YscU recognizes translocators as export substrates of the Yersinia injectisome

EMBO Journal

Volumn 26, Issue 12, 2007, Pages 3015-3024

  Sorg, Isabel ^a   Wagner, Stefanie ^a   Amstutz, Marlise ^a   Müller, Shirley A ^a   Broz, Petr ^a   Lussi, Yvonne ^a   Engel, Andreas ^a   Cornelis, Guy R ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Effectors; Targeting; Translocation; Type III secretion; Yops

Indexed keywords

BACTERIAL PROTEIN; CARRIER PROTEIN; PROTEIN LCRV; PROTEIN YOPB; PROTEIN YOPD; PROTEIN YSCU; UNCLASSIFIED DRUG; YERSINIA OUTER PROTEIN E;

ARTICLE; BACTERIUM MUTANT; INJECTISOME; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN SECRETION; PROTEIN TRANSPORT; TYPE III SECRETION SYSTEM; YERSINIA;

BACTERIAL PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; MUTATION; PROTEIN BINDING; PROTEIN TRANSPORT; YERSINIA;

YERSINIA;

EID: 34250840609     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601731     Document Type: Article

References (53)

1. Agrain C, Callebaut I, Journet L, Sorg I, Paroz C, Mota LJ, Cornelis GR (2005a) Characterization of a type III secretion substrate specificity switch (T3S4) domain in YscP from Yersinia enterocolitica. Mol Microbiol 56: 54-67
2. Agrain C, Sorg I, Paroz C, Cornelis GR (2005b) Secretion of YscP from Yersinia enterocolitica is essential to control the length of the injectisome needle but not to change the type III secretion substrate specificity. Mol Microbiol 57: 1415-1427
3. 2+ dependency, is related to exsB of Pseudomonas aeruginosa. J Bacteriol 177: 4230-4237
4. Allaoui A, Woestyn S, Sluiters C, Cornelis GR (1994) YscU, a Yersinia enterocolitica inner membrane protein involved in Yop secretion. J Bacteriol 176: 4534-4542
5. Anderson DM, Schneewind O (1997) A mRNA signal for the type III secretion of Yop proteins by Yersinia enterocolitica. Science 278: 1140-1143
6. Anderson DM, Schneewind O (1999) Yersinia enterocolitica type III secretion: an mRNA signal that couples translation and secretion of YopQ. Mol Microbiol 31: 1139-1148
7. Blocker A, Gounon P, Larquet E, Niebuhr K, Cabiaux V, Parsot C, 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. Blocker A, Jouihri N, Larquet E, Gounon P, Ebel F, Parsot C, Sansonetti P, Allaoui A (2001) Structure and composition of the Shigella flexneri 'needle complex', a part of its type III secreton. Mol Microbiol 39: 652-663
9. Burghout P, Beckers F, de Wit E, van Boxtel R, Cornelis GR, Tommassen J, Koster M (2004) Role of the pilot protein YscW in the biogenesis of the YscC secretin in Yersinia enterocolitica. J Bacteriol 186: 5366-5375
10. Cornelis G, Vanootegem JC, Sluiters C (1987) Transcription of the yop regulon from Y. enterocolitica requires trans acting pYV and chromosomal genes. Microb Pathog 2: 367-379
11. Cornelis GR (2006) The type III secretion injectisome. Nat Rev Microbiol 4: 811-825
12. Cornelis GR, Wolf-Watz H (1997) The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol Microbiol 23: 861-867
13. Crepin VF, Shaw R, Abe CM, Knutton S, Frankel G (2005) Polarity of enteropathogenic Escherichia coli EspA filament assembly and protein secretion. J Bacteriol 187: 2881-2889
14. Daniell SJ, Takahashi N, Wilson R, Friedberg D, Rosenshine I, Booy FP, Shaw RK, Knutton S, Frankel G, Aizawa S (2001) The filamentous type III secretion translocon of enteropathogenic Escherichia coli. Cell Microbiol 3: 865-871
15. Deng W, Li Y, Hardwidge PR, Frey EA, Pfuetzner RA, Lee S, Gruenheid S, Strynakda NC, Puente JL, Finlay BB (2005) Regulation of type III secretion hierarchy of translocators and effectors in attaching and effacing bacterial pathogens. Infect Immun 73: 2135-2146
16. Ferris HU, Furukawa Y, Minamino T, Kroetz MB, Kihara M, Namba K, Macnab RM (2005) FlhB regulates ordered export of flagellar components via autocleavage mechanism. J Biol Chem 280: 41236-41242
17. Ferris HU, Minamino T (2006) Flipping the switch: bringing order to flagellar assembly. Trends Microbiol 14: 519-526
18. Fields KA, Nilles ML, Cowan C, Straley SC (1999) Virulence role of V antigen of Yersinia pestis at the bacterial surface. Infect Immun 67: 5395-5408
19. Fraser GM, Gonzalez-Pedrajo B, Tame JR, Macnab RM (2003) Interactions of FliJ with the Salmonella type III flagellar export apparatus. J Bacteriol 185: 5546-5554
20. Galan JE, Wolf-Watz H (2006) Protein delivery into eukaryotic cells by type III secretion machines. Nature 444: 567-573
21. Goure J, Broz P, Attree O, Cornelis GR, Attree I (2005) Protective anti-v antibodies inhibit Pseudomonas and Yersinia translocon assembly within host membranes. J Infect Dis 192: 218-225
22. Hakansson S, Schesser K, Persson C, Galyov EE, Rosqvist R, Homble F, 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. Hirano T, Yamaguchi S, Oosawa K, Aizawa S (1994) Roles of FliK and FlhB in determination of flagellar hook length in Salmonella typhimurium. J Bacteriol 176: 5439-5449
24. Hoiczyk E, Blobel G (2001) Polymerization of a single protein of the pathogen Yersinia enterocolitica into needles punctures eukaryotic cells. Proc Natl Acad Sci USA 98: 4669-4674
25. Journet L, Agrain C, Broz P, Cornelis GR (2003) The needle length of bacterial injectisomes is determined by a molecular ruler. Science 302: 1757-1760
26. Kaniga K, Delor I, Cornelis GR (1991) A wide-host-range suicide vector for improving reverse genetics in Gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica. Gene 109: 137-141
27. Knutton S, Rosenshine I, Pallen MJ, Nisan I, Neves BC, Bain C, Wolff C, Dougan G, Frankel G (1998) A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells. EMBO J 17: 2166-2176
28. Kubori T, Galan JE (2002) Salmonella type III secretion-associated protein InvE controls translocation of effector proteins into host cells. J Bacteriol 184: 4699-4708
29. Kubori T, Matsushima Y, Nakamura D, Uralil J, Lara-Tejero M, Sukhan A, Galan JE, Aizawa SI (1998) Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280: 602-605
30. Kubori T, Sukhan A, Aizawa SI, Galan JE (2000) Molecular characterization and assembly of the needle complex of the Salmonella typhimurium type III protein secretion system. Proc Natl Acad Sci USA 97: 10225-10230
31. Kutsukake K, Minamino T, Yokoseki T (1994) Isolation and characterization of FliK-independent flagellation mutants from Salmonella typhimurium. J Bacteriol 176: 7625-7629
32. Lavander M, Sundberg L, Edqvist PJ, Lloyd SA, Wolf-Watz H, Forsberg A (2002) Proteolytic cleavage of the FlhB homologue YscU of Yersinia pseudotuberculosis is essential for bacterial survival but not for type III secretion. J Bacteriol 184: 4500-4509
33. Lavander M, Sundberg L, Edqvist PJ, Lloyd SA, Wolf-Watz H, Forsberg A (2003) Characterisation of the type III secretion protein YscU in Yersinia pseudotuberculosis. YscU cleavage - dispensable for TTSS but essential for survival. Adv Exp Med Biol 529: 109-112
34. Li CM, Brown I, Mansfield J, Stevens C, Boureau T, Romantschuk M, Taira S (2002) The Hrp pilus of Pseudomonas syringae elongates from its tip and acts as a conduit for translocation of the effector protein HrpZ. EMBO J 21: 1909-1915
35. Macnab RM (2003) How bacteria assemble flagella. Annu Rev Microbiol 57: 77-100
36. Magdalena J, Hachani A, Chamekh M, Jouihri N, Gounon P, Blocker A, Allaoui A (2002) Spa32 regulates a switch in substrate specificity of the type III secreton of Shigella flexneri from needle components to Ipa proteins. J Bacteriol 184: 3433-3441
37. Marenne MN, Journet L, Mota LJ, Cornelis GR (2003) Genetic analysis of the formation of the Ysc-Yop translocation pore in macrophages by Yersinia enterocolitica: role of LcrV, yscF and YopN. Microb Pathogen 35: 243-258
38. Marlovits TC, Kubori T, Sukhan A, Thomas DR, Galan JE, Unger VM (2004) Structural insights into the assembly of the type iii secretion needle complex. Science 306: 1040-1042
39. Michiels T, Cornelis GR (1991) Secretion of hybrid proteins by the Yersinia Yop export system. J Bacteriol 173: 1677-1685
40. Minamino T, Macnab RM (2000) Domain structure of Salmonella FlhB, a flagellar export component responsible for substrate specificity switching. J Bacteriol 182: 4906-4914
41. Morita-Ishihara T, Ogawa M, Sagara H, Yoshida M, Katayama E, Sasakawa C (2006) Shigella Spa33 is an essential C-ring component of type III secretion machinery. J Biol Chem 281: 599-607
42. Moriya N, Minamino T, Hughes KT, Macnab RM, Namba K (2006) The type III flagellar export specificity switch is dependent on FliK ruler and a molecular clock. J Mol Biol 359: 466-477
43. Mota LJ, Cornelis GR (2005) The bacterial injection kit: type III secretion systems. Ann Med 37: 234-249
44. Mota LJ, Journet L, Sorg I, Agrain C, Cornelis GR (2005) Bacterial injectisomes: needle length does matter. Science 307: 1278
45. Mueller CA, Broz P, Muller SA, Ringler P, Erne-Brand F, Sorg I, Kuhn M, Engel A, Cornelis GR (2005) The V-antigen of Yersinia forms a distinct structure at the tip of injectisome needles. Science 310: 674-676
46. Sory MP, Boland A, Lambermont I, Cornelis GR (1995) Identi-fication 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
47. 2+. Mol Microbiol 37: 1005-1018
48. Sukhan A, Kubori T, Wilson J, Galan JE (2001) Genetic analysis of assembly of the Salmonella enterica serovar Typhimurium type III secretion-associated needle complex. J Bacteriol 183: 1159-1167
49. Tamano K, Katayama E, Toyotome T, 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
50. Tampakaki AP, Fadouloglou VE, Gazi AD, Panopoulos NJ, Kokkinidis M (2004) Conserved features of type III secretion. Cell Microbiol 6: 805-816
51. Van Gijsegem F, Vasse J, Camus JC, Marenda M, Boucher C (2000) Ralstonia solanacearum produces hrp-dependent pili that are required for PopA secretion but not for attachment of bacteria to plant cells. Mol Microbiol 36: 249-260
52. Williams AW, Yamaguchi S, Togashi F, Aizawa SI, Kawagishi I, Macnab RM (1996) Mutations in fliK and flhB affecting flagellar hook and filament assembly in Salmonella typhimurium. J Bacteriol 178: 2960-2970
53. Zhu K, Gonzalez-Pedrajo B, Macnab RM (2002) Interactions among membrane and soluble components of the flagellar export apparatus of Salmonella. Biochemistry 41: 9516-9524