Molecular characterization of transcriptional regulation of rovA by phoP and rovA in Yersinia pestis

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Zhang, Yiquan ^a   Gao, He ^a,b   Wang, Li ^a   Xiao, Xiao ^a   Tan, Yafang ^a   Guo, Zhaobiao ^a   Zhou, Dongsheng ^a   Yang, Ruifu ^a  

^a BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^b CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL RNA; MAGNESIUM; PHOP PROTEIN; PROTEIN ROVA; UNCLASSIFIED DRUG; PHOP PROTEIN, BACTERIA; ROVA PROTEIN, YERSINIA; TRANSCRIPTION FACTOR;

ARTICLE; AUTOREGULATION; BACTERIAL GENE; BINDING AFFINITY; CONTROLLED STUDY; DNA FOOTPRINTING; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; GENE MUTATION; GENETIC ASSOCIATION; GENETIC COMPLEMENTATION; GENETIC PROCEDURES; GROWTH CURVE; LACZ FUSION ASSAY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIMER EXTENSION ASSAY; PROMOTER REGION; PROTEIN DNA INTERACTION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; ROVA GENE; TEMPERATURE SENSITIVITY; TRANSCRIPTION REGULATION; YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN BINDING; REAL TIME POLYMERASE CHAIN REACTION; REGULON;

YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS;

BACTERIAL PROTEINS; DNA FOOTPRINTING; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC COMPLEMENTATION TEST; PROTEIN BINDING; REAL-TIME POLYMERASE CHAIN REACTION; REGULON; TRANSCRIPTION FACTORS; YERSINIA PESTIS;

EID: 80053146816     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025484     Document Type: Article

References (47)

1. Perry RD, Fetherston JD, (1997) Yersinia pestis-etiologic agent of plague. Clin Microbiol Rev 10: 35-66.
2. Groisman EA, (2001) The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 183: 1835-1842.
3. Lukaszewski RA, Kenny DJ, Taylor R, Rees DG, Hartley MG, et al. (2005) Pathogenesis of Yersinia pestis infection in BALB/c mice: effects on host macrophages and neutrophils. Infect Immun 73: 7142-7150.
4. Oyston PC, Dorrell N, Williams K, Li SR, Green M, et al. (2000) The response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis. Infect Immun 68: 3419-3425.
5. Hitchen PG, Prior JL, Oyston PC, Panico M, Wren BW, et al. (2002) Structural characterization of lipo-oligosaccharide (LOS) from Yersinia pestis: regulation of LOS structure by the PhoPQ system. Mol Microbiol 44: 1637-1650.
6. O'Loughlin JL, Spinner JL, Minnich SA, Kobayashi SD, (2010) Yersinia pestis two-component gene regulatory systems promote survival in human neutrophils. Infect Immun 78: 773-782.
7. Li YL, Gao H, Qin L, Li B, Han YP, et al. (2008) Identification and characterization of PhoP regulon members in Yersinia pestis biovar Microtus. BMC Genomics 9: 143.
8. Perez JC, Shin D, Zwir I, Latifi T, Hadley TJ, et al. (2009) Evolution of a bacterial regulon controlling virulence and Mg(2+) homeostasis. PLoS Genet 5: e1000428.
9. Perez JC, Groisman EA, (2009) Transcription factor function and promoter architecture govern the evolution of bacterial regulons. Proc Natl Acad Sci U S A 106: 4319-4324.
10. Grabenstein JP, Fukuto HS, Palmer LE, Bliska JB, (2006) Characterization of phagosome trafficking and identification of PhoP-regulated genes important for survival of Yersinia pestis in macrophages. Infection and immunity 74: 3727-3741.
11. Ellison DW, Miller VL, (2006) Regulation of virulence by members of the MarR/SlyA family. Curr Opin Microbiol 9: 153-159.
12. Cathelyn JS, Crosby SD, Lathem WW, Goldman WE, Miller VL, (2006) RovA, a global regulator of Yersinia pestis, specifically required for bubonic plague. Proc Natl Acad Sci U S A 103: 13514-13519.
13. Dube PH, Handley SA, Revell PA, Miller VL, (2003) The rovA mutant of Yersinia enterocolitica displays differential degrees of virulence depending on the route of infection. Infect Immun 71: 3512-3520.
14. Nagel G, Lahrz A, Dersch P, (2001) Environmental control of invasin expression in Yersinia pseudotuberculosis is mediated by regulation of RovA, a transcriptional activator of the SlyA/Hor family. Molecular microbiology 41: 1249-1269.
15. Revell PA, Miller VL, (2000) A chromosomally encoded regulator is required for expression of the Yersinia enterocolitica inv gene and for virulence. Molecular microbiology 35: 677-685.
16. Ellison DW, Lawrenz MB, Miller VL, (2004) Invasin and beyond: regulation of Yersinia virulence by RovA. Trends in microbiology 12: 296-300.
17. Heroven AK, Nagel G, Tran HJ, Parr S, Dersch P, (2004) RovA is autoregulated and antagonizes H-NS-mediated silencing of invasin and rovA expression in Yersinia pseudotuberculosis. Molecular microbiology 53: 871-888.
18. Simonet M, Riot B, Fortineau N, Berche P, (1996) Invasin production by Yersinia pestis is abolished by insertion of an IS200-like element within the inv gene. Infect Immun 64: 375-379.
19. Huang XZ, Lindler LE, (2004) The pH 6 antigen is an antiphagocytic factor produced by Yersinia pestis independent of Yersinia outer proteins and capsule antigen. Infect Immun 72: 7212-7219.
20. Derbise A, Chenal-Francisque V, Pouillot F, Fayolle C, Prevost MC, et al. (2007) A horizontally acquired filamentous phage contributes to the pathogenicity of the plague bacillus. Mol Microbiol 63: 1145-1157.
21. Li Y, Dai E, Cui Y, Li M, Zhang Y, et al. (2008) Different region analysis for genotyping Yersinia pestis isolates from China. PLoS ONE 3: e2166.
22. Yang F, Ke Y, Tan Y, Bi Y, Shi Q, et al. (2010) Cell membrane is impaired, accompanied by enhanced type III secretion system expression in Yersinia pestis deficient in RovA regulator. PLoS One 5.e12840.
23. Tran HJ, Heroven AK, Winkler L, Spreter T, Beatrix B, et al. (2005) Analysis of RovA, a transcriptional regulator of Yersinia pseudotuberculosis virulence that acts through antirepression and direct transcriptional activation. J Biol Chem 280: 42423-42432.
24. Zhou D, Tong Z, Song Y, Han Y, Pei D, et al. (2004) Genetics of metabolic variations between Yersinia pestis biovars and the proposal of a new biovar, microtus. J Bacteriol 186: 5147-5152.
25. Zhan L, Han Y, Yang L, Geng J, Li Y, et al. (2008) The cyclic AMP receptor protein, CRP, is required for both virulence and expression of the minimal CRP regulon in Yersinia pestis biovar microtus. Infect Immun 76: 5028-5037.
26. Straley SC, Bowmer WS, (1986) Virulence genes regulated at the transcriptional level by Ca2+ in Yersinia pestis include structural genes for outer membrane proteins. Infect Immun 51: 445-454.
27. El-Robh MS, Busby SJ, (2002) The Escherichia coli cAMP receptor protein bound at a single target can activate transcription initiation at divergent promoters: a systematic study that exploits new promoter probe plasmids. Biochem J 368: 835-843.
28. Chain PS, Carniel E, Larimer FW, Lamerdin J, Stoutland PO, et al. (2004) Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proc Natl Acad Sci U S A 101: 13826-13831.
29. Zhou D, Han Y, Qin L, Chen Z, Qiu J, et al. (2005) Transcriptome analysis of the Mg2+-responsive PhoP regulator in Yersinia pestis. FEMS Microbiol Lett 250: 85-95.
30. Chen PE, Cook C, Stewart AC, Nagarajan N, Sommer DD, et al. (2010) Genomic characterization of the Yersinia genus. Genome Biol 11: R1.
31. Achtman M, Zurth K, Morelli G, Torrea G, Guiyoule A, et al. (1999) Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc Natl Acad Sci U S A 96: 14043-14048.
32. Skurnik M, Peippo A, Ervela E, (2000) Characterization of the O-antigen gene clusters of Yersinia pseudotuberculosis and the cryptic O-antigen gene cluster of Yersinia pestis shows that the plague bacillus is most closely related to and has evolved from Y. pseudotuberculosis serotype O:1b. Mol Microbiol 37: 316-330.
33. Lawrenz MB, Miller VL, (2007) Comparative analysis of the regulation of rovA from the pathogenic yersiniae. J Bacteriol 189: 5963-5975.
34. Herbst K, Bujara M, Heroven AK, Opitz W, Weichert M, et al. (2009) Intrinsic thermal sensing controls proteolysis of Yersinia virulence regulator RovA. PLoS Pathog 5: e1000435.
35. Stoebel DM, Free A, Dorman CJ, (2008) Anti-silencing: overcoming H-NS-mediated repression of transcription in Gram-negative enteric bacteria. Microbiology 154: 2533-2545.
36. Heroven AK, Dersch P, (2006) RovM, a novel LysR-type regulator of the virulence activator gene rovA, controls cell invasion, virulence and motility of Yersinia pseudotuberculosis. Mol Microbiol 62: 1469-1483.
37. Ishihama A, (2000) Functional modulation of Escherichia coli RNA polymerase. Annu Rev Microbiol 54: 499-518.
38. Heroven AK, Bohme K, Rohde M, Dersch P, (2008) A Csr-type regulatory system, including small non-coding RNAs, regulates the global virulence regulator RovA of Yersinia pseudotuberculosis through RovM. Mol Microbiol 68: 1179-1195.
39. Gao H, Zhou D, Li Y, Guo Z, Han Y, et al. (2008) The iron-responsive Fur regulon in Yersinia pestis. J Bacteriol 190: 3063-3075.
40. Li Y, Qiu Y, Gao H, Guo Z, Han Y, et al. (2009) Characterization of Zur-dependent genes and direct Zur targets in Yersinia pestis. BMC Microbiol 9: 128.
41. Cathelyn JS, Ellison DW, Hinchliffe SJ, Wren BW, Miller VL, (2007) The RovA regulons of Yersinia enterocolitica and Yersinia pestis are distinct: evidence that many RovA-regulated genes were acquired more recently than the core genome. Mol Microbiol 66: 189-205.
42. Song H, Kong W, Weatherspoon N, Qin G, Tyler W, et al. (2008) Modulation of the regulatory activity of bacterial two-component systems by SlyA. J Biol Chem 283: 28158-28168.
43. Norte VA, Stapleton MR, Green J, (2003) PhoP-responsive expression of the Salmonella enterica serovar typhimurium slyA gene. Journal of bacteriology 185: 3508-3514.
44. Shi Y, Latifi T, Cromie MJ, Groisman EA, (2004) Transcriptional control of the antimicrobial peptide resistance ugtL gene by the Salmonella PhoP and SlyA regulatory proteins. The Journal of biological chemistry 279: 38618-38625.
45. Kong W, Weatherspoon N, Shi Y, (2008) Molecular mechanism for establishment of signal-dependent regulation in the PhoP/PhoQ system. J Biol Chem 283: 16612-16621.
46. Soncini FC, Vescovi EG, Groisman EA, (1995) Transcriptional autoregulation of the Salmonella typhimurium phoPQ operon. J Bacteriol 177: 4364-4371.
47. Lejona S, Aguirre A, Cabeza ML, Garcia Vescovi E, Soncini FC, (2003) Molecular characterization of the Mg2+-responsive PhoP-PhoQ regulon in Salmonella enterica. J Bacteriol 185: 6287-6294.