Type VI secretion requires a dynamic contractile phage tail-like structure

Nature

Volumn 483, Issue 7388, 2012, Pages 182-186

  Basler, M ^a   Pilhofer, M ^b   Henderson, G P ^b   Jensen, G J ^b   Mekalanos, J J ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN;

BACTERIOPHAGE; MICROSCOPY; PROTEIN; SECRETION; TRANSLOCATION;

ARTICLE; BACTERIAL MEMBRANE; BACTERIOPHAGE; CELL FRACTIONATION; CELL STRUCTURE; ELECTRON TOMOGRAPHY; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; IMMUNOBLOTTING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN STRUCTURE; TARGET CELL; TIME LAPSE IMAGING; TYPE VI SECRETION SYSTEM; VIBRIO CHOLERAE; WHOLE CELL ELECTRON CRYOTOMOGRAPHY;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; BACTERIOPHAGES; CELL MEMBRANE; CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPE TOMOGRAPHY; MICROSCOPY, FLUORESCENCE; VIBRIO CHOLERAE;

BACTERIA (MICROORGANISMS); VIBRIO CHOLERAE;

EID: 84858002430     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature10846     Document Type: Article

References (36)

1. Pukatzki, S. et al. Identification of a conserved bacterial protein secretion systemin Vibrio cholerae using the Dictyosteliumhostmodel system. Proc.Natl Acad. Sci. USA 103, 1528-1533 (2006). (Pubitemid 43191199)
2. Ma, A. T., McAuley, S., Pukatzki, S. & Mekalanos, J. J. Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe 5, 234-243 (2009).
3. Russell, A. B. et al. Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475, 343-347 (2011).
4. MacIntyre, D. L., Miyata, S. T., Kitaoka, M. & Pukatzki, S. The Vibrio cholerae type VI secretion system displays antimicrobial properties. Proc. Natl Acad. Sci. USA 107, 19520-19524 (2010).
5. Schwarz, S. et al. Burkholderia type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog. 6, e1001068 (2010).
6. Hood, R. D. et al. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7, 25-37 (2010).
7. Zheng, J., Ho, B. & Mekalanos, J. J. Genetic analysis of anti-amoebae and antibacterial activities of the type VI secretion system in Vibrio cholerae. PLoS ONE 6, e23876 (2011).
8. Ma, A. T.&Mekalanos, J. J. In vivo actin cross-linking induced by Vibrio cholerae type VI secretion systemis associated with intestinal inflammation. Proc. Natl Acad. Sci. USA 107, 4365-4370 (2010).
9. Pukatzki, S., Ma, A. T., Revel, A. T., Sturtevant, D.& Mekalanos, J. J. Type VI secretion systemtranslocates a phage tail spike-like protein into target cells where it crosslinks actin. Proc. Natl Acad. Sci. USA 104, 15508-15513 (2007). (Pubitemid 47502947)
10. Leiman, P. G. et al. Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc. Natl Acad. Sci. USA 106, 4154-4159 (2009).
11. Pell, L. G., Kanelis, V., Donaldson, L. W., Howell, P. L. & Davidson, A. R. 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. USA 106, 4160-4165 (2009).
12. Leiman, P. G., Chipman, P. R., Kostyuchenko, V. A., Mesyanzhinov, V. V. & Rossmann, M. G. Three-dimensional rearrangement of proteins in the tail of bacteriophage T4 on infection of its host. Cell 118, 419-429 (2004). (Pubitemid 39485662)
13. Lossi, N. S., Dajani, R., Freemont, P.& Filloux, A. Structure-function analysis of HsiF, a gp25-like component of the type VI secretionsystemin Pseudomonas aeruginosa. Microbiology 157, 3292-3305 (2011).
14. Bonemann, G., Pietrosiuk, A., Diemand, A., Zentgraf, H. & Mogk, A. Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO J. 28, 315-325 (2009).
15. Pietrosiuk, A. et al. Molecular basis for the unique role of the AAA1 chaperone ClpV in type VI protein secretion. J. Biol. Chem. 286, 30010-30021 (2011).
16. Mougous, J. D. et al. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312, 1526-1530 (2006). (Pubitemid 43865892)
17. Pedelacq, J. D., Cabantous, S., Tran, T., Terwilliger, T. C. & Waldo, G. S. Engineering and characterization of a superfolder green fluorescent protein. Nature Biotechnol. 24, 79-88 (2006). (Pubitemid 43083170)
18. Cho, H., McManus, H. R., Dove, S. L. & Bernhardt, T. G. Nucleoid occlusion factor SlmA is a DNA-activated FtsZ polymerization antagonist. Proc. Natl Acad. Sci. USA 108, 3773-3778 (2011).
19. Pilhofer, M., Ladinsky, M. S., McDowall, A. W. & Jensen, G. J. Bacterial TEM: new insights from cryo-microscopy. Methods Cell Biol. 96, 21-45 (2010).
20. Aschtgen, M. S., Bernard, C. S., De Bentzmann, S., Lloubes, R. & Cascales, E. SciN is an outermembrane lipoprotein required for type VI secretion in enteroaggregative Escherichia coli. J. Bacteriol. 190, 7523-7531 (2008).
21. Aschtgen, M. S., Thomas, M. S. & Cascales, E. Anchoring the type VI secretion system to the peptidoglycan: TssL, TagL, TagP.what else? Virulence 1, 535-540 (2010).
22. Aschtgen, M. S., Gavioli, M., Dessen, A., Lloubes, R. & Cascales, E. The SciZ protein anchors the enteroaggregative Escherichia coli type VI secretion system to the cell wall. Mol. Microbiol. 75, 886-899 (2010).
23. Kostyuchenko, V. A. et al. The tail structure of bacteriophage T4 and itsmechanism of contraction. Nature Struct. Mol. Biol. 12, 810-813 (2005). (Pubitemid 43086256)
24. Ballister, E. R., Lai, A. H., Zuckermann, R. N., Cheng, Y. & Mougous, J. D. In vitro selfassembly of tailorable nanotubes from a simple protein building block. Proc. Natl Acad. Sci. USA 105, 3733-3738 (2008). (Pubitemid 351723467)
25. Goldberg, S. & Murphy, J. R. Molecular epidemiological studies of United States Gulf Coast Vibrio cholerae strains: integration site of mutator vibriophage VcA-3. Infect. Immun. 42, 224-230 (1983). (Pubitemid 13012458)
26. Bina, J. E. & Mekalanos, J. J. Vibrio cholerae tolC is required for bile resistance and colonization. Infect. Immun. 69, 4681-4685 (2001). (Pubitemid 32574473)
27. Guzman, L. M., Belin, D., Carson, M. J. & Beckwith, J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177, 4121-4130 (1995).
28. Tivol, W. F., Briegel, A. & Jensen, G. J. An improved cryogen for plunge freezing. Microsc. Microanal. 14, 375-379 (2008).
29. Suloway, C. et al. Fully automated, sequential tilt-series acquisition with Leginon. J. Struct. Biol. 167, 11-18 (2009).
30. Zheng, S. Q. et al. UCSF tomography: an integrated software suite for real-time electron microscopic tomographic data collection, alignment, and reconstruction. J. Struct. Biol. 157, 138-147 (2007). (Pubitemid 44880788)
31. Mastronarde, D. N. Correction for non-perpendicularity of beam and tilt axis in tomographic reconstructions with the IMOD package. J. Microsc. 230, 212-217 (2008). (Pubitemid 351594959)
32. Amat, F. et al. Markov random field based automatic image alignment for electron tomography. J. Struct. Biol. 161, 260-275 (2008). (Pubitemid 351375088)
33. Nicastro, D. et al. Themolecular architecture of axonemesrevealed by cryoelectron tomography. Science 313, 944-948 (2006). (Pubitemid 44267380)
34. Pettersen, E. F. et al.UCSFChimera-a visualization systemfor exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
35. Metcalf, W. W. et al. Conditionally replicative and conjugative plasmids carrying lacZ alpha for cloning, mutagenesis, and allele replacement in bacteria. Plasmid 35, 1-13 (1996). (Pubitemid 26066220)
36. Iancu, C. V. et al. Electron cryotomography sample preparation using the Vitrobot. Nature Protocols 1, 2813-2819 (2006).