ZraP is a periplasmic molecular chaperone and a repressor of the zinc-responsive two-component regulator ZraSR

Biochemical Journal

Volumn 442, Issue 1, 2012, Pages 85-93

  Appia Ayme, Corinne ^a   Hall, Andrea ^a   Patrick, Elaine ^a   Rajadurai, Shiny ^a   Clarke, Thomas A ^a   Rowley, Gary ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

Chaperone; CpxP; Polymyxin B; Salmonella; Spy; ZraP

Indexed keywords

ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; CHAPERONE; CPXP PROTEIN; INDOLE; MALATE DEHYDROGENASE; OLIGOMER; PERIPLASMIC PROTEIN; POLYMYXIN B; SPY PROTEIN; UNCLASSIFIED DRUG; ZINC; ZRAP PROTEIN; ZRASR PROTEIN;

ARTICLE; BACTERIAL MEMBRANE; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; GENETIC TRANSCRIPTION; HOMEOSTASIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; SALMONELLA TYPHIMURIUM;

CRYSTALLOGRAPHY, X-RAY; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; INDOLES; MEMBRANE PROTEINS; MOLECULAR CHAPERONES; PERIPLASM; PERIPLASMIC PROTEINS; POLYMYXIN B; REPRESSOR PROTEINS; SALMONELLA TYPHIMURIUM; ZINC;

BACTERIA (MICROORGANISMS); ENTEROBACTERIACEAE; SALMONELLA; SALMONELLA TYPHIMURIUM;

EID: 84856303687     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20111639     Document Type: Article

References (33)

1. Rowley, G., Spector, M., Kormanec, J. and Roberts, M. (2006) Pushing the envelope: extracytoplasmic stress responses in bacterial pathogens. Nat. Rev. Microbiol. 4, 383-394 (Pubitemid 43771856)
2. Danese, P. N. and Silhavy, T. J. (1998) CpxP, a stress-combative member of the Cpx regulon. J. Bacteriol. 180, 831-839 (Pubitemid 28084207)
3. Raivio, T. L., Popkin, D. L. and Silhavy, T. J. (1999) The Cpx envelope stress response is controlled by amplification and feedback inhibition. J. Bacteriol. 181, 5263-5272 (Pubitemid 29416345)
4. Fleischer, R., Heermann, R., Jung, K. and Hunke, S. (2007) Purification, reconstitution, and characterization of the CpxRAP envelope stress system of Escherichia coli. J. Biol. Chem. 282, 8583-8593 (Pubitemid 47093505)
5. Buelow, D. R. and Raivio, T. L. (2005) Cpx signal transduction is influenced by a conserved N-terminal domain in the novel inhibitor CpxP and the periplasmic protease DegP. J. Bacteriol. 187, 6622-6630 (Pubitemid 41356234)
6. DiGiuseppe, P. A. and Silhavy, T. J. (2003) Signal detection and target gene induction by the CpxRA two-component system. J. Bacteriol. 185, 2432-2440 (Pubitemid 36417966)
7. Isaac, D. D., Pinkner, J. S., Hultgren, S. J. and Silhavy, T. J. (2005) The extracytoplasmic adaptor protein CpxP is degraded with substrate by DegP. Proc. Natl. Acad. Sci. U.S.A. 102, 17775-17779 (Pubitemid 41803573)
8. Raivio, T. L., Laird, M. W., Joly, J. C. and Silhavy, T. J. (2000) Tethering of CpxP to the inner membrane prevents spheroplast induction of the cpx envelope stress response. Mol. Microbiol. 37, 1186-1197
9. Thede, G. L., Arthur, D. C., Edwards, R. A., Buelow, D. R., Wong, J. L., Raivio, T. L. and Glover, J. N.M. (2011) Structure of the periplasmic stress response protein CpxP. J. Bacteriol. 193, 2149-2157
10. Zhou, X., Keller, R., Volkmer, R., Krauss, N., Scheerer, P. and Hunke, S. (2011) Structural basis for two-component system inhibition and pilus sensing by the auxiliary CpxP protein. J. Biol. Chem. 286, 9805-9814
11. Hagenmaier, S., Stierhof, Y. D. and Henning, U. (1997) A new periplasmic protein of Escherichia coli which is synthesized in spheroplasts but not in intact cells. J. Bacteriol. 179, 2073-2076 (Pubitemid 27123095)
12. Raffa, R. G. and Raivio, T. L. (2002) A third envelope stress signal transduction pathway in Escherichia coli. Mol. Microbiol. 45, 1599-1611 (Pubitemid 35231977)
13. Kwon, E., Kim, D. Y., Gross, C. A., Gross, J. D. and Kim, K. K. (2010) The crystal structure Escherichia coli Spy. Protein Sci. 19, 2252-2259
14. Quan, S., Koldewey, P., Tapley, T., Kirsch, N., Ruane, K. M., Pfizenmaier, J., Shi, R., Hofmann, S., Foit, L., Ren, G. et al. (2011) Genetic selection designed to stabilize proteins uncovers a chaperone called Spy. Nat. Struct. Mol. Biol. 18, 262-269
15. Noll, M., Petrukhin, K. and Lutsenko, S. (1998) Identification of a novel transcription regulator from Proteus mirabilis, PMTR, revealed a possible role of YJAI protein in balancing zinc in Escherichia coli. J. Biol. Chem. 273, 21393-21401 (Pubitemid 28385435)
16. Leonhartsberger, S., Huber, A., Lottspeich, F. and Böck, A. (2001) The hydH/G genes from Escherichia coli code for a zinc and lead responsive two-component regulatory system. J. Mol. Biol. 307, 93-105 (Pubitemid 33029968)
17. Appia-Ayme, C., Patrick, E., Sullivan, M. J., Alston, M. J., Field, S. J., Abuoun, M., Anjum, M. F. and Rowley, G. (2011) Novel inducers of the envelope stress response BaeSR in Salmonella Typhimurium: BaeR Is critically required for tungstate waste disposal. PLoS ONE 6, e23713
18. 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. U.S.A. 97, 6640-6645 (Pubitemid 30412767)
19. Gemski, Jr, P. and Stocker, B. A. (1967) Transduction by bacteriophage P22 in nonsmooth mutants of Salmonella Typhimurium. J. Bacteriol. 93, 1588-1597
20. Cherepanov, P. P. and Wackernagel, W. (1995) Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158, 9-14
21. Uzzau, S., Figueroa-Bossi, N., Rubino, S. and Bossi, L. (2001) Epitope tagging of chromosomal genes in Salmonella . Proc. Natl. Acad. Sci. U.S.A. 98, 15264-15269 (Pubitemid 34014003)
22. Tedin, K. and Blasi, U. (1996) The RNA chain elongation rate of the lambda late mRNA is unaffected by high levels of ppGpp in the absence of amino acid starvation. J. Biol. Chem. 271, 17675-17686 (Pubitemid 26250737)
23. Demeler, B. (2005) UltraScan - a comprehensive data analysis software package for analytical ultracentrifugation experiments. In Modern Analytical Ultracentrifugation: Techniques and Methods (Scott, D. J., Harding, S. E. and Rowe, A. J., eds), pp. 210-229, Royal Society of Chemistry, U.K.
24. Zhao, W., Xu, M., Liang, Z., Ding, B., Niu, L., Liu, H. and Teng, M. (2011) Structure-based de novo prediction of zinc-binding sites in proteins of unknown function. Bioinformatics 27, 1262-1268
25. Graham, A. I., Hunt, S., Stokes, S. L., Bramall, N., Bunch, J., Cox, A. G., Mcleod, C. W. and Poole, R. K. (2009) Severe zinc depletion of Escherichia coli: roles for high affinity zinc binding by ZinT, zinc transport and zinc-independent proteins. J. Biol. Chem. 284, 18377-18389
26. Bader, M. W., Navarre, W. W., Shiau, W., Nikaido, H., Frye, J. G., McClelland, M., Fang, F. C. and Miller, S. I. (2003) Regulation of Salmonella typhimurium virulence gene expression by cationic antimicrobial peptides. Mol. Microbiol. 50, 219-230 (Pubitemid 37222799)
27. Houry, W. A. (2001) Chaperone-assisted protein folding in the cell cytoplasm. Curr. Protein Pept. Sci. 2, 227-244
28. Merdanovic, M., Clausen, T., Kaiser, M., Huber, R. and Ehrmann, M. (2011) Protein quality control in the bacterial periplasm. Annu. Rev. Microbiol. 65, 149-168
29. Fardini, Y., Trotereau, J., Bottreau, E., Souchard, C., Velge, P. and Virlogeux-Payant, I. (2009) Investigation of the role of the BAM complex and SurA chaperone in outer-membrane protein biogenesis and type III secretion system expression in Salmonella . Microbiology 155, 1613-1622
30. Delaney, J. M. (1990) Requirement of the Escherichia coli dnaK gene for thermotolerance and protection against H2O2. J. Gen. Microbiol. 136, 2113-2118
31. Graham, A. I., Sanguinetti, G., Bramall, N., McLeod, C. W. and Poole, R. K. (2012) Dynamics of a starvation-to-surfeit shift: A transcriptomic and modelling analysis of the bacterial response to zinc reveals transient behaviour of the Fur and SoxS regulators. Microbiology, 158, 284-292
32. Huang, Y., Leming, C. L., Suyemoto, M. and Altier, C. (2007) Genome-wide screen of Salmonella genes expressed during infection in pigs, using in vivo expression technology. Appl. Environ. Microbiol. 73, 7522-7530
33. Hoiseth, S. K. and Stocker, B. A. (1981) Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291, 238-239 (Pubitemid 11081517)