Quantification of type VI secretion system activity in macrophages infected with Burkholderia cenocepacia

Microbiology (United Kingdom)

Volumn 161, Issue 11, 2015, Pages 2161-2173

  Aubert, Daniel F ^a   Hu, Sherry ^a   Valvano, Miguel A ^a,b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

RHO GUANINE NUCLEOTIDE BINDING PROTEIN; ACTIN; TYPE VI SECRETION SYSTEM;

ACTIN FILAMENT; ARTICLE; BACTERIAL INFECTION; BURKHOLDERIA CENOCEPACIA; CONTROLLED STUDY; GENE CLUSTER; GENE DELETION; MACROPHAGE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; TYPE VI SECRETION SYSTEM; ANIMAL; C57BL MOUSE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY;

ACTINS; ANIMALS; BURKHOLDERIA CENOCEPACIA; HOST-PATHOGEN INTERACTIONS; MACROPHAGES; MICE, INBRED C57BL; TYPE VI SECRETION SYSTEMS;

EID: 84947275349     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.000174     Document Type: Article

References (63)

1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. (1990). Basic local alignment search tool. J Mol Biol 215, 403-410.
2. Aschtgen, M. S., Bernard, C. S., De Bentzmann, S., Lloubès, R. & Cascales, E. (2008). SciN is an outer membrane lipoprotein required for type VI secretion in enteroaggregative Escherichia coli. J Bacteriol 190, 7523-7531.
3. Aschtgen, M. S., Thomas, M. S. & Cascales, E. (2010). Anchoring the type VI secretion system to the peptidoglycan: TssL, TagL, TagP… what else? Virulence 1, 535-540.
4. Aubert, D. F., Flannagan, R. S. & Valvano, M. A. (2008). A novel sensor kinase-response regulator hybrid controls biofilm formation and type VI secretion system activity in Burkholderia cenocepacia. Infect Immun 76, 1979-1991.
5. Aubert, D., MacDonald, D. K. & Valvano, M. A. (2010). BcsKC is an essential protein for the type VI secretion system activity in Burkholderia cenocepacia that forms an outer membrane complex with BcsLB. J Biol Chem 285, 35988-35998.
6. Aubert, D. F., O'Grady, E. P., Hamad, M. A., Sokol, P. A. & Valvano, M. A. (2013). The Burkholderia cenocepacia sensor kinase hybrid AtsR is a global regulator modulating quorum-sensing signalling. Environ Microbiol 15, 372-385.
7. Basler, M., Pilhofer, M., Henderson, G. P., Jensen, G. J. & Mekalanos, J. J. (2012). Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483, 182-186.
8. Bönemann, G., Pietrosiuk, A., Diemand, A., Zentgraf, H. & Mogk, A. (2009). Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO J 28, 315-325.
9. Bönemann, G., Pietrosiuk, A. & Mogk, A. (2010). Tubules and donuts: a type VI secretion story. Mol Microbiol 76, 815-821.
10. Boyer, F., Fichant, G., Berthod, J., Vandenbrouck, Y. & Attree, I. (2009). Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources? BMC Genomics 10, 104.
11. Brooks, T. M., Unterweger, D., Bachmann, V., Kostiuk, B. & Pukatzki, S. (2013). Lytic activity of the Vibrio cholerae type VI secretion toxin VgrG-3 is inhibited by the antitoxin TsaB. J Biol Chem 288, 7618-7625.
12. Burns, J. L., Jonas, M., Chi, E. Y., Clark, D. K., Berger, A. & Griffith, A. (1996). Invasion of respiratory epithelial cells by Burkholderia (Pseudomonas) cepacia. Infect Immun 64, 4054-4059.
13. Clemens, D. L., Ge, P., Lee, B. Y., Horwitz, M. A. & Zhou, Z. H. (2015). Atomic structure of T6SS reveals interlaced array essential to function. Cell 160, 940-951.
14. Cohen, S. N., Chang, A. C. & Hsu, L. (1972). Nonchromosomal antibiotic resistance in bacteria: genetic transformation of Escherichia coli by R-factor DNA. Proc Natl Acad Sci U S A 69, 2110-2114.
15. Costa, T. R., Felisberto-Rodrigues, C., Meir, A., Prevost, M. S., Redzej, A., Trokter, M. & Waksman, G. (2015). Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nat Rev Microbiol 13, 343-359.
16. Cox, G. W., Mathieson, B. J., Gandino, L., Blasi, E., Radzioch, D. & Varesio, L. (1989). Heterogeneity of hematopoietic cells immortalized by v-myc/v-raf recombinant retrovirus infection of bone marrow or fetal liver. J Natl Cancer Inst 81, 1492-1496.
17. Craig, F. F., Coote, J. G., Parton, R., Freer, J. H. & Gilmour, N. J. (1989). A plasmid which can be transferred between Escherichia coli and Pasteurella haemolytica by electroporation and conjugation. J Gen Microbiol 135, 2885-2890.
18. Drevinek, P. & Mahenthiralingam, E. (2010). Burkholderia cenocepacia in cystic fibrosis: epidemiology and molecular mechanisms of virulence. Clin Microbiol Infect 16, 821-830.
19. Durand, E., Zoued, A., Spinelli, S., Watson, P. J., Aschtgen, M. S., Journet, L., Cambillau, C. & Cascales, E. (2012). Structural characterization and oligomerization of the TssL protein, a component shared by bacterial type VI and type IVb secretion systems. J Biol Chem 287, 14157-14168.
20. Durand, E., Cambillau, C., Cascales, E. & Journet, L. (2014). VgrG, Tae, Tle, and beyond: the versatile arsenal of type VI secretion effectors. Trends Microbiol 22, 498-507.
21. English, G., Byron, O., Cianfanelli, F. R., Prescott, A. R. & Coulthurst, S. J. (2014). Biochemical analysis of TssK, a core component of the bacterial type VI secretion system, reveals distinct oligomeric states of TssK and identifies a TssK-TssFG subcomplex. Biochem J 461, 291-304.
22. Felisberto-Rodrigues, C., Durand, E., Aschtgen, M. S., Blangy, S., Ortiz-Lombardia, M., Douzi, B., Cambillau, C. & Cascales, E. (2011). Towards a structural comprehension of bacterial type VI secretion systems: characterization of the TssJ-TssM complex of an Escherichia coli pathovar. PLoS Pathog 7, e1002386.
23. 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.
24. 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.
25. Flannagan, R. S., Jaumouillé, V., Huynh, K. K., Plumb, J. D., Downey, G. P., Valvano, M. A. & Grinstein, S. (2012). Burkholderia cenocepacia disrupts host cell actin cytoskeleton by inactivating Rac and Cdc42. Cell Microbiol 14, 239-254.
26. Hamad, M. A., Skeldon, A. M. & Valvano, M. A. (2010). Construction of aminoglycoside-sensitive Burkholderia cenocepacia strains for use in studies of intracellular bacteria with the gentamicin protection assay. Appl Environ Microbiol 76, 3170-3176.
27. Hunt, T. A., Kooi, C., Sokol, P. A. & Valvano, M. A. (2004). Identification of Burkholderia cenocepacia genes required for bacterial survival in vivo. Infect Immun 72, 4010-4022.
28. Isles, A., Maclusky, I., Corey, M., Gold, R., Prober, C., Fleming, P. & Levison, H. (1984). Pseudomonas cepacia infection in cystic fibrosis: an emerging problem. J Pediatr 104, 206-210.
29. Jiang, F., Waterfield, N. R., Yang, J., Yang, G. & Jin, Q. (2014). A Pseudomonas aeruginosa type VI secretion phospholipase D effector targets both prokaryotic and eukaryotic cells. Cell Host Microbe 15, 600-610.
30. Kanehisa, M. & Goto, S. (2000). KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28, 27-30.
31. Keith, K. E., Hynes, D. W., Sholdice, J. E. & Valvano, M. A. (2009). Delayed association of the NADPH oxidase complex with macrophage vacuoles containing the opportunistic pathogen Burkholderia cenocepacia. Microbiology 155, 1004-1015.
32. Khodai-Kalaki, M., Aubert, D. F. & Valvano, M. A. (2013). Characterization of the AtsR hybrid sensor kinase phosphorelay pathway and identification of its response regulator in Burkholderia cenocepacia. J Biol Chem 288, 30473-30484.
33. Khodai-Kalaki, M., Andrade, A., Fathy Mohamed, Y. & Valvano, M. A. (2015). Burkholderia cenocepacia lipopolysaccharide modification and flagellin glycosylation affect virulence but not innate immune recognition in plants. MBio 6, e00679-e00615.
34. Kudryashev, M., Wang, R. Y., Brackmann, M., Scherer, S., Maier, T., Baker, D., DiMaio, F., Stahlberg, H., Egelman, E. H. & Basler, M. (2015). Structure of the type VI secretion system contractile sheath. Cell 160, 952-962.
35. Lamothe, J., Thyssen, S. & Valvano, M. A. (2004). Burkholderia cepacia complex isolates survive intracellularly without replication within acidic vacuoles of Acanthamoeba polyphaga. Cell Microbiol 6, 1127-1138.
36. Lamothe, J., Huynh, K. K., Grinstein, S. & Valvano, M. A. (2007). Intracellular survival of Burkholderia cenocepacia in macrophages is associated with a delay in the maturation of bacteria-containing vacuoles. Cell Microbiol 9, 40-53.
37. 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.
38. Mahenthiralingam, E., Baldwin, A. & Dowson, C. G. (2008). Burkholderia cepacia complex bacteria: opportunistic pathogens with important natural biology. J Appl Microbiol 104, 1539-1551.
39. Marolda, C. L., Hauröder, B., John, M. A., Michel, R. & Valvano, M. A. (1999). Intracellular survival and saprophytic growth of isolates from the Burkholderia cepacia complex in free-living amoebae. Microbiology 145, 1509-1517.
40. Martin, D. W. & Mohr, C. D. (2000). Invasion and intracellular survival of Burkholderia cepacia. Infect Immun 68, 24-29.
41. Pukatzki, S., Ma, A. T., Revel, A. T., Sturtevant, D. & Mekalanos, J. J. (2007). Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc Natl Acad Sci U S A 104, 15508-15513.
42. Rosales-Reyes, R., Skeldon, A. M., Aubert, D. F. & Valvano, M. A. (2012). The type VI secretion system of Burkholderia cenocepacia affects multiple Rho family GTPases disrupting the actin cytoskeleton and the assembly of NADPH oxidase complex in macrophages. Cell Microbiol 14, 255-273.
43. Russell, A. B., Hood, R. D., Bui, N. K., LeRoux, M., Vollmer, W. & Mougous, J. D. (2011). Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475, 343-347.
44. Russell, A. B., Peterson, S. B. & Mougous, J. D. (2014). Type VI secretion system effectors: poisons with a purpose. Nat Rev Microbiol 12, 137-148.
45. Saini, L. S., Galsworthy, S. B., John, M. A. & Valvano, M. A. (1999). Intracellular survival of Burkholderia cepacia complex isolates in the presence of macrophage cell activation. Microbiology 145, 3465-3475.
46. Sajjan, U. S., Yang, J. H., Hershenson, M. B. & LiPuma, J. J. (2006). Intracellular trafficking and replication of Burkholderia cenocepacia in human cystic fibrosis airway epithelial cells. Cell Microbiol 8, 1456-1466.
47. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. New York: Cold Spring Harbor Laboratory.
48. Schmerk, C. L. & Valvano, M. A. (2013). Burkholderia multivorans survival and trafficking within macrophages. J Med Microbiol 62, 173-184.
49. Schwarz, S., Singh, P., Robertson, J. D., LeRoux, M., Skerrett, S. J., Goodlett, D. R., West, T. E. & Mougous, J. D. (2014). VgrG-5 is a Burkholderia type VI secretion system-exported protein required for multinucleated giant cell formation and virulence. Infect Immun 82, 1445-1452.
50. Shalom, G., Shaw, J. G. & Thomas, M. S. (2007). In vivo expression technology identifies a type VI secretion system locus in Burkholderia pseudomallei that is induced upon invasion of macrophages. Microbiology 153, 2689-2699.
51. Shneider, M. M., Buth, S. A., Ho, B. T., Basler, M., Mekalanos, J. J. & Leiman, P. G. (2013). PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 500, 350-353.
52. Smith, T. F. & Waterman, M. S. (1981). Identification of common molecular subsequences. J Mol Biol 147, 195-197.
53. Suarez, G., Sierra, J. C., Erova, T. E., Sha, J., Horneman, A. J. & Chopra, A. K. (2010). A type VI secretion system effector protein, VgrG1, from Aeromonas hydrophila that induces host cell toxicity by ADP ribosylation of actin. J Bacteriol 192, 155-168.
54. Thomson, E. L. S. & Dennis, J. J. (2013). Common duckweed (Lemna minor) is a versatile high-throughput infection model for the Burkholderia cepacia complex and other pathogenic bacteria. PLoS One 8, e80102.
55. Toesca, I. J., French, C. T. & Miller, J. F. (2014). The type VI secretion system spike protein VgrG5 mediates membrane fusion during intercellular spread by pseudomallei group Burkholderia species. Infect Immun 82, 1436-1444.
56. Uehlinger, S., Schwager, S., Bernier, S. P., Riedel, K., Nguyen, D. T., Sokol, P. A. & Eberl, L. (2009). Identification of specific and universal virulence factors in Burkholderia cenocepacia strains by using multiple infection hosts. Infect Immun 77, 4102-4110.
57. Varga, J. J., Losada, L., Zelazny, A. M., Kim, M., McCorrison, J., Brinkac, L., Sampaio, E. P., Greenberg, D. E., Singh, I. & other authors (2013). Draft genome sequences of Burkholderia cenocepacia ET12 lineage strains K56-2 and BC7. Genome Announc 1, e00841-e00813.
58. Vergunst, A. C., Meijer, A. H., Renshaw, S. A. & O'Callaghan, D. (2010). Burkholderia cenocepacia creates an intramacrophage replication niche in zebrafish embryos, followed by bacterial dissemination and establishment of systemic infection. Infect Immun 78, 1495-1508.
59. Waters, V. (2012). New treatments for emerging cystic fibrosis pathogens other than Pseudomonas. Curr Pharm Des 18, 696-725.
60. Zheng, J. & Leung, K. Y. (2007). Dissection of a type VI secretion system in Edwardsiella tarda. Mol Microbiol 66, 1192-1206.
61. Zheng, J., Ho, B. & Mekalanos, J. J. (2011). Genetic analysis of antiamoebae and anti-bacterial activities of the type VI secretion system in Vibrio cholerae. PLoS One 6, e23876.
62. Zoued, A., Durand, E., Bebeacua, C., Brunet, Y. R., Douzi, B., Cambillau, C., Cascales, E. & Journet, L. (2013). TssK is a trimeric cytoplasmic protein interacting with components of both phage-like and membrane anchoring complexes of the type VI secretion system. J Biol Chem 288, 27031-27041.
63. Zoued, A., Brunet, Y. R., Durand, E., Aschtgen, M. S., Logger, L., Douzi, B., Journet, L., Cambillau, C. & Cascales, E. (2014). Architecture and assembly of the type VI secretion system. Biochim Biophys Acta 1843, 1664-1673.