Structural insights into the inhibition of type VI effector Tae3 by its immunity protein Tai3

Biochemical Journal

Volumn 454, Issue 1, 2013, Pages 59-68

  Dong, Cheng ^a,b   Zhang, Heng ^c   Gao, Zeng Qiang ^b   Wang, Wen Jia ^b   She, Zhun ^b   Liu, Guang Feng ^b   Shen, Yue Quan ^a   Su, Xiao Dong ^c   Dong, Yu Hui ^b  

^a NANKAI UNIVERSITY   (China)

^b INSTITUTE OF HIGH ENERGY PHYSICS   (China)

^c PEKING UNIVERSITY   (China)

Author keywords

Nlpc p60; Type vi amidase effector 3; Type VI amidase immunity 3; Type VI secretion system (T6SS)

Indexed keywords

AMIDASE; HOMODIMER; TAE3 PROTEIN; TAI3 PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CELL VIABILITY; COMPLEX FORMATION; CONFORMATION; IMMUNITY; INTERSPECIFIC COMPETITION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; TYPE VI SECRETION SYSTEM;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CRYSTALLOGRAPHY, X-RAY; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; RALSTONIA PICKETTII;

EID: 84880911951     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20130193     Document Type: Article

References (48)

1. Gerlach, R. G. and Hensel, M. (2007) Protein secretion systems and adhesins: The molecular armory of Gram-negative pathogens. Int. J. Med. Microbiol. 297, 401-415.
2. Silverman, J. M., Brunet, Y. R., Cascales, E. and Mougous, J. D. (2012) Structure and regulation of the type VI secretion system. Annu. Rev. Microbiol. 66, 453-472.
3. Wu, C. F., Lin, J. S., Shaw, G. C. and Lai, E. M. (2012) Acid-induced type VI secretion system is regulated by ExoR-ChvG/ChvI signaling cascade in Agrobacterium tumefaciens. PLoS Pathog. 8, e1002938.
4. Casabona, M. G., Silverman, J. M., Sall, K. M., Boyer, F., Coute, Y., Poirel, J., Grunwald, D., Mougous, J. D., Elsen, S. and Attree, I. (2012) An ABC transporter and an outer membrane lipoprotein participate in posttranslational activation of type VI secretion in Pseudomonas aeruginosa . Environ. Microbiol. 15, 471-486.
5. Pukatzki, S., Ma, A. T., Sturtevant, D., Krastins, B., Sarracino, D., Nelson, W. C., Heidelberg, J. F. and Mekalanos, J. J. (2006) Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc. Natl. Acad. Sci. U.S.A. 103, 1528-1533.
6. 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.
7. Hood, R. D., Singh, P., Hsu, F., Guvener, T., Carl, M. A., Trinidad, R. R., Silverman, J. M., Ohlson, B. B., Hicks, K. G., Plemel, R. L. et al. (2010) A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7, 25-37.
8. 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.
9. 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.
10. 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.
11. 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.
12. 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.
13. 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.
14. Shang, G., Liu, X., Lu, D., Zhang, J., Li, N., Zhu, C., Liu, S., Yu, Q., Zhao, Y., Zhang, H. et al. (2012) Structural insight into how Pseudomonas aeruginosa peptidoglycanhydrolase Tse1 and its immunity protein Tsi1 function. Biochem. J. 448, 201-211.
15. 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.
16. Coenye, T., Goris, J., De Vos, P., Vandamme, P. and LiPuma, J. J. (2003) Classification of Ralstonia pickettii-like isolates from the environment and clinical samples as Ralstonia insidiosa sp. nov. Int. J. Syst. Evol. Microbiol. 53, 1075-1080.
17. Ryan, M. P., Pembroke, J. T. and Adley, C. C. (2007) Ralstonia pickettii in environmental biotechnology: potential and applications. J. Appl. Microbiol. 103, 754-764.
18. Ryan, M. P., Pembroke, J. T. and Adley, C. C. (2006) Ralstonia pickettii: A persistent Gram-negative nosocomial infectious organism. J. Hosp. Infect. 62, 278-284.
19. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326.
20. Terwilliger, T. C. and Berendzen, J. (1999) Automated MAD and MIR structure solution. Acta Crystallogr., Sect. D: Biol. Crystallogr. 55, 849-861.
21. Terwilliger, T. C. (2000) Maximum-likelihood density modification. Acta Crystallogr., Sect. D: Biol. Crystallogr. 56, 965-972.
22. Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W. et al. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 213-221.
23. Cowtan, K. (2006) The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr., Sect. D: Biol. Crystallogr. 62, 1002-1011.
24. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2126-2132.
25. Chen, V. B., Arendall, 3rd W. B., 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., Sect. D: Biol. Crystallogr. 66, 12-21.
26. Thompson, J. D., Gibson, T. J. and Higgins, D. G. (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr. Protoc. Bioinf., 2.3.1-2.3.22.
27. Gouet, P., Robert, X. and Courcelle, E. (2003) ESPript/ENDscript: Extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic Acids Res. 31, 3320-3323.
28. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606-1619.
29. 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.
30. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H. J. and Svergun, D. I. (2003) PRIMUS: A Windows PC-based system for small-Angle scattering data analysis. J. Appl. Crystallogr. 36, 1277-1282.
31. Svergun, D. I. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25, 495-503.
32. Svergun, D., Barberato, C. and Koch, M. H. J. (1995) CRYSOL: A program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28, 768-773.
33. Svergun, D. I., Petoukhov, M. V. and Koch, M. H. J. (2001) Determination of domain structure of proteins from X-ray solution scattering. Biophys. J. 80, 2946-2953.
34. Anantharaman, V. and Aravind, L. (2003) Evolutionary history, structural features and biochemical diversity of the NlpC/P60 superfamily of enzymes. Genome Biol. 4, R11.
35. 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.
36. Rigden, D. J., Jedrzejas, M. J. and Galperin, M. Y. (2003) Amidase domains from bacterial and phage autolysins define a family of γ -D, L-glutamate-specific amidohydrolases. Trends Biochem. Sci. 28, 230-234.
37. Aramini, J. M., Rossi, P., Huang, Y. J., Zhao, L., Jiang, M., Maglaqui, M., Xiao, R., Locke, J., Nair, R., Rost, B. et al. (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.
38. 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-W302.
39. Zhang, H., 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.
40. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797.
41. Both, D., Schneider, G. and Schnell, R. (2011) Peptidoglycan remodeling in Mycobacterium tuberculosis: comparison of structures and catalytic activities of RipA and RipB. J. Mol. Biol. 413, 247-260.
42. Ruggiero, A., Marasco, D., Squeglia, F., Soldini, S., Pedone, E., Pedone, C. and Berisio, R. (2010) Structure and functional regulation of RipA, a mycobacterial enzyme essential for daughter cell separation. Structure 18, 1184-1190.
43. Xu, Q., Abdubek, P., Astakhova, T., Axelrod, H. L., Bakolitsa, C., Cai, X., Carlton, D., Chen, C., Chiu, H. J., Chiu, M. et al. (2010) Structure of the γ -D-glutamyl-L-diamino acid endopeptidase YkfC from Bacillus cereus in complex with L-Ala-γ -D-Glu: insights into substrate recognition by NlpC/P60 cysteine peptidases. Acta Crystallogr., Sect. F: Struct. Biol. Crystal. Commun. 66, 1354-1364.
44. Schechter, I. and Berger, A. (1967) On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27, 157-162.
45. Arai, R., Fukui, S., Kobayashi, N. and Sekiguchi, J. (2012) Solution structure of IseA, an inhibitor protein of DL-endopeptidases from Bacillus subtilis, reveals a novel fold with a characteristic inhibitory loop. J. Biol. Chem. 287, 44736-44748.
46. Cole, C., Barber, J. D. and Barton, G. J. (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 36, W197-W201.
47. Holm, L. and Rosenstrom, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549.
48. Goessweiner-Mohr, N., Grumet, L., Arends, K., Pavkov-Keller, T., Gruber, C. C., Gruber, K., Birner-Gruenberger, R., Kropec-Huebner, A., Huebner, J., Grohmann, E. and Keller, W. (2013) The 2.5A° structure of the Enterococcus conjugation protein TraM resembles VirB8 type IV secretion proteins. J. Biol. Chem. 288, 2018-2028.