Burkholderia type vi secretion systems have distinct roles in eukaryotic and bacterial cell interactions

PLoS Pathogens

Volumn 6, Issue 8, 2010, Pages 77-78

  Schwarz, Sandra ^a   West, T Eoin ^a   Boyer, Frédéric ^b   Chiang, Wen Chi ^c   Carl, Mike A ^a   Hood, Rachel D ^a   Rohmer, Laurence ^a   Tolker Nielsen, Tim ^c   Skerrett, Shawn J ^a   Mougous, Joseph D ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b University Lyon i   (France)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

MYELOID DIFFERENTIATION FACTOR 88; BACTERIAL PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL VIRULENCE; BIOFILM; BURKHOLDERIA; BURKHOLDERIA THAILANDENSIS; CELL CONTACT; CELL INTERACTION; CONTROLLED STUDY; EUKARYOTIC CELL; HOST PATHOGEN INTERACTION; MELIOIDOSIS; MOUSE; NONHUMAN; PHYLOGENY; PSEUDOMONAS FLUORESCENS; PSEUDOMONAS PUTIDA; SERRATIA; SERRATIA PROTEAMACULANS; TYPE IV SECRETION SYSTEM; WILD TYPE; ANIMAL; BACTERIAL SECRETION SYSTEM; BACTERIUM; BURKHOLDERIA INFECTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; IMMUNOLOGY; METABOLISM; PATHOGENICITY; VIRULENCE;

BACTERIA (MICROORGANISMS); BURKHOLDERIA; BURKHOLDERIA THAILANDENSIS; EUKARYOTA; MURINAE; MUS; PSEUDOMONAS FLUORESCENS; PSEUDOMONAS PUTIDA; SERRATIA PROTEAMACULANS;

ANIMALS; BACTERIA; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; BIOFILMS; BURKHOLDERIA; BURKHOLDERIA INFECTIONS; HOST-PARASITE INTERACTIONS; MICE; PHYLOGENY; VIRULENCE;

EID: 77958145264     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001068     Document Type: Article

References (63)

1. Riley MA, Wertz JE (2002) Bacteriocins: evolution, ecology, and application. Annu Rev Microbiol 56: 117-137.
2. Cornelis GR (2006) The type III secretion injectisome. Nat Rev Microbiol 4: 811-825.
3. Bingle LE, Bailey CM, Pallen MJ (2008) Type VI secretion: a beginner's guide. Curr Opin Microbiol 11: 3-8.
4. 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.
5. Cascales E (2008) The type VI secretion toolkit. EMBO Rep 9: 735-741.
6. Filloux A, Hachani A, Bleves S (2008) The bacterial type VI secretion machine: yet another player for protein transport across membranes. Microbiology 154: 1570-1583.
7. Pukatzki S, McAuley SB, Miyata ST (2009) The type VI secretion system: translocation of effectors and effector-domains. Curr Opin Microbiol 12: 11-17.
8. Ma AT, McAuley S, Pukatzki S, Mekalanos JJ (2009) Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe 5: 234-243.
9. Suarez G, Sierra JC, Erova TE, Sha J, Horneman AJ, et al. (2009) A type VI secretion system effector protein VgrG1 from Aeromonas hydrophila that induces host cell toxicity by ADP-ribosylation of actin. J Bacteriol.
10. Hood RD, Singh P, Hsu F, Guvener T, Carl MA, et al. (2010) A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7: 25-37.
11. Mougous JD, Gifford CA, Ramsdell TL, Mekalanos JJ (2007) Threonine phosphorylation post-translationally regulates protein secretion in Pseudomonas aeruginosa. Nat Cell Biol 9: 797-803.
12. Aschtgen MS, Gavioli M, Dessen A, Lloubes R, Cascales E (2010) The SciZ protein anchors the enteroaggregative Escherichia coli Type VI secretion system to the cell wall. Mol Microbiol.
13. Zheng J, Leung KY (2007) Dissection of a type VI secretion system in Edwardsiella tarda. Mol Microbiol 66: 1192-1206.
14. Mougous JD, Cuff ME, Raunser S, Shen A, Zhou M, et al. (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312: 1526-1530.
15. Bonemann 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.
16. Hsu F, Schwarz S, Mougous JD (2009) TagR promotes PpkA-catalysed type VI secretion activation in Pseudomonas aeruginosa. Mol Microbiol 72: 1111-1125.
17. Pukatzki S, Ma AT, Revel AT, Sturtevant D, Mekalanos JJ (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.
18. Kanamaru S (2009) Structural similarity of tailed phages and pathogenic bacterial secretion systems. Proc Natl Acad Sci U S A 106: 4067-4068.
19. Leiman PG, Basler M, Ramagopal UA, Bonanno JB, Sauder JM, et al. (2009) Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc Natl Acad Sci U S A 106: 4154-4159.
20. Pell LG, Kanelis V, Donaldson LW, Howell PL, Davidson AR (2009) The phage lambda major tail protein structure reveals a common evolution for long-tailed phages and the type VI bacterial secretion system. Proc Natl Acad Sci U S A 106: 4160-4165.
21. Wiersinga WJ, van der Poll T, White NJ, Day NP, Peacock SJ (2006) Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei. Nat Rev Microbiol 4: 272-282.
22. Brett PJ, DeShazer D, Woods DE (1998) Burkholderia thailandensis sp. nov., a Burkholderia pseudomallei-like species. Int J Syst Bacteriol 48 Pt 1: 317-320.
23. Kim HS, Schell MA, Yu Y, Ulrich RL, Sarria SH, et al. (2005) Bacterial genome adaptation to niches: divergence of the potential virulence genes in three Burkholderia species of different survival strategies. BMC Genomics 6: 174.
24. Yu Y, Kim HS, Chua HH, Lin CH, Sim SH, et al. (2006) Genomic patterns of pathogen evolution revealed by comparison of Burkholderia pseudomallei, the causative agent of melioidosis, to avirulent Burkholderia thailandensis. BMC Microbiol 6: 46.
25. Nierman WC, DeShazer D, Kim HS, Tettelin H, Nelson KE, et al. (2004) Structural flexibility in the Burkholderia mallei genome. Proc Natl Acad SciUS A 101: 14246-14251.
26. Haraga A, West TE, Brittnacher MJ, Skerrett SJ, Miller SI (2008) Burkholderia thailandensis as a model system for the study of the virulence-associated type III secretion system of Burkholderia pseudomallei. Infect Immun 76: 5402-5411.
27. Schell MA, Ulrich RL, Ribot WJ, Brueggemann EE, Hines HB, et al. (2007) Type VI secretion is a major virulence determinant in Burkholderia mallei. Mol Microbiol 64: 1466-1485.
28. Shalom G, Shaw JG, Thomas MS (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.
29. Pilatz S, Breitbach K, Hein N, Fehlhaber B, Schulze J, et al. (2006) Identification of Burkholderia pseudomallei genes required for the intracellular life cycle and in vivo virulence. Infect Immun 74: 3576-3586.
30. West TE, Frevert CW, Liggitt HD, Skerrett SJ (2008) Inhalation of Burkholderia thailandensis results in lethal necrotizing pneumonia in mice: a surrogate model for pneumonic melioidosis. Trans R Soc Trop Med Hyg 102 Suppl 1: S119-126.
31. Sun GW, Chen Y, Liu Y, Tan GY, Ong C, et al. (2010) Identification of a regulatory cascade controlling Type III Secretion System 3 gene expression in Burkholderia pseudomallei. Mol Microbiol.
32. Janssens S, Beyaert R (2002) A universal role for MyD88 in TLR/IL-1Rmediated signaling. Trends Biochem Sci 27: 474-482.
33. West TE, Hawn TR, Skerrett SJ (2009) Toll-like receptor signaling in airborne Burkholderia thailandensis infection. Infect Immun.
34. Choi KH, Schweizer HP (2006) mini-Tn7 insertion in bacteria with single attTn7 sites: example Pseudomonas aeruginosa. Nat Protoc 1: 153-161.
35. Aschtgen MS, Bernard CS, De Bentzmann S, Lloubes R, Cascales E (2008) SciN is an outer membrane lipoprotein required for Type VI secretion in enteroaggregative Escherichia coli. J Bacteriol.
36. Enos-Berlage JL, Guvener ZT, Keenan CE, McCarter LL (2005) Genetic determinants of biofilm development of opaque and translucent Vibrio parahaemolyticus. Mol Microbiol 55: 1160-1182.
37. Aubert DF, Flannagan RS, Valvano MA (2008) A Novel Sensor Kinase- Response Regulator Hybrid Controls Biofilm Formation and Type VI Secretion System Activity in Burkholderia cenocepacia. Infect Immun.
38. Deretic V, Schurr MJ, Yu H (1995) Pseudomonas aeruginosa, mucoidy and the chronic infection phenotype in cystic fibrosis. Trends Microbiol 3: 351-356.
39. Sauer K, Camper AK, Ehrlich GD, Costerton JW, Davies DG (2002) Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol 184: 1140-1154.
40. Southey-Pillig CJ, Davies DG, Sauer K (2005) Characterization of temporal protein production in Pseudomonas aeruginosa biofilms. J Bacteriol 187: 8114-8126.
41. He SY, Nomura K, Whittam TS (2004) Type III protein secretion mechanism in mammalian and plant pathogens. Biochim Biophys Acta 1694: 181-206.
42. Christie PJ, Vogel JP (2000) Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol 8: 354-360.
43. Burtnick MN, DeShazer D, Nair V, Gherardini FC, Brett PJ (2010) Burkholderia mallei cluster 1 type VI secretion mutants exhibit growth and actin polymerization defects in RAW 264.7 murine macrophages. Infect Immun 78: 88-99.
44. Chobchuenchom W, Bhumiratana A (2003) Isolation and characterization of pathogens attacking Pomacea canaliculata. World Journal of Microbiology and Biotechnology 19: 903-906.
45. Chobchuenchom W, Mongkolsuk S, Bhumiratana A (1996) Biodegradation of 3- chlorobenzoate by Pseudomonas putida 10.2. World Journal of Microbiology and Biotechnology 12: 607-614.
46. Gjermansen M, Nilsson M, Yang L, Tolker-Nielsen T (2009) Characterization of starvation-induced dispersion in Pseudomonas putida biofilms: genetic elements and molecular mechanisms. Mol Microbiol.
47. Tolker-Nielsen T, Brinch UC, Ragas PC, Andersen JB, Jacobsen CS, et al. (2000) Development and dynamics of Pseudomonas sp. biofilms. J Bacteriol 182: 6482-6489.
48. Hinsa SM, O'Toole GA (2006) Biofilm formation by Pseudomonas fluorescens WCS365: a role for LapD. Microbiology 152: 1375-1383.
49. Compant S, Duffy B, Nowak J, Clement C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71: 4951-4959.
50. Gibbs KA, Urbanowski ML, Greenberg EP (2008) Genetic determinants of self identity and social recognition in bacteria. Science 321: 256-259.
51. Blango MG, Mulvey MA (2009) Bacterial landlines: contact-dependent signaling in bacterial populations. Curr Opin Microbiol 12: 177-181.
52. Chandler JR, Duerkop BA, Hinz A, West TE, Herman JP, et al. (2009) Mutational analysis of Burkholderia thailandensis quorum sensing and selfaggregation. J Bacteriol 191: 5901-5909.
53. Horton RM, Ho SN, Pullen JK, Hunt HD, Cai Z, et al. (1993) Gene splicing by overlap extension. Methods Enzymol 217: 270-279.
54. Choi KH, Mima T, Casart Y, Rholl D, Kumar A, et al. (2008) Genetic tools for select-agent-compliant manipulation of Burkholderia pseudomallei. Appl Environ Microbiol 74: 1064-1075.
55. Choi KH, Gaynor JB, White KG, Lopez C, Bosio CM, et al. (2005) A Tn7- based broad-range bacterial cloning and expression system. Nat Methods 2: 443-448.
56. Lambertsen L, Sternberg C, Molin S (2004) Mini-Tn7 transposons for sitespecific tagging of bacteria with fluorescent proteins. Environ Microbiol 6: 726-732.
57. Adachi O, Kawai T, Takeda K, Matsumoto M, Tsutsui H, et al. (1998) Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9: 143-150.
58. Sternberg C, Tolker-Nielsen T (2006) Growing and analyzing biofilms in flow cells. Curr Protoc Microbiol Chapter 1: Unit 1B 2.
59. Sterk P, Kersey PJ, Apweiler R (2006) Genome Reviews: standardizing content and representation of information about complete genomes. Omics 10: 114-118.
60. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
61. Marchler-Bauer A, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, et al. (2009) CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res 37: D205-210.
62. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
63. Gascuel O (1997) BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol 14: 685-695.