Adaptation of the brucellae to their intracellular niche

Molecular Microbiology

Volumn 52, Issue 3, 2004, Pages 621-630

  Roop II, R Martin ^a   Bellaire, Bryan H ^b   Valderas, Michelle Wright ^a   Cardelli, James A ^b  

^a EAST CAROLINA UNIVERSITY   (United States)

^b LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,3 DIHYDROXYBENZOIC ACID; BACTERIUM LIPOPOLYSACCHARIDE;

ADAPTATION; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BRUCELLA; CELLULAR IMMUNITY; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE RESPONSE; INTRACELLULAR SPACE; MACROPHAGE; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PHAGOSOME; PRIORITY JOURNAL; SHORT SURVEY; SIGNAL TRANSDUCTION; TROPHOBLAST;

ADAPTATION, BIOLOGICAL; ANIMALS; BRUCELLACEAE; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; HYDROXYBENZOIC ACIDS; IRON; LIPOPOLYSACCHARIDES; MACROPHAGES; PHAGOSOMES; PREGNANCY; TROPHOBLASTS;

BACTERIA (MICROORGANISMS); BRUCELLA; MAMMALIA; NEGIBACTERIA;

EID: 2442626618     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2004.04017.x     Document Type: Short Survey

References (74)

1. Anderson, T.D., Cheville, N.F., and Meador, V.P. (1986) Pathogenesis of placentitis in the goat inoculated with Brucella abortus. II. Ultrastructural studies. Vet Pathol 23: 227-239.
2. Baldwin, C.L., and Roop, P.M., II (1999) Brucella infections and immunity. In Opportunistic Intracellular Pathogens and Immunity. Paradise, L.J., Friedman, H., and Bendinelli, M. (eds). New York: Plenum, pp. 255-279.
3. Bellaire, B.H., Elzer, P.H., Baldwin, C.L., and Roop, R.M., II (1999) The siderophore 2,3-dihydroxybenzoic acid is not required for virulence of Brucella abortus. BALB/c mice. Infect Immun 67: 2615-2618.
4. Bellaire, B.H., Elzer, P.M., Hagius, S., Walker, J., Baldwin, C.L., and Roop, R.M., II (2003a) Genetic organization and iron-responsive regulation of the Brucella abortus 2,3-dihydroxybenzoic acid biosynthesis operon, a cluster of gene required for wild-type virulence in pregnant cattle. Infect Immun 71: 1794-1803.
5. Bellaire, B.H., Elzer, P.H., Baldwin, C.L., and Roop, R.M., II (2003b) Production of the siderophore 2,3-dihydroxybenzoic acid is required for wild-type growth of Brucella abortus in the presence of erythritol under low-iron conditions in vitro. Infect Immun 71: 2927-2932.
6. Boschiroli, M.L., Foulongne, V., and O'Callaghan, D. (2001) Brucellosis: a worldwide zoonosis. Curr Opin Microbiol 4: 58-64.
7. 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.
8. Brown, L., and Elliott, T. (1996) Efficient translation of the RpoS sigma factor in Salmonella typhimurium requires host factor I, an RNA-binding protein encoded by the hfq gene. J Bacteriol 178: 3763-3770.
9. Celli, J., and Gorvel, J.-P. (2004) Organelle robbery: Brucella interactions with the endoplasmic reticulum. Curr Opin Microbiol 7: 1-5.
10. Celli, J., de Chastellier, C., Franchini, D.-M., Pizarro-Cerda, J., Moreno, E., and Gorvel, J.-P. (2003) Brucella evades macrophage killing via VirB-dependent sustained interactions with the endoplasmic reticulum. J Exp Med 198: 545-556.
11. Charles, T.C., and Nester, G.W. (1993) A chromosomally encoded two-component sensory transduction system is required for virulence of Agrobacterium tumefaciens. J Bacteriol 175: 6614-6625.
12. Cheng, H.-P., and Walker, G.C. (1998) Succinoglycan production by Rhizobium meliloti is regulated through the ExoS-Chvl two-component regulatory system. J Bacteriol 180: 20-26.
13. Cheville, N.F., Olsen, S.C., Jensen, A.E., Stevens, M.G., Florance, A.M., Houng, H.H., et al. (1996) Bacterial persistence and immunity in goats vaccinated with a purE deletion mutant or the parental 16M strain of Brucella melitensis. Infect Immun 64: 2431-2439.
14. Comerci, D.J., Martinez-Lorenzo, M.J., Sieria, R., Gorvel, J.P., and Ugalde, R.A. (2001) Essential role of the VirB machinery in the maturation of the Brucella abortus-containing vacuole. Cell Microbiol 3: 159-168.
15. Crawford, R.M., Van de Berg, L., Yuan, L., Hadfield, L., Warren, R.L., Drazek, E.S., et al. (1996) Deletion of purE attenuates Brucella melitensis infection in mice. Infect Immun 64: 2188-2192.
16. Davis, D.S., and Elzer, P.H. (2002) Brucella vaccines in wildlife. Vet Microbiol 90: 533-544.
17. Del Vecchio, V.G., Kapatral, V., Redkar, R.J., Patra, G., Mujer, C., Los, T., et al. (2002) The genome sequence of the facultative intracellular pathogen Brucella melitensis. Proc Natl Acad Sci USA 99: 443-448.
18. 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.
19. Drazek, E.S., Houng, H.S., Crawford, R.M., Hadfield, T.L., Hoover, D.L., and Warren, R.L. (1995) Deletion of purE attenuates Brucella melitensis 16M for growth in human monocyte-derived macrophages. Infect Immun 63: 3297-3301.
20. Endley, S., McMurray, D., and Ficht, T.A. (2001) Interruption of the cydB locus in Brucella abortus attenuates intracellular survival and virulence in the mouse model of infection. J Bacteriol 183: 2454-2462.
21. Enright, F.M. (1990) The pathogenesis and pathobiology of Brucella infections in domestic animals. In Animal Brucellosis. Nielsen, K.H., and Duncan, J.R. (eds). Boca Raton: CRC Press, pp. 301-320.
22. Eze, M.O., Yuan, L., Crawford, R.M., Paranavitana, C.M., Hadfleld, T.L., Bhattacharjee, A.K., et al. (2000) Effects of opsonization and gamma interferon on growth of Brucella melitensis 16M in mouse peritoneal macrophages in vitro. Infect Immun 68: 257-263.
23. Fernandez-Prada, C.M., Nikolich, M., Vemulapalli, R., Sriranganathan, N., Boyle, S.M., Schurig, G.G., et al. (2001) Deletion of wboA enhances activation of the lectin pathway of complement in Brucella abortus and Brucella melitensis. Infect Immun 69: 4407-4416.
24. 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.
25. 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.
26. Foulongne, V., Walravens, K., Bourg, G., Boschiroli, M.L., Godfroid, J., Ramuz, M., and O'Callaghan, D. (2001) Aromatic compound-dependent Brucella suis is attenuated in both cultured cells and mouse models. Infect Immun 69: 547-550.
27. Gagnon, E., Duclos, S., Rondeau, C., Chevet, E., Cameron, P.M., Steele-Mortimer, O., et al. (2002) Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 110: 119-131.
28. Goldman, B.S., Gabbert, K.K., and Kranz, R.G. (1996) G. The temperature-sensitive growth and survival phenotypes of Escherichia coli cydDC and cydAB strains are due to deficiencies in cytochrome bd and are corrected by exogenous catalase and reducing agents. J Bacteriol 178: 6348-6351.
29. González Carreró, M.I., Sangari, F.J., Agüero, J., and García Lobo, J.M. (2002) Brucella abortus strain 2308 produces brucebactin, a highly efficient catecholic siderophore. Microbiology 148: 353-360.
30. Guzmán-Verri, C., Chaves-Olarte, E., von Eichel-Streiber, C., López-Goñi, I., Thelestam, M., Arvidson, S., et al. (2001) GTPases of the Rho subfamily are required for Brucella abortus internalization in non-professional phagocytes: direct activation of Cdc42. J Biol Chem 276: 44435-44443.
31. Guzmán-Verri, C., Manterola, L., Sola-Landa, A., Parra, A., Cloeckart, 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: 123750-112380.
32. Hall, W.H. (1990) Modern chemotherapy for brucellosis in humans. Rev Infect Dis 12: 1060-1099.
33. Harmon, B.G., Adams, L.G., and Frey, M. (1988) Survival of rough and smooth strains of Brucella abortus in bovine mammary gland macrophages. Am J Vet Res 49: 1092-1097.
34. Hengge-Aronis, R. (1996) Regulation of gene expression during entry into stationary phase. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology. Neidhardt, F.C., Curtiss, R., III, Ingraham, J.L., Lin, E.C.C., Low, K.B., Maganasik, B., et al. (eds). Washington, DC: American Society for Microbiology Press, pp. 1497-1512.
35. Hong, P.C., Tsolis, R.M., and Ficht, T.A. (2000) Identification of genes required for chronic persistence of Brucella abortus in mice. Infect Immun 68: 4102-4107.
36. Jiang, X., and Baldwin, C.L. (1993a) Iron augments macrophage-mediated killing of Brucella abortus alone and in conjunction with interferon-γ. Cell Immunol 148: 397-407.
37. Jiang, X., and Baldwin, C.L. (1993b) Macrophage control of Brucella abortus: role of reactive oxygen intermediates and nitric oxide. Cell Immunol 151: 309-319.
38. 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.
39. Köhler, 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.
40. Köhler, S., Michaux-Charachon, S., Porte, F., Ramuz, M., and Liautard, J.P. (2003) What is the nature of the replicative niche of a stealthy bug named Brucella? Trends Microbiol 11: 215-219.
41. Lestrate, P., Delrue, R.-M., Danese, I., Didembourg, C., Tanimiau, B., Mertens, P., et al. (2000) Identification and characterization of in vivo attenuated mutants of Brucella melitensis. Mol Microbiol 38: 543-551.
42. 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 acute phase of infection in mice. Infect Immun 71: 7053-7060.
43. LeVier, K., Phillips, R.W., Grippe, V.K., Roop, R.M., II, and Walker, G.C. (2000) Similar requirements of a plant symbiont and a mammalian pathogen for prolonged intracellular survival. Science 287: 2492-2493.
44. Li, L., Jia, Y., Hou, Q., Charles, T.C., and Nester, G.W. (2002) A global pH sensor: Agrobacterium sensor protein ChvG regulates acid-inducible genes on its two chromosomes and Ti plasmid. Proc Natl Acad USA 99: 12369-12374.
45. López-Goñi, I., Moriyön, I., and Neilands, J.B. (1992) Identification of 2,3-dihydroxybenzoic acid as a Brucella abortus siderophore. Infect Immun 60: 4496-4503.
46. López-Goñi, I., Guzmán-Verri, C., Manterola, L., Sola-Landa, A., Moriyón, I., and Moreno, E. (2002) Regulation of Brucella virulence by the two-component system BvrR/BvrS. Vet Microbiol 90: 329-339.
47. Meador, V.P., and Deyoe, B.L. (1989) Intracellular localization of Brucella abortus in bovine placenta. Vet Pathol 26: 513-515.
48. Memish, Z., Mah, M.W., Al Mahmoud, S., Al Shaalan, M., and Khan, M.Y. (2000) Brucella bacteraemia: clinical and laboratory observations in 160 patients. J Infect 40: 59-63.
49. Meyer, M.E. (1967) Metabolic characterization of the genus Brucella. VI. Growth stimulation by i-erythritol compared with strain virulence for guinea pigs. J Bacteriol 93: 996-1000.
50. Moreno, E., and Moriyón, I. (2002) Brucella melitensis: a nasty bug with hidden credential for virulence. Proc Natl Acad Sci USA 99: 1-3.
51. S subunit of RNA polymerase in Escherichia coli. J Bacteriol 170: 297-300.
52. 1 in entry and short-term survival of Brucella suis in murine macrophages. Infect Immun 70: 1640-1644.
53. O'Callaghan, D., Cazevieille, C., Allardet-Servent, A., Boschiroli, M.L., Bourg, G., Foulongne, V., et al. (1999) A homologue of the Agrobacterium VirB and Bordetella pertussis PtI type IV secretion systems is essential for intracellular survival of Brucella suis. Mol Microbiol 33: 1210-1220.
54. Parent, M.A., Bellaire, B.H., Murphy, E.A., Roop, R.M., II, Elzer, P.M., and Baldwin, C.L. (2002) Brucella abortus siderophore 2,3-dihydroxybenzoic acid (DHBA) facilitates intracellular survival of the bacteria. Microb Pathog 32: 239-248.
55. 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.
56. Phillips, R.W., and Roop, R.M., II. (2001) The Brucella abortus HtrA functions as an authentic stress response protease but is not required for wild-type virulence in BALB/c mice. Infect Immun 69: 5911-5913.
57. Porte, F., Liautard, J.-P., and Köhler, S. (1999) Early acidification of phagosomes containing Brucella suis is essential for intracellular survival in murine macrophages. Infect Immun 67: 4041-4047.
58. Porte, F., Naroeni, A., Ouahrani-Bettache, S., and Liautard, J.-P. (2003) Role of the Brucella suis lipopolysaccharide O antigen in phagosomal genesis and in inhibition of phagosome-lysosome fusion in murine macrophages. Infect Immun 71: 1481-1490.
59. Price, R.E., Templeton, J.W., Smith, R., III, and Adams, L.G. (1990) Ability of mononuclear phagocytes from cattle naturally resistant or susceptible to brucellosis to control in vivo intracellular survival of Brucella abortus. Infect Immun 58: 879-886.
60. Rasool, O., Freer, E., Moreno, E., and Jarstrand, C. (1992) Effect of Brucella abortus lipopolysaccharide on oxidative metabolism and lysozyme release by human neutrophils. Infect Immun 60: 1699-1702.
61. Rest, R.F., and Robertson, D.C. (1975) Characterization of the electron transport system in Brucella abortus. J Bacteriol 122: 139-144.
62. 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.
63. Robertson, G.T., and Roop, R.M., II. (1999) The Brucella host factor I (HF-I) protein contributes to stress resistance during stationary phase and is a major determinant of virulence in mice. Mol Microbiol 34: 690-700.
64. Roop, R.M., II, Robertson, G.T., Ferguson, G.P., Milford, L.E., Winkler, M.E., and Walker, G.C. (2002) Seeking a niche: putative contributions of the hfq and bacA gene products to the successful adaptation of the brucellae to their intracellular home. Vet Microbiol 90: 349-364.
65. Roop, R.M., II, Gee, J.M., Robertson, G.T., Richardson, J.M., Ng, W.L., and Winkler, M.E. (2003) Brucella stationary phase gene expression and virulence. Annu Rev Microbiol 57: 57-76.
66. Sieira, R., Comerci, D.J., Sanchez, D.O., and Ugalde, R.A. (2000) A homologue of an operon required for DNA transfer in Agrobacterium is required in Brucella abortus for virulence and intracellular replication. J Bacteriol 182: 4849-4855.
67. Sledjeski, D.D., Whitman, C., and Zhang, A. (2001) Hfq is necessary for regulation by the untranslated RNA DsrA. J Bacteriol 183: 1997-2005.
68. Smith, H., Keppie, J., Pearce, J.H., Fuller, R., and Williams, A.E. (1961) The chemical basis of the virulence of Brucella abortus. I. Isolation of Br. abortus from bovine fetal tissue. Br J Exp Pathol 42: 631-637.
69. Smith, H., Williams, A.E., Pearce, J.H., Keppie, J., Harris-Smith, P.W., Fitzgeorge, R.B., and Witt, K. (1962) Foetal erythritol: a cause of the localization of Brucella abortus in bovine contagious abortion. Nature 193: 47-49.
70. Sola-Landa, A., Pizarro-Cerda, J., Grillo, M.J., Moreno, E., Moriyón, I., Blasco, J.M., et al. (1998) A two-component regulatory system playing a critical role in plant pathogens and endosymbionts is present in Brucella abortus and controls cell invasion and virulence. Mol Microbiol 29: 125-138.
71. Sperry, J.F., and Robertson, D.C. (1975) Erythritol catabolism by Brucella abortus. J Bacteriol 121: 619-630.
72. Ugalde, R.A. (1999) Intracellular lifestyle of Brucella spp. Common genes with other animal pathogens, plant pathogens and endosymbionts. Microb Infect 1: 1211-1219.
73. Watarai, M., Makino, S., Fujii, Y., Okamoto, K., and Shirahata, T. (2002) Modulation of Brucella-induced macropinocytosis by lipid rafts mediates intracellular replication. Cell Microbiol 4: 341-355.
74. Young, E.J. (2000) Brucella species. In Mandell, Douglas and Bennet's Principles and Practice of Infectious Disease, 5th edn. Mandell, G.L., Bennett, J.E., and Dolin, R. (eds). Philadelphia, PA: Churchill Livingstone, pp. 2386-2393.