The role of the FliK molecular ruler in hook-length control in Salmonella enterica

Molecular Microbiology

Volumn 75, Issue 5, 2010, Pages 1272-1284

  Erhardt, Marc ^a   Hirano, Takanori ^a   Su, Yichu ^a   Paul, Koushik ^a   Wee, Daniel H ^a   Mizuno, Shino ^b   Aizawa, Shin Ichi ^b   Hughes, Kelly T ^a  

^a UNIVERSITY OF UTAH   (United States)

^b PREFECTURAL UNIVERSITY OF HIROSHIMA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FLIG PROTEIN; FLIK PROTEIN; FLIM PROTEIN; FLIN PROTEIN; UNCLASSIFIED DRUG; FLIK PROTEIN, SALMONELLA;

ARTICLE; BACTERIAL FLAGELLUM; GENE DELETION; GENE EXPRESSION; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN SECRETION; SALMONELLA ENTERICA; WILD TYPE; BIOLOGICAL MODEL; FLAGELLUM; GENETICS; METABOLISM;

SALMONELLA ENTERICA;

BACTERIAL PROTEINS; FLAGELLA; GENE DELETION; MODELS, BIOLOGICAL; SALMONELLA ENTERICA;

EID: 77349103262     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07050.x     Document Type: Article

References (46)

1. Agrain, C., Callebaut, I., Journet, L., Sorg, I., Paroz, C., Mota, L.J. Cornelis, G.R. (2005) Characterization of a Type III secretion substrate specificity switch (T3S4) domain in YscP from Yersinia enterocolitica. Mol Microbiol 56 : 54 67.
2. Berg, H.C. Anderson, R.A. (1973) Bacteria swim by rotating their flagellar filaments. Nature 245 : 380 382.
3. Brown, J.D., Saini, S., Aldridge, C., Herbert, J., Rao, C.V. Aldridge, P.D. (2008) The rate of protein secretion dictates the temporal dynamics of flagellar gene expression. Mol Microbiol 70 : 924 937.
4. Chevance, F.F.V. Hughes, K.T. (2008) Coordinating assembly of a bacterial macromolecular machine. Nat Rev Microbiol 6 : 455 465.
5. Chevance, F.F.V., Takahashi, N., Karlinsey, J.E., Gnerer, J., Hirano, T., Samudrala, R., et al. (2007) The mechanism of outer membrane penetration by the eubacterial flagellum and implications for spirochete evolution. Genes Dev 21 : 2326 2335.
6. Cornelis, G.R. (2006) The type III secretion injectisome. Nat Rev Microbiol 4 : 811 825.
7. Erhardt, M. Hughes, K.T. (2010) C-ring requirement in flagellar type III secretion is bypassed by FlhDC upregulation. Mol Microbiol 75 : 376 393.
8. Ferris, H.U., Furukawa, Y., Minamino, T., Kroetz, M.B., Kihara, M., Namba, K. Macnab, R.M. (2005) FlhB regulates ordered export of flagellar components via autocleavage mechanism. J Biol Chem 280 : 41236 41242.
9. Galan, J.E. Wolf-Watz, H. (2006) Protein delivery into eukaryotic cells by type III secretion machines. Nature 444 : 567 573.
10. Goodier, R.I. Ahmer, B.M. (2001) SirA orthologs affect both motility and virulence. J Bacteriol 183 : 2249 2258.
11. 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.
12. Hirano, T., Shibata, S., Ohnishi, T. Aizawa, S. (2005) N-terminal signal region of FliK is dispensable for length control of the flagellar hook. Mol Microbiol 56 : 346 360.
13. Journet, L., Agrain, C., Broz, P. Cornelis, G.R. (2003) The needle length of bacterial injectisomes is determined by a molecular ruler. Science 302 : 1757 1760.
14. Karlinsey, J.E., Tanaka, S., Bettenworth, V., Yamaguchi, S., Boos, W., Aizawa, S.I. Hughes, K.T. (2000) Completion of the hook-basal body complex of the Salmonella typhimurium flagellum is coupled to FlgM secretion and fliC transcription. Mol Microbiol 37 : 1220 1231.
15. Kawagishi, I., Homma, M., Williams, A.W. Macnab, R.M. (1996) Characterization of the flagellar hook length control protein fliK of Salmonella typhimurium and Escherichia coli. J Bacteriol 178 : 2954 2959.
16. Kojima, S. Blair, D.F. (2004) The bacterial flagellar motor: structure and function of a complex molecular machine. Int Rev Cytol 233 : 93 134.
17. Konishi, M., Kanbe, M., McMurry, J.L. Aizawa, S.I. (2009) Flagellar formation in C-ring defective mutants by overproduction of FliI, the ATPase specific for the flagellar type III secretion. J Bacteriol 191 : 6186 6191.
18. Koroyasu, S., Yamazato, M., Hirano, T. 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.
19. Kutsukake, K., Minamino, T. Yokoseki, T. (1994) Isolation and characterization of FliK-independent flagellation mutants from Salmonella typhimurium. J Bacteriol 176 : 7625 7629.
20. Lee, H.J. Hughes, K.T. (2006) Posttranscriptional control of the Salmonella enterica flagellar hook protein FlgE. J Bacteriol 188 : 3308 3316.
21. Macnab, R.M. (1996) Flagella and motility. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. Neidhardt, F.C., Curtiss, R., III., Ingraham, J.L., Lin, E.C.C., Low, K.B., Magasanik, B. et al. (eds). Washington, DC : ASM Press, pp. 123 145.
22. Macnab, R. (2003) How bacteria assemble flagella. Annu Rev Microbiol 57 : 77 100.
23. Macnab, R.M. (2004) Type III flagellar protein export and flagellar assembly. Biochim Biophys Acta 1694 : 207 217.
24. Makishima, S., Komoriya, K., Yamaguchi, S. Aizawa, S.I. (2001) Length of the flagellar hook and the capacity of the type III export apparatus. Science 291 : 2411 2413.
25. Minamino, T. Macnab, R.M. (2000) Domain structure of Salmonella FlhB, a flagellar export component responsible for substrate specificity switching. J Bacteriol 182 : 4906 4914.
26. Minamino, T. Pugsley, A.P. (2005) Measure for measure in the control of type III secretion hook and needle length. Mol Microbiol 56 : 303 308.
27. Minamino, T., Iino, T. Kutuskake, K. (1994) Molecular characterization of the Salmonella typhimurium flhB operon and its protein products. J Bacteriol 176 : 7630 7637.
28. Minamino, T., González-Pedrajo, B., Yamaguchi, K., Aizawa, S.I. Macnab, R.M. (1999) FliK, the protein responsible for flagellar hook length control in Salmonella, is exported during hook assembly. Mol Microbiol 34 : 295 304.
29. Minamino, T., Ferris, H.U., Moriya, N., Kihara, M. Namba, K. (2006) Two parts of the T3S4 domain of the hook-length control protein FliK are essential for the substrate specificity switching of the flagellar type III export apparatus. J Mol Biol 362 : 1148 1158.
30. Minamino, T., Moriya, N., Hirano, T., Hughes, K.T. Namba, K. (2009) Interaction of FliK with the bacterial flagellar hook is required for efficient export specificity switching. Mol Microbiol 74 : 239 251.
31. Moriya, N., Minamino, T., Hughes, K.T., Macnab, R.M. Namba, K. (2006) The type III flagellar export specificity switch is dependent on FliK ruler and a molecular clock. J Mol Biology 359 : 466 477.
32. Morrissey, J.H. (1981) Silver stain for proteins in polyacrylamide gels: a modified procedure with enhanced uniform sensitivity. Anal Biochem 117 : 307 310.
33. Muramoto, K., Makishima, S., Aizawa, S.I. Macnab, R.M. (1998) Effect of cellular level of FliK on flagellar hook and filament assembly in Salmonella typhimurium. J Mol Biol 277 : 871 882.
34. Muramoto, K., Makishima, S., Aizawa, S. Macnab, R.M. (1999) Effect of hook subunit concentration on assembly and control of length of the flagellar hook of Salmonella. J Bacteriol 181 : 5808 5813. (Pubitemid 29437154)
35. Patterson-Delafield, J., Martinez, R.J., Stocker, B.A. Yamaguchi, S. (1973) A new fla gene in Salmonella typhimurium- flaR- and its mutant phenotype-superhooks. Archiv Mikrobiologie 90 : 107 120.
36. Paul, K., Harmon, J.G. Blair, D.F. (2006) Mutational analysis of the flagellar rotor protein FliN: identification of surfaces important for flagellar assembly and switching. J Bacteriol 188 : 5240 5248.
37. Paul, K., Erhardt, M., Hirano, T., Blair, D.F. Hughes, K.T. (2008) Energy source of flagellar type III secretion. Nature 451 : 489 492.
38. Samatey, F., Matsunami, H., Imada, K., Nagashima, S., Shaikh, T., Thomas, D., et al. (2004) Structure of the bacterial flagellar hook and implication for the molecular universal joint mechanism. Nature 431 : 1062 1068.
39. Sanderson, K.E. Roth, J.R. (1983) Linkage map of Salmonella typhimurium, Edition VI. Microbiol Rev 47 : 410 453.
40. Shaikh, T.R., Thomas, D.R., Chen, J.Z., Samatey, F.A., Matsunami, H., Imada, K., et al. (2005) A partial atomic structure for the flagellar hook of Salmonella typhimurium. Proc Natl Acad Sci USA 102 : 1023 1028.
41. Shibata, S., Takahashi, N., Chevance, F.F.V., Karlinsey, J.E., Hughes, K.T. Aizawa, S. (2007) FliK regulates flagellar hook length as an internal ruler. Mol Microbiol 64 : 1404 1415.
42. Thomas, D.R., Francis, N.R., Xu, C. DeRosier, D.J. (2006) The three-dimensional structure of the flagellar rotor from a clockwise-locked mutant of Salmonella enterica serovar Typhimurium. J Bacteriol 188 : 7039 7048.
43. Wagner, S., Sorg, I., Degiacomi, M., Journet, L., Dal Peraro, M. Cornelis, G.R. (2009) The helical content of the YscP molecular ruler determines the length of the Yersinia injectisome. Mol Microbiol 71 : 692 701.
44. Williams, A.W., Yamaguchi, S., Togashi, F., Aizawa, S.I., Kawagishi, I. Macnab, R.M. (1996) Mutations in fliK and flhB affecting flagellar hook and filament assembly in Salmonella typhimurium. J Bacteriol 178 : 2960 2970.
45. Yonekura, K., Maki-Yonekura, S. Namba, K. (2003) Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424 : 643 650.
46. Zarivach, R., Deng, W., Vuckovic, M., Felise, H.B., Nguyen, H.V., Miller, S.I., et al. (2008) Structural analysis of the essential self-cleaving type III secretion proteins EscU and SpaS. Nature 453 : 124 127.