Importance of the Ornibactin and Pyochelin Siderophore Transport Systems in Burkholderia cenocepacia Lung Infections

Infection and Immunity

Volumn 72, Issue 5, 2004, Pages 2850-2857

  Visser, M B ^a   Majumdar, S ^a   Hani, E ^a   Sokol, P A ^a  

^a Health Sciences Centre Calgary   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FERRIC ORNIBACTIN; FERRIC PYOCHELIN; IRON; SIDEROPHORE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENE; BACTERIAL OUTER MEMBRANE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BURKHOLDERIA CEPACIA; CONTROLLED STUDY; FPTA GENE; GENE FUNCTION; GENE IDENTIFICATION; IRON TRANSPORT; LUNG INFECTION; NONHUMAN; ORBA GENE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT;

ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; BURKHOLDERIA CEPACIA COMPLEX; BURKHOLDERIA INFECTIONS; GENES, BACTERIAL; IRON; LUNG DISEASES; MALE; MUTATION; OLIGOPEPTIDES; PHENOLS; RATS; RATS, SPRAGUE-DAWLEY; SIDEROPHORES; THIAZOLES; VIRULENCE;

EID: 2142643700     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.72.5.2850-2857.2004     Document Type: Article

References (72)

1. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Ankenhauer, R. G. 1992. Cloning of the outer membrane high-affinity Fe(III)-pyochelin receptor of Pseudomonas aeruginosa. J. Bacteriol. 174:4401-4409.
3. Ankenbauer, R. G., and C. D. Cox. 1988. Isolation and characterization of Pseudomonas aeruginosa mutants requiring salicylic acid for pyochelin biosynthesis. J. Bacteriol. 170:5364-5367.
4. Ankenbauer, R. G., and H. N. Quan. 1994. FptA, the Fe(III)-pyochelin receptor of Pseudomonas aeruginosa: a phenolate siderophore receptor homologous to hydroxamate siderophore receptors. J. Bacteriol. 176:307-319.
5. Ausubel, F. M., R. Breut, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1989. Current protocols in molecular biology, vol. 1. John Wiley & Sons. Inc., New York, N.Y.
6. Bitter, W., J. D. Marugg, L. A. de Weger, J. Tommassen, and P. J. Weisheek. 1991. The ferric-pseudobactin receptor PupA of Pseudomonas putida WCS358: homology to TonB-dependent Escherichia coli receptors and specificity of the protein. Mol. Microbiol. 5:647-655.
7. Brickman, T. J., and S. K. Armstrong. 1999. Essential role of the iron-regulated outer membrane receptor FauA in alcaligin siderophore-mediated iron uptake in Bordetella species. J. Bacteriol. 181:5958-5966.
8. Brickman, T. J., and S. K. Armstrong. 1996. The ornithine decarboxylase gene odc is required for alcaligin siderophore biosynthesis in Bordetella spp.: putrescine is a precursor of alcaligin. J. Bacteriol. 178:54-60.
9. Britigan, B. E., G. T. Rasmussen, and C. D. Cox. 1997. Augmentation of oxidant injury to human pulmonary epithelial cells by the Pseudomonas aeruginosa siderophore pyochelin. Infect. Immun. 65:1071-1076.
10. Cash, H. A., D. E. Woods, B. McCullough, W. G. Johanson, Jr., and J. A. Bass. 1979. A rat model of chronic respiratory infection with Pseudomonas aeruginosa. Am. Rev. Respir. Dis. 119:453-459.
11. Chambers, C. E., D. D. McIntyre, M. Mouck, and P. A. Sokol. 1996. Physical and structural characterization of yersiniophore, a siderophore produced by clinical isolates of Yersinia enterocolitica. Biometals 9:157-167.
12. Chipperfield, J. R., and C. Ratledge. 2000. Salicylic acid is not a bacterial siderophore: a theoretical study. Biometals 13:165-168.
13. Coenye, T., and P. Vandamme. 2003. Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ. Microbiol. 5:719-729.
14. Coenye, T., P. Vandamme, J. R. Govan, and J. J. LiPuma. 2001. Taxonomy and identification of the Burkholderia cepacia complex. J. Clin. Microbiol. 39:3427-3436.
15. Coffman, T. J., C. D. Cox, B. L. Edeker, and B. E. Britigan. 1990. Possible role of bacterial siderophores in inflammation. Iron bound to the Pseudomonas siderophore pyochelin can function as a hydroxyl radical catalyst. J. Clin. Investig. 86:1030-1037.
16. Cox, C. D., and R. Graham. 1979. Isolation of an iron-binding compound from Pseudomonas aeruginosa. J. Bacteriol. 137:357-364.
17. Crosa, J. H. 1989. Genetics and molecular biology of siderophore-mediated iron transport in bacteria. Microbiol. Rev. 53:517-530.
18. Cunliffe, H. E., T. R. Merriman, and I. L. Lamont. 1995. Cloning and characterization of pvdS, a gene required for pyoverdine synthesis in Pseudomonas aeruginosa: PvdS is probably is alternative sigma factor. J. Bacteriol. 177:2744-2750.
19. Darling, P., M. Chan, A. D. Cox, and P. A. Sokol. 1998. Siderophore production by cystic fibrosis isolates of Burkholderia cepacia. Infect. Immun. 66:874-877.
20. DeShazer, D., and D. E. Woods. 1996. Broad-host-range cloning and cassette vectors based on the R388 trimethoprim resistance gene. BioTechniques 20:762-764.
21. De Voss, J. J., K. Rutter, B. G. Schroeder, H. Su, Y. Zhu, and C. E. Barry III. 2000. The salicylate-derived mycobactin siderophores of Mycobacterium tuberculosis are essential for growth in macrophages. Proc. Natl. Acad. Sci. USA 97:1252-1257.
22. Drechsel, H., H. Stpban, R. Lotz, H. Hagg, H. Zanner, K. Hankte, and G. Jung. 1995. Structure elucidation of yersiniabactin, a siderophore from highly virulent Yersinia strains. Liebigs Ann. 1727-1733.
23. Figurski, D. H., and D. R. Helenski. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. USA 76:1648-1652.
24. Gensberg, K., K. Hughes, and A. W. Smith. 1992. Siderophore-specific induction of iron uptake in Pseudomonas aeruginosa. J. Gen. Microbiol. 138:2381-2387.
25. Govan, J. R., and V. Deretic. 1996. Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol. Rev. 60:539-574.
26. Govan, J. R., J. E. Hughes, and P. Vandamme. 1996. Burkholderia cepacia: medical, taxonomic and ecological issues. J. Med. Microbiol. 45:395-407.
27. Guerinot, M. L. 1994. Microbial iron transport. Annu. Rev. Microbiol. 48:743-772.
28. Heinrichs, D. E., and K. Poole. 1993. Cloning and sequence analysis of a gene (pchR) encoding an AraC family activator of pyochelin and ferripyochelin receptor synthesis in Pseudomonas aeruginosa. J. Bacteriol. 175:5882-5889.
29. Heinrichs, D. E., and K. Poole. 1996. PchR, a regulator of ferripyochelin receptor gene (fptA) expression in Pseudomonas aeruginosa, functions both as an activator and as a repressor. J. Bacteriol. 178:2586-2592.
30. Henry, D. A., M. E. Campbell, J. J. LiPuma, and D. P. Speert. 1997. Identification of Burkholderia cepacia isolates from patients with cystic fibrosis and use of a simple new selective medium. J. Clin. Microbiol. Clin. Microbiol. 35:614-619.
31. Hoang, T. T., R. R. Karkhoff-Schweizer, A. J. Kutehma, and H. P. Schweizer. 1998. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77-86.
32. Koster, M., J. van de Vossenberg, J. Leong, and P. J. Weisbeek. 1993. Identification and characterization of the pupB gene encoding an inducible ferric-pseudobactin receptor of Pseudomonas putida WCS358. Mol. Microbiol. 8:591-601.
33. Koster, M., W. van Klompenburg, W. Bitter, J. Leong, and P. Weisbeek. 1994. Role for the outer membrane ferric siderophore receptor PupB in signal transduction across the bacterial cell envelope. EMBO J. 13:2805-2813.
34. Leoni, L., N. Orsi, V. de Lorenzo, and P. Visca. 2000. Functional analysis of PvdS, an iron starvation sigma factor of Pseudomonas aeruginosa. J. Bacteriol. 182:1481-1491.
35. Lewenza, S., B. Conway, E. P. Greenberg, and P. A. Sokol. 1999. Quorum sensing in Burkholderia cepacia: identification of the LuxRI homologs CepRI. J. Bacteriol. 181:748-756.
36. Lewenza, S., and P. A. Sokol. 2001. Regulation of ornibactin synthesis and N-acyl-L-homoserine lactone production by CepR in Burkholderia cepacia. J. Bacteriol. 183:2212-2218.
37. Madden, T. L., R. L. Tatusov, and J. Zhang. 1996. Applications of network BLAST server. Methods Enzymol. 266:131-141.
38. Mahenthiralingam, E., A. Baldwin, and P. Vandamme. 2002. Burkholderia cepacia complex infection in patients with cystic fibrosis. J. Med. Microbiol. 51:533-538.
39. Mahenthiralingam, E., T. Coenye, J. W. Chung, D. P. Speert, J. R. Govan, P. Taylor, and P. Vandamme. 2000. Diagnostically and experimentally useful panel of strains from the Burgholderia cepacia complex. J. Clin. Microbiol. 38:910-913.
40. McKevitt, A. I., S. Bajaksouzian, J. D. Klinger, and D. E. Woods. 1989. Purification and characterization of an extracellular protease from Pseudomonas cepacia. Infect. Immun. 57:771-778.
41. Meyer, J. M., P. Azelvandre, and C. Georges. 1992. Iron metabolism in Pseudomonas: salicylic acid, a siderophore of Pseudomonas fluorescens CHAO. Biofactors 4:23-27.
42. Meyer, J. M., D. Hohnadel, and F. Halle. 1989. Cepabactin from Pseudomonas cepacia, a new type of siderophore. J. Gen. Microbiol. 135:1479-1487.
43. Meyer, J. M., V. T. Van, A. Stintzi, O. Berge, and G. Winkelmann. 1995. Ornibactin production and transport properties in strains of Burkholderia vietnamiensis and Burkholderia cepacia (formerly Pseudomonas cepacia). Biometals 8:309-317.
44. Meyer, J. M., and M. A. Abdullah. 1978. The fluorescent pigment of Pseudomonas fluorescens: biosynthesis, purification and physico-chemical properties. J. Gen. Microbiol. 107:319-328.
45. Mietzner, T. A., and S. A. Morse. 1994. The role of iron-binding proteins in the survival of pathogenic bacteria. Annu. Rev. Nutr. 14:471-493.
46. Neilands, J. B. 1995. Siderophores: structure and function of microbial iron transport compounds. J. Biol. Chem. 270:26723-26726.
47. Nielsen, H., J. Engelhrecht, 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.
48. Ohman, D. E., J. C. Sadoff, and B. H. Iglewski. 1980. Toxin A-deficient mutants of Pseudomonas aeruginosa PA103: isolation and characterization. Infect. Immun. 28:899-908.
49. Okujo, N., M. Saito, S. Yamamoto, T. Yoshida, S. Miyoshi, and S. Shinoda. 1994. Structure of vulnibactin, new polyamine-containing siderophore from Vibrio vulnificus. Biometals 7:109-116.
50. Poole, K., S. Neshat, K. Krebes, and D. E. Heinrichs. 1993. Cloning and nucleotide sequence analysis of the ferripyoverdine receptor gene fpvA of Pseudomonas aeruginosa. J. Bacteriol. 175:4597-4604.
51. Ratledge, C., and F. G. Winder. 1962. The accumulation of salicylic acid by Mycobacteria during growth on an iron-deficient medium. Biochem. J. 84:501-506.
52. Ratledge, C., and M. J. Hall. 1970. Uptake of salicylic acid into mycobactin S by growing cells of Mycobacterium smegmatis. FEBS Lett. 10:309-312.
53. Ratledge, C., L. P. Macham, K. A. Brown, and B. J. Marshall. 1974. Iron transport in Mycobacterium smegmatis: a restricted role for salicylic acid in the extracellular environment. Biochim. Biophys. Acta 372:39-51.
54. Reimmann, C., H. M. Patel, L. Serino, M. Barone, C. T. Walsh, and D. Haas. 2001. Essential pchG-dependent reduction in pyochelin biosynthesis of Pseudomonas aeruginosa. J. Bacteriol. 183:813-820.
55. Reimmann, C., L. Serino, M. Beyeler, and D. Haas. 1998. Dihydroaeruginoic acid synthetase and pyochelin synthetase, products of the pchEF genes, are induced by extracellular pyochelin in Pseudomonas aeruginosa. Microbiology 144:3135-3148.
56. Rutherford, K., J. Parkhill, J. Crook, T. Horsnell, P. Rice, M. A. Rajandream, and B. Barrell. 2000. Artemis: sequence visualization and annotation. Bioinformatics 16:944-945.
57. Sambrook. J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
58. Saner, M., K. Hantke, and V. Braun. 1990. Sequence of the fhuE outer-membrane receptor gene of Escherichia coli K12 and properties of mutants. Mol. Microbiol. 4:427-437.
59. Saxena, B., M. Modi, and V. V. Modi. 1986 Isolation and characterization of siderophores from Azospirillium lipoferum D-2. J. Gen. Microbiol. 132:2219-2224.
60. Schwyn, B., and J. B. Nellands. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160:47-56.
61. Sexton, R., P. R. Gill, Jr., M. J. Callanan, D. J. O'Sullivan, D. N. Dowling, and F. O'Gara. 1995. Iron-responsive gene expression in Pseudomonas fluorescens M114: cloning and characterization of a transcription-activating factor, PbrA. Mol. Microbiol. 15:297-306.
62. Simon, R., U. Priefer, and A. Puhler. 1983. A broad host range mobilization system for in vivo genetic enginerering: transposon mutagenesis in gram negative bacteria. Bio/Technology 1:784-791.
63. Sokol, P., P. Darling, S. Lewenza, C. Corbett, and C. Kooi. 2000. Identification of a siderophore receptor required for ferric-ornibactin uptake in Burkholderia cepacia. Infect. Immun. 68:6554-6560.
64. Sokol, P. A. 1986. Production and utilization of pyochelin by clinical isolates of Pseudomonas cepacia. J. Clin. Microbiol. 23:560-562.
65. 5-ornithine M-oxygenase. Infect. Immun. 67:4443-4455.
66. Sokol, P. A., C. J. Lewis, and J. J. Dennis. 1992. Isolation of a novel siderophore from Pseudomonas cepacia. J. Med. Microbiol. 36:18-189.
67. Sokol, P. A., and D. E. Woods. 1988. Effect of pyochelin on Pseudomonas cepacia respiratory infections. Microb. Pathog. 5:197-205.
68. Stephan, H., S. Freund, W. Beek, G. Jung, J. M. Meyer, and G. Winkelmann. 1993. Ornibactins-a new family of siderophores from Pseudomonas. Biometals 6:93-100.
69. Takase, H., H. Nitanai, K. Hoshino, and T. Otani. 2000. Impact of siderophore production on Pseudomonas aeruginosa infections in immunosuppressed mice. Infect. Immun. 68:1834-1839.
70. Vandamme, P., B. Holmes, T. Coenye, J. Goris, E. Mahenthiralingam, J. J. LiPuma, and J. R. Govan. 2003. Burkholderia cenocepacia sp, nov. - a new twist to an old story. Res. Microbiol. 154:91-96.
71. 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. 15:1081-1093.
72. Visca, P., A. Ciervo, V. Sanfilippo, and N. Orsi. 1993. Iron-regulated salicylate synthesis by Pseudomonas spp. J. Gen. Microbiol. 139:1995-2001.