Cyclic voltammetric, fluorescence and biological analysis of purified aeruginosin A, a secreted red pigment of Pseudomonas aeruginosa PAO

Microbiology (United Kingdom)

Volumn 159, Issue 8, 2013, Pages 1736-1747

  Abu, Eme A ^a   Su, Shengchang ^b   Sallans, Larry ^a   Boissy, Raymond E ^b   Greatens, Amanda ^b   Heineman, William R ^a   Hassett, Daniel J ^b  

^a UNIVERSITY OF CINCINNATI   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 6 CARBOXY 10 METHYLPHENAZINIUM BETAINE; AERUGINOSIN A; BACTERIAL PROTEIN; CARBON; PIGMENT; PYOCYANINE; TOXIN; UNCLASSIFIED DRUG;

ARTICLE; BURN; CHEMICAL COMPOSITION; CYCLIC POTENTIOMETRY; CYSTIC FIBROSIS; CYTOTOXICITY; ELECTRIC POTENTIAL; ELECTROCHEMISTRY; ELECTRODE; ESCHERICHIA COLI; FLUORESCENCE; IN VITRO STUDY; KERATINOCYTE; MASS SPECTROMETRY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NONHUMAN; OXIDATION REDUCTION REACTION; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PURIFICATION; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; QUORUM SENSING;

CELLS, CULTURED; ELECTROCHEMISTRY; ESCHERICHIA COLI; FLUORESCENCE; HUMANS; KERATINOCYTES; MASS SPECTROMETRY; ORGANIC CHEMICALS; OXIDATION-REDUCTION; PIGMENTS, BIOLOGICAL; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; STAPHYLOCOCCUS AUREUS;

EID: 84881221961     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.065235-0     Document Type: Article

References (57)

1. Abusriwil, H. & Stockley, R. A. (2007). The interaction of host and pathogen factors in chronic obstructive pulmonary disease exacerbations and their role in tissue damage. Proc Am Thorac Soc 4, 611-617.
2. Bauer, A. W., Perry, D. M. & Kirby, W. M. (1959). Single-disk antibiotic-sensitivity testing of staphylococci; an analysis of technique and results. AMA Arch Intern Med 104, 208-216.
3. BBC (2008). Europe-wide food colour ban call. BBC News Thursday 10 April 2008.
4. Blazevic, D. J., Koepcke, M. H. & Matsen, J. M. (1973). Incidence and identification of Pseudomonas fluorescens and Pseudomonas putida in the clinical laboratory. Appl Microbiol 25, 107-110.
5. Brint, J. M. & Ohman, D. E. (1995). Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of RhlR-RhlI, another set of regulators in strain PAO1 with homology to the autoinducerresponsive LuxR-LuxI family. J Bacteriol 177, 7155-7163.
6. Brown, V. I. & Lowbury, E. J. (1965). Use of an improved cetrimide agar medium and other culture methods for Pseudomonas aeruginosa. J Clin Pathol 18, 752-756.
7. Byng, G. S., Eustice, D. C. & Jensen, R. A. (1979). Biosynthesis of phenazine pigments in mutant and wild-type cultures of Pseudomonas aeruginosa. J Bacteriol 138, 846-852.
8. Centers for Disease Control and Prevention. (2003). Methicillinresistant Staphylococcus aureus infections among competitive sports participants-Colorado, Pennsylvania, and Los Angeles County, 2000-2003. MMWR Morb Mortal Wkly Rep 52, 793-795. Medline.
9. Chotirmall, S. H., O'Donoghue, E., Bennett, K., Gunaratnam, C., O'Neill, S. J. & McElvaney, N. G. (2010). Sputum Candida albicans presages FEV? decline and hospital-treated exacerbations in cystic fibrosis. Chest 138, 1186-1195.
10. Cox, C. D. (1979). Isolation of an iron-binding compound from Pseudomonas aeruginosa. J Bacteriol 137, 357-364.
11. Cox, C. D. (1986). Role of pyocyanin in the acquisition of iron from transferrin. Infect Immun 52, 263-270.
12. Fineran, P. C., Williamson, N. R., Lilley, K. S. & Salmond, G. P. (2007). Virulence and prodigiosin antibiotic biosynthesis in Serratia are regulated pleiotropically by the GGDEF/EAL domain protein, PigX. J Bacteriol 189, 7653-7662.
13. Flugge, K. F. W. (1886). Die Mikroorganismen. F C W Vogel, Leipzig 2 Aufl 1-692.
14. Gibson, J., Sood, A. & Hogan, D. A. (2009). Pseudomonas aeruginosa-Candida albicans interactions: localization and fungal toxicity of a phenazine derivative. Appl Environ Microbiol 75, 504-513.
15. Hansford, G. S., Holliman, F. G. & Herbert, R. B. (1972). Pigments of Pseudomonas species. IV. In vitro and in vivo conversion of 5-methylphenazinium-1-carboxylate into aeruginosin A. J Chem Soc Perkin 1 1, 103-105.
16. Hassan, H. M. & Fridovich, I. (1980). Mechanism of the antibiotic action pyocyanine. J Bacteriol 141, 156-163.
17. Hassett, D. J., Charniga, L., Bean, K. A., Ohman, D. E. & Cohen, M. S. (1992). Response of Pseudomonas aeruginosa to pyocyanin: mechanisms of resistance, antioxidant defenses, and demonstration of a manganese-cofactored superoxide dismutase. Infect Immun 60, 328-336.
18. Hassett, D. J., Ma, J.-F., Elkins, J. G., McDermott, T. R., Ochsner, U. A., West, S. E., Huang, C. T., Fredericks, J., Burnett, S. & other authors (1999). Quorum sensing in Pseudomonas aeruginosa controls expression of catalase and superoxide dismutase genes and mediates biofilm susceptibility to hydrogen peroxide. Mol Microbiol 34, 1082-1093.
19. Hassett, D. J., Ochsner, U. A., de Kievit, T. R., Iglewski, B. H., Passador, L., Livinghouse, T. S., McDermott, T. R. & Whitsett, J. A. (2002). Genetics of quorum sensing circuitry in Pseudomonas aeruginosa: implications for control of pathogenesis, biofilm formation and antibiotic/biocide resistance. In Modern Microbial Genetics, 2nd edn, pp. 261-272. Edited by U. Streips & R. Yasbin. New York: Wiley-Liss Publications.
20. Herbert, R. B. & Holliman, F. G. (1969). Pigments of pseudomonas species. II. Structure of aeruginosin B. J Chem Soc Perkin 1 18, 2517-2520.
21. Hoffman, L. R., Kulasekara, H. D., Emerson, J., Houston, L. S., Burns, J. L., Ramsey, B. W. & Miller, S. I. (2009). Pseudomonas aeruginosa lasR mutants are associated with cystic fibrosis lung disease progression. J Cyst Fibros 8, 66-70.
22. Holder, I. A. (1983). Experimental studies of the pathogenesis of infections due to Pseudomonas aeruginosa: effect of treatment with protease inhibitors. Rev Infect Dis 5 (Suppl. 5), S914-S921.
23. Holliman, F. G. (1969). Pigments of Pseudomonas species. Part I. Structure and synthesis of aeruginosin A. J Chem Soc C 19, 2514-2516.
24. Holloway, B. W. (1955). Genetic recombination in Pseudomonas aeruginosa. J Gen Microbiol 13, 572-581.
25. Jensen, R. A. & Pierson, D. L. (1975). Evolutionary implications of different types of microbial enzymology for L-tyrosine biosynthesis. Nature 254, 667-671.
26. Kandela, S. A., al-Shibib, A. S. & al-Khayat, B. H. (1997). A study of purified pyorubrin produced by local Pseudomonas aeruginosa. Acta Microbiol Pol 46, 37-43.
27. Lau, G. W., Hassett, D. J. & Britigan, B. E. (2005). Modulation of lung epithelial functions by Pseudomonas aeruginosa. Trends Microbiol 13, 389-397.
28. Lewis, J. P. (2010). Metal uptake in host-pathogen interactions: role of iron in Porphyromonas gingivalis interactions with host organisms. Periodontol 2000 52, 94-116.
29. Liu, G. Y. & Nizet, V. (2009). Color me bad: microbial pigments as virulence factors. Trends Microbiol 17, 406-413.
30. Liu, G. Y., Doran, K. S., Lawrence, T., Turkson, N., Puliti, M., Tissi, L. & Nizet, V. (2004). Sword and shield: linked group B streptococcal bhemolysin/ cytolysin and carotenoid pigment function to subvert host phagocyte defense. Proc Natl Acad Sci U S A 101, 14491-14496.
31. Liu, G. Y., Essex, A., Buchanan, J. T., Datta, V., Hoffman, H. M., Bastian, J. F., Fierer, J. & Nizet, V. (2005). Staphylococcus aureus golden pigment impairs neutrophil killing and promotes virulence through its antioxidant activity. J Exp Med 202, 209-215.
32. Loiseau-Marolleau, M. L. (1977). [Virulence of human and environmental strains of "pseudomonas aeruginosa" in mice (author's transl)]. Ann Microbiol (Paris) 128A, 61-68.
33. Mavrodi, D. V., Bonsall, R. F., Delaney, S. M., Soule, M. J., Phillips, G. & Thomashow, L. S. (2001). Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from Pseudomonas aeruginosa PAO1. J Bacteriol 183, 6454-6465.
34. Meyer, J. M., Hohnadel, D., Khan, A. & Cornelis, P. (1990). Pyoverdinfacilitated iron uptake in Pseudomonas aeruginosa: immunological characterization of the ferripyoverdin receptor. Mol Microbiol 4, 1401-1405.
35. Meyer, J.-M., Neely, A., Stintzi, A., Georges, C. & Holder, I. A. (1996). Pyoverdin is essential for virulence of Pseudomonas aeruginosa. Infect Immun 64, 518-523.
36. Morales, D. K., Jacobs, N. J., Rajamani, S., Krishnamurthy, M., Cubillos-Ruiz, J. R. & Hogan, D. A. (2010). Antifungal mechanisms by which a novel Pseudomonas aeruginosa phenazine toxin kills Candida albicans in biofilms. Mol Microbiol 78, 1379-1392.
37. Nurudeen, T. A. & Ahearn, D. G. (1979). Regulation of melanin production by Cryptococcus neoformans. J Clin Microbiol 10, 724-729.
38. Ogunnariwo, J. & Hamilton-Miller, J. M. (1975). Brown- and redpigmented Pseudomonas aeruginosa: differentiation between melanin and pyorubrin. J Med Microbiol 8, 199-203.
39. Palumbo, S. A. (1972). Role of iron and sulfur in pigment and slime formation by Pseudomonas aeruginosa. J Bacteriol 111, 430-436.
40. Pauliukaite, R., Ghica, M. E., Barsan, M. M. & Brett, C. M. A. (2010). Phanzines and polyphenazines in electrochemical sensors and biosensors. Anal Lett 43, 1588-1608.
41. Phillips, I. (1969). Identification of Pseudomonas aeruginosa in the clinical laboratory. J Med Microbiol 2, 9-16.
42. Price-Whelan, A., Dietrich, L. E. P. & Newman, D. K. (2006). Rethinking 'secondary' metabolism: physiological roles for phenazine antibiotics. Nat Chem Biol 2, 71-78.
43. Propst, C. & Lubin, L. (1979). Light-mediated changes in pigmentation of Pseudomonas aeruginosa cultures. J Gen Microbiol 113, 261-266.
44. Ramos, I., Dietrich, L. E., Price-Whelan, A. & Newman, D. K. (2010). Phenazines affect biofilm formation by Pseudomonas aeruginosa in similar ways at various scales. Res Microbiol 161, 187-191.
45. Ran, H., Hassett, D. J. & Lau, G. W. (2003). Human targets of Pseudomonas aeruginosa pyocyanin. Proc Natl Acad Sci U S A 100, 14315-14320.
46. Reszka, K. J., Xiong, Y., Sallans, L., Pasula, R., Olakanmi, O., Hassett, D. J. & Britigan, B. E. (2012). Inactivation of the potent Pseudomonas aeruginosa cytotoxin pyocyanin by airway peroxidases and nitrite. Am J Physiol Lung Cell Mol Physiol 302, L1044-L1056.
47. Saha, S., Thavasi, R. & Jayalakshmi, S. (2008). Phenazine pigments from Pseudomonas aeruginosa and their application as antibacterial agent and food colourants. Res J Microbiol 3, 122-128.
48. 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.
49. Schaber, J. A., Hammond, A., Carty, N. L., Williams, S. C., Colmer- Hamood, J. A., Burrowes, B. H., Dhevan, V., Griswold, J. A. & Hamood, A. N. (2007). Diversity of biofilms produced by quorumsensing- deficient clinical isolates of Pseudomonas aeruginosa. J Med Microbiol 56, 738-748.
50. Sherry, B. A., Alava, G., Tracey, K. J., Martiney, J., Cerami, A. & Slater, A. F. (1995). Malaria-specific metabolite hemozoin mediates the release of several potent endogenous pyrogens (TNF, MIP-1a, and MIP-1b) in vitro, and altered thermoregulation in vivo. J Inflamm 45, 85-96.
51. Takase, H., Nitanai, H., Hoshino, K. & Otani, T. (2000). Requirement of the Pseudomonas aeruginosa tonB gene for high-affinity iron acquisition and infection. Infect Immun 68, 4498-4504.
52. Thomassen, M. J., Demko, C. A., Boxerbaum, B., Stern, R. C. & Kuchenbrod, P. J. (1979). Multiple of isolates of Pseudomonas aeruginosa with differing antimicrobial susceptibility patterns from patients with cystic fibrosis. J Infect Dis 140, 873-880.
53. van Duin, D., Casadevall, A. & Nosanchuk, J. D. (2002). Melanization of Cryptococcus neoformans and Histoplasma capsulatum reduces their susceptibilities to amphotericin B and caspofungin. Antimicrob Agents Chemother 46, 3394-3400.
54. Vukomanovic, D. V., Zoutman, D. E., Stone, J. A., Marks, G. S., Brien, J. F. & Nakatsu, K. (1997). Electrospray mass-spectrometric, spectrophotometric and electrochemical methods do not provide evidence for the binding of nitric oxide by pyocyanine at pH 7. Biochem J 322, 25-29.
55. Wang, Y. & Newman, D. K. (2008). Redox reactions of phenazine antibiotics with ferric (hydr)oxides and molecular oxygen. Environ Sci Technol 42, 2380-2386.
56. Wilson, R., Sykes, D. A., Watson, D., Rutman, A., Taylor, G. W. & Cole, P. J. (1988). Measurement of Pseudomonas aeruginosa phenazine pigments in sputum and assessment of their contribution to sputum sol toxicity for respiratory epithelium. Infect Immun 56, 2515-2517.
57. Yabuuchi, E. & Ohyama, A. (1972). Characterization of "pyomelanin"- producing strains of Pseudomonas aeruginosa. Int J Syst Bacteriol 22, 53-64.