Interaction between FliI ATPase and a flagellar chaperone FliT during bacterial flagellar protein export

Molecular Microbiology

Volumn 83, Issue 1, 2012, Pages 168-178

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

^a OSAKA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c RIKEN Center for Biosystems Dynamics Research   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; AMINO TERMINAL TELOPEPTIDE; BACTERIAL PROTEIN; CARBOXY TERMINAL TELOPEPTIDE; CHAPERONE; MEMBRANE PROTEIN; PROTEIN FLID; PROTEIN FLIL; PROTEIN FLIT; PROTEIN FLIT94; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BACTERIAL FLAGELLUM; BINDING AFFINITY; CONTROLLED STUDY; CYTOPLASM; DISSOCIATION; ENZYME ACTIVITY; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT;

BACTERIAL PROTEINS; FLAGELLA; MOLECULAR CHAPERONES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTON-TRANSLOCATING ATPASES; SALMONELLA TYPHIMURIUM;

BACTERIA (MICROORGANISMS);

EID: 84155162801     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07924.x     Document Type: Article

References (45)

1. Akeda, Y., and Galán, J.E. (2004) Genetic analysis of the Salmonella enterica type III secretion-associated ATPase InvC defines discrete functional domains. J Bacteriol 186: 2402-2412.
2. Akeda, Y., and Galán, J.E. (2005) Chaperone release and unfolding of substrates in type III secretion. Nature 473: 911-915.
3. Andrade, A., Pardo, J.P., Espinosa, N., Pérez-Hernández, G., and González-Pedrajo, B. (2007) Enzymatic characterization of the enteropathogenic Escherichia coli type III secretion ATPase EscN. Arch Biochem Biophys 468: 121-127.
4. 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.
5. Barker, C.S., Meshcheryakova, I.V., Kostyukova, A.S., and Samatey, F.A. (2010) FliO regulation of FliP in the formation of the Salmonella enterica flagellum. PLoS Genet 6: e1001143.
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. Blaylock, B., Riordan, K.E., Missiakas, D.M., and Schneewind, O. (2006) Characterization of the Yersinia enterocolitica type III secretion ATPase YscN and its regulator, YscL. J Bacteriol 188: 3525-3543.
8. Claret, L., Calder, S.R., Higgins, M., and Hughes, C. (2003) Oligomerisation and activation of the FliI ATPase central to bacterial flagellum assembly. Mol Microbiol 48: 1349-1355.
9. Cornelis, G.R. (2006) The type III secretion injectisome. Nat Rev Microbiol 4: 811-825.
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. Fan, F., and Macnab, R.M. (1996) Enzymatic characterization of FliI: an ATPase involved in flagellar assembly in Salmonella typhimurium. J Biol Chem 271: 31981-31988.
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. González-Pedrajo, B., Fraser, G.M., Minamino, T., and Macnab, R.M. (2002) Molecular dissection of Salmonella FliH, a regulator of the ATPase FliI and the type III flagellar protein export pathway. Mol Microbiol 45: 967-982.
14. González-Pedrajo, B., Minamino, T., Kihara, M., and Namba, K. (2006) Interactions between C ring proteins and export apparatus components: a possible mechanism for facilitating type III protein export. Mol Microbiol 60: 984-998.
15. Ibuki, T., Imada, K., Minamino, T., Kato, T., Miyata, T., and Namba, K. (2011) Common architecture between the flagellar protein export apparatus and F- and V-ATPases. Nat Struct Mol Biol 18: 277-282.
16. Iino, T. (1969) Polarity of flagellar growth in Salmonella. J Gen Microbiol 56: 227-239.
17. 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.
18. 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.
19. 1-ATPase subunits. Proc Natl Acad Sci USA 104: 485-490.
20. 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.
21. Jackson, M.W., and Plano, G.V. (2000) Interactions between type III secretion apparatus components from Yersinia pestis detected using the yeast two-hybrid system. FEMS Microbiol Lett 186: 85-90.
22. Kazetani, K., Minamino, T., Miyata, T., Kato, T., and Namba, K. (2009) ATP-induced FliI hexamerization facilitates bacterial flagellar protein export. Biochem Biophys Res Commun 388: 323-327.
23. Lane, M.C., O'Toole, P.W., and Moore, S.A. (2006) Molecular basis of the interaction between the flagellar export proteins FliH and FliI from Helicobacter pylori. J Biol Chem 281: 508-517.
24. Lorenz, C., and Büttner, D. (2009) Functional characterization of the type III secretion ATPase HrcN from the plant pathogen Xanthomonas campestris pv. vesicatoria. J Bacteriol 191: 1414-1428.
25. McMurry, J.L., Murphy, J.W., and González-Pedrajo, B. (2006) The FliN-FliH interaction mediates localization of flagellar export ATPase FliI to the C ring complex. Biochemistry 45: 11790-11798.
26. Macnab, R.M. (2003) How bacteria assemble flagella. Annu Rev Microbiol 57: 77-100.
27. Minamino, T., and Macnab, R.M. (1999) Components of the Salmonella flagellar export apparatus and classification of export substrates. J Bacteriol 181: 1388-1394.
28. Minamino, T., and Macnab, R.M. (2000a) Interactions among components of the Salmonella flagellar export apparatus and its substrates. Mol Microbiol 35: 1052-1064.
29. Minamino, T., and Macnab, R.M. (2000b) FliH, a soluble component of the type III flagellar export apparatus of Salmonella, forms a complex with FliI and inhibits its ATPase activity. Mol Microbiol 37: 1494-1503.
30. Minamino, T., and Namba, K. (2004) Self-assembly and type III protein export of the bacterial flagellum. J Mol Microbiol Biotechnol 7: 5-17.
31. Minamino, T., and Namba, K. (2008) Distinct roles of the FliI ATPase and proton motive force in bacterial flagellar protein export. Nature 451: 485-488.
32. Minamino, T., Tame, J.R.H., Namba, K., and Macnab, R.M. (2001) Proteolytic analysis of the FliH/FliI complex, the ATPase component of the type III flagellar export apparatus of Salmonella. J Mol Biol 312: 1027-1036.
33. Minamino, T., González-Pedrajo, B., Kihara, M., Namba, K., and Macnab, R.M. (2003) The ATPase FliI can interact with the type III flagellar protein export apparatus in the absence of its regulator FliH. J Bacteriol 185: 3983-3988.
34. Minamino, T., Kazetani, K., Tahara, A., Suzuki, H., Furukawa, Y., Kihara, M., and Namba, K. (2006) Oligomerization of the bacterial flagellar ATPase FliI is controlled by its extreme N-terminal region. J Mol Biol 360: 510-519.
35. Minamino, T., Imada, K., and Namba, K. (2008a) Mechanisms of type III protein export for bacterial flagellar assembly. Mol Biosyst 4: 1105-1115.
36. Minamino, T., Imada, K., and Namba, K. (2008b) Molecular motors of the bacterial flagella. Curr Opin Struct Biol 18: 693-701.
37. Minamino, T., Yoshimura, S.D.J., Morimoto, Y.V., González-Pedrajo, B., Kami-ike, N., and Namba, K. (2009) Roles of the extreme N-terminal region of FliH for efficient localization of the FliH-FliI complex to the bacterial flagellar type III export apparatus. Mol Microbiol 74: 1471-1483.
38. 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.
39. 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.
40. Okabe, M., Minamino, T., Imada, K., Namba, K., and Kihara, M. (2009) Role of the N-terminal domain of FliI ATPase in bacterial flagellar protein export. FEBS Lett 583: 743-748.
41. Pallen, M.J., Bailey, C.M., and Beatson, S.A. (2006) Evolutionary links between FliH/YscL-like proteins from bacterial type III secretion systems and second-stalk components of the FoF1 and vacuolar ATPases. Protein Sci 15: 935-941.
42. Paul, K., Harmon, J.G., and 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.
43. Riordan, K.E., Sorg, J.A., Berube, B.J., and Schneewind, O. (2008) Impassable YscP substrates and their impact on the Yersinia enterocolitica type III secretion pathway. J Bacteriol 190: 6204-6216.
44. Sorg, J.A., Blaylock, B., and Schneewind, O. (2006) Secretion signal recognition by YscN, the Yersinia type III secretion ATPase. Proc Natl Acad Sci USA 103: 16490-16495.
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.