Flagellum-mediated biofilm defense mechanisms of Pseudomonas aeruginosa against host-derived lactoferrin

Infection and Immunity

Volumn 77, Issue 10, 2009, Pages 4559-4566

  Leid, Jeff G ^a   Kerr, Mathias ^a   Selgado, Candice ^a   Johnson, Chelsa ^a   Moreno, Gabriel ^a   Smith, Alyssa ^a   Shirtliff, Mark E ^b   O'Toole, George A ^c   Cope, Emily K ^a  

^a NORTHERN ARIZONA UNIVERSITY   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

^c DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LACTOFERRIN; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BACTERIAL GENE; BACTERIAL MUTATION; BACTERIAL STRAIN; BACTERIAL VIABILITY; BACTERICIDAL ACTIVITY; BIOFILM; CELL ISOLATION; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOKINE RELEASE; FLAGELLUM; GENE DISRUPTION; HOST RESISTANCE; HUMAN; HUMAN CELL; INNATE IMMUNITY; LEUKOCYTE; LEUKOCYTE ACTIVATION; LYMPHOCYTE; MICROTITER PLATE ASSAY; MONOCYTE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROVOCATION TEST; PSEUDOMONAS AERUGINOSA;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BIOFILMS; CARRIER PROTEINS; COLONY COUNT, MICROBIAL; FLAGELLA; GENE DELETION; HUMANS; LACTOFERRIN; LEUKOCYTES; MICROBIAL VIABILITY; PSEUDOMONAS AERUGINOSA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 70349420951     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00075-09     Document Type: Article

References (57)

1. Anderson, G. G., S. Moreau-Marquis, B. A. Stanton, and G. A. O'Toole. 2008. In vitro analysis of tobramycin-treated Pseudomonas aeruginosa biofilms on cystic fibrosis-derived airway epithelial cells. Infect. Immun. 76: 1423-1433.
2. Archibald, L. K., and R. P. Gaynes. 1997. Hospital-acquired infections in the United States. The importance of interhospital comparisons. Infect. Dis. Clin. N. Am. 11:245-255.
3. Bellamy, W., M. Takase, K. Yamauchi, H. Wakabayashi, K. Kawase, and M. Tomita. 1992. Identification of the bactericidal domain of lactoferrin. Biochim. Biophys. Acta 1121:130-136.
4. Bellone, M., A. Mondino, and A. Corti. 2008. Vascular targeting, chemotherapy and active immunotherapy: teaming up to attack cancer. Trends Immunol. 29:235-241.
5. Bielecki, P., J. Glik, M. Kawecki, and V. A. Martins dos Santos. 2008. Towards understanding Pseudomonas aeruginosa burn wound infections by profiling gene expression. Biotechnol. Lett. 30:777-790.
6. Bjarnsholt, T., P. O. Jensen, M. Burmolle, M. Hentzer, J. A. Haagensen, H. P. Hougen, H. Calum, K. G. Madsen, C. Moser, S. Molin, N. Hoiby, and M. Givskov. 2005. Pseudomonas aeruginosa tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum-sensing dependent. Microbiology 151:373-383.
7. Bjarnsholt, T., K. Kirketerp-Moller, P. O. Jensen, K. G. Madsen, R. Phipps, K. Krogfelt, N. Hoiby, and M. Givskov. 2008. Why chronic wounds will not heal: a novel hypothesis. Wound Repair Regen. 16:2-10.
8. Boehm, U., T. Klamp, M. Groot, and J. C. Howard. 1997. Cellular responses to interferon-gamma. Annu. Rev. Immunol. 15:749-795.
9. Chmiel, J. F., and P. B. Davis. 2003. State of the art: why do the lungs of patients with cystic fibrosis become infected and why can't they clear the infection? Respir. Res. 4:8.
10. Collins, D. P., B. J. Luebering, and D. M. Shaut. 1998. T-lymphocyte functionality assessed by analysis of cytokine receptor expression, intracellular cytokine expression, and femtomolar detection of cytokine secretion by quantitative flow cytometry. Cytometry 33:249-255.
11. Conway, S. P., K. G. Brownlee, M. Denton, and D. G. Peckham. 2003. Antibiotic treatment of multidrug-resistant organisms in cystic fibrosis. Am. J. Respir. Med. 2:321-332.
12. Costerton, J. W., P. S. Stewart, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322. (Pubitemid 29289651)
13. Costerton, J. W. 2001. Cystic fibrosis pathogenesis and the role of biofilms in persistent infections. Trends Microbiol. 9:50-52. (Pubitemid 32155317)
14. Costerton, J. W. 2002. Anaerobic biofilm infections in cystic fibrosis. Mol. Cell 10:699-700. (Pubitemid 35335624)
15. Dasgupta, M. K., P. Zuberbuhler, A. Abbi, F. L. Harley, N. E. Brown, K. Lam, J. B. Dossetor, and J. W. Costerton. 1987. Combined evaluation of circulating immune complexes and antibodies to Pseudomonas aeruginosa as an immunologic profile in relation to pulmonary function in cystic fibrosis. J. Clin. Immunol. 7:51-58.
16. Ellis, T. N., and B. L. Beaman. 2004. Interferon-gamma activation of polymorphonuclear neutrophil function. Immunology 112:2-12.
17. Farnaud, S., and R. W. Evans. 2003. Lactoferrin - a multifunctional protein with antimicrobial properties. Mol. Immunol. 40:395-405.
18. Faurschou, M., and N. Borregaard. 2003. Neutrophil granules and secretory vesicles in inflammation. Microbes Infect. 5:1317-1327. (Pubitemid 37410245)
19. Fux, C., S. Wilson, and P. Stoodley. 2004. Detachment characteristics and oxacillin resistance of Staphylococcus aureus biofilm emboli in an in vitro catheter infection model. J. Bacteriol. 186:4486-4491.
20. Germiller, J. A., H. K. El-Kashlan, and U. K. Shah. 2005. Chronic Pseudomonas infection of cochlear implants. Otol. Neurotol. 26:196-201.
21. Govan, J. R. W., and V. Deretic. 1996. Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol. Rev. 60:539-574.
22. Govan, J. R., and J. A. Fyfe. 1978. Mucoid Pseudomonas aeruginosa and cystic fibrosis: resistance of the mucoid form to carbenicillin, flucloxacillin and tobramycin and the isolation of mucoid variants in vitro. J. Antimicrob. Chemother. 4:233-240.
23. Hoiby, N., H. Krogh Johansen, C. Moser, Z. Song, O. Ciofu, and A. Kharazmi. 2001. Pseudomonas aeruginosa and the in vitro and in vivo biofilm mode of growth. Microbes Infect. 3:23-35.
24. Homma, M., D. J. DeRosier, and R. M. Macnab. 1990. Flagellar hook and hook-associated proteins of Salmonella typhimurium and their relationship to other axial components of the flagellum. J. Mol. Biol. 213:819-832.
25. Irvin, R. T., J. W. Govan, J. A. Fyfe, and J. W. Costerton. 1981. Heterogeneity of antibiotic resistance in mucoid isolates of Pseudomonas aeruginosa obtained from cystic fibrosis patients: role of outer membrane proteins. Antimicrob. Agents Chemother. 19:1056-1063.
26. Jensen, E. T., A. Kharazmi, K. Lam, J. W. Costerton, and N. Hoiby. 1990. Human polymorphonuclear leukocyte response to Pseudomonas aeruginosa grown in biofilms. Infect. Immun. 58:2383-2386.
27. Jensen, E. T., A. Kharazmi, N. Hoiby, and J. W. Costerton. 1992. Some bacterial parameters influencing the neutrophil oxidative burst response to Pseudomonas aeruginosa biofilms. APMIS 100:727-733.
28. Jensen, P. O., T. Bjarnsholt, R. Phipps, T. B. Rasmussen, H. Calum, L. Christoffersen, C. Moser, P. Williams, T. Pressler, M. Givskov, and N. Hoiby. 2007. Rapid necrotic killing of polymorphonuclear leukocytes is caused by quorum-sensing-controlled production of rhamnolipid by Pseudomonas aeruginosa. Microbiology 153:1329-1338.
29. Jesaitis, A. J., M. J. Franklin, D. Berglund, M. Sasaki, C. I. Lord, J. B. Bleazard, J. E. Duffy, H. Beyenal, and Z. Lewandowski. 2003. Compromised host defense on Pseudomonas aeruginosa biofilms: characterization of neutrophil and biofilm interactions. J. Immunol. 171:4329-4339.
30. Kelley, T. J., and M. L. Drumm. 1998. Inducible nitric oxide synthase expression is reduced in cystic fibrosis murine and human airway epithelial cells. J. Clin. Investig. 102:1200-1207.
31. Kirketerp-Moller, K., P. O. Jensen, M. Fazli, K. G. Madsen, J. Pederson, C. Moser, T. Tolker-Nielsen, N. Hoiby, M. Givskov, and T. Bjarnsholt. 2008. Distribution, organization, and ecology of bacteria in chronic wounds. J. Clin. Microbiol. 46:2717-2722.
32. Koch, C., and N. Hoiby. 2000. Diagnosis and treatment of cystic fibrosis. Respiration 67:239-247.
33. Lam, J., R. Chan, K. Lam, and J. W. Costerton. 1980. Production of mucoid microcolonies by Pseudomonas aeruginosa with infected lungs in cystic fibrosis. Infect. Immun. 28:546-556.
34. Lee, B., J. A. Haagensen, O. Ciofu, J. B. Andersen, N. Hoiby, and S. Molin. 2005. Heterogeneity of biofilms formed by nonmucoid Pseudomonas aeruginosa isolates from patients with cystic fibrosis. J. Clin. Microbiol. 43:5247-5255.
35. Leid, J. G., C. J. Willson, M. E. Shirtliff, D. J. Hassett, M. R. Parsek, and A. K. Jeffers. 2005. The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-gamma-mediated macrophage killing. J. Immunol. 175:7512-7518.
36. Leid, J. G., M. E. Shirtliff, J. W. Costerton, and P. Stoodley. 2002. Human leukocytes adhere, penetrate and respond to Staphylococcus aureus biofilms. Infect. Immun. 70:6339-6345.
37. Li, Y., A. Karlin, J. D. Loike, and S. C. Silverstein. 2002. A critical concentration of neutrophils is required for effective bacterial killing in suspension. Proc. Natl. Acad. Sci. USA 99:8289-8294.
38. Liberati, N. T., J. M. Urbach, S. Miyata, D. G. Lee, E. Drenkard, G. Wu, J. Villanueva, T. Wei, and F. M. Ausubel. 2006. An ordered, non-redundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc. Natl. Acad. Sci. USA 103:2833-2838.
39. Lyczak, J. B., C. L. Cannon, and G. B. Pier. 2002. Lung infections associated with cystic fibrosis. Clin. Microbiol. Rev. 15:194-222.
40. Mah, T. F., and G. A. O'Toole. 2001. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 9:34-39. (Pubitemid 32467503)
41. Murga, R., J. M. Miller, and R. M. Donlan. 2001. Biofilm formation by gram-negative bacteria on central venous catheter connectors: effect of conditioning films in a laboratory model. J. Clin. Microbiol. 39:2294-2297.
42. Nemmar, A., B. Nemery, P. H. Hoet, N. Van Rooijen, and M. F. Hoylaerts. 2005. Silica particles enhance peripheral thrombosis: key role of lung macrophage- neutrophil cross-talk. Am. J. Respir. Crit. Care Med. 171:872-879.
43. Orsi, N. 2004. The antimicrobial activity of lactoferrin: current status and perspectives. BioMetals 17:189-196. (Pubitemid 38987136)
44. O'Toole, G., H. B. Kaplan, and R. Kolter. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:49-79.
45. O'Toole, G. A., and R. Kolter. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295-304.
46. Rumbaugh, K. P., J. A. Griswold, and A. N. Hamood. 2000. The role of quorum sensing in the in vivo virulence of Pseudomonas aeruginosa. Microbes Infect. 2:1721-1731.
47. Sadikot, R. T., T. S. Blackwell, J. W. Christman, and A. S. Prince. 2005. Pathogen-host interactions in Pseudomonas aeruginosa pneumonia. Am. J. Respir. Crit. Care Med. 171:1209-1223.
48. Sauer, K., A. K. Camper, G. D. Ehrlich, J. W. Costerton, and D. G. Davies. 2002. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J. Bacteriol. 184:1140-1154.
49. Sauer, K., and A. K. Camper. 2001. Characterization of phenotypic changes in Pseudomonas putida in response to surface-associated growth. J. Bacteriol. 183:6579-6589.
50. Schaber, J. A., W. J. Trifflo, S. J. Suh, J. W. Oliver, M. C. Hastert, J. A. Griswold, M. Auer, A. N. Hamood, and K. P. Rumbaugh. 2007. Pseudomonas aeruginosa forms biofilms in acute infection independent of cell-to-cell signaling. Infect. Immun. 75:3715-3721.
51. Schierholz, J. M., and J. Beuth. 2001. Implant infections: a haven for opportunistic bacteria. J. Hosp. Infect. 49:87-93.
52. Singh, P. K., M. R. Parsek, E. P. Greenberg, and M. J. Welsh. 2002. A component of innate immunity prevents bacterial biofilm development. Nature 417:552-555.
53. Singh, P. K., A. L. Schaefer, M. R. Parsek, T. O. Moninger, M. J. Welsh, and E. P. Greenberg. 2000. Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407:762-764.
54. Stewart, P. S., and J. W. Costerton. 2001. Antibiotic resistance of bacteria in biofilms. Lancet 358:135-138.
55. Walker, T. S., K. L. Tomlin, G. S. Worthen, K. R. Poch, J. G. Lieber, M. T. Saaverdra, M. B. Fessler, K. C. Malcolm, M. L. Vasil, and J. A. Nick. 2005. Enhanced Pseudomonas aeruginosa biofilm development mediated by human neutrophils. Infect. Immun. 73:3693-3701.
56. Wu, L., O. Estrada, A. Zaborina, M. Bains, L. Shen, J. E. Kohler, N. Patel, M. W. Musch, E. B. Chang, Y.-X. Fu, M. A. Jacobs, M. I. Nishimura, R. E. W. Hancock, J. R. Turner, and J. C. Alverdy. 2005. Recognition of host immune activation by Pseudomonas aeruginosa. Science 309:774-777.
57. Yang, L., J. A. Haagensen, L. Jelsbak, H. K. Johansen, C. Sternberg, N. Hoiby, and S. Molin. 2008. In situ growth rates and biofilm development of Pseudomonas aeruginosa populations in chronic lung infections. J. Bacteriol. 190:2767-2776.