Helicobacter pylori FlhB function: The FlhB C-terminal homologue HP1575 acts as a "spare part" to permit flagellar export when the HP0770 FlhBCC domain is deleted

Journal of Bacteriology

Volumn 188, Issue 21, 2006, Pages 7531-7541

  Wand, Matthew E ^a,c   Sockett, R Elizabeth ^b   Evans, Katy J ^b   Doherty, Neil ^a   Sharp, Paul M ^b   Hardie, Kim R ^b   Winzer, Klaus ^b  

^a QUEEN S MEDICAL CENTRE   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GENE PRODUCT; MUTANT PROTEIN; PROLINE; PROTEIN FLHB; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL GENE; BACTERIAL STRAIN; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DELETION MUTANT; ESCHERICHIA COLI; GENE MUTATION; HELICOBACTER PYLORI; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PROCESSING; PROTEIN TRANSPORT; SALMONELLA ENTERICA;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; CONSERVED SEQUENCE; ESCHERICHIA COLI; FLAGELLA; GENE DELETION; HELICOBACTER PYLORI; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MOVEMENT; PHYLOGENY; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; SALMONELLA ENTERICA; SEQUENCE ALIGNMENT; SEQUENCE DELETION;

ESCHERICHIA COLI; HELICOBACTER PYLORI; HELICOBACTER PYLORI 26695; SALMONELLA ENTERICA;

EID: 33750473415     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00263-06     Document Type: Article

References (42)

1. Alm, R. A., L. S. Ling, D. T. Moir, B. L. King, E. D. Brown, P. C. Doig, D. R. Smith, B. Noonan, B. C. Guild, B. L. deJonge, G. Carmel, P. J. Tummino, A. Caruso, M. Uria-Nickelsen, D. M. Mills, C. Ives, R. Gibson, D. Merberg, S. D. Mills, Q. Jiang, D. E. Taylor, G. F. Vovis, and T. J. Trust. 1999. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397:176-180.
2. Bacher, A., M. Fischer, K. Kis, K. Kugelbrey, S. Mortl, J. Scheuring, S. Weinkauf, S. Eberhardt, K. Schmidt-Base, R. Huber, K. Ritsert, M. Cushman, and R. Ladenstein. 1996. Biosynthesis of riboflavin: structure and mechanism of lumazine. Biochem. Soc. Trans. 24:89-94.
3. Danon, S. J., and K. A. Eaton. 1998. Isogenic flagella mutants of Helicobacter pylori: candidates for an attenuated vaccine? Gut 43:A38.
4. Eaton, K. A., D. R. Morgan, and S. Krakowka. 1992. Motility as a factor in the colonisation of gnotobiotic piglets by Helicobacter pylori. Med. Microbiol. 37:123-127.
5. Fan, F., K. Ohnishi, N. R. Francis, and R. M. Macnab. 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.
6. Fassbinder, F., M. Kist, and S. Bereswill. 2000. Structural and functional analysis of the riboflavin synthesis genes encoding GTP cyclohydrolase II (ribA), DHSP synthase (ribBA), riboflavin synthase (ribC), and riboflavin deaminase/reductase (ribD) from Helicobacter pylori strain P1. FEMS Microbiol. Lett. 191:191-197.
7. Fauconnier, A., A. Allaoui, A. Campos, A. Van Elsen, G. R. Cornelis, and A. Bollen. 1997. Flagellar flhA, flhB and flhE genes, organized in an operon, cluster upstream from the inv locus in Yersinia enterocolitica. Microbiology 143:3461-3471.
8. Ferris, H. U., Y. Furukawa, T. Minamino, M. B. Kroetz, M. Kihara, K. Namba, and R. M. Macnab. 2005. FlhB regulates ordered export of flagellar components via autocleavage mechanism. J. Biol. Chem. 280:41236-41242.
9. Foynes, S., N. Dorrell, S. J. Ward, Z. W. Zhang, A. A. McColm, M. J. G. Farthing, and B. W. Wren. 1999. Functional analysis of the roles of FliQ and FlhB in flagellar expression in Helicobacter pylori. FEMS Microbiol. Lett. 174:33-39.
10. Fraser, G. M., T. Hirano, H. U. Ferris, L. L. Devgan, M. Kihara, and R. M. Macnab. 2003. Substrate specificity of type III flagellar protein export in Salmonella is controlled by subdomain interactions in FlhB. Mol. Microbiol. 48:1043-1047.
11. Geis, G., S. Suerbaum, B. Forsthoff, H. Leying, and W. Opferkuch. 1993. Ultrastructurc and biochemical studies of the flagellar sheath of Helicobacter pylori. J. Med. Microbiol. 38:371-377.
12. Hendricks, J. K., and H. L. T. Mobley. 1997. Helicobaaer pylori ABC transporter: effect of allelic exchange mutagenesis on urease activity. J. Bacteriol. 179:5892-5902.
13. Hirano, T., S. Yamaguchi, K. Oosawa, and S. Aizawa. 1994. Roles of FliK and FlhB in determination of flagellar hook length in Salmonella typhimurium. J. Bacteriol. 176:5439-5449.
14. Huelsenbeck, J. P., and F. Ronquist. 2001. MrBayes: Bayesian inference of phylogeny. Bioinformatics 17:754-755.
15. Koroyasu, S., M. Yamazato, T. Hirano, and S.-I. Aizawa. 1996. Kinetic analysis of the growth rate of the flagellar hook in Salmonella typhimurium by the population balance method. Biophys. J. 74:436-443.
16. Lavander, M., L. Sundberg, P. J. Edqvist, S. A. Lloyd, H. Wolf-Watz, and Å. Forsberg. 2002. Proteolytic cleavage of the FlhB homologue YscU of Yersinia pseudotuberculosis is essential for bacterial survival but not for type III secretion. J. Bacteriol. 184:4500-4509.
17. Macnab, R. M. 1996. Flagella and motility, p. 123-145. in F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schacchter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed. ASM Press, Washington, D.C.
18. Marshall, B. 2002. Helicobacter pylori: 20 years on. Clin. Med. 2:147-152.
19. Matz, C., A. H. van Vliet, J. M. Ketley, and C. W. Penn. 2002. Mutational and transcriptional analysis of the Campylobacter jejuni flagellar biosynthesis gene flhB. Microbiology 148:1679-1685.
20. Ménard, R., P. J. Sonsonetti, and C. Parsot. 1993. Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC and IpaD as effectors of Shigella flexneri entry into epithelial cells. J. Bacteriol. 175:5899-5906.
21. Minamino, T., T. Iino, and K. Kutsukake. 1994. Molecular characterisation of the Salmonella typhimurium flhB operon and its protein products. J. Bacteriol. 176:7630-7637.
22. Minamino, T., and R. M. Macnab. 1999. Components of the Salmonella flagellar export apparatus and classification of export substrates. J. Bacteriol. 181:1388-1394.
23. Minamino, T., and R. M. Macnab. 2000. Interactions among components of the Salmonella flagellar export apparatus and its substrates. Mol. Microbiol. 35:1052-1064.
24. Minamino, T., and R. M. Macnab. 2000. Domain structure of Salmonella FlhB, a flagellar export component responsible for substrate specificity switching. J. Bacteriol. 182:4906-4914.
25. Morehouse, K. A., I. G. Goodfellow, and R. E. Sockett. 2005. A chimeric N-terminal Escherichia coli-C-Terminal Rhodobacter sphaeroides FliG rotor protein supports bidirectional E. coli flagellar rotation and chemotaxis. J. Bacteriol. 187:1695-1701.
26. Niehus, E., H. Gressmann, Y. Fang, R. Schlapbach, M. Dehio, C. Dehio, A. Stack, T. F. Meyer, S. Suerbaum, and C. Josenhans. 2004. Genome-wide analysis of transcriptional hierarchy and feedback regulation in the flagellar system of Helicobacter pylori. Mol. Microbiol. 42:947-961.
27. Pallen, M. J., C. W. Penn, and R. R. Chaudhuri. 2005. Bacterial flagellar diversity in the post-genomic era. Trends Microbiol. 13:143-149.
28. Parkinson, J. S. 1978. Complementation analysis and deletion mapping of Escherichia coli mutants defective in chemotaxis. J. Bacteriol. 135:45-53.
29. Penn, C. W., and C. J. Luke. 1992. Bacterial flagellar diversity and significance in pathogenesis. FEMS Microbiol. Lett. 100:331-336.
30. Pitcher, D. G., N. A. Saunders, and R. J. Owen. 1989. Rapid extraction of bacterial genomic DNA with guanidium thiocyanate. Lett. Appl. Microbiol. 8:151-156.
31. Rambaut, A., and A. J. Drummond. 2003. Tracer, version 1.2. [Online.] http://evolve.zoo.ox.ac.uk/.
32. Ryan, K. A., Q. N. Karim, M. Worku, C. W. Penn, and P. W. O'Toole. 2005. Helicobacter pylori flagellar hook-filament transition is controlled by a FliK functional homolog encoded by the gene HP0906. J. Bacteriol. 187:5742-5750.
33. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N. Y.
34. Segura, A., E. Duque, A. Hurtado, and J. L. Ramos. 2001. Mutations in genes involved in the flagellar export apparatus of the solvent-tolerant Pseudomonas putida DOT-TIE strain impair motility and lead to hypersensitivity to toluene shocks. J. Bacteriol. 183:4127-4133.
35. Suerbaum, S., and P. Michetti. 2002. Helicobacter pylori infection. N. Engl. J. Med. 347:1175-1186.
36. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence-weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
37. Tomb, J.-F., O. White, A. R. Kerlavage, R. A. Clayton, G. C. Sutton, R. D. Fleischmann, K. A. Ketchum, H. P. Klenk, S. Gill, B. A. Dougherty, K. Nelson, J. Quackenbush, L. Zhou, E. F. Kirkness, S. Peterson, B. Loftus, D. Richardson, R. Dodson, H. G. Khalak, A. Glodek, K. McKenny, L. M. Fitzegerald, N. Lee, M. D. Adams, E. K. Hickey, D. E. Berg, J. D. Gocayne, T. R. Utterback, J. D. Peterson, J. M. Kelley, M. D. Cotton, J. M. Weidman, C. Fujii, C. Bowman, L. Watthey, E. Wallin, W. S. Hayes, M. Borodovsky, P. D. Karpi, H. O. Smith, C. M. Fraser, and J. C. Venter. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-547.
38. Trieu-Cuot, P., G. Gerbaud, T. Lambert, and P. Courvalin. 1985. In vivo transfer of genetic information between gram-positive and gram-negative bacteria. EMBO J. 4:3583-3587.
39. Van Arnam, J. S., J. L. McMurry, M. Kihara, and R. M. Macnab. 2004. Analysis of an engineered Salmonella flagellar fusion protein, FliR-FlhB. J. Bacteriol. 186:2495-2498.
40. Wang, Y., and D. E. Taylor. 1990. Chloramphenicol resistance in Campylobacter coli: nucleotide sequence, expression, and cloning vector construction. Gene 94:23-28.
41. Williams, A. W., S. Yamaguchi, F. Togashi, S. I. Aizawa, I. Kawagishi, and R. M. Macnab. 1996. Mutations in fliK and flhB affecting flageilar hook and filament assembly in Salmonella typhimurium. J. Bacteriol. 178:2960-2970.
42. Yanish-Perron, C., J. Vieira, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-109.