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Abstract:

VjbR is a LuxR homolog that regulates transcription of many genes including important virulence determinants of the facultative intracellular pathogen Brucella abortus. This transcription factor belongs to a family of regulators that participate in a cell-cell communication process called quorum sensing, which enables bacteria to respond to changes in cell population density by monitoring concentration of self produced autoinducer molecules. Unlike almost all other LuxR-type proteins, VjbR binds to DNA and activates transcription in the absence of any autoinducer signal. To investigate the mechanisms by which Brucella induces VjbR-mediated transcriptional activation, and to determine how inappropriate spatio-temporal expression of the VjbR target genes is prevented, we focused on the study of expression of vjbR itself. By assaying different parameters related to the intracellular lifestyle of Brucella, we identified a restricted set of conditions that triggers VjbR protein expression. Such conditions required the convergence of two signals of different nature: a specific pH value of 5.5 and the presence of urocanic acid, a metabolite involved in the connection between virulence and metabolism of Brucella. In addition, we also observed an urocanic acid, pH-dependent expression of RibH2 and VirB7, two additional intracellular survival-related proteins of Brucella. Analysis of promoter activities and determination of mRNA levels demonstrated that the urocanic acid-dependent mechanisms that induced expression of VjbR, RibH2, and VirB7 act at the post-transcriptional level. Taken together, our findings support a model whereby Brucella induces VjbR-mediated transcription by modulating expression of VjbR in response to specific signals related to the changing environment encountered within the host. © 2012 Arocena et al.

Registro:

Documento: Artículo
Título:Expression of VjbR under nutrient limitation conditions is regulated at the post-transcriptional level by specific acidic pH values and urocanic acid
Autor:Arocena, G.M.; Zorreguieta, A.; Sieira, R.
Filiación:Fundación Instituto Leloir - IBBA-CONICET, Buenos Aires, Argentina
Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Palabras clave:messenger RNA; RibH2 protein; transcription factor; unclassified drug; urocanic acid; VirB7 protein; VjbR protein; article; bacterial gene; bacterial metabolism; bacterial survival; bacterial virulence; Brucella; controlled study; gene expression; intracellular bacterium; nonhuman; nutrient limitation; pH; promoter region; protein expression; transcription initiation; transcription regulation; VjbR gene; Bacterial Proteins; Brucella abortus; Gene Expression Regulation, Bacterial; Glutamic Acid; Hydrogen-Ion Concentration; Quorum Sensing; Transcription Factors; Urocanic Acid; Virulence; Brucella; Brucella melitensis biovar Abortus
Año:2012
Volumen:7
Número:4
DOI: http://dx.doi.org/10.1371/journal.pone.0035394
Título revista:PLoS ONE
Título revista abreviado:PLoS ONE
ISSN:19326203
CAS:urocanic acid, 104-98-3; Bacterial Proteins; Glutamic Acid, 56-86-0; Transcription Factors; Urocanic Acid, 104-98-3
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_19326203_v7_n4_p_Arocena.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_19326203_v7_n4_p_Arocena

Referencias:

  • Corbel, M.J., Brucellosis: an overview (1997) Emerg Infect Dis, 3, pp. 213-221
  • Pizarro-Cerda, J., Meresse, S., Parton, R.G., van der Goot, G., Sola-Landa, A., Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes (1998) Infect Immun, 66, pp. 5711-5724
  • Porte, F., Liautard, J.P., Kohler, S., Early acidification of phagosomes containing Brucella suis is essential for intracellular survival in murine macrophages (1999) Infect Immun, 67, pp. 4041-4047
  • Starr, T., Ng, T.W., Wehrly, T.D., Knodler, L.A., Celli, J., Brucella intracellular replication requires trafficking through the late endosomal/lysosomal compartment (2008) Traffic, 9, pp. 678-694
  • Boschiroli, M.L., Ouahrani-Bettache, S., Foulongne, V., Michaux-Charachon, S., Bourg, G., The Brucella suis virB operon is induced intracellularly in macrophages (2002) Proc Natl Acad Sci U S A, 99, pp. 1544-1549
  • O'Callaghan, D., Cazevieille, C., Allardet-Servent, A., Boschiroli, M.L., Bourg, G., A homologue of the Agrobacterium tumefaciens VirB and Bordetella pertussis Ptl type IV secretion systems is essential for intracellular survival of Brucella suis (1999) Mol Microbiol, 33, pp. 1210-1220
  • Celli, J., de Chastellier, C., Franchini, D.M., Pizarro-Cerda, J., Moreno, E., Brucella evades macrophage killing via VirB-dependent sustained interactions with the endoplasmic reticulum (2003) J Exp Med, 198, pp. 545-556
  • de Barsy, M., Jamet, A., Filopon, D., Nicolas, C., Laloux, G., Identification of a Brucella spp. secreted effector specifically interacting with human small GTPase Rab2 (2011) Cell Microbiol, 13, pp. 1044-1058
  • de Jong, M.F., Sun, Y.H., den Hartigh, A.B., van Dijl, J.M., Tsolis, R.M., Identification of VceA and VceC, two members of the VjbR regulon that are translocated into macrophages by the Brucella type IV secretion system (2008) Mol Microbiol, 70, pp. 1378-1396
  • Marchesini, M.I., Herrmann, C.K., Salcedo, S.P., Gorvel, J.P., Comerci, D.J., In search of Brucella abortus type IV secretion substrates: screening and identification of four proteins translocated into host cells through VirB system (2011) Cell Microbiol, 13, pp. 1261-1274
  • Sieira, R., Comerci, D.J., Pietrasanta, L.I., Ugalde, R.A., Integration host factor is involved in transcriptional regulation of the Brucella abortus virB operon (2004) Mol Microbiol, 54, pp. 808-822
  • Sieira, R., Arocena, G.M., Bukata, L., Comerci, D.J., Ugalde, R.A., Metabolic control of virulence genes in Brucella abortus: HutC coordinates virB expression and the histidine utilization pathway by direct binding to both promoters (2010) J Bacteriol, 192, pp. 217-224
  • Rambow-Larsen, A.A., Petersen, E.M., Gourley, C.R., Splitter, G.A., Brucella regulators: self-control in a hostile environment (2009) Trends Microbiol, 17, pp. 371-377
  • Delrue, R.M., Deschamps, C., Leonard, S., Nijskens, C., Danese, I., A quorum-sensing regulator controls expression of both the type IV secretion system and the flagellar apparatus of Brucella melitensis (2005) Cell Microbiol, 7, pp. 1151-1161
  • Arocena, G.M., Sieira, R., Comerci, D.J., Ugalde, R.A., Identification of the quorum-sensing target DNA sequence and N-Acyl homoserine lactone responsiveness of the Brucella abortus virB promoter (2010) J Bacteriol, 192, pp. 3434-3440
  • McAnulla, C., Edwards, A., Sanchez-Contreras, M., Sawers, R.G., Downie, J.A., Quorum-sensing-regulated transcriptional initiation of plasmid transfer and replication genes in Rhizobium leguminosarum biovar viciae (2007) Microbiology, 153, pp. 2074-2082
  • Yang, M., Giel, J.L., Cai, T., Zhong, Z., Zhu, J., The LuxR family quorum-sensing activator MrtR requires its cognate autoinducer for dimerization and activation but not for protein folding (2009) J Bacteriol, 191, pp. 434-438
  • Tsai, C.S., Winans, S.C., LuxR-type quorum-sensing regulators that are detached from common scents (2010) Mol Microbiol, 77, pp. 1072-1082
  • Patankar, A.V., Gonzalez, J.E., Orphan LuxR regulators of quorum sensing (2009) FEMS Microbiol Rev, 33, pp. 739-756
  • Taminiau, B., Daykin, M., Swift, S., Boschiroli, M.L., Tibor, A., Identification of a quorum-sensing signal molecule in the facultative intracellular pathogen Brucella melitensis (2002) Infect Immun, 70, pp. 3004-3011
  • Weeks, J.N., Galindo, C.L., Drake, K.L., Adams, G.L., Garner, H.R., Brucella melitensis VjbR and C12-HSL regulons: contributions of the N-dodecanoyl homoserine lactone signaling molecule and LuxR homologue VjbR to gene expression (2010) BMC Microbiol, 10, p. 167
  • Schafer, A., Tauch, A., Jager, W., Kalinowski, J., Thierbach, G., Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum (1994) Gene, 145, pp. 69-73
  • Bonomi, H.R., Marchesini, M.I., Klinke, S., Ugalde, J.E., Zylberman, V., An atypical riboflavin pathway is essential for Brucella abortus virulence (2010) PLoS One, 5, pp. e9435
  • Becker, A., Schmidt, M., Jager, W., Puhler, A., New gentamicin-resistance and lacZ promoter-probe cassettes suitable for insertion mutagenesis and generation of transcriptional fusions (1995) Gene, 162, pp. 37-39
  • Sambrook, J.F.E., Maniatis, T., (1989) Molecular Cloning: A Laboratory Manual, , New York, Cold Spring Harbor Laboratory Press
  • Martinez-Nunez, C., Altamirano-Silva, P., Alvarado-Guillen, F., Moreno, E., Guzman-Verri, C., The two-component system BvrR/BvrS regulates the expression of the type IV secretion system VirB in Brucella abortus (2010) J Bacteriol, 192, pp. 5603-5608
  • Rambow-Larsen, A.A., Rajashekara, G., Petersen, E., Splitter, G., Putative quorum-sensing regulator BlxR of Brucella melitensis regulates virulence factors including the type IV secretion system and flagella (2008) J Bacteriol, 190, pp. 3274-3282
  • Uzureau, S., Lemaire, J., Delaive, E., Dieu, M., Gaigneaux, A., Global analysis of quorum sensing targets in the intracellular pathogen Brucella melitensis 16 M (2010) J Proteome Res, 9, pp. 3200-3217
  • Kohler, S., Foulongne, V., Ouahrani-Bettache, S., Bourg, G., Teyssier, J., The analysis of the intramacrophagic virulome of Brucella suis deciphers the environment encountered by the pathogen inside the macrophage host cell (2002) Proc Natl Acad Sci U S A, 99, pp. 15711-15716
  • Zhang, X.X., Rainey, P.B., Genetic analysis of the histidine utilization (hut) genes in Pseudomonas fluorescens SBW25 (2007) Genetics, 176, pp. 2165-2176
  • Uzureau, S., Godefroid, M., Deschamps, C., Lemaire, J., de Bolle, X., Mutations of the quorum sensing-dependent regulator VjbR lead to drastic surface modifications in Brucella melitensis (2007) J Bacteriol, 189, pp. 6035-6047
  • Patey, G., Qi, Z., Bourg, G., Baron, C., O'Callaghan, D., Swapping of periplasmic domains between Brucella suis VirB8 and a pSB102 VirB8 homologue allows heterologous complementation (2006) Infect Immun, 74, pp. 4945-4949
  • Rouot, B., Alvarez-Martinez, M.T., Marius, C., Menanteau, P., Guilloteau, L., Production of the type IV secretion system differs among Brucella species as revealed with VirB5- and VirB8-specific antisera (2003) Infect Immun, 71, pp. 1075-1082
  • Broughton, E.S., Jahans, K.L., The differentiation of Brucella species by substrate specific tetrazolium reduction (1997) Vet Microbiol, 57, pp. 253-271
  • Dorrell, N., Guigue-Talet, P., Spencer, S., Foulonge, V., O'Callaghan, D., Investigation into the role of the response regulator NtrC in the metabolism and virulence of Brucella suis (1999) Microb Pathog, 27, pp. 1-11

Citas:

---------- APA ----------
Arocena, G.M., Zorreguieta, A. & Sieira, R. (2012) . Expression of VjbR under nutrient limitation conditions is regulated at the post-transcriptional level by specific acidic pH values and urocanic acid. PLoS ONE, 7(4).
http://dx.doi.org/10.1371/journal.pone.0035394
---------- CHICAGO ----------
Arocena, G.M., Zorreguieta, A., Sieira, R. "Expression of VjbR under nutrient limitation conditions is regulated at the post-transcriptional level by specific acidic pH values and urocanic acid" . PLoS ONE 7, no. 4 (2012).
http://dx.doi.org/10.1371/journal.pone.0035394
---------- MLA ----------
Arocena, G.M., Zorreguieta, A., Sieira, R. "Expression of VjbR under nutrient limitation conditions is regulated at the post-transcriptional level by specific acidic pH values and urocanic acid" . PLoS ONE, vol. 7, no. 4, 2012.
http://dx.doi.org/10.1371/journal.pone.0035394
---------- VANCOUVER ----------
Arocena, G.M., Zorreguieta, A., Sieira, R. Expression of VjbR under nutrient limitation conditions is regulated at the post-transcriptional level by specific acidic pH values and urocanic acid. PLoS ONE. 2012;7(4).
http://dx.doi.org/10.1371/journal.pone.0035394