Ferrous iron is a significant component of bioavailable iron in cystic fibrosis airways

mBio

Volumn 4, Issue 4, 2013, Pages

  Hunter, Ryan C ^a   Asfour, Fadi ^c   Dingemans, Jozef ^d,e   Osuna, Brenda L ^f   Samad, Tahoura ^a   Malfroot, Anne ^g   Cornelis, Pierre ^d   Newman, Dianne K ^a,b  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^c CHILDREN S HOSPITAL LOS ANGELES   (United States)

^d DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^e BELGIAN NUCLEAR RESEARCH CENTRE   (Belgium)

^f UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^g UNIVERSITY HOSPITAL BRUSSELS   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

FERRIC ION; FERROUS ION; IRON CHELATING AGENT;

ADOLESCENT; ADULT; ARTICLE; BACTERIAL GENE; BIOAVAILABILITY; BIOFILM; BQSRS GENE; CHELATION THERAPY; CHILD; CONTROLLED STUDY; CYSTIC FIBROSIS; DISEASE COURSE; DISEASE SEVERITY; ENVIRONMENT; HOST; HUMAN; IN VITRO STUDY; INFECTION CONTROL; MICROBIAL COMMUNITY; MORTALITY; NONHUMAN; OPPORTUNISTIC INFECTION; OXIDATION; PRIORITY JOURNAL; PSEUDOMONAS INFECTION; PSEUDOMONAS PNEUMONIA; RESPIRATORY SYSTEM; SCHOOL CHILD; SPUTUM; TRANSCRIPTION REGULATION;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

EID: 84883420466     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00557-13     Document Type: Article

References (52)

1. Rajan S, Saiman L. 2002. Pulmonary infections in patients with cystic fibrosis. Semin. Respir. Infect. 17:47-56.
2. Bjarnsholt T, Jensen PO, Fiandaca MJ, Pedersen J, Hansen CR, Andersen CB, Pressler T, Givskov M, Hoiby N. 2009. Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients. Pediatr. Pulmonol. 44:547-558.
3. Alvarez-Ortega C, Harwood CS. 2007. Responses of Pseudomonas aeruginosa to low oxygen indicate that growth in the cystic fibrosis lung is by aerobic respiration. Mol. Microbiol. 65:153-165.
4. Palmer KL, Aye LM, Whiteley M. 2007. Nutritional cues control Pseudomonas aeruginosa multicellular behavior in cystic fibrosis sputum. J. Bacteriol. 189:8079-8087.
5. Worlitzsch D, Tarran R, Ulrich M, Schwab U, Cekici A, Meyer KC, Birrer P, Bellon G, Berger J, Weiss T, Botzenhart K, Yankaskas JR, Randell S, Boucher RC, Döring G. 2002. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J. Clin. Invest. 109:317-325.
6. Aanaes K, Rickelt LF, Johansen HK, von Buchwald C, Pressler T, Hoiby N, Jensen PO. 2011. Decreased mucosal oxygen tension in the maxillary sinuses in patients with cystic fibrosis. J. Cyst. Fibros. 10:114-120.
7. Yang L, Jelsbak L, Molin S. 2011. Microbial ecology and adaptation in cystic fibrosis airways. Environ. Microbiol. 13:1682-1689.
8. Fischbach MA, Lin H, Liu DR, Walsh CT. 2006. How pathogenic bacteria evade mammalian sabotage in the battle for iron. Nat. Chem. Biol. 2:132-138.
9. Skaar EP. 2010. The battle for iron between bacterial pathogens and their vertebrate hosts. PLoS Pathog. 6:e1000949. doi:10.1371/ journal.ppat.1000949.
10. Singh PK, Parsek MR, Greenberg EP, Welsh MJ. 2002. A component of innate immunity prevents bacterial biofilm development. Nature 417: 552-555.
11. Singh PK. 2004. Iron sequestration by human lactoferrin stimulates Pseudomonas aeruginosa surface motility and blocks biofilm formation. Proc. Natl. Acad. Sci. U. S. A. 17:267-270.
12. Banin E, Vasil ML, Greenberg EP. 2005. Iron and Pseudomonas aeruginosa biofilm formation. Proc. Natl. Acad. Sci. U. S. A. 102:11076-11081.
13. Banin E, Brady KM, Greenberg EP. 2006. Chelator-induced dispersal and killing of Pseudomonas aeruginosa cells in a biofilm. Appl. Environ. Microbiol. 72:2064-2069.
14. O'May CY, Sanderson K, Roddam LF, Kirov SM, Reid DW. 2009. Iron-binding compounds impair Pseudomonas aeruginosa biofilm formation, especially under anaerobic conditions. J. Med. Microbiol. 58: 765-773.
15. Moreau-Marquis S, O'Toole GA, Stanton BA. 2009. Tobramycin and FDA-approved iron chelators eliminate Pseudomonas aeruginosa biofilms on cystic fibrosis cells. Am. J. Respir. Cell Mol. Biol. 41:305-313.
16. Carton ML, Maddocks S, Gillingham P, Craven CJ, Andrews SC. 2006. Feo-transport of ferrous iron into bacteria. Biometals 2:143-157.
17. Kaneko Y, Thoendel M, Olakanmi O, Britigan BE, Singh PK. 2007. The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial and antibiofilm activity. J. Clin. Invest. 117: 877-888.
18. Banin E, Lozinski A, Brady KM, Berenshtein E, Butterfield PW, Moshe M, Chevion M, Greenberg EP, Banin E. 2008. The potential of desferrioxamine-gallium as an anti-Pseudomonas therapeutic agent. Proc. Natl. Acad. Sci. U. S. A. 105:16761-16766.
19. Galli F, Battistoni A, Gambari R, Pompella A, Bragonzi A, Pilolli F, Iuliano L, Piroddi M, Dechecchi MC, Cabrini G, Working Group on Inflammation in Cystic Fibrosis. 2012. Oxidative stress and antioxidant therapy in cystic fibrosis. Biochim. Biophys. Acta 1822:690-713.
20. Garg S, Rose AL, Waite TD. 2007. Superoxide mediated reduction of organically complexed iron(III): comparison of non-dissociative and dissociative reduction pathways. Environ. Sci. Technol. 41:3205-3212.
21. Koley D, Ramsey MM, Bard AJ, Whiteley M. 2011. Discovery of a biofilm electrocline using real-time 3D metabolite analysis. Proc. Natl. Acad. Sci. U. S. A. 108:19996-20001.
22. Hunter RC, Klepac-Ceraj V, Lorenzi MM, Grotzinger H, Martin TR, Newman DK. 2012. Phenazine content in the cystic fibrosis respiratory tract negatively correlates with lung function and microbial complexity. Am. J. Respir. Cell Mol. Biol. 47:738-745.
23. Cox CD. 1986. Role of pyocyanin in the acquisition of iron from transferrin. Infect. Immun. 52:263-270.
24. Reid DW, Carroll V, O'May C, Champion A, Kirov SM. 2007. Increased airway iron as a potential factor in the persistence of Pseudomonas aeruginosa infection in cystic fibrosis airways. Eur. Respir. J. 30:286-292.
25. Stites SW, Walters B, O'Brien-Ladner AR, Bailey K, Wesselius LJ. 1998. Increased iron and ferritin content of sputum from patients with cystic fibrosis or chronic bronchitis. Chest 114:814-819.
26. Ghio AJ, Roggli VL, Soukup JM, Richards JH, Randell SH, Muhlebach MS. 2013. Iron accumulates in the lavage and explanted lungs of cystic fibrosis patients. J. Cyst. Fibros. 12:390-398.
27. Mateos F, Brock JH, Pérez-Arellano JL. 1998. Iron metabolism in the lower respiratory tract. Thorax 53:594-600.
28. Moreau-Marquis S, Bomberger JM, Anderson GG, Swiatecka-Urban A, Ye S, O'Toole GA, Stanton BA. 2008. The Delta-F508-CFTR mutation results in increased biofilm formation by Pseudomonas aeruginosa by increasing iron availability. Am. J. Physiol. Lung Cell. Mol. Physiol. 295: L25-L37.
29. Miller RA, Britigan BE. 1995. Protease-cleaved iron-transferrin augments oxidant-mediated endothelial cell injury via hydroxyl radical formation. J. Clin. Invest. 95:2491-2500.
30. Wang Y, Newman DK. 2008. Redox reactions of phenazine antibiotics with ferric (hydr)oxides and molecular oxygen. Environ. Sci. Technol. 42:2380-2386.
31. Wang Y, Wilks JC, Danhorn T, Ramos I, Croal L, Newman DK. 2011. Phenazine-1-carboxylic acid promotes bacterial biofilm development via ferrous iron acquisition. J. Bacteriol. 193:3606-3617.
32. Kreamer NN, Wilks JC, Marlow JJ, Coleman ML, Newman DK. 2012. BqsR/BqsS constitute a two-component system that senses extracellular Fe(II) in Pseudomonas aeruginosa. J. Bacteriol. 194:1195-1204.
33. Konings AF, Martin LW, Sharples KJ, Roddam LF, Latham R, Reid DW, Lamont IL. 2013. Pseudomonas aeruginosa uses multiple pathways to acquire iron during chronic infection in cystic fibrosis lungs. Infect. Immun. 81:2697-2704.
34. Vasil ML, Ochsner UA. 1999. The response of Pseudomonas aeruginosa to iron: genetics, biochemistry, and virulence. Mol. Microbiol. 34:399-413.
35. Cornelis P, Matthijs S, Van Oeffelen L. 2009. Iron uptake regulation in Pseudomonas aeruginosa. Biometals 22:15-22.
36. Gifford AH, Moulton LA, Dorman DB, Olbina G, Westerman M, Parker HW, Stanton BA, O'Toole GA. 2012. Iron homeostasis during cystic fibrosis pulmonary exacerbation. Clin. Transl. Sci. 5:368-373.
37. Pezzulo AA, Tang XX, Hoegger MJ, Alaiwa MH, Ramachandran S, Moninger TO, Karp PH, Wohlford-Lenane CL, Haagsman HP, van Eijk M, Bánfi B, Horswill AR, Stoltz DA, McCray PB, Welsh MJ, Zabner J. 2012. Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung. Nature 487:109-115.
38. Panter SS. 1994. Release of iron from hemoglobin. Methods Enzymol. 231:502-514.
39. Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman LR, D'Argenio DA, Miller SI, Ramsey BW, Speert DP, Moskowitz SM, Burns JL, Kaul R, Olson MV. 2006. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc. Natl. Acad. Sci. U. S. A. 103:8487-8492.
40. Chen X, Stewart PS. 2002. Role of electrostatic interactions in cohesion of bacterial biofilms. Appl. Microbiol. Biotechnol. 59:718-720.
41. Musk DJ, Banko DA, Hergenrother PJ. 2005. Iron salts perturb biofilm formation and disrupt existing biofilms of Pseudomonas aeruginosa. Chem. Biol. 12:789-796.
42. Donlan RM, Costerton JW. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15:167-193.
43. Hill D, Rose B, Pajkos A, Robinson M, Bye P, Bell S, Elkins M, Thompson B, MacLeod C, Aaron SD. Harbour C. 2005. Antibiotic susceptibilities of Pseudomonas aeruginosa isolates derived from patients with cystic fibrosis under aerobic, anaerobic, and biofilm conditions. J. Clin. Microbiol. 43:5085-5090.
44. Miller MR, Crapo R, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, Enright P, van der Grinten CP, Gustafsson P, Jensen R, Johnson DC, MacIntyre N, McKay R, Navajas D, Pedersen OF, Pellegrino R, Viegi G, Wanger J, ATS/ERS Task Force. 2005. General considerations for lung function testing. Eur. Respir. J. 26:153-161.
45. Flume PA, O'Sullivan BP, Robinson KA, Goss CH, Mogayzel PJ, Willey-Courand DB, Bujan J, Finder J, Lester M, Quittell L, Rosenblatt R, Vender RL, Hazle L, Sabadosa K, Marshall B, Cystic Fibrosis Foundation, Pulmonary Therapies Committee. 2007. Cystic fibrosis pulmonary guidelines: chronic medications for maintenance of lung health. Am. J. Respir. Crit. Care Med. 176:957-969.
46. Lovley DR, Phillips EJ. 1987. Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl. Environ. Microbiol. 53:1536-1540.
47. Lim YW, Schmieder R, Haynes M, Furlan M, Willner D, Abbott K, Edwards R, Evangelista J, Conrad D, Rohwer F. 2012. Metagenomics and metatranscriptomics: Windows on CF-associated viral and microbial communities. J. Cyst. Fibros. 12:154-164.
48. De Vos D, Lim A, Jr, Pirnay JP, Struelens M, Vandenvelde C, Duinslaeger L, Vanderkelen A, Cornelis P. 1997. Direct detection and identification of Pseudomonas aeruginosa in clinical samples such as skin biopsy specimens and expectorations by multiplex PCR based on two outer membrane lipoprotein genes, oprI and oprL. J. Clin. Microbiol. 35: 1295-1299.
49. Wolfgang MC, Jyot J, Goodman AL, Ramphal R, Lory S. 2004. Pseudomonas aeruginosa regulates flagellin expression as part of a global response to airway fluid from cystic fibrosis patients. Proc. Natl. Acad. Sci. U. S. A. 101:6664-6668.
50. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T) method. Methods 25:402-408.
51. Tomlin KL, Malott RJ, Ramage G, Storey DG, Sokol PA, Ceri H. 2005. Quorum-sensing mutations affect attachment and stability of Burkholderia cenocepacia biofilms. Appl. Environ. Microbiol. 71:5208-5218.
52. Martin LW, Reid DW, Sharples KJ, Lamont IL. 2011. Pseudomonas siderophores in the sputum of patients with cystic fibrosis. Biometals 24: 1059-1067.