Genetic characterization of a multicomponent signal transduction system controlling the expression of cable pili in Burkholderia cenocepacia

Journal of Bacteriology

Volumn 186, Issue 12, 2004, Pages 3826-3836

  Tomich, Mladen ^a,c   Mohr, Christian D ^a,b  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; PHOSPHOTRANSFERASE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM PILUS; BURKHOLDERIA CEPACIA; CARBOXY TERMINAL SEQUENCE; CBLA GENE; CBLR GENE; CBLS GENE; CBLT GENE; CELL ORGANELLE; CYSTIC FIBROSIS; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC CODE; GENETIC TRANSCRIPTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; SIGNAL TRANSDUCTION;

BACTERIAL PROTEINS; BURKHOLDERIA CEPACIA COMPLEX; FIMBRIAE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN KINASES; SEQUENCE ANALYSIS, DNA; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); BURKHOLDERIA; BURKHOLDERIA CENOCEPACIA; BURKHOLDERIA CEPACIA; NEGIBACTERIA;

EID: 2942571208     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.12.3826-3836.2004     Document Type: Article

References (44)

1. Ansaldi, M., C. Jourlin-Castelli, M. Lepelletier, L. Theraulaz, and V. Mejean. 2001. Rapid dephosphorylation of the TorR response regulator by the TorS unorthodox sensor in Escherichia coli. J. Bacteriol. 183:2691-2695.
2. Boyd, J. M., T. Koga, and S. Lory. 1994. Identification and characterization of PilS, an essential regulator of pilin expression in Pseudomonas aeruginosa. Mol. Gen. Genet. 3:565-574.
3. Burbulys, D., K. A. Trach, and J. A. Hoch. 1991. Initiation of sporulation in Bacillus subtilis is controlled by a multicomponent phosphorelay. Cell 64:545-552.
4. Burkholder, W. H. 1950. Sour skin: a bacterial rot of onion bulbs. Phytopathology 40:115-117.
5. Butler, S., C. Doherty, J. Hughes, J. Nelson, and J. Govan. 1995. Burkholderia cepacia and cystic fibrosis: do natural environments present a potential hazard? J. Clin. Microbiol. 33:1001-1004.
6. Coenye, T., P. Vandamme, J. R. W. Govan, and J. J. LiPuma. 2001. Taxonomy and identification of the Burkholderia cepacia complex. J. Clin. Microbiol. 39:3427-3436.
7. Cotter, P. A., and A. M. Jones. 2003. Phosphorelay control of virulence gene expression in Bordetella. Trends Microbiol. 11:367-373.
8. DeShazer, D., and D. E. Woods. 1996. Broad-host-range cloning and cassette vectors based on the R388 trimethoprim resistance gene. BioTechniques 20:762-764.
9. Fabret, C., V. A. Feher, and J. A. Hoch. 1999. Two-component signal transduction in Bacillus subtilis: how one organism sees its world. J. Bacteriol. 181:1975-1983.
10. Fisher, S. L., W. Jiang, B. L. Wanner, and C. T. Walsh. 1995. Cross-talk between the histidine protein kinase VanS and the response regulator PhoB. Characterization and identification of a VanS domain that inhibits activation of PhoB. J. Biol. Chem. 270:23143-23149.
11. Freeman, J. A., and B. L. Bassler. 1999. Sequence and function of LuxU: a two-component phosphorelay protein that regulates quorum sensing in Vibrio harveyi. J. Bacteriol. 181:899-906.
12. Georgellis, D., O. Kwon, P. De Wulf, and E. C. Lin. 1998. Signal decay through a reverse phosphorelay in the Arc two-component signal transduction system. J. Biol. Chem. 273:32864-32869.
13. Gober, J. W., and L. Shapiro. 1992. A developmentally regulated Caulobacter flagellar promoter is activated by 3′ enhancer and IHF binding elements. Mol. Biol. Cell 3:913-926.
14. Govan, J. R. W., and V. Deretic. 1996. Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol. Rev. 60:539-574.
15. Grebe, T. W., and J. B. Stock. 1999. The histidine protein kinase superfamily. Adv. Microb. Physiol. 41:139-227.
16. Hoch, J. A. 2000. Two-component and phosphorelay signal transduction. Curr. Opin. Microbiol. 3:165-170.
17. Hung, D. L., T. L. Raivio, C. H. Jones, T. J. Silhavy, and S. J. Hultgren. 2001. Cpx signaling pathway monitors biogenesis and affects assembly and expression of P pili. EMBO J. 20:1508-1518.
18. Jiang, M., W. Shao, M. Perego, and J. A. Hoch. 2000. Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis. Mol. Microbiol. 38:535-542.
19. Jordi, B. J. A. M., B. Dagberg, L. A. M. de Haan, A. M. Hamers, B. A. M. van der Zeijst, W. Gaastra, and B. E. Uhlin. 1992. The positive regulator CfaD overcomes the repression mediated by histone-like protein H-NS (H1) in the CFA/ I fimbrial operon of Escherichia coli. EMBO J. 11:2627-2632.
20. Kwon, O., D. Georgellis, and E. C. Lin. 2000. Phosphorelay as the sole physiological route of signal transmission by the Arc two-component system of Escherichia coli. J. Bacteriol. 182:3858-3862.
21. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
22. Mahenthiralingam, E., A. Baldwin, and P. Vandamme. 2002. Burkholderia cepacia complex infection in patients with cystic fibrosis. J. Med. Microbiol. 51:533-538.
23. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
24. Murphree, D., B. Froehlich, and J. R. Scott. 1997. Transcriptional control of genes encoding CS1 pili: negative regulation by a silencer and positive regulation by Rns. J. Bacteriol. 179:5736-5743.
25. Raivio, T. L., and T. J. Silhavy. 1999. The sigmaE and Cpx regulatory pathways: overlapping but distinct envelope stress responses. Curr. Opin. Microbiol. 2:159-165.
26. Richardson, J., D. E. Stead, and R. H. Coutts. 2001. Incidence of the cblA major subunit pilin gene amongst Burkholderia species. FEMS Microbiol. Lett. 196:61-66.
27. Sajjan, U., L. Liu, A. Lu, T. Spilker, J. Forstner, and J. J. LiPuma. 2002. Lack of cable pili expression by cblA-containing Burkholderia cepacia complex. Microbiology 148:3477-3484.
28. Sajjan, U. S., M. Corey, M. A. Karmali, and J. F. Forstner. 1992. Binding of Pseudomonas cepacia to normal human intestinal mucin and respiratory mucin from patients with cystic fibrosis. J. Clin. Investig. 89:648-656.
29. Sajjan, U. S., and J. F. Forstner. 1992. Identification of the mucin-binding adhesin of Pseudomonas cepacia isolated from patients with cystic fibrosis. Infect. Immun. 60:1434-1440.
30. Sajjan, U. S., L. Sun, R. Goldstein, and J. F. Forstner. 1995. 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.
31. Sajjan, U. S., F. A. Sylvester, and J. F. Forstner. 2000. Cable-piliated Burkholderia cepacia binds to cytokeratin 13 of epithelial cells. Infect. Immun. 68:1787-1795.
32. Sajjan, U. S., H. Xie, M. D. Lefebre, M. A. Valvano, and J. F. Forstner. 2003. Identification and molecular analysis of cable pilus biosynthesis genes in Burkholderia cepacia. Microbiology 149:961-971.
33. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
34. Simon, R., U. Priefer, and A. Puhler. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Bio/Technology 1:784-790.
35. Stock, A. M., V. L. Robinson, and P. N. Goudreau. 2000. Two-component signal transduction. Annu. Rev. Biochem. 69:183-215.
36. + Pseudomonas (Burkholderia) cepacia causing CF centre epidemics in North America and Britain. Nat. Med. 1:661-666.
37. Taha, M. K., B. Dupuy, W. Saurin, M. So, and C. Marchal. 1991. Control of pilus expression in Neisseria gonorrhoeae as an original system in the family of two-component regulators. Mol. Microbiol. 5:137-148.
38. Takeda, S.-I., Y. Fujisawa, M. Matsubara, H. Alba, and T. Mizuno. 2001. A novel feature of the multistep phosphorelay in Escherichia coli: a revised model of the RcsC→YojN→RcsB signalling pathway implicated in capsular synthesis and swarming behaviour. Mol. Microbiol. 40:440-450.
39. Tomich, M., C. A. Herfst, J. W. Golden, and C. D. Mohr. 2002. Role of flagella in Burkholderia cepacia host cell invasion. Infect. Immun. 70:1799-1806.
40. Tomich, M., and C. D. Mohr. 2003. Adherence and autoaggregation phenotypes of a Burkholderia cenocepacia cable pilus mutant. FEMS Microbiol. Lett. 228:287-297.
41. Tomich, M., and C. D. Mohr. 2004. Transcriptional and posttranscriptional control of cable pilus gene expression in Burkholderia cenocepacia. J. Bacteriol. 186:1009-1020.
42. Uhl, M. A., and J. F. Miller. 1996. Integration of multiple domains in a two-component sensor protein: the Bordetella pertussis BvgAS phosphorelay. EMBO J. 15:1028-1036.
43. Vandamme, P., B. Holmes, T. Coenye, J. Goris, E. Mahenthiralingam, J. J. LiPuma, and J. R. Govan. 2003. Burkholderia cenocepacia sp. nov. - a new twist to an old story. Res. Microbiol. 154:91-96.
44. Verhamme, D. T., J. C. Arents, P. W. Postma, W. Crielaard, and K. J. Hellingwerf. 2002. Investigation of in vivo cross-talk between key two-component systems of Escherichia coli. Microbiology 148:69-78.