Mannitol promotes adherence of an outbreak strain of Burkholderia multivorans via an exopolysaccharide-independent mechanism that is associated with upregulation of newly identified fimbrial and afimbrial adhesins

Microbiology (United Kingdom)

Volumn 159, Issue 4, 2013, Pages 771-781

  Denman, Carmen C ^a   Brown, Alan R ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EXOPOLYSACCHARIDE; FIBRONECTIN; MANNITOL; MUCIN;

ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIUM ADHERENCE; BACTERIUM ISOLATE; BURKHOLDERIA MULTIVORANS; CYSTIC FIBROSIS; DNA SEQUENCE; GENE LOCUS; HUMAN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

ADHESINS, BACTERIAL; ANIMALS; BACTERIAL ADHESION; BURKHOLDERIA; BURKHOLDERIA INFECTIONS; CYSTIC FIBROSIS; DISEASE MODELS, ANIMAL; DISEASE OUTBREAKS; FIMBRIAE, BACTERIAL; HUMANS; LEPIDOPTERA; MANNITOL; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; UP-REGULATION;

BURKHOLDERIA CEPACIA COMPLEX; BURKHOLDERIA MULTIVORANS;

EID: 84875726087     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.064832-0     Document Type: Article

References (46)

1. Acord, J., Maskell, J. & Sefton, A. (2005). A rapid microplate method for quantifying inhibition of bacterial adhesion to eukaryotic cells. J Microbiol Methods 60, 55-62.
2. Ammendolia, M. G., Bertuccini, L., Iosi, F., Minelli, F., Berlutti, F., Valenti, P. & Superti, F. (2010). Bovine lactoferrin interacts with cable pili of Burkholderia cenocepacia. Biometals 23, 531-542.
3. Balder, R., Lipski, S., Lazarus, J. J., Grose, W., Wooten, R. M., Hogan, R. J., Woods, D. E. & Lafontaine, E. R. (2010). Identification of Burkholderia mallei and Burkholderia pseudomallei adhesins for human respiratory epithelial cells. BMC Microbiol 10, 250.
4. Baldwin, A., Mahenthiralingam, E., Thickett, K. M., Honeybourne, D., Maiden, M. C., Govan, J. R., Speert, D. P., Lipuma, J. J., Vandamme, P. & Dowson, C. G. (2005). Multilocus sequence typing scheme that provides both species and strain differentiation for the Burkholderia cepacia complex. J Clin Microbiol 43, 4665-4673.
5. Baldwin, A., Mahenthiralingam, E., Drevinek, P., Pope, C., Waine, D. J., Henry, D. A., Speert, D. P., Carter, P., Vandamme, P. & other authors (2008). Elucidating global epidemiology of Burkholderia multivorans in cases of cystic fibrosis by multilocus sequence typing. J Clin Microbiol 46, 290-295.
6. Bartholdson, S. J., Brown, A. R., Mewburn, B. R., Clarke, D. J., Fry, S. C., Campopiano, D. J. & Govan, J. R. (2008). Plant host and sugar alcohol induced exopolysaccharide biosynthesis in the Burkholderia cepacia complex. Microbiology 154, 2513-2521.
7. Bilton, D., Robinson, P., Cooper, P., Gallagher, C. G., Kolbe, J., Fox, H., Jaques, A., Charlton, B. & CF301 Study Investigators (2011). Inhaled dry powder mannitol in cystic fibrosis: an efficacy and safety study. Eur Respir J 38, 1071-1080.
8. Brisse, S., Cordevant, C., Vandamme, P., Bidet, P., Loukil, C., Chabanon, G., Lange, M. & Bingen, E. (2004). Species distribution and ribotype diversity of Burkholderia cepacia complex isolates from French patients with cystic fibrosis. J Clin Microbiol 42, 4824- 4827.
9. Bylund, J., Burgess, L. A., Cescutti, P., Ernst, R. K. & Speert, D. P. (2006). Exopolysaccharides from Burkholderia cenocepacia inhibit neutrophil chemotaxis and scavenge reactive oxygen species. J Biol Chem 281, 2526-2532.
10. Clode, F. E., Kaufmann, M. E., Malnick, H. & Pitt, T. L. (2000). Distribution of genes encoding putative transmissibility factors among epidemic and nonepidemic strains of Burkholderia cepacia from cystic fibrosis patients in the United Kingdom. J Clin Microbiol 38, 1763-1766.
11. Coenye, T. & Vandamme, P. (2003). Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ Microbiol 5, 719-729.
12. Conway, B. A., Chu, K. K., Bylund, J., Altman, E. & Speert, D. P. (2004). Production of exopolysaccharide by Burkholderia cenocepacia results in altered cell-surface interactions and altered bacterial clearance in mice. J Infect Dis 190, 957-966.
13. Cunha, M. V., Sousa, S. A., Leitão, J. H., Moreira, L. M., Videira, P. A. & Sá-Correia, I. (2004). Studies on the involvement of the exopolysaccharide produced by cystic fibrosis-associated isolates of the Burkholderia cepacia complex in biofilm formation and in persistence of respiratory infections. J Clin Microbiol 42, 3052-3058.
14. Daviskas, E., Anderson, S. D., Jaques, A. & Charlton, B. (2010). Inhaled mannitol improves the hydration and surface properties of sputum in patients with cystic fibrosis. Chest 137, 861-868.
15. Ferreira, A. S., Leitão, J. H., Silva, I. N., Pinheiro, P. F., Sousa, S. A., Ramos, C. G. & Moreira, L. M. (2010). Distribution of cepacian biosynthesis genes among environmental and clinical Burkholderia strains and role of cepacian exopolysaccharide in resistance to stress conditions. Appl Environ Microbiol 76, 441-450.
16. Figurski, D. H. & Helinski, D. R. (1979). Replication of an origincontaining derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci U S A 76, 1648-1652.
17. Flannagan, R. S., Aubert, D., Kooi, C., Sokol, P. A. & Valvano, M. A. (2007). Burkholderia cenocepacia requires a periplasmic HtrA protease for growth under thermal and osmotic stress and for survival in vivo. Infect Immun 75, 1679-1689.
18. Flannagan, R. S., Linn, T. & Valvano, M. A. (2008). A system for the construction of targeted unmarked gene deletions in the genus Burkholderia. Environ Microbiol 10, 1652-1660.
19. 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.
20. Hodak, H., Wohlkönig, A., Smet-Nocca, C., Drobecq, H., Wieruszeski, J. M., Sénéchal, M., Landrieu, I., Locht, C., Jamin, M. & Jacob-Dubuisson, F. (2008). The peptidyl-prolyl isomerase and chaperone Par27 of Bordetella pertussis as the prototype for a new group of parvulins. J Mol Biol 376, 414-426.
21. Jaques, A., Daviskas, E., Turton, J. A., McKay, K., Cooper, P., Stirling, R. G., Robertson, C. F., Bye, P. T., Lesouëf, P. N. & other authors (2008). Inhaled mannitol improves lung function in cystic fibrosis. Chest 133, 1388-1396.
22. Jones, A. M., Dodd, M. E., Govan, J. R., Barcus, V., Doherty, C. J., Morris, J. & Webb, A. K. (2004). Burkholderia cenocepacia and Burkholderia multivorans: influence on survival in cystic fibrosis. Thorax 59, 948-951.
23. Kalish, L. A., Waltz, D. A., Dovey, M., Potter-Bynoe, G., McAdam, A. J., Lipuma, J. J., Gerard, C. & Goldmann, D. (2006). Impact of Burkholderia dolosa on lung function and survival in cystic fibrosis. Am J Respir Crit Care Med 173, 421-425.
24. Kim, J. F., Ham, J. H., Bauer, D. W., Collmer, A. & Beer, S. V. (1998). The hrpC and hrpN operons of Erwinia chrysanthemi EC16 are flanked by plcA and homologs of hemolysin/adhesin genes and accompanying activator/transporter genes. Mol Plant Microbe Interact 11, 563-567.
25. Liou, T. G., Adler, F. R., Fitzsimmons, S. C., Cahill, B. C., Hibbs, J. R. & Marshall, B. C. (2001). Predictive 5-year survivorship model of cystic fibrosis. Am J Epidemiol 153, 345-352.
26. LiPuma, J. J. (2010). The changing microbial epidemiology in cystic fibrosis. Clin Microbiol Rev 23, 299-323.
27. Loutet, S. A. & Valvano, M. A. (2010). A decade of Burkholderia cenocepacia virulence determinant research. Infect Immun 78, 4088- 4100.
28. 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.
29. Mil-Homens, D. & Fialho, A. M. (2012). A BCAM0223 mutant of Burkholderia cenocepacia is deficient in hemagglutination, serum resistance, adhesion to epithelial cells and virulence. PLoS ONE 7, e41747.
30. Mil-Homens, D., Rocha, E. P. & Fialho, A. M. (2010). Genome-wide analysis of DNA repeats in Burkholderia cenocepacia J2315 identifies a novel adhesin-like gene unique to epidemic-associated strains of the ET-12 lineage. Microbiology 156, 1084-1096.
31. NØrskov-Lauritsen, N., Johansen, H. K., Fenger, M. G., Nielsen, X. C., Pressler, T., Olesen, H. V. & HØiby, N. (2010). Unusual distribution of Burkholderia cepacia complex species in Danish cystic fibrosis clinics may stem from restricted transmission between patients. J Clin Microbiol 48, 2981-2983.
32. Robinson, M., Daviskas, E., Eberl, S., Baker, J., Chan, H. K., Anderson, S. D. & Bye, P. T. (1999). The effect of inhaled mannitol on bronchial mucus clearance in cystic fibrosis patients: a pilot study. Eur Respir J 14, 678-685.
33. Rojas, C. M., Ham, J. H., Deng, W. L., Doyle, J. J. & Collmer, A. (2002). HecA, a member of a class of adhesins produced by diverse pathogenic bacteria, contributes to the attachment, aggregation, epidermal cell killing, and virulence phenotypes of Erwinia chrysanthemi EC16 on Nicotiana clevelandii seedlings. Proc Natl Acad Sci U S A 99, 13142-13147.
34. Sage, A., Linker, A., Evans, D. J. & Lessie, T. G. (1990). Hexose phosphate metabolism and exopolysaccharide formation in Pseudomonas cepacia. Curr Microbiol 20, 191-198.
35. Sajjan, S. U. & Forstner, J. F. (1992). Identification of the mucinbinding adhesin of Pseudomonas cepacia isolated from patients with cystic fibrosis. Infect Immun 60, 1434-1440.
36. Seed, K. D. & Dennis, J. J. (2008). Development of Galleria mellonella as an alternative infection model for the Burkholderia cepacia complex. Infect Immun 76, 1267-1275.
37. Sokurenko, E. V., Chesnokova, V., Dykhuizen, D. E., Ofek, I., Wu, X. R., Krogfelt, K. A., Struve, C., Schembri, M. A. & Hasty, D. L. (1998). Pathogenic adaptation of Escherichia coli by natural variation of the FimH adhesin. Proc Natl Acad Sci U S A 95, 8922-8926.
38. Teper, A., Jaques, A. & Charlton, B. (2011). Inhaled mannitol in patients with cystic fibrosis: a randomised open-label dose response trial. J Cyst Fibros 10, 1-8.
39. Urban, T. A., Goldberg, J. B., Forstner, J. F. & Sajjan, U. S. (2005). Cable pili and the 22-kilodalton adhesin are required for Burkholderia cenocepacia binding to and transmigration across the squamous epithelium. Infect Immun 73, 5426-5437.
40. Varga, J. J., Losada, L., Zelazny, A. M., Brinkac, L., Harkins, D., Radune, D., Hostetler, J., Sampaio, E. P., Ronning, C. M. & other authors (2012). Draft genome sequence determination for cystic fibrosis and chronic granulomatous disease Burkholderia multivorans isolates. J Bacteriol 194, 6356-6357.
41. Vial, L., Chapalain, A., Groleau, M. C. & Déziel, E. (2011). The various lifestyles of the Burkholderia cepacia complex species: a tribute to adaptation. Environ Microbiol 13, 1-12.
42. Weissman, S. J., Chattopadhyay, S., Aprikian, P., Obata-Yasuoka, M., Yarova-Yarovaya, Y., Stapleton, A., Ba-Thein, W., Dykhuizen, D., Johnson, J. R. & Sokurenko, E. V. (2006). Clonal analysis reveals high rate of structural mutations in fimbrial adhesins of extraintestinal pathogenic Escherichia coli. Mol Microbiol 59, 975-988.
43. Whiteford, M. L., Wilkinson, J. D., McColl, J. H., Conlon, F. M., Michie, J. R., Evans, T. J. & Paton, J. Y. (1995). Outcome of Burkholderia (Pseudomonas) cepacia colonisation in children with cystic fibrosis following a hospital outbreak. Thorax 50, 1194-1198.
44. Winsor, G. L., Khaira, B., Van Rossum, T., Lo, R., Whiteside, M. D. & Brinkman, F. S. (2008). The Burkholderia Genome Database: facilitating flexible queries and comparative analyses. Bioinformatics 24, 2803-2804.
45. Zlosnik, J. E., Hird, T. J., Fraenkel, M. C., Moreira, L. M., Henry, D. A. & Speert, D. P. (2008). Differential mucoid exopolysaccharide production by members of the Burkholderia cepacia complex. J Clin Microbiol 46, 1470-1473.
46. Zlosnik, J. E., Costa, P. S., Brant, R., Mori, P. Y., Hird, T. J., Fraenkel, M. C., Wilcox, P. G., Davidson, A. G. & Speert, D. P. (2011). Mucoid and nonmucoid Burkholderia cepacia complex bacteria in cystic fibrosis infections. Am J Respir Crit Care Med 183, 67-72.