Interactions of bacterial flagellar chaperone-substrate complexes with FlhA contribute to co-ordinating assembly of the flagellar filament

Molecular Microbiology

Volumn 90, Issue 6, 2013, Pages 1249-1261

  Kinoshita, Miki ^a   Hara, Noritaka ^a   Imada, Katsumi ^a   Namba, Keiichi ^a,b   Minamino, Tohru ^a  

^a OSAKA UNIVERSITY   (Japan)

^b RIKEN Center for Biosystems Dynamics Research   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; CHAPERONE SUBSTRATE COMPLEX; FLGK PROTEIN; FLGL PROTEIN; FLGN FLGK COMPLEX; FLHA PROTEIN; FLIC PROTEIN; FLID PROTEIN; FLIS FLIC COMPLEX; FLIT FLID COMPLEX; HYBRID PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL FLAGELLUM; BINDING AFFINITY; CONTROLLED STUDY; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN STRUCTURE; PROTEIN TRANSPORT;

BACTERIA (MICROORGANISMS);

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; CONSERVED SEQUENCE; FLAGELLA; MEMBRANE PROTEINS; MOLECULAR CHAPERONES; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; SALMONELLA TYPHIMURIUM;

EID: 84890123592     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12430     Document Type: Article

References (48)

1. Aldridge, P., Karlinsey, J.E., and Hughes, K.T. (2003) The type III secretion chaperone FlgN regulates flagellar assembly via a negative feedback loop containing its chaperone substrates FlgK and FlgL. Mol Microbiol 49: 1333-1345.
2. Aldridge, P., Karlinsey, J.E., Becker, E., Chevance, F.F., and Hughes, K.T. (2006) Flk prevents premature secretion of the anti sigma factor FlgM into the periplasm. Mol Microbiol 60: 630-642.
3. Asakura, S., Egusgi, G., and Iino, T. (1964) Reconstitution of bacteria flagella in vitro. J Mol Biol 10: 42-56.
4. Auvray, F., Thomas, J., Fraser, G.M., and Hughes, C. (2001) Flagellin polymerisation control by a cytosolic export chaperone. J Mol Biol 308: 221-229.
5. Bange, G., Kümmerer, N., Engel, C., Bozkurt, G., Wild, K., and Sinning, I. (2010) FlhA provides the adaptor for coordinated delivery of late flagella building blocks to the type III secretion system. Proc Natl Acad Sci USA 107: 11295-11300.
6. Bennett, J.C., Thomas, J., Fraser, G.M., and Hughes, C. (2001) Substrate complexes and domain organization of the Salmonella flagellar export chaperones FlgN and FliT. Mol Microbiol 39: 781-791.
7. Brown, J.D., Saini, S., Aldridge, C., Herbert, J., Rao, C.V., and Aldridge, P.D. (2008) The rate of protein secretion dictates the temporal dynamics of flagellar gene expression. Mol Microbiol 70: 924-937.
8. Chevance, F.F., and Hughes, K.T. (2008) Coordinating assembly of a bacterial macromolecular machine. Nat Rev Microbiol 6: 455-465.
9. Erhardt, M., Hirano, T., Su, Y., Paul, K., Wee, D.H., Mizuno, S., etal. (2010) The role of FliK molecular ruler in hook-length control in Salmonella enterica. Mol Microbiol 75: 1272-1284.
10. Evans, L.D.B., Stafford, G.P., Ahmed, S., Fraser, G.M., and Hughes, C. (2006) An escort mechanism for cycling of export chaperones during flagellum assembly. Proc Natl Acad Sci USA 103: 17474-17479.
11. Evdokimov, A.G., Phan, J., Tropea, J.E., Routzahn, K.M., Peters, H.K., Pokross, M., and Waugh, D.S. (2003) Similar modes of polypeptide recognition by export chaperones in flagellar biosynthesis and type III secretion. Nat Struct Biol 10: 789-793.
12. Fraser, G.M., Bennett, J.C.Q., and Hughes, C. (1999) Substrate-specific binding of hook-associated proteins by FlgN and FliT, putative chaperones for flagellum assembly. Mol Microbiol 32: 569-580.
13. Furukawa, Y., Imada, K., Vonderviszt, F., Matsunami, H., Sano, K., Kutsukake, K., and Namba, K. (2002) Interactions between bacterial flagellar axial proteins in their monomeric state in solution. J Mol Biol 318: 889-900.
14. Hara, N., Namba, K., and Minamino, T. (2011) Genetic characterization of conserved charged residues in the bacterial flagellar type III export protein FlhA. PLoS ONE 6: e22417.
15. Hirano, T., Minamino, T., Namba, K., and Macnab, R.M. (2003) Substrate specificity class and the recognition signal for Salmonella type III flagellar export. J Bacteriol 185: 2485-2492.
16. Hirano, T., Mizuno, S., Aizawa, S., and Hughes, K.T. (2009) Mutations in flk, flgG, flhA, and flhE that affect the flagellar type III secretion specificity switch in Salmonella enterica. J Bacteriol 19: 3938-3949.
17. Homma, M., Fujita, H., Yamaguchi, S., and Iino, T. (1984) Excretion of unassembled flagellin by Salmonella typhimurium mutants deficient in hook-associated proteins. J Bacteriol 159: 1056-1059.
18. Hughes, K.T., Gillen, K.L., Semon, M.J., and Karlinsey, J.E. (1993) Sensing structural intermediates in bacterial flagellar assembly by export of a negative regulator. Science 262: 1277-1280.
19. Ikeda, T., Oosawa, K., and Hotani, H. (1996) Self-assembly of the filament capping protein, FliD, of bacterial flagella into an annular structure. J Mol Biol 259: 679-686.
20. Imada, K., Vonderviszt, F., Furukawa, Y., Oosawa, K., and Namba, K. (1998) Assembly characteristics of flagellar cap protein HAP2 of Salmonella: decamer and pentamer in the pH-sensitive equilibrium. J Mol Biol 277: 883-891.
21. Imada, K., Minamino, T., Kinoshita, M., Furukawa, Y., and Namba, K. (2010) Structural insight into the regulatory mechanisms of interactions of the flagellar type III chaperone FliT with its binding partners. Proc Natl Acad Sci USA 107: 8812-8817.
22. Kinoshita, M., Yamane, M., Matsunami, H., Minamino, T., Namba, K., and Imada, K. (2009) Purification, crystallization and preliminary X-ray analysis of FliT, a bacterial flagellar substrate-specific export chaperone. Acta Crystallograph Sect F Struct Biol Cryst Commun 65: 825-828.
23. Kutsukake, K. (1994) Excretion of the anti-sigma factor through a flagellar substructure couples flagellar gene expression with flagellar assembly in Salmonella typhimurium. Mol Gen Genet 243: 605-612.
24. Kutsukake, K. (1997) Hook-length control of the export-switching machinery involves a double-locked gate in Salmonella typhimurium flagellar morphogenesis. J Bacteriol 179: 1268-1273.
25. Kutsukake, K., and Iino, T. (1994) Role of the FliA-FlgM regulatory system on the transcriptional control of the flagellar regulon and flagellar formation in Salmonella typhimurium. J Bacteriol 176: 3598-3605.
26. Kutsukake, K., Ohya, Y., and Iino, T. (1990) Transcriptional analysis of the flagellar regulon of Salmonella typhimurium. J Bacteriol 172: 741-747.
27. Kutsukake, K., Okada, T., Yokoseki, T., and Iino, T. (1994) Sequence analysis of the flgA gene and its adjacent region in Salmonella typhimurium, and identification of another flagellar gene, flgN. Gene 143: 49-54.
28. Minamino, T. (2013) Protein export through the bacterial flagellar type III export pathway. Biochim Biophys Acta pii: S0167-4889(13)00327-3. doi:10.1016/j.bbamcr.2013.09.005
29. Minamino, T., and Macnab, R.M. (1999) Components of the Salmonella flagellar export apparatus and classification of export substrates. J Bacteriol 181: 1388-1394.
30. Minamino, T., and Macnab, R.M. (2000a) Domain structure of Salmonella FlhB, a flagellar export component responsible for substrate specificity switching. J Bacteriol 182: 4906-4919.
31. Minamino, T., and Macnab, R.M. (2000b) Interactions among components of the Salmonella flagellar export apparatus and its substrates. Mol Microbiol 35: 1052-1064.
32. Minamino, T., Doi, H., and Kutsukake, K. (1999a) Substrate specificity switching of the flagellum-specific export apparatus during flagellar morphogenesis in Salmonella typhimurium. Biosci Biotechnol Biochem 63: 1301-1303.
33. Minamino, T., González-Pedrajo, B., Yamaguchi, K., Aizawa, S.-I., and Macnab, R.M. (1999b) FliK, the protein responsible for flagellar hook length control in Salmonella, is exported during hook assembly. Mol Microbiol 34: 295-304.
34. Minamino, T., Ferris, H.U., Moriya, N., Kihara, M., and 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.
35. Minamino, T., Imada, K., and Namba, K. (2008) Mechanisms of type III protein export for bacterial flagellar assembly. Mol Biosyst 4: 1105-1115.
36. Minamino, T., Moriya, N., Hirano, T., Hughes, K.T., and Namba, K. (2009) Interaction of FliK with the bacterial flagellar hook is required for efficient export specificity switching. Mol Microbiol 74: 239-251.
37. Minamino, T., Morimoto, Y.V., Hara, N., and Namba, K. (2011) An energy transduction mechanism used in bacterial type III protein export. Nat Commun 2: 475. doi:10.1038/ncomms1488
38. Minamino, T., Kinoshita, M., Imada, K., and Namba, K. (2012a) Interaction between FliI ATPase and a flagellar chaperone FliT during bacterial flagellar export. Mol Microbiol 83: 168-178.
39. Minamino, T., Kinoshita, M., Hara, N., Takeuchi, S., Hida, A., Koya, S., etal. (2012b) Interaction of a bacterial flagellar chaperone FlgN with FlhA is required for efficient export of its cognate substrates. Mol Microbiol 83: 775-788.
40. Moore, S.A., and Jia, Y. (2010) Structure of the cytoplasmic domain of the flagellar secretion apparatus component FlhA from Helicobacter pylori. J Biol Chem 285: 21060-21069.
41. Ohnishi, K., Kutsukake, K., Suzuki, H., and Iino, T. (1992) A novel transcriptional regulation in the flagellar regulon of Salmonella typhimurium: an anti-sigma factor inhibits the activity of the flagellum-specific sigma factor, sigma F. J Bacteriol 176: 2272-2281.
42. Ohnishi, K., Ohto, Y., Aizawa, S.-I., Macnab, R.M., and Iino, T. (1994) FlgD is a scaffolding protein needed for flagellar hook assembly in Salmonella typhimurium. J Bacteriol 176: 2272-2281.
43. Saijo-Hamano, Y., Minamino, T., Macnab, R.M., and Namba, K. (2004) Structural and functional analysis of the C-terminal cytoplasmic domain of FlhA, an integral membrane component of the type III flagellar protein export apparatus in Salmonella. J Mol Biol 343: 457-466.
44. Saijo-Hamano, Y., Imada, K., Minamino, T., Kihara, M., Shimada, M., Kitao, A., and Namba, K. (2010) Structure of the cytoplasmic domain of FlhA and implication for flagellar type III protein export. Mol Microbiol 76: 260-268.
45. Thomas, J., Stafford, G.P., and Hughes, C. (2004) Docking of cytosolic chaperone-substrate complexes at the membrane ATPase during flagellar type III protein export. Proc Natl Acad Sci USA 101: 3945-3950.
46. Yamaguchi, S., Fujita, H., Sugata, K., Taira, T., and Iino, T. (1984) Genetic analysis of H2, the structural gene for phase-2 flagellin in Salmonella. J Gen Microbiol 130: 255-265.
47. Yokoseki, T., Kutsukake, K., Ohnishi, K., and Iino, T. (1995) Functional analysis of the flagellar genes in the fliD operon of Salmonella typhimurium. Microbiology 141: 1715-1722.
48. Yokoseki, T., Iino, T., and Kutsukake, K. (1996) Negative regulation by fliD, fliS, and fliT of the export of the flagellum-specific anti-sigma factor, FlgM, in Salmonella typhimurium. J Bacteriol 178: 899-901.