1887

Abstract

which causes serious infections in immunocompromised patients, produces numerous virulence factors, including exotoxin A and the siderophore pyoverdine. As production of these virulence factors is influenced by the host environment, we examined the effect serum has on global transcription within strain PAO1 at different phases of growth in an iron-deficient medium. At early exponential phase, serum significantly enhanced expression of 138 genes, most of which are repressed by iron, including , and the pyoverdine synthesis genes. However, serum did not interfere with the repression of these genes by iron. Serum enhanced expression in a mutant of PAO1 but not in a mutant. The serum iron-binding protein apotransferrin, but not ferritin, enhanced and expression. However, in PAO1 grown in a chemically defined medium that contains no iron, serum but not apotransferrin enhanced and expression. While complement inactivation failed to eliminate this effect, albumin absorption reduced the effect of serum on and expression in the iron-deficient medium chelexed tryptic soy broth dialysate. Additionally, albumin absorption eliminated the effect of serum on and expression in the chemically defined medium. These results suggest that serum enhances the expression of iron-controlled genes by two mechanisms: one through apotransferrin and another one through albumin.

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2012-02-01
2019-10-13
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References

  1. Ambrosi C. , Leoni L. , Visca P. . ( 2002; ). Different responses of pyoverdine genes to autoinduction in Pseudomonas aeruginosa and the group Pseudomonas fluorescens–Pseudomonas putida. . Appl Environ Microbiol 68:, 4122–4126. [CrossRef] [PubMed]
    [Google Scholar]
  2. Anzaldi L. L. , Skaar E. P. . ( 2010; ). Overcoming the heme paradox: heme toxicity and tolerance in bacterial pathogens. . Infect Immun 78:, 4977–4989. [CrossRef] [PubMed]
    [Google Scholar]
  3. Ardehali R. , Shi L. , Janatova J. , Mohammad S. F. , Burns G. L. . ( 2003; ). The inhibitory activity of serum to prevent bacterial adhesion is mainly due to apo-transferrin. . J Biomed Mater Res A 66:, 21–28. [CrossRef] [PubMed]
    [Google Scholar]
  4. Barton H. A. , Johnson Z. , Cox C. D. , Vasil A. I. , Vasil M. L. . ( 1996; ). Ferric uptake regulator mutants of Pseudomonas aeruginosa with distinct alterations in the iron-dependent repression of exotoxin A and siderophores in aerobic and microaerobic environments. . Mol Microbiol 21:, 1001–1017. [CrossRef] [PubMed]
    [Google Scholar]
  5. Branski L. K. , Al-Mousawi A. , Rivero H. , Jeschke M. G. , Sanford A. P. , Herndon D. N. . ( 2009; ). Emerging infections in burns. . Surg Infect (Larchmt) 10:, 389–397. [CrossRef] [PubMed]
    [Google Scholar]
  6. Cornelis P. . ( 2010; ). Iron uptake and metabolism in pseudomonads. . Appl Microbiol Biotechnol 86:, 1637–1645. [CrossRef] [PubMed]
    [Google Scholar]
  7. Cornelis P. , Aendekerk S. . ( 2004; ). A new regulator linking quorum sensing and iron uptake in Pseudomonas aeruginosa. . Microbiology 150:, 752–756. [CrossRef] [PubMed]
    [Google Scholar]
  8. Cornelis P. , Matthijs S. , Van Oeffelen L. . ( 2009; ). Iron uptake regulation in Pseudomonas aeruginosa. . Biometals 22:, 15–22. [CrossRef] [PubMed]
    [Google Scholar]
  9. Cunliffe H. E. , Merriman T. R. , Lamont I. L. . ( 1995; ). Cloning and characterization of pvdS, a gene required for pyoverdine synthesis in Pseudomonas aeruginosa: PvdS is probably an alternative sigma factor. . J Bacteriol 177:, 2744–2750.[PubMed]
    [Google Scholar]
  10. DeRisi J. . ( 2001; ). Overview of nucleic acid arrays.. In Current Protocols in Molecular Biology, 22.1.1–22.1.7. http://dx.doi.org/10.1002/0471142727.mb2201s49 [CrossRef]
    [Google Scholar]
  11. Foster J. F. . ( 1977; ). Binding properties of albumin. . In Albumin Structure, Function and Uses, pp. 53–84. Edited by Rosenoer V. M. , Oratz M. , Rothschild M. A. . . Oxford:: Pergamon;.
    [Google Scholar]
  12. Frank D. W. . ( 1997; ). The exoenzyme S regulon of Pseudomonas aeruginosa. . Mol Microbiol 26:, 621–629. [CrossRef] [PubMed]
    [Google Scholar]
  13. Gaines J. M. , Carty N. L. , Colmer-Hamood J. A. , Hamood A. N. . ( 2005; ). Effect of static growth and different levels of environmental oxygen on toxA and ptxR expression in the Pseudomonas aeruginosa strain PAO1. . Microbiology 151:, 2263–2275. [CrossRef] [PubMed]
    [Google Scholar]
  14. Garber M. , Urisman A. . ( 2001; ). Protocol for reverse transcription and amino-allyl coupling of RNA. . Stanford, CA:: Stanford Functional Genomics Facility;. http://www.microarray.org/sfgf/docView.do?type=2; accessed 23 June 2011.
  15. González-Chávez S. A. , Arévalo-Gallegos S. , Rascón-Cruz Q. . ( 2009; ). Lactoferrin: structure, function and applications. . Int J Antimicrob Agents 33:, e301–e308. [CrossRef] [PubMed]
    [Google Scholar]
  16. Hammond A. , Dertien J. , Colmer-Hamood J. A. , Griswold J. A. , Hamood A. N. . ( 2010; ). Serum inhibits P. aeruginosa biofilm formation on plastic surfaces and intravenous catheters. . J Surg Res 159:, 735–746. [CrossRef] [PubMed]
    [Google Scholar]
  17. Hamood A. N. , Colmer-Hamood J. A. , Carty N. L. . ( 2004; ). Regulation of Pseudomonas aeruginosa exotoxin A synthesis. . In Pseudomonas: Virulence and Gene Regulation, pp. 389–423. Edited by Ramos J.-L. . . New York, NY:: Kluwer Academic/Plenum Publishers;. [CrossRef]
    [Google Scholar]
  18. Hauser A. R. . ( 2009; ). The type III secretion system of Pseudomonas aeruginosa: infection by injection. . Nat Rev Microbiol 7:, 654–665. [CrossRef] [PubMed]
    [Google Scholar]
  19. Heinrichs D. E. , Poole K. . ( 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.[PubMed]
    [Google Scholar]
  20. Hider R. C. , Silva A. M. , Podinovskaia M. , Ma Y. . ( 2010; ). Monitoring the efficiency of iron chelation therapy: the potential of nontransferrin-bound iron. . Ann N Y Acad Sci 1202:, 94–99. [CrossRef] [PubMed]
    [Google Scholar]
  21. Jacobs M. A. , Alwood A. , Thaipisuttikul I. , Spencer D. , Haugen E. , Ernst S. , Will O. , Kaul R. , Raymond C. . & other authors ( 2003; ). Comprehensive transposon mutant library of Pseudomonas aeruginosa. . Proc Natl Acad Sci U S A 100:, 14339–14344. [CrossRef] [PubMed]
    [Google Scholar]
  22. Juhas M. , Wiehlmann L. , Huber B. , Jordan D. , Lauber J. , Salunkhe P. , Limpert A. S. , von Götz F. , Steinmetz I. . & other authors ( 2004; ). Global regulation of quorum sensing and virulence by VqsR in Pseudomonas aeruginosa. . Microbiology 150:, 831–841. [CrossRef] [PubMed]
    [Google Scholar]
  23. Kim J. , Ahn K. , Min S. , Jia J. , Ha U. , Wu D. , Jin S. . ( 2005; ). Factors triggering type III secretion in Pseudomonas aeruginosa. . Microbiology 151:, 3575–3587. [CrossRef] [PubMed]
    [Google Scholar]
  24. Li W. , Lyte M. , Freestone P. P. , Ajmal A. , Colmer-Hamood J. A. , Hamood A. N. . ( 2009; ). Norepinephrine represses the expression of toxA and the siderophore genes in Pseudomonas aeruginosa. . FEMS Microbiol Lett 299:, 100–109. [CrossRef] [PubMed]
    [Google Scholar]
  25. Ma J. F. , Ochsner U. A. , Klotz M. G. , Nanayakkara V. K. , Howell M. L. , Johnson Z. , Posey J. E. , Vasil M. L. , Monaco J. J. , Hassett D. J. . ( 1999; ). Bacterioferritin A modulates catalase A (KatA) activity and resistance to hydrogen peroxide in Pseudomonas aeruginosa. . J Bacteriol 181:, 3730–3742.[PubMed]
    [Google Scholar]
  26. Miller J. H. . ( 1972; ). Experiments in Molecular Genetics. Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory;.
    [Google Scholar]
  27. Nairz M. , Schroll A. , Sonnweber T. , Weiss G. . ( 2010; ). The struggle for iron – a metal at the host–pathogen interface. . Cell Microbiol 12:, 1691–1702. [CrossRef] [PubMed]
    [Google Scholar]
  28. Ochsner U. A. , Vasil M. L. . ( 1996; ). Gene repression by the ferric uptake regulator in Pseudomonas aeruginosa: cycle selection of iron-regulated genes. . Proc Natl Acad Sci U S A 93:, 4409–4414. [CrossRef] [PubMed]
    [Google Scholar]
  29. Ochsner U. A. , Vasil A. I. , Vasil M. L. . ( 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:, 7194–7201.[PubMed]
    [Google Scholar]
  30. Ochsner U. A. , Johnson Z. , Lamont I. L. , Cunliffe H. E. , Vasil M. L. . ( 1996; ). Exotoxin A production in Pseudomonas aeruginosa requires the iron-regulated pvdS gene encoding an alternative sigma factor. . Mol Microbiol 21:, 1019–1028. [CrossRef] [PubMed]
    [Google Scholar]
  31. Ochsner U. A. , Wilderman P. J. , Vasil A. I. , Vasil M. L. . ( 2002; ). GeneChip expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes. . Mol Microbiol 45:, 1277–1287. [CrossRef] [PubMed]
    [Google Scholar]
  32. Ohman D. E. , Sadoff J. C. , Iglewski B. H. . ( 1980; ). Toxin A-deficient mutants of Pseudomonas aeruginosa PA103: isolation and characterization. . Infect Immun 28:, 899–908.[PubMed]
    [Google Scholar]
  33. Peluso L. , de Luca C. , Bozza S. , Leonardi A. , Giovannini G. , Lavorgna A. , De Rosa G. , Mascolo M. , Ortega De Luna L. . & other authors ( 2010; ). Protection against Pseudomonas aeruginosa lung infection in mice by recombinant OprF-pulsed dendritic cell immunization. . BMC Microbiol 10:, 9. [CrossRef] [PubMed]
    [Google Scholar]
  34. Peters T. Jr . ( 1996; ). The albumin molecule: its structure and chemical properties. . In All About Albumin: Biochemistry, Genetics and Medical Applications, pp. 9–75. Edited by Peters T. . . San Diego:: Academic Press;.
    [Google Scholar]
  35. Pier G. B. , Ramphal R. . ( 2005; ). Pseudomonas aeruginosa. . In Mandell, Douglas, and Bennett's Principles and Practice of Infectious Diseases, pp. 2587–2615. Edited by Mandel G. L. , Bennett J. E. , Dolin R. . . Philadelphia:: Elsevier/Churchill Livingstone;.
    [Google Scholar]
  36. Rondeau P. , Bourdon E. . ( 2011; ). The glycation of albumin: structural and functional impacts. . Biochimie 93:, 645–658. [CrossRef] [PubMed]
    [Google Scholar]
  37. Sadikot R. T. , Blackwell T. S. , Christman J. W. , Prince A. S. . ( 2005; ). Pathogen–host interactions in Pseudomonas aeruginosa pneumonia. . Am J Respir Crit Care Med 171:, 1209–1223. [CrossRef] [PubMed]
    [Google Scholar]
  38. Schaber J. A. , Carty N. L. , McDonald N. A. , Graham E. D. , Cheluvappa R. , Griswold J. A. , Hamood A. N. . ( 2004; ). Analysis of quorum sensing-deficient clinical isolates of Pseudomonas aeruginosa. . J Med Microbiol 53:, 841–853. [CrossRef] [PubMed]
    [Google Scholar]
  39. Silva A. M. , Hider R. C. . ( 2009; ). Influence of non-enzymatic post-translation modifications on the ability of human serum albumin to bind iron. Implications for non-transferrin-bound iron speciation. . Biochim Biophys Acta 1794:, 1449–1458.[PubMed] [CrossRef]
    [Google Scholar]
  40. Smith R. S. , Iglewski B. H. . ( 2003; ). P. aeruginosa quorum-sensing systems and virulence. . Curr Opin Microbiol 6:, 56–60. [CrossRef] [PubMed]
    [Google Scholar]
  41. Stachel S. E. , An G. , Flores C. , Nester E. W. . ( 1985; ). A Tn3 lacZ transposon for the random generation of beta-galactosidase gene fusions: application to the analysis of gene expression in Agrobacterium. . EMBO J 4:, 891–898.[PubMed]
    [Google Scholar]
  42. Stintzi A. , Cornelis P. , Hohnadel D. , Meyer J. M. , Dean C. , Poole K. , Kourambas S. , Krishnapillai V. . ( 1996; ). Novel pyoverdine biosynthesis gene(s) of Pseudomonas aeruginosa PAO. . Microbiology 142:, 1181–1190. [CrossRef] [PubMed]
    [Google Scholar]
  43. Storey D. G. , Frank D. W. , Farinha M. A. , Kropinski A. M. , Iglewski B. H. . ( 1990; ). Multiple promoters control the regulation of the Pseudomonas aeruginosa regA gene. . Mol Microbiol 4:, 499–503. [CrossRef] [PubMed]
    [Google Scholar]
  44. van Delden C. . ( 2004; ). Virulence factors in Pseudomonas aeruginosa . . In Pseudomonas: Virulence and Gene Regulation, pp. 3–45. Edited by Ramos J.-L. . . New York:: Kluwer Academic/Plenum Publishers;.
    [Google Scholar]
  45. Vasil M. L. , Ochsner U. A. . ( 1999; ). The response of Pseudomonas aeruginosa to iron: genetics, biochemistry and virulence. . Mol Microbiol 34:, 399–413. [CrossRef] [PubMed]
    [Google Scholar]
  46. Wang J. , Pantopoulos K. . ( 2011; ). Regulation of cellular iron metabolism. . Biochem J 434:, 365–381. [CrossRef] [PubMed]
    [Google Scholar]
  47. West S. E. , Sample A. K. , Runyen-Janecky L. J. . ( 1994; ). The vfr gene product, required for Pseudomonas aeruginosa exotoxin A and protease production, belongs to the cyclic AMP receptor protein family. . J Bacteriol 176:, 7532–7542.[PubMed]
    [Google Scholar]
  48. Wilderman P. J. , Sowa N. A. , FitzGerald D. J. , FitzGerald P. C. , Gottesman S. , Ochsner U. A. , Vasil M. L. . ( 2004; ). Identification of tandem duplicate regulatory small RNAs in Pseudomonas aeruginosa involved in iron homeostasis. . Proc Natl Acad Sci U S A 101:, 9792–9797. [CrossRef] [PubMed]
    [Google Scholar]
  49. Wilson M. J. , McMorran B. J. , Lamont I. L. . ( 2001; ). Analysis of promoters recognized by PvdS, an extracytoplasmic-function sigma factor protein from Pseudomonas aeruginosa. . J Bacteriol 183:, 2151–2155. [CrossRef] [PubMed]
    [Google Scholar]
  50. Winsor G. L. , Van Rossum T. , Lo R. , Khaira B. , Whiteside M. D. , Hancock R. E. , Brinkman F. S. . ( 2009; ). Pseudomonas Genome Database: facilitating user-friendly, comprehensive comparisons of microbial genomes. . Nucleic Acids Res 37: (Database issue), D483–D488. [CrossRef] [PubMed]
    [Google Scholar]
  51. Yang I. V. , Chen E. , Hasseman J. P. , Liang W. , Frank B. C. , Wang S. , Sharov V. , Saeed A. I. , White J. . & other authors ( 2002; ). Within the fold: assessing differential expression measures and reproducibility in microarray assays. . Genome Biol 3:, h0062.[PubMed]
    [Google Scholar]
  52. Ye R. W. , Haas D. , Ka J. O. , Krishnapillai V. , Zimmermann A. , Baird C. , Tiedje J. M. . ( 1995; ). Anaerobic activation of the entire denitrification pathway in Pseudomonas aeruginosa requires Anr, an analog of Fnr. . J Bacteriol 177:, 3606–3609.[PubMed]
    [Google Scholar]
  53. Zheng P. , Sun J. , Geffers R. , Zeng A. P. . ( 2007; ). Functional characterization of the gene PA2384 in large-scale gene regulation in response to iron starvation in Pseudomonas aeruginosa. . J Biotechnol 132:, 342–352. [CrossRef] [PubMed]
    [Google Scholar]
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