Limited role for iron regulation in Coxiella burnetii Pathogenesis

Infection and Immunity

Volumn 76, Issue 5, 2008, Pages 2189-2201

  Briggs, Heather L ^a   Pul, Nicolein ^a   Seshadri, Rekha ^b   Wilson, Mary J ^a   Tersteeg, Claudia ^a   Russell Lodrigue, Kasi E ^a   Andoh, Masako ^a   Bäumler, Andreas J ^c   Samuel, James E ^a  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^b Institute for Genome Research   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEFEROXAMINE; FERRIC UPTAKE REGULATOR; IRON; MUTANT PROTEIN; REACTIVE OXYGEN METABOLITE; BACTERIAL PROTEIN; CATION TRANSPORT PROTEIN; IRON BINDING PROTEIN; IRON UPTAKE REGULATION PROTEIN, BACTERIA; IRON-UPTAKE REGULATION PROTEIN, BACTERIA; REPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GROWTH; BACTERIAL INFECTION; CATION EFFLUX PUMP GENE; CONTROLLED STUDY; COXIELLA BURNETII; ESCHERICHIA COLI; FEMALE; GENE; GENE EXPRESSION; GENE IDENTIFICATION; IRON BINDING PROTEIN ENCODING GENE; IRON OVERLOAD; IRON RESTRICTION; IRON TRANSPORTER GENE; MOLECULAR CLONING; MOUSE; NONHUMAN; PATHOGENESIS; PLASMID; PREDICTOR VARIABLE; PRIORITY JOURNAL; PROMOTER REGION; REGULON; SPLENOMEGALY; TISSUE CULTURE; TITRIMETRY; TRANSCRIPTION REGULATION; AMINO ACID SEQUENCE; ANIMAL; BACTERIAL COUNT; BAGG ALBINO MOUSE; BINDING SITE; BIOSYNTHESIS; CELL LINE; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MACROPHAGE; METABOLISM; METHODOLOGY; MICROBIOLOGY; MOLECULAR GENETICS; PATHOGENICITY; PHYSIOLOGY; Q FEVER; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; BINDING SITES; CATION TRANSPORT PROTEINS; CELL LINE; COLONY COUNT, MICROBIAL; COXIELLA BURNETII; DEFEROXAMINE; ESCHERICHIA COLI; FEMALE; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC COMPLEMENTATION TEST; IRON; IRON-BINDING PROTEINS; MACROPHAGES; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS (GENETICS); Q FEVER; REGULON; REPRESSOR PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 42949137049     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01609-07     Document Type: Article

References (65)

1. Allard, K. A., V. K. Viswanathan, and N. P. Cianciotto. 2006. IbtA and IbtB are required for production of the Legionella pneumophila siderophore legiobactin. J. Bacteriol. 188:1351-1363.
2. Andoh, M., T. Naganawa, A Hotta, T. Yamaguchi, H. Fukushi, T. Masegi, and K. Hirai. 2003. SCID mouse model for lethal Q fever. Infect. Immun. 71:4717-4723.
3. Andoh, M., G. Zhang, K. E. Russell-Lodrigue, H. R. Shive, B. R. Weeks, and J. E. Samuel. 2007. T cells are essential for bacterial clearance, and gamma interferon, tumor necrosis factor alpha, and B cells are crucial for disease development in Coxiella burnetii infection in mice. Infect. Immun. 75:3245-3255.
4. Andrews, S. C., A K. Robinson, and F. Rodriguez-Quinones. 2003. Bacterial iron homeostasis. FEMS Microbiol. Rev. 27:215-237.
5. Anton, A., A Weltrowski, C. J. Haney, S. Franke, G. Grass, C. Rensing, and D. H. Nies. 2004. Characteristics of zinc transport by two bacterial cation diffusion facilitators from Ralstonia metallidurans CH34 and Escherichia coli. J. Bacteriol. 186:7499-7507.
6. Bagg, A., and J. B. Neilands. 1985. Mapping of a mutation affecting regulation of iron uptake systems in Escherichia coli K-12. J. Bacteriol. 161:450-453.
7. Bereswill, S., F. Lichte, T. Vey, F. Fassbinder, and M. Kist. 1998. Cloning and characterization of the fur gene from Helicobacter pylori. FEMS Microbiol. Lett. 159:193-200.
8. Berón, W., M. G. Gutierrez, M. Rabinovitch, and M. I. Colombo. 2002. Coxiella burnetii localizes in a Rab7-labeled compartment with autophagic characteristics. Infect. Immun. 70:5816-5821.
9. Brennan, R. E., K. Russell, G. Zhang, and J. E. Samuel. 2004. Both inducible nitric oxide synthase and NADPH oxidase contribute to the control of virulent phase I Coxiella burnetii infections. Infect. Immun. 72:6666-6675.
10. Brennan, R. E., and J. E. Samuel. 2003. Evaluation of Coxiella burnetii antibiotic susceptibilities by real-time PCR assay. J. Clin. Microbiol. 41:1869-1874.
11. Briggs, H. L., M. J. Wilson, R. Seshadri, and J. E. Samuel. 2005. Fur-regulated genes in Coxiella burnetii. Ann. N. Y. Acad. Sci. 1063:68-72.
12. Byrd, T. F., and M. A Horwitz. 1989. Interferon gamma-activated human monocytes downregulate transferrin receptors and inhibit the intracellular multiplication of Legionella pneumophila by limiting the availability of iron. J. Clin. Investig. 83:1457-1465.
13. Centers for Disease Control and Prevention. 13 February 2003, posting date. Q fever. Centers for Disease Control and Prevention, Atlanta, GA. http://www.cdc.gov/ncidod/dvrd/qfever/index.htm.
14. Damiani, G., C. Kiyotaki, W. Soeller, J. Peisach, and B. Bloom. 1980. Macrophage variants in oxygen metablism. J. Exp. Med. 152:808-822.
15. Delany, I., R. Ieva, C. Alaimo, R. Rappuoli, and V. Scarlato. 2003. The iron-responsive regulator fur is transcriptionally autoregulated and not essential in Neisseria meningitidis. J. Bacteriol. 185:6032-6041.
16. Delany, I., G. Spohn, A. B. Pacheco, R. Ieva, C. Alaimo, R. Rappuoli, and V. Scarlato. 2002. Autoregulation of Helicobacter pylori Fur revealed by functional analysis of the iron-binding site. Mol. Microbiol. 46:1107-1122.
17. Delany, I., G. Spohn, R. Rappuoli, and V. Scarlato. 2001. The Fur repressor controls transcription of iron-activated and -repressed genes in Helicobacter pylori. Mol. Microbiol. 42:1297-1309.
18. Desai, P. J., A. Angerer, and C. A. Genco. 1996. Analysis of Fur binding to operator sequences within the Neisseria gonorrhoeae fbpA promoter. J. Bacteriol. 178:5020-5023.
19. Escolar, L., J. Perez-Martin, and V. de Lorenzo. 1999. Opening the iron box: transcriptional metalloregulation by the Fur protein. J. Bacteriol. 181:6223-6229.
20. Foster, J. W., and H. K. Hall. 1992. Effect of Salmonella typhimurium ferric uptake regulator (fur) mutations on iron- and pH-regulated protein synthesis. J. Bacteriol. 174:4317-4323.
21. Funahashi, T., K. Moriya, S. Uemura, S. Miyoshi, S. Shinoda, S. Narimatsu, and S. Yamamoto. 2002. Identification and characterization of pvuA, a gene encoding the ferric vibrioferrin receptor protein in Vibrio parahaemolyticus. J. Bacteriol. 184:936-946.
22. Goldberg, M., L. S. Belkowski, and B. R. Bloom. 1990. Regulation of macrophage function by interferon-gamma. Somatic cell genetic approaches in murine macrophage cell lines to mechanisms of growth inhibition, the oxidative burst, and expression of the chronic granulomatous disease gene. J. Clin. Investig. 85:563-569.
23. Gomes, M. S., G. Dom, J. Pedrosa, J. R. Boelaert, and R. Appelberg. 1999. Effects of iron deprivation on Mycobacterium avium growth. Tuber. Lung Dis. 79:321-328.
24. Grass, G., M. Otto, B. Fricke, C. J. Haney, C. Rensing, D. H. Nies, and D. Munkelt. 2005. FieF (YiiP) from Escherichia coli mediates decreased cellular accumulation of iron and relieves iron stress. Arch. Microbiol. 183:9-18.
25. Hantke, K. 1984. Cloning of the repressor protein gene of iron-regulated systems in Escherichia coli K12. Mol. Gen. Genet. 197:337-341.
26. Hantke, K. 1981. Regulation of ferric iron transport in Escherichia coli K12: isolation of a constitutive mutant. Mol. Gen. Genet. 182:288-292.
27. Haraszthy, V. I., S. F. Jordan, and J. J. Zambon. 2006. Identification of Fur-regulated genes in Actinobacillus actinomycetemcomitans. Microbiology 152:787-796.
28. Heinzen, R. A., T. Hackstadt, and J. E. Samuel. 1999. Developmental biology of Coxiella burnettii. Trends Microbiol. 7:149-154.
29. Hickey, E. K., and N. P. Cianciotto. 1997. An iron- and fur-repressed Legionella pneumophila gene that promotes intracellular infection and encodes a protein with similarity to the Escherichia coli aerobactin synthetases. Infect. Immun. 65:133-143.
30. Hickey, E. K., and N. P. Cianciotto. 1994. Cloning and sequencing of the Legionella pneumophila fur gene. Gene 143:117-121.
31. Holbein, B. E., K. W. Jericho, and G. C. Likes. 1979. Neisseria meningitidis infection in mice: influence of iron, variations in virulence among strains, and pathology. Infect. Immun. 24:545-551.
32. Howe, D., and L. P. Mallavia. 2000. Coxiella burnetii exhibits morphological change and delays phagolysosomal fusion after internalization by J774A.1 cells. Infect. Immun. 68:3815-3821.
33. Howe, D., and L. P. Mallavia. 1999. Coxiella burnetii infection increases transferrin receptors on J774A.1 cells. Infect. Immun. 67:3236-3241.
34. Kammler, M., C. Schon, and K. Hantke. 1993. Characterization of the ferrous iron uptake system of Escherichia coli. J. Bacteriol. 175:6212-6219.
35. Kurz, T., B. Gustafsson, and U. T. Brunk. 2006. Intralysosomal iron chelation protects against oxidative stress-induced cellular damage. FEBS J. 273:3106-3117.
36. Lee, H. J., K. J. Park, A. Y. Lee, S. G. Park, B. C. Park, K. H. Lee, and S. J. Park. 2003. Regulation of fur expression by RpoS and fur in Vibrio vulnificus. J. Bacteriol. 185:5891-5896.
37. Liles, M. R., T. A. Scheel, and N. P. Cianciotto. 2000. Discovery of a non-classical siderophore, legiobactin, produced by strains of Legionella pneumophila. J. Bacteriol. 182:749-757.
38. Lounis, N., C. Truffot-Pernot, J. Grosset, V. R. Gordeuk, and J. R. Boelaert. 2001. Iron and Mycobacterium tuberculosis infection. J. Clin. Virol. 20:123-126.
39. Maniatis, T. E., E. F. Fritsch, and J. Sambrook. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
40. Marrie, T. J. 1990. Epidemiology of Q fever, p. 49-70. In T. J. Marrie (ed.), Q fever, vol. 1: the disease. CRC Press, Boca Raton, FL.
41. Massé, E., and S. Gottesman. 2002. A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc. Natl. Acad. Sci. USA 99:4620-4625.
42. Maurin, M., and D. Raoult. 1999. Q fever. Clin. Microbiol. Rev. 12:518-553.
43. Miller, J. H. 1972. Experiments in molecular genetics. Cold Springs Laboratory Press, Cold Springs Harbor, NY.
44. Nathan, C., and M. U. Shiloh. 2000. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl. Acad. Sci. USA 97:8841-8848.
45. Nielsen, H., J. Engelbrecht, S. Brunak, and G. von Heijne. 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10:1-6.
46. Nielsen, H., and A. Krogh. 1998. Prediction of signal peptides and signal anchors by a hidden Markov model. Proc. Int. Conf. Intell. Syst. Mol. Biol. 6:122-130.
47. Parker, D., R. M. Kennan, G. S. Myers, I. T. Paulsen, and J. I. Rood. 2005. Identification of a Dichelobacter nodosus ferric uptake regulator and determination of its regulatory targets. J. Bacteriol. 187:366-375.
48. Persson, H. L., Z. Yu, O. Tirosh, J. W. Eaton, and U. T. Brunk. 2003. Prevention of oxidant-induced cell death by lysosomotropic iron chelators. Free Radic. Biol. Med. 34:1295-1305.
49. Poch, M. T., and W. Johnson. 1993. Ferric reductases of Legionella pneumophila. Biometals 6:107-114.
50. Pohl, E., J. C. Haller, A. Mijovilovich, W. Meyer-Klaucke, E. Garman, and M. L. Vasil. 2003. Architecture of a protein central to iron homeostasis: crystal structure and spectroscopic analysis of the ferric uptake regulator. Mol. Microbiol. 47:903-915.
51. Rau, A., S. Wyllie, J. Whittimore, and J. E. Raulston. 2005. Identification of Chlamydia trachomatis genomic sequences recognized by chlamydial divalent cation-dependent regulator A (DcrA). J. Bacteriol. 187:443-448.
52. Robey, M., and N. P. Cianciotto. 2002. Legionella pneumophila feoAB promotes ferrous iron uptake and intracellular infection. Infect. Immun. 70:5659-5669.
53. Samrakandi, M. M., S. L. Cirillo, D. A. Ridenour, L. E. Bermudez, and J. D. Cirillo. 2002. Genetic and phenotypic differences between Legionella pneumophila strains. J. Clin. Microbiol. 40:1352-1362.
54. Sawatzki, G., F. A. Hoffmann, and B. Kubanek. 1983. Acute iron overload in mice: pathogenesis of Salmonella typhimurium infection. Infect. Immun. 39:659-665.
55. Seshadri, R., I. T. Paulsen, J. A Eisen, T. D. Read, K. E. Nelson, W. C. Nelson, N. L. Ward, H. Tettelin, T. M. Davidsen, M. J. Beanan, R. T. Deboy, S. C. Daugherty, L. M. Brinkac, R. Madupu, R. J. Dodson, H. M. Khouri, K. H. Lee, H. A. Carty, D. Scanlan, R. A Heinzen, H. A Thompson, J. E. Samuel, C. M. Fraser, and J. F. Heidelberg. 2003. Complete genome sequence of the Q.-fever pathogen Coxiella burnetii. Proc. Natl. Acad. Sci. USA 100:5455-5460.
56. Sheehan, D. C., and B. B. Hrapchak. 1987. Theory and practice of histotechnology, 2nd ed. Batteile Press, Columbus, OH.
57. Stojiljkovic, I., A. J. Baumler, and K. Hantke. 1994. Fur regulon in gram-negative bacteria. Identification and characterization of new iron-regulated Escherichia coli genes by a fur titration assay. J. Mo. Biol. 236:531-545.
58. Sullivan, J. T., E. F. Jeffery, J. D. Shannon, and G. Ramakrishnan. 2006. Characterization of the siderophore of Francisella tularensis and role of fslA in siderophore production. J. Bacteriol. 188:3785-3795.
59. Tolmasky, M. E., A. M. Wertheimer, L. A. Actis, and J. H. Crosa. 1994. Characterization of the Vibrio anguillarum fur gene: role in regulation of expression of the FatA outer membrane protein and catechols. J. Bacteriol. 176:213-220.
60. Touati, D. 2000. Iron and oxidative stress in bacteria. Arch. Biochem. Biophys. 373:1-6.
61. Tsolis, R. M., A J. Baumler, I. Stojiljkovic, and F. Heffron. 1995. Fur regulon of Salmonella typhimurium: identification of new iron-regulated genes. J. Bacteriol. 177:4628-4637.
62. Viswanathan, V. K., P. H. Edelstein, C. D. Pope, and N. P. Cianciotto. 2000. The Legionella pneumophila iraAB locus is required for iron assimilation, intracellular infection, and virulence. Infect. Immun. 68:1069-1079.
63. Wright, A C., L. M. Simpson, and J. D. Oliver. 1981. Role of iron in the pathogenesis of Vibrio vulnificus infections. Infect. Immun. 34:503-507.
64. Zhang, G., K. Kiss, R. Seshadri, L. R. Hendrix, and J. E. Samuel. 2004. Identification and cloning of immunodominant antigens of Coxiella burnetii. Infect. Immun. 72:844-852.
65. Zheng, M., B. Doan, T. D. Schneider, and G. Storz. 1999. OxyR and SoxRS regulation of fur. J. Bacteriol. 181:4639-4643.