Lytic activity of the Vibrio cholerae type VI secretion toxin VgrG-3 is inhibited by the antitoxin TsaB

Journal of Biological Chemistry

Volumn 288, Issue 11, 2013, Pages 7618-7625

  Brooks, Teresa M ^a   Unterweger, Daniel ^a   Bachmann, Verena ^a   Kostiuk, Benjamin ^a   Pukatzki, Stefan ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

C-TERMINAL EXTENSIONS; DIRECT INTERACTIONS; GRAM-NEGATIVE BACTERIA; MICROBIAL COMPETITION; PEPTIDOGLYCANS; SECRETION SYSTEMS; TOXIN ACTIVITY; VIBRIO CHOLERAE;

PHYSIOLOGY;

TOXIC MATERIALS;

ANTITOXIN; BACTERIAL PROTEIN; LYSOZYME; PEPTIDOGLYCAN; TYPE SIX SECRETION ANTITOXIN B; UNCLASSIFIED DRUG; VALINE GLYCINE REPEAT G 3 PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; TOXIN STRUCTURE; TYPE IV SECRETION SYSTEM; TYPE SIX SECRETION ANTITOXIN B GENE; VIBRIO CHOLERAE;

ANTITOXINS; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CELL WALL; CLONING, MOLECULAR; COMPUTATIONAL BIOLOGY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN-ION CONCENTRATION; HYDROLYSIS; MODELS, BIOLOGICAL; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; VIBRIO CHOLERAE; VIRULENCE; VIRULENCE FACTORS;

EID: 84875179267     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.436725     Document Type: Article

References (26)

1. 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
2. Ballister, E. R., Lai, A. H., Zuckermann, R. N., Cheng, Y., and Mougous, J. D. (2008) In vitro self-assembly of tailorable nanotubes from a simple protein building block. Proc. Natl. Acad. Sci. U.S.A. 105, 3733-3738
3. 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
4. Hachani, A., Lossi, N. S., Hamilton, A., Jones, C., Bleves, S., Albesa-Jové, D., and Filloux, A. (2011) Type VI secretion system in Pseudomonas aeruginosa: secretion and multimerization of VgrG proteins. J. Biol. Chem. 286, 12317-12327
5. 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
6. 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
7. 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
8. Blondel, C. J., Jiménez, J. C., Contreras, I., and Santiviago, C. A. (2009) Comparative genomic analysis uncovers 3 novel loci encoding type six secretion systems differentially distributed in Salmonella serotypes. BMC Genomics 10, 354
9. 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
10. 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
11. 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
12. Basler, M., and Mekalanos, J. J. (2012) Type 6 secretion dynamics within and between bacterial cells. Science 337, 815
13. Hoyle, B. D., and Beveridge, T. J. (1984) Metal binding by the peptidoglycan sacculus of Escherichia coli K-12. Can J. Microbiol. 30, 204-211
14. MacIntyre, D. L., Miyata, S. T., Kitaoka, M., and Pukatzki, S. (2010) The Vibrio cholerae type VI secretion system displays antimicrobial properties. Proc. Natl. Acad. Sci. U.S.A. 107, 19520-19524
15. Miyata, S. T., Kitaoka, M., Brooks, T. M., McAuley, S. B., and Pukatzki, S. (2011) Vibrio cholerae requires the type VI secretion system virulence factor VasX to kill Dictyostelium discoideum. Infect Immun. 79, 2941-2949
16. Wilkesman, J., and Kurz, L. (2009) Protease Analysis by Zymography: A review on tehcniques and patents. Recent Pat. Biotechnol. 3, 175-184
17. Schmelcher, M., Waldherr, F., and Loessner, M. J. (2012) Listeria bacteriophage peptidoglycan hydrolases feature high thermoresistance and reveal increased activity after divalent metal cation substitution. Appl. Microbiol. Biotechnol. 93, 633-643
18. Son, B., Yun, J., Lim, J. A., Shin, H., Heu, S., and Ryu, S. (2012) Characterization of LysB4, an endolysin from the Bacillus cereus-infecting bacteriophage B4. BMC Microbiol. 12, 33
19. Zhang, H., Gao, Z. Q., Wang, W. J., Liu, G. F., Xu, J. H., Su, X. D., and Dong, Y. H. (2013) Structure of the type VI effector-immunity complex (Tae4-Tai4) provides novel insights into the inhibition mechanism of the effector by its immunity protein. J. Biol. Chem. 288, 5928-5939
20. Russell, A. B., Singh, P., Brittnacher, M., Bui, N. K., Hood, R. D., Carl, M. A., Agnello, D. M., Schwarz, S., Goodlett, D. R., Vollmer, W., and Mougous, J. D. (2012) A widespread bacterial type VI secretion effector superfamily identified using a heuristic approach. Cell Host Microbe. 11, 538-549
21. Yamaguchi, Y., Park, J. H., and Inouye, M. (2011) Toxin-antitoxin systems in bacteria and archaea. Annu. Rev. Genet. 45, 61-79
22. Li, M., Le Trong, I., Carl, M. A., Larson, E. T., Chou, S., De Leon, J. A., Dove, S. L., Stenkamp, R. E., and Mougous, J. D. (2012) Structural basis for type VI secretion effector recognition by a cognate immunity protein. PLoS Pathog. 8, e1002613
23. Kanamaru, S., Gassner, N. C., Ye, N., Takeda, S., and Arisaka, F. (1999) The C-terminal fragment of the precursor tail lysozyme of bacteriophage T4 stays as a structural component of the baseplate after cleavage. J Bacteriol. 181, 2739-2744
24. Zahrl, D., Wagner, M., Bischof, K., Bayer, M., Zavecz, B., Beranek, A., Ruckenstuhl, C., Zarfel, G. E., and Koraimann, G. (2005) Peptidoglycan degradation by specialized lytic transglycosylases associated with type III and type IV secretion systems. Microbiology 151, 3455-3467
25. Pukatzki, S., Ma, A. T., Revel, A. T., Sturtevant, D., and 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
26. Moran, A. P., Gupta, A., and Joshi, L. (2011) Sweet-talk: role of host glycosylation in bacterial pathogenesis of the gastrointestinal tract. Gut. 60, 1412-1425