The interaction dynamics of a negative feedback loop regulates flagellar number in Salmonella enterica serovar Typhimurium

Molecular Microbiology

Volumn 78, Issue 6, 2010, Pages 1416-1430

  Aldridge, Christine ^a,b   Poonchareon, Kritchai ^a,b   Saini, Supreet ^c   Ewen, Thomas ^a,b   Soloyva, Alexandra ^b   Rao, Christopher V ^c   Imada, Katsumi ^d   Minamino, Tohru ^d,e   Aldridge, Phillip D ^a,b  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d OSAKA UNIVERSITY   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DNA; PROTEIN FLHC; PROTEIN FLHD; PROTEIN FLID; PROTEIN FLIT; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL GROWTH; COMPLEX FORMATION; CONTROLLED STUDY; DNA PROTEIN COMPLEX; GENE DELETION; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; SALMONELLA TYPHIMURIUM;

BACTERIAL PROTEINS; FLAGELLA; GENE EXPRESSION REGULATION, BACTERIAL; PROTEIN BINDING; SALMONELLA TYPHIMURIUM;

SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 78649658125     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07415.x     Document Type: Article

References (42)

1. Adler, J., and Templeton, B. (1967) The effect of environmental conditions on the motility of Escherichia coli. J Gen Microbiol 46: 175-184.
2. Aldridge, P., Karlinsey, J., and Hughes, K.T. (2003) The type III secretion chaperone FlgN regulates flagellar assembly via a negative feedback loop containing its chaperone substrates FlgK and FlgL. Mol Microbiol 49: 1333-1345.
3. Aldridge, P., Karlinsey, J.E., Becker, E., Chevance, F.F., and Hughes, K.T. (2006a) Flk prevents premature secretion of the anti-sigma factor FlgM into the periplasm. Mol Microbiol 60: 630-643.
4. 28 factor FlgM. Genes Dev 20: 2315-2326.
5. Bange, G., Kummerer, N., Engel, C., Bozkurt, G., Wild, K., and Sinning, I. (2010) FlhA provides the adaptor for coordinated delivery of late flagella building blocks to the type III secretion system. Proc Natl Acad Sci USA 107: 11295-11300.
6. Barkai, N., and Leibler, S. (1997) Robustness in simple biochemical networks. Nature 387: 913-917.
7. Bonifield, H.R., Yamaguchi, S., and Hughes, K.T. (2000) The flagellar hook protein, FlgE, of Salmonella enterica serovar Typhimurium is posttranscriptionally regulated in response to the stage of flagellar assembly. J Bacteriol 182: 4044-4050.
8. Brown, J.D., Saini, S., Aldridge, C., Herbert, J., Rao, C.V., and Aldridge, P.D. (2008) The rate of protein secretion dictates the temporal dynamics of flagellar gene expression. Mol Microbiol 70: 924-937.
9. Chilcott, G.S., and Hughes, K.T. (2000) Coupling of Flagellar Gene Expression to Flagellar Assembly in Salmonella enterica Serovar Typhimurium and Escherichia coli. Microbiol Mol Biol Rev 64: 694-708.
10. Claret, L., and Hughes, C. (2000) Functions of the subunits in the FlhD(2)C(2) transcriptional master regulator of bacterial flagellum biogenesis and swarming. J Mol Biol 303: 467-478.
11. Darnton, N., Turner, L., Rojevsky, S., and Berg, H.C. (2007) On torque and tumbling in swimming Escherichia coli. J Bacteriol 189: 1756-1764.
12. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
13. Davis, R.W., Botstein, D., Roth, J.R., and Cold Spring Harbor N.Y. Laboratory of Quantitative Biology (1980) Advanced Bacterial Genetics: A Manual for Genetic Engineering. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
14. Erhardt, M., and Hughes, K.T. (2010) C-ring requirement in flagellar type III secretion is bypassed by FlhDC upregulation. Mol Microbiol 75: 376-393.
15. Evans, L.D., Stafford, G.P., Ahmed, S., Fraser, G.M., and Hughes, C. (2006) An escort mechanism for cycling of export chaperones during flagellum assembly. Proc Natl Acad Sci USA 103: 17474-17479.
16. Fraser, G.M., Bennett, J.C., and Hughes, C. (1999) Substrate-specific binding of hook-associated proteins by FlgN and FliT, putative chaperones for flagellum assembly. Mol Microbiol 32: 569-580.
17. Gillen, K.L., and Hughes, K.T. (1991a) Molecular characterization of flgM, a gene encoding a negative regulator of flagellin synthesis in Salmonella typhimurium. J Bacteriol 173: 6453-6459.
18. Gillen, K.L., and Hughes, K.T. (1991b) Negative regulatory loci coupling flagellin synthesis to flagellar assembly in Salmonella typhimurium. J Bacteriol 173: 2301-2310.
19. Goodier, R.I., and Ahmer, B.M. (2001) SirA orthologs affect both motility and virulence. J Bacteriol 183: 2249-2258.
20. Hughes, K.T., Gillen, K.L., Semon, M.J., and Karlinsey, J.E. (1993) Sensing structural intermediates in bacterial flagellar assembly by export of a negative regulator. Science 262: 1277-1280.
21. Iino, T. (1974) Assembly of Salmonella flagellin in vitro and in vivo. J Supramol Struct 2: 372-384.
22. Imada, K., Minamino, T., Kinoshita, M., Furukawa, Y., and Namba, K. (2010) Structural insight into the regulatory mechanisms of interactions of the flagellar type III chaperone FliT with its binding partners. Proc Natl Acad Sci USA 107: 8812-8817.
23. Karlinsey, J.E., Tanaka, S., Bettenworth, V., Yamaguchi, S., Boos, W., Aizawa, S.I., and Hughes, K.T. (2000) Completion of the hook-basal body complex of the Salmonella typhimurium flagellum is coupled to FlgM secretion and fliC transcription. Mol Microbiol 37: 1220-1231.
24. Kutsukake, K., and Iino, T. (1994) Role of the FliA-FlgM regulatory system on the transcriptional control of the flagellar regulon and flagellar formation in Salmonella typhimurium. J Bacteriol 176: 3598-3605.
25. Kutsukake, K., Ikebe, T., and Yamamoto, S. (1999) Two novel regulatory genes, fliT and fliZ, in the flagellar regulon of Salmonella. Genes Genet Syst 74: 287-292.
26. Liu, X., Fujita, N., Ishihama, A., and Matsumura, P. (1995) The C-terminal region of the alpha subunit of Escherichia coli RNA polymerase is required for transcriptional activation of the flagellar level II operons by the FlhD/FlhC complex. J Bacteriol 177: 5186-5188.
27. Murray, H., and Errington, J. (2008) Dynamic control of the DNA replication initiation protein DnaA by Soj/ParA. Cell 135: 74-84.
28. Ohnishi, K., Kutsukake, K., Suzuki, H., and Iino, T. (1990) Gene fliA encodes an alternative sigma factor specific for flagellar operons in Salmonella typhimurium. Mol Gen Genet 221: 139-147.
29. Overgaard, M., Borch, J., Jorgensen, M.G., and Gerdes, K. (2008) Messenger RNA interferase RelE controls relBE transcription by conditional cooperativity. Mol Microbiol 69: 841-857.
30. Pruss, B.M., and Matsumura, P. (1996) A regulator of the flagellar regulon of Escherichia coli, flhD, also affects cell division. J Bacteriol 178: 668-674.
31. Pruss, B.M., and Matsumura, P. (1997) Cell cycle regulation of flagellar genes. J Bacteriol 179: 5602-5604.
32. Saijo-Hamano, Y., Imada, K., Minamino, T., Kihara, M., Shimada, M., Kitao, A., and Namba, K. (2010) Structure of the cytoplasmic domain of FlhA and implication for flagellar type III protein export. Mol Microbiol 76: 260-268.
33. 2-dependent flagellar gene expression. J Bacteriol 190: 4979-4988.
34. Schaechter, M., Maaloe, O., and Kjeldgaard, N.O. (1958) Dependency on medium and temperature of cell size and chemical composition during balanced grown of Salmonella typhimurium. J Gen Microbiol 19: 592-606.
35. Schuck, P. (1998) Sedimentation analysis of noninteracting and self-associating solutes using numerical solutions to the Lamm equation. Biophys J 75: 1503-1512.
36. Schuck, P. (2003) On the analysis of protein self- association by sedimentation velocity analytical ultracentrifugation. Anal Biochem 320: 104-124.
37. Soutourina, O.A., and Bertin, P.N. (2003) Regulation cascade of flagellar expression in Gram-negative bacteria. FEMS Microbiol Rev 27: 505-523.
38. 2. Microbiology 151: 1779-1788.
39. Turner, L., Ryu, W.S., and Berg, H.C. (2000) Real-time imaging of fluorescent flagellar filaments. J Bacteriol 182: 2793-2801.
40. Vogel, H.J., and Bonner, D.M. (1956) Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem 218: 97-106.
41. Wang, S., Fleming, R.T., Westbrook, E.M., Matsumura, P., and McKay, D.B. (2006) Structure of the Escherichia coli FlhDC complex, a prokaryotic heteromeric regulator of transcription. J Mol Biol 355: 798-808.
42. 2 factor in the transcriptional control of the flagellar regulon in Salmonella enterica serovar Typhimurium. J Bacteriol 188: 6703-6708.