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OmpR, a Central Integrator of Several Cellular Responses in Yersinia enterocolitica

Part of the Advances in Experimental Medicine and Biology book series (AEMB,volume 954)

Abstract

The molecular responses of bacteria to signals from the external environment are complex, but two-component transduction systems are known to play an important role. Here, we summarize the findings of our studies to elucidate the function of the EnvZ/OmpR system in the control of a wide range of physiological processes in Yersinia enterocolitica (bio-serotype 2/O9) that are involved in environmental and host-associated stress adaptation and virulence. Our results provide evidence that OmpR participates in the adaptation of Y. enterocolitica to high osmolarity, oxidative, and low pH stresses. Moreover, they show that the OmpR response regulator both positively and negatively modulates the expression of multiple genes implicated in the control of physiological processes, such as outer membrane permeability, motility, adhesion and invasion abilities, as well as biofilm formation, and this regulation may be fine-tuned in response to changing environmental conditions.

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References

  • Aepfelbacher M, Zumbihl R, Rukdeschel K et al (1999) The tranquilizing injection of Yersinia proteins: a pathogen’s strategy to resist host defense. Biol Chem 380:795–802

    CrossRef  PubMed  CAS  Google Scholar 

  • Aiba H, Nakasai F, Mizushima S et al (1989) Evidence for the physiological importance of the phosphotransfer between the two regulatory components, EnvZ and OmpR, in osmoregulation in Escherichia coli. J Biol Chem 264:14090–14094

    PubMed  CAS  Google Scholar 

  • Badger JL, Miller VL (1998) Expression of invasin and motility are coordinately regulated in Yersinia enterocolitica. J Bacteriol 180:793–800

    PubMed  CAS  Google Scholar 

  • Bang IS, Kim BH, Foster JW, Park YK (2000) OmpR regulates the stationary-phase acid tolerance response of Salmonella enterica serovar typhimurium. J Bacteriol 182:2245–2252

    CrossRef  PubMed  CAS  Google Scholar 

  • Batzilla J, Höper D, Antonenka U et al (2011) Complete genome sequence of Yersinia enterocolitica subsp. palearctica serogroup O:3. J Bacteriol 193:2067

    CrossRef  PubMed  CAS  Google Scholar 

  • Bernardini MJ, Fontaine A, Sansonetti PJ (1990) The two-component regulatory system OmpR-EnvZ controls the virulence of Shigella flexneri. J Bacteriol 172:6274–6281

    PubMed  CAS  Google Scholar 

  • Bottone EJ (1997) Yersinia enterocolitica: the charisma continues. Clin Microbiol Rev 10:257–276

    PubMed  CAS  Google Scholar 

  • Bourret RB, Brokovich KA, Simon MI (1991) Signal transduction pathways involving protein phosphorylation in prokaryotes. Annu Rev Biochem 60:401–441

    CrossRef  PubMed  CAS  Google Scholar 

  • Brzostek K, Hrebenda J (1988) Outer-membrane permeability to β-lactam antibiotics in Yersinia enterocolitica. J Gen Microbiol 134:1535–1540

    PubMed  CAS  Google Scholar 

  • Brzostek K, Nichols WW (1990) Outer membrane permeability and porin proteins of Yersinia enterocolitica. FEMS Microbiol Lett 58:275–277

    PubMed  CAS  Google Scholar 

  • Brzostek K, Raczkowska A (2007) The YompC protein of Yersinia enterocolitica: molecular and physiological characterization. Folia Microbiol 52:73–80

    CrossRef  CAS  Google Scholar 

  • Brzostek K, Hrebenda J, Benz R, Boos W (1989) The OmpC protein of Yersinia enterocolitica: purification and properties. Res Microbiol 140:599–614

    PubMed  CAS  Google Scholar 

  • Brzostek K, Raczkowska A, Zasada A (2003) The osmotic regulator OmpR is involved in the response of Yersinia enterocolitica O:9 to environmental stresses and survival within macrophages. FEMS Microbiol Lett 228:265–271

    CrossRef  PubMed  CAS  Google Scholar 

  • Brzostek K, Brzóstkowska M, Bukowska I et al (2007) OmpR negatively regulates expression of invasin in Yersinia enterocolitica. Microbiol 153:2416–2425

    CrossRef  CAS  Google Scholar 

  • Cornelis GR, Boland A, Boyd AP et al (1998) The virulence plasmid of Yersinia, an antihost genome. Microbiol Mol Biol Rev 62:1315–1352

    PubMed  CAS  Google Scholar 

  • Dorman CJ, Chatfield S, Higgins CF et al (1989) Characterization of porin and ompR mutants of a ­virulent strain of Salmonella typhimurium: ompR mutants are attenuated in vivo. Infect Immun 57: 2136–2140

    PubMed  CAS  Google Scholar 

  • Dorrell N, Li SR, Everest PH et al (1998) Construction and characterisation of a Yersinia enterocolitica O:8 ompR mutant. FEMS Microbiol Lett 165:145–151

    CrossRef  PubMed  CAS  Google Scholar 

  • 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

    CrossRef  PubMed  CAS  Google Scholar 

  • Flamez C, Ricard I, Arafah S et al (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

    CrossRef  PubMed  CAS  Google Scholar 

  • Francez-Charlot A, Laugel B, Van Gemert A et al (2003) RcsCDB His-Asp phosphorelay system negatively regulates the flhDC operon in Escherichia coli. Mol Microbiol 49:823–832

    CrossRef  PubMed  CAS  Google Scholar 

  • Gao H, Zhang Y, Han Y et al (2011) Phenotypic and transcriptional analysis of the osmotic regulator OmpR in Yersinia pestis. BMC Microbiol 23:11–39

    Google Scholar 

  • Heroven AK, Nagel G, Tran HJ et al (2004) RovA is autoregulated and antagonizes H-NS-mediated silencing of invasin and rovA expression in Yersinia pseudotuberculosis. Mol Microbiol 53:871–888

    CrossRef  PubMed  CAS  Google Scholar 

  • Heroven AK, Böhme K, Tran-Winkler H et al (2007) Regulatory elements implicated in the environmental control of invasin expression in enteropathogenic Yersinia. Adv Exp Med Biol 603:156–166

    CrossRef  PubMed  Google Scholar 

  • Higashitani A, Nishimura Y, Hara H et al (1993) Osmoregulation of the fatty acid receptor gene fadL in Escherichia coli. Mol Gen Genet 240:339–347

    PubMed  CAS  Google Scholar 

  • Hoch J, Silhavy T (1995) Two-component signal transduction. ASM Press, Washington, DC

    Google Scholar 

  • Horne SM, Prüss BM (2006) Global gene regulation in Yersinia enterocolitica: effect of FliA on the expression levels of flagellar and plasmid-encoded virulence genes. Arch Microbiol 185:115–126

    CrossRef  PubMed  CAS  Google Scholar 

  • Hu Y, Wang Y, Ding L et al (2009) Positive regulation of flhDC expression by OmpR in Yersinia pseudotuberculosis. Microbiology 155:3622–3631

    CrossRef  PubMed  CAS  Google Scholar 

  • Iriarte M, Stainier I, Mikulskis AV et al (1995) The fliA gene encoding sigma 28 in Yersinia enterocolitica. J Bacteriol 177:2299–2304

    PubMed  CAS  Google Scholar 

  • Jubelin G, Vianney A, Beloin C et al (2005) CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli. J Bacteriol 187: 2038–2049

    CrossRef  PubMed  CAS  Google Scholar 

  • Kapatral V, Olson JW, Pepe JC et al (1996) Temperature-dependent regulation of Yersinia enterocolitica class III flagellar genes. Mol Microbiol 19:1061–1071

    CrossRef  PubMed  CAS  Google Scholar 

  • Kapatral V, Campbell JW, Minnich SA et al (2004) Gene array analysis of Yersinia enterocolitica FlhD and FlhC: regulation of enzymes affecting synthesis and degradation of carbamoylphosphate. Microbiology 7:2289–2300

    CrossRef  Google Scholar 

  • Kenney LJ (2002) Structure/function relationships in OmpR and other winged-helix transcription factors. Curr Opin Microbiol 5:135–141

    CrossRef  PubMed  CAS  Google Scholar 

  • Kim TJ, Young BM, Young GM (2008) Effect of flagellar mutations on Yersinia enterocolitica biofilm formation. Appl Environ Microbiol 74:5466–5474

    CrossRef  PubMed  CAS  Google Scholar 

  • Lawrenz MB, Miller VL (2007) Comparative analysis of the regulation of rovA from the pathogenic yersiniae. J Bacteriol 189:5963–5975

    CrossRef  PubMed  CAS  Google Scholar 

  • Lee AK, Detweiler CS, Falkow S (2000) OmpR regulates the two-component system SsrA-SsrB in Salmonella pathogenicity island 2. J Bacteriol 182:771–781

    CrossRef  PubMed  CAS  Google Scholar 

  • Lee VT, Mazmanian SK, Schneewind O (2001) A program of Yersinia enterocolitica type III reaction is activated by specific signal. J Bacteriol 183:4970–4978

    CrossRef  PubMed  CAS  Google Scholar 

  • Marceau M (2005) Transcriptional regulation in Yersinia: an update. Curr Issues Mol Biol 7:151–177

    PubMed  CAS  Google Scholar 

  • 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 Sly/Hor family. Mol Microbiol 41:1249–1269

    CrossRef  PubMed  CAS  Google Scholar 

  • Neubauer H, Aleksic S, Hensel A et al (2000) Yersinia enterocolitica 16 S rRNA gene types belong to the same genospecies but form three homology groups. Int J Med Microbiol 290:61–64

    CrossRef  PubMed  CAS  Google Scholar 

  • O’Loughlin JL, Spinner JL, Minnich SA et al (2010) Yersinia pestis two-component gene regulatory systems promote survival in human neutrophils. Infect Immun 78:773–782

    CrossRef  PubMed  Google Scholar 

  • Pepe J, Miller VL (1993) Yersinia enterocolitica invasin: a primary role in the initiation of infection. Proc Natl Acad Sci USA 90:6473–6477

    CrossRef  PubMed  CAS  Google Scholar 

  • Pepe JC, Badger JL, Miller VL (1994) Growth phase and low pH affect the thermal regulation of the Yersinia enterocolitica inv gene. Mol Microbiol 11:123–135

    CrossRef  PubMed  CAS  Google Scholar 

  • Raczkowska A, Brzostek K (2004) Identification of OmpR protein and its role in invasion properties of Yersinia enterocolitica. P J Microbiol 53:11–16

    CAS  Google Scholar 

  • Raczkowska A, Skorek K, Bielecki J, Brzostek K (2011a) OmpR controls Yersinia enterocolitica motility by positive regulation of flhDC expression. Antonie Van Leeuwenhoek 99:381–394

    CrossRef  PubMed  Google Scholar 

  • Raczkowska A, Skorek K, Brzóstkowska M et al (2011b) Pleiotropic effects of a Yersinia enterocolitica ompR mutation on adherent-invasive abilities and biofilm formation. FEMS Microbiol Lett. doi:10.1111/j.1574-6968.2011.02308.x

  • Russo FD, Silhavy TJ (1990) EnvZ controls the concentration of phosphoryled OmpR to mediate osmoregulation of the porin genes. J Mol Biol 222:567–580

    CrossRef  Google Scholar 

  • Shin S, Park C (1995) Modulation of flagellar expression in Escherichia coli by acetyl phosphate and the osmoregulator OmpR. J Bacteriol 177:4696–4702

    PubMed  CAS  Google Scholar 

  • Skurnik M, Wolf-Watz H (1989) Analysis of the yopA gene encoding the Yop1 virulence determinants of Yersinia spp. Mol Microbiol 3:517–529

    CrossRef  PubMed  CAS  Google Scholar 

  • Stock JB, Ninfa AJ, Stock AM (1989) Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol Rev 53:450–490

    PubMed  CAS  Google Scholar 

  • Straley SC, Perry RD (1995) Environmental modulation of gene expression and pathogenesis in Yersinia. Trends Microbiol 3:310–317

    CrossRef  PubMed  CAS  Google Scholar 

  • Webb JS, Givskov M, Kjelleberg S (2003) Bacterial biofilms: prokaryotic adventures in multicellularity. Curr Opin Microbiol 6:578–585

    CrossRef  PubMed  CAS  Google Scholar 

  • Young GM, Smith MJ, Minnich SA et al (1999) The Yersinia enterocolitica motility master regulatory operon flhDC is required for flagellin production, swimming motility, and swarming motility. J Bacteriol 181:2823–2833

    PubMed  CAS  Google Scholar 

  • Young GM, Badger JL, Miller VL (2000) Motility is required to initiate host cell invasion by Yersinia enterocolitica. Infect Immun 68:4323–4326

    CrossRef  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the Polish Ministry of Science and Higher Education (grant N303 009 32/0537).

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Correspondence to Katarzyna Brzostek .

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Brzostek, K., Skorek, K., Raczkowska, A. (2012). OmpR, a Central Integrator of Several Cellular Responses in Yersinia enterocolitica . In: de Almeida, A., Leal, N. (eds) Advances in Yersinia Research. Advances in Experimental Medicine and Biology, vol 954. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-3561-7_40

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