Brucella Stationary-Phase Gene Expression and Virulence

Annual Review of Microbiology

Volumn 57, Issue , 2003, Pages 57-76

  Roop II, R Martin ^a   Gee, Jason M ^a   Robertson, Gregory T ^b   Richardson, John M ^b   Ng, Wai Leung ^b   Winkler, Malcolm E ^b  

^a EAST CAROLINA UNIVERSITY   (United States)

^b ELI LILLY AND COMPANY   (United States)

Author keywords

Bacterial pathogenesis; Bacterial stress response; Brucellosis; Intracellular pathogens; Macrophage

Indexed keywords

GENE PRODUCT;

ADAPTATION; ANIMAL CELL; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM IDENTIFICATION; BRUCELLA; BRUCELLOSIS; CELL COMPARTMENTALIZATION; CELL KILLING; GENE EXPRESSION REGULATION; GENE SEQUENCE; GENETIC CODE; MACROPHAGE ACTIVATION; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PHAGOSOME; PHENOTYPE; PRIORITY JOURNAL; REVIEW;

ANIMALS; BRUCELLA; BRUCELLOSIS; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; HOST FACTOR 1 PROTEIN; HUMANS; PHAGOSOMES; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); BRUCELLA; BRUCELLA MELITENSIS; BRUCELLA MELITENSIS BIOVAR ABORTUS; MAMMALIA; MURINAE; NEGIBACTERIA; PROKARYOTA;

EID: 0242693171     PISSN: 00664227     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.micro.57.030502.090803     Document Type: Review

References (109)

1. Alcantara R, Roop RM II. 2001. Brucella abortus mutants with nutritional defects show attenuation in culture macrophages and in experimentally infected mice. Proc. Conf. Res. Work. Anim. Dis., 82nd, St. Louis, p. 89. Ames: Iowa State Univ. Press
2. Azam A, Iwata A, Nishimura A, Ueda S, Ishihama A. 1999. Growth-phase dependent variation in protein composition of the Escherichia coli nucleoid. J. Bacteriol. 181:6361-70
3. Baldwin CL, Roop RM II. 1999. Brucella infections and immunity. In Opportunistic Intracellular Pathogens and Immunity, ed. LJ Paradise, H Friedman, M Bendinelli, pp. 255-79. New York: Plenum
4. Beale SI. 1996. Biosynthesis of hemes. See Ref. 64a, pp. 731-48
5. Beck BL, Tabatabai LB, Mayfield JE. 1990. A protein isolated from Brucella abortus is a Cu-Zn superoxide dismutase. Biochemistry 29:372-76
6. Begley TP, Downs DM, Ealick SE, McLafferty FW, Van Loon PGM, et al. 1999. Thiamin biosynthesis in prokaryotes. Arch. Microbiol. 171:293-300
7. Boschiroli ML, Ouahrani-Bettache S, Foulongne V, Michaux-Charachon S, Bourg G, et al. 2002. The Brucella suis virB operon is induced intracellularly in macrophages. Proc. Natl. Acad. Sci. USA 99:1544-49
8. Boschiroli ML, Ouahrani-Bettache S, Foulongne V, Michaux-Charachon S, Bourg G, et al. 2002. Type IV secretion and Brucella virulence. Vet. Microbiol. 90:341-48
9. Brown L, Elliott T. 1996. Efficient translation of the RpoS sigma factor in Salmonella typhimurium requires host factor I, an RNA-binding protein encoded by the hfq gene. J. Bacteriol. 178:3763-70
10. Brown T, Valderas MW, Roop RM II. 2002. Do the gadB and gadC gene products contribute to stationary phase acid resistance of Brucella abortus? Presented at Annu. Meet. North Carolina Branch Am. Soc. Microbiol., Raleigh
11. Bryk R, Lima CD, Erdjument-Bromage H, Tempst P, Nathan C. 2002. Metabolic enzymes of mycobacteria linked to antioxidant defense by a thioredoxin-like protein. Science 295:1073-77
12. Carmichael LE. 1990. Brucella canis. See Ref. 67a, pp. 335-50
13. Castanie-Cornet MP, Penfound TA, Smith D, Elliott JF, Foster JW. 1999. Control of acid resistance in Escherichia coli. J. Bacteriol. 181:3525-35
14. Chang Y-Y, Cronan JE Jr. 1999. Membrane cyclopropane fatty acid content is a major factor in acid resistance in Escherichia coli. Mol. Microbiol. 33:249-59
15. Choi SH, Baumler DJ, Kaspar CW. 2000. Contribution of dps to acid stress tolerance and oxidative stress tolerance in Escherichia coli O157:H7. Appl. Environ. Microbiol. 66:3911-16
16. Christopher GW, Cieslak TJ, Pavlin JA, Eitzen EM. 1997. Biological warfare. A historical perspective. JAMA 278:412-17
17. Corbel MJ, Brinley-Morgan WJ. 1984. Genus Brucella. In Bergey's Manual of Systematic Bacteriology, ed. NR Krieg, JG Holt, 1:377-88. Baltimore: Williams & Wilkins
18. Crawford RM, Van de Berg L, Yuan L, Hadfield T, Warren RL, et al. 1996. Deletion of purE attenuates Brucella melitensis infection in mice. Infect. Immun. 64: 2188-92
19. Delrue RM, Martinez-Lorenzo M, Lestrate P, Danese I, Bielarz V, et al. 2001. Identification of Brucella spp. genes involved in intracellular trafficking. Cell. Microbiol. 3:487-97
20. DelVecchio VG, Kapatral V, Redkar RJ, Patra G, Mujer C, et al. 2002. The genome of the facultative intracellular pathogen Brucella melitensis. Proc. Natl. Acad. Sci. USA 99:443-48
21. Demple B, Halbrook J, Linn S. 1983. Escherichia coli xth mutants are hypersensitive to hydrogen peroxide. J. Bacteriol. 153:1079-82
22. Deqiu S, Donglou X, Jiming Y. 2002. Epidemiology and control of brucellosis in China. Vet. Microbiol. 90:165-82
23. Drazek ES, Houng HS, 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. 63:3297-301
24. 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. 183:2454-62
25. Enright FM. 1990. The pathogenesis and pathobiology of Brucella infections in domestic animals. See Ref. 67a, pp. 301-20
26. Fang FC, DeGroote MA, Foster JW, Baumler AJ, Ochsner U, et al. 1999. Virulent Salmonella typhimurium has two periplasmic Cu,Zn-superoxide dismutases. Proc. Natl. Acad. Sci. USA 96: 7502-7
27. Foulongne V, Bourg G, Cazevieille C, Michaux-Charachon S, O'Callaghan D. 2000. Identification of Brucella suis gene affecting intracellular survival in an in vitro human macrophage infection model by signature-tagged transposon mutagenesis. Infect. Immun. 68:1297-303
28. Foulongne V, Walravens K, Bourg G, Boschiroli ML, Godfroid J, et al. 2001. Aromatic compound-dependent Brucella suis is attenuated in both cultured cells and mouse models. Infect. Immun. 69:547-50
29. Franz DR, Jahrling PB, Friedlander AM, McClain DJ, Hoover DL, et al. 1997. Clinical recognition and management of patients exposed to biological warfare agents. JAMA 278:399-411
30. Franze de Fernandez MT, Hayward WS, August JT. 1972. Bacterial proteins required for the efficient replication of phage Qβ ribonucleic acid. Purification and properties of host factor I, a ribonucleic acid-binding protein. J. Biol. Chem. 247:824-31
31. Gajiwala KS, Burley SK. 2000. HdeA, a periplasmic protein that supports acid resistance in pathogenic enteric bacteria. J. Mol. Biol. 295:605-12
32. Gee J, Roop RM II. 2002. An evaluation of the role of the periplasmic superoxide dismutase in the pathogenesis of Brucella abortus. Presented at Annu. Meet. North Carolina Branch Am. Soc. Microbiol., Raleigh
33. Gerhardt P. 1958. The nutrition of brucellae. Microbiol. Rev. 22:81-98
34. Godfroid J, Käsbohrer A. 2002. Brucellosis in the European Union and Norway at the turn of the twenty-first century. Vet. Microbiol. 90:135-46
35. Gorvel JP, Moreno E. 2002. Brucella intracellular life: from invasion to intracellular replication. Vet. Microbiol. 90:281-97
36. Harmon BG, Adams LG, Frey M. 1988. Survival of rough and smooth strains of Brucella abortus in bovine mammary gland macrophages. Am. J. Vet. Res. 49:1092-97
37. Harmon BG, Adams LG, Templeton JW, Smith R III. 1989. Macrophage function in mammary glands of Brucella abortus-infected cows and cows that resisted infection after inoculation of Brucella abortus. Am. J. Vet. Res. 50:459-65
38. Henge-Aronis R. 1996. Regulation of gene expression during entry into stationary phase. See Ref. 64a, pp. 1497-512
39. S (RpoS) subunit of RNA polymerase. Microbiol. Mol. Biol. Rev. 66:373-95
40. 2 fixation and microaerobosis. J. Bacteriol. 172:2071-78
41. Hillas PJ, Soto de Alba F, Oyarzabal J, Wilks A, Ortiz de Montellano PR. 2000. The AhpC and AhpD antioxidant defense system of Mycobacterium tuberculosis. J. Biol. Chem. 275:18801-9
42. Hohmann S, Meacock PA. 1998. Thiamin metabolism and thiamin diphosphate-dependent enzymes in the yeast Saccharomyces cerevisiae: genetic regulation. Biochim. Biophys. Acta 1385: 210-19
43. Hong PC, Tsolis RM, Ficht TA. 2000. Identification of genes required for chronic persistence of Brucella abortus in mice. Infect. Immun. 68:4102-7
44. Huisman GW, Siegele DA, Zambrano MA, Kolter R. 1996. Morphological and physiological changes during stationary phase. See Ref. 64a, pp. 1672-82
45. S)-regulated genes in Salmonella enterica serovar typhimurium. J. Bacteriol. 182:5749-56
46. Jiang X, Baldwin CL. 1993. Macrophage control of Brucella abortus: role of reactive oxygen intermediates and nitric oxide. Cell. Immunol. 151:309-19
47. Kauffman AM, Meltzer MI, Schmid GP. 1997. The economic impact of a bioterrorist attack: Are prevention and post attack intervention programs justifiable? Emerg. Infect. Dis. 3:83-94
48. Kim J-A, Mayfield J. 2000. Identification of Brucella abortus OxyR and its role in control of catalase expression. J. Bacteriol. 182:5631-33
49. Kim J-A, Sha Z, Mayfield JE. 2000. Regulation of Brucella abortus catalase. Infect. Immun. 68:3681-86
50. Köhler S, Foulongne V, Ouahrani-Bettache S, Bourg G, Teyssier J, et al. 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 99:15711-16
51. Köhler S, Layssac M, Naroeni A, Gentschev I, Rittig M, Liautard JP. 2001. Secretion of listeriolysin by Brucella suis inhibits its intramacrophagic replication. Infect. Immun. 69:2753-56
52. Köhler S, Porte F, Jubier-Maurin V, Ouahrani-Bettache S, Teyssier J, Liautard JP. 2002. The intramacrophagic environment of Brucella suis and bacterial response. Vet. Microbiol. 90:299-309
53. Latifi A, Foglino M, Tanaka K, Williams P, Lazdunski A. 1996. A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol. Microbiol. 21:1137-46
54. Latimer E, Simmers J, Sriranganathan N, Roop RM II, Schurig GG, Boyle SM. 1992. Brucella abortus deficient in copper/zinc superoxide dismutase is virulent in BALB/c mice. Microb. Pathog. 12:105-13
55. 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 287:2492-93
56. Loewen PC, Hu B, Strutinsky J, Sparling R. 1998. Regulation in the rpoS regulon of Escherichia coli. Can. J. Microbiol. 44:707-17
57. Majdalani N, Cunning C, Sledjeski D, Elliott T, Gottesman S. 1998. DsrA RNA regulates translation of RpoS message by an anti-sense mechanism, independent of its action as an antisilencer of transcription. Proc. Natl. Acad. Sci. USA 95:12464-67
58. Martinez A, Kolter R. 1997. Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J. Bacteriol. 179:5188-94
59. Meador VP, Deyoe BL. 1989. Intracellular localization of Brucella abortus in bovine placenta. Vet. Pathol. 26:513-15
60. 3 in Rhizobium etli. J. Bacteriol. 179:6887-93
61. Montaraz JA, Winter AJ. 1986. Comparison of living and nonliving vaccines for Brucella abortusin BALB/c mice. Infect. Immun. 53:245-51
62. Moreno E, Moriyón I. 2002. Brucella melitensis: a nasty bug with hidden credentials for virulence. Proc. Natl. Acad. Sci. USA 99:1-3
63. Muffler A, Fischer D, Hengge-Aronis R. 1996. The RNA-binding protein HFI, known as a host factor for phage Qβ RNA replication, is essential for rpoS translation in Escherichia coli. Genes Dev. 10:1143-51
64. S subunit of RNA polymerase in Escherichia coli. J. Bacteriol. 179:297-300
65. Neidhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Low LB, et al. eds. 1996. Escherichia coli and Salmonella typhimurium. Cellular and Molecular Biology. Washington, DC: ASM Press
66. Nicoletti PL. 1989. Relationship between animal and human disease. See Ref. 104a, pp. 41-52
67. Nicoletti P, Chase A. 1987. The use of antibiotics to control canine brucellosis. Compend. Contin. Educ. Pract. Vet. 9:1063
68. Nicoletti P, Milward FW, Hoffman E, Altvater L. 1985. Efficacy of long-lasting oxytetracycline alone or combined with streptomycin in the treatment of bovine brucellosis. J. Am. Vet. Med. Assoc. 187:493-95
69. Nielsen K, Duncan JR, eds. 1990. Animal Brucellosis. Boca Raton: CRC
70. O'Callaghan D, Cazevielle C, Allardet-Servent A, Boschiroli ML, Bourg G, et al. 1999. A homologue of the Agrobacterium tumefaciens VirB and Bordetella pertussis Ptl type IV secretions systems is essential for intracellular survival of Brucella suis. Mol. Microbiol. 33:1210-20
71. Parent M, LeVier K, Walker G, Robertson G, Bellaire B, et al. 1999. Assessing the pathogenesis of several Brucella abortus 2308 mutants in interferon-γ knockout mice. Proc. Conf. Res. Work. Anim. Dis., 80th, Chicago, p. 10. Ames: Iowa State Univ. Press
72. Paulsen IT, Seshadri R, Nelson KE, Eisen JA, Heidelberg JF, et al. 2002. The Brucella suis genome reveals fundamental similarities between animal and plant pathogens and symbionts. Proc. Natl. Acad. Sci. USA 99:13148-53
73. Phillips RW, Buczynski G, Robertson GT, Cardelli J, Roop RM II. 1997. Characterization of Brucella-containing phagosomes in murine peritoneal macrophages. Proc. Conf. Res. Work. Anim. Dis., 78th, Chicago, p. 61. Ames: Iowa State Univ. Press
74. Phillips RW, Elzer PH, Roop RM II. 1995. A Brucella melitensis high temperature requirement A (htrA) deletion mutant demonstrates a stress response defective phenotype in vitro and transient attenuation in the BALB/c mouse model. Microb. Pathog. 19:277-84
75. Poole LB, Ellis HR. 1996. Flavin-dependent alkyl hydroperoxide reductase from Salmonella typhimurium. 1. Purification and enzymatic activities of overexpressed AhpF and AhpC proteins. Biochemistry 35:56-64
76. Porte F, Liautard JP, Köhler S. 1999. Early acidification of phagosomes containing Brucella suis is essential for intracellular survival in murine macrophages. Infect. Immun. 67:4041-47
77. Ragan V. 2002. The Animal and Plant Health Inspection Service (APHIS) brucellosis eradication program in the United States. Vet. Microbiol. 90:11-18
78. Refai M. 2002. Incidence and control of brucellosis in the Near East region. Vet. Microbiol. 90:81-110
79. Renukaradhya GJ, Isloor S, Rajasekhar M. 2002. Epidemiology, zoonotic aspects, vaccination and control/eradication of brucellosis in India. Vet. Microbiol. 90:165-82
80. Rest RF, Robertson DC. 1975. Characterization of the electron transport system of Brucella abortus. J. Bacteriol. 122:139-44
81. Rice CW, Hempfling WP. 1978. Oxygen-limited continuous culture and respiratory energy conservation in Escherichia coli. J. Bacteriol. 134:115-24
82. 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. 34:690-700
83. Roop RM II, Robertson GT, Grippe VK, Kovach ME, LeVier K, et al. 2000. Virulence of Brucella melitensis hfq, katE and bacA mutants in pregnant goats. Presented at Annu. Brucellosis Research Conf., 53rd, Nimes, France
84. Samartino LE. 2002. Brucellosis in Argentina. Vet. Microbiol. 90:71-80
85. Schellhorn HE. 1994. Regulation of hydroperoxidase (catalase) expression in Escherichia coli. FEMS Microbiol. Lett. 131:113-19
86. Seaver LC, Imlay JA. 2001. Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J. Bacteriol. 183:7173-81
87. Sha Z, Stabel TJ, Mayfield JE. 1994. Brucella abortus catalase is a periplasmic protein lacking a standard signal sequence. J. Bacteriol. 176:7375-77
88. Sieira R, Comerci DJ, Sanchez DO, Ugalde RA. 2000. A homologue of an operon required for DNA transfer in Agrobacterium is required in Brucella abortus for virulence and intracellular replication. J. Bacteriol. 182:4849-55
89. Sledjeski DD, Whitman C, Zhang A. 2001. Hfq is necessary for regulation by the untranslated RNA DsrA. J. Bacteriol. 183:1997-2005
90. Smith T. 1919. A characteristic localization of Bacillus abortus in the bovine fetal membranes. J. Exp. Med. 29:451-55
91. Sriranganathan N, Boyle SM, Schurig GG, Misra H. 1990. Superoxide dismutases of virulent and avirulent strains of Brucella abortus. Vet. Microbiol. 26:359-66
92. Strohmeier Gort A, Ferber DM, Imlay JA. 1999. The regulation and role of the periplasmic copper, zinc superoxide dismutase of Escherichia coli. Mol. Microbiol. 32:179-91
93. Taminiau B, Daykin M, Swift S, Boschiroli M-L, Tibor A, et al. 2002. Identification of a quorum-sensing signal molecule in the facultative intracellular pathogen Brucella melitensis. Infect. Immun. 70:3004-11
94. Tatum FM, Detilleux PG, Sacks JM, Halling SM. 1992. 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. 60:2863-69
95. Tseng C-P, Yu C-C, Lin H-H, Chang C-Y, Kuo J-T. 2001. Oxygen-and growth rate-dependent regulation of Escherichia coli fumarase (FumA, FumB, and FumC) activity. J. Bacteriol. 183:461-67
96. Tsui HC, Leung HE, Winkler ME. 1994. Characterization of broadly pleiotropic phenotypes caused by an hfq insertion mutation in Escherichia coli K-12. Mol. Microbiol. 13:35-49
97. Ueda Y, Yumoto N, Tokushige M, Fukui K, Ohya-Nishiguchi H. 1991. Purification and characterization of two types of fumarase from Escherichia coli. J. Biochem. 109:728-33
98. United States Department of Health and Human Services. 1996. Additional requirements for facilities transferring or receiving select agents: final rule (42 CFR Part 72). Fed. Regist. 61:55190-200
99. United States Department of Health and Human Services. 1999. Biosafety in Microbiological and Biomedical Laboratories, pp. 90-91. Washington, DC: U.S. Gov. Print. Off. 4th ed.
100. Watarai M, Makino S, Shirahata T. 2002. An essential virulence protein of Brucella abortus, VirB4, requires an intact nucleoside-triphosphate-binding domain. Microbiol. 148:1439-46
101. S-dependent genes associated with the stationary-phase acid-resistance phenotype of Shigella flexneri. Mol. Microbiol. 21:925-40
102. Wayne LG, Sohaskey CD. 2001. Non-replicating persistence of Mycobacterium tuberculosis. Annu. Rev. Microbiol. 55:139-63
103. Woods SA, Schwartzbach SD, Guest JR. 1988. Two biochemically distinct classes of fumarase in Escherichia coli. Biochim. Biophys. Acta 954:14-26
104. Young EJ. 1989. Clinical manifestations of human brucellosis. See Ref. 104a, pp. 97-126
105. Young EJ. 1989. Treatment of brucellosis in humans. See Ref. 104a, pp. 127-41
106. Young EJ. 2000. Brucella species. In Mandell, Douglas and Bennett's Principles and Practices of Infectious Diseases, ed. GL Mandell, JE Bennett, R Dolin, pp. 2386-93. Philadelphia: Churchill-Livingstone
107. Young EJ, Corbel MJ, eds. 1989. Brucellosis: Clinical and Laboratory Aspects. Boca Raton: CRC
108. Zhang A, Wassarman KM, Ortega J, Steven AC, Storz G. 2002. The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs. Mol. Cell. 9:11-22
109. Zhao G, Ceci P, Ilari A, Giangiacomo L, Laue TM, et al. 2002. Iron and hydrogen peroxide detoxification properties of DNA-binding protein from starved cells. A ferritin-like DNA-binding protein of Escherichia coli. J. Biol. Chem. 277:27689-96