The multifarious, multireplicon Burkholderia cepacia complex

Nature Reviews Microbiology

Volumn 3, Issue 2, 2005, Pages 144-156

  Mahenthiralingam, Eshwar ^a   Urban, Teresa A ^b   Goldberg, Joanna B ^b  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMICROBIAL CATIONIC PEPTIDE; BETA LACTAM ANTIBIOTIC; CHLORAMPHENICOL; PENICILLIN G; QUINOLINE DERIVED ANTIINFECTIVE AGENT; TRIMETHOPRIM;

ANTIBIOTIC RESISTANCE; BACTERIAL GENOME; BACTERIAL INFECTION; BACTERIAL TRANSMISSION; BACTERIAL VIRULENCE; BIOREMEDIATION; BURKHOLDERIA CEPACIA COMPLEX; CHRONIC DISEASE; CYSTIC FIBROSIS; GENETIC VARIABILITY; HUMAN; LUNG FUNCTION; LUNG INFECTION; NONHUMAN; OPPORTUNISTIC INFECTION; PATHOGENESIS; PHENOTYPE; PLANT PATHOGEN INTERACTION; PRIORITY JOURNAL; REPLICON; REVIEW; SPECIES DIFFERENCE; SYMPTOMATOLOGY;

BURKHOLDERIA CEPACIA COMPLEX; BURKHOLDERIA INFECTIONS; CYSTIC FIBROSIS; GENOME, BACTERIAL; HUMANS; OPPORTUNISTIC INFECTIONS; REPLICON; VIRULENCE; VIRULENCE FACTORS;

EID: 13444251656     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro1085     Document Type: Review

References (143)

1. Coenye, T., Vandamme, P., Govan, J. R. & LiPuma, J. J. Taxonomy and identification of the Burkholderia cepacia complex. J. Clin. Microbiol. 39, 3427-3436 (2001).
2. Burkholder, W. H. Sour skin, a bacterial rot of onion bulbs. Phytopathol. 40, 115-117 (1950).
3. Parke, J. L. & Gurian-Sherman, D. Diversity of the Burkholderia cepacia complex and implications for risk assessment of biological control strains. Annu. Rev. Phytopathol. 39, 225-258 (2001).
4. Lessie, T. G., Hendrickson, W., Manning, B. D. & Devereux, R. Genomic complexity and plasticity of Burkholderia cepacia. FEMS Microbiol. Lett. 144, 117-128 (1996).
5. Govan, J. R., Hughes, J. E. & Vandamme, P. Burkholderia cepacia: medical, taxonomic and ecological issues. J. Med. Microbiol. 45, 395-407 (1996).
6. Yabuuchi, E. et al. Proposal of Burkholderia gen. nov. and transfer of seven species of the genus Pseudomonas homology group II to the new genus, with the type species Burkholderia cepacia (Palleroni and Holmes 1981) comb. nov. Microbiol. Immunol. 36, 1251-1275 (1992).
7. Vandamme, P. et al. 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 (1997).
8. Isles, A. et al. Pseudomonas cepacia infection in cystic fibrosis: an emerging problem. J. Pediatr. 104, 206-210 (1984).
9. Goldmann, D. A. & Klinger, J. D. Pseudomonas cepacia: biology, mechanisms of virulence, epidemiology. J. Pediatr. 108, 806-812 (1986).
10. Banerjee, D. & Stableforth, D. The treatment of respiratory Pseudomonas infection in cystic fibrosis: what drug and which way? Drugs 60, 1053-1064 (2000).
11. LiPuma, J. J. Burkholderia cepacia. Management issues and new insights. Clin. Chest Med. 19, 473-486 (1998).
12. Moore, J. E. & Elborn, J. S. Burkholderia cepacia and cystic fibrosis - 50 years on. Commun. Dis. Public Health 4, 114-116 (2001).
13. Chernish, R. N. & Aaron, S. D. Approach to resistant Gram-negative bacterial pulmonary infections in patients with cystic fibrosis. Curr. Opin. Pulm. Med. 9, 509-515 (2003).
14. Coenye, T. & Vandamme, F. Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ. Microbiol. 5, 719-729 (2003).
15. Gonzalez, C. F., Pettit, E. A., Valadez, V. A. & Provin, E. M. Mobilization, cloning, and sequence determination of a plasmid-encoded polygalacturonase from a phytopathogenic Burkholderia (Pseudomonas) cepacia. Mol. Plant Microbe Interact. 10, 840-851 (1997).
16. Engledow, A. S., Medrano, E. G., Mahenthiralingam, E., LiPuma, J. J. & Gonzalez, C. F. Involvement of a plasmid-encoded type IV secretion system in the plant tissue watersoaking phenotype of Burkholderia cenocepacia. J. Bacteriol. 186, 6015-6024 (2004).
17. Steffan, R. J., Sperry, K. L., Walsh, M. T., Vainberg, S. & Condee, C. W. Field-scale evaluation of in situ bioaugmentation for remediation of chlorinated solvents in groundwater. Environ. Sci. Technol. 33, 2771-2781 (1999).
18. Hutchinson, G. R. et al. Home-use nebulizers: a potential primary source of Burkholderia cepacia and other colistin-resistant, Gram-negative bacteria in patients with cystic fibrosis. J. Clin. Microbiol. 34, 584-587 (1996).
19. Oie, S. & Kamiya, A. Microbial contamination of antiseptics and disinfectants. Am. J. Infect. Control 24, 389-395 (1996).
20. Huang, C. H. et al. Characteristics of patients with Burkholderia cepacia bacteremia. J. Microbiol. Immunol. Infect. 34, 215-219 (2001).
21. Speert, D. P. Understanding Burkholderia cepacia: epidemiology, genomovars, and virulence. Infect. Med. 18, 49-56 (2001).
22. Johnston, R. B. Jr. Clinical aspects of chronic granulomatous disease. Curr. Opin. Hematol. 8, 17-22 (2001).
23. Guide, S. V. et al. Reinfection, rather than persistent infection, in patients with chronic granulomatous disease. J. Infect. Dis. 187, 845-853 (2003).
24. Govan, J. R. et al. Evidence for transmission of Pseudomonas cepacia by social contact in cystic fibrosis. Lancet 342, 15-19 (1993).
25. Tablan, O. C. et al. Pseudomonas cepacia colonization in patients with cystic fibrosis: risk factors and clinical outcome. J. Pediatr. 107, 382-387 (1985).
26. Mahenthiralingam, E. et al. Infection with Burkholderia cepacia complex genomovars in patients with cystic fibrosis: virulent transmissible strains of genomovar III can replace Burkholderia multivorans. Clin. Infect. Dis. 33, 1469-1475 (2001).
27. Corey, M. & Farewell, V. Determinants of mortality from cystic fibrosis in Canada, 1970-1989. Am. J. Epidemiol. 143, 1007-1017 (1996).
28. Frangolias, D. D. et al. Burkholderia cepacia in cystic fibrosis. Variable disease course. Am. J. Respir. Crit. Care Med. 160, 1572-1577 (1999).
29. Mahenthiralingam, E., Baldwin, A. & Vandamme, P. Burkholderia cepacia complex infection in patients with cystic fibrosis. J. Med. Microbiol. 51, 533-538 (2002).
30. LiPuma, J. J., Dasen, S. E., Nielson, D. W., Stern, R. C. & Stull, T. L. Person-to-person transmission of Pseudomonas cepacia between patients with cystic fibrosis. Lancet 336, 1094-1096 (1990).
31. Siddiqui, A. H. et al. An episodic outbreak of genetically related Burkholderia cepacia among non-cystic fibrosis patients at a university hospital. Infect. Control Hosp. Epidemiol. 22, 419-422 (2001).
32. Holmes, A. et al. An epidemic of Burkholderia cepacia transmitted between patients with and without cystic fibrosis. J. Infect Dis. 179, 1197-1205 (1999).
33. Saiman, L. & Siegel, J. Infection control in cystic fibrosis. Clin. Microbiol. Rev. 17, 57-71 (2004).
34. Gibson, R. L., Burns, J. L. & Ramsey, B. W. Pathophysiology and management of pulmonary infections in cystic fibrosis. Am. J. Respir. Crit. Care Med. 168, 918-951 (2003).
35. Duff, A. J. Psychological consequences of segregation resulting from chronic Burkholderia cepacia infection in adults with CF. Thorax 57, 756-758 (2002).
36. LiPuma, J. J. Preventing Burkholderia cepacia complex infection in cystic fibrosis: is there a middle ground? J. Pediatr. 141, 467-469 (2002).
37. LiPuma, J. J., Spilker, T, Coenye, T. & Gonzalez, C. F. An epidemic Burkholderia cepacia complex strain identified in soil. Lancet 359, 2002-2003 (2002).
38. Holmes, A., Govan, J. & Goldstein, R. Agricultural use of Burkholderia (Pseudomonas) cepacia: a threat to human health? Emerg. Infect. Dis. 4, 221-227 (1998).
39. LiPuma, J. J. & Mahenthiralingam, E. Commercial use of Burkholderia cepacia. Emerg. Infect. Dis. 5, 305-306 (1999 ).
40. Biddick, R., Spilker, T., Martin, A. & LiPuma, J. J. Evidence of transmission of Burkholderia cepacia, Burkholderia multivorans and Burkholderia dolosa among persons with cystic fibrosis. FEMS Microbiol. Lett. 228, 57-62 (2003).
41. Cunha, M. V. et al. Molecular analysis of Burkholderia cepacia complex isolates from a Portuguese cystic fibrosis center: a 7-year study. J. Clin. Microbiol. 41, 4113-4120 (2003).
42. LiPuma, J. J. et al. Ribotype analysis of Pseudomonas cepacia from cystic fibrosis treatment centers. J. Pediatr. 113, 859-862 (1988).
43. Coenye, T. & LiPuma, J. J. Multilocus restriction typing: a novel tool for studying global epidemiology of Burkholderia cepacia complex infection in cystic fibrosis. J. Infect Dis. 185, 1454-1462 (2002).
44. Chen, J. S., Witzmann, K. A., Spilker, T., Fink, R. J. & LiPuma, J. J. Endemicity and inter-city spread of Burkholderia cepacia genomovar III in cystic fibrosis. J. Pediatr. 139, 643-649 (2001).
45. Johnson, W. M., Tyler, S. D. & Rozee, K. R. Linkage analysis of geographic and clinical clusters in Pseudomonas cepacia infections by multilocus enzyme electrophoresis and ribotyping. J. Clin. Microbiol. 32, 924-930 (1994).
46. Sajjan, U. S., Sun, L., Goldstein, R. & Forstner, J. F. 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 (1995).
47. Sajjan, U. S. & Forstner, J. F. Role of a 22-kilodalton pilin protein in binding of Pseudomonas cepacia to buccal epithelial cells. Infect. Immun. 61, 3157-3163 (1993).
48. Mahenthiralingam, E., Simpson, D. A. & Speert, D. P. Identification and characterization of a novel DNA marker associated with epidemic Burkholderia cepacia strains recovered from patients with cystic fibrosis. J. Clin. Microbiol. 35, 808-816 (1997).
49. Coenye, T., Spilker, T., Van Schoor, A., LiPuma, J. J. & Vandamme, P. Recovery of Burkholderia cenocepacia strain PHDC from cystic fibrosis patients in Europe. Thorax 59, 952-954 (2004).
50. Nierman, W. C. et al. Structural flexibility in the Burkholderia mallei genome. Proc. Natl Acad Sci. USA 101, 14246-14251 (2004).
51. Holden, M. T G. et al. Genomic plasticity of the causative agent of melioidosis, Burkholderia pseudomallei. Proc. Natl Acad. Sci. USA 101, 14240-14245 (2004).
52. Stanier R. Y., Palleroni, N. J. & Doudoroff, M. The aerobic pseudomonads: a taxonomic study. J. Gen. Microbiol. 43, 159-271 (1966).
53. Venter, J. C. et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66-74 (2004).
54. Vermis, K., Coenye, T., Mahenthiralingam, E., Nelis, H. J. & Vandamme, P. Evaluation of species-specific recA-based PCR tests for genomovar level identification within the Burkholderia cepacia complex. J. Med. Microbiol. 51, 937-940 (2002).
55. Hacker, J. & Kaper, J. B. Pathogenicity islands and the evolution of microbes. Annu. Rev. Microbiol. 54, 641-679 (2000).
56. Holden, M. T. & Parkhill, J. The sequencing and analysis of the Burkholderia cenocepacia genome. Pediatr. Pulmonol. Suppl. 25, 286 (2003).
57. Baldwin, A., Sokol, P. A., Parkhill, J. & Mahenthiralingam, E. The Burkholderia cepacia epidemic strain marker is part of a novel genomic, island encoding both virulence and metabolism-associated genes in Burkholderia cenocepacia. Infect. Immun. 72, 1537-1547 (2004).
58. Summer, E. J. et al. Burkholderia cenocepacia phage BcepMu and a family of Mu-like phages encoding potential pathogenesis factors. J. Mol. Biol. 340, 49-65 (2004).
59. Cox, A. D. & Wilkinson, S. G. Ionizing groups in lipopolysaccharides of Pseudomonas cepacia in relation to antibiotic resistance. Mol. Microbiol. 5, 641-646 (1991).
60. Shimomura, H. et al. Unusual interaction of a lipopolysaccharide isolated from Burkholderia cepacia with polymyxin B. Infect. Immun. 71, 5225-5230 (2003).
61. Vinion-Dubiel, A. D. & Goldberg, J. B. Lipopolysaccharide of Burkholderia cepacia complex. J. Endotoxin Res. 9, 201-213 (2003).
62. Vinion-Dubiel, A. D. et al. Correlation of wbil genotype, serotype, and isolate source within species of the Burkholderia cepacia complex. J. Clin. Microbiol. 42, 4121-4126 (2004).
63. Ortega, X. et al. Reconstitution of O-specific lipopolysaccharide expression in the Burkholderia cenocepacia strain J2315 that is associated with transmissible infections in patients with cystic fibrosis. J. Bacteriol. (in the press).
64. Reeves, P. P. & Wang, L. Genomic organization of LPS-specific loci. Curr. Top. Microbiol. Immunol. 264, 109-135 (2002).
65. Shaw, D., Poxton, I. R. & Govan, J. R. Biological activity of Burkholderia (Pseudomonas) cepacia lipopolysaccharide. FEMS Immunol. Med. Microbiol. 11, 99-106 (1995).
66. Hughes, J. E., Stewart J., Barclay, G. R. & Govan, J. R. Priming of neutrophil respiratory burst activity by lipopolysaccharide from Burkholderia cepacia. Infect. Immun. 65, 4281-4287 (1997).
67. Reddi, K., Phagoo, S. B., Anderson, K. D. & Warburton, D. Burkholderia cepacia-induced IL-8 gene expression in an alveolar epithelial cell line: signaling through CD14 and mitogen-activated protein kinase. Pediatr Res. 54, 297-305 (2003).
68. Mathee, K. et al. Mucoid conversion of Pseudomonas aeruginosa by hydrogen peroxide: a mechanism for virulence activation in the cystic fibrosis lung. Microbiology 145, 1349-1357 (1999).
69. Conway, B. A., Venu, V. & Speert, D. P. Biofilm formation and acyl homoserine lactone production in the Burkholderia cepacia complex. J. Bacteriol. 184, 5678-5685 (2002).
70. Desai, M., Buhler, T., Weller, P. H. & Brown, M. R. Increasing resistance of planktonic and biofilm cultures of Burkholderia cepacia to ciprofloxacin and ceftazidime during exponential growth. J. Antimicrob. Chemother. 42, 153-160 (1998).
71. Tomlin, K. L., Coll, O. R & Ceri, H. Interspecies biofilms of Pseudomonas aeruginosa and Burkholderia cepacia. Can. J. Microbiol. 47, 949-954 (2001).
72. Riedel, K. et al. N-acylhomoserine-lactone-mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology 147, 3249-3262 (2001).
73. Huber, B. et al. Genetic analysis of functions involved in the late stages of biofilm development in Burkholderia cepacia H111. Mol. Microbiol. 46, 411-426 (2002).
74. Lazdunski, A. M., Ventre, I. & Sturgis, J. N. Regulatory circuits and communication in Gram-negative bacteria. Nature Rev. Microbiol. 2, 581-592 (2004).
75. Lewenza, S., Conway, B., Greenberg, E. P. & Sokol, P. A. Quorum sensing in Burkholderia cepacia: identification of the LuxRI homologs CepRI. J. Bacteriol. 181, 748-756 (1999).
76. Venturi, V., Friscina, A., Bertani, I., Devescovi, G. & Aguilar C. Quorum sensing in the Burkholderia cepacia complex. Res. Microbiol. 155, 238-244 (2004).
77. Sokol, P. A. et al. The CepIR quorum-sensing system contributes to the virulence of Burkholderia cenocepacia respiratory infections. Microbiology 149, 3649-3658 (2003).
78. Kothe, M. et al. Killing of Caenorhabditis elegans by Burkholderia cepacia is controlled by the cep quorum-sensing system. Cell. Microbiol. 5, 343-351 (2003).
79. LiPuma, J. J. et al. Disproportionate distribution of Burkholderia cepacia complex species and transmissibility markers in cystic fibrosis. Am. J. Respir. Crit. Care Med. 164, 92-96 (2001).
80. Speert, D. P., Henry, D., Vandamme, P., Corey, M. & Mahenthiralingam, E. Epidemiology of Burkholderia cepacia complex in patients with cystic fibrosis, Canada. Emerg. Infect. Dis. 8, 181-187 (2002).
81. Burns, J. L., Lien, D. M. & Hedin, L. A. Isolation and characterization of dihydrofolate reductase from trimethoprim-susceptible and trimethoprim-resistant Pseudomonas cepacia. Antimicrob. Agents Chemother. 33, 1247-1251 (1989).
82. Burns, J. L., Wadsworth, C. D., Barry, J. J. & Goodall, C. P. Nucleotide sequence analysis of a gene from Burkholderia (Pseudomonas) cepacia encoding an outer membrane lipoprotein involved in multiple antibiotic resistance. Antimicrob. Agents Chemother. 40, 307-313 (1996).
83. Chiesa, C., Labrozzi, P. H. & Aronoff, S. C. Decreased baseline β-lactamase production and inducibility associated with increased piperacillin susceptibility of Pseudomonas cepacia isolated from children with cystic fibrosis. Pediatr. Res. 20, 1174-1177 (1986).
84. Aronoff, S. C. Outer membrane permeability in Pseudomonas cepacia: diminished porin content in a β-lactam-resistant mutant and in resistant cystic fibrosis isolates. Antimicrob. Agents Chemother. 32, 1636-1639 (1988).
85. Burns, J. L., Hedin, L. A. & Lien, D. M. Chloramphenicol resistance in Pseudomonas cepacia because of decreased permeability. Antimicrob. Agents Chemother. 33, 136-141 (1989).
86. Beckman, W. & Lessie, T. G. Response of Pseudomonas cepacia to β-lactam antibiotics: utilization of penicillin G as the carbon source. J. Bacteriol. 140, 1126-1128 (1979).
87. Speert, D. P., Bond, M., Woodman, R. C. & Curnutte, J. T. Infection with Pseudomonas cepacia in chronic granulomatous disease: role of nonoxidative killing by neutrophils in host defense. J. Infect. Dis. 170, 1524-1531 (1994).
88. Goldstein, R. et al. Structurally variant classes of pilus appendage fibers coexpressed from Burkholderia (Pseudomonas) cepacia. J. Bacteriol. 177, 1039-1052 (1995).
89. + Pseudomonas (Burkholderia) cepacia causing CF centre epidemics in North America and Britain. Nature Med. 1, 661-666 (1995).
90. Sajjan, U., Wu, Y., Kent, G. & Forstner, J. Preferential adherence of cable-pillated Burkholderia cepacia to respiratory epithelia of CF knockout mice and human cystic fibrosis lung explants. J. Med. Microbiol. 49, 875-885. (2000).
91. Sakellaris, H. & Scott, J. R. New tools in an old trade: CS1 pilus morphogenesis. Mol. Microbiol. 30, 681-687 (1998).
92. Sajjan, U. S., Xie, H., Lefebre, M. D., Valvano, M. A. & Forstner, J. F. Identification and molecular analysis of cable pilus biosynthesis genes in Burkholderia cepacia. Microbiology 149, 961-971 (2003).
93. Koehler, D. R. et al. Protection of Cftr knockout mice from acute lung infection by a helper-dependent adenoviral vector expressing Cftr in airway epithelia. Proc. Natl Acad. Sci. USA 100, 15364-15369 (2003).
94. Tomich, M. & Mohr, C. D. Transcriptional and posttranscriptional control of cable pilus gene expression in Burkholderia cenocepacia. J. Bacteriol. 186, 1009-1020 (2004).
95. Sajjan, U. S., Corey, M., Karmali, M. A. & Forstner, J. F. Binding of Pseudomonas cepacia to normal human intestinal much and respiratory mucin from patients with cystic fibrosis. J. Clin. Invest. 89, 648-656 (1992).
96. Sajjan, S. U. & Forstner, J. F. Identification of the mucin-binding adhesin of Pseudomonas cepacia isolated from patients with cystic fibrosis. Infect. Immun. 60, 1434-1440 (1992).
97. Hales, B. A., Morgan, J. A., Hart, C. A. & Winstanley, C. Variation in flagellin genes and proteins of Burkholderia cepacia. J. Bacteriol. 180, 1110-1118 (1998).
98. Montie, T. C. & Stover, G. B. Isolation and characterization of flagellar preparations from Pseudomonas species. J. Clin. Microbiol. 18, 452-456 (1983).
99. Tomich, M., Herfst, C. A., Golden, J. W. & Mohr, C. D. Role of flagella in host cell invasion by Burkholderia cepacia. Infect. Immun. 70, 1799-1806 (2002).
100. Urban, T. A. et al. Contribution of Burkholderia cenocepacia flagella to infectivity and inflammation. Infect. Immun. 72, 5126-5134 (2004).
101. Hayashi, F. et al. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410, 1099-1103 (2001).
102. Hunt, T. A., Kooi, C., Sokol, P. A. & Valvano, M. A. Identification of Burkholderia cenocepacia genes required for bacterial survival in vivo. Infect. Immun. 72, 4010-4022 (2004).
103. McMenamin, J. D., Zaccone, T. M., Coenye, T., Vandamme, P. & LiPuma, J. J. Misidentification of Burkholderia cepacia in US cystic fibrosis treatment centers: an analysis of 1,051 recent sputum isolates. Chest 117, 1661-1665 (2000).
104. Miller, M. B. & Gilligan, P. H. Laboratory aspects of management of chronic pulmonary infections in patients with cystic fibrosis. J. Clin. Microbiol. 41, 4009-4015 (2003).
105. Mahenthiralingam, E. et al. 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 (2000).
106. Mahenthiralingam, E., Campbell, M. E., Henry, D. A. & Speert, D. P. Epidemiology of Burkholderia cepacia infection in patients with cystic fibrosis: analysis by randomly amplified polymorphic DNA fingerprinting. J. Clin. Microbiol. 34, 2914-2920. (1996).
107. Coenye, T., Spilker, T., Martin, A. & LiPuma, J. J. Comparative assessment of genotyping methods for epidemiologic study of Burkholderia cepacia genomovar III. J. Clin. Microbiol. 40, 3300-3307 (2002).
108. Speert, D. P., Steen, B., Halsey, K. & Kwan, E. A murine model for infection with Burkholderia cepacia with sustained persistence in the spleen. Infect. Immun. 67, 4027-4032 (1999).
109. Davidson, D. J. et al. Lung disease in the cystic fibrosis mouse exposed to bacterial pathogens. Nature Genet. 9, 351-357 (1995).
110. -/- mice. Infect. Immun. 69, 5138-5150 (2001).
111. 5-oxygenase. Infect. Immun. 67, 4443-4455 (1999).
112. Cieri, M. V., Mayer-Hamblett, N., Griffith, A. & Burns, J. L. Correlation between an in vitro invasion assay and a murine model of Burkholderia cepacia lung infection. Infect. Immun. 70, 1081-1086 (2002).
113. Chu, K. K., Davidson, D. J., Halsey, T. K., Chung, J. W. & Speert, D. P. Differential persistence among genomovars of the Burkholderia cepacia complex in a murine model of pulmonary infection. Infect. Immun. 70, 2715-2720 (2002).
114. Burns, J. L. et al. Invasion of respiratory epithelial calls by Burkholderia (Pseudomonas) cepacia. Infect. Immun. 64, 4054-4059 (1996).
115. Keig, P. M., Ingham, E. & Kerr, K. G. Invasion of human type II pneumocytes by Burkholderia cepacia. Microb. Pathog. 30, 167-170 (2001).
116. Schwab, U. et al. Patterns of epithelial cell invasion by different species of the Burkholderia cepacia complex in well-differentiated human airway epithelia. Infect. Immun. 70, 4547-4555 (2002).
117. Sajjan, U., Keshavjee, S. & Forstner, J. Responses of well-differentiated airway epithelial cell cultures from healthy donors and patients with cystic fibrosis to Burkholderia cenocepacia infection. Infect. Immun. 72, 4188-4199 (2004).
118. Sajjan, U., Ackerley, C. & Forstner, J. Interaction of cblA/adhesin-positive Burkholderia cepacia with squamous epithelium. Cell. Microbiol. 4, 73-86 (2002).
119. Saini, L. S., Galsworthy, S. B., John, M. A. & Valvano, M. A. Intracellular survival of Burkholderia cepacia complex isolates in the presence of macrophage cell activation. Microbiology 145, 3465-3475 (1999).
120. Marolda, C. L., Hauroder, B., John, M. A., Michel, R. & Valvano, M. A. Intracellular survival and saprophytic growth of isolates from the Burkholderia cepacia complex in free-living amoebae. Microbiology 145, 1509-1517 (1999).
121. Lamothe, J., Thyssen, S. & Valvano, M. A. Burkholderia cepacia complex isolates survive intracellularly without replication within acidic vacuoles of Acanthamoeba polyphaga. Cell. Microbiol. 6, 1127-1138 (2004).
122. Bernier, S. P., Silo-Suh, L., Woods, D. E., Ohman, D. E. & Sokol, P. A. Comparative analysis of plant and animal models for characterization of Burkholderia cepacia virulence. Infect. Immun. 71, 5306-5313 (2003).
123. Vandamme, P. et al. Burkholderia cenocepacia sp. nov. - a new twist to an old story. Res. Microbiol. 154, 91-96 (2003).
124. Coenye, T & LiPuma, J. J. Population structure analysis of Burkholderia cepacia genomovar III: varying degrees of genetic recombination characterize major clonal complexes. Microbiology 149, 77-88 (2003).
125. Vandamme, P. et al. Identification and population structure of Burkholderia stabilis sp nov (formerly Burkholderia cepacia genomovar IV). J. Clin. Microbiol. 38, 1042-1047 (2000).
126. Coenye, T. et al. Burkholderia cepacia genomovar VI, a new member of the Burkholderia cepacia complex isolated from cystic fibrosis patients. Int. J. Syst Evol. Microbiol. 51, 271-279 (2001).
127. Vermis, K. et al. Proposal to accommodate Burkholderia cepacia genomovar VI as Burkholderia dolosa sp. nov. Int J. Syst. Evol. Microbiol. 54, 689-691 (2004).
128. Coenye, T. et al. 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 (2001).
129. Vandamme, P. et al. Burkholderia anthina sp. nov. and Burkholderia pyrrocinia, two additional Burkholderia cepacia complex bacteria, may confound results of new molecular diagnostic tools. FEMS Immunol. Med. Microbiol. 33, 143-149 (2002).
130. Nzula, S., Vandamme, P. & Govan, J. R. Influence of taxonomic status on the in vitro antimicrobial susceptibility of the Burkholderia cepacia complex. J. Antimicrob. Chemother. 50, 265-269 (2002).
131. Tomich, M. & Mohr, C. D. Adherence and autoaggregation phenotypes of a Burkholderia cenocepacia cable pilus mutant. FEMS Microbiol. Lett. 228, 287-297 (2003).
132. Lefebre, M. & Valvano, M. In vitro resistance of Burkholderia cepacia complex isolates to reactive oxygen species in relation to catalase and superoxide dismutase production. Microbiology 147, 97-109 (2001).
133. Chung, J. W., Altman, E., Beveridge, T. J. & Speert, D. P. Colonial morphology of Burkholderia cepacia complex genomovar III: implications in exopolysaccharide production, pilus expression, and persistence in the mouse. Infect. Immun. 71, 904-909 (2003 ).
134. Sist, P. et al. Macromolecular and solution properties of Cepacian: the exopolysaccharide produced by a strain of Burkholderia cepacia isolated from a cystic fibrosis patient. Carbohydr. Res. 338, 1861-1867 (2003).
135. Conway, B. A., Chu, K. K., Bylund, J., Altman, E. & Speert, D. P. Production of exopolysaccharide by Burkholderia cenocepacia results in altered cell-surface interactions and altered bacterial clearance in mice. J. Infect. Dis. 190, 957-966 (2004).
136. Bevivino, A. et al. Burkholderia cepacia complex bacteria from clinical and environmental sources in Italy: genomovar status and distribution of traits related to virulence and transmissibility. J. Clin. Microbiol. 40, 846-851 (2002).
137. Corbett, C. R., Burtnick, M. N., Kool, C., Woods, D. E. & Sokol, P. A. An extracellular zinc metalloprotease gene of Burkholderia cepacia. Microbiology 149, 2263-2271 (2003).
138. Hutchison, M. L., Poxton, I. R. & Govan, J. R. Burkholderia cepacia produces a hemolysin that is capable of including apoptosis and degranulation of mammalian phagocytes. Infect. Immun. 66, 2033-2039 (1998).
139. Zughaier, S. M., Ryley, H. C. & Jackson, S. K. 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 (1999).
140. Visser, M. B., Majumdar, S., Hani, E. & Sokol, P. A. Importance of the ornibactin and pyochelin siderophore transport systems in Burkholderia cenocepacia lung infections. Infect. Immun. 72, 2850-2857 (2004).
141. Tomich, M., Griffith, A., Herfst, C. A., Burns, J. L. & Mohr, C. D. Attenuated virulence of a Burkholderia cepacia type III secretion mutant in a murine model of infection. Infect. Immun. 71, 1405-1415 (2003).
142. Glendinning, K. J. et al. Sequence divergence in type III secretion gene clusters of the Burkholderia cepacia complex. FEMS Microbiol. Lett. 235, 229-235 (2004).
143. Caroff, M. & Karibian, D. Structure of bacterial lipopolysaccharides. Carbohydr. Res. 338, 2431-2447 (2003).