1887

Chapter 6 : Iron Regulation and Virulence in Gram-Negative Bacterial Pathogens with as a Paradigm

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in
Zoomout

Iron Regulation and Virulence in Gram-Negative Bacterial Pathogens with as a Paradigm, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818524/9781555816766_Chap06-1.gif /docserver/preview/fulltext/10.1128/9781555818524/9781555816766_Chap06-2.gif

Abstract:

This chapter covers the role of iron regulation in the virulence of gram-negative bacterial pathogens, where possible, using as a paradigm. In most gram-negative bacteria, including , the alterations in mRNA and protein levels in response to iron availability are due to inherent iron requirements and iron homeostasis mechanisms controlled by two primary regulatory systems: the iron (Fe) uptake regulation protein Fur and the small RNA (sRNA) RyhB or its analogs (e.g., PrrF and NrrF). The chapter focuses on these two regulators, their regulons, and their roles in virulence. While Fur and RyhB regulons are often described separately, they are in fact interrelated regulatory networks. In a variation on the mRNA degradation theme for sodB, RyhB selectively promotes degradation of only the 3' portion of the iscRSUA mRNA, while preserving expression of IscR, a transcription factor encoded by the first gene of the operon. The chapter then focuses on the iron transport systems of . A section on RyhB regulatory mechanisms explains that RyhB regulation increases the pools of both shikimate and serine, while indirectly contributing to expression of the enterobactin biosynthesis genes. The mechanisms of Fur activation, Mn-Fur regulation, and apo-Fur regulation as well as the different regulatory mechanisms of RyhB are addressed. However, the complexity of iron regulation mechanisms and their role in microbial pathogenesis will likely provide interesting questions to resolve for decades to come.

Citation: Perry R, McDonough K. 2013. Iron Regulation and Virulence in Gram-Negative Bacterial Pathogens with as a Paradigm, p 106-132. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch6
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of Figure 1
Figure 1

Model of Fe-Fur transcriptional repression and Fur box motifs. (A) Fur boxes for Fe-Fur binding generally overlap the −10 region of regulated promoters. During iron limitation, cytoplasmic Fe levels are sufficiently low so that Fur is primarily in its apo form. apo-Fur dimers have a lower affinity for binding to the Fur box, allowing RNA polymerase access, and transcription proceeds. Under iron surplus conditions, Fe in the bacterial cytoplasm is bound by Fur. Fe-Fur dimers bind to Fur boxes, preventing access of RNA polymerase to the promoter region, thereby preventing transcription. (B) Three alternative interpretations of Fur box motifs are shown. Arrows indicate the direct or indirect repeated sequences. The Lavrrar et al. 2002 model and data provided from the crystallographic structure of FurPa support a model in which two Fur dimmers bind on opposite sides of the DNA helix of a single Fur box, in a Fur-dependent promoter, as shown in panel A ( ). This view is also supported by the consistent observation that Fur from and protects no less than 27 to 30 bp in DNase I assays ( ). doi:10.1128/9781555818524.ch6f1

Citation: Perry R, McDonough K. 2013. Iron Regulation and Virulence in Gram-Negative Bacterial Pathogens with as a Paradigm, p 106-132. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch6
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Alignment of Fur amino acid sequences from (Ec), (Yp), (Vc), and P. aeruginosa (Pa). The four sequences were aligned using ClustalW2 ( ) and the EMBL-EBI website. α-Helical regions (bold, purple text and [α] labels) and β-strands (bold, green text and [β] labels) are shown for Fur based on X-ray data ( ). A consensus sequence (Con) based on these four sequences is shown. Asterisks indicate identical residues, while colons and periods indicate conservative and semiconservative changes, respectively. Residues involved in Zn binding at the Zn1 structural binding site (underlined, bold, blue text) are shown for all Fur proteins except Fur. Residues for the regulatory site for Fe binding (site 2) are shown as underlined, bold, red text for Fur and Fur. While these residues are conserved in Fur, four different Cys residues (also in underlined, bold, blue text) have been implicated in Zn binding and dimerization. However, Fur has only a single Cys residue, which functions only in dimerization. Zn1, site 1, and the Cys residues are conserved in Fur although no structure/function analyses have been performed on the protein. doi:10.1128/9781555818524.ch6f2

Citation: Perry R, McDonough K. 2013. Iron Regulation and Virulence in Gram-Negative Bacterial Pathogens with as a Paradigm, p 106-132. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch6
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

Genetic organization of the fur locus. Designated arrows represent , , and (upstream of ) genes and show their direction of transcription. Smaller arrows indicate promoters. Transcriptional regulators CRP, Fur, OxyR, and SoxS are shown “bound” to their binding sites (similarly colored figures on the double DNA strand) within promoter regions. Indirect regulation of translation by RyhB through translation of is not shown here (see Fig. 6C ). The three alternative mRNAs are shown. Genes, transcriptional regulators, and promoter elements are not drawn to scale. doi:10.1128/9781555818524.ch6f3

Citation: Perry R, McDonough K. 2013. Iron Regulation and Virulence in Gram-Negative Bacterial Pathogens with as a Paradigm, p 106-132. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch6
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
Figure 4

Model of direct transcriptional activation of by Fur. During iron limitation (A), transcription is repressed since apo-Fur does not bind to the five upstream Fur boxes. This allows H-NS to bind at these sites and other sites in the promoter region. Interaction among H-NS proteins bends the DNA, preventing access of RNA polymerase to the promoter region. Under iron surplus conditions (B), Fe-Fur binds to the upstream Fur boxes, preventing H-NS binding and interaction. This prevents occlusion of the promoter region, allowing RNA polymerase to bind and initiate transcription. doi:10.1128/9781555818524.ch6f4

Citation: Perry R, McDonough K. 2013. Iron Regulation and Virulence in Gram-Negative Bacterial Pathogens with as a Paradigm, p 106-132. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch6
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 5
Figure 5

Model of indirect regulation of by Fur through RyhB. RyhB is expressed under low-iron conditions (A) because apo-Fur has a low affinity for binding to the Fur box in the promoter and consequently does not repress transcription. RyhB sRNA base-pairs with mRNA, causing downregulation of translation in an Hfq- and RNase E-dependent manner. Under iron-replete conditions (B), Fe-Fur binds to the promoter and prevents its transcription. SodB is expressed in the absence of RyhB-mediated repression. doi:10.1128/9781555818524.ch6f5

Citation: Perry R, McDonough K. 2013. Iron Regulation and Virulence in Gram-Negative Bacterial Pathogens with as a Paradigm, p 106-132. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch6
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 6
Figure 6

Models showing various RyhB regulatory mechanisms. (A) RyhB sRNA base-pairs with a region of the mRNA that contains translation initiation signals (green arrow), blocking ribosome access (light blue oblongs). Hfq (purple octagon) binds both RyhB and RNase E (scissors), promoting cleavage of the mRNA by the RNA degradosome (not shown). (B) RyhB base-pairing with the cysE mRNA reduces, but does not eliminate, ribosome binding and translational readthrough to produce low levels of CysE protein (red pentagon). (C) RyhB base-pairing with the open reading frame upstream of in some organisms prevents translational readthrough into , indirectly downregulating translation. (D) RyhB's interaction with the mRNA is similar to that of mRNA, except that it base-pairs with a sequence at the start of an internal cistron rather than the 5′ end. A strong hairpin structure upstream of this binding prevents the first cistron from degradation, leaving only the portion of the mRNA intact. Blue pentagons represent IscR protein that is translated from this truncated message. (E) RyhB base-pairing with mRNA alters the mRNA folding to make the translational start site available for ribosome binding, increasing translation of . Blue pentagons represent ShiA protein. doi:10.1128/9781555818524.ch6f6

Citation: Perry R, McDonough K. 2013. Iron Regulation and Virulence in Gram-Negative Bacterial Pathogens with as a Paradigm, p 106-132. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch6
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555818524.chap6
1. Alamuri, P.,, N. Mehta,, A. Burk,, and R. J. Maier. 2006. Regulation of the Helicobacter pylori Fe-S cluster synthesis protein NifS by iron, oxidative stress conditions, and Fur. J. Bacteriol. 188:53255330.
2. Alice, A. F.,, H. Naka,, and J. H. Crosa. 2008. Global gene expression as a function of the iron status of the bacterial cell: influence of differentially expressed genes in the virulence of the human pathogen Vibrio vulnificus. Infect. Immun. 76:40194037.
3. Amarasinghe, J. J.,, F. A. Scannapieco,, and E. M. Haase. 2009. Transcriptional and translational analysis of biofilm determinants of Aggregatibacter actinomycetemcomitans in response to environmental perturbation. Infect. Immun. 77:28962907.
4. Andrews, S. C.,, A. K. Robinson,, and F. Rodríguez-Quiñones. 2003. Bacterial iron homeostasis. FEMS Microbiol. Rev. 27:215237.
5. Arhin, A.,, and C. Boucher. 2010. The outer membrane protein OprQ and adherence of Pseudomonas aeruginosa to human fibronectin. Microbiology 156:14151423.
6. Bagg, A.,, and J. B. Neilands. 1987. Ferric uptake regulation protein acts as a repressor, employing iron(II) as a cofactor to bind the operator of an iron transport operon in Escherichia coli. Biochemistry 26:54715477.
7. Bagg, A.,, and J. B. Neilands. 1985. Mapping of a mutation affecting regulation of iron uptake systems in Escherichia coli K-12. J. Bacteriol. 161:450453.
8. Banin, E.,, M. L. Vasil,, and E. P. Greenberg. 2005. Iron and Pseudomonas aeruginosa biofilm formation. Proc. Natl. Acad. Sci. USA 102:1107611081.
9. Bearden, S. W.,, and R. D. Perry. 1999. The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague. Mol. Microbiol. 32:403414.
10. Bearden, S. W.,, T. M. Staggs,, and R. D. Perry. 1998. An ABC transporter system of Yersinia pestis allows utilization of chelated iron by Escherichia coli SAB11. J. Bacteriol. 180:11351147.
11. Bearson, B. L.,, L. Wilson,, and J. W. Foster. 1998. A low pH-inducible, PhoPQ-dependent acid tolerance response protects Salmonella typhimurium against inorganic acid stress. J. Bacteriol. 180:24092417.
12. Belasco, J. G. 2010. All things must pass: contrasts and commonalities in eukaryotic and bacterial mRNA decay. Nat. Rev. Mol. Cell Biol. 11:467478.
13. Bennett, R. L.,, and L. I. Rothfield. 1976. Genetic and physiological regulation of intrinsic proteins of the outer membrane of Salmonella typhimurium. J. Bacteriol. 127:498504.
14. Bereswill, S.,, S. Greiner,, A. H. M. van Vliet,, B. Waidner,, F. Fassbinder,, E. Schiltz,, J. G. Kusters,, and M. Kist. 2000. Regulation of ferritin-mediated cytoplasmic iron storage by the ferric uptake regulator homolog (Fur) of Helicobacter pylori. J. Bacteriol. 182:59485953.
15. Berish, S. A.,, S. Subbarao,, C.-Y. Chen,, D. L. Trees,, and S. A. Morse. 1993. Identification and cloning of a fur homolog from Neisseria gonorrhoeae. Infect. Immun. 61:45994606.
16. Bijlsma, J. J. E.,, B. Waidner,, A. H. M. van Vliet,, N. J. Hughes,, S. Häg,, S. Bereswill,, D. J. Kelly,, C. M. J. E. Vandenbroucke-Grauls,, M. Kist,, and J. G. Kusters. 2002. The Helicobacter pylori homologue of the ferric uptake regulator is involved in acid resistance. Infect. Immun. 70:606611.
17. Bobrov, A. G.,, O. Kirillina,, D. A. Ryjenkov,, C. M. Waters,, P. A. Price,, J. D. Fetherston,, D. Mack,, W. E. Goldman,, M. Gomelsky,, and R. D. Perry. 2011. Systematic analysis of cyclic di-GMP signalling enzymes and their role in biofilm formation and virulence in Yersinia pestis. Mol. Microbiol. 79:533551.
18. Bollinger, C. J.,, and P. T. Kallio. 2007. Impact of the small RNA RyhB on growth, physiology and heterologous protein expression in Escherichia coli. FEMS Microbiol. Lett. 275:221228.
19. Braun, V.,, S. Mahren,, and A. Sauter. 2006. Gene regulation by transmembrane signaling. BioMetals 19:103113.
20. Brennan, R. G.,, and T. M. Link. 2007. Hfq structure, function and ligand binding. Curr. Opin. Microbiol. 10:125133.
21. Brickman, T.,, and S. Armstrong. 2009. Temporal signaling and differential expression of Bordetella iron transport systems: the role of ferrimones and positive regulators. BioMetals 22:3341.
22. Brickman, T. J.,, and S. K. Armstrong. 1995. Bordetella pertussis fur gene restores iron repressibility of siderophore and protein expression to deregulated Bordetella bronchiseptica mutants. J. Bacteriol. 177:268270.
23. Bury-Moné, S.,, J.-M. Thiberge,, M. Contreras,, A. Maitournam,, A. Labigne,, and H. De Reuse. 2004. Responsiveness to acidity via metal ion regulators mediates virulence in the gastric pathogen Helicobacter pylori. Mol. Microbiol. 53:623638.
24. Calderwood, S. B.,, and J. J. Mekalanos. 1987. Iron regulation of shiga-like toxin expression in Escherichia coli is mediated by the fur locus. J. Bacteriol. 169:47594764.
25. Calhoun, L. N.,, and Y. M. Kwon. 2011a. The ferritin-like protein Dps protects Salmonella enterica serotype Enteritidis from the Fenton-mediated killing mechanism of bactericidal antibiotics. Int. J. Antimicrob. Agents 37:261265.
26. Calhoun, L. N.,, and Y. M. Kwon. 2011b. Structure, function and regulation of the DNA-binding protein Dps and its role in acid and oxidative stress resistance in Escherichia coli: a review. J. Appl. Microbiol. 110:375386.
27. Carpenter, B. M.,, H. Gancz,, S. L. Benoit,, S. Evans,, C. H. Olsen,, S. L. J. Michel, R. J. Maier, and D. S. Merrell. 2010. Mutagenesis of conserved amino acids of Helicobacter pylori Fur reveals residues important for function. J. Bacteriol. 192:50375052.
28. Carpenter, B. M.,, J. M. Whitmire,, and D. S. Merrell. 2009. This is not your mother’s repressor: the complex role of Fur in pathogenesis. Infect. Immun. 77:25902601.
29. Carpousis, A. J. 2007. The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Annu. Rev. Microbiol. 61:7187.
30. Carrondo, M. A. 2003. Ferritins, iron uptake and storage from the bacterioferritin viewpoint. EMBO J. 22:19591968.
31. Carson, S. D. B.,, C. E. Thomas,, and C. Elkins. 1996. Cloning and sequencing of a Haemophilus ducreyi fur homolog. Gene 176:125129.
32. Celesnik, H.,, A. Deana,, and J. G. Belasco. 2007. Initiation of RNA decay in Escherichia coli by 5 pyrophosphate removal. Mol. Cell 27:7990.
33. Chauvaux, S.,, M.-L. Rosso,, L. Frangeul,, C. Lacroix,, L. Labarre,, A. Schiavo,, M. Marceau,, M.-A. Dillies,, J. Foulon,, J.-Y. Coppée,, C. Médigue,, M. Simonet,, and E. Carniel. 2007. Transcriptome analysis of Yersinia pestis in human plasma: an approach for discovering bacterial genes involved in septicaemic plague. Microbiology 153:31123124.
34. Cornelis, P.,, S. Matthijs,, and L. Van Oeffelen. 2009. Iron uptake regulation in Pseudomonas aeruginosa. BioMetals 22:1522.
35. Costerton, J. W.,, P. S. Stewart,, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:13181322.
36. Coy, M.,, C. Doyle,, J. Besser,, and J. B. Neilands. 1994. Site-directed mutagenesis of the ferric uptake regulation gene of Escherichia coli. BioMetals 7:292298.
37. Coy, M.,, and J. B. Neilands. 1991. Structural dynamics and functional domains of the Fur protein. Biochemistry 30:82018210.
38. Cui, J.,, H. Piao,, S. Jin,, H. S. Na,, Y. Hong,, H. E. Choy,, and P. Y. Ryu. 2009. Effect of iron on cytolysin A expression in Salmonella enterica serovar Typhi. J. Microbiol. 47:479485.
39. Davis, B. M.,, M. Quinones,, J. Pratt,, Y. Ding,, and M. K. Waldor. 2005. Characterization of the small untranslated RNA RyhB and its regulon in Vibrio cholerae. J. Bacteriol. 187:40054014.
40. Deana, A.,, H. Celesnik,, and J. G. Belasco. 2008. The bacterial enzyme RppH triggers messenger RNA degradation by 5 pyrophosphate removal. Nature 451:355358.
41. 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. 185:60326041.
42. Delany, I.,, R. Ieva,, A. Soragni,, M. Hilleringmann,, R. Rappuoli,, and V. Scarlato. 2005. In vitro analysis of protein-operator interactions of the NikR and Fur metal-responsive regulators of coregulated genes in Helicobacter pylori. J. Bacteriol. 187:77037715.
43. Delany, I.,, R. Rappuoli,, and V. Scarlato. 2004. Fur functions as an activator and as a repressor of putative virulence genes in Neisseria meningitidis. Mol. Microbiol. 52:10811090.
44. Delany, I.,, G. Spohn,, A.-B. F. 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. 46:11071122.
45. 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. 42:12971309.
46. de Lorenzo, V.,, M. Herrero,, F. Giovannini,, and J. B. Neilands. 1988. Fur (ferric uptake regulation) protein and CAP (catabolite-activator protein) modulate transcription of fur gene in Escherichia coli. Eur. J. Biochem. 173:537546.
47. de Lorenzo, V.,, J. Perez-Martín,, L. Escolar,, G. Pesole,, and G. Bertoni,. 2004. Mode of binding of the Fur protein to target DNA: negative regulation of iron-controlled gene expression, p. 185196. In J. H. Crosa,, A. R. Mey,, and S. M. Payne (ed.), Iron Transport in Bacteria. ASM Press, Washington, DC.
48. de Lorenzo, V.,, S. Wee,, M. Herrero,, and J. B. Neilands. 1987. Operator sequences of the aerobactin operon of plasmid ColV-K30 binding the ferric uptake regulation (fur) repressor. J. Bacteriol. 169:26242630.
49. Deng, W.,, V. Burland,, G. Plunkett III,, A. Boutin,, G. F. Mayhew,, P. Liss,, N. T. Perna,, D. J. Rose,, B. Mau,, S. Zhou,, D. C. Schwartz,, J. D. Fetherston,, L. E. Lindler,, R. R. Brubaker,, G. V. Plano,, S. C. Straley, K. A. McDonough, M. L. Nilles, J. S. Matson, F. R. Blattner, and R. D. Perry. 2002. Genome sequence of Yersinia pestis KIM. J. Bacteriol. 184:46014611.
50. Desnoyers, G.,, A. Morissette,, K. Prevost,, and E. Massé. 2009. Small RNA-induced differential degradation of the polycistronic mRNA iscRSUA. EMBO J. 28:15511561.
51. Dubos, R. J.,, and J. W. Geiger. 1946. Preparation and properties of Shiga toxin and toxoid. J. Exp. Med. 84:143156.
52. Eisen, R. J.,, S. W. Bearden,, A. P. Wilder,, J. A. Montenieri,, M. F. Antolin,, and K. L. Gage. 2006. Early-phase transmission of Yersinia pestis by unblocked fleas as a mechanism explaining rapidly spreading plague epizootics. Proc. Natl. Acad. Sci. USA 103:1538015385.
53. Ellermeier, J. R.,, and J. M. Slauch. 2008. Fur regulates expression of the Salmonella pathogenicity island 1 type III secretion system through HilD. J. Bacteriol. 190:476486.
54. Ernst, F. D.,, G. Homuth,, J. Stoof,, U. Mäder,, B. Waidner,, E. J. Kuipers,, M. Kist,, J. G. Kusters,, S. Bereswill,, and A. H. M. van Vliet. 2005. Iron-responsive regulation of the Helicobacter pylori iron-cofactored superoxide dismutase SodB is mediated by Fur. J. Bacteriol. 187:36873692.
55. Ernst, J. F.,, R. L. Bennett,, and L. I. Rothfield. 1978. Constitutive expression of the iron-enterochelin and ferrichrome uptake systems in a mutant strain of Salmonella typhimurium. J. Bacteriol. 135:928934.
56. Escolar, L.,, J. Pérez-Martín,, and V. de Lorenzo. 1998. Binding of the Fur (ferric uptake regulator) repressor of Escherichia coli to arrays of the GATAAT sequence. J. Mol. Biol. 283:537547.
57. Escolar, L.,, J. Pérez-Martín,, and V. de Lorenzo. 1999. Opening the iron box: transcriptional metalloregulation by the Fur protein. J. Bacteriol. 181:62236229.
58. Escolar, L.,, J. Pérez-Martín,, and V. de Lorenzo. 2000. Evidence of an unusually long operator for the Fur repressor in the aerobactin promoter of Escherichia coli. J. Biol. Chem. 275:2470924714.
59. Fetherston, J. D.,, V. J. Bertolino,, and R. D. Perry. 1999. YbtP and YbtQ: two ABC transporters required for iron uptake in Yersinia pestis. Mol. Microbiol. 32:289299.
60. Fetherston, J. D.,, O. Kirillina,, A. G. Bobrov,, J. T. Paulley,, and R. D. Perry. 2010. The yersiniabactin transport system is critical for the pathogenesis of bubonic and pneumonic plague. Infect. Immun. 78:20452052.
61. Forman, S.,, M. J. Nagiec,, J. Abney,, R. D. Perry,, and J. D. Fetherston. 2007. Analysis of the aerobactin and ferric hydroxamate uptake systems of Yersinia pestis. Microbiology 153:23322341.
62. Forman, S.,, J. Paulley,, J. Fetherston,, Y.-Q. Cheng,, and R. Perry. 2010. Yersinia ironomics: comparison of iron transporters among Yersinia pestis biotypes and its nearest neighbor, Yersinia pseudotuberculosis. BioMetals 23:275294.
63. Fréchon, D.,, and E. Le Cam. 1994. Fur (ferric uptake regulation) protein interaction with target DNA: comparison of gel retardation, footprinting and elecron microscopy analyses. Biochem. Biophys. Res. Commun. 201:346355.
64. Frohlich, K. S.,, and J. Vogel. 2009. Activation of gene expression by small RNA. Curr. Opin. Microbiol. 12:674682.
65. Gage, K. L.,, and M. Y. Kosoy. 2005. Natural history of plague: perspectives from more than a century of research. Annu. Rev. Entomol. 50:505528.
66. Gancz, H.,, S. Censini,, and D. S. Merrell. 2006. Iron and pH homeostasis intersect at the level of Fur regulation in the gastric pathogen Helicobacter pylori. Infect. Immun. 74:602614.
67. Gao, H.,, D. Zhou,, Y. Li,, Z. Guo,, Y. Han,, Y. Song,, J. Zhai,, Z. Du,, X. Wang,, J. Lu,, and R. Yang. 2008. The iron-responsive Fur regulon in Yersinia pestis. J. Bacteriol. 190:30633075.
68. Gardner, S. E.,, S. E. Fowlston,, and W. L. George. 1990. Effect of iron on production of a possible virulence factor by Plesiomonas shigelloides. J. Clin. Microbiol. 28:811813.
69. Giel, J. L.,, D. Rodionov,, M. Liu,, F. R. Blattner,, and P. J. Kiley. 2006. IscR-dependent gene expression links iron-sulphur cluster assembly to the control of O2-regulated genes in Escherichia coli. Mol. Microbiol. 60:10581075.
70. Glick, R.,, C. Gilmour,, J. Tremblay,, S. Satanower,, O. Avidan,, E. Déziel,, E. P. Greenberg,, K. Poole,, and E. Banin. 2010. Increase in rhamnolipid synthesis under iron-limiting conditions influences surface motility and biofilm formation in Pseudomonas aeruginosa. J. Bacteriol. 192:29732980.
71. Gong, S.,, S. W. Bearden,, V. A. Geoffroy,, J. D. Fetherston,, and R. D. Perry. 2001. Characterization of the Yersinia pestis Yfu ABC iron transport system. Infect. Immun. 67:28292837.
72. Gottesman, S.,, C. A. McCullen,, M. Guillier,, C. K. Vanderpool,, N. Majdalani,, J. Benhammou,, K. M. Thompson,, P. C. FitzGerald,, N. A. Sowa,, and D. J. FitzGerald. 2006. Small RNA regulators and the bacterial response to stress. Cold Spring Harbor Symp. Quant. Biol. 71:111.
73. Grifantini, R.,, E. Frigimelica,, I. Delany,, E. Bartolini,, S. Giovinazzi,, S. Balloni,, S. Agarwal,, G. Galli,, C. Genco,, and G. Grandi. 2004. Characterization of a novel Neisseria meningitidis Fur and iron-regulated operon required for protection from oxidative stress: utility of DNA microarray in the assignment of the biological role of hypothetical genes. Mol. Microbiol. 54:962979.
74. Guina, T.,, S. O. Purvine,, E. C. Yi,, J. Eng,, D. R. Goodlett,, R. Aebersold,, and S. I. Miller. 2003. Quantitative proteomic analysis indicates increased synthesis of a quinolone by Pseudomonas aeruginosa isolates from cystic fibrosis airways. Proc. Natl. Acad. Sci. USA 100:27712776.
75. Gunn, J. S. 2008. The Salmonella PmrAB regulon: lipopolysaccharide modifications, antimicrobial peptide resistance and more. Trends Microbiol. 16:284290.
76. Hall, H. K.,, and J. W. Foster. 1996. The role of Fur in the acid tolerance response of Salmonella typhimurium is physiologically and genetically separable from its role in iron acquisition. J. Bacteriol. 178:56835691.
77. Halsey, T. A.,, A. Vazquez-Torres,, D. J. Gravdahl,, F. C. Fang,, and S. J. Libby. 2004. The ferritin-like Dps protein is required for Salmonella enterica serovar Typhimurium oxidative stress resistance and virulence. Infect. Immun. 72:11551158.
78. Han, Y.,, J. Qiu,, Z. Guo,, H. Gao,, Y. Song,, D. Zhou,, and R. Yang. 2007. Comparative transcriptomics in Yersinia pestis: a global view of environmental modulation of gene expression. BMC Microbiol. 7:96.
79. Hancock, V.,, L. Ferrières,, and P. Klemm. 2008. The ferric yersiniabactin uptake receptor FyuA is required for efficient biofilm formation by urinary tract infectious Escherichia coli in human urine. Microbiology 154:167175.
80. Hantke, K. 2005. Bacterial zinc uptake and regulators. Curr. Opin. Microbiol. 8:196202.
81. Hantke, K. 1984. Cloning of the repressor protein gene of iron-regulated systems in Escherichia coli K12. Mol. Gen. Genet. 197:337341.
82. Hantke, K. 1982. Negative control of iron uptake system in Escherichia coli. FEMS Microbiol. Lett. 15:8386.
83. Hantke, K. 1981. Regulation of ferric iron transport in Escherichia coli K12: isolation of a constitutive mutant. Mol. Gen. Genet. 182:288292.
84. Hantke, K. 1987. Selection procedure for deregulated iron transport mutants (fur) in Escherichia coli K 12: fur not only affects iron metabolism. Mol. Gen. Genet. 210:135139.
85. Hassett, D. J.,, M. L. Howell,, U. A. Ochsner,, M. L. Vasil,, Z. Johnson,, and G. E. Dean. 1997. An operon containing fumC and sodA encoding fumarase C and manganese superoxide dismutase is controlled by the ferric uptake regulator in Pseudomonas aeruginosa: fur mutants produce elevated alginate levels. J. Bacteriol. 179:14521459.
86. Herold, S.,, J. C. Paton,, P. Srimanote,, and A. W. Paton. 2009. Differential effects of short-chain fatty acids and iron on expression of iha in Shiga-toxigenic Escherichia coli. Microbiology 155:35543563.
87. Herrmann, K. M.,, and L. M. Weaver. 1999. The shikimate pathway. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:473503.
88. 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. 65:133143.
89. Hindré, T.,, H. Brüggemann,, C. Buchrieser,, and Y. Héchard. 2008. Transcriptional profiling of Legionella pneumophila biofilm cells and the influence of iron on biofilm formation. Microbiology 154:3041.
90. Holmes, K.,, F. Mulholland,, B. M. Pearson,, C. Pin,, J. McNicholl-Kennedy,, J. M. Ketley,, and J. M. Wells. 2005. Campylobacter jejuni gene expression in response to iron limitation and the role of Fur. Microbiology 151:243257.
91. Ikeda, J. S.,, A. Janakiraman,, D. G. Kehres,, M. E. Maguire,, and J. M. Slauch. 2005. Transcriptional regulation of sitABCD of Salmonella enterica serovar Typhimurium by MntR and Fur. J. Bacteriol. 187:912922.
92. Ikeda, Y.,, M. Yagi,, T. Morita,, and H. Aiba. 2011. Hfq binding at RhlB-recognition region of RNase E is crucial for the rapid degradation of target mRNAs mediated by sRNAs in Escherichia coli. Mol. Microbiol. 79:419432.
93. Inglesby, T. V.,, D. T. Dennis,, D. A. Henderson,, J. G. Bartlett,, M. S.Ascher, E. Eitzen, A. D. Fine, A. M. Friedlander, J. Hauer, J. F. Koerner, M. Layton, J. McDade, M. T. Osterholm, T. O’Toole, G. Parker, T. M. Perl, P. K. Russell, M. Schoch-Spana, and K. Tonat. 2000. Plague as a biological weapon: medical and public health management. JAMA 283:22812290.
94. Jackson, S.,, and T. W. Burrows. 1956. The virulence-enhancing effect of iron on non-pigmented mutants of virulent strains of Pasteurella pestis. Br. J. Exp. Pathol. 37:577583.
95. Jacobsen, I.,, J. Gerstenberger,, A. D. Gruber,, J. T. Bossé,, P. R. Langford,, I. Hennig-Pauka,, J. Meens,, and G.-F. Gerlach. 2005. Deletion of the ferric uptake regulator Fur impairs the in vitro growth and virulence of Actinobacillus pleuropneumoniae. Infect. Immun. 73:37403744.
96. Jacques, J. F.,, S. Jang,, K. Prevost,, G. Desnoyers,, M. Desmarais,, J. Imlay,, and E. Massé. 2006. RyhB small RNA modulates the free intracellular iron pool and is essential for normal growth during iron limitation in Escherichia coli. Mol. Microbiol. 62:11811190.
97. Johnston, A.,, J. Todd,, A. Curson,, S. Lei,, N. Nikolaidou-Katsaridou,, M. Gelfand,, and D. Rodionov. 2007. Living without Fur: the subtlety and complexity of iron-responsive gene regulation in the symbiotic bacterium Rhizobium and other α-proteobacteria. BioMetals 20:501511.
98. Karjalainen, T. K.,, D. G. Evans,, D. J. Evans, Jr., D. Y. Graham, and C.-H. Lee. 1991. Iron represses the expression of CFA/I fimbriae of enterotoxigenic E. coli. Microb. Pathog. 11:317323.
99. Kim, J.-S.,, M.-H. Sung,, D.-H. Kho,, and J. K. Lee. 2005. Induction of manganese-containing superoxide dismutase is required for acid tolerance in Vibrio vulnificus. J. Bacteriol. 187:59845995.
100. Kirillina, O.,, A. G. Bobrov,, J. D. Fetherston,, and R. D. Perry. 2006. A hierarchy of iron uptake systems: Yfu and Yiu are functional in Yersinia pestis. Infect. Immun. 74:61716178.
101. Lamont, I. L.,, P. A. Beare,, U. Ochsner,, A. I. Vasil,, and M. L. Vasil. 2002. Siderophore-mediated signaling regulates virulence factor production in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 99:70727077.
102. Lankford, C. E. 1973. Bacterial assimilation of iron. CRC Crit. Rev. Microbiol. 2:273331.
103. Larkin, M. A.,, G. Blackshields,, N. P. Brown,, R. Chenna,, P. A. McGettigan,, H. McWilliam,, F. Valentin,, I. M. Wallace,, A. Wilm,, R. Lopez,, J. D. Thompson,, T. J. Gibson,, and D. G. Higgins. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:29472948.
104. Lathem, W. W.,, S. D. Crosby,, V. L. Miller,, and W. E. Goldman. 2005. Progression of primary pneumonic plague: a mouse model of infection, pathology, and bacterial transcriptional activity. Proc. Natl. Acad. Sci. USA 102:1778617791.
105. Lavrrar, J. L.,, C. A. Christoffersen,, and M. A. McIntosh. 2002. Fur-DNA interactions at the bidirectional fepDGC-entS promoter region in Escherichia coli. J. Mol. Biol. 322:983995.
106. Lease, R. A.,, and M. Belfort. 2000a. Riboregulation by DsrA RNA: trans-actions for global economy. Mol. Microbiol. 38:667672.
107. Lease, R. A.,, and M. Belfort. 2000b. A trans-acting RNA as a control switch in Escherichia coli: DsrA modulates function by forming alternative structures. Proc. Natl. Acad. Sci. USA 97:99199924.
108. Lee, H.-J.,, S. H. Bang,, K.-H. Lee,, and S.-J. Park. 2007. Positive regulation of fur gene expression via direct interaction of Fur in a pathogenic bacterium, Vibrio vulnificus. J. Bacteriol. 189:26292636.
109. 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. 185:58915896.
110. Lee, J.-W.,, and J. Helmann. 2007. Functional specialization within the Fur family of metalloregulators. BioMetals 20:485499.
111. Lee-Lewis, H.,, and D. M. Anderson. 2010. Absence of inflammation and pneumonia during infection with nonpigmented Yersinia pestis reveals a new role for the pgm locus in pathogenesis. Infect. Immun. 78:220230.
112. Lencčo, J.,, M. Hubálek,, P. Larsson,, A. Fucčíková,, M. Brychta,, A. Macela,, and J. Stulík. 2007. Proteomics analysis of the Francisella tularensis LVS response to iron restriction: induction of the F. tularensis pathogenicity island proteins IglABC. FEMS Microbiol. Lett. 269:1121.
113. Loprasert, S.,, R. Sallabhan,, W. Whangsuk,, and S. Mongkolsuk. 2000. Characterization and mutagenesis of fur gene from Burkholderia pseudomallei. Gene 254:129137.
114. Luke, N. R.,, A. J. Howlett,, J. Shao,, and A. A. Campagnari. 2004. Expression of type IV pili by Moraxella catarrhalis is essential for natural competence and is affected by iron limitation. Infect. Immun. 72:62626270.
115. Lymberopoulos, M. H.,, S. Houle,, F. Daigle,, S. Léveillé,, A. Brée,, M. Moulin-Schouleur,, J. R. Johnson,, and C. M. Dozois. 2006. Characterization of Stg fimbriae from an avian pathogenic Escherichia coli O78:K80 strain and assessment of their contribution to colonization of the chicken respiratory tract. J. Bacteriol. 188:64496459.
116. Maki, K.,, K. Uno,, T. Morita,, and H. Aiba. 2008. RNA, but not protein partners, is directly responsible for translational silencing by a bacterial Hfq-binding small RNA. Proc. Natl. Acad. Sci. USA 105:1033210337.
117. Massé, E.,, F. E. Escorcia,, and S. Gottesman. 2003. Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev. 17:23742383.
118. 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 99:46204625.
119. Massé, E.,, C. K. Vanderpool,, and S. Gottesman. 2005. Effect of RyhB small RNA on global iron use in Escherichia coli. J. Bacteriol. 187:69626971.
120. Merrell, D. S.,, L. J. Thompson,, C. C. Kim,, H. Mitchell,, L. S. Tompkins,, A. Lee,, and S. Falkow. 2003. Growth phase-dependent response of Helicobacter pylori to iron starvation. Infect. Immun. 71:65106525.
121. Mey, A. R.,, S. A. Craig,, and S. M. Payne. 2005a. Characterization of Vibrio cholerae RyhB: the RyhB regulon and role of ryhB in biofilm formation. Infect. Immun. 73:57065719.
122. Mey, A. R.,, E. E. Wyckoff,, V. Kanukurthy,, C. R. Fisher,, and S. M. Payne. 2005b. Iron and Fur regulation in Vibrio cholerae and the role of Fur in virulence. Infect. Immun. 73:81678178.
123. Mey, A. R.,, E. E. Wyckoff,, A. G. Oglesby,, E. Rab,, R. K. Taylor,, and S. M. Payne. 2002. Identification of the Vibrio cholerae enterobactin receptors VctA and IrgA: IrgA is not required for virulence. Infect. Immun. 70:34193426.
124. Mills, S. A.,, and M. A. Marletta. 2005. Metal binding characteristics and role of iron oxidation in the ferric uptake regulator from Escherichia coli. Biochemistry 44:1355313559.
125. Mitarai, N.,, J. A. Benjamin,, S. Krishna,, S. Semsey,, Z. Csiszovszki,, E. Massé,, and K. Sneppen. 2009. Dynamic features of gene expression control by small regulatory RNAs. Proc. Natl. Acad. Sci. USA 106:1065510659.
126. Moll, I.,, T. Afonyushkin,, O. Vytvytska,, V. R. Kaberdin,, and U. Blasi. 2003. Coincident Hfq binding and RNase E cleavage sites on mRNA and small regulatory RNAs. RNA 9:13081314.
127. Morita, T.,, and H. Aiba. 2011. RNase E action at a distance: degradation of target mRNAs mediated by an Hfq-binding small RNA in bacteria. Genes Dev. 25:294298.
128. Morita, T.,, K. Maki,, and H. Aiba. 2005. RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs. Genes Dev. 19:21762186.
129. Murphy, E. R.,, and S. M. Payne. 2007. RyhB, an iron-responsive small RNA molecule, regulates Shigella dysenteriae virulence. Infect. Immun. 75:34703477.
130. Musk, D. J.,, D. A. Banko,, and P. J. Hergenrother. 2005. Iron salts perturb biofilm formation and disrupt existing biofilms of Pseudomonas aeruginosa. Chem. Biol. 12:789796.
131. Najimi, M.,, M. L. Lemos,, and C. R. Osorio. 2009. Identification of iron regulated genes in the fish pathogen Aeromonas salmonicida subsp. salmonicida: genetic diversity and evidence of conserved iron uptake systems. Vet. Microbiol. 133:377382.
132. Nandal, A.,, C. C. O. Huggins,, M. R. Woodhall,, J. McHugh,, F. Rodríguez-Quiñones,, M. A. Quail,, J. R. Guest,, and S. C. Andrews. 2010. Induction of the ferritin gene (ftnA) of Escherichia coli by Fe2+-Fur is mediated by reversal of H-NS silencing and is RyhB independent. Mol. Microbiol. 75:637657.
133. Niederhoffer, E. C.,, C. M. Naranjo,, K. L. Bradley,, and J. A. Fee. 1990. Control of Escherichia coli superoxide dismutase (sodA and sodB) genes by the ferric uptake regulation (fur) locus. J. Bacteriol. 172:19301938.
134. Ochsner, U. A.,, A. I. Vasil,, and M. L. Vasil. 1995. Role of the ferric uptake regulator of Pseudomonas aeruginosa in the regulation of siderophores and exotoxin A expression: purification and activity on iron-regulated promoters. J. Bacteriol. 177:71947201.
135. Ochsner, U. A.,, and M. L. Vasil. 1996. Gene repression by the ferric uptake regulator in Pseudomonas aeruginosa: cycle selection of iron-regulated genes. Proc. Natl. Acad. Sci. USA 93:44094414.
136. Ochsner, U. A.,, P. J. Wilderman,, A. I. Vasil,, and M. L. Vasil. 2002. GeneChip® expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes. Mol. Microbiol. 45:12771287.
137. Oglesby, A. G.,, J. M. Farrow III,, J.-H. Lee,, A. P. Tomaras,, E. P. Greenberg,, E. C. Pesci,, and M. L. Vasil. 2008. The influence of iron on Pseudomonas aeruginosa physiology: a regulatory link between iron and quorum sensing. J. Biol. Chem. 283:1555815567.
138. Oglesby, A. G.,, E. R. Murphy,, V. R. Iyer,, and S. M. Payne. 2005. Fur regulates acid resistance in Shigella flexneri via RyhB and ydeP. Mol. Microbiol. 58:13541367.
139. Outten, F. W.,, O. Djaman,, and G. Storz. 2004. A suf operon requirement for Fe-S cluster assembly during iron starvation in Escherichia coli. Mol. Microbiol. 52:861872.
140. Padalon-Brauch, G.,, R. Hershberg,, M. Elgrably-Weiss,, K. Baruch,, I. Rosenshine,, H. Margalit,, and S. Altuvia. 2008. Small RNAs encoded within genetic islands of Salmonella typhimurium show host-induced expression and role in virulence. Nucleic Acids Res. 36:19131927.
141. Palyada, K.,, D. Threadgill,, and A. Stintzi. 2004. Iron acquisition and regulation in Campylobacter jejuni. J. Bacteriol. 186:47144729.
142. Patzer, S. I.,, and K. Hantke. 2001. Dual repression by Fe2+-Fur and Mn2+-MntR of the mntH gene, encoding an NRAMP-Like Mn2+ transporter in Escherichia coli. J. Bacteriol. 183:48064813.
143. Payne, S. M. 1988. Iron and virulence in the family Enterobacteriaceae. CRC Crit. Rev. Microbiol. 16:81111.
144. Payne, S. M.,, E. E. Wyckoff,, E. R. Murphy,, A. G. Oglesby,, M. L.Boulette, and N. M. Davies. 2006. Iron and pathogenesis of Shigella: iron acquisition in the intracellular environment. BioMetals 19:173180.
145. Pecqueur, L.,, B. D’Autréaux,, J. Dupuy,, Y. Nicolet,, L. Jacquamet,, B. Brutscher,, I. Michaud-Soret,, and B. Bersch. 2006. Structural changes of Escherichia coli ferric uptake regulator during metal-dependent dimerization and activation explored by NMR and X-ray crystallography. J. Biol. Chem. 281:2128621295.
146. Perry, R. D.,, J. Abney,, I. Mier, Jr., Y. Lee, S. W. Bearden, and J. D. Fetherston. 2003. Regulation of the Yersinia pestis Yfe and Ybt iron transport systems. Adv. Exp. Med. Biol. 529:275283.
147. Perry, R. D.,, A. G. Bobrov,, O. Kirillina,, and J. D. Fetherston. Yersinia pestis transition metal divalent cation transporters. Adv. Exp. Med. Biol., in press.
148. Perry, R. D.,, A. G. Bobrov,, O. Kirillina,, H. A. Jones,, L. L. Pedersen,, J. Abney,, and J. D. Fetherston. 2004. Temperature regulation of the hemin storage (Hms+) phenotype of Yersinia pestis is posttranscriptional. J. Bacteriol. 186:16381647.
149. Perry R. D.,, S. K. Craig,, J. Abney,, A. G. Bobrov,, O. Kirillina,, I. Mier, Jr.,, H. Truszczynska,, and J. D. Fetherston. 2012. Manganese transporters Yfe and Mnth are Fur-regulated and important for the virulence of Yersinia pestis. Microbiology 158:804815.
150. Perry, R. D.,, and J. D. Fetherston. 1997. Yersinia pestis—etiologic agent of plague. Clin. Microbiol. Rev. 10:3566.
151. Perry, R. D.,, and J. D. Fetherston. 2011. Yersiniabactin iron uptake: mechanisms and role in Yersinia pestis pathogenesis. Microbes Infect. 13:808817.
152. Perry, R. D.,, I. Mier, Jr., and J. D. Fetherston. 2007. Roles of the Yfe and Feo transporters of Yersinia pestis in iron uptake and intracellular growth. BioMetals 20:699703.
153. Pieper, R.,, S.-T. Huang,, P. P. Parmar,, D. J. Clark,, H. Alami,, R. D. Fleischmann,, R. D. Perry,, and S. N. Peterson. 2010. Proteomic analysis of iron acquisition, metabolic and regulatory responses of Yersinia pestis to iron starvation. BMC Microbiol. 10:30.
154. 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. 47:903915.
155. Preston, M. J.,, S. M. Fleiszig,, T. S. Zaidi,, J. B. Goldberg,, V. D. Shortridge,, M. L. Vasil,, and G. B. Pier. 1995. Rapid and sensitive method for evaluating Pseudomonas aeruginosa virulence factors during corneal infections in mice. Infect. Immun. 63:34973501.
156. Prevost, K.,, H. Salvail,, G. Desnoyers,, J. F. Jacques,, E. Phaneuf,, and E. Massé. 2007. The small RNA RyhB activates the translation of shiA mRNA encoding a permease of shikimate, a compound involved in siderophore synthesis. Mol. Microbiol. 64:12601273.
157. Prince, R. W.,, C. D. Cox,, and M. L. Vasil. 1993. Coordinate regulation of siderophore and exotoxin A production: molecular cloning and sequencing of the Pseudomonas aeruginosa fur gene. J. Bacteriol. 175:25892598.
158. Prince, R. W.,, D. G. Storey,, A. I. Vasil,, and M. L. Vasil. 1991. Regulation of toxA and regA by the Escherichia coli fur gene and identification of a Fur homologue in Pseudomonas aeruginosa PA103 and PA01. Mol. Microbiol. 5:28232831.
159. Privalle, C. T.,, and I. Fridovich. 1993. Iron specificity of the Fur-dependent regulation of the biosynthesis of the manganese-containing superoxide dismutase in Escherichia coli. J. Biol. Chem. 268:51785181.
160. Rashid, R. A.,, P. I. Tarr,, and S. L. Moseley. 2006. Expression of the Escherichia coli IrgA homolog adhesin is regulated by the ferric uptake regulation protein. Microb. Pathog. 41:207217.
161. Rossi, M.-S.,, J. D. Fetherston,, S. Létoffé,, E. Carniel,, R. D. Perry,, and J.-M. Ghigo. 2001. Identification and characterization of the hemophore-dependent heme acquisition system of Yersinia pestis. Infect. Immun. 69:67076717.
162. Runyen-Janecky, L.,, E. Dazenski,, S. Hawkins,, and L. Warner. 2006. Role and regulation of the Shigella flexneri Sit and MntH systems. Infect. Immun. 74:46664672.
163. Salvail, H.,, P. Lanthier-Bourbonnais,, J. M. Sobota,, M. Caza,, J. A. Benjamin,, M. E. Mendieta,, F. Lepine,, C. M. Dozois,, J. Imlay,, and E. Massé. 2010. A small RNA promotes siderophore production through transcriptional and metabolic remodeling. Proc. Natl. Acad. Sci. USA 107:1522315228.
164. Santos, J. A.,, C. J. González,, T. M. López,, A. Otero,, and M. L. García-López. 1999. Hemolytic and elastolytic activities influenced by iron in Plesiomonas shigelloides. J. Food Prot. 62:14751477.
165. Schäffer, S.,, K. Hantke,, and V. Braun. 1985. Nucleotide sequence of the iron regulatory gene fur. Mol. Gen. Genet. 200:110113.
166. Schmitt, M. P.,, and S. M. Payne. 1988. Genetics and regulation of enterobactin genes in Shigella flexneri. J. Bacteriol. 170:55795587.
167. Sebastian, S.,, S. Agarwal,, J. R. Murphy,, and C. A. Genco. 2002. The gonococcal Fur regulon: identification of additional genes involved in major catabolic, recombination, and secretory pathways. J. Bacteriol. 184:39653974.
168. Sebbane, F.,, N. Lemaître,, D. E. Sturdevant,, R. Rebeil,, K. Virtaneva,, S. F. Porcella,, and B. J. Hinnebusch. 2006. Adaptive response of Yersinia pestis to extracellular effectors of innate immunity during bubonic plague. Proc. Natl. Acad. Sci. USA 103:1176611771.
169. Sha, J.,, M. Lu,, and A. K. Chopra. 2001. Regulation of the cytotoxic enterotoxin gene in Aeromonas hydrophila: characterization of an iron uptake regulator. Infect. Immun. 69:63706381.
170. Sheikh, M. A.,, and G. L. Taylor. 2009. Crystal structure of the Vibrio cholerae ferric uptake regulator (Fur) reveals insights into metal co-ordination. Mol. Microbiol. 72:12081220.
171. Singh, P. K. 2004. Iron sequestration by human lactoferrin stimulates P. aeruginosa surface motility and blocks biofilm formation. BioMetals 17:267270.
172. Smith, A.,, N. I. Hooper,, N. Shipulina,, and W. T. Morgan. 1996. Heme binding by a bacterial repressor protein, the gene product of the ferric uptake regulation (fur) gene of Escherichia coli. J. Protein Chem. 15:575583.
173. Staggs, T. M.,, J. D. Fetherston,, and R. D. Perry. 1994. Pleiotropic effects of a Yersinia pestis fur mutation. J. Bacteriol. 176:76147624.
174. Staggs, T. M.,, and R. D. Perry. 1991. Identification and cloning of a fur regulatory gene in Yersinia pestis. J. Bacteriol. 173:417425.
175. Stoebner, J. A.,, and S. M. Payne. 1988. Iron-regulated hemolysin production and utilization of heme and hemoglobin by Vibrio cholerae. Infect. Immun. 56:28912895.
176. Stojiljkovic, I.,, and K. Hantke. 1995. Functional domains of the Escherichia coli ferric uptake regulator protein (Fur). Mol. Gen. Genet. 247:199205.
177. Tardat, B.,, and D. Touati. 1993. Iron and oxygen regulation of Escherichia coli MnSOD expression: competition between the global regulators Fur and ArcA for binding to DNA. Mol. Microbiol. 9:5363.
178. Thomas, C. E.,, and P. F. Sparling. 1994. Identification and cloning of fur homologue from Neisseria meningitidis. Mol. Microbiol. 11:725737.
179. Thompson, J. M.,, H. A. Jones,, and R. D. Perry. 1999. Molecular characterization of the hemin uptake locus (hmu) from Yersinia pestis and analysis of hmu mutants for hemin and hemoprotein utilization. Infect. Immun. 67:38793892.
180. 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. 176:213220.
181. Tomich, M.,, and C. D. Mohr. 2004. Transcriptional and posttranscriptional control of cable pilus gene expression in Burkholderia cenocepacia. J. Bacteriol. 186:10091020.
182. Torres, A. G.,, L. Milflores-Flores,, J. G. Garcia-Gallegos,, S. D. Patel,, A. Best,, R. M. La Ragione,, Y. Martinez-Laguna,, and M. J.Woodward. 2007. Environmental regulation and colonization attributes of the long polar fimbriae (LPF) of Escherichia coli O157:H7. Int. J. Med. Microbiol. 297:177185.
183. Touati, D.,, M. Jacques,, B. Tardat,, L. Bouchard,, and S. Despied. 1995. Lethal oxidative damage and mutagenesis are generated by iron in Δfur mutants of Escherichia coli: protective role of superoxide dismutase. J. Bacteriol. 177:23052314.
184. Troxell, B.,, M. L. Sikes,, R. C. Fink,, A. Vazquez-Torres,, J. Jones-Carson,, and H. M. Hassan. 2011. Fur negatively regulates hns and is required for the expression of HilA and virulence in Salmonella enterica serovar Typhimurium. J. Bacteriol. 193:497505.
185. Valentin-Hansen, P.,, M. Eriksen,, and C. Udesen. 2004. The bacterial Sm-like protein Hfq: a key player in RNA transactions. Mol. Microbiol. 51:15251533.
186. Valenzuela, M.,, J. P. Albar,, A. Paradela,, and H. Toledo. 2011. Helicobacter pylori exhibits a Fur-dependent acid tolerance response. Helicobacter 16:189199.
187. Vasil, M. L. 2007. How we learnt about iron acquisition in Pseudomonas aeruginosa: a series of very fortunate events. BioMetals 20:587601.
188. Vasil, M. L.,, and U. A. Ochsner. 1999. The response of Pseudomonas aeruginosa to iron: genetics, biochemistry and virulence. Mol. Microbiol. 34:399413.
189. Večerek, B.,, I. Moll,, and U. Bläsi. 2007. Control of Fur synthesis by the non-coding RNA RyhB and iron-responsive decoding. EMBO J. 26:965975.
190. Venturi, V.,, C. Ottevanger,, M. Bracke,, and P. Weisbeek. 1995. Iron regulation of siderophore biosynthesis and transport in Pseudomonas putida WCS358: involvement of a transcriptional activator and of the Fur protein. Mol. Microbiol. 15:10811093.
191. Vetter, S. M.,, R. J. Eisen,, A. M. Schotthoefer,, J. A. Montenieri,, J. L.Holmes, A. G. Bobrov, S. W. Bearden, R. D. Perry, and K. L. Gage. 2010. Biofilm formation is not required for early-phase transmission of Yersinia pestis. Microbiology 156:22162225.
192. Waidner, B.,, S. Greiner,, S. Odenbreit,, H. Kavermann,, J. Velayudhan,, F. Stähler,, J. Guhl,, E. Bissé,, A. H. M. van Vliet,, S. C. Andrews,, J. G.Kusters, D. J. Kelly, R. Haas, M. Kist, and S. Bereswill. 2002. Essential role of ferritin Pfr in Helicobacter pylori iron metabolism and gastric colonization. Infect. Immun. 70:39233929.
193. Wang, F.,, S. Cheng,, K. Sun,, and L. Sun. 2008. Molecular analysis of the fur (ferric uptake regulator) gene of a pathogenic Edwardsiella tarda strain. J. Microbiol. 46:350355.
194. Watnick, P. I.,, T. Eto,, H. Takahashi,, and S. B. Calderwood. 1997. Purification of Vibrio cholerae Fur and estimation of its intracellular abundance by antibody sandwich enzyme-linked immunosorbent assay. J. Bacteriol. 179:243247.
195. Wilderman, P. J.,, N. A. Sowa,, D. J. FitzGerald,, P. C. FitzGerald,, S. Gottesman,, U. A. Ochsner,, and M. L. Vasil. 2004. Identification of tandem duplicate regulatory small RNAs in Pseudomonas aeruginosa involved in iron homeostasis. Proc. Natl. Acad. Sci. USA 101:97929797.
196. Wilmes-Riesenberg, M. R.,, B. Bearson,, J. W. Foster,, and R. Curtis III. 1996. Role of the acid tolerance response in virulence of Salmonella typhimurium. Infect. Immun. 64:10851092.
197. Wu, Y.,, and F. W. Outten. 2009. IscR controls iron-dependent biofilm formation in Escherichia coli by regulating type I fimbria expression. J. Bacteriol. 191:12481257.
198. Wyckoff, E. E.,, A. R. Mey,, and S. M. Payne. 2007. Iron acquisition in Vibrio cholerae. BioMetals 20:405416.
199. Xiong, Y. Q.,, M. L. Vasil,, Z. Johnson,, U. A. Ochsner,, and A. S. Bayer. 2000. The oxygen- and iron-dependent sigma factor pvdS of Pseudomonas aeruginosa is an important virulence factor in experimental infective endocarditis. J. Infect. Dis. 181:10201026.
200. Yang, Y.,, D. P. Harris,, F. Luo,, L. Wu,, A. B. Parsons,, A. V. Palumbo,, and J. Zhou. 2008. Characterization of the Shewanella oneidensis Fur gene: roles in iron and acid tolerance response. BMC Genomics 9:S11.
201. Zheng, M.,, B. Doan,, T. D. Schneider,, and G. Storz. 1999. OxyR and SoxRS regulation of fur. J. Bacteriol. 181:46394643.
202. Zhou, D.,, L. Qin,, Y. Han,, J. Qiu,, Z. Chen,, B. Li,, Y. Song,, J. Wang,, Z. Guo,, J. Zhai,, Z. Du,, X. Wang,, and R. Yang. 2006. Global analysis of iron assimilation and fur regulation in Yersinia pestis. FEMS Microbiol. Lett. 258:917.
203. Zhu, C.,, M. Ngeleka,, A. A. Potter,, and B. J. Allan. 2002. Effect of fur mutation on acid-tolerance response and in vivo virulence of avian septicemic Escherichia coli. Can. J. Microbiol. 48:458462.

Tables

Generic image for table
Table 1

Iron transport systems of

Citation: Perry R, McDonough K. 2013. Iron Regulation and Virulence in Gram-Negative Bacterial Pathogens with as a Paradigm, p 106-132. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch6

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error