Brucella pathogenesis, genes identified from random large-scale screens

FEMS Microbiology Letters

Volumn 231, Issue 1, 2004, Pages 1-12

  Delrue, Rose May ^a   Lestrate, Pascal ^a   Tibor, Anne ^a   Letesson, Jean Jacques ^a   De Bolle, Xavier ^a  

^a UNIVERSITY OF NAMUR   (Belgium)

Author keywords

Brucella; Intracellular survival; Virulence

Indexed keywords

ADHESIN; AMINO ACID; BACTERIAL DNA; BACTERIAL RNA; BACTERIAL TOXIN; CHAPERONE; METAL; NITROGEN; OUTER MEMBRANE PROTEIN; PEPTIDOGLYCAN; SUGAR; VIRULENCE FACTOR; VITAMIN;

AMINO ACID METABOLISM; BACTERIAL COLONIZATION; BACTERIAL FLAGELLUM; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIAL MEMBRANE; BACTERIAL METABOLISM; BACTERIAL VIRULENCE; BACTERIUM MUTANT; BACTERIUM PILUS; BRUCELLA; BRUCELLA MELITENSIS; BRUCELLA SUIS; BRUCELLOSIS; CARBOHYDRATE METABOLISM; CARBOHYDRATE TRANSPORT; DNA METABOLISM; EUKARYOTIC CELL; FIMBRIA; GENE FUNCTION; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC CODE; GENETIC SCREENING; GRAM NEGATIVE BACTERIUM; HOST PATHOGEN INTERACTION; HUMAN; METAL METABOLISM; NITROGEN METABOLISM; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PATHOGENICITY; PATHOGENICITY ISLAND; PLASMID; PRIORITY JOURNAL; REDUCTION; REGULATORY MECHANISM; RNA METABOLISM; SECRETION; SHORT SURVEY; STRESS; SYMBIOSIS; UNINDEXED SEQUENCE;

BACTERIA (MICROORGANISMS); BRUCELLA; BRUCELLA MELITENSIS BIOVAR SUIS; EUKARYOTA; PROTEOBACTERIA;

EID: 0842265916     PISSN: 03781097     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0378-1097(03)00963-7     Document Type: Short Survey

References (87)

1. DelVecchio V.G., Kapatral V., Elzer P., Patra G., Mujer C.V. The genome of Brucella melitensis. Vet. Microbiol. 90:2002;587-592.
2. Paulsen I.T., Seshadri R., Nelson K.E., Eisen J.A., Heidelberg J.F., Read T.D., Dodson R.J., Umayam L., Brinkac L.M., Beanan M.J., Daugherty S.C., Deboy R.T., Durkin A.S., Kolonay J.F., Madupu R., Nelson W.C., Ayodeji B., Kraul M., Shetty J., Malek J., Van Aken S.E., Riedmuller S., Tettelin H., Gill S.R., White O., Salzberg S.L., Hoover D.L., Lindler L.E., Halling S.M., Boyle S.M., Fraser C.M. The Brucella suis genome reveals fundamental similarities between animal and plant pathogens and symbionts. Proc. Natl. Acad. Sci. USA. 99:2002;13148-13153.
3. Moreno E., Moriyon I. Brucella melitensis: a nasty bug with hidden credentials for virulence. Proc. Natl. Acad. Sci. USA. 99:2002;1-3.
4. Gorvel J.P., Moreno E. Brucella intracellular life: from invasion to intracellular replication. Vet. Microbiol. 90:2002;281-297.
5. Liautard J.P., Gross A., Dornand J., Köhler S. Interactions between professional phagocytes and Brucella spp. Microbiologia. 12:1996;197-206.
6. Pizarro-Cerda J., Moreno E., Sanguedolce V., Mege J.L., Gorvel J.P. Virulent Brucella abortus prevents lysosome fusion and is distributed within autophagosome-like compartments. Infect. Immun. 66:1998;2387-2392.
7. Pizarro-Cerda J., Meresse S., Parton R.G., van der Goot G., Sola-Landa A., Lopez-Goni I., Moreno E., Gorvel J.P. Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes. Infect. Immun. 66:1998;5711-5724.
8. Celli J., de Chastellier C., Franchini D.M., Pizarro-Cerda J., Moreno E., Gorvel J.P. Brucella evades macrophage killing via VirB-dependent sustained interactions with the endoplasmic reticulum. J. Exp. Med. 198:2003;545-556.
9. Smith H. What happens to bacterial pathogens in vivo? Trends Microbiol. 6:1998;239-243.
10. Plommet M., Plommet A.M. Virulence of Brucella: bacterial growth and decline in mice. Ann. Rech. Vét. 19:1988;65-67.
11. Kim S., Watarai M., Kondo Y., Erdenebaatar J., Makino S., Shirahata T. Isolation and characterization of mini-Tn5Km2 insertion mutants of Brucella abortus deficient in internalization and intracellular growth in HeLa cells. Infect. Immun. 71:2003;3020-3027.
12. Köhler S., Foulongne V., Ouahrani-Bettache S., Bourg G., Teyssier J., Ramuz M., Liautard J.P. 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. 99:2002;15711-15716.
13. Allen C.A., Adams L.G., Ficht T.A. Transposon-derived Brucella abortus rough mutants are attenuated and exhibit reduced intracellular survival. Infect. Immun. 66:1998;1008-1016.
14. Godfroid F., Taminiau B., Danese I., Denoel P., Tibor A., Weynants V., Cloeckaert A., Godfroid J., Letesson J.J. 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. 66:1998;5485-5493.
15. Delrue, R.-M. (2002) Contribution à l'analyse des mécanismes moléculaires impliqués dans le trafic intracellulaire de Brucella melitensis 16M. Presses Universitaires de Namur, Namur.
16. Delrue R.M., Martinez-Lorenzo M., Lestrate P., Danese I., Bielarz V., Mertens P., De Bolle X., Tibor A., Gorvel J.P., Letesson J.J. Identification of Brucella spp. genes involved in intracellular trafficking. Cell. Microbiol. 3:2001;487-497.
17. O'Callaghan D., Cazevieille C., Allardet-Servent A., Boschiroli M.L., Bourg G., Foulongne V., Frutos P., Kulakov Y., Ramuz M. A homologue of the Agrobacterium tumefaciens VirB and Bordetella pertussis Ptl type IV secretion systems is essential for intracellular survival of Brucella suis. Mol. Microbiol. 33:1999;1210-1220.
18. Sieira R., Comerci D.J., Sanchez D.O., Ugalde R.A. A homologue of an operon required for DNA transfer in Agrobacterium is required in Brucella abortus for virulence and intracellular multiplication. J. Bacteriol. 182:2000;4849-4855.
19. Lestrate P., Delrue R.M., Danese I., Didembourg C., Taminiau B., Mertens P., De Bolle X., Tibor A., Tang C.M., Letesson J.J. Identification and characterization of in vivo attenuated mutants of Brucella melitensis. Mol. Microbiol. 38:2000;543-551.
20. Lestrate P., Dricot A., Delrue R.M., Lambert C., Martinelli V., De Bolle X., Letesson J.J., Tibor A. Attenuated signature-tagged mutagenesis mutants of Brucella melitensis identified during the acute phase of infection in mice. Infect. Immun. 71:2003;7053-7060.
21. Hong P.C., Tsolis R.M., Ficht T.A. Identification of genes required for chronic persistence of Brucella abortus in mice. Infect. Immun. 68:2000;4102-4107.
22. Foulongne V., Bourg G., Cazevieille C., Michaux-Charachon S., O'Callaghan D. Identification of Brucella suis genes affecting intracellular survival in an in vitro human macrophage infection model by signature-tagged transposon mutagenesis. Infect. Immun. 68:2000;1297-1303.
23. Eskra L., Canavessi A., Carey M., Splitter G. Brucella abortus genes identified following constitutive growth and macrophage infection. Infect. Immun. 69:2001;7736-7742.
24. Köhler S., Ouahrani-Bettache S., Layssac M., Teyssier J., Liautard J.P. Constitutive and inducible expression of green fluorescent protein in Brucella suis. Infect. Immun. 67:1999;6695-6697.
25. Jubier-Maurin V., Rodrigue A., Ouahrani-Bettache S., Layssac M., Mandrand-Berthelot M.A., Köhler S., Liautard J.P. Identification of the nik gene cluster of Brucella suis: regulation and contribution to urease activity. J. Bacteriol. 183:2001;426-434.
26. Fernandez-Prada C.M., Zelazowska E.B., Nikolich M., Hadfield T.L., Roop R.M. II, Robertson G.L., Hoover D.L. Interactions between Brucella melitensis and human phagocytes: bacterial surface O-polysaccharide inhibits phagocytosis, bacterial killing, and subsequent host cell apoptosis. Infect. Immun. 71:2003;2110-2119.
27. Porte F., Naroeni A., Ouahrani-Bettache S., Liautard J.P. Role of the Brucella suis lipopolysaccharide O antigen in phagosomal genesis and in inhibition of phagosome-lysosome fusion in murine macrophages. Infect. Immun. 71:2003;1481-1490.
28. Naroeni A., Porte F. Role of cholesterol and the ganglioside GM(1) in entry and short-term survival of Brucella suis in murine macrophages. Infect. Immun. 70:2002;1640-1644.
29. Moriyon I., Lopez-Goni I. Structure and properties of the outer membranes of Brucella abortus and Brucella melitensis. Int. Microbiol. 1:1998;19-26.
30. Tibor A., Wansard V., Bielartz V., Delrue R.M., Danese I., Michel P., Walravens K., Godfroid J., Letesson J.J. Effect of omp10 or omp19 deletion on Brucella abortus outer membrane properties and virulence in mice. Infect. Immun. 70:2002;5540-5544.
31. Guzman-Verri C., Manterola L., Sola-Landa A., Parra A., Cloeckaert A., Garin J., Gorvel J.P., Moriyon I., Moreno E., Lopez-Goni I. 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. 99:2002;12375-12380.
32. Lopez-Goni I., Guzman-Verri C., Manterola L., Sola-Landa A., Moriyon I., Moreno E. Regulation of Brucella virulence by the two-component system BvrR/BvrS. Vet. Microbiol. 90:2002;329-339.
33. Edmonds M.D., Cloeckaert A., Elzer P.H. Brucella species lacking the major outer membrane protein Omp25 are attenuated in mice and protect against Brucella melitensis and Brucella ovis. Vet. Microbiol. 88:2002;205-221.
34. Forestier C., Deleuil F., Lapaque N., Moreno E., Gorvel J.P. Brucella abortus lipopolysaccharide in murine peritoneal macrophages acts as a down-regulator of T cell activation. J. Immunol. 165:2000;5202-5210.
35. Jubier-Maurin V.V., Boigegrain R.A., Cloeckaert A., Gross A., Alvarez-Martinez M.T., Terraza A., Liautard J., Köhler S., Rouot B., Dornand J., Liautard J.P. Major outer membrane protein Omp25 of Brucella suis is involved in inhibition of tumor necrosis factor alpha production during infection of human macrophages. Infect. Immun. 69:2001;4823-4830.
36. Ding Z., Atmakuri K., Christie P.J. The outs and ins of bacterial type IV secretion substrates. Trends Microbiol. 11:2003;527-535.
37. Watarai M., Makino S., Fujii Y., Okamoto K., Shirahata T. Modulation of Brucella-induced macropinocytosis by lipid rafts mediates intracellular replication. Cell Microbiol. 4:2002;341-355.
38. Comerci D.J., Martinez-Lorenzo M.J., Sieira R., Gorvel J.P., Ugalde R.A. Essential role of the VirB machinery in the maturation of the Brucella abortus-containing vacuole. Cell. Microbiol. 3:2001;159-168.
39. Rouot B., Alvarez-Martinez M.T., Marius C., Menanteau P., Guilloteau L., Boigegrain R.A., Zumbihl R., O'Callaghan D., Domke N., Baron C. Production of the type IV secretion system differs among Brucella species as revealed with VirB5- and VirB8-specific antisera. Infect. Immun. 71:2003;1075-1082.
40. Letesson J.J., Lestrate P., Delrue R.M., Danese I., Bellefontaine F., Fretin D., Taminiau B., Tibor A., Dricot A., Deschamps C., Haine V., Leonard S., Laurent T., Mertens P., Vandenhaute J., De Bolle X. Fun stories about Brucella: the 'furtive nasty bug'. Vet. Microbiol. 90:2002;317-328.
41. Young G.M., Schmiel D.H., Miller V.L. A new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein-secretion system. Proc. Natl. Acad. Sci. USA. 96:1999;6456-6461.
42. Luscombe, N.M., Austin, S.E., Berman, H.M. and Thornton, J.M. (2000) An overview of the structures of protein-DNA complexes. Genome Biol. 1, REVIEWS001.1-REVIEWS001.37.
43. Dorrell N., Spencer S., Foulonge V., Guigue-Talet P., O'Callaghan D., Wren B.W. Identification, cloning and initial characterisation of FeuPQ in Brucella suis: a new sub-family of two-component regulatory systems. FEMS Microbiol. Lett. 162:1998;143-150.
44. Sola-Landa A., Pizarro-Cerda J., Grillo M.J., Moreno E., Moriyon I., Blasco J.M., Gorvel J.P., Lopez-Goni I. 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. 29:1998;125-138.
45. Guzman-Verri C., Chaves-Olarte E., von Eichel-Streiber C., Lopez-Goni I., Thelestam M., Arvidson S., Gorvel J.P., Moreno E. GTPases of the Rho subfamily are required for Brucella abortus internalization in nonprofessional phagocytes: direct activation of Cdc42. J. Biol. Chem. 276:2001;44435-44443.
46. Taminiau B., Daykin M., Swift S., Boschiroli M.L., Tibor A., Lestrate P., De Bolle X., O'Callaghan D., Williams P., Letesson J.J. Identification of a quorum-sensing signal molecule in the facultative intracellular pathogen Brucella melitensis. Infect. Immun. 70:2002;3004-3011.
47. Chatterji D., Ojha A.K. Revisiting the stringent response, ppGpp and starvation signaling. Curr. Opin. Microbiol. 4:2001;160-165.
48. Kuroda M., Wilson T.H., Tsuchiya T. Regulation of galactoside transport by the PTS. J. Mol. Microbiol. Biotechnol. 3:2001;381-384.
49. Bellaire B.H., Elzer P.H., Hagius S., Walker J., Baldwin C.L., Roop R.M. II. 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. 71:2003;1794-1803.
50. Eschenbrenner M., Wagner M.A., Horn T.A., Kraycer J.A., Mujer C.V., Hagius S., Elzer P., DelVecchio V.G. Comparative proteome analysis of Brucella melitensis vaccine strain Rev 1 and a virulent strain, 16M. J. Bacteriol. 184:2002;4962-4970.
51. Boschiroli M.L., Ouahrani-Bettache S., Foulongne V., Michaux-Charachon S., Bourg G., Allardet-Servent A., Cazevieille C., Liautard J.P., Ramuz M., O'Callaghan D. The Brucella suis virB operon is induced intracellularly in macrophages. Proc. Natl. Acad. Sci. USA. 99:2002;1544-1549.
52. Essenberg R.C., Seshadri R., Nelson K., Paulsen I. Sugar metabolism by Brucellae. Vet. Microbiol. 90:2002;249-261.
53. Crawford R.M., Van De Verg L., Yuan L., Hadfield T.L., Warren R.L., Drazek E.S., Houng H.H., Hammack C., Sasala K., Polsinelli T., Thompson J., Hoover D.L. Deletion of purE attenuates Brucella melitensis infection in mice. Infect. Immun. 64:1996;2188-2192.
54. Briones G., Inon de Iannino N., Roset M., Vigliocco A., Paulo P.S., Ugalde R.A. Brucella abortus cyclic beta-1,2-glucan mutants have reduced virulence in mice and are defective in intracellular replication in HeLa cells. Infect. Immun. 69:2001;4528-4535.
55. Murphy P.J., Heycke N., Banfalvi Z., Tate M.E., de Bruijn F.J., Kondorosi A., Tempe J., Schell J. Genes for the catabolism and synthesis of an opine-like compound in Rhizobium meliloti are closely linked on the Sym plasmid. Proc. Natl. Acad. Sci. USA. 84:1987;493-497.
56. Murphy P.J., Heycke N., Trenz S.P., Ratet P., de Bruijn F.J., Schell J. Synthesis of an opine-like compound, a rhizopine, in alfalfa nodules is symbiotically regulated. Proc. Natl. Acad. Sci. USA. 85:1988;9133-9137.
57. Bahar M., de Majnik J., Wexler M., Fry J., Poole P.S., Murphy P.J. A model for the catabolism of rhizopine in Rhizobium leguminosarum involves a ferredoxin oxygenase complex and the inositol degradative pathway. Mol. Plant Microbe Interact. 11:1998;1057-1068.
58. Gray J., Wang J., Gelvin S.B. Mutation of the miaA gene of Agrobacterium tumefaciens results in reduced vir gene expression. J. Bacteriol. 174:1992;1086-1098.
59. Murayama N., Shimizu H., Takiguchi S., Baba Y., Amino H., Horiuchi T., Sekimizu K., Miki T. Evidence for involvement of Escherichia coli genes pmbA, csrA and a previously unrecognized gene tldD, in the control of DNA gyrase by letD (ccdB) of sex factor F. J. Mol. Biol. 256:1996;483-502.
60. Scarlato V., Arico B., Rappuoli R. DNA topology affects transcriptional regulation of the pertussis toxin gene of Bordetella pertussis in Escherichia coli and in vitro. J. Bacteriol. 175:1993;4764-4771.
61. Köhler S., Teyssier J., Cloeckaert A., Rouot B., Liautard J.P. Participation of the molecular chaperone DnaK in intracellular growth of Brucella suis within U937-derived phagocytes. Mol. Microbiol. 20:1996;701-712.
62. Ekaza E., Teyssier J., Ouahrani-Bettache S., Liautard J.P., Köhler S. Characterization of Brucella suis clpB and clpAB mutants and participation of the genes in stress responses. J. Bacteriol. 183:2001;2677-2681.
63. Ekaza E., Guilloteau L., Teyssier J., Liautard J.P., Köhler S. Functional analysis of the ClpATPase ClpA of Brucella suis, and persistence of a knockout mutant in BALB/c mice. Microbiology. 146:2000;1605-1616.
64. Endley S., McMurray D., Ficht T.A. Interruption of the cydB locus in Brucella abortus attenuates intracellular survival and virulence in the mouse model of infection. J. Bacteriol. 183:2001;2454-2462.
65. Sperry J.F., Robertson D.C. Erythritol catabolism by Brucella abortus. J. Bacteriol. 121:1975;619-630.
66. Wang M., Qureshi N., Soeurt N., Splitter G. High levels of nitric oxide production decrease early but increase late survival of Brucella abortus in macrophages. Microb. Pathog. 31:2001;221-230.
67. Collet J.F., Bardwell J.C. Oxidative protein folding in bacteria. Mol. Microbiol. 44:2002;1-8.
68. Hacker J., Kaper J.B. Pathogenicity islands and the evolution of microbes. Annu. Rev. Microbiol. 54:2000;641-679.
69. Vergunst A.C., van Lier M.C., den Dulk-Ras A., Hooykaas P.J. Recognition of the Agrobacterium tumefaciens VirE2 translocation signal by the VirB/D4 transport system does not require VirE1. Plant Physiol. 133:2003;978-988.
70. Vergunst A.C., Schrammeijer B., den Dulk-Ras A., de Vlaam C.M., Regensburg-Tuink T.J., Hooykaas P.J. VirB/D4-dependent protein translocation from Agrobacterium into plant cells. Science. 290:2000;979-982.
71. Ugalde J.E., Czibener C., Feldman M.F., Ugalde R.A. Identification and characterization of the Brucella abortus phosphoglucomutase gene: role of lipopolysaccharide in virulence and intracellular multiplication. Infect. Immun. 68:2000;5716-5723.
72. Parent M.A., Bellaire B.H., Murphy E.A., Roop R.M. II, Elzer P.H., Baldwin C.L. Brucella abortus siderophore 2,3-dihydroxybenzoic acid (DHBA) facilitates intracellular survival of the bacteria. Microb. Pathog. 32:2002;239-248.
73. Bellaire B.H., Elzer P.H., Baldwin C.L., Roop R.M. II. The siderophore 2,3-dihydroxybenzoic acid is not required for virulence of Brucella abortus in BALB/c mice. Infect. Immun. 67:1999;2615-2618.
74. Foulongne V., Walravens K., Bourg G., Boschiroli M.L., Godfroid J., Ramuz M., O'Callaghan D. Aromatic compound-dependent Brucella suis is attenuated in both cultured cells and mouse models. Infect. Immun. 69:2001;547-550.
75. LeVier K., Phillips R.W., Grippe V.K., Roop R.M. II, Walker G.C. Similar requirements of a plant symbiont and a mammalian pathogen for prolonged intracellular survival. Science. 287:2000;2492-2493.
76. 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. 16:1998;1640-1645.
77. Briones G., Inon de Iannino N., Steinberg M., Ugalde R.A. Periplasmic cyclic 1,2-beta-glucan in Brucella spp. is not osmoregulated. Microbiology. 143:1997;1115-1124.
78. Rosinha G.M., Freitas D.A., Miyoshi A., Azevedo V., Campos E., Cravero S.L., Rossetti O., Splitter G., Oliveira S.C. Identification and characterization of a Brucella abortus ATP-binding cassette transporter homolog to Rhizobium meliloti ExsA and its role in virulence and protection in mice. Infect. Immun. 70:2002;5036-5044.
79. Alvarez-Martinez M.T., Machold J., Weise C., Schmidt-Eisenlohr H., Baron C., Rouot B. The Brucella suis homologue of the Agrobacterium tumefaciens chromosomal virulence operon chvE is essential for sugar utilization but not for survival in macrophages. J. Bacteriol. 183:2001;5343-5351.
80. Tatum F.M., Morfitt D.C., Halling S.M. Construction of a Brucella abortus RecA mutant and its survival in mice. Microb. Pathog. 14:1993;177-185.
81. Almiron M., Martinez M., Sanjuan N., Ugalde R.A. Ferrochelatase is present in Brucella abortus and is critical for its intracellular survival and virulence. Infect. Immun. 69:2001;6225-6230.
82. Robertson G.T., Roop R.M. Jr. 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. 34:1999;690-700.
83. Robertson G.T., Kovach M.E., Allen C.A., Ficht T.A., Roop R.M. II. The Brucella abortus Lon functions as a generalized stress response protease and is required for wild-type virulence in BALB/c mice. Mol. Microbiol. 35:2000;577-588.
84. Roop R.M. II, Phillips R.W., Hagius S., Walker J.V., Booth N.J., Fulton W.T., Edmonds M.D., Elzer P.H. Re-examination of the role of the Brucella melitensis HtrA stress response protease in virulence in pregnant goats. Vet. Microbiol. 82:2001;91-95.
85. Phillips R.W., Roop R.M. II. Brucella abortus HtrA functions as an authentic stress response protease but is not required for wild-type virulence in BALB/c mice. Infect. Immun. 69:2001;5911-5913.
86. Latimer E., Simmers J., Sriranganathan N., Roop R.M. II, Schurig G.G., Boyle S.M. Brucella abortus deficient in copper/zinc superoxide dismutase is virulent in BALB/c mice. Microb. Pathog. 12:1992;105-113.
87. Tatum F.M., Detilleux P.G., Sacks J.M., Halling S.M. Construction of Cu-Zn superoxide dismutase deletion mutants of Brucella abortus: analysis of survival in vitro in epithelial and phagocytic cells and in vivo in mice. Infect. Immun. 60:1992;2863-2869.