Structure of the type vi effector-immunity complex (Tae4-Tai4) provides novel insights into the inhibition mechanism of the effector by its immunity protein

Journal of Biological Chemistry

Volumn 288, Issue 8, 2013, Pages 5928-5939

  Zhang, Heng ^a   Gao, Zeng Qiang ^b   Wang, Wen Jia ^b   Liu, Guang Feng ^b   Xu, Jian Hua ^b   Su, Xiao Dong ^a   Dong, Yu Hui ^b  

^a PEKING UNIVERSITY   (China)

^b INSTITUTE OF HIGH ENERGY PHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNITY PROTEINS; INHIBITION MECHANISMS; INTERACTION MODULES;

BIOCHEMISTRY; BIOLOGY;

PROTEINS;

BACTERIAL PROTEIN; TYPE 4 AMIDASE EFFECTOR 4 PROTEIN; TYPE 4 AMIDASE IMMUNITY 4 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL IMMUNITY; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; ENTEROBACTER CLOACAE; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SALMONELLA TYPHIMURIUM; STRUCTURE ACTIVITY RELATION; TYPE IV SECRETION SYSTEM; ULTRACENTRIFUGATION; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; ENTEROBACTER CLOACAE; GENE EXPRESSION REGULATION, BACTERIAL; IMMUNE SYSTEM; LIGANDS; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SALMONELLA TYPHIMURIUM; SURFACE PLASMON RESONANCE;

EID: 84874342857     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.434357     Document Type: Article

References (37)

1. Cambronne, E. D., and Roy, C. R. (2006) Recognition and delivery of effector proteins into eukaryotic cells by bacterial secretion systems. Traffic 7, 929-939
2. 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
3. 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
4. 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 Pathogens 8, e1002613
5. Zou, T., Yao, X., Qin, B., Zhang, M., Cai, L., Shang, W., Svergun, D. I., Wang, M., Cui, S., and Jin, Q. (2012) Crystal structure of Pseudomonas aeruginosa Tsi2 reveals a stably folded superhelical antitoxin. J. Mol. Biol. 417, 351-361
6. 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 type VI secretion effector superfamily identified using a heuristic approach. Cell Host Microbe 11, 538-549
7. Benz, J., Sendlmeier, C., Barends, T. R., and Meinhart, A. (2012) Structural insights into the effector-immunity system Tse1/Tsi1 from Pseudomonas aeruginosa. PLoS ONE 7, e40453
8. Chou, S., Bui, N. K., Russell, A. B., Lexa, K. W., Gardiner, T. E., LeRoux, M., Vollmer, W., and Mougous, J. D. (2012) Structure of a peptidoglycan amidase effector targeted to Gram-negative bacteria by the type VI secretion system. Cell Rep. 1, 656-664
9. Ding, J., Wang, W., Feng, H., Zhang, Y., and Wang, D. C. (2012) Structural insights into the Pseudomonas aeruginosa type VI virulence effector Tse1 bacteriolysis and self-protection mechanisms. J. Biol. Chem. 287, 26911-26920
10. Zhang, H., Gao, Z. Q., Su, X. D, and Dong, Y. H. (2012) Crystal structure of type VI effector Tse1 from Pseudomonas aeruginosa. FEBS Lett. 586, 3193-3199
11. Zhang, H., Gao, Z. Q., Wang, W. J., Liu, G. F., Shtykova, E. V., Xu, J. H., Li, L. F., Su, X. D., and Dong, Y. H. (2012) The crystal structure of the MPN domain from COP9 signalosome subunit CSN6. FEBS Lett. 586, 1147-1153
12. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
13. Sheldrick, G. M. (2010) Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr. D Biol. Crystallogr. 66, 479-485
14. Terwilliger, T. C. (2000) Maximum likelihood density modification. Acta Crystallogr. D Biol. Crystallogr. 56, 965-972
15. Cowtan, K. (2006) The Buccaneer software for automated model building. Acta Crystallogr. D Biol. Crystallogr. 62, 1002-1011
16. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
17. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., Mc-Coy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K., and Terwilliger, T. C. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948-1954
18. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
19. Chen, V. B., Arendall, W. B., 3rd., Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21
20. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H., and Svergun, D. I. (2003) PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr. 36, 1277-1282
21. Svergun, D. I. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25, 495-503
22. Svergun, D. I., Barberato, C., and Koch, M. H. (1995) CRYSOL: a program to evaluate x-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28, 768-773
23. Svergun, D. I., Petoukhov, M. V., and Koch, M. H. (2001) Determination of domain structure of proteins from x-ray solution scattering. Biophys. J. 80, 2946-2953
24. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606-1619
25. Morris, G. M., Huey, R., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., and Olson, A. J. (2009) AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J. Comput. Chem. 30, 2785-2791
26. Anantharaman, V., and Aravind, L. (2003) Evolutionary history, structural features, and biochemical diversity of the NlpC/P60 superfamily of enzymes. Genome Biol. 4, R11
27. Bateman, A., and Rawlings, N. D. (2003) The CHAP domain: a large family of amidases including GSP amidase and peptidoglycan hydrolases. Trends Biochem. Sci. 28, 234-237
28. Rigden, D. J., Jedrzejas, M. J., and Galperin, M. Y. (2003) Amidase domains from bacterial and phage autolysins define a family of β-D,L-glutamatespecific amidohydrolases. Trends Biochem. Sci. 28, 230-234
29. Holm, L., Kääriäinen, S., Rosenström, P., and Schenkel, A. (2008) Searching protein structure databases with DaliLite v. 3. Bioinformatics 24, 2780-2781
30. Xu, Q., Abdubek, P., Astakhova, T., Axelrod, H. L., Bakolitsa, C., Cai, X., Carlton, D., Chen, C., Chiu, H. J., Chiu, M., Clayton, T., Das, D., Deller, M. C., Duan, L., Ellrott, K., Farr, C. L., Feuerhelm, J., Grant, J. C., Grzechnik, A., Han, G. W., Jaroszewski, L., Jin, K. K., Klock, H. E., Knuth, M. W., Kozbial, P., Krishna, S. S., Kumar, A., Lam, W. W., Marciano, D., Miller, M. D., Morse, A. T., Nigoghossian, E., Nopakun, A., Okach, L., Puckett, C., Reyes, R., Tien, H. J., Trame, C. B., van den Bedem, H., Weekes, D., Woo-ten, T., Yeh, A., Hodgson, K. O., Wooley, J., Elsliger, M. A., Deacon, A. M., Godzik, A., Lesley, S. A., and Wilson, I. A. (2010) Structure of the β-Dglutamyl-L- diamino acid endopeptidase YkfC from Bacillus cereus in complex with L-Ala-β-D-Glu: insights into substrate recognition by NlpC/ P60 cysteine peptidases. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 66, 1354-1364
31. Krissinel, E., and Henrick, K. (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D Biol. Crystallogr. 60, 2256-2268
32. Schechter, I., and Berger, A. (1967) On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27, 157-162
33. Landau, M., Mayrose, I., Rosenberg, Y., Glaser, F., Martz, E., Pupko, T., and Ben-Tal, N. (2005) ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res. 33, W299-302
34. Aramini, J. M., Rossi, P., Huang, Y. J., Zhao, L., Jiang, M., Maglaqui, M., Xiao, R., Locke, J., Nair, R., Rost, B., Acton, T. B., Inouye, M., and Montelione, G. T. (2008) Solution NMR structure of the NlpC/P60 domain of lipoprotein Spr from Escherichia coli: structural evidence for a novel cysteine peptidase catalytic triad. Biochemistry 47, 9715-9717
35. Takai, H., Xie, Y., de Lange, T., and Pavletich, N. P. (2010) Tel2 structure and function in the Hsp90-dependent maturation of mTOR and ATR complexes. Genes Dev. 24, 2019-2030
36. Park, J. T., and Uehara, T. (2008) How bacteria consume their own exoskeletons (turnover and recycling of cell wall peptidoglycan). Microbiol. Mol. Biol. Rev. 72, 211-227
37. Smith, T. J., Blackman, S. A., and Foster, S. J. (2000) Autolysins of Bacillus subtilis: multiple enzymes with multiple functions. Microbiology 146, 249-262