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. 1996 Dec;64(12):5417–5420. doi: 10.1128/iai.64.12.5417-5420.1996

Adhesion of Pseudomonas aeruginosa to respiratory mucins and expression of mucin-binding proteins are increased by limiting iron during growth.

A Scharfman 1, H Kroczynski 1, C Carnoy 1, E Van Brussel 1, G Lamblin 1, R Ramphal 1, P Roussel 1
PMCID: PMC174541  PMID: 8945599

Abstract

The attachment of Pseudomonas aeruginosa to human respiratory mucus represents an important step in the development of lung infection, especially in cystic fibrosis. Local factors in the respiratory tract, such as osmolarity or iron concentration, might influence this colonization. In the present work, we have observed that overall levels of adhesion of two nonmucoid, nonpiliated strains of P. aeruginosa, 1244-NP and PAK-NP, to human airway mucins were higher when these strains were grown in a minimal medium of low osmolarity (M9) than when they were grown in a rich medium of higher osmolarity (tryptic soy broth [TSB]). However, increasing the NaCl concentration of M9 to increase the osmolarity did not modify the level of binding. In order to find out whether these differences were due to variations in nutrients, the influence of iron concentration was investigated: the levels of binding of the two strains increased after TSB was depleted of iron and decreased after iron was added to M9. Since the outer membranes from the two strains have been shown to contain proteins reacting with human bronchial mucins, we compared the mucin-binding proteins expressed by the two strains grown in different media. When the nonpiliated strains 1244-NP and PAK-NP were grown in the different media, previously observed mucin-binding bands were detected in the 42- to 48-kDa range but additional mucin-binding bands in the 77- to 85-kDa range were detected when these strains were grown in M9 or iron-deprived TSB. These results demonstrate that the adhesion of P. aeruginosa and the expression of mucin-binding proteins in the outer membranes of nonpiliated P. aeruginosa are affected by the iron content of the medium in which the bacteria are grown and not by the osmolarity.

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Selected References

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  1. Ankenbauer R. G. Cloning of the outer membrane high-affinity Fe(III)-pyochelin receptor of Pseudomonas aeruginosa. J Bacteriol. 1992 Jul;174(13):4401–4409. doi: 10.1128/jb.174.13.4401-4409.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Berry A., DeVault J. D., Chakrabarty A. M. High osmolarity is a signal for enhanced algD transcription in mucoid and nonmucoid Pseudomonas aeruginosa strains. J Bacteriol. 1989 May;171(5):2312–2317. doi: 10.1128/jb.171.5.2312-2317.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bowes D., Clark A. E., Corrin B. Ultrastructural localisation of lactoferrin and glycoprotein in human bronchial glands. Thorax. 1981 Feb;36(2):108–115. doi: 10.1136/thx.36.2.108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cacalano G., Kays M., Saiman L., Prince A. Production of the Pseudomonas aeruginosa neuraminidase is increased under hyperosmolar conditions and is regulated by genes involved in alginate expression. J Clin Invest. 1992 Jun;89(6):1866–1874. doi: 10.1172/JCI115791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cantin A. Cystic fibrosis lung inflammation: early, sustained, and severe. Am J Respir Crit Care Med. 1995 Apr;151(4):939–941. doi: 10.1164/ajrccm.151.4.7697269. [DOI] [PubMed] [Google Scholar]
  6. Carnoy C., Ramphal R., Scharfman A., Lo-Guidice J. M., Houdret N., Klein A., Galabert C., Lamblin G., Roussel P. Altered carbohydrate composition of salivary mucins from patients with cystic fibrosis and the adhesion of Pseudomonas aeruginosa. Am J Respir Cell Mol Biol. 1993 Sep;9(3):323–334. doi: 10.1165/ajrcmb/9.3.323. [DOI] [PubMed] [Google Scholar]
  7. Carnoy C., Scharfman A., Van Brussel E., Lamblin G., Ramphal R., Roussel P. Pseudomonas aeruginosa outer membrane adhesins for human respiratory mucus glycoproteins. Infect Immun. 1994 May;62(5):1896–1900. doi: 10.1128/iai.62.5.1896-1900.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Clamp J. R., Creeth J. M. Some non-mucin components of mucus and their possible biological roles. Ciba Found Symp. 1984;109:121–136. doi: 10.1002/9780470720905.ch9. [DOI] [PubMed] [Google Scholar]
  9. Devaraj N., Sheykhnazari M., Warren W. S., Bhavanandan V. P. Differential binding of Pseudomonas aeruginosa to normal and cystic fibrosis tracheobronchial mucins. Glycobiology. 1994 Jun;4(3):307–316. doi: 10.1093/glycob/4.3.307. [DOI] [PubMed] [Google Scholar]
  10. Haas B., Kraut J., Marks J., Zanker S. C., Castignetti D. Siderophore presence in sputa of cystic fibrosis patients. Infect Immun. 1991 Nov;59(11):3997–4000. doi: 10.1128/iai.59.11.3997-4000.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hancock R. E., Poole K., Benz R. Outer membrane protein P of Pseudomonas aeruginosa: regulation by phosphate deficiency and formation of small anion-specific channels in lipid bilayer membranes. J Bacteriol. 1982 May;150(2):730–738. doi: 10.1128/jb.150.2.730-738.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hancock R. E., Siehnel R., Martin N. Outer membrane proteins of Pseudomonas. Mol Microbiol. 1990 Jul;4(7):1069–1075. doi: 10.1111/j.1365-2958.1990.tb00680.x. [DOI] [PubMed] [Google Scholar]
  13. Heinrichs D. E., Young L., Poole K. Pyochelin-mediated iron transport in Pseudomonas aeruginosa: involvement of a high-molecular-mass outer membrane protein. Infect Immun. 1991 Oct;59(10):3680–3684. doi: 10.1128/iai.59.10.3680-3684.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Jacques M., Bélanger M., Diarra M. S., Dargis M., Malouin F. Modulation of Pasteurella multocida capsular polysaccharide during growth under iron-restricted conditions and in vivo. Microbiology. 1994 Feb;140(Pt 2):263–270. doi: 10.1099/13500872-140-2-263. [DOI] [PubMed] [Google Scholar]
  15. Jaffar-Bandjee M. C., Lazdunski A., Bally M., Carrère J., Chazalette J. P., Galabert C. Production of elastase, exotoxin A, and alkaline protease in sputa during pulmonary exacerbation of cystic fibrosis in patients chronically infected by Pseudomonas aeruginosa. J Clin Microbiol. 1995 Apr;33(4):924–929. doi: 10.1128/jcm.33.4.924-929.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Joris L., Dab I., Quinton P. M. Elemental composition of human airway surface fluid in healthy and diseased airways. Am Rev Respir Dis. 1993 Dec;148(6 Pt 1):1633–1637. doi: 10.1164/ajrccm/148.6_Pt_1.1633. [DOI] [PubMed] [Google Scholar]
  17. LeGeros R. Z., Orly I., LeGeros J. P., Gomez C., Kazimiroff J., Tarpley T., Kerebel B. Scanning electron microscopy and electron probe microanalyses of the crystalline components of human and animal dental calculi. Scanning Microsc. 1988 Mar;2(1):345–356. [PubMed] [Google Scholar]
  18. Masson P. L., Heremans J. F., Schonne E. Lactoferrin, an iron-binding protein in neutrophilic leukocytes. J Exp Med. 1969 Sep 1;130(3):643–658. doi: 10.1084/jem.130.3.643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ochsner U. A., Vasil A. I., Vasil M. L. 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. 1995 Dec;177(24):7194–7201. doi: 10.1128/jb.177.24.7194-7201.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Prince R. W., Cox C. D., Vasil M. L. Coordinate regulation of siderophore and exotoxin A production: molecular cloning and sequencing of the Pseudomonas aeruginosa fur gene. J Bacteriol. 1993 May;175(9):2589–2598. doi: 10.1128/jb.175.9.2589-2598.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ramphal R., Carnoy C., Fievre S., Michalski J. C., Houdret N., Lamblin G., Strecker G., Roussel P. Pseudomonas aeruginosa recognizes carbohydrate chains containing type 1 (Gal beta 1-3GlcNAc) or type 2 (Gal beta 1-4GlcNAc) disaccharide units. Infect Immun. 1991 Feb;59(2):700–704. doi: 10.1128/iai.59.2.700-704.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ramphal R., Guay C., Pier G. B. Pseudomonas aeruginosa adhesins for tracheobronchial mucin. Infect Immun. 1987 Mar;55(3):600–603. doi: 10.1128/iai.55.3.600-603.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ramphal R., Koo L., Ishimoto K. S., Totten P. A., Lara J. C., Lory S. Adhesion of Pseudomonas aeruginosa pilin-deficient mutants to mucin. Infect Immun. 1991 Apr;59(4):1307–1311. doi: 10.1128/iai.59.4.1307-1311.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ramphal R., Pyle M. Evidence for mucins and sialic acid as receptors for Pseudomonas aeruginosa in the lower respiratory tract. Infect Immun. 1983 Jul;41(1):339–344. doi: 10.1128/iai.41.1.339-344.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Reddy M. S. Human tracheobronchial mucin: purification and binding to Pseudomonas aeruginosa. Infect Immun. 1992 Apr;60(4):1530–1535. doi: 10.1128/iai.60.4.1530-1535.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Simel D. L., Mastin J. P., Pratt P. C., Wisseman C. L., Shelburne J. D., Spock A., Ingram P. Scanning electron microscopic study of the airways in normal children and in patients with cystic fibrosis and other lung diseases. Pediatr Pathol. 1984;2(1):47–64. doi: 10.3109/15513818409041187. [DOI] [PubMed] [Google Scholar]
  27. Simpson D. A., Ramphal R., Lory S. Genetic analysis of Pseudomonas aeruginosa adherence: distinct genetic loci control attachment to epithelial cells and mucins. Infect Immun. 1992 Sep;60(9):3771–3779. doi: 10.1128/iai.60.9.3771-3779.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Thompson A. B., Bohling T., Payvandi F., Rennard S. I. Lower respiratory tract lactoferrin and lysozyme arise primarily in the airways and are elevated in association with chronic bronchitis. J Lab Clin Med. 1990 Feb;115(2):148–158. [PubMed] [Google Scholar]
  29. Vishwanath S., Ramphal R. Adherence of Pseudomonas aeruginosa to human tracheobronchial mucin. Infect Immun. 1984 Jul;45(1):197–202. doi: 10.1128/iai.45.1.197-202.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Yates J. M., Morris G., Brown M. R. Effect of iron concentration and growth rate on the expression of protein G in Pseudomonas aeruginosa. FEMS Microbiol Lett. 1989 Apr;49(2-3):259–262. doi: 10.1016/0378-1097(89)90049-9. [DOI] [PubMed] [Google Scholar]

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