A novel siderophore system is essential for the growth of Pseudomonas aeruginosa in airway mucus

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Gi, Mia ^a   Lee, Kang Mu ^a   Kim, Sang Cheol ^a   Yoon, Joo Heon ^a   Yoon, Sang Sun ^a,b   Choi, Jae Young ^a  

^a Brain Korea 21 Plus Project for Medical Science   (South Korea)

^b Yonsei University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

AZETIDINE 2 CARBOXYLIC ACID; CHLORIDE; FERRIC CHLORIDE; FERRIC ION; IRON; NICOTIANAMINE; OLIGOPEPTIDE; PHENOL DERIVATIVE; PYOCHELIN; PYOVERDINE; SIDEROPHORE; THIAZOLE DERIVATIVE;

ANALOGS AND DERIVATIVES; ANIMAL; BACTERIAL GENE; BIOSYNTHESIS; C57BL MOUSE; CHEMISTRY; COCULTURE; CYTOLOGY; DEFICIENCY; DRUG EFFECTS; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; HUMAN; MALE; METABOLISM; MICROARRAY ANALYSIS; MICROBIAL VIABILITY; MICROBIOLOGY; MOUSE; MUCUS; MUTATION; PATHOLOGY; PRIMARY CELL CULTURE; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; SECRETION (PROCESS); TRACHEA;

ANIMALS; AZETIDINECARBOXYLIC ACID; CHLORIDES; COCULTURE TECHNIQUES; EPITHELIAL CELLS; FERRIC COMPOUNDS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HUMANS; IRON; MALE; MICE; MICE, INBRED C57BL; MICROARRAY ANALYSIS; MICROBIAL VIABILITY; MUCUS; MUTATION; OLIGOPEPTIDES; PHENOLS; PRIMARY CELL CULTURE; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; SIDEROPHORES; THIAZOLES; TRACHEA;

EID: 84943651128     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep14644     Document Type: Article

References (65)

1. Folkesson, A. et al. Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective. Nat Rev Microbiol 10, 841-851, doi: 10.1038/nrmicro2907 (2012).
2. Bassi, G. L., Ferrer, M., Marti, J. D., Comaru, T. & Torres, A. Ventilator-associated pneumonia. Semin. Respir. Crit. Care Med. 35, 469-481, doi: 10.1055/s-0034-1384752 (2014).
3. Azzopardi, E. A. et al. Gram negative wound infection in hospitalised adult burn patients-systematic review and metanalysis. PLoS One 9, e95042, doi: 10.1371/journal.pone.0095042 (2014).
4. Smith, J. J., Travis, S. M., Greenberg, E. P. & Welsh, M. J. Cystic fibrosis airway epithelia fail to kill bacteria because of abnormal airway surface fluid. Cell 85, 229-236 (1996).
5. Regnis, J. A. et al. Mucociliary clearance in patients with cystic fibrosis and in normal subjects. Am. J. Respir. Crit. Care Med. 150, 66-71, doi: 10.1164/ajrccm.150.1.8025774 (1994).
6. Zahm, J. M. et al. X-ray microanalysis of airway surface liquid collected in cystic fibrosis mice. Am. J. Physiol. Lung Cell Mol. Physiol. 281, L309-313 (2001).
7. Matsui, H. et al. Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell 95, 1005-1015 (1998).
8. Worlitzsch, D. et al. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J. Clin. Invest. 109, 317-325, doi: 10.1172/JCI13870 (2002).
9. Yoon, S. S. et al. Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis. Dev Cell 3, 593-603 (2002).
10. Yoon, M. Y., Lee, K. M., Park, Y. & Yoon, S. S. Contribution of cell elongation to the biofilm formation of Pseudomonas aeruginosa during anaerobic respiration. PLoS One 6, e16105, doi: 10.1371/journal.pone.0016105 (2011).
11. Lee, K. M. et al. Vitamin B12-mediated restoration of defective anaerobic growth leads to reduced biofilm formation in Pseudomonas aeruginosa. Infect Immun 80, 1639-1649, doi: 10.1128/IAI.06161-11 (2012).
12. Dubin, R. F., Robinson, S. K. & Widdicombe, J. H. Secretion of lactoferrin and lysozyme by cultures of human airway epithelium. Am. J. Physiol. Lung Cell Mol. Physiol. 286, L750-755, doi: 10.1152/ajplung.00326.2003 (2004).
13. Puchelle, E., Jacqot, J. & Zahm, J. M. In vitro restructuring effect of human airway immunoglobulins A and lysozyme on airway secretions. Eur. J. Respir. Dis. Suppl. 153, 117-122 (1987).
14. Sagel, S. D., Sontag, M. K. & Accurso, F. J. Relationship between antimicrobial proteins and airway inflammation and infection in cystic fibrosis. Pediatr. Pulmonol. 44, 402-409, doi: 10.1002/ppul.21028 (2009).
15. Poole, K. & McKay, G. A. Iron acquisition and its control in Pseudomonas aeruginosa: many roads lead to Rome. Front. Biosci. 8, d661-686 (2003).
16. Guerinot, M. L. Microbial iron transport. Annu. Rev. Microbiol. 48, 743-772, doi: 10.1146/annurev.mi.48.100194.003523 (1994).
17. Mason, D. Y. & Taylor, C. R. Distribution of transferrin, ferritin, and lactoferrin in human tissues. J. Clin. Pathol. 31, 316-327 (1978).
18. Hoegy, F., Mislin, G. L. & Schalk, I. J. Pyoverdine and pyochelin measurements. Methods Mol. Biol. 1149, 293-301, doi: 10.1007/978-1-4939-0473-0-24 (2014).
19. Lamont, I. L., Beare, P. A., Ochsner, U., Vasil, A. I. & Vasil, M. L. Siderophore-mediated signaling regulates virulence factor production in Pseudomonasaeruginosa. Proc. Natl. Acad. Sci. USA 99, 7072-7077, doi: 10.1073/pnas.092016999 (2002).
20. Beare, P. A., For, R. J., Martin, L. W. & Lamont, I. L. Siderophore-mediated cell signalling in Pseudomonas aeruginosa: divergent pathways regulate virulence factor production and siderophore receptor synthesis. Mol. Microbiol. 47, 195-207 (2003).
21. De Vos, D. et al. Study of pyoverdine type and production by Pseudomonas aeruginosa isolated from cystic fibrosis patients: prevalence of type II pyoverdine isolates and accumulation of pyoverdine-negative mutations. Arch. Microbiol. 175, 384-388 (2001).
22. Nguyen, A. T. et al. Adaptation of iron homeostasis pathways by a Pseudomonas aeruginosa pyoverdine mutant in the cystic fibrosis lung. J. Bacteriol. 196, 2265-2276, doi: 10.1128/JB.01491-14 (2014).
23. Takase, H., Nitanai, H., Hoshino, K. & Otani, T. Impact of siderophore production on Pseudomonas aeruginosa infections in immunosuppressed mice. Infect. Immun. 68, 1834-1839 (2000).
24. Ochsner, U. A., Johnson, Z. & Vasil, M. L. Genetics and regulation of two distinct haem-uptake systems, phu and has, in Pseudomonas aeruginosa. Microbiology 146, (Pt 1) 185-198 (2000).
25. Takase, H., Nitanai, H., Hoshino, K. & Otani, T. Requirement of the Pseudomonas aeruginosa tonB gene for high-affinity iron acquisition and infection. Infect. Immun. 68, 4498-4504 (2000).
26. Cartron, M. L., Maddocks, S., Gillingham, P., Craven, C. J. & Andrews, S. C. Feo-transport of ferrous iron into bacteria. Biometals 19, 143-157, doi: 10.1007/s10534-006-0003-2 (2006).
27. Fahy, J. V. & Dickey, B. F. Airway mucus function and dysfunction. N. Engl. J. Med. 363, 2233-2247, doi: 10.1056/NEJMra0910061 (2010).
28. Bingle, C. D. et al. Human LPLUNC1 is a secreted product of goblet cells and minor glands of the respiratory and upper aerodigestive tracts. Histochem Cell Biol 133, 505-515, doi: 10.1007/s00418-010-0683-0 (2010).
29. Bartlett, J. A. et al. PLUNC: a multifunctional surfactant of the airways. Biochem Soc Trans 39, 1012-1016, doi: 10.1042/BST0391012 (2011).
30. Parker, D. & Prince, A. Innate immunity in the respiratory epithelium. Am J Respir Cell Mol Biol 45, 189-201, doi: 10.1165/rcmb.2011-0011RT (2011).
31. Thornton, D. J. et al. Respiratory mucins: identification of core proteins and glycoforms. Biochem J 316, (Pt 3) 967-975 (1996).
32. Crosa, J. H. Genetics and molecular biology of siderophore-mediated iron transport in bacteria. Microbiol. Rev. 53, 517-530 (1989).
33. Vasil, M. L. & Ochsner, U. A. The response of Pseudomonas aeruginosa to iron: genetics, biochemistry and virulence. Mol Microbiol 34, 399-413 (1999).
34. Farnaud, S. & Evans, R. W. Lactoferrin-a multifunctional protein with antimicrobial properties. Mol. Immunol. 40, 395-405 (2003).
35. Jacquot, J., Hayem, A. & Galabert, C. Functions of proteins and lipids in airway secretions. Eur Respir J 5, 343-358 (1992).
36. Tu, W. Y. et al. Cellular iron distribution in Bacillus anthracis. J. Bacteriol. 194, 932-940, doi: 10.1128/JB.06195-11 (2012).
37. Visca, P., Imperi, F. & Lamont, I. L. Pyoverdine siderophores: from biogenesis to biosignificance. Trends Microbiol. 15, 22-30, doi: 10.1016/j.tim.2006.11.004 (2007).
38. Vasil, M. L. How we learnt about iron acquisition in Pseudomonas aeruginosa: a series of very fortunate events. Biometals 20, 587-601, doi: 10.1007/s10534-006-9067-2 (2007).
39. Becker, R., Grun, M. & Scholz, G. Nicotianamine and the distribution of iron into the apoplasm and symplasm of tomato (Lycopersicon esculentum Mill.): I. Determination of the apoplasmic and symplasmic iron pools in roots and leaves of the cultivar Bonner Beste and its nicotianamine-less mutant chloronerva. Planta 187, 48-52, doi: 10.1007/BF00201622 (1992).
40. Takahashi, M. et al. Role of nicotianamine in the intracellular delivery of metals and plant reproductive development. Plant Cell 15, 1263-1280 (2003).
41. Girod, S., Zahm, J. M., Plotkowski, C., Beck, G. & Puchelle, E. Role of the physiochemical properties of mucus in the protection of the respiratory epithelium. Eur. Respir. J. 5, 477-487 (1992).
42. Yoon, S. S. & Hassett, D. J. Chronic Pseudomonas aeruginosa infection in cystic fibrosis airway disease: metabolic changes that unravel novel drug targets. Expert Rev Anti Infect Ther 2, 611-623 (2004).
43. Gerson, C. et al. The lactoperoxidase system functions in bacterial clearance of airways. Am. J. Respir. Cell Mol. Biol. 22, 665-671, doi: 10.1165/ajrcmb.22.6.3980 (2000).
44. Hoegger, M. J. et al. Cystic fibrosis. Impaired mucus detachment disrupts mucociliary transport in a piglet model of cystic fibrosis. Science 345, 818-822, doi: 10.1126/science.1255825 (2014).
45. Palmer, K. L., Mashburn, L. M., Singh, P. K. & Whiteley, M. Cystic fibrosis sputum supports growth and cues key aspects of Pseudomonas aeruginosa physiology. J. Bacteriol. 187, 5267-5277, doi: 10.1128/JB.187.15.5267-5277.2005 (2005).
46. Yoon, S. S. et al. Anaerobic killing of mucoid Pseudomonas aeruginosa by acidified nitrite derivatives under cystic fibrosis airway conditions. J Clin Invest 116, 436-446, doi: 10.1172/JCI24684 (2006).
47. Cole, A. M., Dewan, P. & Ganz, T. Innate antimicrobial activity of nasal secretions. Infect. Immun. 67, 3267-3275 (1999).
48. Son, M. S., Matthews, W. J., Jr., Kang, Y., Nguyen, D. T. & Hoang, T. T. In vivo evidence of Pseudomonas aeruginosa nutrient acquisition and pathogenesis in the lungs of cystic fibrosis patients. Infect. Immun. 75, 5313-5324, doi: 10.1128/IAI.01807-06 (2007).
49. Hare, N. J. et al. Proteomics of Pseudomonas aeruginosa Australian epidemic strain 1 (AES-1) cultured under conditions mimicking the cystic fibrosis lung reveals increased iron acquisition via the siderophore pyochelin. J. Proteome Res. 11, 776-795, doi: 10.1021/pr200659h (2012).
50. Ochsner, U. A., Wilderman, P. J., Vasil, A. I. & Vasil, M. L. GeneChip expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes. Mol Microbiol 45, 1277-1287 (2002).
51. Lory, S., Jin, S., Boyd, J. M., Rakeman, J. L. & Bergman, P. Differential gene expression by Pseudomonas aeruginosa during interaction with respiratory mucus. Am. J. Respir. Crit. Care Med. 154, S183-186, doi: 10.1164/ajrccm/154.4-Pt-2.S183 (1996).
52. Cornelis, P., Matthijs, S. & Van Oeffelen, L. Iron uptake regulation in Pseudomonas aeruginosa. Biometals 22, 15-22, doi: 10.1007/s10534-008-9193-0 (2009).
53. Lamont, I. L., Konings, A. F. & Reid, D. W. Iron acquisition by Pseudomonas aeruginosa in the lungs of patients with cystic fibrosis. Biometals 22, 53-60, doi: 10.1007/s10534-008-9197-9 (2009).
54. Cornelis, P. Iron uptake and metabolism in pseudomonads. Appl. Microbiol. Biotechnol. 86, 1637-1645, doi: 10.1007/s00253-010-2550-2 (2010).
55. Nozoye, T. et al. Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J. Biol. Chem. 286, 5446-5454, doi: 10.1074/jbc.M110.180026 (2011).
56. von Wiren, N. et al. Nicotianamine chelates both FeIII and FeII. Implications for metal transport in plants. Plant Physiol. 119, 1107-1114 (1999).
57. Beckmann, C. et al. Use of phage display to identify potential Pseudomonas aeruginosa gene products relevant to early cystic fibrosis airway infections. Infect. Immun. 73, 444-452, doi: 10.1128/IAI.73.1.444-452.2005 (2005).
58. Mashburn, L. M., Jett, A. M., Akins, D. R. & Whiteley, M. Staphylococcus aureus serves as an iron source for Pseudomonas aeruginosa during in vivo coculture. J. Bacteriol. 187, 554-566, doi: 10.1128/JB.187.2.554-566.2005 (2005).
59. Bielecki, P. et al. In-vivo expression profiling of Pseudomonas aeruginosa infections reveals niche-specific and strain-independent transcriptional programs. PLoS One 6, e24235, doi: 10.1371/journal.pone.0024235 (2011).
60. Yoon, J. H., Gray, T., Guzman, K., Koo, J. S. & Nettesheim, P. Regulation of the secretory phenotype of human airway epithelium by retinoic acid, triiodothyronine, and extracellular matrix. Am J Respir Cell Mol Biol 16, 724-731, doi: 10.1165/ajrcmb.16.6.9191474 (1997).
61. Lee, K. M. et al. Activation of cholera toxin production by anaerobic respiration of trimethylamine N-oxide in Vibrio cholerae. J Biol Chem 287, 39742-39752, doi: 10.1074/jbc.M112.394932 (2012).
62. Kim, Y. J. et al. Hypoxia-mediated mechanism of MUC5AC production in human nasal epithelia and its implication in rhinosinusitis. PLoS One 9, e98136, doi: 10.1371/journal.pone.0098136 (2014).
63. Newman, J. R. & Fuqua, C. Broad-host-range expression vectors that carry the L-arabinose-inducible Escherichia coli araBAD promoter and the araC regulator. Gene 227, 197-203 (1999).
64. Rumbaugh, K. P., Colmer, J. A., Griswold, J. A. & Hamood, A. N. The effects of infection of thermal injury by Pseudomonas aeruginosa PAO1 on the murine cytokine response. Cytokine 16, 160-168, doi: 10.1006/cyto.2001.0960 (2001).
65. Gi, M. et al. A drug-repositioning screening identifies pentetic acid as a potential therapeutic agent for suppressing the elastasemediated virulence of Pseudomonas aeruginosa. Antimicrob Agents Chemother 58, 7205-7214, doi: 10.1128/AAC.03063-14 (2014).