Identification of VceA and VceC, two members of the VjbR regulon that are translocated into macrophages by the Brucella type IV secretion system

Molecular Microbiology

Volumn 70, Issue 6, 2008, Pages 1378-1396

  De Jong, Maarten F ^a,b   Sun, Yao Hui ^a   Den Hartigh, Andreas B ^a   Van Dijl, Jan Maarten ^b   Tsolis, Renée M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BETA LACTAMASE; CARRIER PROTEIN; FLAGELLIN; GLUCAN SYNTHASE; TRANSCRIPTION FACTOR LUXR; UNCLASSIFIED DRUG; VCE A PROTEIN; VCE C PROTEIN; VIRB PROTEIN; VJBR PROTEIN;

ARTICLE; BACTERIAL GENETICS; BACTERIAL STRAIN; BRUCELLA; BRUCELLA ABORTUS; BRUCELLA SUIS; CELL SURVIVAL; CONTROLLED STUDY; ENZYME SUBSTRATE; FRAGMENTATION REACTION; GENE CONTROL; GENOME; HOST CELL; LEGIONELLA PNEUMOPHILA; MACROPHAGE; MICROBIAL COMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN EXPRESSION; REGULON;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; BRUCELLA ABORTUS; BRUCELLA SUIS; CELL LINE; CONSENSUS SEQUENCE; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC COMPLEMENTATION TEST; MACROPHAGES; MICE; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; REGULON; SECRETORY PATHWAY;

BRUCELLA; BRUCELLA MELITENSIS BIOVAR ABORTUS; BRUCELLA SUIS 1330; LEGIONELLA PNEUMOPHILA;

EID: 56749156682     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06487.x     Document Type: Article

References (71)

1. Altman, E. Segal, G. (2008) The response regulator CpxR directly regulates expression of several Legionella pneumophila icm/dot components as well as new translocated substrates. J Bacteriol 190 : 1985 1996.
2. Arellano-Reynoso, B., Lapaque, N., Salcedo, S., Briones, G., Ciocchini, A.E., Ugalde, R., et al. (2005) Cyclic beta-1,2-glucan is a Brucella virulence factor required for intracellular survival. Nat Immunol 6 : 618 625.
3. Arenas, G.N., Staskevich, A.S., Aballay, A. Mayorga, L.S. (2000) Intracellular trafficking of Brucella abortus in J774 macrophages. Infect Immun 68 : 4255 4263.
4. Backert, S. Meyer, T.F. (2006) Type IV secretion systems and their effectors in bacterial pathogenesis. Curr Opin Microbiol 9 : 207 217.
5. Bailey, T.L. Gribskov, M. (1998) Combining evidence using p-values: application to sequence homology searches. Bioinformatics 14 : 48 54.
6. Berger, K.H. Isberg, R.R. (1993) Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol Microbiol 7 : 7 19.
7. Berger, B.R. Christie, P.J. (1994) Genetic complementation analysis of the Agrobacterium tumefaciens virB operon: virB2 through virB11 are essential virulence genes. J Bacteriol 176 : 3646 3660.
8. Boch, J., Joardar, V., Gao, L., Robertson, T.L., Lim, M. Kunkel, B.N. (2002) Identification of Pseudomonas syringae pv. tomato genes induced during infection of Arabidopsis thaliana. Mol Microbiol 44 : 73 88.
9. Boschiroli, M.L., Ouahrani-Bettache, S., Foulongne, V., Michaux-Charachon, S., Bourg, G., Allardet-Servent, A., et al. (2002) The Brucella suis virB operon is induced intracellularly in macrophages. Proc Natl Acad Sci USA 99 : 1544 1549.
10. Briones, G., Inon de Iannino, N., Roset, M., Vigliocco, A., Paulo, P.S. Ugalde, R.A. (2001) Brucella abortus cyclic beta-1,2-glucan mutants have reduced virulence in mice and are defective in intracellular replication in HeLa cells. Infect Immun 69 : 4528 4535.
11. Cambronne, E.D. Roy, C.R. (2007) The Legionella pneumophila IcmSW complex interacts with multiple Dot/Icm effectors to facilitate type IV translocation. PLoS Pathog 3 : e188.
12. Celli, J., de Chastellier, C., Franchini, D.M., Pizarro-Cerda, J., Moreno, E. Gorvel, J.P. (2003) Brucella evades macrophage killing via VirB-dependent sustained interactions with the endoplasmic reticulum. J Exp Med 198 : 545 556.
13. Celli, J., Salcedo, S.P. Gorvel, J.P. (2005) Brucella coopts the small GTPase Sar1 for intracellular replication. Proc Natl Acad Sci USA 102 : 1673 1678.
14. Chain, P.S., Comerci, D.J., Tolmasky, M.E., Larimer, F.W., Malfatti, S.A., Vergez, L.M., et al. (2005) Whole-genome analyses of speciation events in pathogenic Brucellae. Infect Immun 73 : 8353 8361.
15. Charpentier, X. Oswald, E. (2004) Identification of the secretion and translocation domain of the enteropathogenic and enterohemorrhagic Escherichia coli effector Cif, using TEM-1 beta-lactamase as a new fluorescence-based reporter. J Bacteriol 186 : 5486 5495.
16. Chen, J., de Felipe, K.S., Clarke, M., Lu, H., Anderson, O.R., Segal, G. Shuman, H.A. (2004) Legionella effectors that promote nonlytic release from protozoa. Science 303 : 1358 1361.
17. Christie, P.J. (2004) Type IV secretion: the Agrobacterium VirB/D4 and related conjugation systems. Biochim Biophys Acta 1694 : 219 234.
18. Comerci, D.J., Martinez-Lorenzo, M.J., Sieira, R., Gorvel, J.P. Ugalde, R.A. (2001) Essential role of the VirB machinery in the maturation of the Brucella abortus-containing vacuole. Cell Microbiol 3 : 159 168.
19. Conover, G.M., Derre, I., Vogel, J.P. Isberg, R.R. (2003) The Legionella pneumophila LidA protein: a translocated substrate of the Dot/Icm system associated with maintenance of bacterial integrity. Mol Microbiol 48 : 305 321.
20. Covacci, A. Rappuoli, R. (1993) Pertussis toxin export requires accessory genes located downstream from the pertussis toxin operon. Mol Microbiol 8 : 429 434.
21. Delrue, R.M., Martinez-Lorenzo, M., Lestrate, P., Danese, I., Bielarz, V., Mertens, P., et al. (2001) Identification of Brucella spp. genes involved in intracellular trafficking. Cell Microbiol 3 : 487 497.
22. Delrue, R.M., Deschamps, C., Leonard, S., Nijskens, C., Danese, I., Schaus, J.M., et al. (2005) A quorum-sensing regulator controls expression of both the type IV secretion system and the flagellar apparatus of Brucella melitensis. Cell Microbiol 7 : 1151 1161.
23. Dozot, M., Boigegrain, R.A., Delrue, R.M., Hallez, R., Ouahrani-Bettache, S., Danese, I., et al. (2006) The stringent response mediator Rsh is required for Brucella melitensis and Brucella suis virulence, and for expression of the type IV secretion system virB. Cell Microbiol 8 : 1791 1802.
24. Feeley, J.C., Gibson, R.J., Gorman, G.W., Langford, N.C., Rasheed, J.K., Mackel, D.C. Baine, W.B. (1979) Charcoal-yeast extract agar: primary isolation medium for Legionella pneumophila. J Clin Microbiol 10 : 437 441.
25. de Felipe, K.S., Pampou, S., Jovanovic, O.S., Pericone, C.D., Kalachikov, S.F., Ye, S. Shuman, H.A. (2005) Evidence for acquisition of Legionella type IV secretion substrates via interdomain horizontal gene transfer. J Bacteriol 187 : 7716 7726.
26. de Felipe, K.S., Glover, R.T., Charpentier, X., Anderson, O.R., Reyes, M., Pericone, C.D. Shuman, H.A. (2008) Legionella eukaryotic-like type IV substrates interfere with organelle trafficking. PLoS Pathog 4 : e1000117.
27. Fretin, D., Fauconnier, A., Kohler, S., Halling, S., Leonard, S., Nijskens, C., et al. (2005) The sheathed flagellum of Brucella melitensis is involved in persistence in a murine model of infection. Cell Microbiol 7 : 687 698.
28. Fullner, K.J. (1998) Role of Agrobacterium virB genes in transfer of T complexes and RSF1010. J Bacteriol 180 : 430 434.
29. Haine, V., Sinon, A., Van Steen, F., Rousseau, S., Dozot, M., Lestrate, P., et al. (2005) Systematic targeted mutagenesis of Brucella melitensis 16M reveals a major role for GntR regulators in the control of virulence. Infect Immun 73 : 5578 5586.
30. Halling, S.M., Peterson-Burch, B.D., Bricker, B.J., Zuerner, R.L., Qing, Z., Li, L.L., et al. (2005) Completion of the genome sequence of Brucella abortus and comparison to the highly similar genomes of Brucella melitensis and Brucella suis. J Bacteriol 187 : 2715 2726.
31. den Hartigh, A.B., Sun, Y.-H., Sondervan, D., Heuvelmans, N., Reinders, M.O., Ficht, T.A. Tsolis, R.M. (2004) Differential requirements for VirB1 and VirB2 during Brucella abortus infection. Infect Immun 72 : 5143 5149.
32. Hohlfeld, S., Pattis, I., Puls, J., Plano, G.V., Haas, R. Fischer, W. (2006) A C-terminal translocation signal is necessary, but not sufficient for type IV secretion of the Helicobacter pylori CagA protein. Mol Microbiol 59 : 1624 1637.
33. Hong, P.C., Tsolis, R.M. Ficht, T.A. (2000) Identification of genes required for chronic persistence of Brucella abortus in mice. Infect Immun 68 : 4102 4107.
34. Hubber, A.M., Sullivan, J.T. Ronson, C.W. (2007) Symbiosis-induced cascade regulation of the Mesorhizobium loti R7A VirB/D4 type IV secretion system. Mol Plant Microbe Interact 20 : 255 261.
35. Kulakov, Y.K., Guigue-Talet, P.G., Ramuz, M.R. O'Callaghan, D. (1997) Response of Brucella suis 1330 and B. canis RM6/66 to growth at acid pH and induction of an adaptive acid tolerance response. Res Microbiol 148 : 145 151.
36. Leonard, S., Ferooz, J., Haine, V., Danese, I., Fretin, D., Tibor, A., et al. (2007) FtcR is a new master regulator of the flagellar system of Brucella melitensis 16M with homologs in Rhizobiaceae. J Bacteriol 189 : 131 141.
37. LeVier, K., Phillips, R.W., Grippe, V.K., Roop, R.M., 2nd. Walker, G.C. (2000) Similar requirements of a plant symbiont and a mammalian pathogen for prolonged intracellular survival. Science 287 : 2492 2493.
38. Lindeberg, M., Stavrinides, J., Chang, J.H., Alfano, J.R., Collmer, A., Dangl, J.L., et al. (2005) Proposed guidelines for a unified nomenclature and phylogenetic analysis of type III Hop effector proteins in the plant pathogen Pseudomonas syringae. Mol Plant Microbe Interact 18 : 275 282.
39. Luo, Z.Q. Isberg, R.R. (2004) Multiple substrates of the Legionella pneumophila Dot/Icm system identified by interbacterial protein transfer. Proc Natl Acad Sci USA 101 : 841 846.
40. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, New York.
41. Moreno, E., Stackebrandt, E., Dorsch, M., Wolters, J., Busch, M. Mayer, H. (1990) Brucella abortus 16S rRNA and lipid A reveal a phylogenetic relationship with members of the alpha-2 subdivision of the class Proteobacteria. J Bacteriol 172 : 3569 3576.
42. Nagai, H. Roy, C.R. (2001) The DotA protein from Legionella pneumophila is secreted by a novel process that requires the Dot/Icm transporter. EMBO J 20 : 5962 5970.
43. Nagai, H., Cambronne, E.D., Kagan, J.C., Amor, J.C., Kahn, R.A. Roy, C.R. (2005) A C-terminal translocation signal required for Dot/Icm-dependent delivery of the Legionella RalF protein to host cells. Proc Natl Acad Sci USA 102 : 826 831.
44. O'Callaghan, D., Cazevieille, C., Allardet-Servent, A., Boschiroli, M.L., Bourg, G., Foulongne, V., et al. (1999) A homologue of the Agrobacterium tumefaciens VirB and Bordetella pertussis Ptl type IV secretion systems is essential for intracellular survival of Brucella suis. Mol Microbiol 33 : 1210 1220.
45. Pappas, K.M. Winans, S.C. (2003) A LuxR-type regulator from Agrobacterium tumefaciens elevates Ti plasmid copy number by activating transcription of plasmid replication genes. Mol Microbiol 48 : 1059 1073.
46. Patey, G., Qi, Z., Bourg, G., Baron, C. O'Callaghan, D. (2006) Swapping of periplasmic domains between Brucella suis VirB8 and a pSB102 VirB8 homologue allows heterologous complementation. Infect Immun 74 : 4945 4949.
47. Paulsen, I., Seshadri, R., Nelson, K., Eisen, J., Heidelberg, J., Read, T., et al. (2002) The Brucella suis genome reveals fundamental similarities between animal and plant pathogens and symbionts. Proc Natl Acad Sci USA 99 : 13148 13153.
48. Pei, J., Wu, Q., Kahl-McDonagh, M. Ficht, T.A. (2008) Cytotoxicity in macrophages infected with rough Brucella mutants is type IV secretion system dependent. Infect Immun 76 : 30 37.
49. Pizarro-Cerda, J., Meresse, S., Parton, R.G., van der Goot, G., Sola-Landa, A., Lopez-Goni, I., et al. (1998a) Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes. Infect Immun 66 : 5711 5724.
50. Pizarro-Cerda, J., Moreno, E., Sanguedolce, V., Mege, J.L. Gorvel, J.P. (1998b) Virulent Brucella abortus prevents lysosome fusion and is distributed within autophagosome-like compartments. Infect Immun 66 : 2387 2392.
51. Raffatellu, M., Sun, Y.H., Wilson, R.P., Tran, Q.T., Chessa, D., Andrews-Polymenis, H.L., et al. (2005) Host restriction of Salmonella enterica serotype Typhi is not caused by functional alteration of SipA, SopB, or SopD. Infect Immun 73 : 7817 7826.
52. Rambow-Larsen, A.A., Rajashekara, G., Petersen, E. Splitter, G. (2008) Putative quorum-sensing regulator BlxR of Brucella melitensis regulates virulence factors including the type IV secretion system and flagella. J Bacteriol 190 : 3274 3282.
53. Rouot, B., Alvarez-Martinez, M.T., Marius, C., Menanteau, P., Guilloteau, L., Boigegrain, R.A., et al. (2003) Production of the type IV secretion system differs among Brucella species as revealed with VirB5- and VirB8-specific antisera. Infect Immun 71 : 1075 1082.
54. Schulein, R., Guye, P., Rhomberg, T.A., Schmid, M.C., Schroder, G., Vergunst, A.C., et al. (2005) A bipartite signal mediates the transfer of type IV secretion substrates of Bartonella henselae into human cells. Proc Natl Acad Sci USA 102 : 856 861.
55. Shadel, G.S. Baldwin, T.O. (1991) The Vibrio fischeri LuxR protein is capable of bidirectional stimulation of transcription and both positive and negative regulation of the luxR gene. J Bacteriol 173 : 568 574.
56. Shadel, G.S. Baldwin, T.O. (1992) Positive autoregulation of the Vibrio fischeri luxR gene. LuxR and autoinducer activate cAMP-catabolite gene activator protein complex-independent and -dependent luxR transcription. J Biol Chem 267 : 7696 7702.
57. Shaner, N.C., Campbell, R.E., Steinbach, P.A., Giepmans, B.N., Palmer, A.E. Tsien, R.Y. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22 : 1567 1572.
58. Shohdy, N., Efe, J.A., Emr, S.D. Shuman, H.A. (2005) Pathogen effector protein screening in yeast identifies Legionella factors that interfere with membrane trafficking. Proc Natl Acad Sci USA 102 : 4866 4871.
59. Sieira, R., Comerci, D.J., Sanchez, D.O. Ugalde, R.A. (2000) A homologue of an operon required for DNA transfer in Agrobacterium is required in Brucella abortus for virulence and intracellular multiplication. J Bacteriol 182 : 4849 4855.
60. Sieira, R., Comerci, D.J., Pietrasanta, L.I. Ugalde, R.A. (2004) Integration host factor is involved in transcriptional regulation of the Brucella abortus virB operon. Mol Microbiol 54 : 808 822.
61. Sun, Y.H., Rolan, H.G. Tsolis, R.M. (2007) Injection of flagellin into the host cell cytosol by Salmonella enterica serotype Typhimurium. J Biol Chem 282 : 33897 33901.
62. Taminiau, B., Daykin, M., Swift, S., Boschiroli, M.L., Tibor, A., Lestrate, P., et al. (2002) Identification of a quorum-sensing signal molecule in the facultative intracellular pathogen Brucella melitensis. Infect Immun 70 : 3004 3011.
63. Thijs, I.M., De Keersmaecker, S.C., Fadda, A., Engelen, K., Zhao, H., McClelland, M., et al. (2007) Delineation of the Salmonella enterica serovar Typhimurium HilA regulon through genome-wide location and transcript analysis. J Bacteriol 189 : 4587 4596.
64. Uzureau, S., Godefroid, M., Deschamps, C., Lemaire, J., De Bolle, X. Letesson, J.J. (2007) Mutations of the quorum sensing-dependent regulator VjbR lead to drastic surface modifications in Brucella melitensis. J Bacteriol 189 : 6035 6047.
65. Vergunst, A.C., Schrammeijer, B., den Dulk-Ras, A., de Vlaam, C.M., Regensburg-Tuink, T.J. Hooykaas, P.J. (2000) VirB/D4-dependent protein translocation from Agrobacterium into plant cells. Science 290 : 979 982.
66. Vergunst, A.C., van Lier, M.C., den Dulk-Ras, A., Stuve, T.A., Ouwehand, A. Hooykaas, P.J. (2005) Positive charge is an important feature of the C-terminal transport signal of the VirB/D4-translocated proteins of Agrobacterium. Proc Natl Acad Sci USA 102 : 832 837.
67. Weiss, A.A., Johnson, F.D. Burns, D.L. (1993) Molecular characterization of an operon required for pertussis toxin secretion. Proc Natl Acad Sci USA 90 : 2970 2974.
68. White, C.E. Winans, S.C. (2007) The quorum-sensing transcription factor TraR decodes its DNA binding site by direct contacts with DNA bases and by detection of DNA flexibility. Mol Microbiol 64 : 245 256.
69. Worley, M.J., Ching, K.H. Heffron, F. (2000) Salmonella SsrB activates a global regulon of horizontally acquired genes. Mol Microbiol 36 : 749 761.
70. Zlokarnik, G., Negulescu, P.A., Knapp, T.E., Mere, L., Burres, N., Feng, L., et al. (1998) Quantitation of transcription and clonal selection of single living cells with beta-lactamase as reporter. Science 279 : 84 88.
71. Zusman, T., Aloni, G., Halperin, E., Kotzer, H., Degtyar, E., Feldman, M. Segal, G. (2007) The response regulator PmrA is a major regulator of the icm/dot type IV secretion system in Legionella pneumophila and Coxiella burnetii. Mol Microbiol 63 : 1508 1523.