Disulphide cross-linking between the stator and the bearing components in the bacterial flagellar motor

Journal of Biochemistry

Volumn 148, Issue 3, 2010, Pages 309-318

  Hizukuri, Yohei ^a,b   Kojima, Seiji ^a   Homma, Michio ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

bacterial flagella; disulphide bond; Escherichia coli; P ring; stator

Indexed keywords

CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; CYSTEINE; MOLECULAR MOTOR; MUTANT PROTEIN;

ARTICLE; CONTROLLED STUDY; CYTOPLASM; DISULFIDE BOND; ESCHERICHIA COLI; FLAGELLUM; MUTAGENESIS; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN CROSS LINKING;

BACTERIAL PROTEINS; CROSS-LINKING REAGENTS; DISULFIDES; ESCHERICHIA COLI PROTEINS; FLAGELLA; MOLECULAR MOTOR PROTEINS; MUTANT PROTEINS; PROTEIN BINDING;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 77956435557     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvq067     Document Type: Article

References (49)

1. Macnab, R.M. (2003) How bacteria assemble flagella. Annu. Rev. Microbiol. 57, 77-100
2. Blair, D.F. and Berg, H.C. (1990) The MotA protein of E. coli is a proton-conducting component of the flagellar motor. Cell 60, 439-449
3. Dean, G.E., Macnab, R.M., Stader, J., Matsumura, P., and Burks, C. (1984) Gene sequence and predicted amino acid sequence of the motA protein, a membraneassociated protein required for flagellar rotation in Escherichia coli. J. Bacteriol. 159, 991-999
4. Stader, J., Matsumura, P., Vacante, D., Dean, G.E., and Macnab, R.M. (1986) Nucleotide sequence of the Escherichia coli motB gene and site-limited incorporation of its product into the cytoplasmic membrane. J. Bacteriol. 166, 244-252
5. Stolz, B. and Berg, H.C. (1991) Evidence for interactions between MotA and MotB, torque-generating elements of the flagellar motor of Escherichia coli. J. Bacteriol. 173, 7033-7037
6. Akiba, T., Yoshimura, H., and Namba, K. (1991) Monolayer crystallization of flagellar L-P rings by sequential addition and depletion of lipid. Science 252, 1544-1546
7. Jones, C.J., Macnab, R.M., Okino, H., and Aizawa, S. (1990) Stoichiometric analysis of the flagellar hook-(basal-body) complex of Salmonella typhimurium. J. Mol. Biol. 212, 377-387 (Pubitemid 20130735)
8. Sosinsky, G.E., Francis, N.R., DeRosier, D.J., Wall, J.S., Simon, M.N., and Hainfeld, J. (1992) Mass determination and estimation of subunit stoichiometry of the bacterial hook-basal body flagellar complex of Salmonella typhimurium by scanning transmission electron microscopy. Proc. Natl Acad. Sci. USA 89, 4801-4805
9. Homma, M., Komeda, Y., Iino, T., and Macnab, R.M. (1987) The flaFIX gene product of Salmonella typhimurium is a flagellar basal body component with a signal peptide for export. J. Bacteriol. 169, 1493-1498
10. Kubori, T., Shimamoto, N., Yamaguchi, S., Namba, K., and Aizawa, S. (1992) Morphological pathway of flagellar assembly in Salmonella typhimurium. J. Mol. Biol. 226, 433-446
11. Nambu, T. and Kutsukake, K. (2000) The Salmonella FlgA protein, a putativeve periplasmic chaperone essential for flagellar P ring formation. Microbiology 146, 1171-1178
12. Dailey, F.E. and Berg, H.C. (1993) Mutants in disulfide bond formation that disrupt flagellar assembly in Escherichia coli. Proc. Natl Acad. Sci. USA 90, 1043-1047
13. Hizukuri, Y., Yakushi, T., Kawagishi, I., and Homma, M. (2006) Role of the intramolecular disulfide bond in FlgI, the flagellar P-ring component of Escherichia coli. J. Bacteriol. 188, 4190-4197
14. Hizukuri, Y., Kojima, S., Yakushi, T., Kawagishi, I., and Homma, M. (2008) Systematic Cys mutagenesis of FlgI, the flagellar P-ring component of Escherichia coli. Microbiology 154, 810-817
15. Zhou, J., Fazzio, R.T., and Blair, D.F. (1995) Membrane topology of the MotA protein of Escherichia coli. J. Mol. Biol. 251, 237-242
16. Chun, S.Y. and Parkinson, J.S. (1988) Bacterial motility: membrane topology of the Escherichia coli MotB protein. Science 239, 276-278
17. Braun, T.F., Al-Mawsawi, L.Q., Kojima, S., and Blair, D.F. (2004) Arrangement of core membrane segments in the MotA/MotB proton-channel complex of Escherichia coli. Biochemistry 43, 35-45
18. Kojima, S. and Blair, D.F. (2004) Solubilization and purification of the MotA/MotB complex of Escherichia coli. Biochemistry 43, 26-34
19. Sato, K. and Homma, M. (2000) Functional reconstitution of the Na-driven polar flagellar motor component of Vibrio alginolyticus. J. Biol. Chem. 275, 5718-5722 (Pubitemid 30115213)
20. Yorimitsu, T., Kojima, M., Yakushi, T., and Homma, M. (2004) Multimeric structure of the PomA/PomB channel complex in the Na-driven flagellar motor of Vibrio alginolyticus. J. Biochem. 135, 43-51
21. Reid, S.W., Leake, M.C., Chandler, J.H., Lo, C.J., Armitage, J.P., and Berry, R.M. (2006) The maximum number of torque-generating units in the flagellar motor of Escherichia coli is at least 11. Proc. Natl Acad. Sci. USA 103, 8066-8071
22. Blair, D.F. (2003) Flagellar movement driven by proton translocation. FEBS Lett. 545, 86-95
23. De Mot, R. and Vanderleyden, J. (1994) The C-terminal sequence conservation between OmpA-related outer membrane proteins and MotB suggests a common function in both gram-positive and gram-negative bacteria, possibly in the interaction of these domains with peptidoglycan. Mol. Microbiol. 12, 333-334
24. Koebnik, R. (1995) Proposal for a peptidoglycanassociating alpha-helical motif in the C-terminal regions Cross-linking between MotB and FlgIof some bacterial cell-surface proteins. Mol. Microbiol. 16, 1269-1270
25. Roujeinikova, A. (2008) Crystal structure of the cell wall anchor domain of MotB, a stator component of the bacterial flagellar motor: implications for peptidoglycan recognition. Proc. Natl Acad. Sci. USA 105, 10348-10353
26. Kojima, S., Imada, K., Sakuma, M., Sudo, Y., Kojima, C., Minamino, T., Homma, M., and Namba, K. (2009) Stator assembly and activation mechanism of the flagellar motor by the periplasmic region of MotB. Mol. Microbiol. 73, 710-718
27. Bouveret, E., Benedetti, H., Rigal, A., Loret, E., and Lazdunski, C. (1999) In vitro characterization of peptidoglycan-associated lipoprotein (PAL)-peptidoglycan and PAL-TolB interactions. J. Bacteriol. 181, 6306-6311
28. Lazzaroni, J.C. and Portalier, R. (1992) The excC gene of Escherichia coli K-12 required for cell envelope integrity encodes the peptidoglycan- associated lipoprotein (PAL). Mol. Microbiol. 6, 735-742
29. Leduc, M., Ishidate, K., Shakibai, N., and Rothfield, L. (1992) Interactions of Escherichia coli membrane lipoproteins with the murein sacculus. J. Bacteriol. 174, 7982-7988
30. Mizuno, T. (1979) A novel peptidoglycan-associated lipoprotein found in the cell envelope of Pseudomonas aeruginosa and Escherichia coli. J. Biochem. 86, 991-1000
31. Hizukuri, Y., Morton, J.F., Yakushi, T., Kojima, S., and Homma, M. (2009) The peptidoglycan-binding (PGB) domain of the Escherichia coli Pal protein can also function as the PGB domain in E. coli flagellar motor protein MotB. J. Biochem. 146, 219-229
32. Leake, M.C., Chandler, J.H., Wadhams, G.H., Bai, F., Berry, R.M., and Armitage, J.P. (2006) Stoichiometry and turnover in single, functioning membrane protein complexes. Nature 443, 355-358
33. Fukuoka, H., Wada, T., Kojima, S., Ishijima, A., and Homma, M. (2009) Sodium-dependent dynamic assembly of membrane complexes in sodium-driven flagellar motors. Mol. Microbiol. 71, 825-835
34. Paulick, A., Koerdt, A., Lassak, J., Huntley, S., Wilms, I., Narberhaus, F., and Thormann, K.M. (2009) Two different stator systems drive a single polar flagellum in Shewanella oneidensis MR-1. Mol. Microbiol. 71, 836-850
35. Yakushi, T., Hattori, N., and Homma, M. (2005) Deletion analysis of the carboxyl-terminal region of the PomB component of the Vibrio alginolyticus polar flagellar motor. J. Bacteriol. 187, 778-784
36. Fukuoka, H., Yakushi, T., Kusumoto, A., and Homma, M. (2005) Assembly of motor proteins, PomA and PomB, in the Na-driven stator of the flagellar motor. J. Mol. Biol. 351, 707-717
37. Kojima, S., Furukawa, Y., Matsunami, H.,Minamino, T., and Namba, K. (2008) Characterization of the periplasmic domain of MotB and implications for its role in the stator assembly of the bacterial flagellar motor. J. Bacteriol. 190, 3314-3322
38. Terashima, H., Fukuoka, H., Yakushi, T., Kojima, S., and Homma, M. (2006) The Vibrio motor proteins, MotX and MotY, are associated with the basal body of Na-driven flagella and required for stator formation. Mol. Microbiol. 62, 1170-1180
39. Okabe, M., Yakushi, T., and Homma, M. (2005) Interactions of MotX with MotY and with the PomA/ PomB sodium ion channel complex of the Vibrio alginolyticus polar flagellum. J. Biol. Chem. 280, 25659-25664
40. Togashi, F., Yamaguchi, S., Kihara, M., Aizawa, S.I., and Macnab, R.M. (1997) An extreme clockwise switch bias mutation in fliG of Salmonella typhimurium and its suppression by slow-motile mutations in motA and motB. J. Bacteriol. 179, 2994-3003
41. Fung, D.C. and Berg, H.C. (1995) Powering the flagellar motor of Escherichia coli with an external voltage source. Nature 375, 809-812
42. Kudryashev, M., Cyrklaff, M., Wallich, R., Baumeister, W., and Frischknecht, F. (2009) Distinct in situ structures of the Borrelia flagellar motor. J. Struct. Biol. 69, 54-61
43. Ohnishi, K., Homma, M., Kutsukake, K., and Iino, T. (1987) Formation of flagella lacking outer rings by flaM, flaU, and flaY mutants of Escherichia coli. J. Bacteriol. 169, 1485-1488
44. Hosking, E.R., Vogt, C., Bakker, E.P., and Manson, M.D. (2006) The Escherichia coli MotAB proton channel unplugged. J. Mol. Biol. 364, 921-937
45. Morimoto, Y.V., Che, Y.S., Minamino, T., and Namba, K. (2010) Proton-conductivity assay of plugged and unplugged MotA/B proton channel by cytoplasmic pHluorin expressed in Salmonella. FEBS Lett. 584, 1268-1272
46. Parkinson, J.S. and Houts, S.E. (1982) Isolation and behavior of Escherichia coli deletion mutants lacking chemotaxis functions. J. Bacteriol. 151, 106-113
47. Slocum, M.K. and Parkinson, J.S. (1983) Genetics of methyl-accepting chemotaxis proteins in Escherichia coli: organization of the tar region. J. Bacteriol. 155, 565-577
48. Guzman, L.M., Belin, D.M., Carson, J., and Beckwith, J. (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177, 4121-4130
49. Bartolome, B., Jubete, Y., Martinez, E., and de la Cruz, F. (1991) Construction and properties of a family of pACYC184-derived cloning vectors compatible with pBR322 and its derivatives. Gene 102, 75-78