Temperature-regulated microcolony formation by Burkholderia pseudomallei requires pilA and enhances association with cultured human cells

Infection and Immunity

Volumn 74, Issue 9, 2006, Pages 5374-5381

  Boddey, Justin A ^a,b   Flegg, Cameron P ^a   Day, Chris J ^a   Beacham, Ifor R ^a   Peak, Ian R ^a  

^a GRIFFITH UNIVERSITY   (Australia)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL COLONIZATION; BACTERIUM ADHERENCE; BACTERIUM PILUS; BURKHOLDERIA PSEUDOMALLEI; CELL CULTURE; COLONY FORMATION; DISEASE TRANSMISSION; ENDEMIC DISEASE; GENOME ANALYSIS; HOST RESISTANCE; HUMAN; HUMAN CELL; INFECTION CONTROL; MELIOIDOSIS; PATHOGENESIS; PRIORITY JOURNAL; SEQUENCE ANALYSIS; THERMOREGULATION; TRANSCRIPTION REGULATION;

BACTERIAL ADHESION; BIOFILMS; BURKHOLDERIA PSEUDOMALLEI; CELLS, CULTURED; FIMBRIAE PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; POLYVINYL CHLORIDE; TEMPERATURE; TRANSCRIPTION, GENETIC; VARIATION (GENETICS);

EID: 33748068125     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00569-06     Document Type: Article

References (53)

1. Ahmed, K., H. D. R. Enciso, H. Masaki, M. Tao, A. Omori, P. Tharavichikul, and T. Nagatake. 1999. Attachment of Burkholderia pseudomallei to pharyngeal epithelial cells: a highly pathogenic bacteria with low attachment ability. Am. J. Trop. Med. Hyg. 60:90-93.
2. Anuntagool, N., P. Aramsri, T. Panichakul, V. R. Wuthiekanun, R. Ki-noshita, N. J. White, and S. Sirisinha. 2000. Antigenic heterogeneity of lipopolysaccharide among Burkholderia pseudomallei clinical isolates. Southeast Asian J. Trop. Med. Public Health 31:46-152.
3. Bieber, D. S., S. W. Ramer, C.-Y. Wu, M. W. J. T. Toru, R. E. Fernandez, and G. K. Schoolnik. 1998. Type IV pili, transient bacterial aggregates and virulence of enterpathogenic Escherichia coli. Science 280:2114-2118.
4. Brett, P. J., D. DeShazer, and D. E. Woods. 1997. Characterization of Burkholderia pseudomallei and Burkholderia pseudomallei-like strains. Epidemiol. Infect. 118:137-148.
5. Brown, N. F., and I. R. Beacham. 2000. Cloning and analysis of genomic differences unique to Burkholderia pseudomallei by comparison with B. thailandensis. J. Med. Microbiol. 49:993-1001.
6. Brown, N. F., J. A. Boddey, C. P. Flegg, and I. R. Beacham. 2002. Adherence of Burkholderia pseudomallei cells to cultured human epithelial cell lines is regulated by growth temperature. Infect. Immun. 70:974-980.
7. Costerton, J. W., P. S. Stewart, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322.
8. Craig, L., M. E. Pique, and J. A. Tainer. 2004. Type IV pilus structure and bacterial pathogenicity. Nat. Rev. Microbiol. 2:363-378.
9. Currie, B. J. 2000. Melioidosis: an Australian perspective of an emerging infectious disease, vol. 8. Australian Society for Microbiology, Melbourne, Australia.
10. Currie, B. J., D. A. Fisher, D. M. Howard, J. N. Burrow, S. Selvanayagam, P. L. Snelling, N. M. Anstey, and M. J. Mayo. 2000. The epidemiology of melioidosis in Australia and Papua New Guinea. Acta Trop. 74:121-127.
11. Currie, B. J., D. A. Fisher, D. M. Howard, J. N. C. Burrow, D. Lo, S. Selva-nayagam, N. M. Anstey, S. E. Huffam, P. L. Snelling, P. J. Marks, D. P. Stephens, G. D. Lum, S. P. Jacups, and V. L. Krause. 2000. Endemic melioidosis in tropical northern Australia: a 10-year prospective study and review of the literature. Clin. Infect. Dis. 31:981-986.
12. Dance, D. A. B. 1990. Melioidosis. Rev. Med. Microbiol. 1:143-150.
13. Dance, D. A. B. 2000. Melioidosis as an emerging global problem. Acta Trop. 74:115-119.
14. Day, C. J., M. S. Kim, S. R. Stephens, W. E. Simcock, C. J. Aitken, G. C. Nicholsen, and N. A. Morrison. 2004. Gene array identification of osteoclast genes: differential inhibition of osteoclastogenesis by cyclosporin A and granulocyte macrophage colony stimulating factor. J. Cell. Biochem. 91:303-315.
15. Deghmane, A.-E., D. Giorgini, L. Maigre, and M.-K. Taha. 2004. Analysis in vitro and in vivo of the transcriptional regulator CrgA of Neisseria meningitidis upon contact with target cells. Mol. Microbiol. 53:917-927.
16. Dehio, C., M. Meyer, J. Berger, H. Schwarz, and C. Lanz. 1997. Interaction of Bartonella henselae with endothelial cells results in bacterial aggregation on the cell surface and the subsequent engulfment and internalisation of the bacterial aggregate by a unique structure, the invasome. J. Cell Sci. 110:2141-2154.
17. Ellis, J. F., and R. W. Titball. 1999. Burkholderia pseudomallei: medical, veterinary and environmental aspects. Infect. Dis. Rev. 1:174-181.
18. Essex-Lopresti, A. E., J. A. Boddey, R. Thomas, M. P. Smith, M. G. Hartley, T. Atkins, N. F. Brown, C. H. Tsang, I. R. A. Peak, J. Hill, I. R. Beacham, and R. W. Titball. 2005. A type IV pilin, PilA, contributes to adherence of Burkholderia pseudomallei and virulence in vivo. Infect. Immun. 73:1260-1264.
19. Falkow, S., R. R. Isberg, and D. A. Portnoy. 1992. The interaction of bacteria with mammalian cells. Annu. Rev. Cell Biol. 8:333-363.
20. Finlay, B. B., and S. Falkow. 1997. Common themes in microbial pathogenicity revisited. Microbiol. Mol. Biol. Rev. 61:136-169.
21. Fux, C. A., J. W. Costerton, P. S. Stewart, and P. Stoodley. 2005. Survival strategies of infectious biofilms. Trends Microbiol. 13:34-40.
22. Gori, A. H., K. Ahmed, G. Martinez, H. Masaki, K. Watanabe, and T. Nagatake. 1999. Mediation of attachment of Burkholderia pseudomallei to human pharyngeal epithelial cells by the asialoganglioside GM1-GM2 receptor complex. Am. J. Trop. Med. Hyg. 61:473-475.
23. Guard, R. W., F. A. Khafagi, M. C. Brigden, and L. R. Ashdown. 1984. Melioidosis in Far North Queensland. A clinical and epidemiological review of twenty cases. Am. J. Trop. Med. Hyg. 33:467-473.
24. Holden, M. T. G., R. W. Titball, S. J. Peacock, A. M. Cerdeno-Tarraga, T. Atkins, L. C. Crossman, T. L. Pitt, C. Churcher, K. Mungall, S. D. Bentley, M. Sebaihia, N. R. Thomson, N. Bason, I. R. Beacham, K. Brooks, K. A. Brown, N. F. Brown, G. L. Challis, I. Cherevach, T. Chillingworth, A. Cronin, B. Crossett, P. Davis, D. DeShazer, T. Feltwell, A. Fraser, Z. Hance, H. Hauser, S. Holroyd, K. Jagels, K. E. Keith, M. Maddison, S. Moule, C. Price, M. A. Quail, E. Rabbinowitsch, K. Rutherford, M. Sanders, M. Simmonds, S. Songsivilai, K. Stevens, S. Tumapa, M. Vesaratchavest, S. Whitehead, C. Yeats, B. G. Barrell, P. C. F. Osyston, and J. Parkhill. 2004. Genomic plasticity of the causative agent of melioidosis, Burkholderia pseudomallei. Proc. Natl. Acad. Sci. USA 101:14240-14245.
25. Howe, C., A. Sampath, and M. Spotnitz. 1971. The Pseudomallei group: a review. J. Infect. Dis. 124:598-606.
26. Hultgren, S. J., S. Abraham, M. Caparon, P. Falk, J. W. St. Geme III, and S. Normark. 1993. Pilus and nonpilus bacterial adhesins: assembly and function in cell recognition. Cell 73:887-901.
27. Kanai, K., Y. Suzuki, E. Kondo, Y. Maejima, D. Miyamoto, T. Suzuki, and T. Kurata. 1997. Specific binding of Burkholderia pseudomallei cells and their cell surface acid phosphatase to gangliotetraosylceramide (asialo GM1) and gangliotriaosylceramide (asialo GM2). Southeast Asian J. Trop. Med. Public Health 28:781-790.
28. Kespichayawattana, W., P. Intachote, P. Utaisincharoen, and S. Sirisinha. 2004. Virulent Burkholderia pseudomallei is more efficient than avirulent Burkholderia thailandensis in invasion of and adherence to cultured human epithelial cells. Microb. Pathog. 36:287-292.
29. Kirn, T. J., M. J. Lafferty, C. M. Sandoe, and R. K. Taylor. 2000. Delineation of pilin domains required for bacterial association into microcolonies and intestinal colonization by Vibrio cholerae. Mol. Microbiol. 35:896-910.
30. Klemm, P., L. Hjerrild, M. Gjermansen, and M. A. Schembri. 2004. Structure-function analysis of the self-recognising antigen 43 autotransporter protein from Escherichia coli. Mol. Microbiol. 51:283-296.
31. Korbsrisate, S., M. Vanaporn, P. Kerdsuk, W. Kespichayawattana, P. Vattanaviboon, P. Kiatpapan, and G. Lertmemongkolchai. 2005. The Burkholderia pseudomallei RpoE (AlgU) operon is involved in environmental stress tolerance and biofilm formation. FEMS Microbiol. Lett. 252:243-249.
32. Leelarasamee, A., and S. Bovornkitti. 1989. Melioidosis: review and update. Rev. Infect. Dis. 11:413-425.
33. Loprasert, S., R. Sallabhan, W. Whangsuk, and S. Mongkolsuk. 2002. The Burkholderia pseudomallei oxyR gene: expression analysis and mutant characterisation. Gene 296:161-169.
34. Marenda, M., B. Brito, D. Callard, S. Genin, P. Barberis, C. Boucher, and M. Arlat. 1998. PrhA controls a novel regulatory pathway required for the specific induction of Ralstonia solanacearum hrp genes in the presence of plant cells. Mol. Microbiol. 27:437-453.
35. Matz, C., T. Bergfeld, S. A. Rice, and S. Kjelleberg. 2004. Microcolonies, quorum sensing and cytotoxicity determine the survival of Pseudomonas aeruginosa biofilms exposed to protozoan grazing. Environ. Microbiol. 6:218-226.
36. Merz, A. J., and M. So. 2000. Interactions of pathogenic Neisseriae with epithelial cell membranes. Annu. Rev. Dev. Biol. 16:423-457.
37. Milton, D. L., R. O'Toole, P. Horstedt, and H. Wolf-Watz. 1996. Flagellin A is essential for the virulence of Vibrio anguillarum. J. Bacteriol. 178:1310-1319.
38. O'Toole, G., H. B. Kaplan, and R. Kolter. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:49-79.
39. O'Toole, G. A., and R. Kolter. 1998. Flagella and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295-304.
40. Ou, K., C. Ong, S. Y. Koh, F. Rodrigues, S. H. Sim, D. Wong, C. H. Ooi, K. C. Ng, H. Jikuya, C. C. Yau, S. Y. Soon, D. Kesuma, M. A. Lee, and P. Tan. 2005. Integrative genomic, transcriptional, and proteomic diversity in natural isolates of the human pathogen Burkholderia pseudomallei. J. Bacteriol. 187:4276-4285.
41. Penfold, R. J., and J. M. Pemberton. 1992. An improved suicide vector for the construction of chromosomal insertion mutations in bacteria. Gene 118:145-146.
42. Reisner, A., N. Hoiby, T. Tolker-Nielsen, and S. Molin. 2005. Microbial pathogenesis and biofilm development. Contrib. Microbiol. 12:114-131.
43. Rosenau, A., P. Y. Sizaret, J. M. Musser, A. Godeau, and R. Quentin. 1993. Adherence to human cells of a cryptic Haemophilus genospecies responsible for genital and neonatal infections. Infect. Immun. 61:4112-4118.
44. Taweechaisupapong, S., C. Kaewpa, C. Arunyanart, P. Kanla, P. Homchampa, S. Sirishna, T. Proungvitaya, and S. Wongratanacheewin. 2005. Virulence of Burkholderia pseudomallei does not correlate with biofilm formation. Microb. Pathog. 3:77-85.
45. Thomas, R., and T. Brooks. 2004. Common oligosaccharide moieties inhibit the adherence of typical and atypical respiratory pathogens. J. Med. Microbiol. 53:833-840.
46. Tobe, T., and C. Sasakawa. 2001. Role of bundle-forming pilus of enteropathogenic Escherichia coli in host cell adherence and in microcolony development. Cell. Microbiol. 3:579-585.
47. Ulett, G. C., B. J. Currie, T. W. Clair, M. Mayo, N. Ketheesan, J. Labrooy, D. Gal, R. Norton, C. A. Smith, J. Barnes, J. Warner, and R. G. Hirst 2001. Burkholderia pseudomallei virulence: definition, stability and association with clonality. Microbes Infect. 3:621-631.
48. Vorachit, M., P. Chongtrakool, S. Arkomsean, and S. Boonsong. 2000. Antimicrobial resistance in Burkholderia pseudomallei. Acta Trop. 74:139-144.
49. Vorachit, M., K. Lam, P. Jayanetra, and J. W. Costerton. 1995. Electron microscopy study of the mode of growth of Pseudomonas pseudomallei in vitro and in vivo. J. Trop. Med. Hyg. 98:379-391.
50. Vorachit, M., K. Lam, P. Jayanetra, and J. W. Costerton. 1993. Resistance of Pseudomaonas pseudomallei growing as a biofilm on silastic discs to ceftazidime and co-trimoxazole. Antimicrob. Agents Chemother. 37:2000-2002.
51. White, N. J. 2003. Melioidosis. Lancet 361:1715-1722.
52. Wiersinga, W. J., T. van der Poll, N. J. White, N. P. Day, and S. J. Peacock. 2006. Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei. Nat. Rev. Microbiol. 4:272-282.
53. Woods, D. E. 2002. The use of animal infection models to study the pathogenesis of melioidosis and glanders. Trends Microbiol. 10:483-484.