{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T16:45:42Z","timestamp":1790873142696,"version":"4.1.0"},"reference-count":109,"publisher":"Annual Reviews","issue":"1","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Annu. Rev. Microbiol."],"published-print":{"date-parts":[[2003,10]]},"abstract":"<jats:p>\u25aa Abstract\u2002 The capacity of the Brucella spp. to establish and maintain long-term residence in the phagosomal compartment of host macrophages is critical to their ability to produce chronic infections in their mammalian hosts. The RNA binding protein host factor I (HF-I) encoded by the hfq gene is required for the efficient translation of the stationary-phase \u03c3 factor RpoS in many bacteria, and a Brucella abortus hfq mutant displays a phenotype in vitro, which suggests that it has a generalized defect in stationary-phase physiology. The inability of the B. abortus hfq mutant to survive and replicate in a wild-type manner in cultured murine macrophages, and the profound attenuation displayed by this strain and its B. melitensis counterpart in experimentally infected animals indicate that stationary-phase physiology plays an essential role in the capacity of the brucellae to establish and maintain long-term intracellular residence in host macrophages. The nature of the Brucella HF-I-regulated genes that have been identified to date suggests that the corresponding gene products contribute to the remarkable capacity of the brucellae to resist the harsh environmental conditions they encounter during their prolonged residence in the phagosomal compartment.<\/jats:p>","DOI":"10.1146\/annurev.micro.57.030502.090803","type":"journal-article","created":{"date-parts":[[2003,5,6]],"date-time":"2003-05-06T00:15:44Z","timestamp":1052180144000},"page":"57-76","source":"Crossref","is-referenced-by-count":83,"title":["<i>Brucella<\/i>Stationary-Phase Gene Expression and Virulence"],"prefix":"10.1146","volume":"57","author":[{"given":"R. Martin","family":"Roop II","sequence":"first","affiliation":[{"name":"Department of Microbiology and Immunology, East Carolina University School of Medicine, Greenville, North Carolina 27858-4354;"},{"name":"Lilly Research Laboratories, Lilly Corporate Center, Indianapolis, Indiana 46285;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jason M.","family":"Gee","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, East Carolina University School of Medicine, Greenville, North Carolina 27858-4354;"},{"name":"Lilly Research Laboratories, Lilly Corporate Center, Indianapolis, Indiana 46285;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gregory T.","family":"Robertson","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, East Carolina University School of Medicine, Greenville, North Carolina 27858-4354;"},{"name":"Lilly Research Laboratories, Lilly Corporate Center, Indianapolis, Indiana 46285;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"John M.","family":"Richardson","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, East Carolina University School of Medicine, Greenville, North Carolina 27858-4354;"},{"name":"Lilly Research Laboratories, Lilly Corporate Center, Indianapolis, Indiana 46285;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wai-Leung","family":"Ng","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, East Carolina University School of Medicine, Greenville, North Carolina 27858-4354;"},{"name":"Lilly Research Laboratories, Lilly Corporate Center, Indianapolis, Indiana 46285;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Malcolm E.","family":"Winkler","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, East Carolina University School of Medicine, Greenville, North Carolina 27858-4354;"},{"name":"Lilly Research Laboratories, Lilly Corporate Center, Indianapolis, Indiana 46285;"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"22","reference":[{"key":"b1","unstructured":"Alcantara R, Roop RMII . 2001.Brucella abortusmutants 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"},{"key":"b2","doi-asserted-by":"crossref","first-page":"6361","DOI":"10.1128\/JB.181.20.6361-6370.1999","volume":"181","author":"Azam A","year":"1999","journal-title":"J. Bacteriol."},{"key":"b3","unstructured":"Baldwin CL, Roop RMII . 1999.Brucellainfections and immunity. InOpportunistic Intracellular Pathogens and Immunity, ed. LJ Paradise, H Friedman, M Bendinelli, pp. 255\u201379. New York: Plenum"},{"key":"b4","unstructured":"Beale SI. 1996. Biosynthesis of hemes. See Ref.64A, pp. 731\u201348"},{"key":"b5","doi-asserted-by":"publisher","DOI":"10.1021\/bi00454a010"},{"key":"b6","doi-asserted-by":"publisher","DOI":"10.1007\/s002030050713"},{"key":"b7","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.032514299"},{"key":"b8","doi-asserted-by":"publisher","DOI":"10.1016\/S0378-1135(02)00219-5"},{"key":"b9","doi-asserted-by":"publisher","DOI":"10.1128\/jb.178.13.3763-3770.1996"},{"key":"b10","unstructured":"Brown T, Valderas MW, Roop RMII . 2002.Do the gadB and gadC gene products contribute to stationary phase acid resistance ofBrucella abortus? Presented at Annu. Meet. North Carolina Branch Am. Soc. Microbiol., Raleigh"},{"key":"b11","doi-asserted-by":"publisher","DOI":"10.1126\/science.1067798"},{"key":"b12","unstructured":"Carmichael LE. 1990.Brucella canis. See Ref.67A, pp. 335\u201350"},{"key":"b13","doi-asserted-by":"crossref","first-page":"3525","DOI":"10.1128\/JB.181.11.3525-3535.1999","volume":"181","author":"Castanie-Cornet MP","year":"1999","journal-title":"J. Bacteriol."},{"key":"b14","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.1999.01456.x"},{"key":"b15","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.66.9.3911-3916.2000"},{"key":"b16","doi-asserted-by":"publisher","DOI":"10.1001\/jama.278.5.412"},{"key":"b17","unstructured":"Corbel MJ, Brinley-Morgan WJ. 1984. GenusBrucella. InBergey's Manual of Systematic Bacteriology, ed. NR Krieg, JG Holt, 1:377\u201388. Baltimore: Williams & Wilkins"},{"key":"b18","doi-asserted-by":"crossref","first-page":"2188","DOI":"10.1128\/iai.64.6.2188-2192.1996","volume":"64","author":"Crawford RM","year":"1996","journal-title":"Infect. Immun."},{"key":"b19","doi-asserted-by":"publisher","DOI":"10.1046\/j.1462-5822.2001.00131.x"},{"key":"b20","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.221575398"},{"key":"b21","doi-asserted-by":"crossref","first-page":"1079","DOI":"10.1128\/jb.153.2.1079-1082.1983","volume":"153","author":"Demple B","year":"1983","journal-title":"J. Bacteriol."},{"key":"b22","doi-asserted-by":"publisher","DOI":"10.1016\/S0378-1135(02)00252-3"},{"key":"b23","doi-asserted-by":"crossref","first-page":"3297","DOI":"10.1128\/iai.63.9.3297-3301.1995","volume":"63","author":"Drazek ES","year":"1995","journal-title":"Infect. Immun."},{"key":"b24","doi-asserted-by":"publisher","DOI":"10.1128\/JB.183.8.2454-2462.2001"},{"key":"b25","unstructured":"Enright FM. 1990. The pathogenesis and pathobiology ofBrucellainfections in domestic animals. See Ref.67A, pp. 301\u201320"},{"key":"b26","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.96.13.7502"},{"key":"b27","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.68.3.1297-1303.2000"},{"key":"b28","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.69.1.547-550.2001"},{"key":"b29","doi-asserted-by":"publisher","DOI":"10.1001\/jama.278.5.399"},{"key":"b30","doi-asserted-by":"crossref","first-page":"824","DOI":"10.1016\/S0021-9258(19)45681-0","volume":"247","author":"Franze de Fernandez MT","year":"1972","journal-title":"J. Biol. Chem."},{"key":"b31","doi-asserted-by":"publisher","DOI":"10.1006\/jmbi.1999.3347"},{"key":"b32","unstructured":"Gee J, Roop RMII . 2002.An evaluation of the role of the periplasmic superoxide dismutase in the pathogenesis ofBrucella abortus. Presented at Annu. Meet. North Carolina Branch Am. Soc. Microbiol., Raleigh"},{"key":"b33","first-page":"81","volume":"22","author":"Gerhardt P","year":"1958","journal-title":"Microbiol. Rev."},{"key":"b34","doi-asserted-by":"publisher","DOI":"10.1016\/S0378-1135(02)00217-1"},{"key":"b35","doi-asserted-by":"publisher","DOI":"10.1016\/S0378-1135(02)00214-6"},{"key":"b36","first-page":"1092","volume":"49","author":"Harmon BG","year":"1988","journal-title":"Am. J. Vet. Res."},{"key":"b37","first-page":"459","volume":"50","author":"Harmon BG","year":"1989","journal-title":"Am. J. Vet. Res."},{"key":"b38","unstructured":"Henge-Aronis R. 1996. Regulation of gene expression during entry into stationary phase. See Ref.64A, pp. 1497\u2013512"},{"key":"b39","doi-asserted-by":"publisher","DOI":"10.1128\/MMBR.66.3.373-395.2002"},{"key":"b40","doi-asserted-by":"publisher","DOI":"10.1128\/jb.172.4.2071-2078.1990"},{"key":"b41","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M001001200"},{"key":"b42","doi-asserted-by":"publisher","DOI":"10.1016\/S0167-4838(98)00069-7"},{"key":"b43","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.68.7.4102-4107.2000"},{"key":"b44","unstructured":"Huisman GW, Siegele DA, Zambrano MA, Kolter R. 1996. Morphological and physiological changes during stationary phase. See Ref.64A, pp. 1672\u201382"},{"key":"b45","doi-asserted-by":"publisher","DOI":"10.1128\/JB.182.20.5749-5756.2000"},{"key":"b46","doi-asserted-by":"publisher","DOI":"10.1006\/cimm.1993.1241"},{"key":"b47","doi-asserted-by":"publisher","DOI":"10.3201\/eid0302.970201"},{"key":"b48","doi-asserted-by":"publisher","DOI":"10.1128\/JB.182.19.5631-5633.2000"},{"key":"b49","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.68.7.3861-3866.2000"},{"key":"b50","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.232454299"},{"key":"b51","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.69.4.2753-2756.2001"},{"key":"b52","doi-asserted-by":"publisher","DOI":"10.1016\/S0378-1135(02)00215-8"},{"key":"b53","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.1996.00063.x"},{"key":"b54","doi-asserted-by":"publisher","DOI":"10.1016\/0882-4010(92)90113-3"},{"key":"b55","doi-asserted-by":"publisher","DOI":"10.1126\/science.287.5462.2492"},{"key":"b56","doi-asserted-by":"publisher","DOI":"10.1139\/cjm-44-8-707"},{"key":"b57","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.95.21.12462"},{"key":"b58","doi-asserted-by":"publisher","DOI":"10.1128\/jb.179.16.5188-5194.1997"},{"key":"b59","doi-asserted-by":"publisher","DOI":"10.1177\/030098588902600609"},{"key":"b60","doi-asserted-by":"publisher","DOI":"10.1128\/jb.179.22.6887-6893.1997"},{"key":"b61","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1128\/iai.53.2.245-251.1986","volume":"53","author":"Montaraz JA","year":"1986","journal-title":"Infect. Immun."},{"key":"b62","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.022622699"},{"key":"b63","doi-asserted-by":"publisher","DOI":"10.1101\/gad.10.9.1143"},{"key":"b64","doi-asserted-by":"publisher","DOI":"10.1128\/jb.179.1.297-300.1997"},{"key":"b65","unstructured":"Neidhardt FC, Curtiss RIII , Ingraham JL, Lin ECC, Low LB, et al. eds. 1996. Escherichia coliandSalmonella typhimurium.Cellular and Molecular Biology. Washington, DC: ASM Press"},{"key":"b66","unstructured":"Nicoletti PL. 1989. Relationship between animal and human disease. See Ref.104A, pp. 41\u201352"},{"key":"b67","first-page":"1063","volume":"9","author":"Nicoletti P","year":"1987","journal-title":"Compend. Contin. Educ. Pract. Vet."},{"key":"b68","first-page":"493","volume":"187","author":"Nicoletti P","year":"1985","journal-title":"J. Am. Vet. Med. Assoc."},{"key":"b69","volume-title":"Animal Brucellosis.","author":"Nielsen K","year":"1990"},{"key":"b70","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.1999.01569.x"},{"key":"b71","unstructured":"Parent M, LeVier K, Walker G, Robertson G, Bellaire B, et al. 1999. Assessing the pathogenesis of severalBrucella abortus2308 mutants in interferon-\u03b3 knockout mice.Proc. Conf. Res. Work. Anim. Dis., 80th, Chicago, p. 10. Ames: Iowa State Univ. Press"},{"key":"b72","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.192319099"},{"key":"b73","unstructured":"Phillips RW, Buczynski G, Robertson GT, Cardelli J, Roop RMII . 1997. Characterization ofBrucella-containing phagosomes in murine peritoneal macrophages.Proc. Conf. Res. Work. Anim. Dis., 78th, Chicago, p. 61. Ames: Iowa State Univ. Press"},{"key":"b74","doi-asserted-by":"publisher","DOI":"10.1016\/S0882-4010(96)80001-5"},{"key":"b75","doi-asserted-by":"publisher","DOI":"10.1021\/bi951887s"},{"key":"b76","doi-asserted-by":"crossref","first-page":"4041","DOI":"10.1128\/IAI.67.8.4041-4047.1999","volume":"67","author":"Porte F","year":"1999","journal-title":"Infect. Immun."},{"key":"b77","doi-asserted-by":"publisher","DOI":"10.1016\/S0378-1135(02)00240-7"},{"key":"b78","doi-asserted-by":"publisher","DOI":"10.1016\/S0378-1135(02)00248-1"},{"key":"b79","doi-asserted-by":"publisher","DOI":"10.1016\/S0378-1135(02)00253-5"},{"key":"b80","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1128\/jb.122.1.139-144.1975","volume":"122","author":"Rest RF","year":"1975","journal-title":"J. Bacteriol."},{"key":"b81","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1128\/jb.134.1.115-124.1978","volume":"134","author":"Rice CW","year":"1978","journal-title":"J. Bacteriol."},{"key":"b82","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.1999.01629.x"},{"key":"b83","unstructured":"Roop RMII , Robertson GT, Grippe VK, Kovach ME, LeVier K, et al. 2000.Virulence ofBrucella melitensis hfq, katEandbacAmutants in pregnant goats. Presented at Annu. Brucellosis Research Conf., 53rd, Nimes, France"},{"key":"b84","doi-asserted-by":"publisher","DOI":"10.1016\/S0378-1135(02)00247-X"},{"key":"b85","doi-asserted-by":"publisher","DOI":"10.1016\/0378-1097(95)00215-Q"},{"key":"b86","doi-asserted-by":"publisher","DOI":"10.1128\/JB.183.24.7173-7181.2001"},{"key":"b87","doi-asserted-by":"publisher","DOI":"10.1128\/jb.176.23.7375-7377.1994"},{"key":"b88","doi-asserted-by":"publisher","DOI":"10.1128\/JB.182.17.4849-4855.2000"},{"key":"b89","doi-asserted-by":"publisher","DOI":"10.1128\/JB.183.6.1997-2005.2001"},{"key":"b90","doi-asserted-by":"publisher","DOI":"10.1084\/jem.29.5.451"},{"key":"b91","doi-asserted-by":"publisher","DOI":"10.1016\/0378-1135(91)90029-F"},{"key":"b92","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.1999.01343.x"},{"key":"b93","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.70.6.3004-3011.2002"},{"key":"b94","doi-asserted-by":"crossref","first-page":"2863","DOI":"10.1128\/iai.60.7.2863-2869.1992","volume":"60","author":"Tatum FM","year":"1992","journal-title":"Infect. Immun."},{"key":"b95","doi-asserted-by":"publisher","DOI":"10.1128\/JB.183.2.461-467.2001"},{"key":"b96","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2958.1994.tb00400.x"},{"key":"b97","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.jbchem.a123448"},{"key":"b98","first-page":"55190","volume":"61","author":"United States Department of Health and Human Services.","year":"1996","journal-title":"Fed. Regist."},{"key":"b99","unstructured":"United States Department of Health and Human Services.1999.Biosafety in Microbiological and Biomedical Laboratories, pp. 90\u201391. Washington, DC: U.S. Gov. Print. Off. 4th ed."},{"key":"b100","doi-asserted-by":"publisher","DOI":"10.1099\/00221287-148-5-1439"},{"key":"b101","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.1996.00058.x"},{"key":"b102","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.micro.55.1.139"},{"key":"b103","doi-asserted-by":"publisher","DOI":"10.1016\/0167-4838(88)90050-7"},{"key":"b104","doi-asserted-by":"crossref","unstructured":"Young EJ. 1989. Clinical manifestations of human brucellosis. See Ref.104A, pp. 97\u2013126","DOI":"10.1201\/9781003068518-10"},{"key":"b105","doi-asserted-by":"crossref","unstructured":"Young EJ. 1989. Treatment of brucellosis in humans. See Ref.104A, pp. 127\u201341","DOI":"10.1201\/9781003068518-11"},{"key":"b106","unstructured":"Young EJ. 2000.Brucellaspecies. InMandell, Douglas and Bennett's Principles and Practices of Infectious Diseases, ed. GL Mandell, JE Bennett, R Dolin, pp. 2386\u201393. Philadelphia: Churchill-Livingstone"},{"key":"b107","volume-title":"Brucellosis: Clinical and Laboratory Aspects.","author":"Young EJ","year":"1989"},{"key":"b108","doi-asserted-by":"publisher","DOI":"10.1023\/A:1020660230497"},{"key":"b109","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M202094200"}],"container-title":["Annual Review of Microbiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.annualreviews.org\/doi\/pdf\/10.1146\/annurev.micro.57.030502.090803","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,4,26]],"date-time":"2023-04-26T07:37:18Z","timestamp":1682494638000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.annualreviews.org\/doi\/10.1146\/annurev.micro.57.030502.090803"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2003,10]]},"references-count":109,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2003,10]]}},"alternative-id":["10.1146\/annurev.micro.57.030502.090803"],"URL":"https:\/\/doi.org\/10.1146\/annurev.micro.57.030502.090803","relation":{},"ISSN":["0066-4227","1545-3251"],"issn-type":[{"value":"0066-4227","type":"print"},{"value":"1545-3251","type":"electronic"}],"subject":[],"published":{"date-parts":[[2003,10]]}}}