OmpR positively regulates urease expression to enhance acid survival of Yersinia pseudotuberculosis

Microbiology

Volumn 155, Issue 8, 2009, Pages 2522-2531

  Hu, Yangbo ^a,c   Lu, Pei ^a,c   Wang, Yao ^a   Ding, Lisha ^a,c   Atkinson, Steve ^b   Chen, Shiyun ^a  

^a WUHAN INSTITUTE OF VIROLOGY   (China)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; OUTER MEMBRANE PROTEIN REGULATOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR UREABC; TRANSCRIPTION FACTOR UREEF; TRANSCRIPTION FACTOR UREGD; UNCLASSIFIED DRUG; UREA; UREASE;

ARTICLE; BACTERIAL CELL; BACTERIAL MUTATION; BACTERIAL STRAIN; BACTERIAL SURVIVAL; CELL PH; CELL SURVIVAL; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME ACTIVATION; GEL MOBILITY SHIFT ASSAY; GENE CLUSTER; GENE EXPRESSION REGULATION; GENE FUNCTION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEOMICS; REPORTER GENE; YERSINIA PSEUDOTUBERCULOSIS;

ACIDS; BACTERIAL PROTEINS; DNA, BACTERIAL; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN-ION CONCENTRATION; MULTIGENE FAMILY; PROMOTER REGIONS, GENETIC; STRESS, PHYSIOLOGICAL; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC; UREASE; YERSINIA PSEUDOTUBERCULOSIS;

BACTERIA (MICROORGANISMS); YERSINIA PSEUDOTUBERCULOSIS;

EID: 69949123816     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.028381-0     Document Type: Article

References (53)

1. Akada, J. K., Shirai, M., Takeuchi, H., Tsuda, M. & Nakazawa, T. (2000). Identification of the urease operon in Helicobacter pylori and its control by mRNA decay in response to pH. Mol Microbiol 36, 1071-1084.
2. Allen, K. J., Lepp, D., McKellar, R. C. & Griffiths, M. W. (2008). Examination of stress and virulence gene expression in Escherichia coli O157:H7 using targeted microarray analysis. Foodborne Pathog Dis 5, 437-447.
3. Atkinson, S., Throup, J. P., Stewart, G. S. & Williams, P. (1999). A hierarchical quorum-sensing system in Yersinia pseudotuberculosis is involved in the regulation of motility and clumping. Mol Microbiol 33, 1267-1277.
4. Bandara, A. B., Contreras, A., Contreras-Rodriguez, A., Martins, A. M., Dobrean, V., Poff-Reichow, S., Rajasekaran, P., Sriranganathan, N., Schurig, G. G. & Boyle, S. M. (2007). Brucella suis urease encoded by ure1 but not ure2 is necessary for intestinal infection of BALB/c mice. BMC Microbiol 7, 57.
5. Bang, I. S., Kim, B. H., Foster, J. W. & Park, Y. K. (2000). OmpR regulates the stationary-phase acid tolerance response of Salmonella enterica serovar typhimurium. J Bacteriol 182, 2245-2252.
6. Bearson, S., Bearson, B. & Foster, J. W. (1997). Acid stress responses in enterobacteria. FEMS Microbiol Lett 147, 173-180.
7. Bearson, B. L., Wilson, L. & Foster, J. W. (1998). A low pH-inducible, PhoPQ-dependent acid tolerance response protects Salmonella typhimurium against inorganic acid stress. J Bacteriol 180, 2409-2417.
8. Berk, P. A., Jonge, R., Zwietering, M. H., Abee, T. & Kieboom, J. (2005). Acid resistance variability among isolates of Salmonella enterica serovar Typhimurium DT104. J Appl Microbiol 99, 859-866.
9. Blankenhorn, D., Phillips, J. & Slonczewski, J. L. (1999). Acid- and base-induced proteins during aerobic and anaerobic growth of Escherichia coli revealed by two-dimensional gel electrophoresis. J Bacteriol 181, 2209-2216.
10. Boot, I. R., Cash, P. & O'Byrne, C. (2002). Sensing and adapting to acid stress. Antonie Van Leeuwenhoek 81, 33-42.
11. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
12. Brzostek, K., Brzostkowska, M., Bukowska, I., Karwicka, E. & Raczkowska, A. (2007). OmpR negatively regulates expression of invasin in Yersinia enterocolitica. Microbiology 153, 2416-2425.
13. Castanie-Cornet, M. P., Penfound, T. A., Smith, D., Elliott, J. F. & Foster, J. W. (1999). Control of acid resistance in Escherichia coli. J Bacteriol 181, 3525-3535.
14. Castillo, A., Lucia, L. M., Goodson, K. J., Savell, J. W. & Acuff, G. R. (1999). Decontamination of beef carcass surface tissue by steam vacuuming alone and combined with hot water and lactic acid sprays. J Food Prot 62, 146-151.
15. Coker, C., Bakare, O. O. & Mobley, H. L. (2000). H-NS is a repressor of the Proteus mirabilis urease transcriptional activator gene ureR. J Bacteriol 182, 2649-2653.
16. Dattelbaum, J. D., Lockatell, C. V., Johnson, D. E. & Mobley, H. L. (2003). UreR, the transcriptional activator of the Proteus mirabilis urease gene cluster, is required for urease activity and virulence in experimental urinary tract infections. Infect Immun 71, 1026-1030.
17. De Koning-Ward, T. F. & Robins-Browne, R. M. (1995). Contribution of urease to acid tolerance in Yersinia enterocolitica. Infect Immun 63, 3790-3795.
18. De Koning-Ward, T. F., Ward, A. C. & Robins-Browne, R. M. (1994). Characterisation of the urease-encoding gene complex of Yersinia enterocolitica. Gene 145, 25-32.
19. Delany, I., Ieva, R., Soragni, A., Hilleringmann, M., Rappuoli, R. & Scarlato, V. (2005). In vitro analysis of protein-operator interactions of the NikR and Fur metal-responsive regulators of coregulated genes in Helicobacter pylori. J Bacteriol 187, 7703-7715.
20. Flamez, C., Ricard, I., Arafah, S., Simonet, M. & Marceau, M. (2008). Phenotypic analysis of Yersinia pseudotuberculosis 32777 response regulator mutants: new insights into two-component system regulon plasticity in bacteria. Int J Med Microbiol 298, 193-207.
21. Foster, J. W. (2004). Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Microbiol 2, 898-907.
22. Giannella, R. A., Broitman, S. A. & Zamcheck, N. (1972). Gastric acid barrier to ingested microorganisms in man: studies in vivo and in vitro. Gut 13, 251-256.
23. Grabenstein, J. P., Marceau, M., Pujol, C., Simonet, M. & Bliska, J. B. (2004). The response regulator PhoP of Yersinia pseudotuberculosis is important for replication in macrophages and for virulence. Infect Immun 72, 4973-4984.
24. Heuveling, J., Possling, A. & Hengge, R. (2008). A role for Lon protease in the control of the acid resistance genes of Escherichia coli. Mol Microbiol 69, 534-547.
25. Huang, Y. Y., Deng, J. Y., Gu, J., Zhang, Z. P., Maxwell, A., Bi, L. J., Chen, Y. Y., Zhou, Y. F., Yu, Z. N. & Zhang, X. E. (2006). The key DNA-binding residues in the C-terminal domain of Mycobacterium tuberculosis DNA gyrase A subunit (GyrA). Nucleic Acids Res 34, 5650-5659.
26. Karimova, G., Pidoux, J., Ullmann, A. & Ladant, D. (1998). A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci U S A 95, 5752-5756.
27. Lee, I. S., Slonczewski, J. L. & Foster, J. W. (1994). A low-pH-inducible, stationary-phase acid tolerance response in Salmonella typhimurium. J Bacteriol 176, 1422-1426.
28. Lee, Y. H., Kim, B. H., Kim, J. H., Yoon, W. S., Bang, S. H. & Park, Y. K. (2007). CadC has a global translational effect during acid adaptation in Salmonella enterica serovar Typhimurium. J Bacteriol 189, 2417-2425.
29. Lennox, E. S. (1955). Transduction of linked genetic characters of the host by bacteriophage P1. Virology 1, 190-206.
30. Leyer, G. J., Wang, L. L. & Johnson, E. A. (1995). Acid adaptation of Escherichia coli O157:H7 increases survival in acidic foods. Appl Environ Microbiol 61, 3752-3755.
31. Lin, J., Lee, I. S., Frey, J., Slonczewski, J. L. & Foster, J. W. (1995). Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri, and Escherichia coli. J Bacteriol 177, 4097-4104.
32. Maroncle, N., Rich, C. & Forestier, C. (2006). The role of Klebsiella pneumoniae urease in intestinal colonization and resistance to gastrointestinal stress. Res Microbiol 157, 184-193.
33. Marshall, B. J., Barrett, L. J., Prakash, C., McCallum, R. W. & Guerrant, R. L. (1990). Urea protects Helicobacter (Campylobacter) pylori from the bactericidal effect of acid. Gastroenterology 99, 697-702.
34. Masuda, N. & Church, G. M. (2003). Regulatory network of acid resistance genes in Escherichia coli. Mol Microbiol 48, 699-712.
35. Miller, J. H. (1992). A Short Course in Bacterial Genetics: a Laboratory Manual and Handbook for Escherichia coli and Related Bacteria. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
36. Mujacic, M. & Baneyx, F. (2007). Chaperone Hsp31 contributes to acid resistance in stationary-phase Escherichia coli. Appl Environ Microbiol 73, 1014-1018.
37. Nagano, T., Kiyohara, T., Suzuki, K., Tsubokura, M. & Otsuki, K. (1997). Identification of pathogenic strains within serogroups of Yersinia pseudotuberculosis and the presence of non-pathogenic strains isolated from animals and the environment. J Vet Med Sci 59, 153-158.
38. O'Toole, R., Milton, D. L. & Wolf-Watz, H. (1996). Chemotactic motility is required for invasion of the host by the fish pathogen Vibrio anguillarum. Mol Microbiol 19, 625-637.
39. Pflock, M., Kennard, S., Delany, I., Scarlato, V. & Beier, D. (2005). Acid-induced activation of the urease promoters is mediated directly by the ArsRS two-component system of Helicobacter pylori. Infect Immun 73, 6437-6445.
40. Pflock, M., Finsterer, N., Joseph, B., Mollenkopf, H., Meyer, T. F. & Beier, D. (2006a). Characterization of the ArsRS regulon of Helicobacter pylori, involved in acid adaptation. J Bacteriol 188, 3449-3462.
41. Pflock, M., Kennard, S., Finsterer, N. & Beier, D. (2006b). Acid-responsive gene regulation in the human pathogen Helicobacter pylori. J Biotechnol 126, 52-60.
42. Richard, H. T. & Foster, J. W. (2003). Acid resistance in Escherichia coli. Adv Appl Microbiol 52, 167-186.
43. Rose, R. E. (1988). The nucleotide sequence of pACYC184. Nucleic Acids Res 16, 355.
44. Rosqvist, R., Skurnik, M. & Wolf-Watz, H. (1988). Increased virulence of Yersinia pseudotuberculosis by two independent mutations. Nature 334, 522-524.
45. Ruiz, C., McMurry, L. M. & Levy, S. B. (2008). Role of the multidrug resistance regulator MarA in global regulation of the hdeAB acid resistance operon in Escherichia coli. J Bacteriol 190 , 1290-1297.
46. Sayed, A. K., Odom, C. & Foster, J. W. (2007). The Escherichia coli AraC-family regulators GadX and GadW activate gadE, the central activator of glutamate-dependent acid resistance. Microbiology 153, 2584-2592.
47. Simon, R., Priefer, U. & Pühler, A. (1983). A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Biotechnology 1, 784-791.
48. Stingl, K. & De Reuse, H. (2005). Staying alive overdosed: how does Helicobacter pylori control urease activity? Int J Med Microbiol 295, 307-315.
49. Takada, A., Umitsuki, G., Nagai, K. & Wachi, M. (2007). RNase E is required for induction of the glutamate-dependent acid resistance system in Escherichia coli. Biosci Biotechnol Biochem 71, 158-164.
50. Tramonti, A., De Canio, M., Delany, I., Scarlato, V. & De Biase, D. (2006). Mechanisms of transcription activation exerted by GadX and GadW at the gadA and gadBC gene promoters of the glutamate-based acid resistance system in Escherichia coli. J Bacteriol 188, 8118-8127.
51. Tucker, D. L., Tucker, N. & Conway, T. (2002). Gene expression profiling of the pH response in Escherichia coli. J Bacteriol 184, 6551-6558.
52. Yoshida, T., Qin, L., Egger, L. A. & Inouye, M. (2006). Transcription regulation of ompF and ompC by a single transcription factor, OmpR. J Biol Chem 281, 17114-17123.
53. Young, G. M., Amid, D. & Miller, V. L. (1996). A bifunctional urease enhances survival of pathogenic Yersinia enterocolitica and Morganella morganii at low pH. J Bacteriol 178, 6487-6495.