Phenazine virulence factor binding to extracellular DNA is important for Pseudomonas aeruginosa biofilm formation

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Das, Theerthankar ^a   Kutty, Samuel K ^a   Tavallaie, Roya ^a   Ibugo, Amaye I ^a   Panchompoo, Janjira ^a   Sehar, Shama ^a   Aldous, Leigh ^a   Yeung, Amanda W S ^a   Thomas, Shane R ^a   Kumar, Naresh ^a   Gooding, J Justin ^a   Manefield, Mike ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; DEOXYRIBONUCLEASE I; DNA; PHENAZINE DERIVATIVE; PROTEIN BINDING; PYOCYANINE; VIRULENCE FACTOR;

BIOFILM; CHEMISTRY; ELECTRON TRANSPORT; EXTRACELLULAR SPACE; METABOLISM; OXIDATION REDUCTION REACTION; PATHOGENICITY; PHYSIOLOGY; PSEUDOMONAS AERUGINOSA; THERMODYNAMICS; VISCOSITY;

ANTIOXIDANTS; BIOFILMS; DEOXYRIBONUCLEASE I; DNA; ELECTRON TRANSPORT; EXTRACELLULAR SPACE; OXIDATION-REDUCTION; PHENAZINES; PROTEIN BINDING; PSEUDOMONAS AERUGINOSA; PYOCYANINE; THERMODYNAMICS; VIRULENCE FACTORS; VISCOSITY;

EID: 84940855151     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep08398     Document Type: Article

References (40)

1. Pricewhelan, A., Dietrich, L. E. P. & Newman, D. K. Rethinking secondary metabolism: physiological roles for phenazine antibiotics. Nat. Chem. Biol. 2, 71-78 (2006).
2. Bjarnsholt, T. et al. Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients. Pediatr. Pulmonol 44, 547-558 (2009).
3. Bass, J. I. F. et al. Extracellular DNA: A Major proinflammatory component of Pseudomonas aeruginosa biofilms. J. Immunol. 184, 6386-6395 (2010).
4. Tredget, E. E. et al. Epidemiology of infections with Pseudomonas aeruginosa in burn patients: the role of hydrotherapy. Clin. Infect. Dis. 15, 941-949 (1992).
5. Mittal, R., Aggarwal, S., Sharma, S., Chhibber, S. & Harjai, K. Urinary tract infections caused by Pseudomonas aeruginosa: A minireview. J. Infect. Public Health 2, 101-111 (2009).
6. Busscher, H. J. et al. Biomaterial-associated infection: locating the finish line in the race for the surface. Sci. Transl. Med. 4, 153rv10 (2012).
7. Allesen-Holm, M. et al. A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol. Microbiol. 59, 1114-1128 (2006).
8. De Kievit, T. R. Quorum sensing in Pseudomonas aeruginosa biofilms. Environ. Microbiol. 11, 279-288 (2009).
9. Whitchurch, C. B., Tolker-Nielsen, T. Ragas, P. C. & Mattick, J. S. Extracellular DNA required for bacterial biofilm formation. Science 295, 1487 (2002).
10. Das, T., and Sharma., P. K., Busscher, H. J., van der Mei, H. C. & Krom, B. P. Role of extracellular DNA in initial bacterial adhesion and surface aggregation. Appl. Environ. Microbiol. 76, 3405-3408 (2010).
11. Swartjes, J. J. T. M. et al. A functional DNase I coating to prevent adhesion of bacteria and the formation of biofilm. Adv. Funct. Mat. 22, 2843-2849 (2012).
12. Das, T., and Krom., B. P., van der Mei, H. C., Busscher, H. J. & Sharma, P. K. DNAmediated bacterial aggregation is dictated by acid-base interactions. Soft Matters 7, 2927-2935 (2011).
13. Liu, H. et al. Role of DNA in bacterial aggregation. Curr. Microbiol. 57, 139-144 (2008).
14. Petersen, F. C., Tao, L. & Scheie, A. A. DNA binding-uptake system: a link between cell-to-cell communication and biofilm formation. J. Bacteriol. 187, 4392-4400 (2005).
15. Dominiak, D. M., Nielsen, J. L. & Nielsen, P. H. Extracellular DNA is abundant and important for microcolony strength in mixed microbial biofilms. Environ. Microbiol. 13, 710-721 (2011).
16. Rada, B. et al. Pyocyanin-enhanced neutrophil extracellular trap formation requires the NADPH oxidase. PLoS One 8, e54205 (2013).
17. Das, T. & Manefield, M. Pyocyanin promotes extracellular DNA release in Pseudomonas aeruginosa. PLoS One 7, e46718 (2012).
18. Shak, S., and Capon., D. J., Hellmiss, R., Marsters, S. A. & Baker, C. L. Recombinant human DNase I reduces the viscosity of cystic fibrosis sputum. Proc. Nat. Acad. Sci. USA 87, 9188-9192 (1990).
19. Kanthakumar, K. et al. Mechanisms of action of Pseudomonas aeruginosa pyocyanin on human ciliary beat in vitro. Infect. Immun. 61, 2848-2853 (1993).
20. Das, T., and Kutty., S. K., Kumar, N. & Manefield, M. Pyocyanin facilitates extracellular DNA binding to Pseudomonas aeruginosa influencing cell surface properties and aggregation. PLoS ONE 8, e58299 (2013).
21. Agarwal, S., Jangir, D. K. & Mehrotra, R. Spectroscopic studies of the effects of anticancer drug mitoxantrone interaction with calf-thymus DNA. J. Photochem. Photobiol. B: biology 120, 177-182 (2013).
22. Jangir, D. K., Tyagi, G., Mehrotra, R. & Kundu, S. Carboplatin interaction with calf-thymus DNA: a FTIR spectroscopic approach. J. Mol. Struct. 969, 126-129 (2010).
23. Alex, S. & Dupuis, P. FT-IR and Raman investigation of cadmium binding by DNA. Inorg. Chimica. Acta. 157, 271-281 (1989).
24. Jangir, D. K., and Dey., S. K., Kundu, S. & Mehrotra, R. Assessment of amsacrine binding with DNA using UV-visible, circular dichroism and Raman spectroscopic techniques. J. Photochem. Photobiol. B: biology 114, 38-43 (2012).
25. Muren, N. B., and Olmon., E. D., & Barton, J. K. Solution, surface, and single molecule platforms for the study of DNA-mediated charge transport. Phys. Chem. Chem. Phys. 14, 13754-13771 (2012).
26. Christopher, P. K., Chinweike, O., Zwoisaint, M. C., Followsd, M. J. & Dietrich, L. E. P. Morphological optimization for access to dual oxidants in biofilms. Proc. Nat. Acad. Sci. USA 111, 208-213 (2014).
27. Cheluvappa, R., Shimmon, R., Dawson, M., Hilmer, S. N. & Le Couteur, D. G. Reactions of Pseudomonas aeruginosa pyocyanin with reduced glutathione. Acta. Biochim. Pol. 55, 571-80 (2008).
28. De Vleesschauwer, D., Cornelis, P. & Höfte, M. Redox-active pyocyanin secreted by Pseudomonas aeruginosa 7NSK2 triggers systemic resistance to Magnaporthe grisea but enhances Rhizoctonia solani susceptibility in rice. Mol. Plant. Microbe. Interact. 19, 1406-1419 (2006).
29. O'Malley, Y. Q., Reszka, J. K., Spitz, D. R., Denning, G. M. & Britigan, B. E. Pseudomonas aeruginosa pyocyanin directly oxidizes glutathione and decreases its level in airway epithelial cells. Am. J. Physiol. Lung. Cell. Mol. Physiol. 287, 94-103 (2004).
30. Erdem, G., Öner, C., Önal, A. M., Kisakurek, D. & Ögus, A. Free radical mediated interaction of ascorbic acid and ascorbate/Cu(II) with viral and plasmid DNAs. J. Biosci. 19, 9-17 (1994).
31. Soos, Z. G., and Keller., H. J., Moroni, W. & Nothe, D. Phenazine cation radical salts: charge-transfer complexes with TCNQ. Annal. NY Acad. Sci. 313, 442-458 (1978).
32. Frei, B., Stocker, R. & Ames, B. N. Antioxidant defenses and lipid peroxidation in human blood plasma. Proc. Natl. Acad. Sci U S A. 85, 9748-9752 (1988).
33. Das, T., & Manefield, M. Phenazine production enhances extracellular DNA release via hydrogen peroxide generation in Pseudomonas aeruginosa. Commun. Integ. Bio. 6, e23570 (2013).
34. Fuchs, H. J. et al. Effect of Aerosolized Recombinant Human DNase on Exacerbations of Respiratory Symptoms and on Pulmonary Function in Patients with Cystic Fibrosis. N. Engl. J. Med. 331, 637-642 (1994).
35. Kostenko, V., Ceri, H. & Martinuzzi, R. J. Increased tolerance of Staphylococcus aureus to vancomycin in viscous media. FEMA Immunol. Med. Microbiol. 51, 277-288 (2007).
36. Sanders, N. N. et al. Cystic fibrosis sputum a barrier to the transport of nanospheres. Am. J. Respir. Crit. Care Med. 162, 1905-1911 (2000).
37. McGrath, L. T. et al. Oxidative stress during acute respiratory exacerbations in cystic fibrosis. Thorax. 54, 518-523 (1999).
38. Ghezzi, P. Role of glutathione in immunity and inflammation in the lung. Int. J. Gen. Med. 4, 105-113 (2011).
39. Suh, D. & Chaires, J. B. Criteria for the mode of binding of DNA binding agents. Bioorg. Med. Chem. 3, 723-728 (1995).
40. Gooding, J. J., Erokhin, P. & Hibbert, D. B. Parameters important in tuning the response of monolayer enzyme electrodes fabricated using self-assembled monolayers of alkanethiols. Biosens. Bioelectron 15, 229-239 (2000).