella. Annu. Rev. Genet., 26, 131-158.
27. 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.
28. 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.
29. Ménard, R., Sansonetti, P.J. and Parsot, C. (1994) The secretion of Shigella flexneri invasins is induced by the epithelial cell and controlled by IpaB and IpaD. EMBO J., 13, 5293-5302.
30. Pallen, M.J., Dougan, G. and Frankel, G. (1997) Coiled-coil domains in proteins secreted by type III secretion systems. Mol. Microbiol., 25, 423-425.
31. Parsot, C. (1994) Shigella flexneri: genetics of entry and intercellular dissemination in epithelial cells. Curr. Top. Microbiol. Immunol., 192, 217-241.
32. 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.
33. Patterson-Delafield, J., Martinez, R.J., Stocker, B.A. and Yamaguchi, S. (1973) A new fla gene in Salmonella typhimurium flaR and its mutant phenotype - superhooks. Arch. Mikrobiol., 90, 107-120.
34. Sasakawa, C., Kamata, K., Sakai, T., Murayama, S.Y., Makino, S. and Yoshikawa, M. (1986) 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.
35. 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.
36. 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.
37. Sasakawa, C., Buysse, J. and Watanabe, H. (1992) The large virulence plasmid of Shigella. Curr. Top. Microbiol. Immunol., 180, 21-44.
38. Sasakawa, C., Komatsu, 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.
39. 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.
40. Tran Van Nhieu, G. and Sansonetti, P.J. (1999) Mechanism of Shigella entry into epithelial cells. Curr. Opin. Microbiol., 2, 51-55.
41. 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.
42. 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.
43. Uchiya, K.-i., Tobe, T., Komatsu, K., Suzuki, T., Watarai, M., Fukuda, I., Yoshikawa, M. and Sasakawa, C. (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.
44. 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.
45. Watarai, M., Tobe, T., Yoshikawa, M. and Sasakawa, C. (1995) Contact of Shigella with host cells triggers release of Ipa invasins and is an essential function of invasiveness. EMBO J., 14, 2461-2470.