Burkholderia cenocepacia requires the RpoN sigma factor for biofilm formation and intracellular trafficking within macrophages

Infection and Immunity

Volumn 76, Issue 3, 2008, Pages 1059-1067

  Saldías, M Soledad ^a   Lamothe, Julie ^a   Wu, Robert ^a   Valvano, Miguel A ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

RED FLUORESCENT PROTEIN; SIGMA FACTOR RPON; VIRULENCE FACTOR; RPON PROTEIN, BURKHOLDERIA CENOCEPACIA; SIGMA FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL GENE; BACTERIAL MEMBRANE; BACTERIAL VIRULENCE; BIOFILM; BIOSYNTHESIS; BURKHOLDERIA CENOCEPACIA; CELL VACUOLE; CONTROLLED STUDY; CYSTIC FIBROSIS; GENE INSERTION; INTRACELLULAR TRANSPORT; LYSOSOME; MACROPHAGE; MORBIDITY; MORTALITY; MOUSE; MUTANT; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN SECRETION; REGULON; RESPIRATORY TRACT INFECTION; RPON GENE; SURVIVAL; WILD TYPE; ANIMAL; BURKHOLDERIA CEPACIA COMPLEX; CELL LINE; FLAGELLUM; GENE DELETION; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; LOCOMOTION; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ANIMALS; BIOFILMS; BURKHOLDERIA CEPACIA COMPLEX; CELL LINE; FLAGELLA; GENE DELETION; GENETIC COMPLEMENTATION TEST; HUMANS; LOCOMOTION; LYSOSOMES; MACROPHAGES; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; PHAGOSOMES; SIGMA FACTOR; VACUOLES; VIRULENCE FACTORS;

EID: 40749094473     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01167-07     Document Type: Article

References (52)

1. Al-Younes, H. M., T. Rudel, and T. F. Meyer. 1999. Characterization and intracellular trafficking pattern of vacuoles containing Chlamydia pneumoniae in human epithelial cells. Cell. Microbiol. 1:237-247.
2. Barnett, M. J., C. J. Toman, R. F. Fisher, and S. R. Long. 2004. A dual-genome symbiosis chip for coordinate study of signal exchange and development in a prokaryote-host interaction. Proc. Natl. Acad. Sci. USA 101: 16636-16641.
3. Berg, G., L. Eberl, and A. Hartmann. 2005. The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ. Microbiol. 7:1673-1685.
4. Bittner, M., S. Saldías, C. Estevez, M. Zaldivar, C. L. Marolda, M. A. Valvano, and I. Contreras. 2002. O-antigen expression in Salmonella enterica serovar Typhi is regulated by nitrogen availability through RpoN-mediated transcriptional control of the rfaH gene. Microbiology 148:3789-3799.
5. Blair, D. F., and H. C. Berg. 1990. The MotA protein of E. coli is a proton-conducting component of the flagellar motor. Cell 60:439-449.
6. Coenye, T., and P. Vandamme. 2003. Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ. Microbiol. 5:719-729.
7. Cohen, S. N., A. C. Chang, and L. Hsu. 1972. Nonchromosomal antibiotic resistance in bacteria: genetic transformation of Escherichia coli by R-factor DNA. Proc. Natl. Acad. Sci. USA 69:2110-2114.
8. Craig, F. F., J. G. Coote, R. Parton, J. H. Freer, and N. J. Gilmour. 1989. A plasmid which can be transferred between Escherichia coli and Pasteurella haemolytica by electroporation and conjugation. J. Gen. Microbiol. 135:2885-2890.
9. Delory, M., R. Hallez, J. J. Letesson, and X. De Bolle. 2006. An RpoH-like heat shock sigma factor is involved in stress response and virulence in Brucella melitensis 16M. J. Bacteriol. 188:7707-7710.
10. Eissenberg, L. G., and W. E. Goldman. 1988. Fusion of lysosomes with phagosomes containing Histoplasma capsulatum: use of fluoresceinated dextran. Adv. Exp. Med. Biol. 239:53-61.
11. Fang, F. C. 2005. Sigma cascades in prokaryotic regulatory networks. Proc. Natl. Acad. Sci. USA 102:4933-4934.
12. Figurski, D. H., and D. R. Helinski. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. USA 76:1648-1652.
13. Flannagan, R. S., D. Aubert, C. Kooi, P. A. Sokol, and M. A. Valvano. 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.
14. Goldberg, J. B., and T. Dahnke. 1992. Pseudomonas aeruginosa AlgB, which modulates the expression of alginate, is a member of the NtrC subclass of prokaryotic regulators. Mol. Microbiol. 6:59-66.
15. Govan, J. R., J. E. Hughes, and P. Vandamme. 1996. Burkholderia cepacia: medical, taxonomic and ecological issues. J. Med. Microbiol. 45:395-407.
16. Haggie, P. M., and A. S. Verkman. 2007. Cystic fibrosis transmembrane conductance regulator-independent phagosomal acidification in macrophages. J. Biol. Chem. 282:31422-31428.
17. Hmama, Z., K. Sendide, A. Talal, R. Garcia, K. Dobos, and N. E. Reiner. 2004. Quantitative analysis of phagolysosome fusion in intact cells: inhibition by mycobacterial lipoarabinomannan and rescue by an 1α,25-dihydroxyvitamin D3-phosphoinositide 3-kinase pathway. J. Cell Sci. 117:2131-2140.
18. E, is critically important for the virulence of Salmonella typhimurium. Infect. Immun. 67:1560-1568.
19. Hunt, T. A., C. Kooi, P. A. Sokol, and M. A. Valvano. 2004. Identification of Burkholderia cenocepacia genes required for bacterial survival in vivo. Infect. Immun. 72:4010-4022.
20. Inglis, T. J., and J. L. Sagripanti. 2006. Environmental factors that affect the survival and persistence of Burkholderia pseudomallei. Appl. Environ. Microbiol. 72:6865-6875.
21. 54 and the transcriptional regulator FleQ of Legionella pneumophila, which are both involved in the regulation cascade of flagellar gene expression. J. Bacteriol. 186:2540-2547.
22. Jagannathan, A., C. Constantinidou, and C. W. Penn. 2001. Roles of rpoN, fliA, and flgR in expression of flagella in Campylobacter jejuni. J. Bacteriol. 183:2937-2942.
23. Kazmierczak, M. J., M. Wiedmann, and K. J. Boor. 2005. Alternative sigma factors and their roles in bacterial virulence. Microbiol. Mol. Biol. Rev. 69:527-543.
24. Keith, K. E., L. Killip, P. He, G. R. Moran, and M. A. Valvano. 2007. Burkholderia cenocepacia C5424 produces a pigment with antioxidant properties using a homogentisate intermediate. J. Bacteriol. 189:9057-9065.
25. Keith, K. E., and M. A. Valvano. 2007. Characterization of SodC, a periplasmic superoxide dismutase from Burkholderia cenocepacia. Infect. Immun. 75:2451-2460.
26. Kessler, B., S. Marqués, T. Köhler, J. L. Ramos, K. N. Timmis, and V. de Lorenzo. 1994. Cross talk between catabolic pathways in Pseudomonas putida: XylS-dependent and -independent activation of the TOL meta operon requires the same cis-acting sequences within the Pm promoter. J. Bacteriol. 176:5578-5582.
27. Kim, J., Y. Kang, O. Choi, Y. Jeong, J. E. Jeong, J. Y. Lim, M. Kim, J. S. Moon, H. Suga, and I. Hwang. 2007. Regulation of polar flagellum genes is mediated by quorum sensing and FlhDC in Burkholderia glumae. Mol. Microbiol. 64:165-179.
28. Klose, K. E., and J. J. Mekalanos. 1998. Distinct roles of an alternative sigma factor during both free-swimming and colonizing phases of the Vibrio cholerae pathogenic cycle. Mol. Microbiol. 28:501-520.
29. Lamothe, J., K. K. Huynh, S. Grinstein, and M. A. Valvano. 2007. Intracellular survival of Burkholderia cenocepacia in macrophages is associated with a delay in the maturation of bacterium-containing vacuoles. Cell. Microbiol. 9:40-53.
30. Lamothe, J., S. Thyssen, and M. A. Valvano. 2004. Burkholderia cepacia complex isolates survive intracellularly without replication within acidic vacuoles of Acanthamoeba polyphaga. Cell. Microbiol. 6:1127-1138.
31. Lemon, K. P., D. E. Higgins, and R. Kolter. 2007. Flagellar motility is critical for Listeria monocytogenes biofilm formation. J. Bacteriol. 189:4418-4424.
32. Mahenthiralingam, E., T. Coenye, J. W. Chung, D. P. Speert, J. R. Govan, P. Taylor, and P. Vandamme. 2000. Diagnostically and experimentally useful panel of strains from the Burkholderia cepacia complex. J. Clin. Microbiol. 38:910-913.
33. Mahenthiralingam, E., and D. P. Speert. 1995. Nonopsonic phagocytosis of Pseudomonas aeruginosa by macrophages and polymorphonuclear leukocytes requires the presence of the bacterial flagellum. Infect. Immun. 63:4519-4523.
34. Mahenthiralingam, E., T. A. Urban, and J. B. Goldberg. 2005. The multifarious, multireplicon Burkholderia cepacia complex. Nat. Rev. Microbiol. 3:144-156.
35. Maloney, K. E., and M. A. Valvano. 2006. The mgtC gene of Burkholderia cenocepacia is required for growth under magnesium limitation conditions and intracellular survival in macrophages. Infect. Immun. 74:5477-5486.
36. Marolda, C. L., B. Hauröder, M. A. John, R. Michel, and M. A. Valvano. 1999. Intracellular survival and saprophytic growth of isolates from the Burkholderia cepacia complex in free-living amoebae. Microbiology 145:1509-1517.
37. Merrick, M. J. 1993. In a class of its own - the RNA polymerase sigma factor sigma 54 (sigma N). Mol. Microbiol. 10:903-909.
38. O'Toole, G., H. B. Kaplan, and R. Kolter. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:49-79.
39. Pratt, L. A., and R. Kolter. 1998. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, Chemotaxis and type I pili. Mol. Microbiol. 30:285-293.
40. Reitzer, L. 2003. Nitrogen assimilation and global regulation in Escherichia coli. Annu. Rev. Microbiol. 57:155-176.
41. 54-dependent genes in Escherichia coli. Microbiol. Mol. Biol. Rev. 65:422-444.
42. Saini, L., S. Galsworthy, M. John, and M. A. Valvano. 1999. Intracellular survival of Burkholderia cepacia complex isolates in the presence of macrophage cell activation. Microbiology 145:3465-3475.
43. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
44. Soutourina, O. A., and P. N. Bertin. 2003. Regulation cascade of flagellar expression in gram-negative bacteria. FEMS Microbiol. Rev. 27:505-523.
45. Studholme, D. J. 2002. Enhancer-dependent transcription in Salmonella enterica Typhimurium: new members of the sigmaN regulon inferred from protein sequence homology and predicted promoter sites. J. Mol. Microbiol. Biotechnol. 4:367-374.
46. Tomich, M., C. A. Herfst, J. W. Golden, and C. D. Mohr. 2002. Role of flagella in host cell invasion by Burkholderia cepacia. Infect. Immun. 70:1799-1806.
47. Totten, P. A., J. C. Lara, and S. Lory. 1990. The rpoN gene product of Pseudomonas aeruginosa is required for expression of diverse genes, including the flagellin gene. J. Bacteriol. 172:389-396.
48. Valvano, M. A. 2006. Infections by Burkholderia spp.: the psychodramatic life of an opportunistic pathogen. Future Microbiol. 1:145-149.
49. Valvano, M. A., K. E. Keith, and S. T. Cardona. 2005. Survival and persistence of opportunistic Burkholderia species in host cells. Curr. Opin. Microbiol. 8:99-105.
50. Reference deleted.
51. Via, L. E., R. A. Fratti, M. McFalone, E. Pagán-Ramos, D. Deretic, and V. Deretic. 1998. Effects of cytokines on mycobacterial phagosome maturation. J. Cell. Sci. 111:897-905.
52. Yip, E. S., B. T. Grublesky, E. A. Hussa, and K. L. Visick. 2005. A novel, conserved cluster of genes promotes symbiotic colonization and sigma-dependent biofilm formation by Vibrio fischeri. Mol. Microbiol. 57:1485-1498.