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

Molecular Microbiology

Volumn 74, Issue 6, 2009, Pages 1471-1483

  Minamino, Tohru ^a,b   Yoshimura, Shinsuke D J ^a   Morimoto, Yusuke V ^a   González Pedrajo, Bertha ^c   Kami Ike, Nobunori ^a   Namba, Keiichi ^a  

^a OSAKA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ALANINE; BACTERIAL PROTEIN; FLAGELLAR TYPE III PROTEIN; MEMBRANE PROTEIN; PROTEIN FLIH; PROTEIN FLIL; TYROSINE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL FLAGELLUM; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; FLUORESCENCE MICROSCOPY; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; CELL MEMBRANE; ESCHERICHIA COLI; FLAGELLA; GENES, REPORTER; LUMINESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN TRANSPORT; PROTON-TRANSLOCATING ATPASES; RECOMBINANT FUSION PROTEINS; SALMONELLA TYPHIMURIUM; SEQUENCE DELETION;

BACTERIA (MICROORGANISMS);

EID: 72049109167     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06946.x     Document Type: Article

References (39)

1. Cornelis, G.R. (2006) The type III secretion injectisome. Nat Rev Microbiol 4: 811-825.
2. 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. (Pubitemid 26422223)
3. Fan, F., Ohnishi, K., Francis, N.R., and Macnab, R.M. (1997) The FliP and FliR proteins of Salmonella typhimurium, putative components of the type III flagellar export apparatus, are located in the flagellar basal body. Mol Microbiol 26: 1035-1046. (Pubitemid 27507887)
4. Francis, N.R., Sosinsky, G.E., Thomas, D., and DeRosier, D.J. (1994) Isolation, characterization, and structure of bacterial flagellar motors containing the switch complex. J Mol Biol 235: 1261-1270. (Pubitemid 24148928)
5. Fraser, G.M., Hirano, T., Ferris, H.U., Devgan, L.L., Kihara, M., and Macnab, R.M. (2003) Substrate specificity of type III flagellar protein export in Salmonella is controlled by subdomain interactions in FlhB. Mol Microbiol 48: 1043-1057. (Pubitemid 36628268)
6. 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. (Pubitemid 35007441)
7. 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.
8. Hirano, T., Mizuno, S., Aizawa, S.-I., 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 181: 3938-3949.
9. Katayama, E., Shiraishi, T., Oosawa, K., Baba, N., and Aizawa, S.-I. (1996) Geometry of the flagellar motor in the cytoplasmic membrane of Salmonella typhimurium as determined by stereo-photogrammetry of quick-freeze deep-etch replica images. J Mol Biol 255: 458-475. (Pubitemid 26105569)
10. Kazetani, K.I., 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.
11. Kihara, M., Minamino, T., Yamaguchi, S., and Macnab, R.M. (2001) Intergenic suppression between the flagellar MS ring protein FliF of Salmonella and FlhA, a membrane component of its export apparatus. J Bacteriol 183: 1655-1662. (Pubitemid 32172308)
12. Kubori. T., Shimamoto, N., Yamaguchi, S., Namba, K., and Aizawa, S.-I. (1992) Morphological pathway of flagellar assembly in Salmonella typhimurium. J Mol Biol 226: 433-446.
13. Kutsukake, K., Ohya, Y., and Iino, T. (1990) ranscriptional analysis of the flagellar regulon of Salmonella typhimurium. J Bacteriol 172: 741-747. (Pubitemid 20070384)
14. 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.
15. Macnab, R.M. (2003) How bacteria assemble flagella. Annu Rev Microbiol 57: 77-100.
16. Minamino, T., and Macnab, R.M. (1999) Components of the Salmonella flagellar export apparatus and classification of export substrates. J Bacteriol 181: 1388-1394. (Pubitemid 29110795)
17. Minamino, T., and Macnab, R.M. (2000a) Interactions among components of the Salmonella flagellar export apparatus and its substrates. Mol Microbiol 35: 1052-1064. (Pubitemid 30137775)
18. 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. (Pubitemid 30774862)
19. Minamino, T., and Macnab, R.M. (2000c) Domain structure of Salmonella FlhB, a flagellar export component responsible for substrate specificity switching. J Bacteriol 182: 4906-4919.
20. Minamino, T., and Namba, K. (2004) Self-assembly and type III protein export of the bacterial flagellum. J Mol Microbiol Biotechnol 7: 5-17. (Pubitemid 38721126)
21. 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. (Pubitemid 351158881)
22. Minamino, T., Iino, T., and Kutsukake, K. (1994) Molecular characterization of the Salmonella typhimurium flhB operon and its protein products. J Bacteriol 176: 7630-7637. (Pubitemid 24382042)
23. Minamino, T., Chu, R., Yamaguchi, S., and Macnab, R.M. (2000) Role of FliJ in flagellar protein export in Salmonella. J Bacteriol 182: 4207-4215. (Pubitemid 30463783)
24. Minamino, T., González-Pedrajo, B., Oosawa, K., Namba, K., and Macnab, R.M. (2002) Structural properties of FliH, an ATPase regulatory component of the Salmonella type III flagellar export apparatus. J Mol Biol 322: 281-290.
25. 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. (Pubitemid 36735952)
26. Minamino, T., Kazetani, K.-I., 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. (Pubitemid 43927831)
27. Minamino, T., Imada, K., and Namba, K. (2008a) Mechanisms of type III protein export for bacterial flagellar assembly. Mol Biosyst 4: 1105-1115.
28. Minamino, T., Imada, K., and Namba, K. (2008b) Molecular motors of the bacterial flagella. Curr Opin Struct Biol 18: 693-701.
29. Murphy, G.E., Leadbetter, J.R., and Jensen, G.J. (2006) In situ structure of the complete Treponema primitia flagellar motor. Nature 442: 1062-1064.
30. 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. (Pubitemid 24118176)
31. Ohnishi, K., Fan, F., Schoenhals, G.J., Kihara, M., and Macnab, R.M. (1997) The FliO, FliP, FliQ, and FliR proteins of Salmonella typhimurium: putative components for flagellar assembly. J Bacteriol 179: 6092-6099. (Pubitemid 27419034)
32. 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.
33. 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. (Pubitemid 44051490)
34. Paul, K., Erhardt, M., Hirano, T., Blair, D.F., and Hughes, K.T. (2008) Energy source of flagellar type III secretion. Nature 451: 489-492. (Pubitemid 351158887)
35. 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. (Pubitemid 39296878)
36. Turner, L., Ryue, W.S., and Berg, H.C. (2000) Real-time imaging of fluorescent flagellar filaments. J Bacteriol 182: 2793-2801. (Pubitemid 30246910)
37. Van Arnam, J.S., McMurry, J.L., Kihara, M., and Macnab, R.M. (2004) Analysis of an engineered Salmonella flagellar fusion protein, FliR-FlhB. J Bacteriol 186: 2495-2498. (Pubitemid 38451855)
38. 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. (Pubitemid 14157108)
39. Yamaguchi, S., Aizawa, S.-I., Kihara, M., Isomura, M., Jones, C.J., and Macnab, R.M. (1986) Genetic evidence for a switching and energy-transducing complex in the flagellar motor of Salmonella typhimurium. J Bacteriol 168: 1172-1179. (Pubitemid 17226800)