Differential expression of iron acquisition genes by Brucella melitensis and Brucella canis during macrophage infection

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Eskra, Linda ^a   Covert, Jill ^b   Glasner, Jeremy ^a   Splitter, Gary ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; BACTERIAL GENE; BRUCELLA CANIS; BRUCELLA MELITENSIS; BRUCELLOSIS; CONTROLLED STUDY; ENTEROBACTIN GENE; FERRIC ANGUIBACTIN GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE OVEREXPRESSION; IRON TRANSPORT; MACROPHAGE FUNCTION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; RNA ISOLATION; TONB GENE; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; ANIMAL; CELL LINE; CYTOLOGY; DNA MICROARRAY; GENETICS; INTRACELLULAR SPACE; ISOLATION AND PURIFICATION; MACROPHAGE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; REPRODUCIBILITY; SPECIES DIFFERENCE; TIME;

ANIMALIA; BACTERIA (MICROORGANISMS); BRUCELLA; BRUCELLA MELITENSIS; BRUCELLA MELITENSIS BIOVAR CANIS; MAMMALIA; MURINAE;

BACTERIAL RNA; IRON; TRANSCRIPTOME;

ANIMALS; BRUCELLA CANIS; BRUCELLA MELITENSIS; CELL LINE; GENES, BACTERIAL; INTRACELLULAR SPACE; IRON; MACROPHAGES; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REPRODUCIBILITY OF RESULTS; RNA, BACTERIAL; SPECIES SPECIFICITY; TIME FACTORS; TRANSCRIPTOME;

EID: 84857715761     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031747     Document Type: Article

References (52)

1. Paulley JT, Anderson ES, Roop RM, (2007) Brucella abortus requires the heme transporter BhuA for maintenance of chronic infection in BALB/c mice. Infect Immun 75: 5248-5254.
2. Lopez-Goni I, Moriyon I, Neilands JB, (1992) Identification of 2,3-dihydroxybenzoic acid as a Brucella abortus siderophore. Infect Immun 60: 4496-4503.
3. Braun V, (2001) Iron uptake mechanisms and their regulation in pathogenic bacteria. Int J Med Microbiol 291: 67-79.
4. Noinaj N, Guillier M, Barnard TJ, Buchanan SK, (2010) TonB-dependent transporters: regulation, structure, and function. Annu Rev Microbiol 64: 43-60.
5. Martirosyan A, Moreno E, Gorvel JP, (2011) An evolutionary strategy for a stealthy intracellular Brucella pathogen. Immunol Rev 240: 211-234.
6. Lapaque NFF, de Chastellier C, Mishal Z, Jolly G, Moreno E, et al. (2006) Characterization of Brucella abortus lipopolysaccharide macrodomains as mega rafts. Cell Microbiol 8: 197-206.
7. Rajashekara G, Glasner JD, Glover DA, Splitter GA, (2004) Comparative whole-genome hybridization reveals genomic islands in Brucella species. J Bacteriol 186: 5040-5051.
8. Watarai MMS, Fujii Y, Okamoto K, Shirahata T, (2002) Modulation of Brucella-induced macropinocytosis by lipid rafts mediates intracellular replication. Cell Microbiol 4: 341-355.
9. Detilleux PG, Deyoe BL, Cheville NF, (1990) Entry and intracellular localization of Brucella spp. in Vero cells: fluorescence and electron microscopy. Vet Pathol 27: 317-328.
10. 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: 1481-1490.
11. Talaat AM, Hunter P, Johnston SA, (2000) Genome-directed primers for selective labeling of bacterial transcripts for DNA microarray analysis. Nat Biotechnol 18: 679-682.
12. Kendziorski C, Newton M, Lan H, Gould M, (2003) On parametric empirical Bayes methods for comparing multiple groups using replicated gene expression profiles. Stat Med 22: 3899-3914.
13. Pruitt KD, Tatusova T, Maglott DR, (2007) NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 35: D61-65.
14. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, et al. (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4: 41.
15. Snyder EE, Kampanya N, Lu J, Nordberg EK, Karur HR, et al. (2007) PATRIC: the VBI PathoSystems Resource Integration Center. Nucleic Acids Res 35: D401-406.
16. Pfaffl M, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
17. Eskra L, Canavessi A, Carey M, Splitter G, (2001) Brucella abortus genes identified following constitutive growth and macrophage infection. Infect Immun 69: 7736-7742.
18. Rittig MG, Kaufmann A, Robins A, Shaw B, Sprenger H, et al. (2003) Smooth and rough lipopolysaccharide phenotypes of Brucella induce different intracellular trafficking and cytokine/chemokine release in human monocytes. J Leukoc Biol 74: 1045-1055.
19. Sathiyaseelan J, Jiang X, Baldwin CL, (2000) Growth of Brucella abortus in macrophages from resistant and susceptible mouse strains. Clin Exp Immunol 121: 289-294.
20. Caron E, Liautard JP, Köhler S, (1994) Differentiated U937 cells exhibit increased bactericidal activity upon LPS activation and discriminate between virulent and avirulent Listeria and Brucella species. J Leukoc Biol 56: 174-181.
21. Lourenço RF, Kohler C, Gomes SL, (2011) A two-component system, an anti-sigma factor and two paralogous ECF sigma factors are involved in the control of general stress response in Caulobacter crescentus. Mol Microbiol 80: 1598-1612.
22. Staron A, Mascher T, (2010) General stress response in α-proteobacteria: PhyR and beyond. Mol Microbiol 78: 271-277.
23. Herrou J, Foreman R, Fiebig A, Crosson S, (2010) A structural model of anti-anti-σ inhibition by a two-component receiver domain: the PhyR stress response regulator. Mol Microbiol 78: 290-304.
24. Singh V, Chandra D, Srivastava BS, Srivastava R, (2011) Downregulation of Rv0189c, encoding a dihydroxyacid dehydratase, affects growth of Mycobacterium tuberculosis in vitro and in mice. Microbiology 157: 38-46.
25. Eschenbrenner M, Horn TA, Wagner MA, Mujer CV, Miller-Scandle TL, et al. (2006) Comparative proteome analysis of laboratory grown Brucella abortus 2308 and Brucella melitensis 16 M. J Proteome Res 5: 1731-1740.
26. Venugopal A, Bryk R, Shi S, Rhee K, Rath P, et al. (2011) Virulence of Mycobacterium tuberculosis depends on lipoamide dehydrogenase, a member of three multienzyme complexes. Cell Host Microbe 9.
27. Beckett D, (2005) The Escherichia coli biotin regulatory system: a transcriptional switch. J Nutr Biochem 16: 411-415.
28. Zolkiewski M, (2006) A camel passes through the eye of a needle: protein unfolding activity of Clp ATPases. Mol Microbiol 61: 1094-1100.
29. Köhler SEE, Paquet JY, Walravens K, Teyssier J, Godfroid J, et al. (2002) Induction of dnaK through its native heat shock promoter is necessary for intramacrophagic replication of Brucella suis. Infect Immun 70: 1631-1634.
30. Ekaza E, Guilloteau L, Teyssier J, Liautard JP, Köhler S, (2000) Functional analysis of the ClpATPase ClpA of Brucella suis, and persistence of a knockout mutant in BALB/c mice. Microbiology 146: 1605-1616.
31. Phillips RW, Roop RM, (2001) 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.
32. Roop RM, Phillips RW, Hagius S, Walker JV, Booth NJ, et al. (2001) Re-examination of the role of the Brucella melitensis HtrA stress response protease in virulence in pregnant goats. Vet Microbiol 82: 91-95.
33. Iwanczyk J, Leong V, Ortega J, (2011) Factors Defining the Functional Oligomeric State of Escherichia coli DegP Protease. PLoS One 6: e18944.
34. Gandara B, Merino AL, Rogel MA, Martinez-Romero E, (2001) Limited genetic diversity of Brucella spp. J Clin Microbiol 39: 235-240.
35. Verger JM, Grimont F, Grimont PA, Grayon M, (1985) Brucella, a monospecific genus as shown by deoxyribonucleic acid hybridization. Int J Syst Bacteriol 35: 292-295.
36. Hsieh PF, Lin TL, Lee CZ, Tsai SF, Wang JT, (2008) Serum-induced iron-acquisition systems and TonB contribute to virulence in Klebsiella pneumoniae causing primary pyogenic liver abscess. J Infect Dis 197: 1717-1727.
37. Parent MA, Bellaire BH, Murphy EA, Roop RM, Elzer PH, et al. (2002) Brucella abortus siderophore 2,3-dihydroxybenzoic acid (DHBA) facilitates intracellular survival of the bacteria. Microb Pathog 32: 239-248.
38. Bellaire BH, Elzer PH, Hagius S, Walker J, Baldwin CL, et al. (2003) Genetic organization and iron-responsive regulation of the Brucella abortus 2,3-dihydroxybenzoic acid biosynthesis operon, a cluster of genes required for wild-type virulence in pregnant cattle. Infect Immun 71: 1794-1803.
39. Gonzalez Carrero MI, Sangari FJ, Aguero J, Garcia Lobo JM, (2002) Brucella abortus strain 2308 produces brucebactin, a highly efficient catecholic siderophore. Microbiology 148: 353-360.
40. Bellaire B, Elzer P, Baldwin C, Roop R, (1999) The siderophore 2,3-dihydroxybenzoic acid is not required for virulence of Brucella abortus in BALB/c mice. Infect Immun 67: 2615-2618.
41. Jain N, Rodriguez AC, Kimsawatde G, Seleem MN, Boyle SM, et al. (2011) Effect of entF deletion on iron acquisition and erythritol metabolism by Brucella abortus 2308. FEMS Microbiol Lett 316: 1-6.
42. Martínez M, Ugalde RA, Almirón M, (2006) Irr regulates brucebactin and 2,3-dihydroxybenzoic acid biosynthesis, and is implicated in the oxidative stress resistance and intracellular survival of Brucella abortus. Microbiology 152: 2591-2598.
43. Hibbing M, Fuqua C, (2011) Anti-parallel and Interlinked Control of Cellular Iron Levels by the Irr and RirA Regulators of Agrobacterium tumefaciens. J Bacteriol 193: 3461-3472.
44. Tsolis RM, Baumler AJ, Heffron F, Stojiljkovic I, (1996) Contribution of TonB- and Feo-mediated iron uptake to growth of Salmonella typhimurium in the mouse. Infect Immun 64: 4549-4556.
45. Reeves SA, Torres AG, Payne SM, (2000) TonB is required for intracellular growth and virulence of Shigella dysenteriae. Infect Immun 68: 6329-6336.
46. Danese I, Haine V, Delrue RM, Tibor A, Lestrate P, et al. (2004) The Ton system, an ABC transporter, and a universally conserved GTPase are involved in iron utilization by Brucella melitensis 16 M. Infect Immun 72: 5783-5790.
47. Brickman TJ, Kang HY, Armstrong SK, (2001) Transcriptional activation of Bordetella alcaligin siderophore genes requires the AlcR regulator with alcaligin as inducer. J Bacteriol 183: 483-489.
48. Anderson ES, Paulley JT, Roop RM, (2008) The AraC-like transcriptional regulator DhbR is required for maximum expression of the 2,3-dihydroxybenzoic acid biosynthesis genes in Brucella abortus 2308 in response to iron deprivation. J Bacteriol 190: 1838-1842.
49. Lamontagne J, Béland M, Forest A, Côté-Martin A, Nassif N, et al. (2010) Proteomics-based confirmation of protein expression and correction of annotation errors in the Brucella abortus genome. BMC Genomics 11: 300.
50. Supuran CT, Scozzafava A, Clare BW, (2002) Bacterial protease inhibitors. Med Res Rev 22: 329-372.
51. Koprivnjak T, Peschel A, (2011) Bacterial resistance mechanisms against host defense peptides. Cell Mol Life Sci May 11 [Epub ahead of print].
52. Steele KH, Baumgartner JE, Valderas MW, Roop RM, (2010) Comparative study of the roles of AhpC and KatE as respiratory antioxidants in Brucella abortus 2308. J Bacteriol 192: 4912-4922.