Yersiniabactin iron uptake: Mechanisms and role in Yersinia pestis pathogenesis

Microbes and Infection

Volumn 13, Issue 10, 2011, Pages 808-817

  Perry, Robert D ^a   Fetherston, Jacqueline D ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Iron transport; Plague; Siderophore; Yersinia pestis; Yersiniabactin

Indexed keywords

FERRIC UPTAKE REGULATOR; IRON; UNCLASSIFIED DRUG; YERSINIABACTIN; YERSINIABACTIN A;

BACTERIAL GENE; BACTERIAL VIRULENCE; BIOSYNTHESIS; BUBONIC PLAGUE; CITROBACTER; ENTEROBACTER; ESCHERICHIA COLI; EXPERIMENTAL MODEL; GENE LOCUS; GENETIC REGULATION; GENETIC TRANSCRIPTION; HUMAN; IRON TRANSPORT; KLEBSIELLA; NONHUMAN; PATHOGENESIS; PHOTORHABDUS; PLAGUE; PNEUMONIC PLAGUE; PRIORITY JOURNAL; PROTEIN SECRETION; SALMONELLA; SEPTICEMIC PLAGUE; SERRATIA; SHORT SURVEY; YERSINIA PESTIS;

GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; IRON; PHENOLS; PLAGUE; THIAZOLES; VIRULENCE FACTORS; YERSINIA PESTIS;

YERSINIA PESTIS;

EID: 79960837602     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2011.04.008     Document Type: Short Survey

References (69)

1. Eisen R.J., Gage K.L. Adaptive strategies of Yersinia pestis to persist during inter-epizootic and epizootic periods. Vet. Res. 2009, 40:01.
2. Perry R.D., Fetherston J.D. Yersinia pestis - etiologic agent of plague. Clin. Microbiol. Rev. 1997, 10:35-66.
3. Hinnebusch B.J., Erickson D.L. Yersinia pestis biofilm in the flea vector and its role in the transmission of plague. Curr. Top. Microbiol. Immunol. 2008, 322:229-248.
4. Inglesby T.V., Dennis D.T., Henderson D.A., Bartlett J.G., Ascher M.S., Eitzen E., Fine A.D., Friedlander A.M., Hauer J., Koerner J.F., Layton M., McDade J., Osterholm M.T., O'Toole T., Parker G., Perl T.M., Russell P.K., Schoch-Spana M., Tonat K. Plague as a biological weapon: medical and public health management. J. Amer. Med. Assoc. 2000, 283:2281-2290.
5. Anisimov A.P., Lindler L.E., Pier G.B. Intraspecific diversity of Yersinia pestis. Clin. Microbiol. Rev. 2004, 17:434-464.
6. Zhou D., Tong Z., Song Y., Han Y., Pei D., Pang X., Zhai J., Li M., Cui B., Qi Z., Jin L., Dai R., Du Z., Wang J., Guo Z., Wang J., Huang P., Yang R. Genetics of metabolic variations between Yersinia pestis biovars and the proposal of a new biovar, microtus. J. Bacteriol. 2004, 186:5147-5152.
7. Jackson S., Burrows T.W. The virulence-enhancing effect of iron on non-pigmented mutants of virulent strains of Pasteurella pestis. Br. J. Exp. Pathol. 1956, 37:577-583.
8. Wake A., Misawa M., Matsui A. Siderochrome production by Yersinia pestis and its relation to virulence. Infect. Immun. 1975, 12:1211-1213.
9. Brubaker R.R., Surgalla M.J. Pesticins. I. Pesticin-bacterium interrelationships and environmental factors influencing activity. J. Bacteriol. 1961, 82:940-949.
10. Brubaker R.R. Mutation rate to nonpigmentation in Pasteurella pestis. J. Bacteriol. 1969, 98:1404-1406.
11. Fetherston J.D., Lillard J.W., Perry R.D. Analysis of the pesticin receptor from Yersinia pestis: role in iron-deficient growth and possible regulation by its siderophore. J. Bacteriol. 1995, 177:1824-1833.
12. Kutyrev V.V., Filippov A.A., Oparina O.S., Protsenko O.A. Analysis of Yersinia pestis chromosomal determinants Pgm+ and Psts associated with virulence. Microb. Pathog. 1992, 12:177-186.
13. Rakin A., Saken E., Harmsen D., Heesemann J. The pesticin receptor of Yersinia enterocolitica: a novel virulence factor with dual function. Mol. Microbiol. 1994, 13:253-263.
14. Heesemann J., Hantke K., Vocke T., Saken E., Rakin A., Stojiljkovic I., Berner R. Virulence of Yersinia enterocolitica is closely associated with siderophore production, expression of an iron-repressible outer membrane polypeptide of 65 000 Da and pesticin sensitivity. Mol. Microbiol. 1993, 8:397-408.
15. Heesemann J. Chromosomal-encoded siderophores are required for mouse virulence of enteropathogenic Yersinia species. FEMS Microbiol. Lett. 1987, 48:229-233.
16. Haag H., Hantke K., Drechsel H., Stojiljkovic I., Jung G., Zähner H. Purification of yersiniabactin: a siderophore and possible virulence factor of Yersinia enterocolitica. J. Gen. Microbiol. 1993, 139:2159-2165.
17. Chambers C.E., McIntyre D.D., Mouck M., Sokol P.A. Physical and structural characterization of yersiniophore, a siderophore produced by clinical isolates of Yersinia enterocolitica. Biometals 1996, 9:157-167.
18. Drechsel H., Stephan H., Lotz R., Haag H., Zähner H., Hantke K., Jung G. Structure elucidation of yersiniabactin, a siderophore from highly virulent Yersinia strains. Liebigs Ann. 1995, 1995:1727-1733.
19. Perry R.D., Balbo P.B., Jones H.A., Fetherston J.D., DeMoll E. Yersiniabactin from Yersinia pestis: biochemical characterization of the siderophore and its role in iron transport and regulation. Microbiology 1999, 145:1181-1190.
20. Carniel E., Mazigh D.D., Mollaret H.H.H.H. Expression of iron-regulated proteins in Yersinia species and their relation to virulence. Infect. Immun. 1987, 55:277-280.
21. Carniel E., Mercereau-Puijalon O., Bonnefoy S. The gene coding for the 190,000-dalton iron-regulated protein of Yersinia species is present only in the highly pathogenic strains. Infect. Immun 1989, 57:1211-1217.
22. Bearden S.W., Fetherston J.D., Perry R.D. Genetic organization of the yersiniabactin biosynthetic region and construction of avirulent mutants in Yersinia pestis. Infect. Immun. 1997, 65:1659-1668.
23. Gehring A.M., DeMoll E., Fetherston J.D., Mori I., Mayhew G.F., Blattner F.R., Walsh C.T., Perry R.D. Iron acquisition in plague: modular logic in enzymatic biogenesis of yersiniabactin by Yersinia pestis. Chem. Biol. 1998, 5:573-586.
24. Walsh C.T., Marshall C.G. Iron Transport in Bacteria 2004, 18-37. ASM Press, Washington, D.C. J.H. Crosa, A.R. Mey, S.M. Payne (Eds.).
25. Bobrov A.G., Geoffroy V.A., Perry R.D. Yersiniabactin production requires the thioesterase domain of HMWP2 and YbtD, a putative phosphopantetheinylate transferase. Infect. Immun. 2002, 70:4204-4214.
26. Gehring A.M., Mori I., Perry R.D., Walsh C.T. The nonribosomal peptide synthetase HMWP2 forms a thiazoline ring during biogenesis of yersiniabactin, an iron-chelating virulence factor of Yersinia pestis. Biochemistry 1998, 37:11637-11650.
27. Geoffroy V.A., Fetherston J.D., Perry R.D. Yersinia pestis YbtU and YbtT are involved in synthesis of the siderophore yersiniabactin but have different effects on regulation. Infect. Immun. 2000, 68:4452-4461.
28. Guilvout I., Mercereau-Puijalon O., Bonnefoy S., Pugsley A.P., Carniel E. High-molecular-weight protein 2 of Yersinia enterocolitica is homologous to AngR of Vibrio anguillarum and belongs to a family of proteins involved in nonribosomal peptide synthesis. J. Bacteriol. 1993, 175:5488-5504.
29. McLoughlin S.M., Kelleher N.L. Monitoring multiple active sites on thiotemplate enzymes in parallel: a molecular movie of yersiniabactin bioassembly. J. Am. Chem. Soc. 2005, 127:14984-14985.
30. Miller D.A., Luo L., Hillson N., Keating T.A., Walsh C.T. Yersiniabactin synthetase: a four-protein assembly line producing the nonribosomal peptide/polyketide hybrid siderophore of Yersinia pestis. Chem. Biol. 2002, 9:333-449.
31. Miller M.C., Fetherston J.D., Pickett C.L., Bobrov A.G., Weaver R.H., DeMoll E., Perry R.D. Reduced synthesis of the Ybt siderophore or production of aberrant Ybt-like molecules activates transcription of yersiniabactin genes in Yersinia pestis. Microbiology 2010, 156:2226-2238.
32. Pfeifer B.A., Wang C.C.C., Walsh C.T., Khosla C. Biosynthesis of yersiniabactin, a complex polyketide-nonribosomal peptide, using Escherichia coli as a heterologous host. Appl. Environ. Microbiol. 2003, 69:6698-6702.
33. Miller M.C., Parkin S., Fetherston J.D., Perry R.D., DeMoll E. Crystal structure of ferric-yersiniabactin, a virulence factor of Yersinia pestis. J. Inorg. Biochem. 2006, 100:1495-1500.
34. Furrer J.L., Sanders D.N., Hook-Barnard I.G., McIntosh M.A. Export of the siderophore enterobactin in Escherichia coli: involvement of a 43 kDa membrane exporter. Mol. Microbiol. 2002, 44:1225-1234.
35. Brickman T.J., Armstrong S.K. Bordetella AlcS transporter functions in alcaligin siderophore export and is central to inducer sensing in positive regulation of alcaligin system gene expression. J. Bacteriol. 2005, 187:3650-3661.
36. Ó Cuív P., Clarke P., Lynch D., O'Connell M. Identification of rhtX and fptX, novel genes encoding proteins that show homology and function in the utilization of the siderophores rhizobactin 1021 by Sinorhizobium meliloti and pyochelin by Pseudomonas aeruginosa, respectively. J. Bacteriol. 2004, 186:2996-3005.
37. Michel L., Bachelard A., Reimmann C. Ferripyochelin uptake genes are involved in pyochelin-mediated signalling in Pseudomonas aeruginosa. Microbiology 2007, 153:1508-1518.
38. Fetherston J.D., Bertolino V.J., Perry R.D. YbtP and YbtQ: two ABC transporters required for iron uptake in Yersinia pestis. Mol. Microbiol. 1999, 32:289-299.
39. Ferber D.M., Fowler J.M., Brubaker R.R. Mutations to tolerance and resistance to pesticin and colicins in Escherichia coli. J. Bacteriol. 1981, 146:506-511.
40. Fetherston J.D., Perry R.D. The pigmentation locus of Yersinia pestis KIM6+ is flanked by an insertion sequence and includes the structural genes for pesticin sensitivity and HMWP2. Mol. Microbiol. 1994, 13:697-708.
41. Perry R.D., Shah J., Bearden S.W., Thompson J.M., Fetherston J.D. Yersinia pestis TonB: role in iron, heme and hemoprotein utilization. Infect. Immun. 2003, 71:4159-4162.
42. Fetherston J.D., Kirillina O., Bobrov A.G., Paulley J.T., Perry R.D. The yersiniabactin transport system is critical for the pathogenesis of bubonic and pneumonic plague. Infect. Immun 2010, 70:2045-2052.
43. Buchanan S.K. Type I secretion and multidrug efflux: transport through the TolC channel-tunnel. Trends Biochem. Sci. 2001, 28:3-6.
44. Deng W., Burland V., Plunkett G., Boutin A., Mayhew G.F., Liss P., Perna N.T., Rose D.J., Mau B., Zhou S., Schwartz D.C., Fetherston J.D., Lindler L.E., Brubaker R.R., Plano G.V., Straley S.C., McDonough K.A., Nilles M.L., Matson J.S., Blattner F.R., Perry R.D. Genome sequence of Yersinia pestis KIM. J. Bacteriol. 2002, 184:4601-4611.
45. Brem D., Pelludat C., Rakin A., Jacobi C.A., Heesemann J. Functional analysis of yersiniabactin transport genes of Yersinia enterocolitica. Microbiology 2001, 147:1115-1127.
46. Lesic B., Carniel E. Yersinia Molecular and Cellular Biology 2004, 285-306. Horizon Bioscience, Norfolk, UK. E. Carniel, B.J. Hinnebusch (Eds.).
47. Lesic B., Bach S., Ghigo J.-M., Dobrindt U., Hacker J., Carniel E. Excision of the high-pathogenicity island of Yersinia pseudotuberculosis requires the combined actions of its cognate integrase and Hef, a new recombination directionality factor. Mol. Microbiol. 2004, 52:1337-1348.
48. Lesic B., Carniel E. Horizontal transfer of the high-pathogenicity island of Yersinia pseudotuberculosis. J. Bacteriol. 2005, 187:3352-3358.
49. Bultreys A., Gheysen I., de Hoffmann E. Yersiniabactin production by Pseudomonas syringae and Escherichia coli, and description of a second yersiniabactin locus evolutionary group. Appl. Environ. Microbiol. 2006, 72:3814-3825.
50. Gao H., Zhou D., Li Y., Guo Z., Han Y., Song Y., Zhai J., Du Z., Wang X., Lu J., Yang R. The iron-responsive Fur regulon in Yersinia pestis. J. Bacteriol. 2008, 190:3063-3075.
51. Perry R.D., Fetherston J.D. Yersinia Molecular and Cellular Biology 2004, 257-283. Horizon Bioscience, Norfolk, U.K. E. Carniel, B.J. Hinnebusch (Eds.).
52. Staggs T.M., Perry R.D. Fur regulation in Yersinia species. Mol. Microbiol. 1992, 6:2507-2515.
53. Fetherston J.D., Bearden S.W., Perry R.D. YbtA, an AraC-type regulator of the Yersinia pestis pesticin/yersiniabactin receptor. Mol. Microbiol. 1996, 22:315-325.
54. Perry R.D., Abney J., Mier I., Lee Y., Bearden S.W., Fetherston J.D. Regulation of the Yersinia pestis Yfe and Ybt iron transport systems. Adv. Exp. Med. Biol. 2003, 529:275-283.
55. Braun V., Braun M., Killmann H. Iron Transport in Bacteria 2004, 158-177. ASM Press, Washington D.C. J.H. Crosa, A.R. Mey, S.M. Payne (Eds.).
56. Poole K. Iron Transport in Bacteria 2004, 293-310. ASM Press, Washington, D.C. J.H. Crosa, A.R. Mey, S.M. Payne (Eds.).
57. Anisimov R., Brem D., Heesemann J., Rakin A. Molecular mechanism of YbtA-mediated transcriptional regulation of divergent overlapping promoters ybtA and irp6 of Yersinia enterocolitica. FEMS Microbiol. Lett. 2005, 250:27-32.
58. Anisimov R., Brem D., Heesemann J., Rakin A. Transcriptional regulation of high pathogenicity island iron uptake genes by YbtA. Int. J. Med. Microbiol. 2005, 295:19-28.
59. Pelludat C., Rakin A., Jacobi C.A., Schubert S., Heesemann J. The yersiniabactin biosynthetic gene cluster of Yersinia enterocolitica: organization and siderophore-dependent regulation. J. Bacteriol. 1998, 180:538-546.
60. Chauvaux S., Rosso M.-L., Frangeul L., Lacroix C., Labarre L., Schiavo A., Marceau M., Dillies M.-A., Foulon J., Coppée J.-Y., Médigue C., Simonet M., Carniel E. Transcriptome analysis of Yersinia pestis in human plasma: an approach for discovering bacterial genes involved in septicaemic plague. Microbiology 2007, 153:3112-3124.
61. Une T., Brubaker R.R. In vivo comparison of avirulent Vwa- and Pgm- or Pstr phenotypes of yersiniae. Infect. Immun. 1984, 43:895-900.
62. Buchrieser C., Prentice M., Carniel E. The 102-kilobase unstable region of Yersinia pestis comprises a high-pathogenicity island linked to a pigmentation segment which undergoes internal rearrangement. J. Bacteriol. 1998, 180:2321-2329.
63. Fetherston J.D., Schuetze P., Perry R.D. 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. 1992, 6:2693-2704.
64. Sebbane F., Jarrett C., Gardner D., Long D., Hinnebusch B.J. Role of the Yersinia pestis yersiniabactin iron acquisition system in the incidence of flea-borne plague. PLoS ONE 2010, 5:e14379.
65. Sebbane F., Lemaître N., Sturdevant D.E., Rebeil R., Virtaneva K., Porcella S.F., Hinnebusch B.J. Adaptive response of Yersinia pestis to extracellular effectors of innate immunity during bubonic plague. Proc. Natl. Acad. Sci. USA 2006, 103:11766-11771.
66. Jacobi C.A., Gregor S., Rakin A., Heesemann J. Expression analysis of the yersiniabactin receptor gene fyuA and the heme receptor hemR of Yersinia enterocolitica in vitro and in vivo using the reporter genes for green fluorescent protein and luciferase. Infect. Immun. 2001, 69:7772-7782.
67. Lee-Lewis H., Anderson D.M. Absence of inflammation and pneumonia during infection with nonpigmented Yersinia pestis reveals a new role for the pgm locus in pathogenesis. Infect. Immun. 2009, 78:220-230.
68. Cellier M.F., Courville P., Campion C. Nramp1 phagocyte intracellular metal withdrawal defense. Microbes Infect. 2007, 9:1662-1670.
69. Michel L., González N., Jagdeep S., Nguyen-Ngoc T., Reimmann C. PchR-box recognition by the AraC-type regulator PchR of Pseudomonas aeruginosa requires the siderophore pyochelin as an effector. Mol. Microbiol. 2005, 58:495-509.