The Salmonella type III secretion system virulence effector forms a new hexameric chaperone assembly for export of effector/chaperone complexes

Journal of Bacteriology

Volumn 197, Issue 4, 2015, Pages 672-675

  Tsai, Chi Lin ^a   Burkinshaw, Brianne J ^b   Strynadka, Natalie C J ^b   Tainer, John A ^a  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CHAPERONE; DIMER; BACTERIAL PROTEIN; SIGE PROTEIN, BACTERIA; SIGMA FACTOR; SOPB PROTEIN, BACTERIA;

AMINO ACID COMPOSITION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; BACTERIAL VIRULENCE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; GENETIC ANALYSIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; NONHUMAN; NOTE; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN SECRETION; RADIATION SCATTERING; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; TYPE III SECRETION SYSTEM; X RAY CRYSTALLOGRAPHY; CHEMISTRY; METABOLISM; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM;

BACTERIA (MICROORGANISMS); EUKARYOTA; SALMONELLA; SIGE;

BACTERIAL PROTEINS; MOLECULAR CHAPERONES; SALMONELLA TYPHIMURIUM; SIGMA FACTOR;

EID: 84921812568     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02524-14     Document Type: Note

References (33)

1. Cornelis GR. 2006. The type III secretion injectisome. Nat Rev Microbiol 4:811-825. http://dx.doi.org/10.1038/nrmicro1526.
2. Burkinshaw BJ, Strynadka NCJ. 2014. Assembly and structure of the T3SS. Biochim Biophys Acta 1843:1649-1663. http://dx.doi.org/10.1016/j.bbamcr.2014.01.035.
3. Abrusci P, Vergara-Irigaray M, Johnson S, Beeby MD, Hendrixson DR, Roversi P, Friede ME, Deane JE, Jensen GJ, Tang CM, Lea SM. 2013. Architecture of the major component of the type III secretion system export apparatus. Nat Struct Mol Biol 20:99-104. http://dx.doi.org/10.1038/nsmb.2452.
4. Romo-Castillo M, Andrade A, Espinosa N, Monjarás Feria J, Soto E, Díaz-Guerrero M, González-Pedrajo B. 2014. EscO, a functional and structural analog of the flagellar FliJ protein, is a positive regulator of EscN ATPase activity of the enteropathogenic Escherichia coli injectisome. J Bacteriol 196:2227-2241. http://dx.doi.org/10.1128/JB.01551-14.
5. Zarivach R, Vuckovic M, Deng W, Finlay BB, Strynadka NCJ. 2007. Structural analysis of a prototypical ATPase from the type III secretion system. Nat Struct Mol Biol 14:131-137. http://dx.doi.org/10.1038/nsmb1196.
6. Kawamoto A, Morimoto YV, Miyata T, Minamino T, Hughes KT, Kato T, Namba K. 2013. Common and distinct structural features of Salmonella injectisome and flagellar basal body. Sci Rep 3:3369. http://dx.doi.org/10.1038/srep03369.
7. Wood SE, Jin J, Lloyd SA. 2008. YscP and YscU switch the substrate specificity of the Yersinia type III secretion system by regulating export of the inner rod protein YscI. J Bacteriol 190:4252-4262. http://dx.doi.org/10.1128/JB.00328-08.
8. Lefebre MD, Galán JE. 2014. The inner rod protein controls substrate switching and needle length in a Salmonella type III secretion system. Proc Natl Acad Sci U S A 111:817-822. http://dx.doi.org/10.1073/pnas.1319698111.
9. Mota LJ, Journet L, Sorg I, Agrain C, Cornelis GR. 2005. Bacterial injectisomes: needle length does matter. Science 307:1278. http://dx.doi.org/10.1126/science.1107679.
10. Radics J, Königsmaier L, Marlovits TC. 2014. Structure of a pathogenic type 3 secretion system in action. Nat Struct Mol Biol 21:82-87. http://dx.doi.org/10.1038/nsmb.2722.
11. Akeda Y, Galán JE. 2005. Chaperone release and unfolding of substrates in type III secretion. Nature 437:911-915. http://dx.doi.org/10.1038/nature03992.
12. Stebbins CE, Galán JE. 2001. Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature 414:77-81. http://dx.doi.org/10.1038/35102073.
13. Lilic M, Vujanac M, Stebbins CE. 2006. A common structural motif in the binding of virulence factors to bacterial secretion chaperones. Mol Cell 21:653-664. http://dx.doi.org/10.1016/j.molcel.2006.01.026.
14. Roblin P, Dewitte F, Villeret V, Biondi EG, Bompard C. 2015. A Salmonella type three secretion effector/chaperone complex adopts a hexameric ring-like structure. J Bacteriol 197:688-698. http://dx.doi.org/10.1128/JB.02294-14.
15. Roblin P, Lebrun P, Rucktooa P, Dewitte F, Lens Z, Receveur-Brechot V, Raussens V, Villeret V, Bompard C. 2013. The structural organization of the N-terminus domain of SopB, a virulence factor of Salmonella, depends on the nature of its protein partners. Biochim Biophys Acta 1834::2564-2572. http://dx.doi.org/10.1016/j.bbapap.2013.09.014.
16. Luo Y, Bertero MG, Frey EA, Pfuetzner RA, Wenk MR, Creagh L, Marcus SL, Lim D, Sicheri F, Kay C, Haynes C, Finlay BB, Strynadka NC. 2001. Structural and biochemical characterization of the type III secretion chaperones CesT and SigE. Nat Struct Biol 8:1031-1036. http://dx.doi.org/10.1038/nsb717.
17. Claret L, Calder SR, Higgins M, Hughes C. 2003. Oligomerization and activation of the FliI ATPase central to bacterial flagellum assembly. Mol Microbiol 48:1349-1355. http://dx.doi.org/10.1046/j.1365-2958.2003.03506.x.
18. Reindl S, Ghosh A, Williams GJ, Lassak K, Neiner T, Hernche A-L, Alberts S-V, Tainer JA. 2013. Insights into FlaI functions in archaeal motor assembly and motility from structures, conformations, and genetics. Mol Cell 49:1069-1082. http://dx.doi.org/10.1016/j.molcel.2013.01.014.
19. Minamino T, Morimoto YV, Hara N, Namba K. 2011. An energy transduction mechanism used in bacterial flagellar type III protein export. Nat Commun 2:475. http://dx.doi.org/10.1038/ncomms1488.
20. Ibuki T, Imada K, Minamino T, Kato T, Miyata T, Namba K. 2011. Common architecture of the flagellar type III protein export apparatus and F- and V-type ATPases. Nat Struct Mol Biol 18:277-282. http://dx.doi.org/10.1038/nsmb.1977.
21. Arnold R, Brandmaier S, Kleine F, Tischler P, Heinz E, Behrens S, Niinikoski A, Mewes H-W, Horn M, Rattei T. 2009. Sequence-based prediction of type III secreted proteins. PLoS Pathog 5:e1000376. http://dx.doi.org/10.1371/journal.ppat.1000376.
22. Dean P. 2011. Functional domains and motifs of bacterial type III effector proteins and their roles in infection. FEMS Microbiol Rev 35:1100-1125. http://dx.doi.org/10.1111/j.1574-6976.2011.00271.x.
23. Allison SE, Tuinema BR, Everson ES, Sugiman-Marangos S, Zhang K, Junop MS, Coombes BK. 2014. Identification of the docking site between a type III secretion system ATPase and a chaperone for effector cargo. J Biol Chem 289:23734-23744. http://dx.doi.org/10.1074/jbc. M114.578476.
24. Minamino T, Kazetani K-I, Tahara A, Suzuki H, Furukawa Y, Kihara M, Namba K. 2006. Oligomerization of the bacterial flagellar ATPase FliI is controlled by its extreme N-terminal region. J Mol Biol 360:510-519. http://dx.doi.org/10.1016/j.jmb.2006.05.010.
25. Akeda Y, Galán JE. 2004. Genetic analysis of the Salmonella enterica type III secretion-associated ATPase InvC defines discrete functional domains. J Bacteriol 186:2402-2412. http://dx.doi.org/10.1128/JB.186.8.2402-2412.2004.
26. Pozidis C, Chalkiadaki A, Gomez-Serrano A, Stahlberg H, Brown I, Tampakaki AP, Lustig A, Sianidis G, Politou AS, Engel A, Panopoulos NJ, Mansfield J, Pugsley AP, Karamanou S, Economou A. 2003. Type III protein translocase: HrcN is a peripheral ATPase that is activated by oligomerization. J Biol Chem 278:25816-25824. http://dx.doi.org/10.1074/jbc. M301903200.
27. Mills E, Baruch K, Aviv G, Nitzan M, Rosenshine I. 2013. Dynamics of the type III secretion system activity of enteropathogenic Escherichia coli. mBio 4:e00303-13. http://dx.doi.org/10.1128/mBio.00303-13.
28. Schlumberger MC, Müller AJ, Ehrbar K, Winnen B, Duss I, Stecher B, Hardt W-D. 2005. Real-time imaging of type III secretion: Salmonella SipA injection into host cells. Proc Natl Acad Sci U S A 102:12548-12553. http://dx.doi.org/10.1073/pnas.0503407102.
29. Mills E, Baruch K, Charpentier X, Kobi S, Rosenshine I. 2008. Real-time analysis of effector translocation by the type III secretion system of enteropathogenic Escherichia coli. Cell Host Microbe 3:104-113. http://dx.doi.org/10.1016/j.chom.2007.11.007.
30. Craig L, Pique ME, Tainer JA. 2004. Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2:363-378. http://dx.doi.org/10.1038/nrmicro885.
31. Craig L, Volkmann N, Arvai AS, Pique ME, Yeager M, Egelman EH, Tainer JA. 2006. Type IV pilus structure by cryo-electron microscopy and crystallography: implications for pilus assembly and functions. Mol Cell 23:651-662. http://dx.doi.org/10.1016/j.molcel.2006.07.004.
32. Hura GL, Budworth H, Dyer KN, Rambo RP, Hammel M, McMurray CT, Tainer JA. 2013. Comprehensive macromolecular conformations mapped by quantitative SAXS analyses. Nat Methods 10:453-454. http://dx.doi.org/10.1038/nmeth.2453.
33. Rambo RP, Tainer JA. 2013. Accurate assessment of mass, models and resolution by small-angle scattering. Nature 496:477-481. http://dx.doi.org/10.1038/nature12070.