Skip to main content
Top
Published in: Medical Microbiology and Immunology 4/2009

01-11-2009 | Review

Survival of the fittest: how Brucella strains adapt to their intracellular niche in the host

Authors: R. Martin Roop II, Jennifer M. Gaines, Eric S. Anderson, Clayton C. Caswell, Daniel W. Martin

Published in: Medical Microbiology and Immunology | Issue 4/2009

Login to get access

Abstract

Brucella strains produce abortion and infertility in their natural hosts and a zoonotic disease in humans known as undulant fever. These bacteria do not produce classical virulence factors, and their capacity to successfully survive and replicate within a variety of host cells underlies their pathogenicity. Extensive replication of the brucellae in placental trophoblasts is associated with reproductive tract pathology in natural hosts, and prolonged persistence in macrophages leads to the chronic infections that are a hallmark of brucellosis in both natural hosts and humans. This review describes how Brucella strains have efficiently adapted to their intracellular lifestyle in the host.
Literature
1.
go back to reference Alcantara RB, Read RD, Valderas MW, Brown TD, Roop RM II (2004) Intact purine biosynthesis pathways are required for wild-type virulence of Brucella abortus 2308 in the BALB/c mouse model. Infect Immun 72:4911–4917PubMedCrossRef Alcantara RB, Read RD, Valderas MW, Brown TD, Roop RM II (2004) Intact purine biosynthesis pathways are required for wild-type virulence of Brucella abortus 2308 in the BALB/c mouse model. Infect Immun 72:4911–4917PubMedCrossRef
2.
go back to reference Alexander B, Schnurrenberger PR, Brown RR (1981) Numbers of Brucella abortus in the placenta, umbilicus and fetal fluid of two naturally infected cows. Vet Rec 108:500PubMed Alexander B, Schnurrenberger PR, Brown RR (1981) Numbers of Brucella abortus in the placenta, umbilicus and fetal fluid of two naturally infected cows. Vet Rec 108:500PubMed
3.
go back to reference Allen CA, Adams LG, Ficht TA (1998) Transposon-derived Brucella abortus rough mutants are attenuated and exhibit reduced intracellular survival. Infect Immun 66:1008–1016PubMed Allen CA, Adams LG, Ficht TA (1998) Transposon-derived Brucella abortus rough mutants are attenuated and exhibit reduced intracellular survival. Infect Immun 66:1008–1016PubMed
4.
go back to reference Almirón M, Martínez M, Sanjuan N, Ugalde RA (2001) Ferrochelatase is present in Brucella abortus and is critical for its intracellular survival and virulence. Infect Immun 69:6225–6230PubMedCrossRef Almirón M, Martínez M, Sanjuan N, Ugalde RA (2001) Ferrochelatase is present in Brucella abortus and is critical for its intracellular survival and virulence. Infect Immun 69:6225–6230PubMedCrossRef
5.
go back to reference Alton GG (1990) Brucella melitensis. In: Nielsen K, Duncan JR (eds) Animal brucellosis. CRC, Boca Raton, pp 383–409 Alton GG (1990) Brucella melitensis. In: Nielsen K, Duncan JR (eds) Animal brucellosis. CRC, Boca Raton, pp 383–409
6.
go back to reference Alton GG (1990) Brucella suis. In: Nielsen K, Duncan JR (eds) Animal brucellosis. CRC, Boca Raton, pp 411–422 Alton GG (1990) Brucella suis. In: Nielsen K, Duncan JR (eds) Animal brucellosis. CRC, Boca Raton, pp 411–422
7.
go back to reference Anderson ES, Paulley JT, Gaines JM, Valderas MW, Martin DW, Menscher E, Brown TD, Burns CS, Roop RM II (2009) The manganese transporter MntH is a critical virulence determinant for Brucella abortus 2308 in experimentally infected mice. Infect Immun 77:3466–3474PubMedCrossRef Anderson ES, Paulley JT, Gaines JM, Valderas MW, Martin DW, Menscher E, Brown TD, Burns CS, Roop RM II (2009) The manganese transporter MntH is a critical virulence determinant for Brucella abortus 2308 in experimentally infected mice. Infect Immun 77:3466–3474PubMedCrossRef
8.
go back to reference Arenas GN, Staskevich AS, Aballay J, Mayorga LS (2000) Intracellular trafficking of Brucella abortus in J774 macrophages. Infect Immun 68:4255–4263PubMedCrossRef Arenas GN, Staskevich AS, Aballay J, Mayorga LS (2000) Intracellular trafficking of Brucella abortus in J774 macrophages. Infect Immun 68:4255–4263PubMedCrossRef
9.
go back to reference Arenas-Gamboa AM, Ficht TA, Kahl-McDonagh MM, Rice-Ficht AC (2008) Immunization with a single dose of a microencapsulated Brucella melitensis mutant enhances protection against wild-type challenge. Infect Immun 76:2448–2455PubMedCrossRef Arenas-Gamboa AM, Ficht TA, Kahl-McDonagh MM, Rice-Ficht AC (2008) Immunization with a single dose of a microencapsulated Brucella melitensis mutant enhances protection against wild-type challenge. Infect Immun 76:2448–2455PubMedCrossRef
10.
go back to reference Arrelano-Reynoso B, Lapaque N, Salcedo S, Briones G, Ciocchini AE, Ugalde R, Moreno E, Moriyón I, Gorvel JP (2005) Cyclic β-1, 2-glucan is a Brucella virulence factor required for intracellular survival. Nat Immunol 6:618–625CrossRef Arrelano-Reynoso B, Lapaque N, Salcedo S, Briones G, Ciocchini AE, Ugalde R, Moreno E, Moriyón I, Gorvel JP (2005) Cyclic β-1, 2-glucan is a Brucella virulence factor required for intracellular survival. Nat Immunol 6:618–625CrossRef
11.
go back to reference Bahlawane C, McIntosh M, Krol E, Becker A (2008) Sinorhizobium meliloti regulator MucR couples exopolysaccharide synthesis and motility. Mol Plant Microbe Interact 21:1498–1509PubMedCrossRef Bahlawane C, McIntosh M, Krol E, Becker A (2008) Sinorhizobium meliloti regulator MucR couples exopolysaccharide synthesis and motility. Mol Plant Microbe Interact 21:1498–1509PubMedCrossRef
12.
13.
go back to reference Bandara AB, Contreras A, Contreras-Rodriguez A, Martins AM, Dobrean V, Poff-Richow S, Rajasekaran P, Sriranganathan N, Schurig GG, Boyle SM (2007) Brucella suis urease encoded by ure1 but not ure2 is necessary for intestinal infection of BALB/c mice. BMC Microbiol 7:57PubMedCrossRef Bandara AB, Contreras A, Contreras-Rodriguez A, Martins AM, Dobrean V, Poff-Richow S, Rajasekaran P, Sriranganathan N, Schurig GG, Boyle SM (2007) Brucella suis urease encoded by ure1 but not ure2 is necessary for intestinal infection of BALB/c mice. BMC Microbiol 7:57PubMedCrossRef
14.
go back to reference Barquero-Calvo E, Chaves-Olarte E, Weiss DS, Guzmán-Verri C, Chacón-Díaz C, Rucavado A, Moriyón I, Moreno E (2007) Brucella abortus uses a stealthy strategy to avoid activation of the innate immune system during the onset of infection. PLoS ONE 7:e631CrossRef Barquero-Calvo E, Chaves-Olarte E, Weiss DS, Guzmán-Verri C, Chacón-Díaz C, Rucavado A, Moriyón I, Moreno E (2007) Brucella abortus uses a stealthy strategy to avoid activation of the innate immune system during the onset of infection. PLoS ONE 7:e631CrossRef
15.
go back to reference Barquero-Calvo E, Conde-Alvarez R, Chacón-Díaz C, Quesada-Lobo L, Martirosyan A, Guzmán-Verri C, Iriarte M, Mancek-Keber M, Jerala R, Gorvel JP, Moriyón I, Moreno E, Chaves-Olarte E (2009) The differential interaction of Brucella and Ochrobactrum with innate immunity reveals traits related to the evolution of stealthy pathogens. PLoS ONE 4:e5893PubMedCrossRef Barquero-Calvo E, Conde-Alvarez R, Chacón-Díaz C, Quesada-Lobo L, Martirosyan A, Guzmán-Verri C, Iriarte M, Mancek-Keber M, Jerala R, Gorvel JP, Moriyón I, Moreno E, Chaves-Olarte E (2009) The differential interaction of Brucella and Ochrobactrum with innate immunity reveals traits related to the evolution of stealthy pathogens. PLoS ONE 4:e5893PubMedCrossRef
16.
go back to reference Batut J, Andersson SGE, O’Callaghan D (2004) The evolution of chronic infection strategies in the α-proteobacteria. Nat Rev Microbiol 2:933–945PubMedCrossRef Batut J, Andersson SGE, O’Callaghan D (2004) The evolution of chronic infection strategies in the α-proteobacteria. Nat Rev Microbiol 2:933–945PubMedCrossRef
17.
go back to reference Bellaire BH, Elzer PH, Baldwin CL, Roop RM II (1999) The siderophore 2, 3-dihydroxybenzoic acid is not required for virulence of Brucella abortus in BALB/c mice. Infect Immun 67:2615–2618PubMed Bellaire BH, Elzer PH, Baldwin CL, Roop RM II (1999) The siderophore 2, 3-dihydroxybenzoic acid is not required for virulence of Brucella abortus in BALB/c mice. Infect Immun 67:2615–2618PubMed
18.
go back to reference Bellaire BH, Elzer PH, Hagius S, Walker J, Baldwin CL, Roop RM II (2003) Genetic organization and iron-responsive regulation of the Brucella abortus 2, 3-dihydoxybenzoic acid biosynthesis operon, a cluster of genes required for wild-type virulence in pregnant cattle. Infect Immun 71:1794–1803PubMedCrossRef Bellaire BH, Elzer PH, Hagius S, Walker J, Baldwin CL, Roop RM II (2003) Genetic organization and iron-responsive regulation of the Brucella abortus 2, 3-dihydoxybenzoic acid biosynthesis operon, a cluster of genes required for wild-type virulence in pregnant cattle. Infect Immun 71:1794–1803PubMedCrossRef
19.
go back to reference Bellaire BH, Elzer PH, Baldwin CL, Roop RM II (2003) 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 71:2927–2932PubMedCrossRef Bellaire BH, Elzer PH, Baldwin CL, Roop RM II (2003) 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 71:2927–2932PubMedCrossRef
20.
go back to reference Bellaire BH, Roop RM II, Cardelli JA (2005) Opsonized virulent Brucella abortus replicates within nonacidic, endoplasmic reticulum-negative, LAMP-1-positive phagosomes in human monocytes. Infect Immun 73:3702–3713PubMedCrossRef Bellaire BH, Roop RM II, Cardelli JA (2005) Opsonized virulent Brucella abortus replicates within nonacidic, endoplasmic reticulum-negative, LAMP-1-positive phagosomes in human monocytes. Infect Immun 73:3702–3713PubMedCrossRef
21.
go back to reference Billard E, Cazevieille C, Dornand J, Gross A (2005) High susceptibility of human dendritic cells to invasion by the intracellular pathogens Brucella suis, B. abortus and B. melitensis. Infect Immun 73:8418–8424PubMedCrossRef Billard E, Cazevieille C, Dornand J, Gross A (2005) High susceptibility of human dendritic cells to invasion by the intracellular pathogens Brucella suis, B. abortus and B. melitensis. Infect Immun 73:8418–8424PubMedCrossRef
22.
go back to reference Billard E, Dornand J, Gross A (2007) Brucella suis prevents human dendritic cell maturation and antigen presentation through regulation of tumor necrosis factor alpha secretion. Infect Immun 75:4980–4989PubMedCrossRef Billard E, Dornand J, Gross A (2007) Brucella suis prevents human dendritic cell maturation and antigen presentation through regulation of tumor necrosis factor alpha secretion. Infect Immun 75:4980–4989PubMedCrossRef
23.
go back to reference Blasco JM (2003) Epididymite contagieuse du belier ou infection à Brucella ovis. In: Lefevre PC, Blancou J, Chermette R (eds) Principales maladies infectieuses et parasitaires du bétail. Lavoiser, Paris, pp 905–917 Blasco JM (2003) Epididymite contagieuse du belier ou infection à Brucella ovis. In: Lefevre PC, Blancou J, Chermette R (eds) Principales maladies infectieuses et parasitaires du bétail. Lavoiser, Paris, pp 905–917
24.
go back to reference Boschiroli ML, Ouahrani-Bettache S, Foulongne V, Michaux-Charachon S, Bourg G, Allardet-Servent A, Cazevieille C, Liautard JP, Ramuz M, O’Callaghan D (2002) The Brucella suis virB operon is induced intracellularly in macrophages. Proc Natl Acad Sci USA 99:1544–1549PubMedCrossRef Boschiroli ML, Ouahrani-Bettache S, Foulongne V, Michaux-Charachon S, Bourg G, Allardet-Servent A, Cazevieille C, Liautard JP, Ramuz M, O’Callaghan D (2002) The Brucella suis virB operon is induced intracellularly in macrophages. Proc Natl Acad Sci USA 99:1544–1549PubMedCrossRef
25.
go back to reference Boussau B, Karlberg EO, Frank AC, Legault BA, Andersson SGE (2004) Computational inference of scenarios for α-proteobacterial genome evolution. Proc Natl Acad Sci USA 101:9722–9727PubMedCrossRef Boussau B, Karlberg EO, Frank AC, Legault BA, Andersson SGE (2004) Computational inference of scenarios for α-proteobacterial genome evolution. Proc Natl Acad Sci USA 101:9722–9727PubMedCrossRef
26.
go back to reference Briones G, Iñón de Iannino N, Roset M, Vigliocco A, Paulo PS, Ugalde RA (2001) Brucella abortus cyclic α-1, 2-glucan mutants have reduced virulence in mice and are defective in intracellular replication in HeLa cells. Infect Immun 69:4528–4535PubMedCrossRef Briones G, Iñón de Iannino N, Roset M, Vigliocco A, Paulo PS, Ugalde RA (2001) Brucella abortus cyclic α-1, 2-glucan mutants have reduced virulence in mice and are defective in intracellular replication in HeLa cells. Infect Immun 69:4528–4535PubMedCrossRef
27.
go back to reference Brown TD (2007) The glutamate decarboxylase genes, gadBC, are not required for Brucella abortus resistance to low pH or virulence in the mouse model. MS thesis, East Carolina University Brown TD (2007) The glutamate decarboxylase genes, gadBC, are not required for Brucella abortus resistance to low pH or virulence in the mouse model. MS thesis, East Carolina University
28.
go back to reference Bryk R, Griffin P, Nathan C (2000) Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407:211–215PubMedCrossRef Bryk R, Griffin P, Nathan C (2000) Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407:211–215PubMedCrossRef
29.
go back to reference Burkhardt S, Jiménez de Bagüés MP, Liautard JP, Köhler S (2005) Analysis of the behavior of eryC mutants of Brucella suis attenuated in macrophages. Infect Immun 73:6782–6790PubMedCrossRef Burkhardt S, Jiménez de Bagüés MP, Liautard JP, Köhler S (2005) Analysis of the behavior of eryC mutants of Brucella suis attenuated in macrophages. Infect Immun 73:6782–6790PubMedCrossRef
30.
31.
go back to reference Castanie-Cornet MP, Penfound TA, Smith D, Elliott JF, Foster JW (1999) Control of acid resistance in Escherichia coli. J Bacteriol 181:3525–3535PubMed Castanie-Cornet MP, Penfound TA, Smith D, Elliott JF, Foster JW (1999) Control of acid resistance in Escherichia coli. J Bacteriol 181:3525–3535PubMed
32.
go back to reference Celli J, de Chastellier C, Franchini DM, Pizarro-Cerda J, Moreno E, Gorvel JP (2003) Brucella evades macrophage killing via VirB-dependent sustained interactions with the endoplasmic reticulum. J Exp Med 198:545–556PubMedCrossRef Celli J, de Chastellier C, Franchini DM, Pizarro-Cerda J, Moreno E, Gorvel JP (2003) Brucella evades macrophage killing via VirB-dependent sustained interactions with the endoplasmic reticulum. J Exp Med 198:545–556PubMedCrossRef
33.
go back to reference Cellier MF, Courville P, Campion C (2007) Nramp1 phagocytic intracellular metal withdrawal defense. Microbes Infect 9:1662–1670PubMedCrossRef Cellier MF, Courville P, Campion C (2007) Nramp1 phagocytic intracellular metal withdrawal defense. Microbes Infect 9:1662–1670PubMedCrossRef
34.
go back to reference Charles TC, Nester EW (1993) A chromosomally encoded two-component sensory transduction system is required for virulence of Agrobacterium tumefaciens. J Bacteriol 175:6614–6625PubMed Charles TC, Nester EW (1993) A chromosomally encoded two-component sensory transduction system is required for virulence of Agrobacterium tumefaciens. J Bacteriol 175:6614–6625PubMed
35.
go back to reference Chen H, Gao K, Kondrosi E, Kondrosi A, Rolfe BG (2005) Functional genomic analysis of global regulator NolR in Sinorhizobium meliloti. Mol Plant Microbe Interact 18:1340–1352PubMedCrossRef Chen H, Gao K, Kondrosi E, Kondrosi A, Rolfe BG (2005) Functional genomic analysis of global regulator NolR in Sinorhizobium meliloti. Mol Plant Microbe Interact 18:1340–1352PubMedCrossRef
36.
go back to reference Cheng HP, Walker GC (1998) Succinoglycan production by Rhizobium meliloti is regulated through the ExoS-ChvI two-component regulatory system. J Bacteriol 180:20–26PubMed Cheng HP, Walker GC (1998) Succinoglycan production by Rhizobium meliloti is regulated through the ExoS-ChvI two-component regulatory system. J Bacteriol 180:20–26PubMed
37.
go back to reference Cheville NF, Jensen AE, Halling SM, Tatum FM, Morfitt DC, Hennager SG, Frerichs WM, Schurig G (1992) Bacterial survival, lymph node changes, and immunologic responses of cattle vaccinated with standard and mutant strains of Brucella abortus. Am J Vet Res 53:1881–1888PubMed Cheville NF, Jensen AE, Halling SM, Tatum FM, Morfitt DC, Hennager SG, Frerichs WM, Schurig G (1992) Bacterial survival, lymph node changes, and immunologic responses of cattle vaccinated with standard and mutant strains of Brucella abortus. Am J Vet Res 53:1881–1888PubMed
38.
go back to reference Cheville NF, Olsen SC, Jensen AE, Stevens MG, Florance AM, Houng HSH, Drazek ES, Warren RL, Hadfield TL, Hoover DL (1996) Bacterial persistence and immunity in goats vaccinated with a purE deletion mutant or the parental 16M strain of Brucella melitensis. Infect Immun 64:2431–2439PubMed Cheville NF, Olsen SC, Jensen AE, Stevens MG, Florance AM, Houng HSH, Drazek ES, Warren RL, Hadfield TL, Hoover DL (1996) Bacterial persistence and immunity in goats vaccinated with a purE deletion mutant or the parental 16M strain of Brucella melitensis. Infect Immun 64:2431–2439PubMed
39.
go back to reference Cirl C, Wieser A, Yadav M, Duerr S, Schubert S, Fischer H, Stappert D, Wantia N, Rodriguez N, Wagner H, Svanborg C, Miethke T (2008) Subversion of Toll-like receptor signaling by a unique family of bacterial Toll/interleukin-1 receptor domain-containing proteins. Nat Med 14:399–406PubMedCrossRef Cirl C, Wieser A, Yadav M, Duerr S, Schubert S, Fischer H, Stappert D, Wantia N, Rodriguez N, Wagner H, Svanborg C, Miethke T (2008) Subversion of Toll-like receptor signaling by a unique family of bacterial Toll/interleukin-1 receptor domain-containing proteins. Nat Med 14:399–406PubMedCrossRef
40.
go back to reference Comerci DJ, Martinez-Lorenzo MJ, Sieira R, Gorvel JP, Ugalde RA (2001) Essential role of the VirB machinery in the maturation of the Brucella abortus-containing vacuole. Cell Microbiol 3:159–168PubMedCrossRef Comerci DJ, Martinez-Lorenzo MJ, Sieira R, Gorvel JP, Ugalde RA (2001) Essential role of the VirB machinery in the maturation of the Brucella abortus-containing vacuole. Cell Microbiol 3:159–168PubMedCrossRef
41.
go back to reference Comerci DJ, Altabe S, de Mendoza D, Ugalde RA (2006) Brucella abortus synthesizes phosphatidylcholine from choline provided by the host. J Bacteriol 188:1929–1934PubMedCrossRef Comerci DJ, Altabe S, de Mendoza D, Ugalde RA (2006) Brucella abortus synthesizes phosphatidylcholine from choline provided by the host. J Bacteriol 188:1929–1934PubMedCrossRef
42.
go back to reference Conde-Alvarez R, Grilló MJ, Salcedo SP, de Miguel MJ, Fugier E, Gorvel JP, Moriyón I, Iriarte M (2006) Synthesis of phosphatidylcholine, a typical eukaryotic phospholipid, is necessary for full virulence of the intracellular bacterial parasite Brucella abortus. Cell Microbiol 8:1322–1335PubMedCrossRef Conde-Alvarez R, Grilló MJ, Salcedo SP, de Miguel MJ, Fugier E, Gorvel JP, Moriyón I, Iriarte M (2006) Synthesis of phosphatidylcholine, a typical eukaryotic phospholipid, is necessary for full virulence of the intracellular bacterial parasite Brucella abortus. Cell Microbiol 8:1322–1335PubMedCrossRef
43.
go back to reference Conover GM, Martinez-Morales F, Heidtman MI, Luo ZQ, Tang M, Chen C, Geiger O, Isberg RR (2008) Phosphatidylcholine synthesis is required for optimal functions of Legionella pneumophila virulence determinants. Cell Microbiol 10:514–528PubMed Conover GM, Martinez-Morales F, Heidtman MI, Luo ZQ, Tang M, Chen C, Geiger O, Isberg RR (2008) Phosphatidylcholine synthesis is required for optimal functions of Legionella pneumophila virulence determinants. Cell Microbiol 10:514–528PubMed
45.
go back to reference Crawford RM, van der Verg L, Yuan L, Hadfield TL, Warren RL, Drazek ES, Houng HSH, Hammack C, Sasala K, Polsinelli T, Thompson J, Hoover DL (1996) Deletion of purE attenuates Brucella melitensis in mice. Infect Immun 64:2188–2192PubMed Crawford RM, van der Verg L, Yuan L, Hadfield TL, Warren RL, Drazek ES, Houng HSH, Hammack C, Sasala K, Polsinelli T, Thompson J, Hoover DL (1996) Deletion of purE attenuates Brucella melitensis in mice. Infect Immun 64:2188–2192PubMed
46.
go back to reference Crawford RP, Huber JD, Adams BS (1990) Epidemiology and surveillance. In: Nielsen K, Duncan JR (eds) Animal brucellosis. CRC, Boca Raton, pp 131–151 Crawford RP, Huber JD, Adams BS (1990) Epidemiology and surveillance. In: Nielsen K, Duncan JR (eds) Animal brucellosis. CRC, Boca Raton, pp 131–151
47.
go back to reference Crichton RR, Wilmet S, Legssyer R, Ward RJ (2002) Molecular and cellular mechanisms of iron homeostasis and toxicity in mammalian cells. J Inorg Biochem 91:9–18PubMedCrossRef Crichton RR, Wilmet S, Legssyer R, Ward RJ (2002) Molecular and cellular mechanisms of iron homeostasis and toxicity in mammalian cells. J Inorg Biochem 91:9–18PubMedCrossRef
48.
go back to reference Dawson CE, Stubberfield EJ, Perrett LL, King AC, Whatmore AM, Bashiruddin JB, Stack JA, MacMillan AP (2008) Phenotypic and molecular characterization of Brucella isolates from marine mammals. BMC Microbiol 8:224PubMedCrossRef Dawson CE, Stubberfield EJ, Perrett LL, King AC, Whatmore AM, Bashiruddin JB, Stack JA, MacMillan AP (2008) Phenotypic and molecular characterization of Brucella isolates from marine mammals. BMC Microbiol 8:224PubMedCrossRef
49.
go back to reference de Jong MF, Sun YH, den Hartigh AB, van Dijl JM, Tsolis RM (2008) Identification of VceA and VceC, two members of the VjbR regulon that are translocated into macrophages by the Brucella type IV secretion system. Mol Microbiol 70:1378–1396PubMedCrossRef de Jong MF, Sun YH, den Hartigh AB, van Dijl JM, Tsolis RM (2008) Identification of VceA and VceC, two members of the VjbR regulon that are translocated into macrophages by the Brucella type IV secretion system. Mol Microbiol 70:1378–1396PubMedCrossRef
50.
go back to reference Delrue RM, Martinez-Lorenzo M, Lestrate P, Danese I, Bielarz V, Mertens P, de Bolle X, Tibor A, Gorvel JP, Letesson JJ (2001) Identification of Brucella spp. genes involved in intracellular trafficking. Cell Microbiol 3:487–497PubMedCrossRef Delrue RM, Martinez-Lorenzo M, Lestrate P, Danese I, Bielarz V, Mertens P, de Bolle X, Tibor A, Gorvel JP, Letesson JJ (2001) Identification of Brucella spp. genes involved in intracellular trafficking. Cell Microbiol 3:487–497PubMedCrossRef
51.
go back to reference Delrue RM, Deschamps C, Leonard S, Nijksens C, Danese I, Schaus JM, Bonnot S, Ferooz J, Tibor A, de Bolle X, Letesson JJ (2005) A quorum-sensing regulator controls expression of both the type IV secretion system and the flagellar apparatus of Brucella melitensis. Cell Microbiol 7:1151–1161PubMedCrossRef Delrue RM, Deschamps C, Leonard S, Nijksens C, Danese I, Schaus JM, Bonnot S, Ferooz J, Tibor A, de Bolle X, Letesson JJ (2005) A quorum-sensing regulator controls expression of both the type IV secretion system and the flagellar apparatus of Brucella melitensis. Cell Microbiol 7:1151–1161PubMedCrossRef
52.
go back to reference Detilleux PG, Deyoe BL, Cheville NF (1990) Entry and intracellular localization of Brucella spp. in Vero cells: fluorescence and electron microscopy. Vet Pathol 27:317–328PubMedCrossRef Detilleux PG, Deyoe BL, Cheville NF (1990) Entry and intracellular localization of Brucella spp. in Vero cells: fluorescence and electron microscopy. Vet Pathol 27:317–328PubMedCrossRef
53.
go back to reference Detilleux PG, Deyoe BL, Cheville NF (1991) Effect of endocytic and metabolic inhibitors on the internalization and intracellular growth of Brucella abortus in Vero cells. Am J Vet Res 52:1658–1664PubMed Detilleux PG, Deyoe BL, Cheville NF (1991) Effect of endocytic and metabolic inhibitors on the internalization and intracellular growth of Brucella abortus in Vero cells. Am J Vet Res 52:1658–1664PubMed
54.
go back to reference D’mello R, Hill S, Poole RK (1996) The cytochrome bd quinol oxidase in Escherichia coli has an extremely high oxygen affinity and two oxygen-binding haems: implications for regulation of activity in vivo by oxygen inhibition. Microbiology 142:755–763PubMedCrossRef D’mello R, Hill S, Poole RK (1996) The cytochrome bd quinol oxidase in Escherichia coli has an extremely high oxygen affinity and two oxygen-binding haems: implications for regulation of activity in vivo by oxygen inhibition. Microbiology 142:755–763PubMedCrossRef
55.
go back to reference Dozot M, Boigegrain RA, Delrue RM, Hallez R, Ouahrani-Bettache S, Danese I, Letesson JJ, de Bolle X, Köhler S (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 8:1791–1802PubMedCrossRef Dozot M, Boigegrain RA, Delrue RM, Hallez R, Ouahrani-Bettache S, Danese I, Letesson JJ, de Bolle X, Köhler S (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 8:1791–1802PubMedCrossRef
56.
go back to reference Drazek ES, Houng HSH, Crawford RM, Hadfield TL, Hoover DL, Warren RL (1995) Deletion of purE attenuates Brucella melitensis 16M for growth in human monocyte-derived macrophages. Infect Immun 63:3297–3301PubMed Drazek ES, Houng HSH, Crawford RM, Hadfield TL, Hoover DL, Warren RL (1995) Deletion of purE attenuates Brucella melitensis 16M for growth in human monocyte-derived macrophages. Infect Immun 63:3297–3301PubMed
57.
go back to reference Dylan T, Ielpi L, Stanfield S, Kashyap L, Douglas C, Yanofsky M, Nester EW, Helinski DR, Ditta G (1986) Rhizobium meliloti genes required for nodule development are related to chromosomal virulence genes in Agrobacterium tumefaciens. Proc Natl Acad Sci USA 83:4403–4407PubMedCrossRef Dylan T, Ielpi L, Stanfield S, Kashyap L, Douglas C, Yanofsky M, Nester EW, Helinski DR, Ditta G (1986) Rhizobium meliloti genes required for nodule development are related to chromosomal virulence genes in Agrobacterium tumefaciens. Proc Natl Acad Sci USA 83:4403–4407PubMedCrossRef
58.
go back to reference Elzer PH, Enright FM, McQuiston JR, Boyle SM, Schurig GG (1998) Evaluation of a rough mutant of Brucella melitensis in pregnant goats. Res Vet Sci 64:259–260PubMedCrossRef Elzer PH, Enright FM, McQuiston JR, Boyle SM, Schurig GG (1998) Evaluation of a rough mutant of Brucella melitensis in pregnant goats. Res Vet Sci 64:259–260PubMedCrossRef
59.
go back to reference Endley S, McMurray D, Ficht TA (2001) Interruption of the cydB locus in Brucella abortus attenuates intracellular survival and virulence in the mouse model of infection. J Bacteriol 183:2454–2462PubMedCrossRef Endley S, McMurray D, Ficht TA (2001) Interruption of the cydB locus in Brucella abortus attenuates intracellular survival and virulence in the mouse model of infection. J Bacteriol 183:2454–2462PubMedCrossRef
60.
go back to reference Enright FM (1990) The pathogenesis and pathobiology of Brucella infection in domestic animals. In: Nielsen K, Duncan JR (eds) Animal brucellosis. CRC, Boca Raton, pp 301–320 Enright FM (1990) The pathogenesis and pathobiology of Brucella infection in domestic animals. In: Nielsen K, Duncan JR (eds) Animal brucellosis. CRC, Boca Raton, pp 301–320
61.
go back to reference Essenberg RC, Seshadri R, Nelson K, Paulsen I (2002) Sugar metabolism by brucellae. Vet Microbiol 90:249–261PubMedCrossRef Essenberg RC, Seshadri R, Nelson K, Paulsen I (2002) Sugar metabolism by brucellae. Vet Microbiol 90:249–261PubMedCrossRef
62.
go back to reference Fang FC (2004) Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat Rev Microbiol 2:820–832PubMedCrossRef Fang FC (2004) Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat Rev Microbiol 2:820–832PubMedCrossRef
63.
go back to reference Ferguson GP, Datta A, Baumgartner J, Roop RM II, Carlson RW, Walker GC (2004) Similarity to peroxisomal-membrane protein family reveals that Sinorhizobium and Brucella BacA affect lipid-A fatty acids. Proc Natl Acad Sci USA 101:5012–5017PubMedCrossRef Ferguson GP, Datta A, Baumgartner J, Roop RM II, Carlson RW, Walker GC (2004) Similarity to peroxisomal-membrane protein family reveals that Sinorhizobium and Brucella BacA affect lipid-A fatty acids. Proc Natl Acad Sci USA 101:5012–5017PubMedCrossRef
64.
go back to reference Ferrero MC, Fossati CA, Baldi PC (2009) Smooth Brucella strains invade and replicate in human lung epithelial cells without inducing cell death. Microbes Infect 11:476–483PubMedCrossRef Ferrero MC, Fossati CA, Baldi PC (2009) Smooth Brucella strains invade and replicate in human lung epithelial cells without inducing cell death. Microbes Infect 11:476–483PubMedCrossRef
65.
go back to reference Forestier C, Moreno E, Pizarro-Cerda J, Gorvel JP (1999) Lysosomal accumulation and recycling of lipopolysaccharide to the cell surface of murine macrophages, an in vitro and in vivo study. J Immunol 162:6784–6791PubMed Forestier C, Moreno E, Pizarro-Cerda J, Gorvel JP (1999) Lysosomal accumulation and recycling of lipopolysaccharide to the cell surface of murine macrophages, an in vitro and in vivo study. J Immunol 162:6784–6791PubMed
66.
go back to reference Forestier C, Deleuil F, Lapaque N, Moreno E, Gorvel JP (2000) Brucella abortus lipopolysaccharide in murine peritoneal macrophages acts as a down-regulator of T cell activation. J Immunol 165:5202–5210PubMed Forestier C, Deleuil F, Lapaque N, Moreno E, Gorvel JP (2000) Brucella abortus lipopolysaccharide in murine peritoneal macrophages acts as a down-regulator of T cell activation. J Immunol 165:5202–5210PubMed
67.
go back to reference Foulongne V, Bourg G, Cazevieille C, Michaux-Charachon S, 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 68:1297–1303PubMedCrossRef Foulongne V, Bourg G, Cazevieille C, Michaux-Charachon S, 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 68:1297–1303PubMedCrossRef
68.
go back to reference Foulongne V, Walravens K, Bourg G, Boschiroli ML, Godfroid J, Ramuz M, O’Callaghan D (2001) Aromatic compound-dependent Brucella suis is attenuated in both cultured cells and mouse models. Infect Immun 69:547–550PubMedCrossRef Foulongne V, Walravens K, Bourg G, Boschiroli ML, Godfroid J, Ramuz M, O’Callaghan D (2001) Aromatic compound-dependent Brucella suis is attenuated in both cultured cells and mouse models. Infect Immun 69:547–550PubMedCrossRef
69.
go back to reference Franz DR, Jahrling PB, Friedlander AM, McClain DJ, Hoover DL, Bryne WR, Pavlin JA, Christopher GW, Eitzen EM (1997) Clinical recognition and management of patients exposed to biological warfare agents. JAMA 278:399–411PubMedCrossRef Franz DR, Jahrling PB, Friedlander AM, McClain DJ, Hoover DL, Bryne WR, Pavlin JA, Christopher GW, Eitzen EM (1997) Clinical recognition and management of patients exposed to biological warfare agents. JAMA 278:399–411PubMedCrossRef
70.
go back to reference Fretin D, Fauconnier A, Köhler S, Halling S, Leonard S, Nisjkens C, Ferooz J, Lestrate P, Delrue RM, Danese I, Vandenhaute J, Tibor A, de Bolle X, Letesson JJ (2005) The sheathed flagellum of Brucella melitensis is involved in persistence in a murine model of infection. Cell Microbiol 7:687–698PubMedCrossRef Fretin D, Fauconnier A, Köhler S, Halling S, Leonard S, Nisjkens C, Ferooz J, Lestrate P, Delrue RM, Danese I, Vandenhaute J, Tibor A, de Bolle X, Letesson JJ (2005) The sheathed flagellum of Brucella melitensis is involved in persistence in a murine model of infection. Cell Microbiol 7:687–698PubMedCrossRef
71.
go back to reference Gaines J, Tjaden B, Carroll B, Baumgartner J, Anderson E, Roop R (2009) The small RNA regulatory twist on expression of sodC in Brucella abortus 2308. Abstr 109th Gen Meet Am Soc Microbiol, Abstr B-042 Gaines J, Tjaden B, Carroll B, Baumgartner J, Anderson E, Roop R (2009) The small RNA regulatory twist on expression of sodC in Brucella abortus 2308. Abstr 109th Gen Meet Am Soc Microbiol, Abstr B-042
72.
go back to reference Gajiwala KS, Burley SK (2000) HdeA, a periplasmic protein that supports acid resistance in pathogenic enteric bacteria. J Mol Biol 295:605–612PubMedCrossRef Gajiwala KS, Burley SK (2000) HdeA, a periplasmic protein that supports acid resistance in pathogenic enteric bacteria. J Mol Biol 295:605–612PubMedCrossRef
73.
go back to reference Gee JM, Kovach ME, Grippe VK, Hagius S, Walker JV, Elzer PH, Roop RM II (2004) Role of catalase in the virulence of Brucella melitensis in pregnant goats. Vet Microbiol 102:111–115PubMedCrossRef Gee JM, Kovach ME, Grippe VK, Hagius S, Walker JV, Elzer PH, Roop RM II (2004) Role of catalase in the virulence of Brucella melitensis in pregnant goats. Vet Microbiol 102:111–115PubMedCrossRef
74.
go back to reference Gee JM, Valderas MW, Kovach ME, Grippe VK, Robertson GT, Ng WL, Richardson JM, Winkler ME, Roop RM II (2005) The Brucella abortus Cu, Zn superoxide dismutase is required for optimal resistance to oxidative killing by murine macrophages and wild-type virulence in experimentally infected mice. Infect Immun 73:2873–2880PubMedCrossRef Gee JM, Valderas MW, Kovach ME, Grippe VK, Robertson GT, Ng WL, Richardson JM, Winkler ME, Roop RM II (2005) The Brucella abortus Cu, Zn superoxide dismutase is required for optimal resistance to oxidative killing by murine macrophages and wild-type virulence in experimentally infected mice. Infect Immun 73:2873–2880PubMedCrossRef
75.
go back to reference Ghosh P (2004) Process of protein transport by the Type III secretion system. Microbiol Mol Biol Rev 68:771–795PubMedCrossRef Ghosh P (2004) Process of protein transport by the Type III secretion system. Microbiol Mol Biol Rev 68:771–795PubMedCrossRef
76.
go back to reference Godfroid F, Taminiau B, Danese I, Denoel P, Tibor A, Weynants V, Cloeckaert A, Godfroid J, Letesson JJ (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 66:5485–5493PubMed Godfroid F, Taminiau B, Danese I, Denoel P, Tibor A, Weynants V, Cloeckaert A, Godfroid J, Letesson JJ (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 66:5485–5493PubMed
77.
go back to reference González-Carreró MI, Sangari FJ, Agüero J, García-Lobo JM (2002) Brucella abortus 2308 produces brucebactin, a highly efficient catecholic siderophore. Microbiology 148:353–360PubMed González-Carreró MI, Sangari FJ, Agüero J, García-Lobo JM (2002) Brucella abortus 2308 produces brucebactin, a highly efficient catecholic siderophore. Microbiology 148:353–360PubMed
78.
go back to reference Gross A, Spiesser S, Terraza A, Rouot B, Caron E, Dornand J (1998) Expression and bactericidal activity of nitric oxide synthase in Brucella suis-infected murine macrophages. Infect Immun 66:1309–1316PubMed Gross A, Spiesser S, Terraza A, Rouot B, Caron E, Dornand J (1998) Expression and bactericidal activity of nitric oxide synthase in Brucella suis-infected murine macrophages. Infect Immun 66:1309–1316PubMed
79.
go back to reference Gross A, Terraza A, Ouahrani-Bettache S, Liautard JP, Dornand J (2000) In vitro Brucella suis infection prevents the programmed cell death of human monocytic cells. Infect Immun 68:342–351PubMedCrossRef Gross A, Terraza A, Ouahrani-Bettache S, Liautard JP, Dornand J (2000) In vitro Brucella suis infection prevents the programmed cell death of human monocytic cells. Infect Immun 68:342–351PubMedCrossRef
80.
go back to reference Guzmán-Verri C, Manterola L, Sola-Landa A, Parra A, Cloeckaert A, Garin J, Gorvel JP, Moriyón I, Moreno E, López-Goñi I (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 99:12375–12380PubMedCrossRef Guzmán-Verri C, Manterola L, Sola-Landa A, Parra A, Cloeckaert A, Garin J, Gorvel JP, Moriyón I, Moreno E, López-Goñi I (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 99:12375–12380PubMedCrossRef
81.
go back to reference Haine V, Sinon A, Van Steen F, Rousseau S, Dozot M, Lestrate P, Lambert C, Letesson JJ, de Bolle X (2005) Systematic targeted mutagenesis of Brucella melitensis 16M reveals a major role for GntR regulators in the control of virulence. Infect Immun 73:5578–5586PubMedCrossRef Haine V, Sinon A, Van Steen F, Rousseau S, Dozot M, Lestrate P, Lambert C, Letesson JJ, de Bolle X (2005) Systematic targeted mutagenesis of Brucella melitensis 16M reveals a major role for GntR regulators in the control of virulence. Infect Immun 73:5578–5586PubMedCrossRef
82.
go back to reference Haine V, Dozot M, Dornand J, Letesson JJ, de Bolle X (2006) NnrA is required for full virulence and regulates several Brucella melitensis denitrification genes. J Bacteriol 188:1615–1619PubMedCrossRef Haine V, Dozot M, Dornand J, Letesson JJ, de Bolle X (2006) NnrA is required for full virulence and regulates several Brucella melitensis denitrification genes. J Bacteriol 188:1615–1619PubMedCrossRef
83.
go back to reference Hernandez-Mora G, Gonzalez-Barrientos R, Morales JA, Chaves-Olarte E, Guzman-Verri C, Baquero-Calvo E, De-Miguel MJ, Marin CM, Blasco JM, Moreno E (2008) Neurobrucellosis in stranded dolphins, Costa Rica. Emerg Infect Dis 14:1430–1433PubMedCrossRef Hernandez-Mora G, Gonzalez-Barrientos R, Morales JA, Chaves-Olarte E, Guzman-Verri C, Baquero-Calvo E, De-Miguel MJ, Marin CM, Blasco JM, Moreno E (2008) Neurobrucellosis in stranded dolphins, Costa Rica. Emerg Infect Dis 14:1430–1433PubMedCrossRef
84.
go back to reference Hong PC, Tsolis RM, Ficht TA (2000) Identification of genes required for chronic persistence of Brucella abortus in mice. Infect Immun 68:4102–4107PubMedCrossRef Hong PC, Tsolis RM, Ficht TA (2000) Identification of genes required for chronic persistence of Brucella abortus in mice. Infect Immun 68:4102–4107PubMedCrossRef
85.
go back to reference Hornback ML, Roop RM II (2006) The Brucella abortus xthA-1 gene product participates in base excision repair and resistance to oxidative killing but is not required for wild-type virulence in the mouse model. J Bacteriol 188:1295–1300PubMedCrossRef Hornback ML, Roop RM II (2006) The Brucella abortus xthA-1 gene product participates in base excision repair and resistance to oxidative killing but is not required for wild-type virulence in the mouse model. J Bacteriol 188:1295–1300PubMedCrossRef
86.
go back to reference Igwebuike UM (2006) Trophoblast cells of ruminant placentas—a minireview. Anim Reprod Sci 93:185–198PubMedCrossRef Igwebuike UM (2006) Trophoblast cells of ruminant placentas—a minireview. Anim Reprod Sci 93:185–198PubMedCrossRef
87.
go back to reference Iñón de Iannino N, Briones G, Tomalsky M, Ugalde RA (1998) Molecular cloning and characterization of cgs, the Brucella abortus cyclic β(1–2) glucan synthetase gene: genetic complementation of Rhizobium meliloti ndvB and Agrobacterium tumefaciens chvB mutants. J Bacteriol 180:4392–4400PubMed Iñón de Iannino N, Briones G, Tomalsky M, Ugalde RA (1998) Molecular cloning and characterization of cgs, the Brucella abortus cyclic β(1–2) glucan synthetase gene: genetic complementation of Rhizobium meliloti ndvB and Agrobacterium tumefaciens chvB mutants. J Bacteriol 180:4392–4400PubMed
88.
go back to reference Iriarte M, González D, Delrue RM, Monreal D, Conde R, López-Goñi I, Letesson JJ, Moriyón I (2004) Brucella lipopolysaccharide: structure, biosynthesis and genetics. In: López-Goñi I, Moriyón I (eds) Brucella: molecular and cellular biology. Horizon Bioscience, Norfolk, pp 159–191 Iriarte M, González D, Delrue RM, Monreal D, Conde R, López-Goñi I, Letesson JJ, Moriyón I (2004) Brucella lipopolysaccharide: structure, biosynthesis and genetics. In: López-Goñi I, Moriyón I (eds) Brucella: molecular and cellular biology. Horizon Bioscience, Norfolk, pp 159–191
89.
go back to reference Jain V, Kumar M, Chatterji D (2006) ppGpp: stringent response and survival. J Microbiol 44:1–10PubMed Jain V, Kumar M, Chatterji D (2006) ppGpp: stringent response and survival. J Microbiol 44:1–10PubMed
90.
go back to reference Jiang X, Leonard B, Benson R, Baldwin CL (1993) Macrophage control of Brucella abortus: role of reactive oxygen intermediates and nitric oxide. Cell Immunol 151:309–319PubMedCrossRef Jiang X, Leonard B, Benson R, Baldwin CL (1993) Macrophage control of Brucella abortus: role of reactive oxygen intermediates and nitric oxide. Cell Immunol 151:309–319PubMedCrossRef
91.
go back to reference Jiménez de Bagüés MP, Loisel-Meyer S, Liautard JP, Jubier-Maurin V (2007) Different roles of the two high-oxygen-affinity terminal oxidases of Brucella suis: cytochrome c oxidase, but not ubiquinol oxidase, is required for persistence in mice. Infect Immun 75:531–535PubMedCrossRef Jiménez de Bagüés MP, Loisel-Meyer S, Liautard JP, Jubier-Maurin V (2007) Different roles of the two high-oxygen-affinity terminal oxidases of Brucella suis: cytochrome c oxidase, but not ubiquinol oxidase, is required for persistence in mice. Infect Immun 75:531–535PubMedCrossRef
92.
go back to reference Kahl-McDonough MM, Ficht TA (2006) Evaluation of protection afforded by Brucella abortus and Brucella melitensis unmarked deletion mutants exhibiting different rates of clearance in BALB/c mice. Infect Immun 74:4048–4057CrossRef Kahl-McDonough MM, Ficht TA (2006) Evaluation of protection afforded by Brucella abortus and Brucella melitensis unmarked deletion mutants exhibiting different rates of clearance in BALB/c mice. Infect Immun 74:4048–4057CrossRef
93.
go back to reference Kahl-McDonough MM, Elzer PH, Hagius SD, Walker JV, Perry QL, Seabury CM, den Hartigh AB, Tsolis RM, Adams LG, Davis DS, Ficht TA (2006) Evaluation of novel Brucella melitensis unmarked deletion mutants for safety and efficacy in the goat model of brucellosis. Vaccine 24:5169–5177CrossRef Kahl-McDonough MM, Elzer PH, Hagius SD, Walker JV, Perry QL, Seabury CM, den Hartigh AB, Tsolis RM, Adams LG, Davis DS, Ficht TA (2006) Evaluation of novel Brucella melitensis unmarked deletion mutants for safety and efficacy in the goat model of brucellosis. Vaccine 24:5169–5177CrossRef
94.
go back to reference Kikuchi H, Kim S, Watanabe K, Watarai M (2006) Brucella abortus D-alanyl-D-alanine carboxypeptidase contributes to its intracellular replication and resistance against nitric oxide. FEMS Microbiol Lett 259:120–125PubMedCrossRef Kikuchi H, Kim S, Watanabe K, Watarai M (2006) Brucella abortus D-alanyl-D-alanine carboxypeptidase contributes to its intracellular replication and resistance against nitric oxide. FEMS Microbiol Lett 259:120–125PubMedCrossRef
95.
go back to reference Kim JA, Sha Z, Mayfield JE (2000) Regulation of Brucella abortus catalase. Infect Immun 68:3681–3866 Kim JA, Sha Z, Mayfield JE (2000) Regulation of Brucella abortus catalase. Infect Immun 68:3681–3866
96.
go back to reference Kim S, Watarai M, Makino S, Shirahata T (2002) Membrane sorting during swimming internalization of Brucella is required for phagosome trafficking decisions. Microb Pathog 33:225–237PubMedCrossRef Kim S, Watarai M, Makino S, Shirahata T (2002) Membrane sorting during swimming internalization of Brucella is required for phagosome trafficking decisions. Microb Pathog 33:225–237PubMedCrossRef
97.
go back to reference Kim S, Watarai M, Kondo Y, Erdenebaatar J, Makino S, 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 71:3020–3027PubMedCrossRef Kim S, Watarai M, Kondo Y, Erdenebaatar J, Makino S, 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 71:3020–3027PubMedCrossRef
98.
go back to reference Kim S, Watanabe K, Shirahata T, Watarai M (2004) Zinc uptake system (znuA locus) of Brucella abortus is essential for intracellular survival and virulence in mice. J Vet Med Sci 66:1059–1063PubMedCrossRef Kim S, Watanabe K, Shirahata T, Watarai M (2004) Zinc uptake system (znuA locus) of Brucella abortus is essential for intracellular survival and virulence in mice. J Vet Med Sci 66:1059–1063PubMedCrossRef
99.
go back to reference Kim S, Watanabe K, Suzuki H, Watarai M (2005) Roles of Brucella abortus SpoT in morphological differentiation and intramacrophagic replication. Microbiology 151:1607–1617PubMedCrossRef Kim S, Watanabe K, Suzuki H, Watarai M (2005) Roles of Brucella abortus SpoT in morphological differentiation and intramacrophagic replication. Microbiology 151:1607–1617PubMedCrossRef
100.
go back to reference Köhler S, Foulongne V, Ouahrani-Bettache S, Bourg G, Teyssier J, Ramuz M, Liautard JP (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 99:15711–15716PubMedCrossRef Köhler S, Foulongne V, Ouahrani-Bettache S, Bourg G, Teyssier J, Ramuz M, Liautard JP (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 99:15711–15716PubMedCrossRef
101.
go back to reference Köhler S, Michaux-Charachon S, Porte F, Ramuz M, Liautard JP (2003) What is the nature of the replicative niche of a stealthy bug named Brucella? Trends Microbiol 11:215–219PubMed Köhler S, Michaux-Charachon S, Porte F, Ramuz M, Liautard JP (2003) What is the nature of the replicative niche of a stealthy bug named Brucella? Trends Microbiol 11:215–219PubMed
102.
go back to reference Lamontagne J, Butler H, Chaves-Olarte E, Hunter J, Schirm M, Paquet C, Tian M, Kearney P, Hamaidi L, Chelsky D, Moriyón I, Moreno E, Paramithiotis E (2007) Extensive cell envelope modulation is associated with virulence in Brucella abortus. J Proteome Res 6:1519–1529PubMedCrossRef Lamontagne J, Butler H, Chaves-Olarte E, Hunter J, Schirm M, Paquet C, Tian M, Kearney P, Hamaidi L, Chelsky D, Moriyón I, Moreno E, Paramithiotis E (2007) Extensive cell envelope modulation is associated with virulence in Brucella abortus. J Proteome Res 6:1519–1529PubMedCrossRef
103.
go back to reference Lamontagne J, Forest A, Marazzo E, Denis F, Butler H, Michaud JF, Boucher L, Pedro I, Villeneuve A, Sitnikov D, Trudel K, Nassif N, Boudjelti D, Tomaki F, Chaves-Olarte E, Guzmán-Verri C, Brunet S, Côté-Martin A, Hunter J, Moreno E, Paramithiotis E (2009) Intracellular adaptation of Brucella abortus. J Proteome Res 8:1594–1609PubMedCrossRef Lamontagne J, Forest A, Marazzo E, Denis F, Butler H, Michaud JF, Boucher L, Pedro I, Villeneuve A, Sitnikov D, Trudel K, Nassif N, Boudjelti D, Tomaki F, Chaves-Olarte E, Guzmán-Verri C, Brunet S, Côté-Martin A, Hunter J, Moreno E, Paramithiotis E (2009) Intracellular adaptation of Brucella abortus. J Proteome Res 8:1594–1609PubMedCrossRef
104.
go back to reference Lapaque N, Takeuchi S, Corrales F, Akira A, Moriyón I, Howard JC, Gorvel JP (2006) Differential inductions of TNF-α and IGTP, IIGP by structurally diverse classic and non-classic lipopolysaccharides. Cell Microbiol 8:401–413PubMedCrossRef Lapaque N, Takeuchi S, Corrales F, Akira A, Moriyón I, Howard JC, Gorvel JP (2006) Differential inductions of TNF-α and IGTP, IIGP by structurally diverse classic and non-classic lipopolysaccharides. Cell Microbiol 8:401–413PubMedCrossRef
105.
go back to reference Lavigne JP, O’Callaghan D, Blanc-Potard AB (2005) Requirement of MgtC for Brucella suis intramacrophage growth: a potential mechanism shared by Salmonella enterica and Mycobacterium tuberculosis for adaptation to a low-Mg2+ environment. Infect Immun 73:3160–3163PubMedCrossRef Lavigne JP, O’Callaghan D, Blanc-Potard AB (2005) Requirement of MgtC for Brucella suis intramacrophage growth: a potential mechanism shared by Salmonella enterica and Mycobacterium tuberculosis for adaptation to a low-Mg2+ environment. Infect Immun 73:3160–3163PubMedCrossRef
106.
go back to reference Lavigne JP, Patey G, Sangari FJ, Bourg G, Ramuz M, O’Callaghan D, Michaux-Charachon S (2005) Identification of a new virulence factor, BvfA, in Brucella suis. Infect Immun 73:5524–5529PubMedCrossRef Lavigne JP, Patey G, Sangari FJ, Bourg G, Ramuz M, O’Callaghan D, Michaux-Charachon S (2005) Identification of a new virulence factor, BvfA, in Brucella suis. Infect Immun 73:5524–5529PubMedCrossRef
107.
go back to reference Léonard S, Ferooz J, Haine V, Danese I, Fretin D, Tibor A, de Walque S, de Bolle X, Letesson JJ (2007) FtcR is a new master regulator of the flagellar system of Brucella melitensis 16M with homologs in Rhizobiaceae. J Bacteriol 189:131–141PubMedCrossRef Léonard S, Ferooz J, Haine V, Danese I, Fretin D, Tibor A, de Walque S, de Bolle X, Letesson JJ (2007) FtcR is a new master regulator of the flagellar system of Brucella melitensis 16M with homologs in Rhizobiaceae. J Bacteriol 189:131–141PubMedCrossRef
108.
go back to reference Lestrate P, Delrue RM, Danese I, Didembourg C, Taminiau B, Mertens P, de Bolle X, Tibor A, Tang CM, Letesson JJ (2000) Identification and characterization of in vivo attenuated mutants of Brucella melitensis. Mol Microbiol 38:543–551PubMedCrossRef Lestrate P, Delrue RM, Danese I, Didembourg C, Taminiau B, Mertens P, de Bolle X, Tibor A, Tang CM, Letesson JJ (2000) Identification and characterization of in vivo attenuated mutants of Brucella melitensis. Mol Microbiol 38:543–551PubMedCrossRef
109.
go back to reference Lestrate P, Dricot A, Delrue RM, Lambert C, Martinelli V, de Bolle X, Letesson JJ, Tibor A (2003) Attenuated signature-tagged mutagenesis mutants of Brucella melitensis identified during the acute phage of infection in mice. Infect Immun 71:7053–7060PubMedCrossRef Lestrate P, Dricot A, Delrue RM, Lambert C, Martinelli V, de Bolle X, Letesson JJ, Tibor A (2003) Attenuated signature-tagged mutagenesis mutants of Brucella melitensis identified during the acute phage of infection in mice. Infect Immun 71:7053–7060PubMedCrossRef
110.
go back to reference LeVier K, Phillips RW, Grippe VK, Roop RM II, Walker GC (2000) Similar requirements of a plant symbiont and a mammalian pathogen for prolonged intracellular survival. Science 287:2492–2493PubMedCrossRef LeVier K, Phillips RW, Grippe VK, Roop RM II, Walker GC (2000) Similar requirements of a plant symbiont and a mammalian pathogen for prolonged intracellular survival. Science 287:2492–2493PubMedCrossRef
111.
go back to reference Li L, Jia Y, Hou Q, Charles TC, Nester EW, Pan SQ (2002) A global pH sensor: Agrobacterium sensor protein ChvG regulates acid-inducible genes on its two chromosomes and Ti plasmid. Proc Natl Acad Sci USA 99:12369–12374PubMedCrossRef Li L, Jia Y, Hou Q, Charles TC, Nester EW, Pan SQ (2002) A global pH sensor: Agrobacterium sensor protein ChvG regulates acid-inducible genes on its two chromosomes and Ti plasmid. Proc Natl Acad Sci USA 99:12369–12374PubMedCrossRef
112.
go back to reference Lin J, Ficht TA (1995) Protein synthesis in Brucella abortus induced during macrophage infection. Infect Immun 63:1409–1414PubMed Lin J, Ficht TA (1995) Protein synthesis in Brucella abortus induced during macrophage infection. Infect Immun 63:1409–1414PubMed
113.
go back to reference Loisel-Meyer S, Jiménez de Bagüés MP, Bassères E, Dornand J, Köhler S, Liautard JP, Jubier-Maurin V (2006) Requirement of norD for Brucella suis virulence in a murine model of in vitro and in vivo infection. Infect Immun 74:1973–1976PubMedCrossRef Loisel-Meyer S, Jiménez de Bagüés MP, Bassères E, Dornand J, Köhler S, Liautard JP, Jubier-Maurin V (2006) Requirement of norD for Brucella suis virulence in a murine model of in vitro and in vivo infection. Infect Immun 74:1973–1976PubMedCrossRef
114.
go back to reference López-Goñi I, Moriyón I, Neilands JB (1992) Identification of 2, 3-dihydroxybenzoic acid as a Brucella abortus siderophore. Infect Immun 60:4496–4503PubMed López-Goñi I, Moriyón I, Neilands JB (1992) Identification of 2, 3-dihydroxybenzoic acid as a Brucella abortus siderophore. Infect Immun 60:4496–4503PubMed
115.
go back to reference Lynch M, Kuramitsu H (2000) Expression and role of superoxide dismutases (SOD) in pathogenic bacteria. Microbes Infect 2:1245–1255PubMedCrossRef Lynch M, Kuramitsu H (2000) Expression and role of superoxide dismutases (SOD) in pathogenic bacteria. Microbes Infect 2:1245–1255PubMedCrossRef
116.
go back to reference Magnusson LU, Farewell A, Nyström T (2005) ppGpp: a global regulator in Escherichia coli. Trends Microbiol 13:236–242PubMedCrossRef Magnusson LU, Farewell A, Nyström T (2005) ppGpp: a global regulator in Escherichia coli. Trends Microbiol 13:236–242PubMedCrossRef
117.
go back to reference Manterola L, Moriyón I, Moreno E, Sola-Landa A, Weiss DS, Koch MHJ, Howe J, Brandenburg K, López-Goñi I (2005) The lipopolysaccharide of Brucella abortus BvrS/BvrR mutants contains lipid modifications and has higher affinity for bactericidal cationic peptides. J Bacteriol 187:5631–5639PubMedCrossRef Manterola L, Moriyón I, Moreno E, Sola-Landa A, Weiss DS, Koch MHJ, Howe J, Brandenburg K, López-Goñi I (2005) The lipopolysaccharide of Brucella abortus BvrS/BvrR mutants contains lipid modifications and has higher affinity for bactericidal cationic peptides. J Bacteriol 187:5631–5639PubMedCrossRef
118.
go back to reference Manterola L, Guzmán-Verri C, Chaves-Olarte E, Barquero-Calvo E, de Miguel MJ, Moriyón I, Grilló MJ, López-Goñi I, Moreno E (2007) BvrR/BvrS-controlled outer membrane proteins Omp3a and Omp3b are not essential for Brucella abortus virulence. Infect Immun 75:4867–4874PubMedCrossRef Manterola L, Guzmán-Verri C, Chaves-Olarte E, Barquero-Calvo E, de Miguel MJ, Moriyón I, Grilló MJ, López-Goñi I, Moreno E (2007) BvrR/BvrS-controlled outer membrane proteins Omp3a and Omp3b are not essential for Brucella abortus virulence. Infect Immun 75:4867–4874PubMedCrossRef
119.
go back to reference Martín-Martín AI, Caro-Hernández P, Orduña A, Vizcaíno N, Fernández-Lago L (2008) Importance of the Omp25/Omp31 family in the internalization and intracellular replication of virulent B. ovis in murine macrophages and HeLa cells. Microbes Infect 10:706–710PubMedCrossRef Martín-Martín AI, Caro-Hernández P, Orduña A, Vizcaíno N, Fernández-Lago L (2008) Importance of the Omp25/Omp31 family in the internalization and intracellular replication of virulent B. ovis in murine macrophages and HeLa cells. Microbes Infect 10:706–710PubMedCrossRef
120.
go back to reference Martínez de Tejada G, Pizarro-Cerdá J, Moreno E, Moriyón I (1995) The outer membranes of Brucella spp. are resistant to bactericidal cationic peptides. Infect Immun 63:3054–3061PubMed Martínez de Tejada G, Pizarro-Cerdá J, Moreno E, Moriyón I (1995) The outer membranes of Brucella spp. are resistant to bactericidal cationic peptides. Infect Immun 63:3054–3061PubMed
121.
go back to reference Master SS, Springer B, Sander P, Boettger EC, Deretic V, Timmins GS (2002) Oxidative stress response genes in Mycobacterium tuberculosis: role of ahpC in resistance to peroxynitrite and stage-specific survival in macrophages. Microbiology 148:3139–3144PubMed Master SS, Springer B, Sander P, Boettger EC, Deretic V, Timmins GS (2002) Oxidative stress response genes in Mycobacterium tuberculosis: role of ahpC in resistance to peroxynitrite and stage-specific survival in macrophages. Microbiology 148:3139–3144PubMed
122.
go back to reference McQuiston JR, Vemulapalli R, Inzana TJ, Schurig GG, Sriranganathan N, Fritzinger D, Hadfield TL, Warren RL, Snellings N, Hoover D, Halling SM, Boyle SM (1999) Genetic characterization of a Tn5-disrupted glycosyltransferase gene homolog in Brucella abortus and its effect on lipopolysaccharide composition and virulence. Infect Immun 67:3830–3835PubMed McQuiston JR, Vemulapalli R, Inzana TJ, Schurig GG, Sriranganathan N, Fritzinger D, Hadfield TL, Warren RL, Snellings N, Hoover D, Halling SM, Boyle SM (1999) Genetic characterization of a Tn5-disrupted glycosyltransferase gene homolog in Brucella abortus and its effect on lipopolysaccharide composition and virulence. Infect Immun 67:3830–3835PubMed
123.
go back to reference Meador VP, Deyoe BL (1989) Intracellular localization of Brucella abortus in bovine placenta. Vet Pathol 26:513–515PubMedCrossRef Meador VP, Deyoe BL (1989) Intracellular localization of Brucella abortus in bovine placenta. Vet Pathol 26:513–515PubMedCrossRef
124.
go back to reference Minder AC, de Rudder KEE, Narberhaus F, Fischer HM, Hennecke H, Geiger O (2001) Phosphatidylcholine levels in Bradyrhizobium japonicum membranes are critical for an efficient symbiosis with the soybean host plant. Mol Microbiol 39:1186–1198PubMedCrossRef Minder AC, de Rudder KEE, Narberhaus F, Fischer HM, Hennecke H, Geiger O (2001) Phosphatidylcholine levels in Bradyrhizobium japonicum membranes are critical for an efficient symbiosis with the soybean host plant. Mol Microbiol 39:1186–1198PubMedCrossRef
125.
go back to reference Moreno E, Berman DT, Boettcher LA (1981) Biological activities of Brucella abortus lipopolysaccharides. Infect Immun 31:362–370PubMed Moreno E, Berman DT, Boettcher LA (1981) Biological activities of Brucella abortus lipopolysaccharides. Infect Immun 31:362–370PubMed
126.
go back to reference Moreno E, Stackenbrandt 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 172:3569–3576PubMed Moreno E, Stackenbrandt 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 172:3569–3576PubMed
127.
go back to reference Moreno E, Moriyón I (2002) Brucella melitensis: a nasty bug with hidden credentials for virulence. Proc Natl Acad Sci USA 99:1–3PubMedCrossRef Moreno E, Moriyón I (2002) Brucella melitensis: a nasty bug with hidden credentials for virulence. Proc Natl Acad Sci USA 99:1–3PubMedCrossRef
128.
go back to reference Moreno E, Gorvel JP (2004) Invasion, intracellular trafficking and replication of Brucella organisms in professional and non-professional phagocytes. In: López-Goñi I, Moriyón I (eds) Brucella: molecular and cellular biology. Horizon Bioscience, Norfolk, pp 287–312 Moreno E, Gorvel JP (2004) Invasion, intracellular trafficking and replication of Brucella organisms in professional and non-professional phagocytes. In: López-Goñi I, Moriyón I (eds) Brucella: molecular and cellular biology. Horizon Bioscience, Norfolk, pp 287–312
129.
go back to reference Naroeni A, Jouy N, Ouahrani-Bettache S, Liautard JP, Porte F (2001) Brucella suis-impaired specific recognition of phagosomes by lysosomes due to phagosomal membrane modifications. Infect Immun 69:486–493PubMedCrossRef Naroeni A, Jouy N, Ouahrani-Bettache S, Liautard JP, Porte F (2001) Brucella suis-impaired specific recognition of phagosomes by lysosomes due to phagosomal membrane modifications. Infect Immun 69:486–493PubMedCrossRef
130.
go back to reference Nicoletti PL (1989) Relationship between animal and human disease. In: Young EJ, Corbel MJ (eds) Brucellosis: clinical and laboratory aspects. CRC, Boca Raton, pp 41–51 Nicoletti PL (1989) Relationship between animal and human disease. In: Young EJ, Corbel MJ (eds) Brucellosis: clinical and laboratory aspects. CRC, Boca Raton, pp 41–51
131.
go back to reference O’Callaghan D, Cazevieille C, Allardet-Servent A, Boschiroli ML, Bourg G, Foulongne V, Frutos P, Kulakov Y, Ramuz M (1999) A homologue of the Agrobacterium tumefaciens VirB and Bordetella Ptl type IV secretion systems is essential for intracellular survival of Brucella suis. Mol Microbiol 33:1210–1220PubMedCrossRef O’Callaghan D, Cazevieille C, Allardet-Servent A, Boschiroli ML, Bourg G, Foulongne V, Frutos P, Kulakov Y, Ramuz M (1999) A homologue of the Agrobacterium tumefaciens VirB and Bordetella Ptl type IV secretion systems is essential for intracellular survival of Brucella suis. Mol Microbiol 33:1210–1220PubMedCrossRef
132.
go back to reference O’Neill LAJ, Bowie AG (2007) The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat Rev Immunol 7:353–364PubMedCrossRef O’Neill LAJ, Bowie AG (2007) The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat Rev Immunol 7:353–364PubMedCrossRef
133.
go back to reference Pappas G, Papadimitriou P, Akritidis N, Christou L, Tsianos EV (2006) The new global map of human brucellosis. Lancet Infect Dis 6:91–99PubMedCrossRef Pappas G, Papadimitriou P, Akritidis N, Christou L, Tsianos EV (2006) The new global map of human brucellosis. Lancet Infect Dis 6:91–99PubMedCrossRef
134.
go back to reference Pappas G, Panagopoulou P, Christou L, Akritidis N (2006) Brucella as a biological weapon. Cell Mol Life Sci 63:2229–2236PubMedCrossRef Pappas G, Panagopoulou P, Christou L, Akritidis N (2006) Brucella as a biological weapon. Cell Mol Life Sci 63:2229–2236PubMedCrossRef
135.
go back to reference Parent MA, Bellaire BH, Murphy EA, Roop RM II, Elzer PH, Baldwin CL (2002) Brucella abortus siderophore 2, 3-dihydroxybenzoic acid (DHBA) facilitates intracellular survival of the bacteria. Microb Pathog 32:239–248PubMedCrossRef Parent MA, Bellaire BH, Murphy EA, Roop RM II, Elzer PH, Baldwin CL (2002) Brucella abortus siderophore 2, 3-dihydroxybenzoic acid (DHBA) facilitates intracellular survival of the bacteria. Microb Pathog 32:239–248PubMedCrossRef
136.
go back to reference Parent MA, Goenka R, Murphy E, LeVier K, Carreiro N, Golding B, Ferguson G, Roop RM II, Walker GC, Baldwin CL (2007) Brucella bacA mutant induces greater pro-inflammatory cytokines than the wild-type parent. Microbes Infect 9:55–62PubMedCrossRef Parent MA, Goenka R, Murphy E, LeVier K, Carreiro N, Golding B, Ferguson G, Roop RM II, Walker GC, Baldwin CL (2007) Brucella bacA mutant induces greater pro-inflammatory cytokines than the wild-type parent. Microbes Infect 9:55–62PubMedCrossRef
137.
go back to reference Paulley JT, Anderson ES, Roop RM II (2007) Brucella abortus requires the heme transporter BhuA for maintenance of chronic infection in BALB/c mice. Infect Immun 75:5248–5254PubMedCrossRef Paulley JT, Anderson ES, Roop RM II (2007) Brucella abortus requires the heme transporter BhuA for maintenance of chronic infection in BALB/c mice. Infect Immun 75:5248–5254PubMedCrossRef
138.
go back to reference Pei J, Ficht TA (2004) Brucella abortus rough mutants are cytopathic for macrophages in culture. Infect Immun 72:440–450PubMedCrossRef Pei J, Ficht TA (2004) Brucella abortus rough mutants are cytopathic for macrophages in culture. Infect Immun 72:440–450PubMedCrossRef
139.
go back to reference Pizarro-Cerda J, Meresse S, Parton RG, van der Goot G, Sola-Landa A, López-Goñi I, Moreno E, Gorvel JP (1998) Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes. Infect Immun 66:5711–5724PubMed Pizarro-Cerda J, Meresse S, Parton RG, van der Goot G, Sola-Landa A, López-Goñi I, Moreno E, Gorvel JP (1998) Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes. Infect Immun 66:5711–5724PubMed
140.
go back to reference Porte F, Liautard JP, Köhler S (1999) Early acidification of phagosomes containing Brucella suis is essential for intracellular survival in murine macrophages. Infect Immun 67:4041–4047PubMed Porte F, Liautard JP, Köhler S (1999) Early acidification of phagosomes containing Brucella suis is essential for intracellular survival in murine macrophages. Infect Immun 67:4041–4047PubMed
141.
go back to reference Porte F, Naroeni A, Ouahrani-Bettache S, Liautard JP (2003) Role of the Brucella suis lipopolysaccharide O antigen in phagosomal genesis and in inhibition of phagosome-lysosome fusion in murine macrophages. Infect Immun 71:1481–1490PubMedCrossRef Porte F, Naroeni A, Ouahrani-Bettache S, Liautard JP (2003) Role of the Brucella suis lipopolysaccharide O antigen in phagosomal genesis and in inhibition of phagosome-lysosome fusion in murine macrophages. Infect Immun 71:1481–1490PubMedCrossRef
142.
go back to reference Posey JE, Gherardini FC (2000) Lack of a role for iron in the Lyme disease pathogen. Science 288:1651–1653PubMedCrossRef Posey JE, Gherardini FC (2000) Lack of a role for iron in the Lyme disease pathogen. Science 288:1651–1653PubMedCrossRef
143.
go back to reference Preisig O, Zufferey R, Thöny-Meyer L, Appleby CA, Hennecke H (1996) A high-affinity cbb 3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum. J Bacteriol 178:1532–1538PubMed Preisig O, Zufferey R, Thöny-Meyer L, Appleby CA, Hennecke H (1996) A high-affinity cbb 3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum. J Bacteriol 178:1532–1538PubMed
144.
go back to reference Puvanesarajah V, Schell FM, Stacey G, Douglas CJ, Nester EW (1985) Role for 2-linked β-D-glucan in the virulence of Agrobacterium tumefaciens. J Bacteriol 164:102–106PubMed Puvanesarajah V, Schell FM, Stacey G, Douglas CJ, Nester EW (1985) Role for 2-linked β-D-glucan in the virulence of Agrobacterium tumefaciens. J Bacteriol 164:102–106PubMed
145.
go back to reference Radhakrishnan GK, Yu Q, Harms JS, Splitter GA (2009) Brucella TIR domain-containing protein mimics properties of the Toll-like receptor adaptor protein TIRAP. J Biol Chem 284:9892–9898PubMedCrossRef Radhakrishnan GK, Yu Q, Harms JS, Splitter GA (2009) Brucella TIR domain-containing protein mimics properties of the Toll-like receptor adaptor protein TIRAP. J Biol Chem 284:9892–9898PubMedCrossRef
146.
go back to reference Rajashekara G, Glover DA, Banai M, O’Callaghan D, Splitter GA (2006) Attenuated bioluminescent Brucella melitensis mutants GR109 (virB4), GR024 (galE), and GR026 (BEMI1090-BMEI1091) confer protection in mice. Infect Immun 74:2925–2936PubMedCrossRef Rajashekara G, Glover DA, Banai M, O’Callaghan D, Splitter GA (2006) Attenuated bioluminescent Brucella melitensis mutants GR109 (virB4), GR024 (galE), and GR026 (BEMI1090-BMEI1091) confer protection in mice. Infect Immun 74:2925–2936PubMedCrossRef
147.
go back to reference Rambow-Larsen AA, 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 190:3274–3282PubMedCrossRef Rambow-Larsen AA, 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 190:3274–3282PubMedCrossRef
148.
go back to reference Rasool O, Freer E, Moreno E, Jarstrand C (1992) Effect of Brucella abortus lipopolysaccharide on oxidative metabolism and lysozyme release by human neutrophils. Infect Immun 60:1699–1702PubMed Rasool O, Freer E, Moreno E, Jarstrand C (1992) Effect of Brucella abortus lipopolysaccharide on oxidative metabolism and lysozyme release by human neutrophils. Infect Immun 60:1699–1702PubMed
149.
go back to reference Rest RF, Robertson DC (1975) Characterization of the electron transport system in Brucella abortus. J Bacteriol 122:139–144PubMed Rest RF, Robertson DC (1975) Characterization of the electron transport system in Brucella abortus. J Bacteriol 122:139–144PubMed
150.
go back to reference Rittig M, Alvarez-Martinez MT, Porte F, Liautard JP, Rouot B (2001) Intracellular survival of Brucella spp. in human monocytes involves conventional uptake but special phagosomes. Infect Immun 69:3995–4006PubMedCrossRef Rittig M, Alvarez-Martinez MT, Porte F, Liautard JP, Rouot B (2001) Intracellular survival of Brucella spp. in human monocytes involves conventional uptake but special phagosomes. Infect Immun 69:3995–4006PubMedCrossRef
151.
go back to reference Rittig MG, Kaufmann A, Robins A, Shaw B, Sprenger H, Gemsa D, Foulongne V, Rouot B, Dornand J (2003) Smooth and rough lipopolysaccharide phenotypes of Brucella induce different intracellular trafficking and cytokine/chemokine release in human monocytes. J Leukoc Biol 74:1045–1055PubMedCrossRef Rittig MG, Kaufmann A, Robins A, Shaw B, Sprenger H, Gemsa D, Foulongne V, Rouot B, Dornand J (2003) Smooth and rough lipopolysaccharide phenotypes of Brucella induce different intracellular trafficking and cytokine/chemokine release in human monocytes. J Leukoc Biol 74:1045–1055PubMedCrossRef
152.
go back to reference Robertson GT, Roop RM II (1999) The Brucella abortus host factor I (HF-I) protein contributes to stress resistance during stationary phase and is a major determinant of virulence in mice. Mol Microbiol 34:690–700PubMedCrossRef Robertson GT, Roop RM II (1999) The Brucella abortus host factor I (HF-I) protein contributes to stress resistance during stationary phase and is a major determinant of virulence in mice. Mol Microbiol 34:690–700PubMedCrossRef
153.
go back to reference Roop RM II, Jeffers G, Bagchi T, Walker J, Enright FM, Schurig GG (1991) Experimental infection of goat fetuses in utero with a stable, rough mutant of Brucella abortus. Res Vet Sci 51:123–127PubMed Roop RM II, Jeffers G, Bagchi T, Walker J, Enright FM, Schurig GG (1991) Experimental infection of goat fetuses in utero with a stable, rough mutant of Brucella abortus. Res Vet Sci 51:123–127PubMed
154.
go back to reference Roop RM II, Robertson GT, Grippe VK, Kovach ME, LeVier K, Hagius S, Walker JV, Booth N, Fulton T, Elzer PH, Walker GC (2000) Virulence of Brucella melitensis hfq, katE and bacA mutants in pregnant goats. Proc Brucellosis 2000 Meet, Abstr 93, p 89 Roop RM II, Robertson GT, Grippe VK, Kovach ME, LeVier K, Hagius S, Walker JV, Booth N, Fulton T, Elzer PH, Walker GC (2000) Virulence of Brucella melitensis hfq, katE and bacA mutants in pregnant goats. Proc Brucellosis 2000 Meet, Abstr 93, p 89
155.
go back to reference Roop RM II, Gee JM, Robertson GT, Richardson JM, Ng WL, Winkler ME (2003) Brucella stationary-phase gene expression and virulence. Annu Rev Microbiol 57:57–76PubMedCrossRef Roop RM II, Gee JM, Robertson GT, Richardson JM, Ng WL, Winkler ME (2003) Brucella stationary-phase gene expression and virulence. Annu Rev Microbiol 57:57–76PubMedCrossRef
156.
go back to reference Roop RM II, Bellaire BH, Valderas MW, Cardelli JA (2004) Adaptation of the brucellae to their intracellular niche. Mol Microbiol 52:621–630PubMedCrossRef Roop RM II, Bellaire BH, Valderas MW, Cardelli JA (2004) Adaptation of the brucellae to their intracellular niche. Mol Microbiol 52:621–630PubMedCrossRef
157.
go back to reference Roop RM II, Bellaire BH, Anderson E, Paulley JT (2004) Iron metabolism in Brucella. In: López-Goñi I, Moriyón I (eds) Brucella: molecular and cellular biology. Horizon Bioscience, Norfolk, pp 243–262 Roop RM II, Bellaire BH, Anderson E, Paulley JT (2004) Iron metabolism in Brucella. In: López-Goñi I, Moriyón I (eds) Brucella: molecular and cellular biology. Horizon Bioscience, Norfolk, pp 243–262
158.
go back to reference Roux CM (2003) Characterization of DNA repair networks of Brucella abortus: analysis of their role in pathogenesis. Doctoral dissertation, University of Louisiana at Lafayette Roux CM (2003) Characterization of DNA repair networks of Brucella abortus: analysis of their role in pathogenesis. Doctoral dissertation, University of Louisiana at Lafayette
159.
go back to reference Salcedo SP, Marchesini MI, Lelouard H, Fugier E, Jolly G, Balor S, Muller A, Lapaque N, Demaria O, Alexapoulou L, Comerci DJ, Ugalde RA, Pierre P, Gorvel JP (2008) Brucella control of dendritic cell maturation is dependent on the TIR-containing protein Btp1. PLoS Pathog 4:e21PubMedCrossRef Salcedo SP, Marchesini MI, Lelouard H, Fugier E, Jolly G, Balor S, Muller A, Lapaque N, Demaria O, Alexapoulou L, Comerci DJ, Ugalde RA, Pierre P, Gorvel JP (2008) Brucella control of dendritic cell maturation is dependent on the TIR-containing protein Btp1. PLoS Pathog 4:e21PubMedCrossRef
160.
go back to reference Samartino LE, Enright FM (1993) Pathogenesis of abortion of bovine brucellosis. Comp Immunol Microbiol Infect Dis 16:95–101PubMedCrossRef Samartino LE, Enright FM (1993) Pathogenesis of abortion of bovine brucellosis. Comp Immunol Microbiol Infect Dis 16:95–101PubMedCrossRef
161.
go back to reference Sanchez-Contrerase M, Bauer WD, Gao M, Robinson JB, Downie JA (2007) Quorum-sensing regulation in rhizobia and its role in symbiotic interactions with legumes. Phil Trans R Soc B 362:1149–1163CrossRef Sanchez-Contrerase M, Bauer WD, Gao M, Robinson JB, Downie JA (2007) Quorum-sensing regulation in rhizobia and its role in symbiotic interactions with legumes. Phil Trans R Soc B 362:1149–1163CrossRef
162.
go back to reference Sangari FJ, Agüero J (1996) Molecular basis of Brucella pathogenicity: an update. Microbiologia 12:207–218PubMed Sangari FJ, Agüero J (1996) Molecular basis of Brucella pathogenicity: an update. Microbiologia 12:207–218PubMed
163.
go back to reference Sangari FJ, Seoane A, Rodríguez MC, Agüero J, García Lobo JM (2007) Characterization of the urease operon of Brucella abortus and assessment of its role in virulence of the bacterium. Infect Immun 75:774–780PubMedCrossRef Sangari FJ, Seoane A, Rodríguez MC, Agüero J, García Lobo JM (2007) Characterization of the urease operon of Brucella abortus and assessment of its role in virulence of the bacterium. Infect Immun 75:774–780PubMedCrossRef
164.
go back to reference Sangari FJ, Grilló MJ, Jiménez de Bagües MP, González-Carreró MI, García-Lobo JM, Blasco JM, Agüero J (1998) The defect in the metabolism of erythritol of the Brucella abortus B19 vaccine strain is unrelated with its attenuated virulence in mice. Vaccine 16:1640–1645PubMedCrossRef Sangari FJ, Grilló MJ, Jiménez de Bagües MP, González-Carreró MI, García-Lobo JM, Blasco JM, Agüero J (1998) The defect in the metabolism of erythritol of the Brucella abortus B19 vaccine strain is unrelated with its attenuated virulence in mice. Vaccine 16:1640–1645PubMedCrossRef
165.
go back to reference Sha Z, Stabel TJ, Mayfield JE (1994) Brucella abortus catalase is a periplasmic protein lacking a standard signal sequence. J Bacteriol 176:7375–7377PubMed Sha Z, Stabel TJ, Mayfield JE (1994) Brucella abortus catalase is a periplasmic protein lacking a standard signal sequence. J Bacteriol 176:7375–7377PubMed
166.
go back to reference Shepard CC (1959) Nonacid-fast bacteria and HeLa cells: their uptake and subsequent intracellular growth. J Bacteriol 77:701–714PubMed Shepard CC (1959) Nonacid-fast bacteria and HeLa cells: their uptake and subsequent intracellular growth. J Bacteriol 77:701–714PubMed
167.
go back to reference Shin S, Roy CR (2008) Host cell processes that influence the intracellular survival of Legionella pneumophila. Cell Microbiol 10:1209–1220PubMedCrossRef Shin S, Roy CR (2008) Host cell processes that influence the intracellular survival of Legionella pneumophila. Cell Microbiol 10:1209–1220PubMedCrossRef
168.
go back to reference Sieira R, Comerci DJ, Sánchez DO, Ugalde RA (2000) A homologue of an operon required for DNA transfer in Agrobacterium is required in Brucella abortus for virulence and intracellular multiplication. J Bacteriol 182:4849–4855PubMedCrossRef Sieira R, Comerci DJ, Sánchez DO, Ugalde RA (2000) A homologue of an operon required for DNA transfer in Agrobacterium is required in Brucella abortus for virulence and intracellular multiplication. J Bacteriol 182:4849–4855PubMedCrossRef
169.
go back to reference Smith H, Williams AE, Pearce JH, Keppie J, Harris-Smith PW, Fitzgeorge RB, Witt K (1962) Foetal erythritol: a cause of the localization of Brucella abortus in bovine contagious abortion. Nature 193:47–49PubMedCrossRef Smith H, Williams AE, Pearce JH, Keppie J, Harris-Smith PW, Fitzgeorge RB, Witt K (1962) Foetal erythritol: a cause of the localization of Brucella abortus in bovine contagious abortion. Nature 193:47–49PubMedCrossRef
170.
go back to reference Sohlenkamp C, Lopez-Lara IM, Geiger O (2003) Biosynthesis of phosphatidylcholine in bacteria. Prog Lipid Res 42:115–162PubMedCrossRef Sohlenkamp C, Lopez-Lara IM, Geiger O (2003) Biosynthesis of phosphatidylcholine in bacteria. Prog Lipid Res 42:115–162PubMedCrossRef
171.
go back to reference Sohn AH, Probert WS, Glaser CA, Gupta N, Bollen AW, Wong JD, Grace EM, McDonald WC (2003) Human neurobrucellosis with intracerebral granuloma caused by a marine mammal Brucella spp. Emerg Infect Dis 9:485–488PubMed Sohn AH, Probert WS, Glaser CA, Gupta N, Bollen AW, Wong JD, Grace EM, McDonald WC (2003) Human neurobrucellosis with intracerebral granuloma caused by a marine mammal Brucella spp. Emerg Infect Dis 9:485–488PubMed
172.
go back to reference Sola-Landa A, Pizarro-Cerdá J, Grilló MJ, Moriyón E, Blasco JM, Gorvel JP, López-Goñi I (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 29:125–138PubMedCrossRef Sola-Landa A, Pizarro-Cerdá J, Grilló MJ, Moriyón E, Blasco JM, Gorvel JP, López-Goñi I (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 29:125–138PubMedCrossRef
173.
go back to reference Spera JM, Ugalde JE, Mucci J, Comerci DJ, Ugalde RA (2006) A B lymphocyte mitogen is a Brucella abortus virulence factor required for persistent infection. Proc Natl Acad Sci USA 103:16514–16519PubMedCrossRef Spera JM, Ugalde JE, Mucci J, Comerci DJ, Ugalde RA (2006) A B lymphocyte mitogen is a Brucella abortus virulence factor required for persistent infection. Proc Natl Acad Sci USA 103:16514–16519PubMedCrossRef
174.
go back to reference Sperry JF, Robertson DC (1975) Erythritol catabolism by Brucella abortus. J Bacteriol 121:619–630PubMed Sperry JF, Robertson DC (1975) Erythritol catabolism by Brucella abortus. J Bacteriol 121:619–630PubMed
175.
go back to reference Sriranganathan N, Boyle SM, Schurig G, Misra H (1991) Superoxide dismutases of virulent and avirulent strains of Brucella abortus. Vet Microbiol 26:359–366PubMedCrossRef Sriranganathan N, Boyle SM, Schurig G, Misra H (1991) Superoxide dismutases of virulent and avirulent strains of Brucella abortus. Vet Microbiol 26:359–366PubMedCrossRef
176.
go back to reference Starr T, Ng TW, Wehrly TD, Knodler LA, Celli J (2008) Brucella intracellular replication requires trafficking through the late endosomal/lysosomal compartment. Traffic 9:678–694PubMedCrossRef Starr T, Ng TW, Wehrly TD, Knodler LA, Celli J (2008) Brucella intracellular replication requires trafficking through the late endosomal/lysosomal compartment. Traffic 9:678–694PubMedCrossRef
177.
go back to reference Storz G, Opdyke JA, Zhang A (2004) Controlling mRNA stability and translation with small, noncoding RNAs. Curr Opin Microbiol 7:140–144PubMedCrossRef Storz G, Opdyke JA, Zhang A (2004) Controlling mRNA stability and translation with small, noncoding RNAs. Curr Opin Microbiol 7:140–144PubMedCrossRef
178.
go back to reference Swartz TE, Tseng TS, Frederickson MA, Paris G, Comerci DJ, Rajashekara G, Kim JG, Mudgett MB, Splitter GA, Ugalde RA, Goldbaum FA, Briggs WR, Bogomolni RA (2007) Blue-light-activated histidine kinases: two-component sensors in bacteria. Science 317:1090–1093PubMedCrossRef Swartz TE, Tseng TS, Frederickson MA, Paris G, Comerci DJ, Rajashekara G, Kim JG, Mudgett MB, Splitter GA, Ugalde RA, Goldbaum FA, Briggs WR, Bogomolni RA (2007) Blue-light-activated histidine kinases: two-component sensors in bacteria. Science 317:1090–1093PubMedCrossRef
179.
go back to reference Taketani S (2005) Acquisition, mobilization and utilization of cellular iron and heme: endless findings and growing evidence of tight regulation. Tohoku J Exp Med 205:297–318PubMedCrossRef Taketani S (2005) Acquisition, mobilization and utilization of cellular iron and heme: endless findings and growing evidence of tight regulation. Tohoku J Exp Med 205:297–318PubMedCrossRef
180.
go back to reference Taminiau B, Daykin M, Swift S, Boschiroli ML, Tibor A, Lestrate P, de Bolle X, O’Callaghan D, Williams P, Letesson JJ (2002) Identification of a quorum-sensing signal molecule in the facultative intracellular pathogen Brucella melitensis. Infect Immun 70:3004–3011PubMedCrossRef Taminiau B, Daykin M, Swift S, Boschiroli ML, Tibor A, Lestrate P, de Bolle X, O’Callaghan D, Williams P, Letesson JJ (2002) Identification of a quorum-sensing signal molecule in the facultative intracellular pathogen Brucella melitensis. Infect Immun 70:3004–3011PubMedCrossRef
181.
go back to reference Tatum FM, Detilleux PG, Sacks JM, Halling SM (1992) Construction of a Cu/Zn superoxide dismutase deletion mutant of Brucella abortus: analysis of survival in vitro in epithelial and phagocytic cells and in vivo in mice. Infect Immun 60:2863–2869PubMed Tatum FM, Detilleux PG, Sacks JM, Halling SM (1992) Construction of a Cu/Zn superoxide dismutase deletion mutant of Brucella abortus: analysis of survival in vitro in epithelial and phagocytic cells and in vivo in mice. Infect Immun 60:2863–2869PubMed
182.
go back to reference Tatum FM, Morfitt DC, Halling SM (1993) Construction of a Brucella abortus RecA mutant and its survival in mice. Microb Pathog 14:177–185PubMedCrossRef Tatum FM, Morfitt DC, Halling SM (1993) Construction of a Brucella abortus RecA mutant and its survival in mice. Microb Pathog 14:177–185PubMedCrossRef
183.
go back to reference Ugalde JE, Czibener C, Feldman MF, Ugalde RA (2000) Identification and characterization of the Brucella abortus phosphoglucomutase gene: role of lipopolysaccharide in virulence and intracellular multiplication. Infect Immun 68:5716–5723PubMedCrossRef Ugalde JE, Czibener C, Feldman MF, Ugalde RA (2000) Identification and characterization of the Brucella abortus phosphoglucomutase gene: role of lipopolysaccharide in virulence and intracellular multiplication. Infect Immun 68:5716–5723PubMedCrossRef
184.
go back to reference Uzureau S, Godefroid M, Deschamps C, Lemaire J, de Bolle X, Letesson JJ (2007) Mutations of the quorum sensing-dependent regulator VjbR lead to drastic surface modifications in Brucella melitensis. J Bacteriol 189:6035–6047PubMedCrossRef Uzureau S, Godefroid M, Deschamps C, Lemaire J, de Bolle X, Letesson JJ (2007) Mutations of the quorum sensing-dependent regulator VjbR lead to drastic surface modifications in Brucella melitensis. J Bacteriol 189:6035–6047PubMedCrossRef
185.
go back to reference Valderas M, Alcantara RB, Baumgartner JE, Bellaire BH, Robertson GT, Ng WL, Richardson JM, Winkler ME, Roop RM II (2005) Role of HdeA in acid resistance and virulence in Brucella abortus 2308. Vet Microbiol 107:307–312PubMedCrossRef Valderas M, Alcantara RB, Baumgartner JE, Bellaire BH, Robertson GT, Ng WL, Richardson JM, Winkler ME, Roop RM II (2005) Role of HdeA in acid resistance and virulence in Brucella abortus 2308. Vet Microbiol 107:307–312PubMedCrossRef
186.
go back to reference Valentin-Hansen P, Eriksen M, Udesen C (2004) The bacterial Sm-like protein: a key player in RNA transactions. Mol Microbiol 51:1525–1533PubMedCrossRef Valentin-Hansen P, Eriksen M, Udesen C (2004) The bacterial Sm-like protein: a key player in RNA transactions. Mol Microbiol 51:1525–1533PubMedCrossRef
188.
go back to reference Waterman SR, Small PLC (1996) Identification of σS-dependent genes associated with the stationary-phase acid-resistance phenotype of Shigella flexneri. Mol Microbiol 21:925–940PubMedCrossRef Waterman SR, Small PLC (1996) Identification of σS-dependent genes associated with the stationary-phase acid-resistance phenotype of Shigella flexneri. Mol Microbiol 21:925–940PubMedCrossRef
189.
go back to reference Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346PubMedCrossRef Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346PubMedCrossRef
190.
go back to reference Weinberg ED (1997) The Lactobacillus anomaly: total iron abstinence. Perspect Biol Med 40:578–583PubMed Weinberg ED (1997) The Lactobacillus anomaly: total iron abstinence. Perspect Biol Med 40:578–583PubMed
191.
go back to reference Wessel M, Klüener S, Gödeke J, Fritz C, Hacker S, Narberhaus F (2006) Virulence of Agrobacterium tumefaciens requires phosphatidylcholine in the bacterial membrane. Mol Microbiol 62:906–915PubMedCrossRef Wessel M, Klüener S, Gödeke J, Fritz C, Hacker S, Narberhaus F (2006) Virulence of Agrobacterium tumefaciens requires phosphatidylcholine in the bacterial membrane. Mol Microbiol 62:906–915PubMedCrossRef
192.
go back to reference Wilson T, de Lisle GW, Marcinkeviciene JA, Blanchard JS, Collins DM (1998) Antisense RNA to ahpC, an oxidative stress defence gene involved in isoniazid resistance, indicates that AhpC of Mycobacterium bovis has virulence properties. Microbiology 144:2687–2695PubMedCrossRef Wilson T, de Lisle GW, Marcinkeviciene JA, Blanchard JS, Collins DM (1998) Antisense RNA to ahpC, an oxidative stress defence gene involved in isoniazid resistance, indicates that AhpC of Mycobacterium bovis has virulence properties. Microbiology 144:2687–2695PubMedCrossRef
193.
go back to reference Winter AJ, Schurig GG, Boyle SM, Sriranganathan N, Bevins JS, Enright FM, Elzer PH, Kopec JD (1996) Protection of BALB/c mice against homologous and heterologous species of Brucella by rough strain vaccines derived from Brucella melitensis and Brucella suis biovar 4. Am J Vet Res 57:677–683PubMed Winter AJ, Schurig GG, Boyle SM, Sriranganathan N, Bevins JS, Enright FM, Elzer PH, Kopec JD (1996) Protection of BALB/c mice against homologous and heterologous species of Brucella by rough strain vaccines derived from Brucella melitensis and Brucella suis biovar 4. Am J Vet Res 57:677–683PubMed
194.
go back to reference Wu Q, Pei J, Turse C, Ficht TA (2006) Mariner mutagenesis of Brucella melitensis reveals genes with previously uncharacterized roles in virulence and survival. BMC Microbiol 6:102PubMedCrossRef Wu Q, Pei J, Turse C, Ficht TA (2006) Mariner mutagenesis of Brucella melitensis reveals genes with previously uncharacterized roles in virulence and survival. BMC Microbiol 6:102PubMedCrossRef
195.
go back to reference Yang X, Becker T, Walters N, Pascual DW (2006) Deletion of znuA virulence factor attenuates Brucella abortus and confers protection against wild-type challenge. Infect Immun 74:3874–3879PubMedCrossRef Yang X, Becker T, Walters N, Pascual DW (2006) Deletion of znuA virulence factor attenuates Brucella abortus and confers protection against wild-type challenge. Infect Immun 74:3874–3879PubMedCrossRef
196.
go back to reference Young EJ (2005) Brucella species. In: Mandell GL, Bennett JE, Dolin R (eds) Mandell, Douglas and Bennett’s principles and practice of infectious diseases, 6th edn. Elsevier Churchill Livingstone, Philadelphia, pp 2669–2685 Young EJ (2005) Brucella species. In: Mandell GL, Bennett JE, Dolin R (eds) Mandell, Douglas and Bennett’s principles and practice of infectious diseases, 6th edn. Elsevier Churchill Livingstone, Philadelphia, pp 2669–2685
197.
go back to reference Zarahik ML, Cullen VL, Fung AM, Libby SJ, Choy SLK, Coburn B, Kehres DG, Maguire ME, Fang FC, Finlay BB (2004) The Salmonella enterica serovar Typhimurium divalent cation transport systems MntH and SitABCD are essential for virulence in an Nramp1 G169 murine typhoid model. Infect Immun 72:5522–5525CrossRef Zarahik ML, Cullen VL, Fung AM, Libby SJ, Choy SLK, Coburn B, Kehres DG, Maguire ME, Fang FC, Finlay BB (2004) The Salmonella enterica serovar Typhimurium divalent cation transport systems MntH and SitABCD are essential for virulence in an Nramp1 G169 murine typhoid model. Infect Immun 72:5522–5525CrossRef
198.
go back to reference Zygmunt MS, Hagius SD, Walker JV, Elzer PH (2006) Identification of Brucella melitensis 16M genes required for bacterial survival in the caprine host. Microbes Infect 8:2849–2854PubMedCrossRef Zygmunt MS, Hagius SD, Walker JV, Elzer PH (2006) Identification of Brucella melitensis 16M genes required for bacterial survival in the caprine host. Microbes Infect 8:2849–2854PubMedCrossRef
Metadata
Title
Survival of the fittest: how Brucella strains adapt to their intracellular niche in the host
Authors
R. Martin Roop II
Jennifer M. Gaines
Eric S. Anderson
Clayton C. Caswell
Daniel W. Martin
Publication date
01-11-2009
Publisher
Springer-Verlag
Published in
Medical Microbiology and Immunology / Issue 4/2009
Print ISSN: 0300-8584
Electronic ISSN: 1432-1831
DOI
https://doi.org/10.1007/s00430-009-0123-8

Other articles of this Issue 4/2009

Medical Microbiology and Immunology 4/2009 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.