Comparison of the RpoH-dependent regulon and general stress response in Neisseria gonorrhoeae

Journal of Bacteriology

Volumn 188, Issue 13, 2006, Pages 4769-4776

  Gunesekere, Ishara C ^a   Kahler, Charlene M ^a,c   Powell, David R ^a   Snyder, Lori A S ^b   Saunders, Nigel J ^b   Rood, Julian I ^a   Davies, John K ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN; HRCA PROTEIN; PROTEIN; REPRESSOR PROTEIN; RPOH PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BETAPROTEOBACTERIA; BINDING SITE; COMPARATIVE STUDY; GAMMAPROTEOBACTERIA; GENE CONTROL; GENE EXPRESSION; GENE OVEREXPRESSION; HOMEOSTASIS; NEISSERIA GONORRHOEAE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REGULON; RPOH GENE; SEQUENCE HOMOLOGY; STRESS; TRANSCRIPTION REGULATION;

GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HEAT; HEAT-SHOCK PROTEINS; NEISSERIA GONORRHOEAE; REGULON; SIGMA FACTOR;

BETAPROTEOBACTERIA; ESCHERICHIA COLI; GAMMAPROTEOBACTERIA; NEISSERIA GONORRHOEAE;

EID: 33745471736     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01807-05     Document Type: Article

References (50)

1. Arsene, F., T. Tomoyasu, and B. Bukau. 2000. The heat shock response of Escherichia coli. Int. J. Food Microbiol. 55:3-9.
2. Baccanari, D. P., R. L. Tansik, S. J. Paterson, and D. Stone. 1984. Characterization and amino acid sequence of Neisseria gonorrhoeae dihydrofolate reductase. J. Biol. Chem. 259:12291-12298.
3. Bernardini, G., G. Renzone, M. Comanducci, R. Mini, S. Arena, C. D'Ambrosio, S. Bambini, L. Trabalzini, G. Grandi, P. Martelli, M. Achtman, A. Scaloni, G. Ratti, and A. Santucci. 2004. Proteome analysis of Neisseria meningitidis serogroup A. Proteomics 4:2893-2926.
4. Black, C. G., J. A. Fyfe, and J. K. Davies. 1998. Absence of an SOS-like system in Neisseria gonorrhoeae. Gene 208:61-66.
5. Boyce, J. D., I. Wilkie, M. Harper, M. L. Paustian, V. Kapur, and B. Adler. 2002. Genomic scale analysis of Pasteurella multocida gene expression during growth within the natural chicken host. Infect. Immun. 70:6871-6879.
6. Chandu, D., and D. Nandi. 2004. Comparative genomics and functional roles of the ATP-dependent proteases Lon and Clp during cytosolic protein degradation. Res. Microbiol. 155:710-719.
7. Dempsey, J. A., W. Litaker, A. Madhure, T. L. Snodgrass, and J. G. Cannon. 1991. Physical map of the chromosome of Neisseria gonorrhoeae FA1090 with locations of genetic markers, including opa and pil genes. J. Bacteriol. 173:5476-5486.
8. Dougan, D. A., A. Mogk, and B. Bukau. 2002. Protein folding and degradation in bacteria: to degrade or not to degrade? That is the question. Cell. Mol. Life Sci. 59:1607-1616.
9. Dudoit, S., and Y. H. Yang. 2003. Bioconductor R packages for exploratory analysis and normalization of cDNA microarray data, p. 45-65. In G. Parmigiani, E. S. Garrett, R. A. Irizarry, and S. L. Zeger (ed.), The analysis of gene expression data: methods and software. Springer Verlag, New York, NY.
10. Fujita, N., and A. Ishihama. 1987. Heat-shock induction of RNA polymerase sigma-32 synthesis in Escherichia coli: transcriptional control and a multiple promoter system. Mol. Gen. Genet. 210:10-15.
11. Fyfe, J. A., C. S. Carrick, and J. K. Davies. 1995. The pilE gene of Neisseria gonorrhoeae MS11 is transcribed from a sigma 70 promoter during growth in vitro. J. Bacteriol. 177:3781-3787.
12. Gao, H., Y. Wang, X. Liu, T. Yan, L. Wu, E. Alm, A. Arkin, D. K. Thompson, and J. Zhou. 2004. Global transcriptome analysis of the heat shock response of Shewanella oneidensis. J. Bacteriol. 186:7796-7803.
13. Graf, P. C., and U. Jakob. 2002. Redox-regulated molecular chaperones. Cell. Mol. Life Sci. 59:1624-1631.
14. Guckenberger, M., S. Kurz, C. Aepinus, S. Theiss, S. Haller, T. Leimbach, U. Panzner, J. Weber, H. Paul, A. Unkmeir, M. Frosch, and G. Dietrich. 2002. Analysis of the heat shock response of Neisseria meningitidis with cDNA- and oligonucleotide-based DNA microarrays. J. Bacteriol. 184:2546-2551.
15. Guisbert, E., C. Herman, C. Z. Lu, and C. A. Gross. 2004. A chaperone network controls the heat shock response in E. coli. Genes Dev. 18:2812-2821.
16. Gunesekere, I. C., C. M. Kahler, C. S. Ryan, L. A. S. Snyder, N. J. Saunders, J. I. Rood, and J. K. Davies. Ecf, an alternative sigma factor from Neisseria gonorrhoeae, controls expression of msrAB, which encodes methionine sulfoxide reductase. J. Bacteriol., in press.
17. Gutierrez, C., and J. C. Devedjian. 1991. Osmotic induction of gene osmC expression in Escherichia coli K12. J. Mol. Biol. 220:959-973.
18. Hager, J., B. L. Staker, and U. Jakob. 2004. Substrate binding analysis of the 23S rRNA methyltransferase RrmJ. J. Bacteriol. 186:6634-6642.
19. Hamilton, H. L., N. M. Dominguez, K. J. Schwartz, K. T. Hackett, and J. P. Dillard. 2005. Neisseria gonorrhoeae secretes chromosomal DNA via a novel type IV secretion system. Mol. Microbiol. 55:1704-1721.
20. Helmann, J. D., M. F. Wu, P. A. Kobel, F. J. Gamo, M. Wilson, M. M. Morshedi, M. Navre, and C. Paddon. 2001. Global transcriptional response of Bacillus subtilis to heat shock. J. Bacteriol. 183:7318-7328.
21. Herman, C., D. Thevenet, R. D'Ari, and P. Bouloc. 1995. Degradation of sigma 32, the heat shock regulator in Escherichia coli, is governed by HflB. Proc. Natl. Acad. Sci. USA 92:3516-3520.
22. Huang, L. H., Y. H. Tseng, and M. T. Yang. 1998. Isolation and characterization of the Xanthomonas campestris rpoH gene coding for a 32-kDa heat shock sigma factor. Biochem. Biophys. Res. Commun. 244:854-860.
23. Kupsch, E. M., D. Aubel, C. P. Gibbs, A. F. Kahrs, T. Rudel, and T. F. Meyer. 1996. Construction of Hermes shuttle vectors: a versatile system useful for genetic complementation of transformable and non-transformable Neisseria mutants. Mol. Gen. Genet. 250:558-569.
24. Laskos, L., C. S. Ryan, J. A. Fyfe, and J. K. Davies. 2004. The RpoH-mediated stress response in Neisseria gonorrhoeae is regulated at the level of activity. J. Bacteriol. 186:8443-8452.
25. Lee, E. H., C. Rouquette-Loughlin, J. P. Folster, and W. M. Shafer. 2003. FarR regulates the farAB-encoded efflux pump of Neisseria gonorrhoeae via an MtrR regulatory mechanism. J. Bacteriol. 185:7145-7152.
26. Motohashi, K., Y. Watanabe, M. Yohda, and M. Yoshida. 1999. Heat-inactivated proteins are rescued by the DnaK.J-GrpE set and ClpB chaperones. Proc. Natl. Acad. Sci. USA 96:7184-7189.
27. 32 homolog (RpoH) and an HrcA repressor in the heat shock response of Agrobacterium tumefaciens. J. Bacteriol. 181:7509-7515.
28. Parkhill, J., M. Achtman, K. D. James, S. D. Bentley, C. Churcher, S. R. Klee, G. Morelli, D. Basham, D. Brown, T. Chillingworth, R. M. Davies, P. Davis, K. Devlin, T. Feltwell, N. Hamlin, S. Holroyd, K. Jagels, S. Leather, S. Moule, K. Mungall, M. A. Quail, M. A. Rajandream, K. M. Rutherford, M. Simmonds, J. Skelton, S. Whitehead, B. G. Spratt, and B. G. Barrell. 2000. Complete DNA sequence of a serogroup A strain of Neisseria meningitidis Z2491. Nature 404:502-506.
29. Permina, E. A., and M. S. Gelfand. 2003. Heat shock (sigma32 and HrcA/CIRCE) regulons in beta-, gamma- and epsilon-proteobacteria. J. Mol. Microbiol. Biotechnol. 6:174-181.
30. Randall, L. L., and S. J. Hardy. 2002. SecB, one small chaperone in the complex milieu of the cell. Cell. Mol. Life Sci. 59:1617-1623.
31. Richmond, C. S., J. E. Glasner, R. Mau, H. Jin, and F. R. Blattner. 1999. Genome-wide expression profiling in Escherichia coli K-12. Nucleic Acids Res. 27:3821-3835.
32. Rosen, R., and E. Z. Ron. 2002. Proteome analysis in the study of the bacterial heat-shock response. Mass Spectrom. Rev. 21:244-265.
33. Saal, L. H., C. Troein, J. Vallon-Christersson, S. Gruvberger, A. Borg, and C. Peterson. 2002. BioArray Software Environment (BASE): a platform for comprehensive management and analysis of microarray data. Genome Biol. 3:SOFTWARE0003.
34. Schneider, T. D., and R. M. Stephens. 1990. Sequence logos: a new way to display consensus sequences. Nucleic Acids Res. 18:6097-6100.
35. Schurr, M. J., and V. Deretic. 1997. Microbial pathogenesis in cystic fibrosis: co-ordinate regulation of heat-shock response and conversion to mucoidy in Pseudomonas aeruginosa. Mol. Microbiol. 24:411-420.
36. Segal, E., E. Billyard, M. So, S. Storzbach, and T. F. Meyer. 1985. Role of chromosomal rearrangement in N. gonorrhoeae pilus phase variation. Cell 40:293-300.
37. Segal, G., and E. Z. Ron. 1995. The dnaKJ operon of Agrobacterium tumefaciens: transcriptional analysis and evidence for a new heat shock promoter. J. Bacteriol. 177:5952-5958.
38. Smoot, L. M., J. C. Smoot, M. R. Graham, G. A. Somerville, D. E. Sturdevant, C. A. Migliaccio, G. L. Sylva, and J. M. Musser. 2001. Global differential gene expression in response to growth temperature alteration in group A Streptococcus. Proc. Natl. Acad. Sci. USA 98:10416-10421.
39. Smyth, G. K. 2004. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Applic. Genet. Mol. Biol. 3:article 3. [On line.] http://www.bepress.com/sagmb/vol3/ iss1/art3.
40. Smyth, G. K., J. Michaud, and H. S. Scott. 2005. Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 21:2067-2075.
41. Stintzi, A. 2003. Gene expression profile of Campylobacter jejuni in response to growth temperature variation. J. Bacteriol. 185:2009-2016.
42. Stohl, E. A., A. K. Criss, and H. S. Seifert. 2005. The transcriptome response of Neisseria gonorrhoeae to hydrogen peroxide reveals genes with previously uncharacterized roles in oxidative damage protection. Mol. Microbiol. 58:520-532.
43. Tauschek, M., C. W. Hamilton, L. A. Hall, C. Chomvarin, J. A. Fyfe, and J. K. Davies. 1997. Transcriptional analysis of the groESL operon of Neisseria gonorrhoeae. Gene 189:107-112.
44. Tettelin, H., N. J. Saunders, J. Heidelberg, A. C. Jeffries, K. E. Nelson, J. A. Eisen, K. A. Ketchum, D. W. Hood, J. F. Peden, R. J. Dodson, W. C. Nelson, M. L. Gwinn, R. DeBoy, J. D. Peterson, E. K. Hickey, D. H. Haft, S. L. Salzberg, O. White, R. D. Fleischmann, B. A. Dougherty, T. Mason, A. Ciecko, D. S. Parksey, E. Blair, H. Cittone, E. B. Clark, M. D. Cotton, T. R. Utterback, H. Khouri, H. Qin, J. Vamathevan, J. Gill, V. Scarlato, V. Masignani, M. Pizza, G. Grandi, L. Sun, H. O. Smith, C. M. Fraser, E. R. Moxon, R. Rappuoli, and J. C. Venter. 2000. Complete genome sequence of Neisseria meningitidis serogroup B strain MC58. Science 287:1809-1815.
45. Ullers, R. S., J. Luirink, N. Harms, F. Schwager, C. Georgopoulos, and P. Genevaux. 2004. SecB is a bona fide generalized chaperone in Escherichia coli. Proc. Natl. Acad. Sci. USA 101:7583-7588.
46. Wang, Q. P., and J. M. Kaguni. 1989. A novel sigma factor is involved in expression of the rpoH gene of Escherichia coli. J. Bacteriol. 171:4248-4253.
47. Yuzawa, H., H. Nagai, H. Mori, and T. Yura. 1993. Heat induction of sigma 32 synthesis mediated by mRNA secondary structure: a primary step of the heat shock response in Escherichia coli. Nucleic Acids Res. 21:5449-5455.
48. Zhao, K., M. Liu, and R. R. Burgess. 2005. The global transcriptional response of Escherichia coli to induced sigma32 protein involves sigma32 regulon activation followed by inactivation and degradation of sigma32 in vivo. J. Biol. Chem. 280:17758-17768.
49. Zhou, Y. N., N. Kusukawa, J. W. Erickson, C. A. Gross, and T. Yura. 1988. Isolation and characterization of Escherichia coli mutants that lack the heat shock sigma factor sigma 32. J. Bacteriol. 170:3640-3649.
50. Zolklewski, M. 1999. ClpB cooperates with DnaK, DnaJ, and GrpE in suppressing protein aggregation. A novel multichaperone system from Escherichia coli. J. Biol. Chem. 274:28083-28086.