Structure of a Peptidoglycan Amidase Effector Targeted to Gram-Negative Bacteria by the Type VI Secretion System

Cell Reports

Volumn 1, Issue 6, 2012, Pages 656-664

  Chou, Seemay ^a   Bui, Nhat Khai ^b   Russell, Alistair B ^a   Lexa, Katrina W ^c   Gardiner, Taylor E ^a   LeRoux, Michele ^a   Vollmer, Waldemar ^b   Mougous, Joseph D ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDASE; PEPTIDOGLYCAN; PROTEIN TSE1; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL WALL; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ISOLATION; ENZYME MODIFICATION; ENZYME SPECIFICITY; ENZYME STRUCTURE; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; NONHUMAN; PSEUDOMONAS AERUGINOSA; TYPE VI SECRETION SYSTEM;

AMIDOHYDROLASES; AMINO ACID SEQUENCE; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CATALYTIC DOMAIN; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; DISACCHARIDES; MASS SPECTROMETRY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDOGLYCAN; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PSEUDOMONAS AERUGINOSA; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; POSIBACTERIA; PSEUDOMONAS AERUGINOSA;

EID: 84863088336     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2012.05.016     Document Type: Article

References (49)

1. 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., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:213-221.
2. Anantharaman V., Aravind L. Evolutionary history, structural features and biochemical diversity of the NlpC/P60 superfamily of enzymes. Genome Biol. 2003, 4:R11.
3. Aramini J.M., Rossi P., Huang Y.J., Zhao L., Jiang M., Maglaqui M., Xiao R., Locke J., Nair R., Rost B., et al. Solution NMR structure of the NlpC/P60 domain of lipoprotein Spr from Escherichia coli: structural evidence for a novel cysteine peptidase catalytic triad. Biochemistry 2008, 47:9715-9717.
4. 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.
5. Bernard C.S., Brunet Y.R., Gueguen E., Cascales E. Nooks and crannies in type VI secretion regulation. J. Bacteriol. 2010, 192:3850-3860.
6. Böth D., Schneider G., Schnell R. Peptidoglycan remodeling in Mycobacterium tuberculosis: comparison of structures and catalytic activities of RipA and RipB. J. Mol. Biol. 2011, 413:247-260.
7. Bui N.K., Gray J., Schwarz H., Schumann P., Blanot D., Vollmer W. The peptidoglycan sacculus of Myxococcus xanthus has unusual structural features and is degraded during glycerol-induced myxospore development. J. Bacteriol. 2009, 191:494-505.
8. Bui N.K., Eberhardt A., Vollmer D., Kern T., Bougault C., Tomasz A., Simorre J.P., Vollmer W. Isolation and analysis of cell wall components from Streptococcus pneumoniae. Anal. Biochem. 2012, 421:657-666.
9. Cascales E. The type VI secretion toolkit. EMBO Rep. 2008, 9:735-741.
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. Davis I.W., Murray L.W., Richardson J.S., Richardson D.C. MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes. Nucleic Acids Res. 2004, 32(Web Server issue). W615-9.
12. Dubey V.K., Pande M., Singh B.K., Jagannadham M.V. Papain-like proteases: Applications of their inhibitors. Afr. J. Biotechnol. 2007, 6:1077-1086.
13. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:2126-2132.
14. Friesner R.A., Banks J.L., Murphy R.B., Halgren T.A., Klicic J.J., Mainz D.T., Repasky M.P., Knoll E.H., Shelley M., Perry J.K., et al. Glide: a new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy. J. Med. Chem. 2004, 47:1739-1749.
15. Friesner R.A., Murphy R.B., Repasky M.P., Frye L.L., Greenwood J.R., Halgren T.A., Sanschagrin P.C., Mainz D.T. Extra precision glide: docking and scoring incorporating a model of hydrophobic enclosure for protein-ligand complexes. J. Med. Chem. 2006, 49:6177-6196.
16. Glauner B. Separation and quantification of muropeptides with high-performance liquid chromatography. Anal. Biochem. 1988, 172:451-464.
17. Goodman A.L., Kulasekara B., Rietsch A., Boyd D., Smith R.S., Lory S. A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev. Cell 2004, 7:745-754.
18. Halgren T.A., Murphy R.B., Friesner R.A., Beard H.S., Frye L.L., Pollard W.T., Banks J.L. Glide: a new approach for rapid, accurate docking and scoring. 2. Enrichment factors in database screening. J. Med. Chem. 2004, 47:1750-1759.
19. Holm L., Rosenström P. Dali server: conservation mapping in 3D. Nucleic Acids Res. 2010, 38(Web Server issue). W545-9.
20. 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., et al. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 2010, 7:25-37.
21. Jani A.J., Cotter P.A. Type VI secretion: not just for pathogenesis anymore. Cell Host Microbe 2010, 8:2-6.
22. Kanamaru S. Structural similarity of tailed phages and pathogenic bacterial secretion systems. Proc. Natl. Acad. Sci. USA 2009, 106:4067-4068.
23. Kelley L.A., Sternberg M.J. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 2009, 4:363-371.
24. Khersonsky O., Tawfik D.S. Enzyme promiscuity: a mechanistic and evolutionary perspective. Annu. Rev. Biochem. 2010, 79:471-505.
25. Laskowski M.A., Osborn E., Kazmierczak B.I. A novel sensor kinase-response regulator hybrid regulates type III secretion and is required for virulence in Pseudomonas aeruginosa. Mol. Microbiol. 2004, 54:1090-1103.
26. Ma A.T., McAuley S., Pukatzki S., Mekalanos J.J. Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe 2009, 5:234-243.
27. MacDowell A.A., Celestre R.S., Howells M., McKinney W., Krupnick J., Cambie D., Domning E.E., Duarte R.M., Kelez N., Plate D.W., et al. Suite of three protein crystallography beamlines with single superconducting bend magnet as the source. J. Synchrotron Radiat. 2004, 11:447-455.
28. MacIntyre D.L., Miyata S.T., Kitaoka M., Pukatzki S. The Vibrio cholerae type VI secretion system displays antimicrobial properties. Proc. Natl. Acad. Sci. USA 2010, 107:19520-19524.
29. Meberg B.M., Sailer F.C., Nelson D.E., Young K.D. Reconstruction of Escherichia coli mrcA (PBP 1a) mutants lacking multiple combinations of penicillin binding proteins. J. Bacteriol. 2001, 183:6148-6149.
30. 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.
31. Murdoch S.L., Trunk K., English G., Fritsch M.J., Pourkarimi E., Coulthurst S.J. The opportunistic pathogen Serratia marcescens utilises Type VI secretion to target bacterial competitors. J Bacteriol. 2011, Published online September 2, 2011. 10.1128/JB.05671-11.
32. Nakimbugwe D., Masschalck B., Atanassova M., Zewdie-Bosüner A., Michiels C.W. Comparison of bactericidal activity of six lysozymes at atmospheric pressure and under high hydrostatic pressure. Int. J. Food Microbiol. 2006, 108:355-363.
33. Nelson K.E., Weinel C., Paulsen I.T., Dodson R.J., Hilbert H., Martins dos Santos V.A., Fouts D.E., Gill S.R., Pop M., Holmes M., et al. Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ. Microbiol. 2002, 4:799-808.
34. 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 system for exploratory research and analysis. J. Comput. Chem. 2004, 25:1605-1612.
35. Russell A.B., Hood R.D., Bui N.K., LeRoux M., Vollmer W., Mougous J.D. Type VI secretion delivers bacteriolytic effectors to target cells. Nature 2011, 475:343-347.
36. Russell A.B., Singh P., Brittnacher M., Bui N.K., Hood R.D., Carl M.A., Agnello D.A., Schwarz S., Goodlett D.R., Vollmer W., et al. A widespread type VI secretion effector superfamily identified using a heuristic approach. Cell Host Microbe 2012, 11:538-549.
37. Schechter I., Berger A. On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 1967, 27:157-162.
38. Schrodinger, LLC (2010). The PyMOL Molecular Graphics System, Version 1.3r1. http://www.pymol.org/.
39. Schwarz S., Hood R.D., Mougous J.D. What is type VI secretion doing in all those bugs?. Trends Microbiol. 2010, 18:531-537.
40. Schwarz S., West T.E., Boyer F., Chiang W.C., Carl M.A., Hood R.D., Rohmer L., Tolker-Nielsen T., Skerrett S.J., Mougous J.D. Burkholderia type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog. 2010, 6:e1001068.
41. Severin A., Tomasz A. Naturally occurring peptidoglycan variants of Streptococcus pneumoniae. J. Bacteriol. 1996, 178:168-174.
42. Silverman J.M., Austin L.S., Hsu F., Hicks K.G., Hood R.D., Mougous J.D. Separate inputs modulate phosphorylation-dependent and -independent type VI secretion activation. Mol. Microbiol. 2011, 82:1277-1290.
43. Srivatsan A., Han Y., Peng J., Tehranchi A.K., Gibbs R., Wang J.D., Chen R. High-precision, whole-genome sequencing of laboratory strains facilitates genetic studies. PLoS Genet. 2008, 4:e1000139.
44. Stover C.K., Pham X.Q., Erwin A.L., Mizoguchi S.D., Warrener P., Hickey M.J., Brinkman F.S., Hufnagle W.O., Kowalik D.J., Lagrou M., et al. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 2000, 406:959-964.
45. Typas A., Banzhaf M., Gross C.A., Vollmer W. From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat. Rev. Microbiol. 2012, 10:123-136.
46. Vollmer W. Bacterial outer membrane evolution via sporulation?. Nat. Chem. Biol. 2012, 8:14-18.
47. Vollmer W., Blanot D., de Pedro M.A. Peptidoglycan structure and architecture. FEMS Microbiol. Rev. 2008, 32:149-167.
48. Xu Q., Abdubek P., Astakhova T., Axelrod H.L., Bakolitsa C., Cai X., Carlton D., Chen C., Chiu H.J., Chiu M., et al. 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. Cryst. Commun. 2010, 66:1354-1364.
49. Yao Q., Cui J., Zhu Y., Wang G., Hu L., Long C., Cao R., Liu X., Huang N., Chen S., et al. A bacterial type III effector family uses the papain-like hydrolytic activity to arrest the host cell cycle. Proc. Natl. Acad. Sci. USA 2009, 106:3716-3721.