Production of exopolysaccharide by Burkholderia cenocepacia results in altered cell-surface interactions and altered bacterial clearance in mice

Journal of Infectious Diseases

Volumn 190, Issue 5, 2004, Pages 957-966

  Conway, Barbara Ann D ^a   Chu, Karen K ^a   Bylund, Johan ^a   Altman, Eleonora ^b   Speert, David P ^a,c  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^c CHILDREN S AND WOMEN S HEALTH CENTRE OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL POLYSACCHARIDE; DEXTRAN; EXOPOLYSACCHARIDE; LACTONE DERIVATIVE; OCTANOYL HOMOSERINE LACTONE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BIOFILM; BURKHOLDERIA CEPACIA; CELL INTERACTION; CELL SURFACE; CYSTIC FIBROSIS; DNA POLYMORPHISM; FEMALE; GENE AMPLIFICATION; HOST PATHOGEN INTERACTION; HOST RESISTANCE; HUMAN; HUMAN CELL; LUNG INFECTION; MACROPHAGE; MOUSE; NEUTROPHIL; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; RANDOM AMPLIFIED POLYMORPHIC DNA; STRAIN DIFFERENCE;

4-BUTYROLACTONE; ANIMALS; BACTERIAL CAPSULES; BIOFILMS; BURKHOLDERIA CEPACIA COMPLEX; BURKHOLDERIA INFECTIONS; CYSTIC FIBROSIS; DISEASE MODELS, ANIMAL; ELECTROPHORESIS, GEL, PULSED-FIELD; FEMALE; HUMANS; MICE; MICE, INBRED BALB C; RANDOM AMPLIFIED POLYMORPHIC DNA TECHNIQUE;

EID: 4344671927     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1086/423141     Document Type: Article

References (59)

1. Govan JR, Brown PH, Maddison J. Evidence for transmission of Pseudomonas cepacia by social contact in cystic fibrosis. Lancet 1993; 342:15-9.
2. Isles A, Maclusky I, Corey M, et al. Pseudomonas cepacia infection in cystic fibrosis; an emerging problem. J Pediatr 1984; 104:206-10.
3. LiPuma JJ, Dasen SE, Nielson DW, Stern RC, Stall TL. Person-to-person transmission of Pseudomonas cepacia between patients with cystic fibrosis. Lancet 1990; 336:527-32.
4. Mahenthiralingam E, Bischof J, Byrne SK, 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 2000; 38:3165-73.
5. Cieri MV, Mayer-Hamblett N, Griffith A, Burns JL. Correlation between an in vitro invasion assay and a murine model of Burkholderia cepacia lung infection. Infect Immun 2002; 70:1081-6.
6. Keig PM, Ingham E, Vandamme PAR, Kerr KG. Differential invasion of respiratory epithelial cells by members of the Burkholderia cepacia complex. Clin Microbiol Infect 2002; 8:47-9.
7. Conway BA, Venu V, Speert DP. Biofilm formation and acyl-homoserine lactone production in the Burkholderia cepacia complex. J Bacteriol 2002; 184:5678-85.
8. Singh PK, Schaefer AL, Parsek MR, Moninger TO, Welsh MJ, Greenberg EP. Quorum sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 2000; 407:762-4.
9. Favre-Bonte S, Pache JC, Robert J, Blanc D, Pechere JC, van Delden C. Detection of Pseudomonas aeruginosa cell-to-cell signals in lung tissue of cystic fibrosis patients. Microb Pathog 2002; 32:143-7.
10. O'Toole G, Kaplan HB, Kolter R. Biofilm formation as microbial development. Annu Rev Microbiol 2000; 54:49-79.
11. Govan JRW, Deretic V. Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 1996; 60:539-74.
12. Deretic V, Schurr MJ, Boucher JC, Martin DW Conversion of Pseudomonas aeruginosa to mucoidy in cystic fibrosis: environmental stress and regulation of bacterial virulence by alternative sigma factors. J Bacteriol 1994; 176:2773-80.
13. Jesaitis AJ, Franklin MJ, Berglund D, et al. Compromised host defense on Pseudomonas aeruginosa biofilms: characterization of neutrophil and biofilm interactions. J Immunol 2003; 171:4329-39.
14. Cérantola S, Lemassu-Jacquier A, Montrozier H. Structural elucidation of a novel exopolysaccharide produced by a mucoid clinical isolate of Burkholderia cepacia. Eur J Biochem 1999; 260:373-83.
15. Richau JA, Leitao JH, Correia M, et al. Molecular typing and exopolysaccharide biosynthesis of Burkholderia cepacia isolates from a Portugese cystic fibrosis center. J Clin Microbiol 2000; 38:1651-5.
16. Chung JW, Altman E, Beveridge TJ, Speert DP. Colonial morphology of Burkholderia cepacia complex genomovar III: implications in exopolysaccharide production, pilus expression, and persistence in the mouse. Infect Immun 2003; 71:904-9.
17. Hareland W, Crawford RL, Chapman PJ, Dagley S. Metabolic function and properties of 4-hydroxyphenylacetic acid 1-hydroxylase from Pseudomonas acidovorans. J Bacteriol 1975; 121:272-85.
18. Mahenthiralingam E, Campbell ME, Henry DA, Speert DP. Epidemiology of Burkholderia cepacia infection in patients with cystic fibrosis: analysis by random amplified polymorphic DNA (RAPD) fingerprinting. J Clin Microbiol 1996; 34:2914-20.
19. Rodley PD, Romling U, Tummler B. A physical genome map of the Burkholderia cepacia type strain. Mol Microbiol 1995; 17:57-67.
20. Chu KK, Davidson DJ, Halsey TK, Chung JW, Speert DP. Differential persistence among genomovars of the Burkholderia cepacia complex in a murine model of pulmonary infection. Infect Immun 2002; 70:2715-20.
21. Boyum A, Lovhaug D, Tresland L, Nordlie EM. Separation of leucocytes: improved cell purity by fine adjustments of gradient medium density and osmolality. Scand J Immunol 1991; 34:697-712.
22. Davidson DJ, Currie AJ, Reid GS, et al. The cationic antimicrobial peptide LL-37 modulates dendritic cell differentiation and dendritic cell-induced T cell polarization. J Immunol 2004; 172:1146-56.
23. Sawardeker JH, Sloneker JH, Jeannes A. Quantitative determination of monosaccharides as their alditol acetates by gas liquid chromatography. Anal Chem 1967; 39:1602-14.
24. Hakomori SJ. A rapid permethylation of glycolipids and polysaccharides by methylsulfinyl carbanion in dimethyl sulfoxide. J Biochem (Tokyo) 1964; 55:205-8.
25. Sadovskaya I, Brisson J-R, Altman E, Mutharia LM. Structural studies of the lipopolysaccharide O-antigen and capsular polysaccharide of Vibrio anguillarum serotype O:2. Carbohydr Res 1996; 283:111-27.
26. Taylor RL, Conrad HE. Stoichiometric depolymerization of polyuronides and glycosaminoglycouronans to monosaccharides following reduction of their carbodiimide-activated carboxyl groups. Biochemistry 1972; 11:1383-8.
27. O'Toole GA, Kolter R. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 1998; 28:449-61.
28. Konstan MW, Berger M. Infection and inflammation of the lung in cystic fibrosis. In: Davis PB, ed. Cystic fibrosis. New York: Marcel Dekker, 1993:219-76.
29. Hancock RE, Mutharia LM, Chan L, Darveau RP, Speert DP, Pier GB. Pseudomonas aeruginosa isolates from patients with cystic fibrosis: a class of serum-sensitive, nontypeable strains deficient in lipopolysaccharide O side chains. Infect Immun 1983; 42:170-7.
30. Cérantola S, Marty N, Montrozier H. Structural studies of the acidic exopolysaccharide produced by a mucoid strain of Burkholderia cepacia, isolated from cystic fibrosis. Carbohydr Res 1996; 285:59-67.
31. Bock K, Pederson C, Pederson H. Carbon-13 nuclear magnetic resonance data for oligosaccharides. Adv Carbohydr Chem Biochem 1984; 42:193-225.
32. 2O. Bull Soc Chim Belg 1975; 84:721-34.
33. Cescutti P, Bosco M, Picotti F, et al. Structural study of the exopolysaccharide produced by a clinical isolate of Burkholderia cepacia. Biochem Biophys Res Comm 2000; 273:1088-94.
34. Huber B, Riedel K, Hentzer M, et al. The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology 2001; 147:2517-28.
35. Hentzer M, Teitzel GM, Balzer GJ, et al. Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J Bacteriol 2001; 183:5395-401.
36. Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 1998; 280:295-8.
37. Lewenza S, Conway B, Greenberg E, Sokol P. Quorum sensing in Burkholderia cepacia: identification of the LuxRI homologs CepRI. J Bacteriol 1999; 181:748-56.
38. Whiteley M, Lee KM, Greenberg EP. Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 1999; 96:13904-9.
39. Pearson JP, Gray KM, Passador L, et al. Structure of the autoinducer required for the expression of Pseudomonas aeruginosa virulence genes. Proc Natl Acad Sci USA 1994; 91:197-201.
40. Tenover FC, Arbeit RD, Goering RV, et al. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 1995; 33:2233-9.
41. Lessie TG, Hendrickson W, Manning BD, Devereux R. Genomic complexity and plasticity of Burkholderia cepacia. FEMS Microbiol Lett 1996; 144:117-28.
42. Mahenthiralingam E, Vandamme P, Campbell ME, 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 2001; 33:1469-75.
43. Boucher JC, Yu H, Mudd MH, Deretic V. Mucoid Pseudomonas aeruginosa in cystic fibrosis: characterization of muc mutations in clinical isolates and analysis of clearance in a mouse model of respiratory infection. Infect Immun 1997; 65:3838-46.
44. Yu H, Hanes M, Chrisp CE, Boucher JC, Deretic V. Microbial pathogenesis in cystic fibrosis: pulmonary clearance of mucoid Pseudomonas aeruginosa and inflammation in a mouse model of repeated respiratory challenge. Infect Immun 1998; 66:280-8.
45. Pedersen SS. Lung infection with alginate-producing, mucoid Pseudomonas aeruginosa in cystic fibrosis. APMIS Suppl 1992; 28:1-79.
46. Pier GB, Coleman F, Grout M, Franklin M, Ohman DE. Role of alginate O acetylation in resistance of mucoid Pseudomonas aeruginosa to opsonic phagocytosis. Infect Immun 2001; 69:1895-901.
47. Pedersen SS, Moller H, Espersen F, Sorensen CH, Jensen T, Hoiby N. Mucosal immunity to Pseudomonas aeruginosa alginate in cystic fibrosis. APMIS 1992; 100:326-34.
48. Barghouthi S, Guerdoud LM, Speert DP. Inhibition by dextran of Pseudomonas aeruginosa adherence to epithelial cells. Am J Respir Crit Care Med 1996; 154:1788-93.
49. Chiu CH, Wong S, Hancock RE, Speert DP. Adherence of Burkholderia cepacia to respiratory tract epithelial cells and inhibition with dextrans. Microbiology 2001; 147:2651-8.
50. Bryan R, Feldman M, Jawetz SC, et al. The effects of aerosolized dextran in a mouse model of Pseudomonas aeruginosa pulmonary infection. J Infect Dis 1999; 179:1449-58.
51. Lewenza S, Sokol PA. Regulation of ornibactin synthesis and N-acyl-L-homoserine lactone production by CepR in Burkholderia cepacia. J Bacteriol 2001; 183:2212-8.
52. Pearson JP, Pesci EC, Iglewski BH. Roles of Pseudomonas aeruginosa las and rh1 quorum-sensing systems in control of elastase and rhamnolipid biosynthesis. J Bacteriol 1997; 179:5756-67.
53. Marketon MM, Glenn SA, Eberhard A, Gonzalez JE. Quorum sensing controls exopolysaccharide production in Sinorhizobium meliloti. J Bacteriol 2003; 185:325-31.
54. Pellock BJ, Teplitski M, Boinay RP, Bauer WD, Walker GC. A LuxR homolog controls production of symbiotically active extracellular polysaccharide II by Sinorhizobium meliloti. J Bacteriol 2002; 184:5067-76.
55. Beck von Bodman S, Majerczak DR, Coplin DL. A negative regulator mediates quorum-sensing control of exopolysaccharide production in Pantoea stewartii subsp. stewartii. Proc Natl Acad Sci USA 1998; 95:7687-92.
56. Talaga P, Stahl B, Wieruszeski JM, et al. Cell-associated glucans of Burkholderia solanacearum and Xanthomonas campestris pv. citri: a new family of periplasmic glucans. J Bacteriol 1996; 178:2263-71.
57. 13C-NMR relaxation. Biopolymers 1991; 31:1581-92.
58. Rief M, Oesterhelt F, Heymann B, Gaub HE. Single molecule force spectroscopy on polysaccharides by atomic force microscopy. Science 1997; 275:1295-7.
59. Marszalek PE, Oberhauser AF, Pang YP, Fernandez JM. Polysaccharide elasticity governed by chair-boat transitions of the glucopyranose ring. Nature 1998; 396:661-4.