Function and molecular architecture of the Yersinia injectisome tip complex

Molecular Microbiology

Volumn 65, Issue 5, 2007, Pages 1311-1320

  Broz, Petr ^a   Mueller, Catherine A ^a   Müller, Shirley A ^a   Philippsen, Ansgar ^a   Sorg, Isabel ^a   Engel, Andreas ^a   Cornelis, Guy R ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AEROMONAS SALMONICIDA; ARTICLE; CELL MEMBRANE; CHEMICAL STRUCTURE; HEMOLYSIS; NONHUMAN; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY; YERSINIA ENTEROCOLITICA;

ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; PORE FORMING CYTOTOXIC PROTEINS; PROTEIN STRUCTURE, QUATERNARY; PROTEIN SUBUNITS; RECOMBINANT FUSION PROTEINS; YERSINIA ENTEROCOLITICA; YERSINIA INFECTIONS;

AEROMONAS SALMONICIDA; PSEUDOMONAS AERUGINOSA; YERSINIA; YERSINIA ENTEROCOLITICA;

EID: 34547908488     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2007.05871.x     Document Type: Article

References (44)

1. Agrain, C., Callebaut, I., Journet, L., Sorg, I., Paroz, C., Mota, L.J., et al. (2005) Characterization of a Type III secretion substrate specificity switch (T3S4) domain in YscP from Yersinia enterocolitica. Mol Microbiol 56 : 54 67.
2. Blocker, A., Gounon, P., Larquet, E., Niebuhr, K., Cabiaux, V., Parsot, C., et al. (1999) The tripartite type III secreton of Shigella flexneri inserts IpaB and IpaC into host membranes. J Cell Biol 147 : 683 693.
3. Boland, A., Sory, M.P., Iriarte, M., Kerbourch, C., Wattiau, P. Cornelis, G.R. (1996) Status of YopM and YopN in the Yersinia Yop virulon: YopM of Y. enterocolitica is internalized inside the cytosol of PU5-1.8 macrophages by the YopB, D, N delivery apparatus. EMBO J 15 : 5191 5201.
4. Burrows, T.W. Bacon, G.A. (1956) The basis of virulence in Pasteurella Pestis: an antigen determining virulence. Br J Exp Pathol 37 : 481 493.
5. Cordes, F.S., Komoriya, K., Larquet, E., Yang, S., Egelman, E.H., Blocker, A., et al. (2003) Helical structure of the needle of the type III secretion system of Shigella flexneri. J Biol Chem 278 : 17103 17107.
6. Cornelis, G.R. (2006) The type III secretion injectisome. Nat Rev Microbiol 4 : 811 825.
7. Cornelis, G.R. Wolf-Watz, H. (1997) The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol Microbiol 23 : 861 867.
8. Cornelis, G., Vanootegem, J.C. Sluiters, C. (1987) Transcription of the yop regulon from Y. enterocolitica requires trans acting pYV and chromosomal genes. Microb Pathog 2 : 367 379.
9. Daniell, S.J., Takahashi, N., Wilson, R., Friedberg, D., Rosenshine, I., Booy, F.P., et al. (2001) The filamentous type III secretion translocon of enteropathogenic Escherichia coli. Cell Microbiol 3 : 865 871.
10. Deane, J.E., Roversi, P., Cordes, F.S., Johnson, S., Kenjale, R., Daniell, S., et al. (2006) Molecular model of a type III secretion system needle: implications for host-cell sensing. Proc Natl Acad Sci USA 103 : 12529 12533.
11. Derewenda, U., Mateja, A., Devedjiev, Y., Routzahn, K.M., Evdokimov, A.G., Derewenda, Z.S., et al. (2004) The structure of Yersinia pestis V-antigen, an essential virulence factor and mediator of immunity against plague. Structure (Camb) 12 : 301 306.
12. Doerrler, W.T. Raetz, C.R. (2005) Loss of outer membrane proteins without inhibition of lipid export in an Escherichia coli YaeT mutant. J Biol Chem 280 : 27679 27687.
13. Erskine, P.T., Knight, M.J., Ruaux, A., Mikolajek, H., Wong Fat Sang, N., Withers, J., et al. (2006) High resolution structure of BipD: an invasion protein associated with the type III secretion system of Burkholderia pseudomallei. J Mol Biol 363 : 125 136.
14. Espina, M., Olive, A.J., Kenjale, R., Moore, D.S., Ausar, S.F., Kaminski, R.W., et al. (2006) IpaD localizes to the tip of the type III secretion system needle of Shigella flexneri. Infect Immun 74 : 4391 4400.
15. Fields, K.A., Nilles, M.L., Cowan, C. Straley, S.C. (1999) Virulence role of V antigen of Yersinia pestis at the bacterial surface. Infect Immun 67 : 5395 5408.
16. Fu, Y. Galan, J.E. (1998) The Salmonella typhimurium tyrosine phosphatase SptP is translocated into host cells and disrupts the actin cytoskeleton. Mol Microbiol 27 : 359 368.
17. Galan, J.E. Wolf-Watz, H. (2006) Protein delivery into eukaryotic cells by type III secretion machines. Nature 444 : 567 573.
18. Goure, J., Pastor, A., Faudry, E., Chabert, J., Dessen, A. Attree, I. (2004) The V antigen of Pseudomonas aeruginosa is required for assembly of the functional PopB/PopD translocation pore in host cell membranes. Infect Immun 72 : 4741 4750.
19. Goure, J., Broz, P., Attree, O., Cornelis, G.R. Attree, I. (2005) Protective anti-V antibodies inhibit Pseudomonas and Yersinia translocon assembly within host membranes. J Infect Dis 192 : 218 225.
20. Hakansson, S., Schesser, K., Persson, C., Galyov, E.E., Rosqvist, R., Homble, F., et al. (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.
21. Johnson, S., Roversi, P., Espina, M., Olive, A., Deane, J.E., Birket, S., et al. (2007) Self-chaperoning of the type III secretion system needle tip proteins IpaD and BipD. J Biol Chem 282 : 4035 4044.
22. Knutton, S., Rosenshine, I., Pallen, M.J., Nisan, I., Neves, B.C., Bain, C., et al. (1998) A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells. EMBO J 17 : 2166 2176.
23. Marenne, M.N., Journet, L., Mota, L.J. Cornelis, G.R. (2003) Genetic Analysis of the formation of the Ysc-Yop translocation pore in macrophages by Yersinia enterocolitica: role of LcrV, YscF and YopN. Microb Pathog 35 : 243 258.
24. Mueller, C.A., Broz, P., Muller, S.A., Ringler, P., Erne-Brand, F., Sorg, I., et al. (2005) The V-antigen of Yersinia forms a distinct structure at the tip of injectisome needles. Science 310 : 674 676.
25. Müller, S.A., Goldie, K.N., Bürki, R., Häring, R. Engel, A. (1992) Factors influencing the precision of quantitative scanning transmission electron microscopy. Ultramicroscopy 46 : 317 334.
26. Neyt, C. 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.
27. Nikolaus, T., Deiwick, J., Rappl, C., Freeman, J.A., Schroder, W., Miller, S.I., et al. (2001) SseBCD proteins are secreted by the type III secretion system of Salmonella pathogenicity island 2 and function as a translocon. J Bacteriol 183 : 6036 6045.
28. Pettersson, J., Holmstrom, A., Hill, J., Leary, S., Frithz-Lindsten, E., von Euler-Matell, A., et al. (1999) The V-antigen of Yersinia is surface exposed before target cell contact and involved in virulence protein translocation. Mol Microbiol 32 : 961 976.
29. Picking, W.L., Nishioka, H., Hearn, P.D., Baxter, M.A., Harrington, A.T., Blocker, A., et al. (2005) IpaD of Shigella flexneri is independently required for regulation of Ipa protein secretion and efficient insertion of IpaB and IpaC into host membranes. Infect Immun 73 : 1432 1440.
30. Robert, V., Volokhina, E.B., Senf, F., Bos, M.P., Van Gelder, P. Tommassen, J. (2006) Assembly factor Omp85 recognizes its outer membrane protein substrates by a species-specific C-terminal motif. PLoS Biol 4 : e377.
31. Rosqvist, R., Magnusson, K.E. Wolf-Watz, H. (1994) Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J 13 : 964 972.
32. Sani, M., Botteaux, A., Parsot, C., Sansonetti, P., Boekema, E.J. Allaoui, A. (2007) IpaD is localized at the tip of the Shigella flexneri type III secretion apparatus. Biochimica et Biophysica Acta 1770 : 307 311.
33. Sanner, M.F., Olson, A.J. Spehner, J.C. (1996) Reduced surface: an efficient way to compute molecular surfaces. Biopolymers 38 : 305 320.
34. Sarker, M.R., Neyt, C., Stainier, I. Cornelis, G.R. (1998) The Yersinia Yop virulon: LcrV is required for extrusion of the translocators YopB and YopD. J Bacteriol 180 : 1207 1214.
35. Saxton, W.O. Baumeister, W. (1982) The correlation averaging of a regularly arranged bacterial cell envelope protein. J Microsc 127 : 127 138.
36. Saxton, W.O., Pitt, T.J. Horner, M. (1979) Digital image processing: the semper system. Ultramicroscopy 4 : 343 354.
37. Sklar, J.G., Wu, T., Gronenberg, L.S., Malinverni, J.C., Kahne, D. Silhavy, T.J. (2007) Lipoprotein SmpA is a component of the YaeT complex that assembles outer membrane proteins in Escherichia coli. Proc Natl Acad Sci USA 104 : 6400 6405.
38. Sorg, I., Wagner, S., Amstutz, M., Muller, S.A., Broz, P., Lussi, Y., et al. (2007) YscU recognizes translocators as export substrates of the Yersinia injectisome. EMBO J 26 : 3015 3024.
39. Sory, M.P., Boland, A., Lambermont, I. 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.
40. 2+. Mol Microbiol 37 : 1005 1018.
41. Veenendaal, A.K., Hodgkinson, J.L., Schwarzer, L., Stabat, D., Zenk, S.F. Blocker, A.J. (2007) The type III secretion system needle tip complex mediates host cell sensing and translocon insertion. Mol Microbiol 63 : 1719 1730.
42. Voulhoux, R., Bos, M.P., Geurtsen, J., Mols, M. Tommassen, J. (2003) Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299 : 262 265.
43. Warawa, J., Finlay, B.B. Kenny, B. (1999) Type III secretion-dependent hemolytic activity of enteropathogenic Escherichia coli. Infect Immun 67 : 5538 5540.
44. Yip, C.K., Finlay, B.B. Strynadka, N.C. (2005) Structural characterization of a type III secretion system filament protein in complex with its chaperone. Nat Struct Mol Biol 12 : 75 81.