Putative virulence factors are released in association with membrane vesicles from Burkholderia cepacia

Canadian Journal of Microbiology

Volumn 49, Issue 10, 2003, Pages 613-624

  Allan, Nick D ^a   Kooi, Cora ^b   Sokol, Pamela A ^b   Beveridge, Terry J ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Burkholderia cepacia; Genomovar; Membrane vesicles; Virulence factors

Indexed keywords

BIOLOGICAL MEMBRANES; ENZYMES; GROWTH KINETICS; PATHOLOGY; TISSUE;

INFECTION; MEMBRANE VESICLES;

BACTERIA;

BACTERIAL ENZYME; BACTERIUM LIPOPOLYSACCHARIDE; METALLOPROTEINASE; PEPTIDOGLYCAN; PHOSPHOLIPASE N; POLYMER; PROTEINASE; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

BACTERIUM; MEMBRANE; VIRULENCE;

ARTICLE; BACTERIAL VIRULENCE; BACTERIUM PILUS; BURKHOLDERIA CEPACIA; CENTRIFUGATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; FILTRATION; FLAGELLUM; MEMBRANE VESICLE; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN DEGRADATION; SUCROSE GRADIENT; ZYMOGRAPHY;

BURKHOLDERIA CEPACIA; BURKHOLDERIA INFECTIONS; CELL MEMBRANE; CENTRIFUGATION, ISOPYCNIC; HUMANS; LIPASE; MICROSCOPY, ELECTRON; PHOSPHOLIPASE C; SERINE ENDOPEPTIDASES; VIRULENCE; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); BURKHOLDERIA; BURKHOLDERIA CEPACIA; NEGIBACTERIA;

EID: 1042267972     PISSN: 00084166     EISSN: None     Source Type: Journal    
DOI: 10.1139/w03-078     Document Type: Article

References (53)

1. Allan, N., and Beveridge, T.J. 1999. Naturally released membrane vesicles from Serratia marcescens contain major nuclease and virulence factors, Proceedings of the Canadian Bacterial Disease Network Annual Meeting, Banff, Alberta, 27-29 April 1999.
2. Bernadsky, G., Beveridge, T.J., and Clarke, A.J. 1994. Analysis of sodium dodecyl sulfate-stable peptidoglycan autolysins of select Gram-negative pathogens by using renaturing polyacrylamide gel electrophoresis. J. Bacteriol. 176: 5225-5232.
3. Beveridge, T.J., and Kadurugamuwa, J.L. 1996. Periplasm, periplasmic spaces, and their relation to bacterial wall structure: novel secretion of selected periplasmic proteins from Pseudomonas aeruginosa. Microb. Drug Resist. 2: 1-8.
4. Burkholder, W.H. 1950. Sour skin, a bacterial rot of onion bulbs. Phytopathology, 40: 115-117.
5. Chu, K.K., Davidson, D.J., Halsey, T.K., Chung, J.W., and Speert, D.P. 2002. Differential persistence among genomovars of the Burkholderia cepacia complex in a murine model of pulmonary infection. Infect. Immun. 70: 2715-2720.
6. Ciofu, O., Beveridge, T.J., Kadurugamuwa, J., Walther-Rosmussen, J., and Høiby, N. 2000. Chromosomal beta-lactamase is packaged into membrane vesicles from Pseudomonas aeruginosa. J. Antimicrob. Chemother. 45: 9-13.
7. Coenye, T., Mahenthiralingam, E., Henry, D., LiPuma, J.L., Laivens, S., Gillis, M., Speert, D.P., and Vandamme, P. 2001. Burkholderia ambifaria sp. nov., a novel member of the Burkholderia cepacia complex including biocontrol and cystic fibrosis-related isolates. Int. J. Syst. Evol. Microbiol. 51: 1481-1490.
8. Corbett, C.R., Burtnick, M.N., Kooi, C., Woods, D.E., and Sokol, P.A. 2003. An extracellular zinc metalloprotease gene of Burkholderia cepacia. Microbiology (Reading, U.K.), 149: 2263-2271.
9. Darveau, R.P., and Hancock, R.E.W. 1983. Procedure for isolation of bacterial lipopolysaccharides from both smooth and rough Pseudomonas aeruginosa and Salmonella typhimurium strains. J. Bacteriol. 155: 831-838.
10. Gilligan, P.H. 1991. Microbiology of airway disease in patients with cystic fibrosis. Clin. Microbiol. Rev. 4: 35-51.
11. Govan, J.R.W., Hughes, J.E., and Vandamme, P. 1996. Burkholderia cepacia: medical, taxonomic and ecological issues. J. Med. Microbiol. 45: 1-15.
12. Hancock, R.E.W., and Nikaido, H. 1978. Outer membranes of Gram-negative bacteria XIX. Isolation from P. aeruginosa PAO1 and use in reconstitution and definition of permeability barrier. J. Bacteriol. 136: 381-390.
13. Hayashi, S., Abe, M., Kimoto, M., Furukawa, S., and Nkazawa, T. 1999. The DsbA-DsbB disulfide bond formation system of Burkholderia cepacia is involved in the production of protease and alkaline phosphatase, motility, metal resistance, and multidrug resistance. Microbiol. Immunol. 44: 41-50.
14. Hitchcock, P.J., and Brown, T.M. 1983. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J. Bacteriol. 154: 269-277.
15. Horstman, A.L., and Kuehn, M.J. 2000. Enterotoxigenic Escherichia coli secretes active heat-labile enterotoxin via outer membrane vesicles. J. Bacteriol. 275: 12 489-12 496.
16. Hughes, J.E., Stewart, J., Barclay, G.R., and Govan, J.R.W. 1997. Priming of neutrophil respiratory burst activity by lipopolysaccharide from Burkholderia cepacia. Infect. Immun. 65: 4281-4287.
17. Hutchison, M.L., and Govan, J.R. 1999. Pathogenicity of microbes associated with cystic fibrosis. Microbes Infect. 1: 1005-1014.
18. Ilses, A.M., Maclusky, I., Corey, M., Gold, R., Probey, C., Fleming, P., and Levison, H. 1984. Pseudomonas cepacia infection in cystic fibrosis: an emerging problem. J. Pediatr. (St. Louis), 86: 206-210.
19. Kadurugamuwa, J.L., and Beveridge, T.J. 1995. Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion. J. Bacteriol. 177: 3998-4008.
20. Kadurugamuwa, J.L., and Beveridge, T.J. 1996. Bacteriolytic effect of membrane vesicles from Pseudomonas aeruginosa on other bacteria including pathogens: conceptually new antibiotics. J. Bacteriol. 178: 2767-2774.
21. Kadurugamuwa, J.L., and Beveridge, T.J. 1997. Natural release of virulence factors in membrane vesicles by Pseudomonas aeruginosa and the effect of aminoglycoside antibiotics on their release. J. Antimicrob. Chemother. 40: 615-621.
22. Karkhanis, Y.D., Zeltner, J.Y., Jackson, J.J., and Carlo, D.L. 1978. A new and improved microassay to determine 2-keto-3-deoxyoctonate in lipopolysaccharide of Gram-negative bacteria. Anal. Biochem. 85: 595-601.
23. Kooi, C., Cox, A., Darling, P., and Sokol, P.A. 1994. Neutralizing antibodies to an extracellular Pseudomonas cepacia protease. Infect. Immun. 62: 2811-2817.
24. Kooi, C., Hodges, R.S., and Sokol, P.A. 1997. Identification of neutralizing epitopes on Pseudomonas aeruginosa elastase and effects of cross-reactions on other thermolysin-like proteases. Infect. Immun. 65: 472-477.
25. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London), 227: 680-685.
26. Larsen, G.Y., Stull, T.L., and Burns, J.L. 1993. Marked phenotypic variablity in Pseudomonas cepacia isolated from a patient with cystic fibrosis. J. Clin. Microbiol. 31: 788-792.
27. Li, Z., Clarke, A.J., and Beveridge, T.J. 1996. A major autolysin of Pseudomonas aeruginosa: subcellular distribution, potential role in cell growth and division, and secretion in surface membrane vesicles. J. Bacteriol. 178: 2479-2488.
28. Li, Z., Clarke, A.J., and Beveridge, T.J. 1998. Gram-negative bacteria produce membrane vesicles which are capable of killing other bacteria. J. Bacteriol. 180: 5478-5483.
29. LiPuma, J.J., Dulaney, B.J., McMenamin, J.D., Whitby, P.W., Stull, T.L., Coenye, T., and Vandamme, P. 1999. Development of rRNA-based PCR assays for the identification of Burkholderia cepacia complex isolates recovered from cystic fibrosis patients. J. Clin. Microbiol. 37: 3167-3170.
30. Lonon, M.K., and Hooke, A.M. 1991. A nonhemolytic phospholipase C produced by Pseudomonas cepacia. Curr. Microbiol. 23: 139-142.
31. Lonon, M.K., Woods, D.E., and Strauss, D.C. 1988. Production of lipase by clinical isolates of Pseudomonas aeruginosa. J. Clin. Microbiol. 26: 979-984.
32. MacDonald, K.L., and Beveridge, T.J. 2002. Bactericidal effect of gentamicin-induced membrane vesicles derived from Pseudomonas aeruginosa PAO1 on gram-positive bacteria. Can. J. Microbiol. 48: 810-820.
33. McKenney, D., and Allison, D.G. 1995. Effects of growth rate and nutrient limitation on virulence factor production in Burkholderia cepacia. J. Bacteriol. 177: 4140-4143.
34. McKevitt, A.I., and Woods, D.E. 1984. Characterization of Pseudomonas cepacia isolates from patients with cystic fibrosis. J. Clin. Microbiol. 19: 291-293.
35. McKevitt, A.I., Bajaksouzian, S., Klinger, J.D., and Woods, D.E. 1989. Purification and characterization of an extracellular protease from Pseudomonas cepacia. Infect. Immun. 57: 771-778.
36. Nelson, J.W., Butler, S.L., Krieg, D., and Govan, J.R.W. 1994. Virulence factors of Burkholderia cepacia. FEMS Immunol. Med. Microbiol. 8: 89-98.
37. Nowotny, A., Behling, U.K., Hammond, B., Lai, C.H., Listgarten, M., Phon, P.H., and Sanari, F. 1982. Release of toxic microvesicles by Actinobacillus actinomycetemcomitans. Infect. Immun. 37: 151-154.
38. Palfreyman, R.W., Watson, M.L., Eden, C., and Smith, A.W. 1997. Induction of biologically active interleukin-8 from lung epithelial cells by Burkholderia (Pseudomonas) cepacia products. Infect. Immun. 65: 617-622.
39. Parr, T.R., Moore, R.A., Moore, L.V., and Hancock, R.E.W. 1987. Role of porins in intrinsic antibiotic resistance of Pseudomonas cepacia. Antimicrob. Agents Chemother. 31: 121-123.
40. Parsons, Y.N., Glendinning, K.J., Thornton, V., Hales, B.A., Hart, C.A., and Winstanley, C. 2001. A putative type III secretion gene cluster is widely distributed in the Burkholderia cepacia complex but absent from genomovar I. FEMS Microbiol. Lett. 203: 103-108.
41. Pavlovskis, O.R., and Wretlind, B. 1979. Assessment of protease (elastase) as a Pseudomonas aeruginosa virulence factor in experimental mouse burn infection. Infect. Immun. 24: 181-187.
42. Sajjan, U.S., Sun, L., Goldstein, R., and Forstner, J.F. 1995. Cable (Cbl) type II pili of cystic fibrosis-associated Burkholderia (Pseudomonas) cepacia: nucleotide sequence of the cblA major subunit pilin gene and novel morphology of the assembled appendage fibers. J. Bacteriol. 177: 1030-1038.
43. Smalley, J.W., Charalabous, P., Birss, A.J., and Hart, C.A. 2001. Detection of heme-binding proteins in epidemic stains of Burkholderia cepacia. Clin. Diagn. Lab. Immunol. 8: 509-514.
44. Speert, D.P., Bond, M., and Woodman, R.C. 1994. Infection with Pseudomonas cepacia in chronic granulomatous disease: role of non-oxidative killing by neutrophils in host defense. J. Infect. Dis. 170: 1524-1531.
45. Speert, D.P., Henry, D., Vandamme, P., Corey, M., and Mahenthiralingam, E. 2002. Epidemiology of Burkholderia cepacia in patients with cystic fibrosis, Canada. Emerg. Infect. Dis. 8: 181-187.
46. Starr, M.P., and Burkholder, W.H. 1941. Lipolytic activity of phytopathogenic bacteria determined by means of spirit blue agar and its taxonomic significance. Phytopathology, 32: 558-564.
47. Straus, D.C., Lonon, M.K., and Hutson, J.C. 1992. Inhibition of rat alveolar macrophage phagocytic function by a Pseudomonas cepacia lipase. J. Med. Microbiol. 37: 335-340.
48. Towbin, H., Stachelin, T., and Gordon, J. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U.S.A. 76: 4350-4354.
49. Tsai, C.M., and Frasch, C.E. 1982. A sensitive silver stain for detecting lipopolysaccharide in polyacrylamide gels. Anal. Biochem. 119: 115-119.
50. Vasil, M.L., Krieg, D.P., Kuhns, J.S., Ogle, J.W., Shortridge, V.D., Ostroff, R.M., and Vasil, A.I. 1990. Molecular analysis of hemolytic and phospholipase activities of Pseudomonas cepacia. Infect. Immun. 58: 4020-4029.
51. Wai, S.M., Takade, A., and Amako, K. 1995. The release of outer membrane vesicles from the strains of enterotoxigenic Escherichia coli. Microbiol. Immunol. 39: 451-456.
52. Weingart, C.L., and Morris-Hooke, A. 1999. A nonhemolytic phopholipase C from Burkholderia cepacia. Curr. Microbiol. 38: 223-238.
53. Wilkinson, S.G., and Pitt, T.L. 1995. Burkholderia (Pseudomonas) cepacia: pathogenicity and resistance. Rev. Med. Microbiol. 6: 1-17.