Differential modulation of innate immune cell functions by the Burkholderia cepacia complex: Burkholderia cenocepacia but not Burkholderia multivorans disrupts maturation and induces necrosis in human dendritic cells

Cellular Microbiology

Volumn 10, Issue 10, 2008, Pages 2138-2149

  Macdonald, Kelly L ^a   Speert, David P ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD83 ANTIGEN; CD86 ANTIGEN; CYTOCHALASIN D; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 6; LIPOCORTIN 5; LIPOPOLYSACCHARIDE; PROPIDIUM IODIDE; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BACTERIAL VIABILITY; BACTERICIDAL ACTIVITY; BURKHOLDERIA; BURKHOLDERIA CENOCEPACIA; BURKHOLDERIA CEPACIA; BURKHOLDERIA MULTIVORANS; CELL DEATH; CELL FUNCTION; CELL MATURATION; CHRONIC GRANULOMATOUS DISEASE; CONTROLLED STUDY; CYSTIC FIBROSIS; CYTOCHEMISTRY; CYTOKINE PRODUCTION; DENDRITIC CELL; FLOW CYTOMETRY; HEAT; HOST; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; INCUBATION TIME; INFECTION SENSITIVITY; INNATE IMMUNITY; LUNG INFECTION; PATHOGENESIS; PATHOGENICITY; PHAGOCYTE; PHAGOCYTOSIS; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; SEPTICEMIA; SUPERNATANT;

ANNEXIN A5; BURKHOLDERIA CEPACIA COMPLEX; CELL SURVIVAL; CELLS, CULTURED; COLONY COUNT, MICROBIAL; CYTOKINES; DENDRITIC CELLS; FLOW CYTOMETRY; HUMANS; NECROSIS; PROPIDIUM; STAINING AND LABELING;

BACTERIA (MICROORGANISMS); BURKHOLDERIA CENOCEPACIA; BURKHOLDERIA CEPACIA COMPLEX; BURKHOLDERIA MULTIVORANS;

EID: 51449100530     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2008.01197.x     Document Type: Article

References (65)

1. Ashany, D., Savir, A., Bhardwaj, N., and Elkon, K.B. (1999) Dendritic cells are resistant to apoptosis through the Fas (CD95/APO-1) pathway. J Immunol 163: 5303-5311.
2. Bamford, S., Ryley, H., and Jackson, S.K. (2007) Highly purified lipopolysaccharides from Burkholderia cepacia complex clinical isolates induce inflammatory cytokine responses via TLR4-mediated MAPK signalling pathways and activation of NFkappaB. Cell Microbiol 9: 532-543.
3. Banchereau, J., and Steinman, R.M. (1998) Dendritic cells and the control of immunity. Nature 392: 245-252.
4. Banchereau, J., Briere, F., Caux, C., Davoust, J., Lebecque, S., Liu, Y.J., et al. (2000) Immunobiology of dendritic cells. Annu Rev Immunol 18: 767-811.
5. Bylund, J., Burgess, L.A., Cescutti, P., Ernst, R.K., and Speert, D.P. (2005a) Exopolysaccharides from Burkholderia cenocepacia inhibit neutrophil chemotaxis and scavenge reactive oxygen species. J Biol Chem 281: 2526-2532.
6. Bylund, J., Campsall, P.A., Ma, R.C., Conway, B.A., and Speert, D.P. (2005b) Burkholderia cenocepacia induces neutrophil necrosis in chronic granulomatous disease. J Immunol 174: 3562-3569.
7. Chaparro, C., Maurer, J., Gutierrez, C., Krajden, M., Chan, C., Winton, T., et al. (2001) Infection with Burkholderia cepacia in cystic fibrosis: Outcome following lung transplantation. Am J Respir Crit Care Med 163: 43-48.
8. Cheung, K.J., Jr, Li, G., Urban, T.A., Goldberg, J.B., Griffith, A., Lu, F., and Burns, J.L. (2007) Pilus-mediated epithelial cell death in response to infection with Burkholderia cenocepacia. Microbes Infect 9: 829-837.
9. Chiu, C.H., Ostry, A., and Speert, D.P. (2001) Invasion of murine respiratory epithelial cells in vivo by Burkholderia cepacia. J Med Microbiol 50: 594-601.
10. 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.
11. Chu, K.K., MacDonald, K.L., Davidson, D.J., and Speert, D.P. (2004) Persistence of Burkholderia multivorans within the pulmonary macrophage in the murine lung. Infect Immun 72: 6142-6147.
12. Colino, J., and Snapper, C.M. (2003) Two distinct mechanisms for induction of dendritic cell apoptosis in response to intact Streptococcus pneumoniae. J Immunol 171: 2354-2365.
13. Corey, M., and Farewell, V. (1996) Determinants of mortality from cystic fibrosis in Canada, 1970-1989. Am J Epidemiol 143: 1007-1017.
14. Cutler, C.W., Jotwani, R., and Pulendran, B. (2001) Dendritic cells: immune saviors or Achilles' heel? Infect Immun 69: 4703-4708.
15. Davidson, D.J., Currie, A.J., Reid, G.S., Bowdish, D.M., MacDonald, K.L., Ma, R.C., et al. (2004) The cationic antimicrobial peptide LL-37 modulates dendritic cell differentiation and dendritic cell-induced T cell polarization. J Immunol 172: 1146-1156.
16. De Soyza, A., Ellis, C.D., Khan, C.M., Corris, P.A., and Demarco de Hormaeche, R. (2004) Burkholderia cenocepacia lipopolysaccharide, lipid A, and proinflammatory activity. Am J Respir Crit Care Med 170: 70-77.
17. De Trez, C., Pajak, B., Brait, M., Glaichenhaus, N., Urbain, J., Moser, M., et al. (2005) TLR4 and Toll-IL-1 receptor domain-containing adapter-inducing IFN-beta, but not MyD88, regulate Escherichia coli-induced dendritic cell maturation and apoptosis in vivo. J Immunol 175: 839-846.
18. Fischer, W., Koch, H.U., and Haas, R. (1983) Improved preparation of lipoteichoic acids. Eur J Biochem 133: 523-530.
19. Folch, J., Lees, M., and Sloane Stanley, G.H. (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509.
20. Gronow, S., Noah, C., Blumenthal, A., Lindner, B., and Brade, H. (2003) Construction of a deep-rough mutant of Burkholderia cepacia ATCC 25416 and characterization of its chemical and biological properties. J Biol Chem 278: 1647-1655.
21. Hendry, J., Butler, S., Elborn, J.S., Govan, J.R., Nelson, J., Shale, D.J., and Webb, A.K. (2000a) Antibody response to Burkholderia cepacia in patients with cystic fibrosis colonized with Burkholderia cepacia and Pseudomonas aeruginosa. J Infect 40: 164-170.
22. Hendry, J., Nixon, L., Dodd, M., Elborn, J.S., Govan, J., Shale, D.J., and Webb, A.K. (2000b) Pulmonary function, serum markers of inflammation, and IgG antibodies to core lipopolysaccharide of Burkholderia cepacia in adults with cystic fibrosis, following colonization with Burkholderia cepacia. Pediatr Pulmonol 29: 8-10.
23. Hirschfeld, M., Ma, Y., Weis, J.H., Vogel, S.N., and Weis, J.J. (2000) Cutting edge: Repurification of lipopolysaccharide eliminates signaling through both human and murine toll-like receptor 2. J Immunol 165: 618-622.
24. Hou, W.S., and Van Parijs, L. (2004) A Bcl-2-dependent molecular timer regulates the lifespan and immunogenicity of dendritic cells. Nat Immunol 5: 583-589.
25. Hutchison, M.L., and Govan, J.R. (1999) Pathogenicity of microbes associated with cystic fibrosis. Microbes Infect 1: 1005-1014.
26. Hutchison, M.L., Poxton, I.R., and Govan, J.R. (1998) Burkholderia cepacia produces a hemolysin that is capable of inducing apoptosis and degranulation of mammalian phagocytes. Infect Immun 66: 2033-2039.
27. Hutchison, M.L., Bonell, E.C., Poxton, I.R., and Govan, J.R. (2000) Endotoxic activity of lipopolysaccharides isolated from emergent potential cystic fibrosis pathogens. FEMS Immunol Med Microbiol 27: 73-77.
28. Isles, A., Maclusky, I., Corey, M., Gold, R., Prober, C., Fleming, P., and Levison, H. (1984) Pseudomonas cepacia infection in cystic fibrosis: an emerging problem. J Pediatr 104: 206-210.
29. Johnston, R.B., Jr (2001) Clinical aspects of chronic granulomatous disease. Curr Opin Hematol 8: 17-22.
30. Kapsenberg, M.L. (2003) Dendritic-cell control of pathogen-driven T-cell polarization. Nat Rev Immunol 3: 984-993.
31. Kooi, C., Subsin, B., Chen, R., Pohorelic, B., and Sokol, P.A. (2006) Burkholderia cenocepacia ZmpB is a broad-specificity zinc metalloprotease involved in virulence. Infect Immun 74: 4083-4093.
32. Lamothe, J., Huynh, K.K., Grinstein, S., and Valvano, M.A. (2007) Intracellular survival of Burkholderia cenocepacia in macrophages is associated with a delay in the maturation of bacteria-containing vacuoles. Cell Microbiol 9: 40-53.
33. Lefebre, M., and Valvano, M. (2001) In vitro resistance of Burkholderia cepacia complex isolates to reactive oxygen species in relation to catalase and superoxide dismutase production. Microbiology 147: 97-109.
34. Lemaire, S., Van Bambeke, F., Mingeot-Leclercq, M.P., and Tulkens, P.M. (2005) Activity of three {beta}-lactams (ertapenem, meropenem and ampicillin) against intraphagocytic Listeria monocytogenes and Staphylococcus aureus. J Antimicrob Chemother 55: 897-904.
35. Leverkus, M., Walczak, H., McLellan, A., Fries, H.W., Terbeck, G., Brocker, E.B., and Kampgen, E. (2000) Maturation of dendritic cells leads to up-regulation of cellular FLICE-inhibitory protein and concomitant down-regulation of death ligand-mediated apoptosis. Blood 96: 2628-2631.
36. Mahenthiralingam, E., Bischof, J., Byrne, S.K., Radomski, C., Davies, J.E., Av-Gay, Y., and Vandamme, P. (2000a) DNA-Based diagnostic approaches for identification of Burkholderia cepacia complex, Burkholderia vietnamiensis, Burkholderia multivorans, Burkholderia stabilis, and Burkholderia cepacia genomovars I and III. J Clin Microbiol 38: 3165-3173.
37. Mahenthiralingam, E., Coenye, T., Chung, J.W., Speert, D.P., Govan, J.R., Taylor, P., and Vandamme, P. (2000b) Diagnostically and experimentally useful panel of strains from the Burkholderia cepacia complex. J Clin Microbiol 38: 910-913.
38. Mahenthiralingam, E., Urban, T.A., and Goldberg, J.B. (2005) The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 3: 144-156.
39. 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.
40. Martin, D.W., and Mohr, C.D. (2000) Invasion and intracellular survival of Burkholderia cepacia. Infect Immun 68: 24-29.
41. Melnikov, A., Zaborina, O., Dhiman, N., Prabhakar, B.S., Chakrabarty, A.M., and Hendrickson, W. (2000) Clinical and environmental isolates of Burkholderia cepacia exhibit differential cytotoxicity towards macrophages and mast cells. Mol Microbiol 36: 1481-1493.
42. Mohr, C.D., Tomich, M., and Herfst, C.A. (2001) Cellular aspects of Burkholderia cepacia infection. Microbes Infect 3: 425-435.
43. Moll, H. (2003) Dendritic cells and host resistance to infection. Cell Microbiol 5: 493-500.
44. Palucka, K., and Banchereau, J. (2002) How dendritic cells and microbes interact to elicit or subvert protective immune responses. Curr Opin Immunol 14: 420-431.
45. Punj, V., Sharma, R., Zaborina, O., and Chakrabarty, A.M. (2003) Energy-generating enzymes of Burkholderia cepacia and their interactions with macrophages. J Bacteriol 185: 3167-3178.
46. Rommens, J.M., Iannuzzi, M.C., Kerem, B., Drumm, M.L., Melmer, G., Dean, M., et al. (1989) Identification of the cystic fibrosis gene: Chromosome walking and jumping. Science 245: 1059-1065.
47. Saini, L.S., Galsworthy, S.B., John, M.A., and Valvano, M.A. (1999) Intracellular survival of Burkholderia cepacia complex isolates in the presence of macrophage cell activation. Microbiology 145: 3465-3475.
48. Sallusto, F., and Lanzavecchia, A. (1994) Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med 179: 1109-1118.
49. Savill, J.S., Henson, P.M., and Haslett, C. (1989) Phagocytosis of aged human neutrophils by macrophages is mediated by a novel 'charge-sensitive' recognition mechanism. J Clin Invest 84: 1518-1527.
50. Segal, B.H., Leto, T.L., Gallin, J.I., Malech, H.L., and Holland, S.M. (2000) Genetic, biochemical, and clinical features of chronic granulomatous disease. Medicine (Baltimore) 79: 170-200.
51. Shaw, D., Poxton, I.R., and Govan, J.R. (1995) Biological activity of Burkholderia (Pseudomonas) cepacia lipopolysaccharide. FEMS Immunol Med Microbiol 11: 99-106.
52. Shimomura, H., Matsuura, M., Saito, S., Hirai, Y., Isshiki, Y., and Kawahara, K. (2001) Lipopolysaccharide of Burkholderia cepacia and its unique character to stimulate murine macrophages with relative lack of interleukin-1beta-inducing ability. Infect Immun 69: 3663-3669.
53. Silipo, A., Molinaro, A., Ierano, T., De Soyza, A., Sturiale, L., Garozzo, D., et al. (2007) The complete structure and pro-inflammatory activity of the lipooligosaccharide of the highly epidemic and virulent gram-negative bacterium Burkholderia cenocepacia ET-12 (strain J2315). Chemistry 13: 3501-3511.
54. Smalley, J.W., Charalabous, P., Birss, A.J., and Hart, C.A. (2001) Detection of heme-binding proteins in epidemic strains of Burkholderia cepacia. Clin Diagn Lab Immunol 8: 509-514.
55. Speert, D.P. (2002) Advances in Burkholderia cepacia complex. Paediatr Respir Rev 3: 230-235.
56. Speert, D.P., Bond, M., Woodman, R.C., and Curnutte, J.T. (1994) Infection with Pseudomonas cepacia in chronic granulomatous disease: role of nonoxidative killing by neutrophils in host defense. J Infect Dis 170: 1524-1531.
57. Speert, D.P., Steen, B., Halsey, K., and Kwan, E. (1999) A murine model for infection with Burkholderia cepacia with sustained persistence in the spleen. Infect Immun 67: 4027-4032.
58. Speert, D.P., Henry, D., Vandamme, P., Corey, M., and Mahenthiralingam, E. (2002) Epidemiology of Burkholderia cepacia complex in patients with cystic fibrosis, Canada. Emerg Infect Dis 8: 181-187.
59. Steinman, R.M., and Banchereau, J. (2007) Taking dendritic cells into medicine. Nature 449: 419-426.
60. Ueno, H., Klechevsky, E., Morita, R., Aspord, C., Cao, T., Matsui, T., et al. (2007) Dendritic cell subsets in health and disease. Immunol Rev 219: 118-142.
61. Vulcano, M., Dusi, S., Lissandrini, D., Badolato, R., Mazzi, P., Riboldi, E., et al. (2004) Toll receptor-mediated regulation of NADPH oxidase in human dendritic cells. J Immunol 173: 5749-5756.
62. Westphal, O., and Jann, K. (1965) Bacterial lipopolysaccharides: extraction with phenol-water and further applications of the procedure. Meth Carbohydr Chem 5: 83-91.
63. Winkelstein, J.A., Marino, M.C., Johnston, R.B., Jr, Boyle, J., Curnutte, J., Gallin, J.I., et al. (2000) Chronic granulomatous disease. Report on a national registry of 368 patients. Medicine (Baltimore) 79: 155-169.
64. Zughaier, S.M., Ryley, H.C., and Jackson, S.K. (1999a) A melanin pigment purified from an epidemic strain of Burkholderia cepacia attenuates monocyte respiratory burst activity by scavenging superoxide anion. Infect Immun 67: 908-913.
65. Zughaier, S.M., Ryley, H.C., and Jackson, S.K. (1999b) Lipopolysaccharide (LPS) from Burkholderia cepacia is more active than LPS from Pseudomonas aeruginosa and Stenotrophomonas maltophilia in stimulating tumor necrosis factor alpha from human monocytes. Infect Immun 67: 1505-1507.