Coevolution of the ATPase ClpV, the sheath proteins TssB and TssC, and the accessory protein TagJ/HsiE1 distinguishes type VI secretion classes

Journal of Biological Chemistry

Volumn 289, Issue 47, 2014, Pages 33032-33043

  Förster, Andreas ^a   Planamente, Sara ^a   Manoli, Eleni ^a   Lossi, Nadine S ^a,b   Freemont, Paul S ^a   Filloux, Alain ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b NOVARTIS PHARMA GMBH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOPHAGES; HYDROPHOBICITY; PHYSIOLOGY; PROTEINS;

EUKARYOTIC CELLS; HYBRID APPROACH; N-TERMINAL DOMAINS; PHYLOGENETIC ANALYSIS; PSEUDOMONAS AERUGINOSA; SECRETION SYSTEMS; STRUCTURAL ALTERATIONS; TUBULAR STRUCTURES;

CRYSTAL STRUCTURE;

ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; CLPV PROTEIN; HSIB1 PROTEIN; HSIE1 PROTEIN; MICROORGANISM PROTEIN; TAGI PROTEIN; TSSB PROTEIN; TSSC PROTEIN; UNCLASSIFIED DRUG; AMINO ACID; BACTERIAL SECRETION SYSTEM; PROTEIN BINDING;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIUM IDENTIFICATION; BINDING AFFINITY; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; GENETIC CONSERVATION; HYDROPHOBICITY; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NONHUMAN; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PSEUDOMONAS AERUGINOSA; SPECIES DIFFERENCE; TYPE VI SECRETION SYSTEM; VIBRIO CHOLERAE; AMINO ACID SEQUENCE; BACTERIAL SECRETION SYSTEM; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; PROTEIN MOTIF; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

ADENOSINE TRIPHOSPHATASES; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMINO ACIDS; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; EVOLUTION, MOLECULAR; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS AERUGINOSA; SPECIES SPECIFICITY; VIBRIO CHOLERAE;

EID: 84911376547     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.600510     Document Type: Article

References (48)

1. Coulthurst, S. J. (2013) The Type VI secretion system: a widespread and versatile cell targeting system. Res. Microbiol. 164, 640-654
2. Ho, B. T., Dong, T. G., and Mekalanos, J. J. (2014) A view to a kill: the bacterial type VI secretion system. Cell Host Microbe 15, 9-21
3. Ma, A. T., McAuley, S., Pukatzki, S., and Mekalanos, J. J. (2009) Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe 5, 234-243
4. Ma, A. T., and Mekalanos, J. J. (2010) In vivo actin cross-linking induced by Vibrio cholerae type VI secretion system is associated with intestinal inflammation. Proc. Natl. Acad. Sci. U.S.A. 107, 4365-4370
5. Pukatzki, S., McAuley, S. B., and Miyata, S. T. (2009) The type VI secretion system: translocation of effectors and effector-domains. Curr. Opin. Microbiol. 12, 11-17
6. Suarez, G., Sierra, J. C., Erova, T. E., Sha, J., Horneman, A. J., and 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
7. Brooks, T. M., Unterweger, D., Bachmann, V., Kostiuk, B., and 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
8. Dong, T. G., Ho, B. T., Yoder-Himes, D. R., and Mekalanos, J. J. (2013) Identification of T6SS-dependent effector and immunity proteins by Tnseq in Vibrio cholerae. Proc. Natl. Acad. Sci. U.S.A. 110, 2623-2628
9. Hood, R. D., Singh, P., Hsu, F., Güvener, T., Carl, M. A., Trinidad, R. R., Silverman, J. M., Ohlson, B. B., Hicks, K. G., Plemel, R. L., Li, M., Schwarz, S., Wang, W. Y., Merz, A. J., Goodlett, D. R., and Mougous, J. D. (2010) A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7, 25-37
10. Murdoch, S. L., Trunk, K., English, G., Fritsch, M. J., Pourkarimi, E., and Coulthurst, S. J. (2011) The opportunistic pathogen Serratia marcescens utilizes type VI secretion to target bacterial competitors. J. Bacteriol. 193, 6057-6069
11. Russell, A. B., Hood, R. D., Bui, N. K., LeRoux, M., Vollmer, W., and Mougous, J. D. (2011) Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475, 343-347
12. Russell, A. B., LeRoux, M., Hathazi, K., Agnello, D. M., Ishikawa, T., Wiggins, P. A., Wai, S. N., and Mougous, J. D. (2013) Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors. Nature 496, 508-512
13. Whitney, J. C., Chou, S., Russell, A. B., Biboy, J., Gardiner, T. E., Ferrin, M. A., Brittnacher, M., Vollmer, W., and Mougous, J. D. (2013) Identification, structure, and function of a novel type VI secretion peptidoglycan glycoside hydrolase effector-immunity pair. J. Biol. Chem. 288, 26616-26624
14. Ma, L. S., Hachani, A., Lin, J. S., Filloux, A., and Lai, E. M. (2014) Agrobacterium tumefaciens deploys a superfamily of type VI secretion DNase effectors as weapons for interbacterial competition in planta. Cell Host Microbe 16, 94-104
15. Hachani, A., Allsopp, L. P., Oduko, Y., and Filloux, A. (2014) The VgrG proteins are "a la carte" delivery systems for bacterial type VI effectors. J. Biol. Chem. 289, 17872-17884
16. Whitney, J. C., Beck, C. M., Goo, Y. A., Russell, A. B., Harding, B. N., De Leon, J. A., Cunningham, D. A., Tran, B. Q., Low, D. A., Goodlett, D. R., Hayes, C. S., and Mougous, J. D. (2014) Genetically distinct pathways guide effector export through the type VI secretion system. Mol. Microbiol. 92, 529-542
17. Fu, Y., Waldor, M. K., and Mekalanos, J. J. (2013) Tn-Seq analysis of Vibrio cholerae intestinal colonization reveals a role for T6SS-mediated antibacterial activity in the host. Cell Host Microbe 14, 652-663
18. Kanamaru, S., Leiman, P. G., Kostyuchenko, V. A., Chipman, P. R., Mesyanzhinov, V. V., Arisaka, F., and Rossmann, M. G. (2002) Structure of the cell-puncturing device of bacteriophage T4. Nature 415, 553-557
19. Aksyuk, A. A., Leiman, P. G., Kurochkina, L. P., Shneider, M. M., Kostyuchenko, V. A., Mesyanzhinov, V. V., and Rossmann, M. G. (2009) The tail sheath structure of bacteriophage T4: a molecular machine for infecting bacteria. EMBO J. 28, 821-829
20. Basler, M., Pilhofer, M., Henderson, G. P., Jensen, G. J., and Mekalanos, J. J. (2012) Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483, 182-186
21. Bönemann, G., Pietrosiuk, A., Diemand, A., Zentgraf, H., and Mogk, A. (2009) Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO J. 28, 315-325
22. Kube, S., Kapitein, N., Zimniak, T., Herzog, F., Mogk, A., and Wendler, P. (2014) Structure of the VipA/B type VI secretion complex suggests a contraction-state-specific recycling mechanism. Cell Rep. 8, 20-30
23. Lossi, N. S., Manoli, E., Förster, A., Dajani, R., Pape, T., Freemont, P., and Filloux, A. (2013) The HsiB1C1 (TssB-TssC) complex of the Pseudomonas aeruginosa type VI secretion system forms a bacteriophage tail sheathlike structure. J. Biol. Chem. 288, 7536-7548
24. Zhang, X. Y., Brunet, Y. R., Logger, L., Douzi, B., Cambillau, C., Journet, L., and Cascales, E. (2013) Dissection of the TssB-TssC interface during type VI secretion sheath complex formation. PLoS One 8, e81074
25. Leiman, P. G., Basler, M., Ramagopal, U. A., Bonanno, J. B., Sauder, J. M., Pukatzki, S., Burley, S. K., Almo, S. C., and Mekalanos, J. J. (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
26. Basler, M., Ho, B. T., and Mekalanos, J. J. (2013) Tit-for-tat: type VI secretion system counterattack during bacterial cell-cell interactions. Cell 152, 884-894
27. Kapitein, N., Bönemann, G., Pietrosiuk, A., Seyffer, F., Hausser, I., Locker, J. K., and Mogk, A. (2013) ClpV recycles VipA/VipB tubules and prevents non-productive tubule formation to ensure efficient type VI protein secretion. Mol. Microbiol. 87, 1013-1028
28. + chaperone ClpV in type VI protein secretion. J. Biol. Chem. 286, 30010-30021
29. + proteins: have engine, will work. Nat. Rev. Mol. Cell Biol. 6, 519-529
30. Zheng, J., Ho, B., and 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
31. Filloux, A., Hachani, A., and Bleves, S. (2008) The bacterial type VI secretion machine: yet another player for protein transport across membranes. Microbiology 154, 1570-1583
32. 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., Walz, T., Joachimiak, A., and Mekalanos, J. J. (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312, 1526-1530
33. Lossi, N. S., Manoli, E., Simpson, P., Jones, C., Hui, K., Dajani, R., Coulthurst, S. J., Freemont, P., and Filloux, A. (2012) The archetype Pseudomonas aeruginosa proteins TssB and TagJ form a novel sub-complex in the bacterial Type VI secretion system. Mol. Microbiol. Biol. Crystallogr. 86, 437-456
34. Kabsch, W. (2010) Xds. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132
35. Battye, T. G., Kontogiannis, L., Johnson, O., Powell, H. R., and Leslie, A. G. (2011) iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D Biol. Crystallogr. 67, 271-281
36. McCoy, A. J. (2007) Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr. D Biol. Crystallogr. 63, 32-41
37. Forouhar, F., Kuzin, A., Seetharaman, J., Lee, I., Zhou, W., Abashidze, M., Chen, Y., Yong, W., Janjua, H., Fang, Y., Wang, D., Cunningham, K., Xiao, R., Acton, T. B., Pichersky, E., Klessig, D. F., Porter, C. W., Montelione, G. T., and Tong, L. (2007) Functional insights from structural genomics. J. Struct. Funct. Genomics 8, 37-44
38. Murshudov, G. N., Skubák, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F., and Vagin, A. A. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367
39. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
40. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
41. Karimova, G., Pidoux, J., Ullmann, A., and Ladant, D. (1998) A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc. Natl. Acad. Sci. U.S.A. 95, 5752-5756
42. Miller, J. H. (1992) A Short Course in Bacterial Genetics: A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria, pp. 71-80, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
43. Kuraku, S., Zmasek, C. M., Nishimura, O., and Katoh, K. (2013) aLeaves facilitates on-demand exploration of metazoan gene family trees on MAFFT sequence alignment server with enhanced interactivity. Nucleic Acids Res. 41, W22-W28
44. Guindon, S., Delsuc, F., Dufayard, J. F., and Gascuel, O. (2009) Estimating maximum likelihood phylogenies with PhyML. Methods Mol. Biol. 537, 113-137
45. Chevenet, F., Brun, C., Bañuls, A. L., Jacq, B., and Christen, R. (2006) TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics 7, 439
46. Schlieker, C., Zentgraf, H., Dersch, P., and Mogk, A. (2005) ClpV, a unique Hsp100/Clp member of pathogenic proteobacteria. Biol. Chem. 386, 1115-1127
47. Bladergroen, M. R., Badelt, K., and Spaink, H. P. (2003) Infection-blocking genes of a symbiotic Rhizobium leguminosarum strain that are involved in temperature-dependent protein secretion. Mol. Plant Microbe Interact. 16, 53-64
48. Bröms, J. E., Lavander, M., and Sjöstedt, A. (2009) A conserved α-helix essential for a type VI secretion-like system of Francisella tularensis. J. Bacteriol. 191, 2431-2446