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Turnover of FlhD and FlhC, master regulator proteins for Salmonella flagellum biogenesis, by the ATP-dependent ClpXP protease

  1. Toshifumi Tomoyasu1,
  2. Akiko Takaya1,
  3. Emiko Isogai2,
  4. Tomoko Yamamoto1

Article first published online: 4 APR 2003

DOI: 10.1046/j.1365-2958.2003.03437.x

Issue

Molecular Microbiology

Molecular Microbiology

Volume 48, Issue 2, pages 443–452, April 2003

Additional Information

How to Cite

Tomoyasu, T., Takaya, A., Isogai, E. and Yamamoto, T. (2003), Turnover of FlhD and FlhC, master regulator proteins for Salmonella flagellum biogenesis, by the ATP-dependent ClpXP protease. Molecular Microbiology, 48: 443–452. doi: 10.1046/j.1365-2958.2003.03437.x

Author Information

  1. 1

    Department of Microbiology and Molecular Genetics, Graduate School of Pharmaceutical Sciences, Chiba University, Chiba, 263–8522, Japan.

  2. 2

    Department of Preventive Dentistry, Health Sciences, University of Hokkaido, Ishikari-Tobetsu, Hokkaido, 061–0293, Japan.

* For correspondence. E-mail tomoko-y @p.chiba-u.ac.jp ; Tel. (+81) 43 290 2928; Fax (+81) 43 290 2929.

Publication History

  1. Issue published online: 4 APR 2003
  2. Article first published online: 4 APR 2003
  3. Accepted 16 December, 2002.

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References

  • Bertin, P., Terao, E., Lee, E.V., Lejeune, P., Colson, C., Danchin, A., and Collatz, E. (1994) The H-NS protein is involved in the biogenesis of flagella in Escherichia coli. J Bacteriol176: 5537–5540.
  • Claret, L., and Hughes, C. (2000a) Functions of the subunits in the FlhD2C2 transcriptional master regulator of bacterial flagellum biogenesis and swarming. J Mol Biol303: 467–478.
  • Claret, L., and Hughes, C. (2000b) Rapid turnover of FlhD and  FlhC,  the  flagellar  regulon  transcriptional  activator proteins, during Proteus swarming. J Bacteriol182: 833–836.
  • Gamer, J., Bujard, H., and Bukau, B. (1992) Physical inter-action between heat shock proteins DnaK, DnaJ, and GrpE and the bacterial heat shock transcription factor σ32. Cell69: 833–842.
  • Goldberg, A.L. (1992) The mechanism and functions of ATP-dependent proteases in bacterial and animal cells. Eur J Biochem203: 9–223.
    Direct Link:
  • Gonzalez, M., Rasulova, F., Maurizi, M.R., and Woodgate, R. (2000) Subunit-specific degradation of the UmuD/D’heterodimer by the ClpXP protease: the role of trans recognition in UmuD′ stability. EMBO J19: 5251–5258.
  • Gottesman, S. (1996) Proteases and their targets in Escherichia coli. Annu Rev Genet30: 465–506.
  • Gottesman, S., and Maurizi, M.R. (1992) Regulation by proteolysis: energy dependent proteases and their targets. Microbiol Rev56: 592–621.
  • Gulig, P.A., and Curtiss, R., III (1987) Plasmid-associated virulence of Salmonella typhimurium. Infect Immun55: 2891–2901.
  • Ibba, M., and Soll, D. (1999) Quality control mechanisms during translation. Science286: 1893–1897.
  • Ikebe, T., Iyoda, S., and Kutsukake, K. (1999) Promoter analysis of the class 2 flagellar operons of Salmonella. Genes Genet Syst74: 179–183.
  • Jenal, U., and Fuchs, T. (1998) An essential protease involved in bacterial cell-cycle control. EMBO J17: 5658–5669.
  • Keiler, K.C., Waller, P.R., and Sauer, R.T. (1996) Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science271: 990–993.
  • Kessel, M., Maurizi, M.R., Kim, B., Kocsis, E., Trus, B.L., Singh, S.K., and Steven, A.C. (1995) Homology in structural organization between E.coli ClpAP protease and the eukaryotic 26 S proteasome. J Mol Biol250: 587–594.
  • Kutsukake, K. (1997) Autogenous and global control of the flagellar master operon, flhD. Salmonella typhimurium. Mol Gen Genet254: 440–448.
  • 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 Bacteriol176: 3538–3605.
  • Kutsukake, K., Iino, T., Komeda, Y., and Yamaguchi, S. (1980) Functional homology of fla genes between Salmonella typhimurium and Escherichia coli. Mol Gen Genet178: 59–67.
  • Kutsukake, K., Ohya, Y., Yamaguchi, S., and Iino, T. (1988) Operon structure of flagellar genes in Salmonella typhimurium. Mol Gen Genet214: 11–15.
  • Kutsukake, K., Ohya, Y., and Iino, T. (1990) Transcriptional analysis of the flagellar regulon of Salmonella typhimurium. J Bacteriol172: 741–747.
  • Laachouch, J.E., Desmet, L., Geuskens, V., Grimaud, R., and Toussaint, A. (1996) Bacteriophage Mu repressor as a target for the Escherichia coli ATP-dependent Clp protease. EMBO J15: 437–444.
  • Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature227: 680–685.
  • Lehnherr, H., and Yarmolinsky, M.B. (1995) Addiction protein Phd of plasmid prophage P1 is a substrate of the ClpXP serine protease of Escherichia coli. Proc Natl Acad Sci USA92: 3274–3277.
  • Levchenko, I., Luo, L., and Baker, T.A. (1995) Disassembly of the Mu transposase tetramer by the ClpX chaperone. Genes Dev9: 2399–2408.
  • Liu, X., and Matsumura, P. (1994) The FlhD/FlhC complex, a transcriptional activator of the Escherichia coli flagellar class II operons. J Bacteriol176: 7345–7351.
  • Lupas, A., Flanagan, J.M., Tamura, T., and Baumeister, W. (1997) Selfcompartmentalizing proteases. Trends Biochem. Sci22: 399–404.
  • Lutz, R., and Bujard, H. (1997) Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I, 1 -I, 2 regulatory elements. Nucleic Acids Res25: 1203–1210.
  • Macnab, R.M. (1996) Flagella and Motility. In Escherichia Coli and Salmonella: Cellular and Molecular Biology. Neidhardt, F.C., Curtiss, R., III, Ingraham, H.L., Lin, E.C.C., Low, K. B., Magasanik, B et al. (eds) . Washington, DC: American Society for Microbiology Press, pp. 123–145.
  • Maurizi, M.R. (1992) Proteases and protein degradation in Escherichia coli. Experientia48: 178–200.
  • Miller, J.H. (1972) Experiments in molecular genetics. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory.
  • Neuwald, A.F., Aravind, L., Spouge, J.L., and Koonin, E.V. (1999) AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res9: 27–43.
  • 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 Genet221: 139–147.
  • Porankiewicz, J., Wang, J., and Clarke, A.K. (1999) New insights into the ATP-dependent Clp protease: Escherichia coli and beyond. Mol Microbiol32: 449–458.
    Direct Link:
  • Rohrwild, M., Coux, O., Huang, H.C., Moerschell, R.P., Yoo, S.J., Seol, J.H., et al. (1996) HslV-HslU: a novel ATP-dependent protease complex in Escherichia coli related to the eukaryotic proteasome. Proc Natl Acad Sci USA93: 5808–5813.
  • Schweder, T., Lee, K.H., Lomovskaya, O., and Matin, A. (1996) Regulation of Escherichia coli starvation sigma factor (sigma s) by ClpXP protease. J Bacteriol178: 470–476.
  • Shi, W., Zhou, Y., Wild, J., Alder, J., and Gross, C.A. (1992) DnaK, DnaJ and GrpE are required for flagellum synthesis. J Bacteriol174: 6256–6263.
  • Simon, R., Priefer, U., and Puhler, A. (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Bio Technol1: 784–791.
  • Takaya, A., Tomoyasu, T., Tokumitsu, A., Morioka, M., and Yamamoto, T. (2002) The ATP-dependent Lon protease of Salmonella enterica serovar Typhimurium regulates invasion and expression of genes carried on Salmonella pathogenicity island 1. J Bacteriol184: 224–232.
  • Tobias, J.W., Shrader, T.E., Rocap, G., and Varshavsky, A. (1991) The N-end rule in bacteria. Science254: 1374–1377.
  • Tomoyasu, T., Ohkishi, T., Ukyo, Y., Tokumitsu, A., Takaya, A., Suzuki, M.et al. (2002) The ClpXP ATP-dependent protease regulates flagellum synthesis in Salmonella enterica    serovar    Typhimurium. J    Bacteriol 184:    645–653.
  • Wang, J., Hartling, J.A., and Flanagan, J.M. (1997) The structure of ClpP at 2.3A resolution suggests a model for ATP-dependent proteolysis. Cell91: 447–456.
  • Wawrzynow, A., Banecki, B., and Zylicz, M. (1996) The Clp ATPases define a novel class of molecular chaperones. Mol Microbiol21: 895–899.
    Direct Link:
  • Wickner, S., Maurizi, M.R., and Gottesman, S. (1999) Posttranslational quality control: folding, refolding, and degrading proteins. Science286: 1888–1893.
  • Wojtkowiak, D., Georgopoulos, C., and Zylicz, M. (1993) Isolation and characterization of ClpX, a new ATP-dependent specificity component of the Clp protease of Escherichia coli. J Biol Chem268: 22609–22617.
  • Yamamoto, T., Hanawa, T., Ogata, S., and Kamiya, S. (1996) Identification and characterization of the Yersinia enterocolitica gsrA gene, which protectively responds to intracellular stress induced by macrophage phagocytosis and to extracellular environmental stress. Infect Immun64: 2980–2987.
  • Yamamoto, T., Hanawa, T., Ogata, S., and Kamiya, S. (1997) The Yersinia enterocolitica GsrA stress protein, involved in intracellular survival, is induced by macrophage phagocytosis. Infect Immun65: 2190–2196.
  • Yamamoto, T., Sashinami, H., Takaya, A., Tomoyasu, T., Matsui, H., Hanawa, T.et al. (2001) Disruption of the genes for ClpXP protease in Salmonella enterica serovar Typhimurium results in a persistent infection in mouse and development of the persistence requires endogenous interferon gamma and tumour necrosis factor alpha. Infect Immun69: 3164–3174.
  • Yokota, T., and Gots, J.S. (1970) Requirement of adenosine 3′, 5′-cyclic phosphate for flagella formation in Escherichia coli and Salmonella typhimurium. J Bacteriol1303: 513–516.
  • Zhou, Y., Gottesman, S., Hoskins, J.R., Maurizi, M.R., and Wickner, S. (2001) The RssB response regulator directly targets sigma (s) for degradation by ClpXP. Genes Dev15: 627–637.
  • Zwickl, P., Baumeister, W., and Steven, A. (2000) Disassembly lines: the proteasome and related ATPase-assisted proteases. Curr Opin Struct Biol10: 242–250.
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