The Brucella pathogens are polarized bacteria

Microbes and Infection

Volumn 15, Issue 14-15, 2013, Pages 998-1004

  Van Der Henst, Charles ^a   De Barsy, Marie ^b   Zorreguieta, Angeles ^c   Letesson, Jean Jacques ^d   De Bolle, Xavier ^d  

^a EPFL   (Switzerland)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c FUNDACIÓN INSTITUTO LELOIR   (Argentina)

^d UNIVERSITY OF NAMUR   (Belgium)

Author keywords

Adhesion; Brucella; Cell cycle; Growth; Host pathogen interaction; Polarity

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; BRUCELLA MONOMERIC AUTOTRANSPORTER PROTEIN; BRUCELLA TRIMERIC AUTOTRANSPORTER PROTEIN; CARRIER PROTEIN; DNA BINDING PROTEIN; ENZYME; PROTEIN AIDB; PROTEIN FUMC; PROTEIN HISTIDINE KINASE; PROTEIN PDHS; UNCLASSIFIED DRUG;

ARTICLE; ASYMMETRIC CELL DIVISION; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BRUCELLA; BRUCELLA ABORTUS; BRUCELLOSIS; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL POLARITY; CELL SYNCHRONIZATION; EHRLICHIA CHAFFEENSIS; HOST PATHOGEN INTERACTION; HUMAN; INNATE IMMUNITY; LIFE CYCLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SCANNING ELECTRON MICROSCOPY;

BRUCELLA;

ADHESION; BRUCELLA; CELL CYCLE; GROWTH; HOST-PATHOGEN INTERACTION; POLARITY;

ADHESINS, BACTERIAL; ANIMALS; ASYMMETRIC CELL DIVISION; BACTERIAL PROTEINS; BRUCELLA; BRUCELLOSIS; CELL CYCLE; DNA REPAIR; FLAGELLA; HOST-PATHOGEN INTERACTIONS; HUMANS;

EID: 84889096255     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2013.10.008     Document Type: Article

References (60)

1. Anderson T.D., Cheville N.F., Meador V.P. Pathogenesis of placentitis in the goat inoculated with Brucella abortus. II. Ultrastructural studies. Vet. Pathol. 1986, 23:227-239.
2. Archambaud C., Salcedo S.P., Lelouard H., Devilard E., de Bovis B., Van Rooijen N., Gorvel J.P., Malissen B. Contrasting roles of macrophages and dendritic cells in controlling initial pulmonary Brucella infection. Eur. J. Immunol. 2010, 40:3458-3471.
3. Batut J., Andersson S.G., O'Callaghan D. The evolution of chronic infection strategies in the alpha-proteobacteria. Nat. Rev. Microbiol. 2004, 2:933-945.
4. Boschiroli M.L., Foulongne V., O'Callaghan D. Brucellosis: a worldwide zoonosis. Curr. Opin. Microbiol. 2001, 4:58-64.
5. Boschiroli M.L., Ouahrani-Bettache S., Foulongne V., Michaux-Charachon S., Bourg G., Allardet-Servent A., Cazevieille C., Lavigne J.P., Liautard J.P., Ramuz M., O'Callaghan D. Type IV secretion and Brucella virulence. Vet. Microbiol. 2002, 90:341-348.
6. Brilli M., Fondi M., Fani R., Mengoni A., Ferri L., Bazzicalupo M., Biondi E.G. The diversity and evolution of cell cycle regulation in alpha-proteobacteria: a comparative genomic analysis. BMC Syst. Biol. 2010, 4:52.
7. Brown P.J., de Pedro M.A., Kysela D.T., Van der Henst C., Kim J., De Bolle X., Fuqua C., Brun Y.V. Polar growth in the alphaproteobacterial order Rhizobiales. Proc. Natl. Acad. Sci. USA 2012, 109:1697-1701.
8. Castaneda-Roldan E.I., Avelino-Flores F., Dall'Agnol M., Freer E., Cedillo L., Dornand J., Giron J.A. Adherence of Brucella to human epithelial cells and macrophages is mediated by sialic acid residues. Cell Microbiol. 2004, 6:435-445.
9. Castaneda-Roldan E.I., Ouahrani-Bettache S., Saldana Z., Avelino F., Rendon M.A., Dornand J., Giron J.A. Characterization of SP41, a surface protein of Brucella associated with adherence and invasion of host epithelial cells. Cell Microbiol. 2006, 8:1877-1887.
10. Celli J., Salcedo S.P., Gorvel J.P. Brucella coopts the small GTPase Sar1 for intracellular replication. Proc. Natl. Acad. Sci. USA 2005, 102:1673-1678.
11. Cheng Z., Miura K., Popov V.L., Kumagai Y., Rikihisa Y. Insights into the CtrA regulon in development of stress resistance in obligatory intracellular pathogen Ehrlichia chaffeensis. Mol. Microbiol. 2011, 82:1217-1234.
12. Cornelis P. Peculiarities of the regulation of the Brucella flagellum. Microbiology 2011, 157:1251-1252.
13. Czibener C., Ugalde J.E. Identification of a unique gene cluster of Brucella spp. that mediates adhesion to host cells. Microbes Infect. Inst. Pasteur 2012, 14:79-85.
14. Dotreppe D., Mullier C., Letesson J.J., De Bolle X. The alkylation response protein AidB is localized at the new poles and constriction sites in Brucella abortus. BMC Microbiol. 2011, 11:257.
15. Dricot A., Rual J.F., Lamesch P., Bertin N., Dupuy D., Hao T., Lambert C., Hallez R., Delroisse J.M., Vandenhaute J., Lopez-Goni I., Moriyon I., Garcia-Lobo J.M., Sangari F.J., Macmillan A.P., Cutler S.J., Whatmore A.M., Bozak S., Sequerra R., Doucette-Stamm L., Vidal M., Hill D.E., Letesson J.J., De Bolle X. Generation of the Brucella melitensis ORFeome version 1.1. Genome Res. 2004, 14:2201-2206.
16. Enright F.M., Araya L.N., Elzer P.H., Rowe G.E., Winter A.J. Comparative histopathology in BALB/c mice infected with virulent and attenuated strains of Brucella abortus. Vet. Immunol. Immunopathol. 1990, 26:171-182.
17. Errington J. Septation and chromosome segregation during sporulation in Bacillus subtilis. Curr. Opin. Microbiol. 2001, 4:660-666.
18. Evinger M., Agabian N. Envelope-associated nucleoid from Caulobacter crescentus stalked and swarmer cells. J. Bacteriol. 1977, 132:294-301.
19. Ferooz J., Letesson J.J. Morphological analysis of the sheathed flagellum of Brucella melitensis. BMC Res. Notes 2010, 3:333.
20. Fretin D., Fauconnier A., Kohler S., Halling S., Leonard S., Nijskens C., Ferooz J., Lestrate P., Delrue R.M., Danese I., Vandenhaute J., Tibor A., DeBolle X., Letesson J.J. The sheathed flagellum of Brucella melitensis is involved in persistence in a murine model of infection. Cell Microbiol. 2005, 7:687-698.
21. Gay B., Mauss H., Sanchez-Teff S. Identification of fibronectins in peritoneal macrophages during the phagocytosis of Brucella. An immunocytochemical study by electron microscopy. Virchows Archiv. B Cell Pathol. Incl. Mol. Pathol. 1986, 52:169-176.
22. Goley E.D., Iniesta A.A., Shapiro L. Cell cycle regulation in Caulobacter: location, location, location. J. Cell Sci. 2007, 120:3501-3507.
23. Hallez R., Bellefontaine A.F., Letesson J.J., De Bolle X. Morphological and functional asymmetry in alpha-proteobacteria. Trends Microbiol. 2004, 12:361-365.
24. Hallez R., Mignolet J., Van Mullem V., Wery M., Vandenhaute J., Letesson J.J., Jacobs-Wagner C., De Bolle X. The asymmetric distribution of the essential histidine kinase PdhS indicates a differentiation event in Brucella abortus. EMBO J. 2007, 26:1444-1455.
25. Hoch J.A. Two-component and phosphorelay signal transduction. Curr. Opin. Microbiol. 2000, 3:165-170.
26. Kohler S., Foulongne V., Ouahrani-Bettache S., Bourg G., Teyssier J., Ramuz M., Liautard J.P. The analysis of the intramacrophagic virulome of Brucella suis deciphers the environment encountered by the pathogen inside the macrophage host cell. Proc. Natl. Acad. Sci. USA 2002, 99:15711-15716.
27. Kumagai Y., Cheng Z., Lin M., Rikihisa Y. Biochemical activities of three pairs of Ehrlichia chaffeensis two-component regulatory system proteins involved in inhibition of lysosomal fusion. Infect. Immun. 2006, 74:5014-5022.
28. Lawler M.L., Brun Y.V. Advantages and mechanisms of polarity and cell shape determination in Caulobacter crescentus. Curr. Opin. Microbiol. 2007, 10:630-637.
29. Matroule J.Y., Lam H., Burnette D.T., Jacobs-Wagner C. Cytokinesis monitoring during development; rapid pole-to-pole shuttling of a signaling protein by localized kinase and phosphatase in Caulobacter. Cell 2004, 118:579-590.
30. Maurin M. Brucellosis at the dawn of the 21st century. Med. Mal. Infect. 2005, 35:6-16.
31. Merker R.I., Smit J. Characterization of the adhesive holdfast of marine and freshwater caulobacters. Appl. Environ. Microbiol. 1988, 54:2078-2085.
32. Mignolet J., Van der Henst C., Nicolas C., Deghelt M., Dotreppe D., Letesson J.J., De Bolle X. PdhS, an old-pole-localized histidine kinase, recruits the fumarase FumC in Brucella abortus. J. Bacteriol. 2010, 192:3235-3239.
33. Moreno E., Stackebrandt E., Dorsch M., Wolters J., Busch M., Mayer H. Brucella abortus 16S rRNA and lipid A reveal a phylogenetic relationship with members of the alpha-2 subdivision of the class Proteobacteria. J. Bacteriol. 1990, 172:3569-3576.
34. Paulsen I.T., Seshadri R., Nelson K.E., Eisen J.A., Heidelberg J.F., Read T.D., Dodson R.J., Umayam L., Brinkac L.M., Beanan M.J., Daugherty S.C., Deboy R.T., Durkin A.S., Kolonay J.F., Madupu R., Nelson W.C., Ayodeji B., Kraul M., Shetty J., Malek J., Van Aken S.E., Riedmuller S., Tettelin H., Gill S.R., White O., Salzberg S.L., Hoover D.L., Lindler L.E., Halling S.M., Boyle S.M., Fraser C.M. The Brucella suis genome reveals fundamental similarities between animal and plant pathogens and symbionts. Proc. Natl. Acad. Sci. USA 2002, 99:13148-13153.
35. Pizarro-Cerda J., Cossart P. Bacterial adhesion and entry into host cells. Cell 2006, 124:715-727.
36. Pizarro-Cerda J., Meresse S., Parton R.G., van der Goot G., Sola-Landa A., Lopez-Goni I., Moreno E., Gorvel J.P. Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes. Infect. Immun. 1998, 66:5711-5724.
37. Pizarro-Cerdá J., Moreno E., Gorvel J.P. Brucella abortus: invasion and survival within professional and non-professional phagocytes. Phagocytosis and Pathogens 1999, vol. 6:201-232. JAI Press, Greenwich, CT. A. Tartakoff, S. Gordon (Eds.).
38. Porte F., Liautard J.P., Kohler S. Early acidification of phagosomes containing Brucella suis is essential for intracellular survival in murine macrophages. Infection and Immunity 1999, 67:4041-4047.
39. Posadas D.M., Ruiz-Ranwez V., Bonomi H.R., Martin F.A., Zorreguieta A. BmaC, a novel autotransporter of Brucella suis, is involved in bacterial adhesion to host cells. Cell Microbiol. 2012, 14:965-982.
40. Purcell E.B., Boutte C.C., Crosson S. Two-component signaling systems and cell cycle control in Caulobacter crescentus. Adv. Exp. Med. and Biol. 2008, 631:122-130.
41. Quon K.C., Marczynski G.T., Shapiro L. Cell cycle control by an essential bacterial two-component signal transduction protein. Cell 1996, 84:83-93.
42. Rikihisa Y. Anaplasma phagocytophilum and Ehrlichia chaffeensis: subversive manipulators of host cells. Nat. Rev. Microbiol. 2010, 8:328-339.
43. Rippa V., Amoresano A., Esposito C., Landini P., Volkert M., Duilio A. Specific DNA binding and regulation of its own expression by the AidB protein in Escherichia coli. J. Bacteriol. 2010, 192:6136-6142.
44. Ruiz-Ranwez V., Posadas D.M., Van der Henst C., Estein S.M., Arocena G.M., Abdian P.L., Martin F.A., Sieira R., De Bolle X., Zorreguieta A. BtaE, an adhesin that belongs to the trimeric autotransporter family, is required for full virulence and defines a specific adhesive pole of Brucella suis. Infection and Immunity 2013, 81:996-1007.
45. Sadowski C., Wilson D., Schallies K., Walker G., Gibson K.E. The Sinorhizobium meliloti sensor histidine kinase CbrA contributes to free-living cell cycle regulation. Microbiology 2013, 159:1552-1563.
46. Salcedo S.P., Chevrier N., Lacerda T.L., Ben Amara A., Gerart S., Gorvel V.A., de Chastellier C., Blasco J.M., Mege J.L., Gorvel J.P. Pathogenic brucellae replicate in human trophoblasts. J. Infect. Dis. 2013, 207:1075-1083.
47. Sallstrom B., Andersson S.G. Genome reduction in the alpha-Proteobacteria. Curr. Opin. Microbiol. 2005, 8:579-585.
48. Samartino L.E., Enright F.M. Pathogenesis of abortion of bovine brucellosis. Comp. Immunol. Microbiol. Infect. Dis. 1993, 16:95-101.
49. Skerker J.M., Laub M.T. Cell-cycle progression and the generation of asymmetry in Caulobacter crescentus. Nat. Rev. Microbiol. 2004, 2:325-337.
50. Starr T., Child R., Wehrly T.D., Hansen B., Hwang S., Lopez-Otin C., Virgin H.W., Celli J. Selective subversion of autophagy complexes facilitates completion of the Brucella intracellular cycle. Cell Host Microbe 2012, 11:33-45.
51. Starr T., Ng T.W., Wehrly T.D., Knodler L.A., Celli J. Brucella intracellular replication requires trafficking through the late endosomal/lysosomal compartment. Traffic 2008, 9:678-694.
52. Terwagne M., Ferooz J., Rolan H.G., Sun Y.H., Atluri V., Xavier M.N., Franchi L., Nunez G., Legrand T., Flavell R.A., De Bolle X., Letesson J.J., Tsolis R.M. Innate immune recognition of flagellin limits systemic persistence of Brucella. Cell Microbiol. 2013, 15:942-960.
53. Teyssier C., Marchandin H., Jumas-Bilak E. The genome of alpha-proteobacteria: complexity, reduction, diversity and fluidity. Can. J. Microbiol. 2004, 50:383-396.
54. Tomlinson A.D., Fuqua C. Mechanisms and regulation of polar surface attachment in Agrobacterium tumefaciens. Curr. Opin. Microbiol. 2009, 12:708-714.
55. Van der Henst C., Beaufay F., Mignolet J., Didembourg C., Colinet J., Hallet B., Letesson J.J., De Bolle X. The histidine kinase PdhS controls cell cycle progression of the pathogenic alphaproteobacterium Brucella abortus. J. Bacteriol. 2012, 194:5305-5314.
56. Van der Henst C., Charlier C., Deghelt M., Wouters J., Matroule J.Y., Letesson J.J., De Bolle X. Overproduced Brucella abortus PdhS-mCherry forms soluble aggregates in Escherichia coli, partially associating with mobile foci of IbpA-YFP. BMC Microbiol. 2010, 10:248.
57. Volkert M.R., Nguyen D.C. Induction of specific Escherichia coli genes by sublethal treatments with alkylating agents. Proc. Natl. Acad. Sci. USA 1984, 81:4110-4114.
58. von Bargen K., Gorvel J.P., Salcedo S.P. Internal affairs: investigating the Brucella intracellular lifestyle. FEMS Microbiol. Rev. 2012, 36:533-562.
59. Woods S.A., Schwartzbach S.D., Guest J.R. Two biochemically distinct classes of fumarase in Escherichia coli. Biochim. Biophys. Acta 1988, 954:14-26.
60. Zygmunt M.S., Hagius S.D., Walker J.V., Elzer P.H. Identification of Brucella melitensis 16M genes required for bacterial survival in the caprine host. Microbes Infect. Inst. Pasteur 2006, 8:2849-2854.