Burkholderia cenocepacia zinc metalloproteases influence resistance to antimicrobial peptides

Microbiology

Volumn 155, Issue 9, 2009, Pages 2818-2825

  Kooi, Cora ^a   Sokol, Pamela A ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA DEFENSIN; BACTERIAL PROTEIN; BETA DEFENSIN 1; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CATHEPSIN G; ELAFIN; ELASTASE; LEUKOCYTE ELASTASE INHIBITOR; METALLOPROTEINASE; PROTAMINE; PROTEIN ZMPA; PROTEIN ZMPB; SECRETORY LEUKOCYTE PROTEINASE INHIBITOR; UNCLASSIFIED DRUG; ZINC DEPENDENDENT METALLOPROTEINASE A; ZINC DEPENDENDENT METALLOPROTEINASE B;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL STRAIN; BURKHOLDERIA CENOCEPACIA; CONTROLLED STUDY; ENZYME INHIBITION; HOST PARASITE INTERACTION; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ALPHA-DEFENSINS; ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIAL PROTEINS; BETA-DEFENSINS; BURKHOLDERIA CEPACIA; BURKHOLDERIA INFECTIONS; DRUG RESISTANCE, BACTERIAL; ELAFIN; HUMANS; METALLOENDOPEPTIDASES; MICROBIAL SENSITIVITY TESTS; SECRETORY LEUKOCYTE PEPTIDASE INHIBITOR; SERINE PROTEINASE INHIBITORS; SUBSTRATE SPECIFICITY;

BURKHOLDERIA CENOCEPACIA;

EID: 69949173618     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.028969-0     Document Type: Article

References (66)

1. Alexander, B. D., Petzold, E. W., Reller, L. B., Palmer, S. M., Davis, R. D., Woods, C. W. & LiPuma, J. J. (2008). Survival after lung transplantation of cystic fibrosis patients infected with Burkholderia cepacia complex. Am J Transplant 8, 1025-1030.
2. Baird, R. M., Brown, H., Smith, A. W. & Watson, M. L. (1999). Burkholderia cepacia is resistant to the antimicrobial activity of airway epithelial cells. Immunopharmacology 44, 267-272.
3. Banemann, A., Deppisch, H. & Gross, R. (1998). The lipopolysaccharide of Bordetella bronchiseptica acts as a protective shield against antimicrobial peptides. Infect Immun 66, 5607-5612.
4. Belaaouaj, A., McCarthy, R., Baumann, M., Gao, Z., Ley, T. J., Abraham, S. N. & Shapiro, S. D. (1998). Mice lacking neutrophil elastase reveal impaired host defense against gram negative bacterial sepsis. Nat Med 4, 615-618.
5. Belaaouaj, A., Kim, K. S. & Shapiro, S. D. (2000). Degradation of outer membrane protein A in Escherichia coli killing by neutrophil elastase. Science 289, 1185-1188.
6. Belas, R., Manos, J. & Suvanasuthi, R. (2004). Proteus mirabilis ZapA metalloprotease degrades a broad spectrum of substrates, including antimicrobial peptides. Infect Immun 72, 5159-5167.
7. Biddick, R., Spilker, T., Martin, A. & LiPuma, J. J. (2003). Evidence of transmission of Burkholderia cepacia, Burkholderia multivorans and Burkholderia dolosa among persons with cystic fibrosis. FEMS Microbiol Lett 228, 57-62.
8. Bressler, A.M., Kaye, K. S., LiPuma, J. J., Alexander, B. D., Moore, C.M., Reller, L. B. & Woods, C.W. (2007). Risk factors for Burkholderia cepacia complex bacteremia among intensive care unit patients without cystic fibrosis: a case-control study. Infect Control Hosp Epidemiol 28, 951-958.
9. Brogden, K. A. (2005). Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3, 238-250.
10. Brown, K. L. & Hancock, R. E. (2006). Cationic host defense (antimicrobial) peptides. Curr Opin Immunol 18, 24-30.
11. Burtnick, M. N. & Woods, D. E. (1999). Isolation of polymyxin Bsusceptible mutants of Burkholderia pseudomallei and molecular characterization of genetic loci involved in polymyxin B resistance. Antimicrob Agents Chemother 43, 2648-2656.
12. Chen, J. S., Witzmann, K. A., Spilker, T., Fink, R. J. & LiPuma, J. J. (2001). Endemicity and inter-city spread of Burkholderia cepacia genomovar III in cystic fibrosis. J Pediatr 139, 643-649.
13. Coenye, T. & LiPuma, J. J. (2003). Molecular epidemiology of Burkholderia species. Front Biosci 8, e55-e67.
14. Coenye, T., Vandamme, P., Govan, J. R. & LiPuma, J. J. (2001). Taxonomy and identification of the Burkholderia cepacia complex. J Clin Microbiol 39, 3427-3436.
15. Coenye, T., Vandamme, P., LiPuma, J. J., Govan, J. R. & Mahenthiralingam, E. (2003). Updated version of the Burkholderia cepacia complex experimental strain panel. J Clin Microbiol 41, 2797-2798.
16. Cooley, J., Takayama, T. K., Shapiro, S. D., Schechter, N. M. & Remold-O'Donnell, E. (2001). The serpin MNEI inhibits elastase-like and chymotrypsin-like serine proteases through efficient reactions at two active sites. Biochemistry 40, 15762-15770.
17. Corbett, C. R., Burtnick, M. N., Kooi, C., Woods, D. E. & Sokol, P. A. (2003). An extracellular zinc metalloprotease gene of Burkholderia cepacia. Microbiology 149, 2263-2271.
18. Corey, M. & Farewell, V. (1996). Determinants of mortality from cystic fibrosis in Canada, 1970-1989. Am J Epidemiol 143, 1007-1017.
19. Cox, A. D. & Wilkinson, S. G. (1991). Ionizing groups in lipopolysaccharides of Pseudomonas cepacia in relation to antibiotic resistance. Mol Microbiol 5, 641-646.
20. Doumas, S., Kolokotronis, A. & Stefanopoulos, P. (2005). Antiinflammatory and antimicrobial roles of secretory leukocyte protease inhibitor. Infect Immun 73, 1271-1274.
21. Drevinek, P., Holden, M. T., Ge, Z., Jones, A. M., Ketchell, I., Gill, R. T. & Mahenthiralingam, E. (2008). Gene expression changes linked to antimicrobial resistance, oxidative stress, iron depletion and retained motility are observed when Burkholderia cenocepacia grows in cystic fibrosis sputum. BMC Infect Dis 8, 121.
22. Gingues, S., Kooi, C., Visser, M. B., Subsin, B. & Sokol, P. A. (2005). Distribution and expression of the ZmpA metalloprotease in the Burkholderia cepacia complex. J Bacteriol 187, 8247-8255.
23. Govan, J. R., Brown, P. H., Maddison, J., Doherty, C. J., Nelson, J. W., Dodd, M., Greening, A. P. & Webb, A. K. (1993). Evidence for transmission of Pseudomonas cepacia by social contact in cystic fibrosis. Lancet 342, 15-19.
24. Govan, J. R., Brown, A. R. & Jones, A. M. (2007). Evolving epidemiology of Pseudomonas aeruginosa and the Burkholderia cepacia complex in cystic fibrosis lung infection. Future Microbiol 2, 153-164.
25. Hansen, L. T., Austin, J. W. & Gill, T. A. (2001). Antibacterial effect of protamine in combination with EDTA and refrigeration. Int J Food Microbiol 66, 149-161.
26. Hartl, D., Latzin, P., Hordijk, P., Marcos, V., Rudolph, C., Woischnik, M., Krauss-Etschmann, S., Koller, B., Reinhardt, D. & other authors (2007). Cleavage of CXCR1 on neutrophils disables bacterial killing in cystic fibrosis lung disease. Nat Med 13, 1423-1430.
27. Hiemstra, P. S., Fernie-King, B. A., McMichael, J., Lachmann, P. J. & Sallenave, J. M. (2004). Antimicrobial peptides: mediators of innate immunity as templates for the development of novel anti-infective and immune therapeutics. Curr Pharm Des 10, 2891-2905.
28. Hwang, B. Y., Varadarajan, N., Li, H., Rodriguez, S., Iverson, B. L. & Georgiou, G. (2007). Substrate specificity of the Escherichia coli outer membrane protease OmpP. J Bacteriol 189, 522-530.
29. Isles, A., Maclusky, I., Corey, M., Gold, R., Prober, C., Fleming, P. & Levison, H. (1984). Pseudomonas cepacia infection in cystic fibrosis: an emerging problem. J Pediatr 104, 206-210.
30. Kooi, C., Corbett, C. R. & Sokol, P. A. (2005). Functional analysis of the Burkholderia cenocepacia ZmpA metalloprotease. J Bacteriol 187, 4421-4429.
31. Kooi, C., Subsin, B., Chen, R., Pohorelic, B. & Sokol, P. A. (2006). Burkholderia cenocepacia ZmpB is a broad-specificity zinc metallo-protease involved in virulence. Infect Immun 74, 4083-4093.
32. LiPuma, J. J. (2005). Update on the Burkholderia cepacia complex. Curr Opin Pulm Med 11, 528-533.
33. LiPuma, J. J., Dasen, S. E., Nielson, D. W., Stern, R. C. & Stull, T. L. (1990). Person-to-person transmission of Pseudomonas cepacia between patients with cystic fibrosis. Lancet 336, 1094-1096.
34. LiPuma, J. J., Spilker, T., Gill, L. H., Campbell, P. W., III, Liu, L. & Mahenthiralingam, E. (2001). Disproportionate distribution of Burkholderia cepacia complex species and transmissibility markers in cystic fibrosis. Am J Respir Crit Care Med 164, 92-96.
35. Loutet, S. A., Flannagan, R. S., Kooi, C., Sokol, P. A. & Valvano, M. A. (2006). A complete lipopolysaccharide inner core oligosaccharide is required for resistance of Burkholderia cenocepacia to antimicrobial peptides and bacterial survival in vivo. J Bacteriol 188, 2073-2080.
36. Mahenthiralingam, E., Coenye, T., Chung, J. W., Speert, D. P., Govan, J. R., Taylor, P. & Vandamme, P. (2000). Diagnostically and experimentally useful panel of strains from the Burkholderia cepacia complex. J Clin Microbiol 38, 910-913.
37. Mahenthiralingam, E., Urban, T. A. & Goldberg, J. B. (2005). The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 3, 144-156.
38. Mahenthiralingam, E., Baldwin, A. & Dowson, C. G. (2008). Burkholderia cepacia complex bacteria: opportunistic pathogens with important natural biology. J Appl Microbiol 104, 1539-1551.
39. McDowell, A., Mahenthiralingam, E., Dunbar, K. E., Moore, J. E., Crowe, M. & Elborn, J. S. (2004). Epidemiology of Burkholderia cepacia complex species recovered from cystic fibrosis patients: issues related to patient segregation. J Med Microbiol 53, 663-668.
40. Mookherjee, N. & Hancock, R. E. (2007). Cationic host defence peptides: innate immune regulatory peptides as a novel approach for treating infections. Cell Mol Life Sci 64, 922-933.
41. Morrison, G. M., Davidson, D. J., Kilanowski, F. M., Borthwick, D. W., Crook, K., Maxwell, A. I., Govan, J. R. & Dorin, J. R. (1998). Mouse beta defensin-1 is a functional homolog of human beta defensin-1. Mamm Genome 9, 453-457.
42. Murray, S., Charbeneau, J., Marshall, B. C. & LiPuma, J. J. (2008). Impact of Burkholderia infection on lung transplantation in cystic fibrosis. Am J Respir Crit Care Med 178, 363-371.
43. Nair, B. M., Cheung, K. J., Jr, Griffith, A. & Burns, J. L. (2004). Salicylate induces an antibiotic efflux pump in Burkholderia cepacia complex genomovar III (B. cenocepacia). J Clin Invest 113, 464-473.
44. Nair, B. M., Joachimiak, L. A., Chattopadhyay, S., Montano, I. & Burns, J. L. (2005). Conservation of a novel protein associated with an antibiotic efflux operon in Burkholderia cenocepacia. FEMS Microbiol Lett 245, 337-344.
45. Potempa, M., Potempa, J., Kantyka, T., Nguyen, K. A., Wawrzonek, K., Manandhar, S. P., Popadiak, K., Riesbeck, K., Eick, S. & Blom, A. M. (2009). Interpain A, a cysteine proteinase from Prevotella intermedia, inhibits complement by degrading complement factor C3. PLoS Pathog 5, e1000316.
46. Rees, D. D. & Brain, J. D. (1995). Effects of cystic fibrosis airway secretions on rat lung: role of neutrophil elastase. Am J Physiol 269, L195-L202.
47. + flux. Nature 416, 291-297.
48. Reik, R., Spilker, T. & LiPuma, J. J. (2005). Distribution of Burkholderia cepacia complex species among isolates recovered from persons with or without cystic fibrosis. J Clin Microbiol 43, 2926-2928.
49. Rinderknecht, H., Geokas, M. C., Silverman, P. & Haverback, B. J. (1968). A new ultrasensitive method for the determination of proteolytic activity. Clin Chim Acta 21, 197-203.
50. Sahly, H., Schubert, S., Harder, J., Rautenberg, P., Ullmann, U., Schroder, J. & Podschun, R. (2003). Burkholderia is highly resistant to human beta-defensin 3. Antimicrob Agents Chemother 47, 1739-1741.
51. Sallenave, J. M. (2000). The role of secretory leukocyte proteinase inhibitor and elafin (elastase-specific inhibitor/ skin-derived antileukoprotease) as alarm antiproteinases in inflammatory lung disease. Respir Res 1, 87-92.
52. Schagger, H. & von Jagow, G. (1987). Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166, 368-379.
53. Schmidtchen, A., Frick, I. M., Andersson, E., Tapper, H. & Bjorck, L. (2002). Proteinases of common pathogenic bacteria degrade and inactivate the antibacterial peptide LL-37. Mol Microbiol 46, 157-168.
54. Shapiro, S. D. (2002). Neutrophil elastase: path clearer, pathogen killer, or just pathologic? Am J Respir Cell Mol Biol 26, 266-268.
55. Shimomura, H., Matsuura, M., Saito, S., Hirai, Y., Isshiki, Y. & Kawahara, K. (2003). Unusual interaction of a lipopolysaccharide isolated from Burkholderia cepacia with polymyxin B. Infect Immun 71, 5225-5230.
56. Sieprawska-Lupa, M., Mydel, P., Krawczyk, K., Wójcik, K., Puklo, M., Lupa, B., Suder, P., Silberring, J., Reed, M. & other authors (2004). Degradation of human antimicrobial peptide LL-37 by Staphylococcus aureus-derived proteinases. Antimicrob Agents Chemother 48, 4673-4679.
57. Simpson, A. J., Maxwell, A. I., Govan, J. R., Haslett, C. & Sallenave, J. M. (1999). Elafin (elastase-specific inhibitor) has anti-microbial activity against gram-positive and gram-negative respiratory pathogens. FEBS Lett 452, 309-313.
58. Speert, D. P., Henry, D., Vandamme, P., Corey, M. & Mahenthiralingam, E. (2002). Epidemiology of Burkholderia cepacia complex in patients with cystic fibrosis, Canada. Emerg Infect Dis 8, 181-187.
59. Sponer, M., Nick, H. P. & Schnebli, H. P. (1991). Different susceptibility of elastase inhibitors to inactivation by proteinases from Staphylococcus aureus and Pseudomonas aeruginosa. Biol Chem Hoppe Seyler 372, 963-970.
60. Stumpe, S., Schmid, R., Stephens, D. L., Georgiou, G. & Bakker, E. P. (1998). Identification of OmpT as the protease that hydrolyzes the antimicrobial peptide protamine before it enters growing cells of Escherichia coli. J Bacteriol 180, 4002-4006.
61. Thwaite, J. E., Hibbs, S., Titball, R. W. & Atkins, T. P. (2006). Proteolytic degradation of human antimicrobial peptide LL-37 by Bacillus anthracis may contribute to virulence. Antimicrob Agents Chemother 50, 2316-2322.
62. Vandamme, P., Holmes, B., Vancanneyt, M., Coenye, T., Hoste, B., Coopman, R., Revets, H., Lauwers, S., Gillis, M. & other authors (1997). Occurrence of multiple genomovars of Burkholderia cepacia in cystic fibrosis patients and proposal of Burkholderia multivorans sp. nov. Int J Syst Bacteriol 47, 1188-1200.
63. Vanlaere, E., LiPuma, J. J., Baldwin, A., Henry, D., De Brandt, E., Mahenthiralingam, E., Speert, D., Dowson, C. & Vandamme, P. (2008). Burkholderia latens sp. nov., Burkholderia diffusa sp. nov., Burkholderia arboris sp. nov., Burkholderia seminalis sp. nov. and Burkholderia metallica sp. nov., novel species within the Burkholderia cepacia complex. Int J Syst Evol Microbiol 58, 1580-1590.
64. Vanlaere, E., Baldwin, A., Gevers, D., Henry, D, De Brandt, E., LiPuma, J. J., Mahenthiralingam, E., Speert, D. P., Dowson, C. & Vandamme, P. (2009). Taxon K, a complex within the Burkholderia cepacia complex, comprises at least two novel species, Burkholderia contaminans sp. nov. and Burkholderia lata sp. nov. Int J Syst Evol Microbiol 59, 102-111.
65. Vial, L., Groleau, M. C., Dekimpe, V. & Deziel, E. (2007). Burkholderia diversity and versatility: an inventory of the extracellular products. J Microbiol Biotechnol 17, 1407-1429.
66. Yount, N. Y. & Yeaman, M. R. (2005). Immunocontinuum: perspectives in antimicrobial peptide mechanisms of action and resistance. Protein Pept Lett 12, 49-67.