Structure of a type III secretion needle at 7-Å resolution provides insights into its assembly and signaling mechanisms

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 12, 2012, Pages 4461-4466

  Fujii, Takashi ^a   Cheung, Martin ^b   Blanco, Amandine ^b   Kato, Takayuki ^a   Blocker, Ariel J ^b   Namba, Keiichi ^a,c  

^a OSAKA UNIVERSITY   (Japan)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c RIKEN Center for Biosystems Dynamics Research   (Japan)

Author keywords

Bacterial protein secretion; Helical image analysis; Shigella pathogenesis

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL PROTEIN MXIH; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BACTERIAL CELL; BACTERIAL NEEDLE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; FLAGELLUM; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; SHIGELLA FLEXNERI; TYPE III SECRETION SYSTEM;

BACTERIAL PROTEINS; CALIBRATION; CELL MEMBRANE; CRYOELECTRON MICROSCOPY; IMAGE PROCESSING, COMPUTER-ASSISTED; MODELS, MOLECULAR; MOLECULAR CONFORMATION; POLYMERS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SHIGELLA FLEXNERI; SIGNAL TRANSDUCTION; TEMPERATURE;

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

EID: 84858633508     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1116126109     Document Type: Article

References (36)

1. Cornelis GR (2006) The type III secretion injectisome. Nat Rev Microbiol 4:811-825.
2. Blocker A, Komoriya K, Aizawa S (2003) Type III secretion systems and bacterial flagella: Insights into their function from structural similarities. Proc Natl Acad Sci USA 100:3027-3030.
3. Blocker A, et al. (2001) Structure and composition of the Shigella flexneri "needle complex,"a part of its type III secreton. Mol Microbiol 39:652-663.
4. Cordes FS, et al. (2003) Helical structure of the needle of the type III secretion system of Shigella flexneri. J Biol Chem 278:17103-17107.
5. Kenjale R, et al. (2005) The needle component of the type III secreton of Shigella regulates the activity of the secretion apparatus. J Biol Chem 280:42929-42937.
6. Schroeder GN, Hilbi H (2008) Molecular pathogenesis of Shigellaspp: Controlling host cell signaling, invasion, and death by type III secretion. Clin Microbiol Rev 21:134-156.
7. Blocker A, et al. (1999) The tripartite type III secreton of Shigella flexneri inserts IpaB and IpaC into host membranes. J Cell Biol 147:683-693.
8. Hodgkinson JL, et al. (2009) Three-dimensional reconstruction of the Shigella T3SS transmembrane regions reveals 12-fold symmetry and novel features throughout. Nat Struct Mol Biol 16:477-485.
9. Veenendaal AK, et al. (2007) The type III secretion system needle tip complex mediates host cell sensing and translocon insertion. Mol Microbiol 63:1719-1730.
10. Torruellas J, Jackson MW, Pennock JW, Plano GV (2005) The Yersinia pestis type III secretion needle plays a role in the regulation of Yop secretion. Mol Microbiol 57:1719-1733.
11. Blocker AJ, et al. (2008) What's the point of the type III secretion system needle? Proc Natl Acad Sci USA 105:6507-6513.
12. Deane JE, 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.
13. Poyraz O, et al. (2010) Protein refolding is required for assembly of the type three secretion needle. Nat Struct Mol Biol 17:788-792.
14. Cordes FS, et al. (2005) Helical packing of needles from functionally altered Shigella type III secretion systems. J Mol Biol 354:206-211.
15. Galkin VE, Schmied WH, Schraidt O, Marlovits TC, Egelman EH (2010) The structure of the Salmonella typhimurium type III secretion system needle shows divergence from the flagellar system. J Mol Biol 396:1392-1397.
16. Fujii T, Iwane AH, Yanagida T, Namba K (2010) Direct visualization of secondary structures of F-actin by electron cryomicroscopy. Nature 467:724-728.
17. Fujii T, Kato T, Namba K (2009) Specific arrangement of alpha-helical coiled coils in the core domain of the bacterial flagellar hook for the universal joint function. Structure 17:1485-1493.
18. Wang Y, et al. (2007) Differences in the electrostatic surfaces of the type III secretion needle proteins PrgI, BsaL, and MxiH. J Mol Biol 371:1304-1314.
19. Zhang L, Wang Y, Picking WL, Picking WD, De Guzman RN (2006) Solution structure of monomeric BsaL, the type III secretion needle protein of Burkholderia pseudomallei. J Mol Biol 359:322-330.
20. Samatey FA, et al. (2004) Structure of the bacterial flagellar hook and implication for the molecular universal joint mechanism. Nature 431:1062-1068.
21. Yonekura K, Maki-Yonekura S, Namba K (2003) Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424:643-650.
22. Quinaud M, et al. (2007) Structure of the heterotrimeric complex that regulates type III secretion needle formation. Proc Natl Acad Sci USA 104:7803-7808.
23. Sun P, Tropea JE, Austin BP, Cherry S, Waugh DS (2008) Structural characterization of the Yersinia pestis type III secretion system needle protein YscF in complex with its heterodimeric chaperone YscE/YscG. J Mol Biol 377:819-830.
24. Yonekura K, et al. (2000) The bacterial flagellar cap as the rotary promoter of flagellin self-assembly. Science 290:2148-2152.
25. Sory MP, Cornelis GR (1994) Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol Microbiol 14:583-594.
26. Sorg I, et al. (2007) YscU recognizes translocators as export substrates of the Yersinia injectisome. EMBO J 26:3015-3024.
27. 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.
28. Iino T (1969) Polarity of flagellar growth in salmonella. J Gen Microbiol 56:227-239.
29. 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.
30. 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.
31. Erhardt M, et al. (2010) The role of the FliK molecular ruler in hook-length control in Salmonella enterica. Mol Microbiol 75:1272-1284.
32. Wagner S, et al. (2009) The helical content of the YscP molecular ruler determines the length of the Yersinia injectisome. Mol Microbiol 71:692-701.
33. Erhardt M, Singer HM,Wee DH, Keener JP, Hughes KT (2011) An infrequent molecular ruler controls flagellar hook length in Salmonella enterica. EMBO J 30:2948-2961.
34. Samatey FA, et al. (2001) Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling. Nature 410:331-337.
35. Maki-Yonekura S, Yonekura K, Namba K (2010) Conformational change of flagellin for polymorphic supercoiling of the flagellar filament. Nat Struct Mol Biol 17:417-422.
36. Egelman EH (2000) A robust algorithm for the reconstruction of helical filaments using single-particle methods. Ultramicroscopy 85:225-234.