Type III flagellar protein export and flagellar assembly

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1694, Issue 1-3 SPEC.ISS., 2004, Pages 207-217

  Macnab, Robert M ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

Bacterial flagellum; Chaperone; FliI ATPase; Morphogenesis; Type III protein export

Indexed keywords

BACTERIAL PROTEIN; CHAPERONE; MEMBRANE PROTEIN;

AMINO TERMINAL SEQUENCE; BACTERIAL FLAGELLUM; BACTERIAL GENE; CARBOXY TERMINAL SEQUENCE; CLUSTER ANALYSIS; COMPARATIVE STUDY; GENE CLUSTER; GENE EXPRESSION; GENOMICS; MOLECULAR WEIGHT; MORPHOGENESIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; REVIEW; VIRULENCE;

BACTERIA; BACTERIAL PROTEINS; FLAGELLA; MEMBRANE TRANSPORT PROTEINS; PROTEIN TRANSPORT; SALMONELLA; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); EUKARYOTA; SALMONELLA;

EID: 8844249277     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2004.04.005     Document Type: Review

References (71)

1. Aizawa S.-I. Sussman M. Medical Microbiology. 2002;155-175 Academic Press, New York, NY
2. Bourret R.B., Stock A.M. Molecular information processing: lessons from bacterial chemotaxis. J. Biol. Chem. 277:2002;9625-9628
3. Stock J.B., Surette M.G. Chemotaxis. Neidhardt F.C., et al. Escherichia coli and Salmonella: Cellular and Molecular Biology. Volume 1:1996;1103-1129 ASM Press, Washington, DC
4. Macnab R.M. Neidhardt F.C., Curtiss R. III, Ingraham J.L., Lin E.C.C., Low K.B., Magasanik B., Reznikoff W.S., Riley M., Schaechter M., Umbarger H.E. Flagella and Motility. Escherichia coli and Salmonella: Cellular and Molecular Biology. 2nd ed.:1996;123-145 ASM Press, Washington, DC
5. Macnab R.M. How bacteria assemble flagella. Annu. Rev. Microbiol. 57:2003;77-100
6. Kutsukake K., Ohya Y., Iino T. Transcriptional analysis of the flagellar regulon of Salmonella typhimurium. J. Bacteriol. 172:1990;741-747
7. Macnab R.M. Genetics and biogenesis of bacterial flagella. Annu. Rev. Genet. 26:1992;129-156
8. Hughes K.T., Gillen K.L., Semon M.J., Karlinsey J.E. Sensing structural intermediates in bacterial flagellar assembly by export of a negative regulator. Science. 262:1993;1277-1280
9. Kutsukake K. Excretion of the anti-sigma factor through a flagellar structure couples flagellar gene expression with flagellar assembly in Salmonella typhimurium. Mol. Gen. Genet. 243:1994;605-612
10. Aldridge P., Hughes K.T. Regulation of flagellar assembly. Curr. Opin. Microbiol. 5:2002;160-165
11. Kubori T., Shimamoto N., Yamaguchi S., Namba K., Aizawa S.-I. Morphological pathway of flagellar assembly in Salmonella typhimurium. J. Mol. Biol. 226:1992;433-446
12. Jones C.J., Macnab R.M. Flagellar assembly in Salmonella typhimurium: analysis with temperature-sensitive mutants. J. Bacteriol. 172:1990;1327-1339
13. Suzuki T., Komeda Y. Incomplete flagellar structures in Escherichia coli mutants. J. Bacteriol. 145:1981;1036-1041
14. Blair D.F., Berg H.C. Restoration of torque in defective flagellar motors. Science. 242:1988;1678-1681
15. Block S.M., Berg H.C. Successive incorporation of force-generating units in the bacterial rotary motor. Nature (London). 309:1984;470-472
16. Jones C.J., Homma M., Macnab R.M. L-, P-, and M-ring proteins of the flagellar basal body of Salmonella typhimurium: gene sequences and deduced protein sequences. J. Bacteriol. 171:1989;3890-3900
17. Homma M., Komeda Y., Iino T., Macnab R.M. The flaFIX gene product of Salmonella typhimurium is a flagellar basal body component with a signal peptide for export. J. Bacteriol. 169:1987;1493-1498
18. Emerson S.U., Tokuyasu K., Simon M.I. Bacterial flagella: polarity of elongation. Science. 169:1970;190-192
19. Iino T. Polarity of flagellar growth in Salmonella. J. Gen. Microbiol. 56:1969;227-239
20. Homma M., DeRosier D.J., Macnab R.M. Flagellar hook and hook-associated proteins of Salmonella typhimurium and their relationship to other axial components of the flagellum. J. Mol. Biol. 213:1990;819-832
21. Homma M., Kutsukake K., Hasebe M., Iino T., Macnab R.M. FlgB, FlgC, FlgF and FlgG. A family of structurally related proteins in the flagellar basal body of Salmonella typhimurium. J. Mol. Biol. 211:1990;465-477
22. Mimori Y., Yamashita I., Murata K., Fujiyoshi Y., Yonekura K., Toyoshima C., Namba K. The structure of the R-type straight flagellar filament of Salmonella at 9 Å resolution by electron cryomicroscopy. J. Mol. Biol. 249:1995;69-87
23. Morgan D.G., Macnab R.M., Francis N.R., DeRosier D.J. Domain organization of the subunit of the Salmonella typhimurium flagellar hook. J. Mol. Biol. 229:1993;79-84
24. Minamino T., Macnab R.M. Components of the Salmonella flagellar export apparatus and classification of export substrates. J. Bacteriol. 181:1999;1388-1394
25. Macnab R.M. The bacterial flagellum: reversible rotary propellor and type III export apparatus. J. Bacteriol. 181:1999;7149-7153
26. Suzuki H., Yonekura K., Murata K., Hirai T., Oosawa K., Namba K. A structural feature in the central channel of the bacterial flagellar FliF ring complex is implicated in Type III protein export. J. Struct. Biol. 124:1998;104-114
27. Fan F., Ohnishi K., Francis N.R., Macnab R.M. 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. 26:1997;1035-1046
28. Kihara M., Minamino T., Yamaguchi S., Macnab R.M. Intergenic suppression between the flagellar MS ring protein FliF of Salmonella and FlhA, a membrane component of its export apparatus. J. Bacteriol. 183:2001;1655-1662
29. Fan F., Macnab R.M. Enzymatic characterization of FliI: an ATPase involved in flagellar assembly in Salmonella typhimurium. J. Biol. Chem. 271:1996;31981-31988
30. González-Pedrajo B., Fraser G.M., Minamino T., Macnab R.M. Molecular dissection of Salmonella FliH, a regulator of the ATPase FliI and the type III flagellar protein export pathway. Mol. Microbiol. 45:2002;967-982
31. Minamino T., Tame J.R.H., Namba K., Macnab R.M. Proteolytic analysis of the FliH/FliI complex, the ATPase component of the type III flagellar export apparatus of Salmonella. J. Mol. Biol. 312:2001;1027-1036
32. Minamino T., González-Pedrajo B., Oosawa K., Namba K., Macnab R.M. Structural properties of FliH, an ATPase regulatory component of the Salmonella type III flagellar export apparatus. J. Mol. Biol. 322:2002;281-290
33. Minamino T., Macnab R.M. Domain structure of Salmonella FlhB, a flagellar export component responsible for substrate-specificity switching. J. Bacteriol. 182:2000;4906-4914
34. Fraser G.M., Hirano T., Ferris H.U., Devgan L.L., Kihara M., Macnab R.M. Substrate specificity of type III flagellar protein export in Salmonella is controlled by subdomain interactions in FlhB. Mol. Microbiol. 48:2003;1043-1057
35. Minamino T., Chu R., Yamaguchi S., Macnab R.M. Role of FliJ in flagellar protein export in Salmonella. J. Bacteriol. 182:2000;4207-4215
36. Fraser G.M., González-Pedrajo, Tame J.R.H., Macnab R.M. Interactions of FliJ with the Salmonella type III flagellar export apparatus. J. Bacteriol. 185:2003;3983-3988
37. Minamino T., González-Pedrajo B., Kihara M., Namba K., Macnab R.M. The ATPase FliI can interact with the type III flagellar protein export apparatus in the absence of its regulator, FliH. J. Bacteriol. 185:2003;5546-5554
38. Fraser G.M., Bennett J.C.Q., Hughes C. Substrate-specific binding of hook-associated proteins by FlgN and FliT, putative chaperones for flagellum assembly. Mol. Microbiol. 32:1999;569-580
39. Bennett J.C.Q., Hughes C. From flagellum assembly to virulence: the extended family of type III export chaperones. Trends Microbiol. 8:2000;202-204
40. Bennett J.C.Q., Thomas J., Fraser G.M., Hughes C. Substrate complexes and domain organization of the Salmonella flagellar export chaperones FlgN and FliT. Mol. Microbiol. 39:2001;781-791
41. Auvray F., Thomas J., Fraser G.M., Hughes C. Flagellin polymerisation control by a cytosolic export chaperone. J. Mol. Biol. 308:2001;221-229
42. Yokoseki T., Kutsukake K., Ohnishi K., Iino T. Functional analysis of the flagellar genes in the fliD operon of Salmonella typhimurium. Microbiology. 141:1995;1715-1722
43. Ozin A.J., Claret L., Auvray F., Hughes C. The FliS chaperone selectively binds the disordered flagellin C-terminal D0 domain central to polymerisation. FEMS Microbiol. Lett. 219:2003;219-224
44. Nambu T., Kutsukake K. The Salmonella FlgA protein, a putative periplasmic chaperone essential for flagellar P ring formation. Microbiology. 146:2000;1171-1178
45. Patterson-Delafield J., Martinez R.J., Stocker B.A.D., Yamaguchi S. A new fla gene in Salmonella typhimurium - flaR - and its mutant phenotype - superhooks. Arch. Mikrobiol. 90:1973;107-120
46. Williams A.W., Yamaguchi S., Togashi F., Aizawa S.-I., Kawagishi I., Macnab R.M. Mutations in fliK and flhB affecting flagellar hook and filament assembly in Salmonella typhimurium. J. Bacteriol. 178:1996;2960-2970
47. Hirano T., Yamaguchi S., Oosawa K., Aizawa S.-I. Roles of FliK and FlhB in determination of flagellar hook length in Salmonella typhimurium. J. Bacteriol. 176:1994;5439-5449
48. Nambu T., Minamino T., Macnab R.M., Kutsukake K. Peptidoglycan- hydrolyzing activity of the FlgJ protein, essential for flagellar rod formation in Salmonella typhimurium. J. Bacteriol. 181:1999;1555-1561
49. Hirano T., Minamino T., Macnab R.M. The role in flagellar rod assembly of the N-terminal domain of Salmonella FlgJ, a flagellum-specific muramidase. J. Mol. Biol. 312:2001;359-369
50. Ohnishi K., Ohto Y., Aizawa S.-I., Macnab R.M., Iino T. FlgD is a scaffolding protein needed for flagellar hook assembly in Salmonella typhimurium. J. Bacteriol. 176:1994;2272-2281
51. Yonekura K., Maki S., Morgan D.G., DeRosier D.J., Vonderviszt F., Imada K., Namba K. The bacterial flagellar cap as the rotary promoter of flagellin self-assembly. Science. 290:2000;2148-2152
52. Nölling J., Breton G., Omelchenko M.V., Makarova K.S., Zeng Q., Gibson R., Lee H.M., Dubois J., Qiu D., Hitti J. Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum. J. Bacteriol. 183:2001;4823-4838
53. Brüggemann H., Bäumer S., Fricke W.F., Wiezer A., Liesegang H., Decker I., Herzberg C., Martínez-Arias R., Merkl R., Henne A., Gottschalk G. The genome sequence of Clostridium tetani, the causative agent of tetanus disease. Proc. Natl. Acad. Sci. U. S. A. 100:2003;1316-1321
54. van Ham R.C.H.J., Kamerbeek J., Palacios C., Rausell C., Abascal F., Bastolla U., Fernández J.M., Jiménez L., Postigo M., Silva F.J., Tamames J., Viguera E., Latorre A., Valencia A., Morán F., Moya A. Reductive genome evolution in Buchnera aphidicola. Proc. Natl. Acad. Sci. U. S. A. 100:2003;581-586
55. Minamino T., Macnab R.M. Interactions among components of the Salmonella flagellar export apparatus and its substrates. Mol. Microbiol. 35:2000;1052-1064
56. Zhu K., González-Pedrajo B., Macnab R.M. Interactions among membrane and soluble components of the flagellar export apparatus of Salmonella. Biochemistry. 41:2002;9516-9524
57. Minamino T., Macnab R.M. 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. 37:2000;1494-1503
58. Claret L., Calder S.R., Higgins M., Hughes C. Oligomerization and activation of the FliI ATPase central to bacterial flagellum assembly. Mol. Microbiol. 48:2003;1349-1355
59. Kornacker M.G., Newton A. Information essential for cell-cycle-dependent secretion of the 591-residue Caulobacter hook protein is confined to a 21-amino-acid sequence near the N-terminus. Mol. Microbiol. 14:1994;73-85
60. Savvides S.N., Yeo H.-J., Beck M.R., Blaesing F., Lurz R., Lanka E., Buhrdorf R., Fischer W., Haas R., Waksman G. VirB11 ATPases are dynamic hexameric assemblies: new insights into bacterial type IV secretion. EMBO J. 22:2003;1969-1980
61. Vonderviszt F., Ishima R., Akasaka K., Aizawa S.-I. Terminal disorder: a common structural feature of the axial proteins of bacterial flagellum? J. Mol. Biol. 226:1992;575-579
62. Vonderviszt F., Kanto S., Aizawa S.-I., Namba K. Terminal regions of flagellin are disordered in solution. J. Mol. Biol. 209:1989;127-133
63. Ikeda T., Asakura S., Kamiya R. Total reconstitution of Salmonella flagellar filaments from hook and purified flagellin and hook-associated proteins in vitro. J. Mol. Biol. 209:1989;109-114
64. Lux R., Kar N., Khan S. Overproduced Salmonella typhimurium flagellar motor switch complexes. J. Mol. Biol. 298:2000;577-583
65. Hirano T., Minamino T., Namba K., Macnab R.M. Substrate specificity classes and the recognition signal for Salmonella type III flagellar export. J. Bacteriol. 185:2003;2485-2492
66. Minamino T., González-Pedrajo B., Yamaguchi K., Aizawa S.-I., Macnab R.M. FliK, the protein responsible for flagellar hook length control in Salmonella, is exported during hook assembly. Mol. Microbiol. 34:1999;295-304
67. Paulus H. Protein splicing and related forms of protein autoprocessing. Annu. Rev. Biochem. 69:2000;447-496
68. Lavander M., Sundberg L., Edqvist P.J., Lloyd S.A., Wolf-Watz H., Forsberg Å. Proteolytic cleavage of the FlhB homologue YscU of Yersinia pseudotuberculosis is essential for bacterial survival but not for type III secretion. J. Bacteriol. 184:2002;4500-4509
69. Hueck C.J. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:1998;379-433
70. Nguyen L., Paulsen I.T., Tchieu J., Hueck C.J., Saier M.H.J. Phylogenetic analyses of the constituents of type III protein secretion systems. J. Mol. Microbiol. Biotechnol. 2:2000;125-144
71. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:1997;3389-3402