Bacterial flagellar axial structure and its construction

Biophysical Reviews

Volumn 10, Issue 2, 2018, Pages 559-570

  Imada, Katsumi ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Axial structure; Bacterial flagellum; Cryo electron microscopy; X ray crystallography

Indexed keywords

FLAGELLIN;

AXIAL STRUCTURE; BACTERIAL FLAGELLUM; BACTERIAL STRUCTURES; GROWTH; NONHUMAN; REVIEW;

EID: 85045513591     PISSN: 18672450     EISSN: 18672469     Source Type: Journal    
DOI: 10.1007/s12551-017-0378-z     Document Type: Review

References (89)

1. Asakura S (1970) Polymerization of flagellin and polymorphism of flagella. Advan Biophys (Japan) 1:99–155
2. Berg HC, Anderson RA (1973) Bacteria swim by rotating their flagellar filaments. Nature 245:380–382
3. Blair DF, Berg HC (1988) Restoration of torque in defective flagellar motors. Science 242:1678–1681
4. Buist G, Kok J, Leenhouts KJ, Dabrowska M, Venema G, Haandrikman AJ (1995) Molecular cloning and nucleotide sequence of the gene encoding the major peptidoglycan hydrolase of Lactococcus lactis, a muramidase needed for cell separation. J Bacteriol 177:1554–1563
5. Calladine CR (1975) Construction of bacterial flagella. Nature 225:121–124
6. Calladine CR (1976) Design requirements for the construction of bacterial flagella. J Theor Biol 57:469–489
7. Calladine CR (1978) Change of waveform in bacterial flagella: the role of mechanics at the molecular level. J Mol Biol 118:457–479
8. Cho SY, Song WS, Hong HJ, Lee GS, Kang SG, Ko HJ, Kim PH, Yoon SI (2017) Tetrameric structure of the flagellar cap protein FliD from Serratia Marcescens. Biochem Biophys Res Commun 489:63–69
9. DePamphilis ML, Adler J (1971a) Purification of intact flagella from Escherichia coli and Bacillus subtilis. J Bacteriol 105:376–383
10. DePamphilis ML, Adler J (1971b) Fine structure and isolation of the hook–basal body complex of flagella from Escherichia coli and Bacillus subtilis. J Bacteriol 105:384–395
11. Francis NR, Sosinsky GE, Thomas D, DeRosier DJ (1994) Isolation, characterization, and structure of bacterial flagellar motors containing the switch complex. J Mol Biol 235:1261–1270
12. Fujii T, Kato T, Hiraoka KD, Miyata T, Minamino T, Chevance FF, Hughes KT, Namba K (2017) Identical folds used for distinct mechanical functions of the bacterial flagellar rod and hook. Nat Commun 8:14276
13. Fujii T, Kato T, Namba K (2009) Specific arrangement of alpha-helical coiled coils in the core domain of the bacterial flagellar hook for the universal joint function. Structure 17:1485–1493
14. Furukawa Y, Imada K, Vonderviszt F, Matsunami H, Sano K-I, Kutsukake K, Namba K (2002) Interactions between bacterial flagellar axial proteins in their monomeric state in solution. J Mol Biol 318:889–900
15. Gourlay LJ, Thomas RJ, Peri C, Conchillo-Solé O, Ferrer-Navarro M, Nithichanon A, Vila J, Daura X, Lertmemongkolchai G, Titball R, Colombo G, Bolognesi M (2015) From crystal structure to in silico epitope discovery in the Burkholderia pseudomallei flagellar hook-associated protein FlgK. FEBS J 282:1319–1333
16. Hasegawa K, Yamashita I, Namba K (1998) Quasi- and nonequivalence in the structure of bacterial flagellar filament. Biophys J 74:569–575
17. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, Goodlett DR, Eng JK, Akira S, Underhill DM, Aderem A (2001) The innate immune response to bacterial flagellin is mediated by toll-like receptor 5. Nature 410:1099–1103
18. Hirano T, Minamino T, Macnab RM (2001) The role in flagellar rod assembly of the N-terminal domain of Salmonella FlgJ, a flagellum-specific muramidase. J Mol Biol 312:359–369
19. Hirano T, Yamaguchi S, Oosawa K, Aizawa S-I (1994) Roles of FliK and FlhB in the determination of flagellar hook length in Salmonella typhimurium. J Bacteriol 176:5439–5449
20. Hiraoka KD, Morimoto YV, Inoue Y, Fujii T, Miyata T, Makino F, Minamino T, Namba K (2017) Straight and rigid flagellar hook made by insertion of the FlgG specific sequence into FlgE. Sci Rep 7:46723
21. Homma M, DeRosier DJ, Macnab RM (1990) Flagellar hook and hook-associated proteins of Salmonella typhimurium and their relationship to other axial components of the flagellum. J Mol Biol 213:819–832
22. Homma M, Fujita H, Yamaguchi S, Iino T (1984) Excretion of unassembled flagellin by Salmonella typhimurium mutants deficient in hook-associated proteins. J Bacteriol 159:1056–1059
23. Homma M, Kutsukake K, Hasebe M, Iino T, Macnab RM (1990) FlgB, FlgC, FlgF and FlgG. A family of structurally related proteins in the flagellar basal body of Salmonella typhimurium. J Mol Biol 211:465–477
24. Homma M, Iino T (1985a) Locations of hook-associated proteins in flagellar structures of Salmonella typhimurium. J Bacteriol 162:183–189
25. Homma M, Iino T (1985b) Excretion of unassebmled hook-associated proteins by Salmonella typhimurium. J Bacteriol 164:1370–1372
26. Hotani H (1982) Micro-video study of moving bacterial flagellar filaments III. Cyclic transformation induced by mechanical force. J Mol Biol 156:791–806
27. Ikeda T, Asakura S, Kamiya R (1985) "Cap" on the tip of Salmonella flagella. J Mol Biol 184:735–737
28. Ikeda T, Homma M, Iino T, Asakura S, Kamiya R (1987) Localization and stoichiometry of hook-associated proteins within Salmonella typhimurium flagella. J Bacteriol 169:1168–1173
29. Ikeda T, Kamiya R, Yamaguchi S (1984) In vitro polymerization of flagellin excreted by a short-flagellum Salmonella typhimurium mutant. J Bacteriol 159:787–789
30. Ikeda T, Oosawa K, Hotani H (1996) Self-assembly of the filament capping protein, FliD, of bacterial flagella into an annular structure. J Mol Biol 259:679–686
31. Ikeda T, Yamaguchi S, Hotani H (1993) Flagellar growth in a filament-less Salmonella fliD mutant supplemented with purfied hook-associated protein 2. J Bacteriol 114:39–44
32. Imada K, Vonderviszt F, Furukawa Y, Oosawa K, Namba K (1998) Assembly charcteristics of flagellar cap protein HAP2 of Salmonella: decamer and pentamer in the pH-sensitive equilibrium. J Mol Biol 277:883–891
33. Jones CJ, Macnab RM, Okino H, Aizawa S-I (1990) Stoichiometric analysis of the flagellar hook-(basal-body) complex of Salmonella typhimurium. J Mol Biol 212:377–387
34. Joris B, Englebert S, Chu C-P, Kariyama R, Daneo-Moore L, Shockman GD, Ghuysen J-M (1992) Modular design of the enterococcus hirae muramidase-2 and Streptococcus faecalis autolysin. FEMS Microbiol Lett 91:257–264
35. Kamiya R, Asakura S (1976) Helical transformations of Salmonella flagellain vitro. J Mol Biol 106:167–186
36. Kamiya R, Asakura S (1977) Flagellar transformations at alkaline pH. J Mol Biol 108:513–518
37. Kamiya R, Asakura S, Wakabayashi K, Namba K (1979) Transition of bacterial flagella from helical to straight forms with different subunit arrangements. J Mol Biol 131:725–742
38. Kitao A, Yonekura K, Maki-Yonekura S, Samatey FA, Imada K, Namba K, Go N (2006) Switch interactions control energy frustration and multiple flagellar filament structures. Proc Natl Acad Sci USA 103:4894–4899
39. Kubori T, Shimamoto N, Yamaguchi S, Namba K, Aizawa S-I (1992) Morphological pathway of flagellar assembly in Salmonella typhimurium. J Mol Biol 226:433–446
40. Kuo WT, Chin KH, Lo WT, Wang AH, Chou SH (2008) Crystal structure of the C-terminal domain of a flagellar hook-capping protein from Xanthomonas campestris. J Mol Biol 381:189–199
41. Kutsukake K, Doi H (1994) Nucleotide sequence of the flgD gene of Salmonella typhimurium which is essential for flagellar hook formation. Biochim Biophys Acta 1218:443–446
42. Kutsukake K, Suzuki T, Yamaguchi S, Iino T (1979) Role of gene flaFV on flagellar hook formation in Salmonella typhimurium. J Bacteriol 140:267–275
43. Larsen SH, Reader RW, Kort EN, Tso W-W, Adler J (1974) Change in direction of flagellar rotation is the basis of the chemotactic response in Escherichia coli. Nature 249:74–77
44. Macnab RM (2003) How bacteria assemble flagella. Annu Rev Microbiol 57:77–100
45. Macnab RM (2004) Type III flagellar protein export and flagellar assembly. Biochim Biophys Acta 1694:207–217
46. Macnab RM, Koshland DE Jr (1972) The gradient-sensing mechanism in bacterial chemotaxis. Proc Natl Acad Sci USA 69:2509–2512
47. Macnab RM, Ornston MK (1977) Normal-to-curly flagellar transitions and their role in bacterial tumbling. Stabilization of an alternative quaternary structure by mechanical force. J Mol Biol 112:1–30
48. Maki S, Vonderviszt F, Furukawa Y, Imada K, Namba K (1998) Plugging interactions of HAP2 pentamer into the distal end of flagellar filament revealed by electron microscopy. J Mol Biol 277:771–777
49. Maki-Yonekura S, Yonekura K, Namba K (2003) Domain movements of HAP2 in the cap-filament complex formation and growth process of the bacterial flagellum. Proc Natl Acad Sci USA 100:15528–15533
50. Maki-Yonekura S, Yonekura K, Namba K (2010) Conformational change of flagellin for polymorphic supercoiling of the flagellar filament. Nat Struct Mol Biol 17:417–422
51. Manson MD, Tedesco P, Berg HC, Harold FM, Van der Drift C (1977) A protonmotive force drives bacterial flagella. Proc Natl Acad Sci USA 4:3060–3064
52. Matsunami H, Barker CS, Yoon YH, Wolf M, Samatey FA (2016) Complete structure of the bacterial flagellar hook reveals extensive set of stabilizing interactions. Nat Commun 7:13425
53. Mimori Y, Yamashita I, Murata K, Fujiyoshi Y, Yonekura K, Toyoshima C, Namba K (1995) The structure of the R-type straight flagellar filament of Salmonella at 9 Å resolution by electron cryomicroscopy. J Mol Biol 249:69–87
54. Mimori-Kiyosue Y, Vonderviszt FC, Namba K (1997) Location of terminal segments of flagellin in the filament structure and their roles in polymerization and polymorphism. J Mol Biol 270:222–237
55. Mimori-Kiyosue Y, Vonderviszt F, Yamashita I, Fujiyoshi Y, Namba K (1996) Direct interaction of flagellin termini essential for polymorphic ability of flagellar filament. Proc Natl Acad Sci USA 93:15108–15113
56. Minamino T, Imada K, Namba K (2008) Mechanisms of type III protein export for bacterial flagellar assembly. Mol BioSyst 4:1105–1115
57. Morgan DG, Owen C, Melanson LA, DeRosier DJ (1995) Structure of bacterial flagellar filaments at 11 Å resolution: packing of the α-helices. J Mol Biol 249:88–110
58. Moriya N, Minamino T, Hughes KT, Macnab RM, Namba K (2006) The type III flagellar export specificity switch is dependent on FliK ruler and a molecular clock. J Mol Biol 359:466–477
59. Moriya N, Minamino T, Imada K, Namba K (2011) Genetic analysis of the bacterial hook-capping protein FlgD responsible for hook assembly. Microbiology 157(Pt 5):1354–1362
60. Nambu T, Minamino T, Macnab RM, Kutsukake K (1999) Peptidoglycan-hydrolyzing activity of the FlgJ protein, essential for flagellar rod formation in Salmonella typhimurium. J Bacteriol 181:1555–1561
61. Nithichanon A, Rinchai D, Gori A, Lassaux P, Peri C, Conchillio-Solé O, Ferrer-Navarro M, Gourlay LJ, Nardini M, Vila J, Daura X, Colombo G, Bolognesi M, Lertmemonkolchai G (2015) Sequence- and structure-based Immunoreactive epitope discovery for Burkholderia pseudomallei Flagellin. PLoS Negl Trop Dis 9:e0003917
62. O’Brien EJ, Bennett PM (1972) Structure of straight flagella from a mutant Salmonella. J Mol Biol 73:133–152
63. Ohnishi K, Ohto Y, Aizawa S-I, Macnab RM, Iino T (1994) FlgD is a scaffolding protein needed for flagellar hook assembly in Salmonella typhimurium. J Bacteriol 176:2272–2281
64. Postel S, Deredge D, Bonsor DA, Yu X, Diederichs K, Helmsing S, Vromen A, Friedler A, Hust M, Egelman EH, Beckett D, Wintrode PL, Sundberg EJ (2016) Bacterial flagellar capping proteins adopt diverse oligomeric states. Elife 5. https://doi.org/10.7554/eLife.18857
65. Pulić I, Cendron L, Salamina M, Polverino de Laureto P, Matković-Čalogović D, Zanotti G (2016) Crystal structure of truncated FlgD from the human pathogen helicobacter pylori. J Struct Biol 194:147–155
66. Saijo-Hamano Y, Matsunami H, Namba K, Imada K (2013) Expression, purification, crystallization and preliminary X-ray diffraction analysis of a core fragment of FlgG, a bacterial flagellar rod protein. Acta Crystallogr Sect F Struct Biol Cryst Commun 69(Pt 5):547–550
67. Saijo-Hamano Y, Uchida N, Namba K, Oosawa K (2004) In vitro characterization of FlgB, FlgC, FlgF, FlgG, and FliE, flagellar basal body proteins of Salmonella. J Mol Biol 339:423–435
68. Samatey FA, Imada K, Nagashima S, Vonderviszt F, Kumasaka T, Yamamoto M, Namba K (2001) Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling. Nature 410:331–337
69. Samatey FA, Matsunami H, Imada K, Nagashima S, Shaikh TR, Thomas DR, Chen JZ, DeRosier DJ, Kitao A, Namba K (2004) Structure of the bacterial flagellar hook and implication for the molecular universal joint mechanism. Nature 431:1062–1068
70. Shaikh TR, Thomas DR, Chen JZ, Samatey FA, Matsunami H, Imada K, Namba K, DeRosier DJ (2005) A partial atomic structure for the flagellar hook of Salmonella typhimurium. Proc Natl Acad Sci USA 102:1023–1028
71. Song WS, Cho SY, Hong HJ, Park SC, Yoon SI (2017) Self-Oligomerizing structure of the flagellar cap protein FliD and its implication in filament assembly. J Mol Biol 429:847–857
72. Song WS, Jeon YJ, Namgung B, Hong M, Yoon SI (2017) A conserved TLR5 binding and activation hot spot on flagellin. Sci Rep 7:40878
73. Song WS, Yoon SI (2014) Crystal structure of FliC flagellin from Pseudomonas aeruginosa and its implication in TLR5 binding and formation of the flagellar filament. Biochem Biophys Res Commun 444:109–115
74. Suzuki T, Iino T (1981) Role of the flaR gene in flagellar hook formation in Salmonella spp. J Bacteriol 148:973–979
75. Suzuki H, Yonekura K, Namba K (2004) Structure of the rotor of the bacterial flagellar motor revealed by electron cryomicroscopy and single-particle image analysis. J Mol Biol 337:105–113
76. Thomas DR, Francis NR, Xu C, DeRosier DJ (2006) The three-dimensional structure of the flagellar rotor from a clockwise-locked mutant of Salmonella enterica serovar typhimurium. J Bacteriol 188:7039–7048
77. Turner L, Ryu WS, Berg HC (2000) Real-time imaging of fluorescent flagellar filaments. J Bacteriol 182:2793–2801
78. Vonderviszt F, Aizawa S, Namba K (1991) Role of the disordered terminal regions of flagellin in filament formation and stability. J Mol Biol 221:1461–1474
79. Vonderviszt F, Imada K, Furukawa Y, Uedaira H, Taniguchi H, Namba K (1998) Mechanism of self-association and filament capping by flagellar HAP2. J Mol Biol 284:1399–1416
80. Vonderviszt F, Ishima R, Akasaka K, Aizawa S (1992) Terminal disorder: a common structural feature of the axial proteins of bacterial flagellum? J Mol Biol 226:575–579
81. Wagenknecht T, DeRosier DJ, Aizawa S-I, Macnab RM (1982) Flagellar hook structures of Caulobacter and Salmonella and their relationship to filament structure. J Mol Biol 162:69–87
82. Wagenknecht T, DeRosier DJ, Shapiro L, Weissborn A (1981) Three-dimensional reconstruction of the flagellar hook from Caulobacter crescentus. J Mol Biol 151:439–465
83. Williams AW, Yamaguchi S, Togashi F, Aizawa S-I, Kawagishi I, Macnab RM (1996) Mutations in FliK and FlhB affecting flagellar hook and filament assembly in Salmonella typhimurium. J Bacteriol 178:2960–2970
84. Yamashita I, Hasegawa K, Suzuki H, Vonderviszt F, Mimori-Kiyosue Y, Namba K (1998) Structure and switching of bacterial flagellar filament studied by X-ray fiber diffraction. Nat Struct Biol 5:125–132
85. Yonekura K, Maki S, Morgan DG, DeRosier DJ, Vonderviszt F, Imada K, Namba K (2000) The bacterial flagellar cap as the rotary promoter of flagellin self-assembly. Science 290:2148–2152
86. Yonekura K, Maki-Yonekura S, Namba K (2003) Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424:643–650
87. Yoon SI, Kurnasov O, Natarajan V, Hong M, Gudkov AV, Osterman AL, Wilson IA (2012) Structural basis of TLR5-flagellin recognition and signaling. Science 335:859–864
88. Zaloba P, Bailey-Elkin BA, Derksen M, Mark BL (2016) Structural and biochemical insights into the peptidoglycan hydrolase domain of FlgJ from Salmonella typhimurium. PLoS One 11:e0149204
89. Zhou H, Luo M, Cai X, Tang J, Niu S, Zhang W, Hu Y, Yin Y, Huang A, Wang D, Wang D (2011) Crystal structure of a novel dimer form of FlgD from P. aeruginosa PAO1. Proteins 2011(79):2346–2351