A direct link between the global regulator PhoP and the Csr regulon in Y. pseudotuberculosis through the small regulatory RNA CsrC

References

• Stock AM, Robinson VL, Goudreau PN. Two-component signal transduction. Annu Rev Biochem 2000; 69:183 - 215; http://dx.doi.org/10.1146/annurev.biochem.69.1.183; PMID: 10966457
   PubMed Web of Science ®Google Scholar
• Gao R, Stock AM. Biological insights from structures of two-component proteins. Annu Rev Microbiol 2009; 63:133 - 54; http://dx.doi.org/10.1146/annurev.micro.091208.073214; PMID: 19575571
   PubMed Web of Science ®Google Scholar
• Mascher T, Helmann JD, Unden G. Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev 2006; 70:910 - 38; http://dx.doi.org/10.1128/MMBR.00020-06; PMID: 17158704
   PubMed Web of Science ®Google Scholar
• Groisman EA. The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 2001; 183:1835 - 42; http://dx.doi.org/10.1128/JB.183.6.1835-1842.2001; PMID: 11222580
   PubMed Web of Science ®Google Scholar
• Gooderham WJ, Hancock RE. Regulation of virulence and antibiotic resistance by two-component regulatory systems in Pseudomonas aeruginosa.. FEMS Microbiol Rev 2009; 33:279 - 94; http://dx.doi.org/10.1111/j.1574-6976.2008.00135.x; PMID: 19243444
   PubMed Web of Science ®Google Scholar
• Brodsky IE, Gunn JS. A bacterial sensory system that activates resistance to innate immune defenses: potential targets for antimicrobial therapeutics. Mol Interv 2005; 5:335 - 7; http://dx.doi.org/10.1124/mi.5.6.4; PMID: 16394247
   PubMed Web of Science ®Google Scholar
• Kato A, Tanabe H, Utsumi R. Molecular characterization of the PhoP-PhoQ two-component system in Escherichia coli K-12: identification of extracellular Mg2+-responsive promoters. J Bacteriol 1999; 181:5516 - 20; PMID: 10464230
   PubMed Web of Science ®Google Scholar
• Soncini FC, Véscovi EG, Groisman EA. Transcriptional autoregulation of the Salmonella typhimurium phoPQ operon. J Bacteriol 1995; 177:4364 - 71; PMID: 7543474
   PubMed Web of Science ®Google Scholar
• Li Y, Gao H, Qin L, Li B, Han Y, Guo Z, Song Y, Zhai J, Du Z, Wang X, et al. Identification and characterization of PhoP regulon members in Yersinia pestis biovar Microtus. BMC Genomics 2008; 9:143; http://dx.doi.org/10.1186/1471-2164-9-143; PMID: 18366809
   PubMed Web of Science ®Google Scholar
• Minagawa S, Ogasawara H, Kato A, Yamamoto K, Eguchi Y, Oshima T, Mori H, Ishihama A, Utsumi R. Identification and molecular characterization of the Mg2+ stimulon of Escherichia coli.. J Bacteriol 2003; 185:3696 - 702; http://dx.doi.org/10.1128/JB.185.13.3696-3702.2003; PMID: 12813061
   PubMed Web of Science ®Google Scholar
• Yamamoto K, Ogasawara H, Fujita N, Utsumi R, Ishihama A. Novel mode of transcription regulation of divergently overlapping promoters by PhoP, the regulator of two-component system sensing external magnesium availability. Mol Microbiol 2002; 45:423 - 38; http://dx.doi.org/10.1046/j.1365-2958.2002.03017.x; PMID: 12123454
   PubMed Web of Science ®Google Scholar
• Lejona S, Aguirre A, Cabeza ML, García Véscovi E, Soncini FC. Molecular characterization of the Mg2+-responsive PhoP-PhoQ regulon in Salmonella enterica.. J Bacteriol 2003; 185:6287 - 94; http://dx.doi.org/10.1128/JB.185.21.6287-6294.2003; PMID: 14563863
   PubMed Web of Science ®Google Scholar
• Fields PI, Swanson RV, Haidaris CG, Heffron F. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci USA 1986; 83:5189 - 93; http://dx.doi.org/10.1073/pnas.83.14.5189; PMID: 3523484
   PubMed Web of Science ®Google Scholar
• Miller SI, Kukral AM, Mekalanos JJ. A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence. Proc Natl Acad Sci USA 1989; 86:5054 - 8; http://dx.doi.org/10.1073/pnas.86.13.5054; PMID: 2544889
   PubMed Web of Science ®Google Scholar
• Oyston PC, Dorrell N, Williams K, Li SR, Green M, Titball RW, Wren BW. The response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis.. Infect Immun 2000; 68:3419 - 25; http://dx.doi.org/10.1128/IAI.68.6.3419-3425.2000; PMID: 10816493
   PubMed Web of Science ®Google Scholar
• Grabenstein JP, Fukuto HS, Palmer LE, Bliska JB. Characterization of phagosome trafficking and identification of PhoP-regulated genes important for survival of Yersinia pestis in macrophages. Infect Immun 2006; 74:3727 - 41; http://dx.doi.org/10.1128/IAI.00255-06; PMID: 16790745
   PubMed Web of Science ®Google Scholar
• O’Loughlin JL, Spinner JL, Minnich SA, Kobayashi SD. Yersinia pestis two-component gene regulatory systems promote survival in human neutrophils. Infect Immun 2010; 78:773 - 82; http://dx.doi.org/10.1128/IAI.00718-09; PMID: 19933831
   PubMed Web of Science ®Google Scholar
• Hitchen PG, Prior JL, Oyston PC, Panico M, Wren BW, Titball RW, Morris HR, Dell A. Structural characterization of lipo-oligosaccharide (LOS) from Yersinia pestis: regulation of LOS structure by the PhoPQ system. Mol Microbiol 2002; 44:1637 - 50; http://dx.doi.org/10.1046/j.1365-2958.2002.02990.x; PMID: 12067350
   PubMed Web of Science ®Google Scholar
• Fields PI, Groisman EA, Heffron F. A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells. Science 1989; 243:1059 - 62; http://dx.doi.org/10.1126/science.2646710; PMID: 2646710
   PubMed Web of Science ®Google Scholar
• Galán JE, Curtiss R 3rd. Virulence and vaccine potential of phoP mutants of Salmonella typhimurium.. Microb Pathog 1989; 6:433 - 43; http://dx.doi.org/10.1016/0882-4010(89)90085-5; PMID: 2671582
   PubMed Web of Science ®Google Scholar
• Bozue J, Mou S, Moody KL, Cote CK, Trevino S, Fritz D, Worsham P. The role of the phoPQ operon in the pathogenesis of the fully virulent CO92 strain of Yersinia pestis and the IP32953 strain of Yersinia pseudotuberculosis.. Microb Pathog 2011; 50:314 - 21; http://dx.doi.org/10.1016/j.micpath.2011.02.005; PMID: 21320584
   PubMed Web of Science ®Google Scholar
• Oyston PC, Dorrell N, Williams K, Li SR, Green M, Titball RW, Wren BW. The response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis.. Infect Immun 2000; 68:3419 - 25; http://dx.doi.org/10.1128/IAI.68.6.3419-3425.2000; PMID: 10816493
   PubMed Web of Science ®Google Scholar
• Fisher ML, Castillo C, Mecsas J. Intranasal inoculation of mice with Yersinia pseudotuberculosis causes a lethal lung infection that is dependent on Yersinia outer proteins and PhoP. Infect Immun 2007; 75:429 - 42; http://dx.doi.org/10.1128/IAI.01287-06; PMID: 17074849
   PubMed Web of Science ®Google Scholar
• Bozue J, Mou S, Moody KL, Cote CK, Trevino S, Fritz D, Worsham P. The role of the phoPQ operon in the pathogenesis of the fully virulent CO92 strain of Yersinia pestis and the IP32953 strain of Yersinia pseudotuberculosis.. Microb Pathog 2011; 50:314 - 21; http://dx.doi.org/10.1016/j.micpath.2011.02.005; PMID: 21320584
   PubMed Web of Science ®Google Scholar
• Perez JC, Groisman EA. Transcription factor function and promoter architecture govern the evolution of bacterial regulons. Proc Natl Acad Sci USA 2009; 106:4319 - 24; http://dx.doi.org/10.1073/pnas.0810343106; PMID: 19251636
   PubMed Web of Science ®Google Scholar
• Perez JC, Shin D, Zwir I, Latifi T, Hadley TJ, Groisman EA. Evolution of a bacterial regulon controlling virulence and Mg(2+) homeostasis. PLoS Genet 2009; 5:e1000428; http://dx.doi.org/10.1371/journal.pgen.1000428; PMID: 19300486
   PubMed Web of Science ®Google Scholar
• Zhou D, Han Y, Qin L, Chen Z, Qiu J, Song Y, Li B, Wang J, Guo Z, Du Z, et al. Transcriptome analysis of the Mg2+-responsive PhoP regulator in Yersinia pestis.. FEMS Microbiol Lett 2005; 250:85 - 95; http://dx.doi.org/10.1016/j.femsle.2005.06.053; PMID: 16061330
   PubMed Web of Science ®Google Scholar
• Zhang Y, Gao H, Wang L, Xiao X, Tan Y, Guo Z, Zhou D, Yang R. Molecular characterization of transcriptional regulation of rovA by PhoP and RovA in Yersinia pestis.. PLoS ONE 2011; 6:e25484; http://dx.doi.org/10.1371/journal.pone.0025484; PMID: 21966533
   PubMed Web of Science ®Google Scholar
• Zhang Y, Wang L, Han Y, Yan Y, Tan Y, Zhou L, Cui Y, Du Z, Wang X, Bi Y, et al. Autoregulation of PhoP/PhoQ and positive regulation of the cyclic AMP receptor protein-cyclic AMP complex by PhoP in Yersinia pestis.. J Bacteriol 2013; 195:1022 - 30; http://dx.doi.org/10.1128/JB.01530-12; PMID: 23264579
   PubMed Web of Science ®Google Scholar
• Heroven AK, Sest M, Pisano F, Scheb-Wetzel M, Steinmann R, Böhme K, Klein J, Münch R, Schomburg D, Dersch P. Crp induces switching of the CsrB and CsrC RNAs in Yersinia pseudotuberculosis and links nutritional status to virulence. Front Cell Infect Microbiol 2012; 2:158; PMID: 23251905
   PubMedGoogle Scholar
• Ellison DW, Miller VL. Regulation of virulence by members of the MarR/SlyA family. Curr Opin Microbiol 2006; 9:153 - 9; http://dx.doi.org/10.1016/j.mib.2006.02.003; PMID: 16529980
   PubMed Web of Science ®Google Scholar
• Cathelyn JS, Ellison DW, Hinchliffe SJ, Wren BW, Miller VL. 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 2007; 66:189 - 205; http://dx.doi.org/10.1111/j.1365-2958.2007.05907.x; PMID: 17784909
   PubMed Web of Science ®Google Scholar
• Cathelyn JS, Crosby SD, Lathem WW, Goldman WE, Miller VL. RovA, a global regulator of Yersinia pestis, specifically required for bubonic plague. Proc Natl Acad Sci USA 2006; 103:13514 - 9; http://dx.doi.org/10.1073/pnas.0603456103; PMID: 16938880
   PubMed Web of Science ®Google Scholar
• Nagel G, Lahrz A, Dersch P. Environmental control of invasin expression in Yersinia pseudotuberculosis is mediated by regulation of RovA, a transcriptional activator of the SlyA/Hor family. Mol Microbiol 2001; 41:1249 - 69; http://dx.doi.org/10.1046/j.1365-2958.2001.02522.x; PMID: 11580832
   PubMed Web of Science ®Google Scholar
• Heroven AK, Dersch P. RovM, a novel LysR-type regulator of the virulence activator gene rovA, controls cell invasion, virulence and motility of Yersinia pseudotuberculosis.. Mol Microbiol 2006; 62:1469 - 83; http://dx.doi.org/10.1111/j.1365-2958.2006.05458.x; PMID: 17074075
   PubMed Web of Science ®Google Scholar
• Dube PH, Handley SA, Revell PA, Miller VL. The rovA mutant of Yersinia enterocolitica displays differential degrees of virulence depending on the route of infection. Infect Immun 2003; 71:3512 - 20; http://dx.doi.org/10.1128/IAI.71.6.3512-3520.2003; PMID: 12761136
   PubMed Web of Science ®Google Scholar
• Revell PA, Miller VL. A chromosomally encoded regulator is required for expression of the Yersinia enterocolitica inv gene and for virulence. Mol Microbiol 2000; 35:677 - 85; http://dx.doi.org/10.1046/j.1365-2958.2000.01740.x; PMID: 10672189
   PubMed Web of Science ®Google Scholar
• Heroven AK, Nagel G, Tran HJ, Parr S, Dersch P. RovA is autoregulated and antagonizes H-NS-mediated silencing of invasin and rovA expression in Yersinia pseudotuberculosis.. Mol Microbiol 2004; 53:871 - 88; http://dx.doi.org/10.1111/j.1365-2958.2004.04162.x; PMID: 15255899
   PubMed Web of Science ®Google Scholar
• Herbst K, Bujara M, Heroven AK, Opitz W, Weichert M, Zimmermann A, Dersch P. Intrinsic thermal sensing controls proteolysis of Yersinia virulence regulator RovA. PLoS Pathog 2009; 5:e1000435; http://dx.doi.org/10.1371/journal.ppat.1000435; PMID: 19468295
   PubMed Web of Science ®Google Scholar
• Heroven AK, Böhme K, Rohde M, Dersch P. A Csr-type regulatory system, including small non-coding RNAs, regulates the global virulence regulator RovA of Yersinia pseudotuberculosis through RovM. Mol Microbiol 2008; 68:1179 - 95; http://dx.doi.org/10.1111/j.1365-2958.2008.06218.x; PMID: 18430141
   PubMed Web of Science ®Google Scholar
• Heroven AK, Böhme K, Dersch P. The Csr/Rsm system of Yersinia and related pathogens: a post-transcriptional strategy for managing virulence. RNA Biol 2012; 9:379 - 91; http://dx.doi.org/10.4161/rna.19333; PMID: 22336760
   PubMed Web of Science ®Google Scholar
• Romeo T, Vakulskas CA, Babitzke P. Post-transcriptional regulation on a global scale: form and function of Csr/Rsm systems. Environ Microbiol 2012; 15:313 - 24; http://dx.doi.org/10.1111/j.1462-2920.2012.02794.x; PMID: 22672726
   PubMed Web of Science ®Google Scholar
• Babitzke P, Romeo T. CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr Opin Microbiol 2007; 10:156 - 63; http://dx.doi.org/10.1016/j.mib.2007.03.007; PMID: 17383221
   PubMed Web of Science ®Google Scholar
• Timmermans J, Van Melderen L. Post-transcriptional global regulation by CsrA in bacteria. Cell Mol Life Sci 2010; 67:2897 - 908; http://dx.doi.org/10.1007/s00018-010-0381-z; PMID: 20446015
   PubMed Web of Science ®Google Scholar
• Grabenstein JP, Marceau M, Pujol C, Simonet M, Bliska JB. The response regulator PhoP of Yersinia pseudotuberculosis is important for replication in macrophages and for virulence. Infect Immun 2004; 72:4973 - 84; http://dx.doi.org/10.1128/IAI.72.9.4973-4984.2004; PMID: 15321989
   PubMed Web of Science ®Google Scholar
• Chavez RG, Alvarez AF, Romeo T, Georgellis D. The physiological stimulus for the BarA sensor kinase. J Bacteriol 2010; 192:2009 - 12; http://dx.doi.org/10.1128/JB.01685-09; PMID: 20118252
   PubMed Web of Science ®Google Scholar
• Mondragón V, Franco B, Jonas K, Suzuki K, Romeo T, Melefors O, Georgellis D. pH-dependent activation of the BarA-UvrY two-component system in Escherichia coli.. J Bacteriol 2006; 188:8303 - 6; http://dx.doi.org/10.1128/JB.01052-06; PMID: 16980446
   PubMed Web of Science ®Google Scholar
• Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003; 31:3406 - 15; http://dx.doi.org/10.1093/nar/gkg595; PMID: 12824337
   PubMed Web of Science ®Google Scholar
• Bordi C, Lamy MC, Ventre I, Termine E, Hachani A, Fillet S, Roche B, Bleves S, Méjean V, Lazdunski A, et al. Regulatory RNAs and the HptB/RetS signalling pathways fine-tune Pseudomonas aeruginosa pathogenesis. Mol Microbiol 2010; 76:1427 - 43; http://dx.doi.org/10.1111/j.1365-2958.2010.07146.x; PMID: 20398205
   PubMed Web of Science ®Google Scholar
• Brencic A, Lory S. Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA. Mol Microbiol 2009; 72:612 - 32; http://dx.doi.org/10.1111/j.1365-2958.2009.06670.x; PMID: 19426209
   PubMed Web of Science ®Google Scholar
• Brencic A, McFarland KA, McManus HR, Castang S, Mogno I, Dove SL, Lory S. The GacS/GacA signal transduction system of Pseudomonas aeruginosa acts exclusively through its control over the transcription of the RsmY and RsmZ regulatory small RNAs. Mol Microbiol 2009; 73:434 - 45; http://dx.doi.org/10.1111/j.1365-2958.2009.06782.x; PMID: 19602144
   PubMed Web of Science ®Google Scholar
• Groisman EA, Mouslim C. Sensing by bacterial regulatory systems in host and non-host environments. Nat Rev Microbiol 2006; 4:705 - 9; http://dx.doi.org/10.1038/nrmicro1478; PMID: 16894339
   PubMed Web of Science ®Google Scholar
• Simonet M, Richard S, Berche P. Electron microscopic evidence for in vivo extracellular localization of Yersinia pseudotuberculosis harboring the pYV plasmid. Infect Immun 1990; 58:841 - 5; PMID: 2307522
   PubMed Web of Science ®Google Scholar
• Pujol C, Bliska JB. The ability to replicate in macrophages is conserved between Yersinia pestis and Yersinia pseudotuberculosis.. Infect Immun 2003; 71:5892 - 9; http://dx.doi.org/10.1128/IAI.71.10.5892-5899.2003; PMID: 14500510
   PubMed Web of Science ®Google Scholar
• Parkhill J, Wren BW, Thomson NR, Titball RW, Holden MT, Prentice MB, Sebaihia M, James KD, Churcher C, Mungall KL, et al. Genome sequence of Yersinia pestis, the causative agent of plague. Nature 2001; 413:523 - 7; http://dx.doi.org/10.1038/35097083; PMID: 11586360
   PubMed Web of Science ®Google Scholar
• Song Y, Tong Z, Wang J, Wang L, Guo Z, Han Y, Zhang J, Pei D, Zhou D, Qin H, et al. Complete genome sequence of Yersinia pestis strain 91001, an isolate avirulent to humans. DNA Res 2004; 11:179 - 97; http://dx.doi.org/10.1093/dnares/11.3.179; PMID: 15368893
   PubMed Web of Science ®Google Scholar
• Grabenstein JP, Fukuto HS, Palmer LE, Bliska JB. Characterization of phagosome trafficking and identification of PhoP-regulated genes important for survival of Yersinia pestis in macrophages. Infect Immun 2006; 74:3727 - 41; http://dx.doi.org/10.1128/IAI.00255-06; PMID: 16790745
   PubMed Web of Science ®Google Scholar
• O’Loughlin JL, Spinner JL, Minnich SA, Kobayashi SD. Yersinia pestis two-component gene regulatory systems promote survival in human neutrophils. Infect Immun 2010; 78:773 - 82; http://dx.doi.org/10.1128/IAI.00718-09; PMID: 19933831
   PubMed Web of Science ®Google Scholar
• Quade N, Mendonca C, Herbst K, Heroven AK, Ritter C, Heinz DW, Dersch P. Structural basis for intrinsic thermosensing by the master regulator RovA of Yersinia. J Biol Chem 2012; 287:35796 - 803; http://dx.doi.org/10.1074/jbc.M112.379156
   PubMed Web of Science ®Google Scholar
• Miller JH. A short course in bacterial genetic: a laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Habor, New York, 1992
   Google Scholar
• Sambrook J. Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratories, Cold Spring Harbor, NY, 2001
   Google Scholar
• Schweer J, Kulkarni D, Kochut A, Pezoldt J, Pisano F, Pils MC, Genth H, Huehn J, Dersch P. The cytotoxic necrotizing factor of Yersinia pseudotuberculosis (CNFY) enhances inflammation and Yop delivery during infection by activation of Rho GTPases. PLoS Pathog 2013; 9:e1003746; http://dx.doi.org/10.1371/journal.ppat.1003746; PMID: 24244167
   PubMedGoogle Scholar
• Böhme K, Steinmann R, Kortmann J, Seekircher S, Heroven AK, Berger E, Pisano F, Thiermann T, Wolf-Watz H, Narberhaus F, et al. Concerted actions of a thermo-labile regulator and a unique intergenic RNA thermosensor control Yersinia virulence. PLoS Pathog 2012; 8:e1002518; http://dx.doi.org/10.1371/journal.ppat.1002518; PMID: 22359501
   PubMed Web of Science ®Google Scholar