The yfe and feo transporters are involved in microaerobic growthand virulence of Yersinia pestis in bubonic plague

Infection and Immunity

Volumn 80, Issue 11, 2012, Pages 3880-3891

  Fetherston, Jacqueline D ^a   Mier, Ildefonso ^a   Perry, Robert D ^a   Truszczynska, Helena ^b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; SIDEROPHORE; YERSINIABACTIN;

ARCA BACTERIAL GENE; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; FEO BACTERIAL GENE; FEOC BACTERIAL GENE; FNR BACTERIAL GENE; GENE EXPRESSION; GENE LOCUS; GENE MUTATION; IRON TRANSPORT; LD 50; NONHUMAN; OPERON; OXYR BACTERIAL GENE; PHENOTYPE; PLAGUE; PRIORITY JOURNAL; RSTAB BACTERIAL GENE; YERSINIA PESTIS;

EID: 84867592145     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00086-12     Document Type: Article

References (94)

1. Anaya-Bergman C, et al. 2010. Porphyromonas gingivalis ferrous iron transporter FeoB1 influences sensitivity to oxidative stress. Infect. Immun. 78:688-696.
2. Artola-Recolons C, et al. 2011. High-resolution crystal structure of MltE, an outer membrane-anchored endolytic peptidoglycan lytic transglycosylase from Escherichia coli. Biochemistry 50:2384 -2386.
3. Bearden SW, Fetherston JD, Perry RD. 1997. Genetic organization of the yersiniabactin biosynthetic region and construction of avirulent mutants in Yersinia pestis. Infect. Immun. 65:1659 -1668.
4. Bearden SW, Perry RD. 1999. The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague. Mol. Microbiol. 32:403-414.
5. Bearden SW, Staggs TM, Perry RD. 1998. An ABC transporter system of Yersinia pestis allows utilization of chelated iron by Escherichia coli SAB11. J. Bacteriol. 180:1135-1147.
6. Beesley ED, Brubaker RR, Janssen WA, Surgalla MJ. 1967. Pesticins. III.Expression of coagulase and mechanism of fibrinolysis. J. Bacteriol. 94:19-26.
7. Boulette ML, Payne SM. 2007. Anaerobic regulation of Shigella flexneri virulence: ArcA regulates fur and iron acquisition genes. J. Bacteriol. 189: 6957-6967.
8. Boyer E, Bergevin I, Malo D, Gros P, Cellier MFM. 2002. Acquisition of Mn(II) in addition to Fe(II) is required for full virulence of Salmonella enterica serovar Typhimurium. Infect. Immun. 70:6032-6042.
9. Brickman T, Armstrong S. 2009. Temporal signaling and differential expression of Bordetella iron transport systems: the role of ferrimones and positive regulators. Biometals 22:33-41.
10. Brickman TJ, Hanawa T, Anderson MT, Suhadolc RJ, Armstrong SK.2008. Differential expression of Bordetella pertussis iron transport system genes during infection. Mol. Microbiol. 70:3-14.
11. Brickman TJ, Vanderpool CK, Armstrong SK. 2006. Heme transport contributes to in vivo fitness of Bordetella pertussis during primary infection in mice. Infect. Immun. 74:1741-1744.
12. Cartron ML, Maddocks S, Gillingham P, Craven CJ, Andrews SC. 2006. Feo-transport of ferrous iron into bacteria. Biometals 19:143-157.
13. Casadaban MJ. 1975. Fusion of the Escherichia coli lac genes to the ara promoter: a general technique using bacteriophage Mu-1 insertions. Proc. Natl. Acad. Sci. U. S. A. 72:809-813.
14. Castilho BA, Olfson P, Casadaban MJ. 1984. Plasmid insertion mutagenesis and lac gene fusion with mini-Mu bacteriophage transposons. J. Bacteriol. 158:488-495.
15. Cavanaugh DC, Randall R. 1959. The role of multiplication of Pasteurella pestis in mononuclear phagocytes in the pathogenesis of flea-borne plague. J. Immunol. 83:348 -363.
16. Chan ACK, et al. 2010. Structure and function of P19, a high-affinity iron transporter of the human pathogen Campylobacter jejuni. J. Mol. Biol.401:590-604.
17. Chatfield CH, Mulhern BJ, Burnside DM, Cianciotto NP. 2011. Legionella pneumophila LbtU acts as a novel, TonB-independent receptor for the legiobactin siderophore. J. Bacteriol. 193:1563-1575.
18. Cherepanov PP, Wackernagel W. 1995. Gene disruption in Escherichia coli: TcR andKmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158:9 -14.
19. Choi E, Groisman EA, Shin D. 2009. Activated by different signals, the PhoP/PhoQ two-component system differentially regulates metal uptake. J. Bacteriol. 191:7174 -7181.
20. Cianciotto N. 2007. Iron acquisition by Legionella pneumophila. Biometals 20:323-331.
21. Crosa JH, Mey AR, Payne SM (ed). 2004. Iron transport in bacteria. ASM Press, Washington, DC.
22. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
23. Deng W, et al. 2002. Genome sequence of Yersinia pestis KIM. J. Bacteriol.184:4601-4611.
24. Dubbels BL, et al. 2004. Evidence for a copper-dependent iron transport system in the marine, magnetotactic bacterium strain MV-1. Microbiology 150:2931-2945.
25. Evans SL, Arceneaux JEL, Byers BR, Martin ME, Aranha H. 1986.Ferrous iron transport in Streptococcus mutans. J. Bacteriol. 168:1096-26.
26. Fetherston JD, Bearden SW, Perry RD. 1996. YbtA, an AraC-type regulator of the Yersinia pestis pesticin/yersiniabactin receptor. Mol. Microbiol.22:315-325.
27. Fetherston JD, Bertolino VJ, Perry RD. 1999. YbtP and YbtQ: two ABC transporters required for iron uptake in Yersinia pestis. Mol. Microbiol. 32:289 -299.
28. Fetherston JD, Kirillina O, Bobrov AG, Paulley JT, Perry RD. 2010. The yersiniabactin transport system is critical for the pathogenesis of bubonic and pneumonic plague. Infect. Immun. 78:2045-2052.
29. Fetherston JD, Lillard JW, Jr, Perry RD. 1995. Analysis of the pesticin receptor from Yersinia pestis: role in iron-deficient growth and possible regulation by its siderophore. J. Bacteriol. 177:1824 -1833.
30. Fetherston JD, Schuetze P, Perry RD. 1992. Loss of the pigmentation phenotype in Yersinia pestis is due to the spontaneous deletion of 102 kb of chromosomal DNA which is flanked by a repetitive element. Mol. Microbiol. 6:2693-2704.
31. Fields KA, Nilles ML, Cowan C, Straley SC. 1999. Virulence role of V antigen of Yersinia pestis at the bacterial surface. Infect. Immun. 67:5395-5408.
32. Fisher CR, et al. 2009. Genetics and virulence association of the Shigella flexneri Sit iron transport system. Infect. Immun. 77:1992-1999.
33. Forman S, Paulley JT, Fetherston JD, Cheng Y-Q, Perry RD. 2010. Yersinia ironomics: comparison of iron transporters among Yersinia pestis biotypes and its nearest neighbor, Yersinia pseudotuberculosis. Biometals 23:275-294.
34. Forman S, et al. 2008. yadBC of Yersinia pestis, a new virulence determinant for bubonic plague. Infect. Immun. 76:578 -587.
35. Gao H, et al. 2008. The iron-responsive Fur regulon in Yersinia pestis. J. Bacteriol. 190:3063-3075.
36. Gong S, Bearden SW, Geoffroy VA, Fetherston JD, Perry RD. 2001. Characterization of the Yersinia pestis Yfu ABC iron transport system.Infect. Immun. 67:2829 -2837.
37. Grabenstein JP, Fukuto HS, Palmer LE, Bliska JB. 2006. Characterization of phagosome trafficking and identification of PhoP-regulated genes important for survival of Yersinia pestis in macrophages. Infect. Immun. 74:3727-3741.
38. Guo J, Nair MKM, Galván EM, Liu S-L, Schifferli DM. 2011. Tn5AraOut mutagenesis for the identification of Yersinia pestis genes involved in resistance towards cationic antimicrobial peptides. Microb. Pathog.51:121-132.
39. Guzman LM, Belin D, Carson MJ, Beckwith J. 1995. Tight regulation,modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177:4121-4130.
40. Hantke K. 1987. Ferrous iron transport mutants in Escherichia coli K12. FEMS Microbiol. Lett. 44:53-57.
41. Higuchi K, Smith JL. 1961. Studies on the nutrition and physiology of Pasteurella pestis. VI. A differential plating medium for the estimation of the mutation rate to avirulence. J. Bacteriol. 81:605-608.
42. Holmes K, et al. 2005. Campylobacter jejuni gene expression in response to iron limitation and the role of Fur. Microbiology 151:243-257.
43. Janakiraman A, Slauch JM. 2000. The putative iron transport system SitABCD encoded on SPI1 is required for full virulence of Salmonella typhimurium. Mol. Microbiol. 35:1146 -1155.
44. Janvier B, et al. 1998. Characterization and gene sequencing of a 19-kDa periplasmic protein of Campylobacter jejuni/coli. Res. Microbiol. 149:95-107.
45. Jeon J, et al. 2008. RstA-promoted expression of the ferrous iron transporter FeoB under iron-replete conditions enhances Fur activity in Salmonella enterica. J. Bacteriol. 190:7326 -7334.
46. Kammler M, Schön C, Hantke K. 1993. Characterization of the ferrous iron uptake system of Escherichia coli. J. Bacteriol. 175:6212-6219.
47. Kaniga K, Delor I, Cornelis GR. 1991. A wide-host-range suicide vector for improving reverse genetics in Gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica. Gene 109:137-141.
48. 2+ transporter of Salmonella enterica serovar Typhimurium. J. Bacteriol. 184:3159 -3166.
49. Kirillina O, Bobrov AG, Fetherston JD, Perry RD. 2006. A hierarchy of iron uptake systems: Yfu and Yiu are functional in Yersinia pestis. Infect. Immun. 74:6171-6178.
50. Koch D, et al. 2011. Characterization of a dipartite iron uptake system from uropathogenic Escherichia coli strain F11. J. Biol. Chem. 286:25317-25330.
51. Lamont I, Konings A, Reid D. 2009. Iron acquisition by Pseudomonas aeruginosa in the lungs of patients with cystic fibrosis. Biometals 22:53-60.
52. Lathem WW, Price PA, Miller VL, Goldman WE. 2007. A plasminogenactivating protease specifically controls the development of primary pneumonic plague. Science 315:509 -513.
53. Lesic B, Carniel E. 2004. The high pathogenicity island: a broad-hostrange pathogenicity island, p 285-306.
54. Carniel E, Hinnebusch BJ (ed), Yersinia molecular and cellular biology Horizon Bioscience, Norfolk, United Kingdom.
55. Lukaszewski RA, et al. 2005. Pathogenesis of Yersinia pestis infection in BALB/c mice: effects on host macrophages and neutrophils. Infect. Immun. 73:7142-7150.
56. Marchler-Bauer A, et al. 2011. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 39:D225-D229.
57. Miller JH. 1992. A short course in bacterial genetics. A laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
58. Naikare H, Palyada K, Panciera R, Marlow D, Stintzi A. 2006. Major role for FeoB in Campylobacter jejuni ferrous iron acquisition, gut colonization, and intracellular survival. Infect. Immun. 74:5433-5444.
59. Paik S, Brown A, Munro CL, Cornelissen CN, Kitten T. 2003. The sloABCR operon of Streptococcus mutans encodes an Mn and Fe transport system required for endocarditis virulence and its Mn-dependent repressor.J. Bacteriol. 185:5967-5975.
60. Palyada K, Threadgill D, Stintzi A. 2004. Iron acquisition and regulation in Campylobacter jejuni. J. Bacteriol. 186:4714-4729.
61. Parkhill J, et al. 2001. Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413:523-527.
62. Perry RD, et al. 2003. Regulation of the Yersinia pestis Yfe and Ybt iron transport systems. Adv. Exp. Med. Biol. 529:275-283.
63. Perry RD, Balbo PB, Jones HA, Fetherston JD, DeMoll E. 1999. Yersiniabactin from Yersinia pestis: biochemical characterization of the siderophore and its role in iron transport and regulation. Microbiology 145:1181-1190.
64. Perry RD, et al. 2012. Yersinia pestis transition metal divalent cation transporters. Adv. Exp. Med. Biol. 954:267-279.
65. +) phenotype of Yersinia pestis is posttranscriptional. J. Bacteriol.186:1638 -1647.
66. Perry RD, Fetherston JD. 2004. Iron and heme uptake systems, p 257-283.
67. Carniel E, Hinnebusch BJ (ed), Yersinia: molecular and cellular biology. Horizon Bioscience, Norfolk, United Kingdom.
68. Perry RD, Mier I, Jr, Fetherston JD. 2007. Roles of the Yfe and Feo transporters of Yersinia pestis in iron uptake and intracellular growth.Biometals 20:699 -703.
69. Perry RD, Shah J, Bearden SW, Thompson JM, Fetherston JD. 2003.Yersinia pestis TonB: role in iron, heme, and hemoprotein utilization. Infect. Immun. 71:4159-4162.
70. Price PA, Jin J, Goldman WE. 2012. Pulmonary infection by Yersinia pestis rapidly establishes a permissive environment for microbial proliferation.Proc. Natl. Acad. Sci. U. S. A. 109:3083-3088.
71. Pujol C, Bliska JB. 2005. Turning Yersinia pathogenesis outside in: subversion of macrophage function by intracellular yersiniae. Clin. Immunol.114:216 -226.
72. Reed LJ, Muench H. 1938. A simple method for estimating fifty percent endpoints. Am. J. Hyg. 27:493-497.
73. Robey M, Cianciotto NP. 2002. Legionella pneumophila feoAB promotes ferrous iron uptake and intracellular infection. Infect. Immun. 70:5659-5669.
74. Runyen-Janecky LJ, Payne SM. 2002. Identification of chromosomal Shigella flexneri genes induced by the eukaryotic intracellular environment.Infect. Immun. 70:4379-4388.
75. Runyen-Janecky LJ, Reeves SA, Gonzales EG, Payne SM. 2003. Contribution of the Shigella flexneri Sit, Iuc, and Feo iron acquisition systems to iron acquisition in vitro and in cultured cells. Infect. Immun. 71:1919-1928.
76. Sabri M, et al. 2008. Contribution of the SitABCD, MntH, and FeoB metal transporters to the virulence of avian pathogenic Escherichia coli O78 strain 7122. Infect. Immun. 76:601-611.
77. Sikkema DJ, Brubaker RR. 1987. Resistance to pesticin, storage of iron, and invasion of HeLa cells by yersiniae. Infect. Immun. 55:572-578.
78. Staggs TM, Perry RD. 1991. Identification and cloning of a fur regulatory gene in Yersinia pestis. J. Bacteriol. 173:417-425.
79. Stojiljkovic I, Cobeljic M, Hantke K. 1993. Escherichia coli K-12 ferrous iron uptake mutants are impaired in their ability to colonize the mouse intestine. FEMS Microbiol. Lett. 108:111-116.
80. Storz G, Zheng M. 2000. Oxidative stress, p 47-59.
81. Storz G, Hengge-Aronis R (ed), Bacterial stress responses. ASM Press, Washington, DC.
82. Straley SC, Harmon PA. 1984. Yersinia pestis grows within phagolysosomes in mouse peritoneal macrophages. Infect. Immun. 45:655-659.
83. Su YC, et al. 2010. Structure of Stenotrophomonas maltophilia FeoA complexed with zinc: a unique prokaryotic SH3-domain protein that possibly acts as a bacterial ferrous iron-transport activating factor. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 66:636-642.
84. Surgalla MJ, Beesley ED. 1969. Congo red-agar plating medium for detecting pigmentation in Pasteurella pestis. Appl. Microbiol. 18:834-837.
85. Suzuki T, Okamura Y, Calugay RJ, Takeyama H, Matsunaga T. 2006. Global gene expression analysis of iron-inducible genes in Magnetospirillum magneticum AMB-1. J. Bacteriol. 188:2275-2279.
86. Thompson JM, Jones HA, Perry RD. 1999. Molecular characterization of the hemin uptake locus (hmu) from Yersinia pestis and analysis of hmu mutants for hemin and hemoprotein utilization. Infect. Immun. 67:3879-3892.
87. Tsolis RM, Báumler AJ, Heffron F, Stojiljkovic I. 1996. Contribution of TonB-and Feo-mediated iron uptake to growth of Salmonella typhimurium in the mouse. Infect. Immun. 64:4549-4556.
88. - or Pstr phenotypes of yersiniae. Infect. Immun. 43:895-900.
89. van Vliet AHM, Wooldridge KG, Ketley JM. 1998. Iron-responsive gene regulation in a Campylobacter jejuni fur mutant. J. Bacteriol. 180:5291-5298.
90. Velayudhan J, et al. 2000. Iron acquisition and virulence in Helicobacter pylori: a major role for FeoB, a high-affinity ferrous iron transporter. Mol.Microbiol. 37:274 -286.
91. Wang RF, Kushner SR. 1991. Construction of versatile low-copynumber vectors for cloning, sequencing and gene expression in Escherichia
92. Wyckoff EE, Mey AR, Leimbach A, Fisher CF, Payne SM. 2006. Characterization of ferric and ferrous iron transport systems in Vibrio cholerae. J. Bacteriol. 188:6515-6523.
93. Zaharik ML, et al. 2004. The Salmonella enterica serovar Typhimurium divalent cation transport systems MntH and SitABCD are essential for virulence in an Nramp1G169 murine typhoid model. Infect. Immun. 72:5522-5525.
94. Zhou D, Hardt W-D, Galán JE. 1999. Salmonella typhimurium encodes a putative iron transport system within the centisome 63 pathogenicity island.Infect. Immun. 67:1974 -1981.