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

RNA Biology

Volumn 11, Issue 5, 2014, Pages 580-593

  Nuss, Aaron M ^a   Schuster, Franziska ^a   Heroven, Ann Kathrin ^a   Heine, Wiebke ^a   Pisano, Fabio ^a   Dersch, Petra ^a  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

Csr system; PhoP; Regulatory RNAs; RovA; Virulence gene regulation; Y. pseudotuberculosis

Indexed keywords

BACTERIAL RNA; CSRC PROTEIN; PHOP PROTEIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; PHOP PROTEIN, BACTERIA; PROTEIN BINDING; REGULATORY RNA SEQUENCE; ROVA PROTEIN, YERSINIA; ROVM PROTEIN, YERSINIA PSEUDOTUBERCULOSIS; SMALL UNTRANSLATED RNA; TRANSCRIPTION FACTOR;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BINDING SITE; DISSOCIATION CONSTANT; DNA FOOTPRINTING; GENE EXPRESSION; GENE EXPRESSION REGULATION; NONHUMAN; PROMOTER REGION; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; REGULON; RNA STABILITY; TRANSCRIPTION INITIATION; YERSINIA PSEUDOTUBERCULOSIS; BIOLOGICAL MODEL; GENETICS; METABOLISM; MICROBIOLOGY; PATHOGENICITY; REGULATORY RNA SEQUENCE; TRANSCRIPTION INITIATION SITE; VIRULENCE; YERSINIA PSEUDOTUBERCULOSIS INFECTION;

BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MODELS, BIOLOGICAL; PROTEIN BINDING; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RNA STABILITY; RNA, BACTERIAL; RNA, SMALL UNTRANSLATED; TRANSCRIPTION FACTORS; TRANSCRIPTION INITIATION SITE; TRANSCRIPTIONAL ACTIVATION; VIRULENCE; YERSINIA PSEUDOTUBERCULOSIS; YERSINIA PSEUDOTUBERCULOSIS INFECTIONS;

EID: 84906346426     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.28676     Document Type: Article

References (63)

1. Stock AM, Robinson VL, Goudreau PN. Two-component signal transduction. Annu Rev Biochem 2000; 69:183-215; PMID:10966457; http://dx.doi.org/10.1146/ annurev.biochem.69.1.183
2. Gao R, Stock AM. Biological insights from structures of two-component proteins. Annu Rev Microbiol 2009; 63:133-54; PMID:19575571; http://dx.doi.org/10.1146/annurev.micro.091208.073214
3. Mascher T, Helmann JD, Unden G. Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev 2006; 70:910-38; PMID:17158704; http://dx.doi.org/10.1128/MMBR.00020-06
4. Groisman EA. The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 2001; 183:1835-42; PMID:11222580; http://dx.doi.org/10.1128/JB.183.6. 1835-1842.2001
5. 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; PMID:19243444; http://dx.doi.org/10.1111/j.1574- 6976.2008.00135.x
6. 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; PMID:16394247; http://dx.doi.org/10.1124/mi.5.6.4
7. 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
8. Soncini FC, Véscovi EG, Groisman EA. Transcriptional autoregulation of the Salmonella typhimurium phoPQ operon. J Bacteriol 1995; 177:4364-71; PMID:7543474
9. 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; PMID:18366809; http://dx.doi.org/10.1186/1471-2164-9-143
10. 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; PMID:12813061; http://dx.doi.org/10.1128/JB.185.13.3696-3702.2003
11. 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; PMID:12123454; http://dx.doi.org/10.1046/j.1365-2958. 2002.03017.x
12. 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; PMID:14563863; http://dx.doi.org/10.1128/JB.185.21.6287-6294.2003
13. Fields PI, Swanson RV, Haidaris CG, Heffron F. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci U S A 1986; 83:5189-93; PMID:3523484; http://dx.doi.org/10.1073/pnas. 83.14.5189
14. Miller SI, Kukral AM, Mekalanos JJ. A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence. Proc Natl Acad Sci U S A 1989; 86:5054-8; PMID:2544889; http://dx.doi.org/10.1073/pnas.86.13.5054
15. 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; PMID:10816493; http://dx.doi.org/10.1128/IAI.68.6.3419-3425.2000
16. 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; PMID:16790745; http://dx.doi.org/10.1128/IAI.00255-06
17. 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; PMID:19933831; http://dx.doi.org/10.1128/IAI. 00718-09
18. 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; PMID:12067350; http://dx.doi.org/10.1046/j.1365-2958.2002. 02990.x
19. Fields PI, Groisman EA, Heffron F. A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells. Science 1989; 243:1059-62; PMID:2646710; http://dx.doi.org/10.1126/science.2646710
20. Galán JE, Curtiss R 3rd. Virulence and vaccine potential of phoP mutants of Salmonella typhimurium. Microb Pathog 1989; 6:433-43; PMID:2671582; http://dx.doi.org/10.1016/0882-4010(89)90085-5
21. 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; PMID:21320584; http://dx.doi.org/10.1016/j.micpath. 2011.02.005
22. 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; PMID:10816493; http://dx.doi.org/10.1128/IAI.68.6.3419-3425.2000
23. 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; PMID:17074849; http://dx.doi.org/10.1128/IAI.01287-06
24. 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; PMID:21320584; http://dx.doi.org/10.1016/j.micpath. 2011.02.005
25. Perez JC, Groisman EA. Transcription factor function and promoter architecture govern the evolution of bacterial regulons. Proc Natl Acad Sci U S A 2009; 106:4319-24; PMID:19251636; http://dx.doi.org/10.1073/pnas.0810343106
26. 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; PMID:19300486; http://dx.doi.org/10.1371/journal.pgen.1000428
27. 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; PMID:16061330; http://dx.doi.org/ 10.1016/j.femsle.2005.06.053
28. 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; PMID:21966533; http://dx.doi.org/10. 1371/journal.pone.0025484
29. 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; PMID:23264579; http://dx.doi.org/10.1128/JB.01530-12
30. 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; http://dx.doi.org/10.3389/fcimb.2012.00158
31. Ellison DW, Miller VL. Regulation of virulence by members of the MarR/SlyA family. Curr Opin Microbiol 2006; 9:153-9; PMID:16529980; http://dx.doi.org/10.1016/j.mib.2006.02.003
32. 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; PMID:17784909; http://dx.doi.org/10.1111/j. 1365-2958.2007.05907.x
33. 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 U S A 2006; 103:13514-9; PMID:16938880; http://dx.doi.org/10.1073/ pnas.0603456103
34. 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; PMID:11580832; http://dx.doi.org/10.1046/j.1365-2958.2001.02522.x
35. 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; PMID:17074075; http://dx.doi.org/10.1111/j.1365-2958.2006.05458.x
36. 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; PMID:12761136; http://dx.doi.org/10.1128/IAI.71.6.3512-3520.2003
37. 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; PMID:10672189; http://dx.doi.org/10.1046/j.1365-2958. 2000.01740.x
38. 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; PMID:15255899; http://dx.doi.org/10.1111/j.1365-2958.2004.04162.x
39. 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; PMID:19468295; http://dx.doi.org/10.1371/journal.ppat.1000435
40. 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; PMID:18430141; http://dx.doi.org/10.1111/j.1365-2958.2008.06218.x
41. 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; PMID:22336760; http://dx.doi.org/10.4161/rna.19333
42. 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; PMID:22672726; http://dx.doi.org/10.1111/j.1462-2920.2012.02794
43. Babitzke P, Romeo T. CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr Opin Microbiol 2007; 10:156-63; PMID:17383221; http://dx.doi.org/10.1016/j.mib.2007.03.007
44. Timmermans J, Van Melderen L. Post-transcriptional global regulation by CsrA in bacteria. Cell Mol Life Sci 2010; 67:2897-908; PMID:20446015; http://dx.doi.org/10.1007/s00018-010-0381-z
45. 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; PMID:15321989; http://dx.doi.org/10.1128/IAI.72.9.4973-4984.2004
46. Chavez RG, Alvarez AF, Romeo T, Georgellis D. The physiological stimulus for the BarA sensor kinase. J Bacteriol 2010; 192:2009-12; PMID:20118252; http://dx.doi.org/10.1128/JB.01685-09
47. 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; PMID:16980446; http://dx.doi.org/10.1128/JB.01052-06
48. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003; 31:3406-15; PMID:12824337; http://dx.doi.org/10.1093/nar/gkg595
49. 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; PMID:20398205; http://dx.doi.org/10.1111/j.1365- 2958.2010.07146.x
50. Brencic A, Lory S. Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA. Mol Microbiol 2009; 72:612-32; PMID:19426209; http://dx.doi.org/10.1111/j.1365-2958.2009.06670.x
51. 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; PMID:19602144; http://dx.doi.org/10.1111/j.1365-2958.2009.06782.x
52. Groisman EA, Mouslim C. Sensing by bacterial regulatory systems in host and non-host environments. Nat Rev Microbiol 2006; 4:705-9; PMID:16894339; http://dx.doi.org/10.1038/nrmicro1478
53. 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
54. Pujol C, Bliska JB. The ability to replicate in macrophages is conserved between Yersinia pestis and Yersinia pseudotuberculosis. Infect Immun 2003; 71:5892-9; PMID:14500510; http://dx.doi.org/10.1128/IAI.71.10.5892-5899.2003
55. 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; PMID:11586360; http://dx.doi.org/10.1038/35097083
56. 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; PMID:15368893; http://dx.doi.org/10.1093/dnares/11.3.179
57. 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; PMID:16790745; http://dx.doi.org/10.1128/IAI.00255-06
58. 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; PMID:19933831; http://dx.doi.org/10.1128/IAI. 00718-09
59. 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; PMID:22936808; http://dx.doi.org/10. 1074/jbc.M112.379156
60. 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.
61. Sambrook J. Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratories, Cold Spring Harbor, NY, 2001.
62. 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; PMID:24244167; http://dx.doi.org/10.1371/journal.ppat.1003746
63. Böhme K, Steinmann R, Kortmann J, Seekricher S, Heroven AK, Berger E, Pisano F, Theirmann T, Wolf-Watz H, Naberhaus F, et al. Concerted actions of thermo-labile regulator and a unique intergenic RNA thermosensor control Yersinia virulence. PLoS Pathog 2012; 8:e1002518; PMID:22359501; http://dx.doi.org/10.1371/journal.ooat.1002518