Structure of the VipA/B type VI secretion complex suggests a contraction-state-specific recycling mechanism

Cell Reports

Volumn 8, Issue 1, 2014, Pages 20-30

  Kube, Sebastian ^a   Kapitein, Nicole ^b,c   Zimniak, Tomasz ^a   Herzog, Franz ^a   Mogk, Axel ^b,c   Wendler, Petra ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN VIPA; PROTEIN VIPB; UNCLASSIFIED DRUG; PROTEIN BINDING; VIRUS PROTEIN;

ARTICLE; BACTERIOPHAGE T4; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN RECYCLING; PROTEIN SECONDARY STRUCTURE; PROTEIN SUBUNIT; STRUCTURAL HOMOLOGY; STRUCTURE ANALYSIS; TYPE VI SECRETION SYSTEM; VALIDATION PROCESS; VIBRIO CHOLERAE; BURKHOLDERIA; DIMERIZATION; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN SECRETION; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; SYMBIOSIS; TYPE IV SECRETION SYSTEM; AMINO ACID SEQUENCE; BACTERIAL SECRETION SYSTEM; CHEMISTRY; ENTEROBACTERIA PHAGE T4; METABOLISM; MICROTUBULE; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; ULTRASTRUCTURE;

BACTERIA (MICROORGANISMS); EUKARYOTA; VIBRIO CHOLERAE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; BACTERIOPHAGE T4; MICROTUBULES; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; VIBRIO CHOLERAE; VIRAL PROTEINS;

EID: 84904068515     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.05.034     Document Type: Article

References (35)

1. Aksyuk A.A., Leiman P.G., Kurochkina L.P., Shneider M.M., Kostyuchenko V.A., Mesyanzhinov V.V., Rossmann M.G. The tail sheath structure of bacteriophage T4: a molecular machine for infecting bacteria. EMBO J. 2009, 28:821-829.
2. Aksyuk A.A., Kurochkina L.P., Fokine A., Forouhar F., Mesyanzhinov V.V., Tong L., Rossmann M.G. Structural conservation of the myoviridae phage tail sheath protein fold. Structure 2011, 19:1885-1894.
3. Amos L.A., Klug A. Three-dimensional image reconstructions of the contractile tail of T4 bacteriophage. J.Mol. Biol. 1975, 99:51-64.
4. Aubert D., MacDonald D.K., Valvano M.A. 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. 2010, 285:35988-35998.
5. Basler M., Pilhofer M., Henderson G.P., Jensen G.J., Mekalanos J.J. Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 2012, 483:182-186.
6. Basler M., Ho B.T., Mekalanos J.J. Tit-for-tat: type VI secretionsystem counterattack during bacterial cell-cell interactions. Cell 2013, 152:884-894.
7. Bönemann 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. 2009, 28:315-325.
8. Bröms J.E., Lavander M., Sjöstedt A. A conserved alpha-helix essential for a type VI secretion-like system of Francisella tularensis. J.Bacteriol. 2009, 191:2431-2446.
9. Bröms J.E., Ishikawa T., Wai S.N., Sjöstedt A. A functional VipA-VipB interaction is required for the type VI secretion system activity of Vibrio cholerae O1 strain A1552. BMC Microbiol. 2013, 13:96.
10. Cascales E., Cambillau C. Structural biology of type VI secretion systems. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2012, 367:1102-1111.
11. Coulthurst S.J. The Type VI secretion system - a widespread and versatile cell targeting system. Res. Microbiol. 2013, 164:640-654.
12. Fokine A., Zhang Z., Kanamaru S., Bowman V.D., Aksyuk A.A., Arisaka F., Rao V.B., Rossmann M.G. The molecular architecture of the bacteriophage T4 neck. J.Mol. Biol. 2013, 425:1731-1744.
13. Hayes C.S., Aoki S.K., Low D.A. Bacterial contact-dependent delivery systems. Annu. Rev. Genet. 2010, 44:71-90.
14. Herzog F., Kahraman A., Boehringer D., Mak R., Bracher A., Walzthoeni T., Leitner A., Beck M., Hartl F.U., Ban N., et al. Structural probing of a protein phosphatase 2A network by chemical cross-linking and mass spectrometry. Science 2012, 337:1348-1352.
15. Kapitein N., Bönemann G., Pietrosiuk A., Seyffer F., Hausser I., Locker J.K., Mogk A. ClpV recycles VipA/VipB tubules and prevents non-productive tubule formation to ensure efficient type VI protein secretion. Mol. Microbiol. 2013, 87:1013-1028.
16. Lander G.C., Saibil H.R., Nogales E. Go hybrid: EM, crystallography, and beyond. Curr. Opin. Struct. Biol. 2012, 22:627-635.
17. Leiman P.G., Shneider M.M. Contractile tail machines of bacteriophages. Adv. Exp. Med. Biol. 2012, 726:93-114.
18. 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 2004, 118:419-429.
19. Leiman P.G., Basler M., Ramagopal U.A., Bonanno J.B., Sauder J.M., Pukatzki S., Burley S.K., Almo S.C., Mekalanos J.J. TypeVIsecretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc. Natl. Acad. Sci. USA 2009, 106:4154-4159.
20. Leiman P.G., Arisaka F., van Raaij M.J., Kostyuchenko V.A., Aksyuk A.A., Kanamaru S., Rossmann M.G. Morphogenesis of the T4 tail and tail fibers. Virol. J. 2010, 7:355.
21. Lossi N.S., Dajani R., Freemont P., Filloux A. Structure-function analysis of HsiF, a gp25-like component of the type VI secretion system, in Pseudomonas aeruginosa. Microbiology 2011, 157:3292-3305.
22. Lossi N.S., Manoli E., Förster A., Dajani R., Pape T., Freemont P., Filloux A. The HsiB1C1 (TssB-TssC) complex of the Pseudomonas aeruginosa type VI secretion system forms a bacteriophage tail sheathlike structure. J.Biol. Chem. 2013, 288:7536-7548.
23. Mougous J.D., Cuff M.E., Raunser S., Shen A., Zhou M., Gifford C.A., Goodman A.L., Joachimiak G., Ordoñez C.L., Lory S., et al. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 2006, 312:1526-1530.
24. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., Ferrin T.E. UCSF Chimera-a visualization systemfor exploratory research and analysis. J.Comput. Chem. 2004, 25:1605-1612.
25. Pietrosiuk A., Lenherr E.D., Falk S., Bönemann G., Kopp J., Zentgraf H., Sinning I., Mogk A. Molecular basis for the unique role of the AAA+ chaperone ClpV in type VI protein secretion. J.Biol. Chem. 2011, 286:30010-30021.
26. Pintilie G.D., Zhang J., Goddard T.D., Chiu W., Gossard D.C. Quantitative analysis of cryo-EM density map segmentation by watershed and scale-space filtering, and fitting of structures by alignment to regions. J.Struct. Biol. 2010, 170:427-438.
27. Pukatzki S., Ma A.T., Revel A.T., Sturtevant D., Mekalanos J.J. Type VI secretion system translocates a phage tail spike-like protein into targetcells where it cross-links actin. Proc. Natl. Acad. Sci. USA 2007, 104:15508-15513.
28. Records A.R. The type VI secretion system: a multipurpose deliverysystem with a phage-like machinery. Mol. Plant Microbe Interact. 2011, 24:751-757.
29. Rost B., Yachdav G., Liu J. The PredictProtein server. Nucleic Acids Res. 2004, 32(Web Server issue):W321-W326.
30. Shneider M.M., Buth S.A., Ho B.T., Basler M., Mekalanos J.J., Leiman P.G. PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 2013, 500:350-353.
31. Silverman J.M., Agnello D.M., Zheng H., Andrews B.T., Li M., Catalano C.E., Gonen T., Mougous J.D. Haemolysin coregulated protein is an exported receptor and chaperone of type VI secretion substrates. Mol. Cell 2013, 51:584-593.
32. Söding J. Protein homology detection by HMM-HMM comparison. Bioinformatics 2005, 21:951-960.
33. Walther-Mauruschat A., Mayer F. Isolation and characterization of polysheaths, phage tail-like defective bacteriophages of Alcaligenes eutrophus H 16. J.Gen. Virol. 1978, 41:239-254.
34. Xu D., Zhang Y. Ab initio protein structure assembly using continuous structure fragments and optimized knowledge-based force field. Proteins 2012, 80:1715-1735.
35. Zhang X.Y., Brunet Y.R., Logger L., Douzi B., Cambillau C., Journet L., Cascales E. Dissection of the TssB-TssC interface duringtype VI secretion sheath complex formation. PLoS ONE 2013, 8:e81074.