Phosphorylated CpxR restricts production of the rova global regulator in Yersinia pseudotuberculosis

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Liu, Junfa ^a,b   Obi, Ikenna R ^a   Thanikkal, Edvin J ^a   Kieselbach, Thomas ^a   Francis, Matthew S ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CPXR PROTEIN; INVASIN; ROVA PROTEIN; UNCLASSIFIED DRUG; ADHESIN; ASPARTIC ACID; BACTERIAL DNA; CPXR PROTEIN, BACTERIA; CUTF PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; INVASIN, YERSINIA; LIPOPROTEIN; OUTER MEMBRANE PROTEIN; ROVA PROTEIN, YERSINIA; TRANSCRIPTION FACTOR;

ARTICLE; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BINDING SITE; BIOACCUMULATION; CONTROLLED STUDY; CYTOPLASM; GENE EXPRESSION REGULATION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; NUCLEASE PROTECTION ASSAY; POLYMERASE CHAIN REACTION; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN PHOSPHORYLATION; SITE DIRECTED MUTAGENESIS; TRANSCRIPTION REGULATION; YERSINIA PSEUDOTUBERCULOSIS; ACETYLATION; ALLELE; AMINO ACID SEQUENCE; BACTERIAL GENE; BIOSYNTHESIS; CHEMISTRY; DNA FOOTPRINTING; ELECTROSPRAY MASS SPECTROMETRY; GENETICS; METABOLISM; MOLECULAR GENETICS; MOLECULAR WEIGHT; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHOSPHORYLATION; PROTEIN BINDING; VIRULENCE;

YERSINIA; YERSINIA PSEUDOTUBERCULOSIS;

ACETYLATION; ADHESINS, BACTERIAL; ALLELES; AMINO ACID SEQUENCE; ASPARTIC ACID; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; BASE SEQUENCE; BINDING SITES; CYTOPLASM; DNA FOOTPRINTING; DNA, BACTERIAL; ESCHERICHIA COLI PROTEINS; GENES, BACTERIAL; LIPOPROTEINS; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TRANSCRIPTION FACTORS; VIRULENCE; YERSINIA PSEUDOTUBERCULOSIS;

EID: 80051831266     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023314     Document Type: Article

References (78)

1. Macritchie DM, Raivio TL, (2009) Envelope stress responses. In: Böck A, Curtiss R, Kaper JB, Karp PD, Neidhardt FC, editors. EcoSal-Escherichia coli and Salmonella: Cellular and Molecular Biology, http://wwwecosalorg Washington, DC. ASM Press.
2. Bury-Mone S, Nomane Y, Reymond N, Barbet R, Jacquet E, et al. (2009) Global analysis of extracytoplasmic stress signaling in Escherichia coli. PLoS Genet 5: e1000651.
3. Price NL, Raivio TL, (2009) Characterization of the Cpx regulon in Escherichia coli strain MC4100. J Bacteriol 191: 1798-1815.
4. De Wulf P, McGuire AM, Liu X, Lin EC, (2002) Genome-wide profiling of promoter recognition by the two-component response regulator CpxR-P in Escherichia coli. J Biol Chem 277: 26652-26661.
5. Raivio TL, Silhavy TJ, (1997) Transduction of envelope stress in Escherichia coli by the Cpx two-component system. J Bacteriol 179: 7724-7733.
6. Raivio TL, Popkin DL, Silhavy TJ, (1999) The Cpx envelope stress response is controlled by amplification and feedback inhibition. J Bacteriol 181: 5263-5272.
7. Isaac DD, Pinkner JS, Hultgren SJ, Silhavy TJ, (2005) The extracytoplasmic adaptor protein CpxP is degraded with substrate by DegP. Proc Natl Acad Sci U S A 102: 17775-17779.
8. Buelow DR, Raivio TL, (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.
9. Volz K, (1993) Structural conservation in the CheY superfamily. Biochemistry 32: 11741-11753.
10. Pogliano J, Dong JM, De Wulf P, Furlong D, Boyd D, et al. (1998) Aberrant cell division and random FtsZ ring positioning in Escherichia coli cpxA* mutants. J Bacteriol 180: 3486-3490.
11. De Wulf P, Lin EC, (2000) Cpx two-component signal transduction in Escherichia coli: excessive CpxR-P levels underlie CpxA* phenotypes. J Bacteriol 182: 1423-1426.
12. De Wulf P, Kwon O, Lin EC, (1999) The CpxRA signal transduction system of Escherichia coli: growth-related autoactivation and control of unanticipated target operons. J Bacteriol 181: 6772-6778.
13. Danese PN, Snyder WB, Cosma CL, Davis LJ, Silhavy TJ, (1995) The Cpx two-component signal transduction pathway of Escherichia coli regulates transcription of the gene specifying the stress-inducible periplasmic protease, DegP. Genes Dev 9: 387-398.
14. Cosma CL, Danese PN, Carlson JH, Silhavy TJ, Snyder WB, (1995) Mutational activation of the Cpx signal transduction pathway of Escherichia coli suppresses the toxicity conferred by certain envelope-associated stresses. Mol Microbiol 18: 491-505.
15. Danese PN, Silhavy TJ, (1998) CpxP, a stress-combative member of the Cpx regulon. J Bacteriol 180: 831-839.
16. Danese PN, Murphy CK, Silhavy TJ, (1995) Multicopy suppression of cold-sensitive sec mutations in Escherichia coli. J Bacteriol 177: 4969-4973.
17. Pogliano J, Lynch AS, Belin D, Lin EC, Beckwith J, (1997) Regulation of Escherichia coli cell envelope proteins involved in protein folding and degradation by the Cpx two-component system. Genes Dev 11: 1169-1182.
18. Wolfe AJ, Parikh N, Lima BP, Zemaitaitis B, (2008) Signal integration by the two-component signal transduction response regulator CpxR. J Bacteriol 190: 2314-2322.
19. Carlsson KE, Liu J, Edqvist PJ, Francis MS, (2007) Extracytoplasmic-stress-responsive pathways modulate type III secretion in Yersinia pseudotuberculosis. Infect Immun 75: 3913-3924.
20. Carlsson KE, Liu J, Edqvist PJ, Francis MS, (2007) Influence of the Cpx Extracytoplasmic-stress-responsive pathway on Yersinia sp.-eukaryotic cell contact. Infect Immun 75: 4386-4399.
21. Naktin J, Beavis KG, (1999) Yersinia enterocolitica and Yersinia pseudotuberculosis. Clin Lab Med 19: 523-536, vi.
22. 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. Mol Microbiol 41: 1249-1269.
23. Revell PA, Miller VL, (2000) A chromosomally encoded regulator is required for expression of the Yersinia enterocolitica inv gene and for virulence. Mol Microbiol 35: 677-685.
24. 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.
25. 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.
26. 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.
27. Bölin I, Wolf-Watz H, (1984) Molecular cloning of the temperature-inducible outer membrane protein 1 of Yersinia pseudotuberculosis. Infect Immun 43: 72-78.
28. Grabenstein JP, Marceau M, Pujol C, Simonet M, Bliska JB, (2004) The response regulator PhoP of Yersinia pseudotuberculosis is important for replication in macrophages and for virulence. Infect Immun 72: 4973-4984.
29. Francis MS, Wolf-Watz H, (1998) YopD of Yersinia pseudotuberculosis is translocated into the cytosol of HeLa epithelial cells: evidence of a structural domain necessary for translocation. Mol Microbiol 29: 799-813.
30. Guzman LM, Belin D, Carson MJ, Beckwith J, (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121-4130.
31. Kinoshita E, Kinoshita-Kikuta E, Takiyama K, Koike T, (2006) Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol Cell Proteomics 5: 749-757.
32. Barbieri CM, Stock AM, (2008) Universally applicable methods for monitoring response regulator aspartate phosphorylation both in vitro and in vivo using Phos-tag-based reagents. Anal Biochem 376: 73-82.
33. Purich DL, (2002) Use of sodium borohydride to detect acyl-phosphate linkages in enzyme reactions. Methods Enzymol 354: 168-177.
34. Head CG, Tardy A, Kenney LJ, (1998) Relative binding affinities of OmpR and OmpR-phosphate at the ompF and ompC regulatory sites. J Mol Biol 281: 857-870.
35. Kussmann M, Lassing U, Sturmer CA, Przybylski M, Roepstorff P, (1997) Matrix-assisted laser desorption/ionization mass spectrometric peptide mapping of the neural cell adhesion protein neurolin purified by sodium dodecyl sulfate polyacrylamide gel electrophoresis or acidic precipitation. J Mass Spectrom 32: 483-493.
36. Rappsilber J, Ishihama Y, Mann M, (2003) Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal Chem 75: 663-670.
37. Jensen SS, Larsen MR, (2007) Evaluation of the impact of some experimental procedures on different phosphopeptide enrichment techniques. Rapid Commun Mass Spectrom 21: 3635-3645.
38. Thingholm TE, Jorgensen TJ, Jensen ON, Larsen MR, (2006) Highly selective enrichment of phosphorylated peptides using titanium dioxide. Nat Protoc 1: 1929-1935.
39. Larsen MR, Thingholm TE, Jensen ON, Roepstorff P, Jorgensen TJ, (2005) Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol Cell Proteomics 4: 873-886.
40. Dodd IB, Egan JB, (1990) Improved detection of helix-turn-helix DNA-binding motifs in protein sequences. Nucleic Acids Res 18: 5019-5026.
41. Galperin MY, (2010) Diversity of structure and function of response regulator output domains. Curr Opin Microbiol 13: 150-159.
42. Yamamoto K, Ishihama A, (2006) Characterization of copper-inducible promoters regulated by CpxA/CpxR in Escherichia coli. Biosci Biotechnol Biochem 70: 1688-1695.
43. Yang Y, Isberg RR, (1997) Transcriptional regulation of the Yersinia pseudotuberculosis pH6 antigen adhesin by two envelope-associated components. Mol Microbiol 24: 499-510.
44. Jubelin G, Vianney A, Beloin C, Ghigo JM, Lazzaroni JC, et al. (2005) CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli. J Bacteriol 187: 2038-2049.
45. 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. Mol Microbiol 53: 871-888.
46. Wolfe AJ, (2005) The acetate switch. Microbiol Mol Biol Rev 69: 12-50.
47. McCleary WR, Stock JB, (1994) Acetyl phosphate and the activation of two-component response regulators. J Biol Chem 269: 31567-31572.
48. Wolfe AJ, Chang DE, Walker JD, Seitz-Partridge JE, Vidaurri MD, et al. (2003) Evidence that acetyl phosphate functions as a global signal during biofilm development. Mol Microbiol 48: 977-988.
49. Mizrahi I, Biran D, Ron EZ, (2006) Requirement for the acetyl phosphate pathway in Escherichia coli ATP-dependent proteolysis. Mol Microbiol 62: 201-211.
50. Snyder WB, Davis LJ, Danese PN, Cosma CL, Silhavy TJ, (1995) Overproduction of NlpE, a new outer membrane lipoprotein, suppresses the toxicity of periplasmic LacZ by activation of the Cpx signal transduction pathway. J Bacteriol 177: 4216-4223.
51. Suntharalingam P, Spencer H, Gallant CV, Martin NL, (2003) Salmonella enterica serovar typhimurium rdoA is growth phase regulated and involved in relaying Cpx-induced signals. J Bacteriol 185: 432-443.
52. Makino K, Amemura M, Kawamoto T, Kimura S, Shinagawa H, et al. (1996) DNA binding of PhoB and its interaction with RNA polymerase. J Mol Biol 259: 15-26.
53. Makino K, Amemura M, Kim SK, Nakata A, Shinagawa H, (1993) Role of the sigma 70 subunit of RNA polymerase in transcriptional activation by activator protein PhoB in Escherichia coli. Genes Dev 7: 149-160.
54. Ramani N, Huang L, Freundlich M, (1992) In vitro interactions of integration host factor with the ompF promoter-regulatory region of Escherichia coli. Mol Gen Genet 231: 248-255.
55. Slauch JM, Silhavy TJ, (1991) cis-acting ompF mutations that result in OmpR-dependent constitutive expression. J Bacteriol 173: 4039-4048.
56. Yoshida T, Qin L, Egger LA, Inouye M, (2006) Transcription regulation of ompF and ompC by a single transcription factor, OmpR. J Biol Chem 281: 17114-17123.
57. Li L, Alvey RM, Bezy RP, Kehoe DM, (2008) Inverse transcriptional activities during complementary chromatic adaptation are controlled by the response regulator RcaC binding to red and green light-responsive promoters. Mol Microbiol 68: 286-297.
58. Gao R, Stock AM, (2010) Molecular strategies for phosphorylation-mediated regulation of response regulator activity. Curr Opin Microbiol 13: 160-167.
59. Rhee JE, Sheng W, Morgan LK, Nolet R, Liao X, et al. (2008) Amino acids important for DNA recognition by the response regulator OmpR. J Biol Chem 283: 8664-8677.
60. Ames SK, Frankema N, Kenney LJ, (1999) C-terminal DNA binding stimulates N-terminal phosphorylation of the outer membrane protein regulator OmpR from Escherichia coli. Proc Natl Acad Sci U S A 96: 11792-11797.
61. Gusa AA, Gao J, Stringer V, Churchward G, Scott JR, (2006) Phosphorylation of the group A Streptococcal CovR response regulator causes dimerization and promoter-specific recruitment by RNA polymerase. J Bacteriol 188: 4620-4626.
62. Perron-Savard P, De Crescenzo G, Le Moual H, (2005) Dimerization and DNA binding of the Salmonella enterica PhoP response regulator are phosphorylation independent. Microbiology 151: 3979-3987.
63. Lawrenz MB, Miller VL, (2007) Comparative analysis of the regulation of rovA from the pathogenic yersiniae. J Bacteriol 189: 5963-5975.
64. 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.
65. 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.
66. 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.
67. 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.
68. Labandeira-Rey M, Brautigam CA, Hansen EJ, (2010) Characterization of the CpxRA regulon in Haemophilus ducreyi. Infect Immun 78: 4779-4791.
69. Mizrahi I, Biran D, Ron EZ, (2009) Involvement of the Pta-AckA pathway in protein folding and aggregation. Res Microbiol 160: 80-84.
70. Otto K, Silhavy TJ, (2002) Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proc Natl Acad Sci U S A 99: 2287-2292.
71. Hirano Y, Hossain MM, Takeda K, Tokuda H, Miki K, (2007) Structural studies of the Cpx pathway activator NlpE on the outer membrane of Escherichia coli. Structure 15: 963-976.
72. Yamamoto K, Ishihama A, (2005) Transcriptional response of Escherichia coli to external copper. Mol Microbiol 56: 215-227.
73. Miyadai H, Tanaka-Masuda K, Matsuyama S, Tokuda H, (2004) Effects of lipoprotein overproduction on the induction of DegP (HtrA) involved in quality control in the Escherichia coli periplasm. J Biol Chem 279: 39807-39813.
74. Chi A, Huttenhower C, Geer LY, Coon JJ, Syka JE, et al. (2007) Analysis of phosphorylation sites on proteins from Saccharomyces cerevisiae by electron transfer dissociation (ETD) mass spectrometry. Proc Natl Acad Sci U S A 104: 2193-2198.
75. Ellison DW, Miller VL, (2006) H-NS represses inv transcription in Yersinia enterocolitica through competition with RovA and interaction with YmoA. J Bacteriol 188: 5101-5112.
76. Ellison DW, Young B, Nelson K, Miller VL, (2003) YmoA negatively regulates expression of invasin from Yersinia enterocolitica. J Bacteriol 185: 7153-7159.
77. Brzostek K, Brzostkowska M, Bukowska I, Karwicka E, Raczkowska A, (2007) OmpR negatively regulates expression of invasin in Yersinia enterocolitica. Microbiology 153: 2416-2425.
78. Lau-Wong IC, Locke T, Ellison MJ, Raivio TL, Frost LS, (2008) Activation of the Cpx regulon destabilizes the F plasmid transfer activator, TraJ, via the HslVU protease in Escherichia coli. Mol Microbiol 67: 516-527.