The sheathed flagellum of Brucella melitensis is involved in persistence in a murine model of infection

Cellular Microbiology

Volumn 7, Issue 5, 2005, Pages 687-698

  Fretin, D ^a,e   Fauconnier, A ^b   Kohler S ^c   Halling, S ^d   Leonard S ^a   Nijskens, C ^a   Ferooz, J ^a   Lestrate, P ^a   Delrue, R M ^a   Danese, I ^e   Vandenhaute, J ^a   Tibor, A ^a   DeBolle, X ^a   Letesson, Jean Jacques ^a  

^a UNIVERSITY OF NAMUR   (Belgium)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^c INSERM   (France)

^d NATIONAL ANIMAL DISEASE CENTER   (United States)

^e Ctr d'Etud Rech Veterinaires A   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL GENE; BACTERIAL VIRULENCE; BRUCELLA MELITENSIS; BRUCELLOSIS; CHRONIC DISEASE; CONTROLLED STUDY; GENE EXPRESSION; GENE MUTATION; HUMAN; HUMAN CELL; INFECTION; MOUSE; NONHUMAN; PERSISTENT INFECTION; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; BACTERIAL PROTEINS; BRUCELLA MELITENSIS; BRUCELLOSIS; CATTLE; CELL LINE; CLONING, MOLECULAR; FEMALE; FLAGELLA; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICROSCOPY, ELECTRON, TRANSMISSION; MUTATION; PROMOTER REGIONS (GENETICS); VIRULENCE FACTORS;

EID: 20244378676     PISSN: 14625814     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2005.00502.x     Document Type: Article

References (74)

1. Abdallah, A.I., Commander, N.J., Woodward, M.J., Spencer, S., Hart, C.A., and Winstanley, C. (2003) Type III secretion homologs are present in Brucella melitensis, B. ovis, and B. suis biovars 1, 2, and 3. Curr Microbiol 46: 241-245.
2. Aldridge, P., and Hughes, K.T. (2002) Regulation of flagellar assembly. Curr Opin Microbiol 5: 160-165.
3. Alton, G.G., Jones, L.M., and Pietz, D.E. (1975) Laboratory techniques in brucellosis, 2nd ed. Monograph Series Number 55. Geneva: World Health Organization.
4. Anderson, P.E., and Gober, J.W. (2000) FlbT, the posttranscriptional regulator of flagellin synthesis in Caulobacter crescentus, interacts with the 5′ untranslated region of flagellin mRNA. Mol Microbiol 38: 41-52.
5. Armitage, J. P. (2004) Bacterial Behavior. New York: Springer-Verlag.
6. Ausubel, F.M. (1989) Current Protocols in Molecular Biology. New York: John Wiley & Sons.
7. Barnett, M.J., Fisher, R.F., Jones, T., Komp, C., Abola, A.P., Barloy-Hubler, F., et al. (2001) Nucleotide sequence and predicted functions of the entire Sinorhizobium meliloti pSymA megaplasmid. Proc Natl Acad Sci USA 98: 9883-9888.
8. Bellefontaine, A.F., Pierreux, C.E., Mertens, P., Vandenhaute, J., Letesson, J.J., and De Bolle, X. (2002) Plasticity of a transcriptional regulation network among alpha-proteobacteria is supported by the identification of CtrA targets in Brucella abortus. Mol Microbiol 43: 945-960.
9. Blocker, A., Komoriya, K., and Aizawa, S. (2003) Type III secretion systems and bacterial flagella: insights into their function from structural similarities. Proc Natl Acad Sci USA 100: 3027-3030.
10. Boschiroli, M.L., Ouahrani-Bettache, S., Foulongne, V., Michaux-Charachon, S., Bourg, G., Allardet-Servent, A., et al. (2002) Type IV secretion and Brucella virulence. Vet Microbiol 90: 341-348.
11. Byrne, B., and Swanson, M.S. (1998) Expression of Legionella pneumophila virulence traits in response to growth conditions. Infect Immun 66: 3029-3034.
12. Capela, D., Barloy-Hubler, F., Gouzy, J., Bothe, G., Ampe, F., Batut, J., et al. (2001) Analysis of the chromosome sequence of the legume symbiont Sinorhizobium meliloti strain 1021. Proc Natl Acad Sci USA 98: 9877-9882.
13. Cloeckaert, A., de Wergifosse, P., Dubray, G., and Limet, J. N. (1990) Identification of seven surface-exposed Brucella outer membrane proteins by use of monoclonal antibodies: immunogold labeling for electron microscopy and enzyme-linked immunosorbent assay. Infect Immun 58: 3980-3987.
14. Cloeckaert, A., Zygmunt, M.S., Dubray, G., and Limet, J.N. (1993) Characterization of O-polysaccharide specific monoclonal antibodies derived from mice infected with the rough Brucella melitensis strain B115. J Gen Microbiol 139: 1551-1556.
15. DelVecchio, V.G., Kapatral, V., Elzer, P., Patra, G., and Mujer, C.V. (2002) The genome of Brucella melitensis. Vet Microbiol 90: 587-592.
16. 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.
17. Denoel, P.A., Vo, T.K., Tibor, A., Weynants, V.E., Trunde, J.M., Dubray, G., et al. (1997) Characterization, occurrence, and molecular cloning of a 39-kilodalton Brucella abortus cytoplasmic protein immunodominant in cattle. Infect Immun 65: 495-502.
18. Dietrich, C., Heuner, K., Brand, B.C., Hacker, J., and Steinert, M. (2001) Flagellum of Legionella pneumophila positively affects the early phase of infection of eukaryotic host cells. Infect Immun 69: 2116-2122.
19. Eggenhofer, E., Haslbeck, M., and Scharf, B. (2004) MotE serves as a new chaperone specific for the periplasmic motility protein, MotC, in Sinorhizobium meliloti. Mol Microbiol 52: 701-712.
20. Elzer, P.H., Phillips, R.W., Kovach, M.E., Peterson, K.M., and Roap, R.M. (1994) Characterization and genetic complementation of a Brucella abortus high-temperature-requirement A (htrA) deletion mutant. Infect Immun 62: 4135-4139.
21. Ficht, T.A. (2003) Intracellular survival of Brucella: defining the link with persistence. Vet Microbiol 92: 213-223.
22. Finan, T.M., Weidner, S., Wong, K., Buhrmester, J., Chain, P., Vorholter, F.J., et al. (2001) The complete sequence of the 1,683-kb pSymB megaplasmid from the N2-fixing endosymbiont Sinorhizobium meliloti. Proc Natl Acad Sci USA 98: 9889-9894.
23. Forestier, C., Deleuil, F., Lapaque, N., Moreno, E., and Gorvel, J.P. (2000) Brucella abortus lipopolysaccharide in murine peritoneal macrophages acts as a down-regulator of T cell activation. J Immunol 165: 5202-5210.
24. Foulongne, V., Bourg, G., Cazevieille, C., Michaux-Charachon, S., and O'Callaghan, D. (2000) Identification of Brucella suis genes affecting intracellular survival in an in vitro human macrophage infection model by signature-tagged transposon mutagenesis. Infect Immun 68: 1297-1303.
25. Fuerst, J.A., and Perry, J.W. (1988) Demonstration of lipopolysaccharide on sheathed flagella of Vibrio cholerae O:1 by protein A-gold immunoelectron microscopy. J Bacteriol 170: 1488-1494.
26. Galibert, F., Finan, T.M., Long, S.R., Puhler, A., Abola, P., Ampe, F., et al. (2001) The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293: 668-672.
27. Ghelardi, E., Celandroni, F., Salvetti, S., Beecher, D.J., Gominet, M., Lereclus, D., et al. (2002) Requirement of flhA for swarming differentiation, flagellin export, and secretion of virulence-associated proteins in Bacillus thuringiensis. J Bacteriol 184: 6424-6433.
28. Godfroid, F., Taminiau, B., Danese, I., Denoel, P., Tibor, A., Weynants, V., et al. (1998) Identification of the perosamine synthetase gene of Brucella melitensis 16M and involvement of lipopolysaccharide O side chain in Brucella survival in mice and in macrophages. Infect Immun 66: 5485-5493.
29. Guzman-Verri, C., Manterola, L., Sola-Landa, A., Parra, A., Cloeckaert, A., Garin, J., et al. (2002) The two-component system BvrR/BvrS essential for Brucella abortus virulence regulates the expression of outer membrane proteins with counterparts in members of the Rhizobiaceae. Proc Natl Acad Sci USA 99: 12375-12380.
30. Hallez, R., Bellefontaine, B., Letesson, J.J., and De Bolle, X. (2004) Morphological and functional asymmetry in α-proteobacteria. Trends Microbiol 12: 361-365.
31. Halling, S.M. (1998) On the presence and organization of open reading frames of the nonmotile pathogen Brucella abortus similar to class II, III, and IV flagellar genes and to LcrD virulence superfamily. Microb Comp Genomics 3: 21-29.
32. Hauwaerts, D., Alexandre, G., Das, S.K., Vanderleyden, J., and Zhulin, I.B. (2002) A major chemotaxis gene cluster in Azospirillum brasilense and relationships between chemotaxis operons in alpha-proteobacteria. FEMS Microbiol Lett 208: 61-67.
33. Hernandez, F., and Monge-Najera, J. (1994) Ultrastructure of the bacteria Campylobacter and Helicobacter: implications for the phylogeny of mammal gastric bacteria. Rev Biol Trop 42 Suppl. 2): 85-92.
34. Jacobs, M., Brown, N., Allie, N., Gulert, R., and Ryffel, B. (2000) Increased resistance to mycobacterial infection in the absence of interleukin-10. Immunology 100: 494-501.
35. Jenal, U., and Shapiro, L. (1996) Cell cycle-controlled proteolysis of a flagellar motor protein that is asymmetrically distributed in the Caulobacter predivisional cell. EMBO J 15: 2393-2406.
36. Jones, B.D., Lee, C.A., and Falkow, S. (1992) Invasion by Salmonella typhimurium is affected by the direction of flagellar rotation. Infect Immun 60: 2475-2480.
37. Josenhans, C., and Suerbaum, S. (2002) The role of motility as a virulence factor in bacteria. Int J Med Microbiol 291: 605-614.
38. Jubier-Maurin, V., Boigegrain, R.A., Cloeckaert, A., Gross, A., Alvarez-Martinez, M.T., Terraza, A., et al. (2001) Major outer membrane protein Omp25 of Brucella suis is involved in inhibition of tumor necrosis factor alpha production during infection of human macrophages. Infect Immun 69: 4823-4830.
39. Kaneko, T., Nakamura, Y., Sato, S., Asamizu, E., Kato, T., Sasamoto, S., et al. (2000a) Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res 7: 331-338.
40. Kaneko, T., Nakamura, Y., Sato, S., Asamizu, E., Kato, T., Sasamoto, S., et al. (2000b) Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti (supplement). DNA Res 7: 381-406.
41. Karlin, S., Barnett, M.J., Campbell, A.M., Fisher, R.F., and Mrazek, J. (2003) Predicting gene expression levels from codon biases in alpha-proteobacterial genomes. Proc Natl Acad Sci USA 100: 7313-7318.
42. Kim, S., Watarai, M., Kondo, Y., Erdenebaatar, J., Makino, S., and Shirahata, T. (2003) Isolation and characterization of mini-Tn5Km2 insertion mutants of Brucella abortus deficient in internalization and intracellular growth in HeLa cells. Infect Immun 71: 3020-3027.
43. Kohler, S., Ouahrani-Bettache, S., Layssac, M., Teyssier, J., and Liautard, J.P. (1999) Constitutive and inducible expression of green fluorescent protein in Brucella suis. Infect Immun 67: 6695-6697.
44. Kohler, S., Foulongne, V., Ouahrani-Bettache, S., Bourg, G., Teyssier, J., Ramuz, M., and Liautard, J.P. (2002) 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 99: 15711-15716.
45. Larsen, M.H., and Boesen, H.T. (2001) Role of flagellum and chemotactic motility of Vibrio anguillarum for phagocytosis by and intracellular survival in fish macrophages. FEMS Microbiol Lett 203: 149-152.
46. Lestrate, P., Delrue, R.M., Danese, I., Didembourg, C., Taminiau, B., Mertens, P., et al. (2000) Identification and characterization of in vivo attenuated mutants of Brucella melitensis. Mol Microbiol 38: 543-551.
47. Lestrate, P., Dricot, A., Delrue, R.M., Lambert, C., Martinelli, V., De Bolle, X., et al. (2003) Attenuated signature-tagged mutagenesis mutants of Brucella melitensis identified during the acute phase of infection in mice. Infect Immun 71: 7053-7060.
48. Lorenz, M.C., and Fink, G.R. (2002) Life and death in a macrophage: role of the glyoxylate cycle in virulence. Eukaryot Cell 1: 657-662.
49. Macnab, R.M. (2003) How bacteria assemble flagella. Annu Rev Microbiol 57: 77-100.
50. Meador, V.P., Tabatabai, L.B., Hagemoser, W.A., and Deyoe, B.L. (1986) Identification of Brucella abortus in formalin-fixed, paraffin-embedded tissues of cows, goats, and mice with an avidin-biotin-peroxidase complex immunoenzymatic staining technique. Am J Vet Res 47: 2147-2150.
51. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
52. Moreno, E., and Moriyon, I. (2002) Brucella melitensis: a nasty bug with hidden credentials for virulence. Proc Natl Acad Sci USA 99: 1-3.
53. Paulsen, I.T., Seshadri, R., Nelson, K.E., Eisen, J.A., Heidelberg, J.F., Read, T.D., 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.
54. Platzer, J., Sterr, W., Hausmann, M., and Schmitt, R. (1997) Three genes of a motility operon and their role in flagellar rotary speed variation in Rhizobium meliloti. J Bacteriol 179: 6391-6399.
55. Ramos, H.C., Rumbo, M., and Sirard, J.C. (2004) Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol 12: 509-517.
56. Rittig, M.G., Alvarez-Martinez, M.T., Porte, F., Liautard, J.P., and Rouot, B. (2001) Intracellular survival of Brucella spp. in human monocytes involves conventional uptake but special phagosomes. Infect Immun 69: 3995-4006.
57. Salgado, H., Moreno-Hagelsieb, G., Smith, T.F., and Collado-Vides, J. (2000) Operons in Escherichia coli: genomic analyses and predictions. Proc Natl Acad Sci USA 97: 6652-6657.
58. Scharf, B., and Schmitt, R. (2002) Sensory transduction to the flagellar motor of Sinorhizobium meliloti. J Mol Microbiol Biotechnol 4: 183-186.
59. Scharf, B., Schuster-Wolff-Buhring, H., Rachel, R., and Schmitt, R. (2001) Mutational analysis of the Rhizobium lupini H13-3 and Sinorhizobium meliloti flagellin genes: importance of flagellin A for flagellar filament structure and transcriptional regulation. J Bacteriol 183: 5334-5342.
60. Scott, C.C., Botelho, R.J., and Grinstein, S. (2003) Phagosome maturation: a few bugs in the system. J Membr Biol 193: 137-152.
61. Simon, R., Priefer, U., and Pühler, A. (1983) A broad host range mobilisation system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Biotechnology 10: 783-791.
62. Song, Y.C., Jin, S., Louie, H., Ng, D., Lau, R., Zhang, Y., et al. (2004) FlaC, a protein of Campylobacter jejuni TGH9011 (ATCC43431) secreted through the flagellar apparatus, binds epithelial cells and influences cell invasion. Mol Microbiol 53: 541-553.
63. Sourjik, V., Sterr, W., Platzer, J., Bos, I., Haslbeck, M., and Schmitt, R. (1998) Mapping of 41 chemotaxis, flagellar and motility genes to a single region of the Sinorhizobium meliloti chromosome. Gene 223: 283-290.
64. Soutourina, O.A., and Bertin, P.N. (2003) Regulation cascade of flagellar expression in Gram-negative bacteria. FEMS Microbiol Rev 27: 505-523.
65. Stabel, J.R., and Stabel, T.J. (1995) Immortalization and characterization of bovine peritoneal macrophages transfected with SV40 plasmid DNA. Vet Immunol Immunopathol 45: 211-220.
66. Szurmant, H., and Ordal, G.W. (2004) Diversity in chemotaxis mechanisms among the Bacteria and Archaea. Microbiol Mol Biol Rev 68: 301-319.
67. Thomashow, M.F., and Cotter, T.W. (1992) Bdellovibrio host dependence: the search for signal molecules and genes that regulate the intraperiplasmic growth cycle. J Bacteriol 174: 5767-5771.
68. Thomashow, L.S., and Rittenberg, S.C. (1985) Isolation and composition of sheathed flagella from Bdellovibrio bacteriovorus 109J. J Bacteriol 163: 1047-1054.
69. Tibor, A., Wansard, V., Bielartz, V., Delrue, R.M., Danese, I., Michel, P., et al. (2002) Effect of omp10 or omp19 deletion on Brucella abortus outer membrane properties and virulence in mice. Infect Immun 70: 5540-5546.
70. Tominaga, A., Mahmoud, M.A., Mukaihara, T., and Enomoto, M. (1994) Molecular characterization of intact, but cryptic, flagellin genes in the genus Shigella. Mol Microbiol 12: 277-285.
71. Umelo, E., and Trust, T.J. (1997) Identification and molecular characterization of two tandemly located flagellin genes from Aeromonas salmonicida A449. J Bacteriol 179: 5292-5299.
72. Weber, I., Fritz, C., Ruttkowski, S., Kreft, A., and Bange, F.C. (2000) Anaerobic nitrate reductase (narGHJI) activity of Mycobacterium bovis BCG in vitro and its contribution to virulence in immunodeficient mice. Mol Microbiol 35: 1017-1025.
73. Yanagi, M., and Yamasato, K. (1993) Phylogenetic analysis of the family Rhizobiaceae and related bacteria by sequencing of 16S rRNA gene using PCR and DNA sequencer. FEMS Microbiol Lett 107: 115-120.
74. Young, G.M., Schmiel, D.H., and Miller, V.L. (1999) A new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein-secretion system. Proc Natl Acad Sci USA 96: 6456-6461.