Erythritol triggers expression of virulence traits in Brucella melitensis

Microbes and Infection

Volumn 15, Issue 6-7, 2013, Pages 440-449

  Petersen, Erik ^a   Rajashekara, Gireesh ^b   Sanakkayala, Neelima ^a   Eskra, Linda ^a   Harms, Jerome ^a   Splitter, Gary ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Brucella; Erythritol; Flagella; Virulence

Indexed keywords

ERYTHRITOL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BRUCELLA; BRUCELLA MELITENSIS; BRUCELLOSIS; CELL DIVISION; CELL INFILTRATION; GENE EXPRESSION; GROWTH INHIBITION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; UPREGULATION;

ANIMALS; BRUCELLA MELITENSIS; BRUCELLOSIS; DISEASE MODELS, ANIMAL; ERYTHRITOL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; MACROPHAGES; MICE; MICROARRAY ANALYSIS; VIRULENCE FACTORS;

BRUCELLA; BRUCELLA MELITENSIS; CAPRA HIRCUS; MUS; SUIDAE;

EID: 84879184111     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2013.02.002     Document Type: Article

References (46)

1. Pappas G., Akritidis N., Bosilkovski M., Tsianos E. Brucellosis. N. Engl. J. Med. 2005, 352:2325-2336.
2. Glynn M.K., Lynn T.V. Brucellosis. J. Am. Vet. Med. Assoc. 2008, 233:900-908.
3. Alexander B., Schnurrenberger P.R., Brown R.R. Numbers of Brucella abortus in the placenta, umbilicus and fetal fluid of two naturally infected cows. Vet. Rec. 1981, 108:500.
4. Smith H., Williams A.E., Pearce J.H., Keppie J., Harris-Smith P.W., Fitz-George R.B., Witt K. Foetal erythritol: a cause of the localization of Brucella abortus in bovine contagious abortion. Nature 1962, 193:47-49.
5. Williams A.E., Keppie J., Smith H. The relation of erythritol usage to virulence in the brucellas. J. Gen. Microbiol. 1964, 37:285-292.
6. Meyer M.E. Metabolic characterization of the genus Brucella. V. Relationship of strain oxidation rate of i-erythritol to strain virulence for guinea pigs. J. Bacteriol. 1966, 92:584-588.
7. Sangari F.J., Grillo M.J., Jimenez De Bagues M.P., Gonzalez-Carrero M.I., Garcia-Lobo J.M., Blasco J.M., Aguero J. The defect in the metabolism of erythritol of the Brucella abortus B19 vaccine strain is unrelated with its attenuated virulence in mice. Vaccine 1998, 16:1640-1645.
8. Burkhardt S., Jimenez de Bagues M.P., Liautard J.P., Kohler S. Analysis of the behavior of eryC mutants of Brucella suis attenuated in macrophages. Infect. Immun. 2005, 73:6782-6790.
9. Anderson J.D., Smith H. The metabolism of erythritol by Brucella abortus. J. Gen. Microbiol. 1965, 38:109-124.
10. Sangari F.J., Aguero J., Garcia-Lobo J.M. The genes for erythritol catabolism are organized as an inducible operon in Brucella abortus. Microbiology 2000, 146(Pt 2):487-495.
11. Rajashekara G., Glover D.A., Krepps M., Splitter G.A. Temporal analysis of pathogenic events in virulent and avirulent Brucella melitensis infections. Cell. Microbiol. 2005, 7:1459-1473.
12. Plommet M. Minimal requirements for growth of Brucella suis and other Brucella species. Zentralbl Bakteriol 1991, 275:436-450.
13. Chen C.Y., Nace G.W., Irwin P.L. A 6×6 drop plate method for simultaneous colony counting and MPN enumeration of Campylobacter jejuni, Listeria monocytogenes, and Escherichia coli. J. Microbiol. Methods 2003, 55:475-479.
14. Petersen E., Chaudhuri P., Gourley C., Harms J., Splitter G. Brucella melitensis cyclic di-GMP phosphodiesterase BpdA controls expression of flagellar genes. J. Bacteriol. 2011, 193:5683-5691.
15. Rambow-Larsen A.A., Rajashekara G., Petersen E., Splitter G. Putative quorum-sensing regulator BlxR of Brucella melitensis regulates virulence factors including the type IV secretion system and flagella. J. Bacteriol. 2008, 190:3274-3282.
16. Rajashekara G., Glasner J.D., Glover D.A., Splitter G.A. Comparative whole-genome hybridization reveals genomic islands in Brucella species. J. Bacteriol. 2004, 186:5040-5051.
17. Kendziorski C.M., Newton M.A., Lan H., Gould M.N. On parametric empirical Bayes methods for comparing multiple groups using replicated gene expression profiles. Stat. Med. 2003, 22:3899-3914.
18. Newton M.A., Kendziorski C.M., Richmond C.S., Blattner F.R., Tsui K.W. On differential variability of expression ratios: improving statistical inference about gene expression changes from microarray data. J. Comput. Biol. 2001, 8:37-52.
19. Keppie J., Williams A.E., Witt K., Smith H. The role of erythritol in the tissue localization of the Brucellae. Br. J. Exp. Pathol. 1965, 46:104-108.
20. Carvalho Neta A.V., Stynen A.P., Paixao T.A., Miranda K.L., Silva F.L., Roux C.M., Tsolis R.M., Everts R.E., Lewin H.A., Adams L.G., Carvalho A.F., Lage A.P., Santos R.L. Modulation of the bovine trophoblastic innate immune response by Brucella abortus. Infect. Immun. 2008, 76:1897-1907.
21. Mc C.N., Beal G.A. Growth and manometric studies on carbohydrate utilization of Brucella. J. Infect. Dis. 1951, 89:266-271.
22. Meyer M.E. Metabolic characterization of the genus Brucella. VI. Growth stimulation by i-erythritol compared with strain virulence for guinea pigs. J. Bacteriol. 1967, 93:996-1000.
23. Keppie J., Witt K., Smith H. The effect of erythritol on the growth of S19 and other attenuated strains of Brucella abortus. Res. Vet. Sci. 1967, 8:294-296.
24. Williams A.E., Keppie J., Smith H. The chemical basis of the virulence of Brucella abortus. III. Foetal erythritol a cause of the localisation of Brucella abortus in pregnant cows. Br. J. Exp. Pathol. 1962, 43:530-537.
25. Fretin D., Fauconnier A., Kohler S., Halling S., Leonard S., Nijskens C., Ferooz J., Lestrate P., Delrue R.M., Danese I., Vandenhaute J., Tibor A., DeBolle X., Letesson J.J. The sheathed flagellum of Brucella melitensis is involved in persistence in a murine model of infection. Cell. Microbiol. 2005, 7:687-698.
26. Bosseray N. Kinetics of placental colonization of mice inoculated intravenously with Brucella abortus at day 15 of pregnancy. Br. J. Exp. Pathol. 1983, 64:612-616.
27. Joshi D.V., Prakash O. Effect of erythritol on different strains of Brucella melitensis. Indian J. Pathol. Bacteriol. 1970, 13:166-172.
28. Parent M.A., Bellaire B.H., Murphy E.A., Roop R.M., Elzer P.H., Baldwin C.L. Brucella abortus siderophore 2,3-dihydroxybenzoic acid (DHBA) facilitates intracellular survival of the bacteria. Microb. Pathog. 2002, 32:239-248.
29. Bellaire B.H., Elzer P.H., Baldwin C.L., Roop R.M. 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 invitro. Infect. Immun. 2003, 71:2927-2932.
30. Jain N., Rodriguez A.C., Kimsawatde G., Seleem M.N., Boyle S.M., Sriranganathan N. Effect of entF deletion on iron acquisition and erythritol metabolism by Brucella abortus 2308. FEMS Microbiol. Lett. 2011, 316:1-6.
31. Eskra L., Covert J., Glasner J., Splitter G. Differential expression of iron acquisition genes by Brucella melitensis and Brucella canis during macrophage infection. PLoS One 2012, 7:e31747.
32. Rest R.F., Robertson D.C. Characterization of the electron transport system in Brucella abortus. J. Bacteriol. 1975, 122:139-144.
33. Sperry J.F., Robertson D.C. Erythritol catabolism by Brucella abortus. J.Bacteriol. 1975, 121:619-630.
34. Delrue R.M., Deschamps C., Leonard S., Nijskens C., Danese I., Schaus J.M., Bonnot S., Ferooz J., Tibor A., De Bolle X., Letesson J.J. A quorum-sensing regulator controls expression of both the type IV secretion system and the flagellar apparatus of Brucella melitensis. Cell. Microbiol. 2005, 7:1151-1161.
35. de Jong M.F., Sun Y.H., den Hartigh A.B., van Dijl J.M., Tsolis R.M. 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. 2008, 70:1378-1396.
36. den Hartigh A.B., Rolan H.G., de Jong M.F., Tsolis R.M. VirB3 to VirB6 and VirB8 to VirB11, but not VirB7, are essential for mediating persistence of Brucella in the reticuloendothelial system. J. Bacteriol. 2008, 190:4427-4436.
37. den Hartigh A.B., Sun Y.H., Sondervan D., Heuvelmans N., Reinders M.O., Ficht T.A., Tsolis R.M. Differential requirements for VirB1 and VirB2 during Brucella abortus infection. Infect. Immun. 2004, 72:5143-5149.
38. Abdallah A.I., Commander N.J., Woodward M.J., Spencer S., Hart C.A., Winstanley C. Type III secretion homologs are present in Brucella melitensis, B. ovis, and B. suis biovars 1, 2, and 3. Curr. Microbiol. 2003, 46:241-245.
39. Zygmunt M.S., Hagius S.D., Walker J.V., Elzer P.H. Identification of Brucella melitensis 16M genes required for bacterial survival in the caprine host. Microbes Infect. 2006, 8:2849-2854.
40. Miao E.A., Andersen-Nissen E., Warren S.E., Aderem A. TLR5 and Ipaf: dual sensors of bacterial flagellin in the innate immune system. Semin. Immunopathol. 2007, 29:275-288.
41. Wolfe A.J., Visick K.L. Get the message out: cyclic-Di-GMP regulates multiple levels of flagellum-based motility. J. Bacteriol. 2008, 190:463-475.
42. Karaolis D.K., Means T.K., Yang D., Takahashi M., Yoshimura T., Muraille E., Philpott D., Schroeder J.T., Hyodo M., Hayakawa Y., Talbot B.G., Brouillette E., Malouin F. Bacterial c-di-GMP is an immunostimulatory molecule. J. Immunol. 2007, 178:2171-2181.
43. Yan H., Chen W. 3',5'-Cyclic diguanylic acid: a small nucleotide that makes big impacts. Chem. Soc. Rev. 2010, 39:2914-2924.
44. Burdette D.L., Monroe K.M., Sotelo-Troha K., Iwig J.S., Eckert B., Hyodo M., Hayakawa Y., Vance R.E. STING is a direct innate immune sensor of cyclic di-GMP. Nature 2011, 478:515-518.
45. Barbier T., Nicolas C., Letesson J.J. Brucella adaptation and survival at the crossroad of metabolism and virulence. FEBS Lett. 2011, 585:2929-2934.
46. Starr T., Child R., Wehrly T.D., Hansen B., Hwang S., Lopez-Otin C., Virgin H.W., Celli J. Selective subversion of autophagy complexes facilitates completion of the Brucella intracellular cycle. Cell Host Microbe 2012, 11:33-45.