Structural insights into the effector - immunity system Tse1/Tsi1 from Pseudomonas aeruginosa

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Benz, Juliane ^a   Sendlmeier, Christina ^a   Barends, Thomas R M ^a   Meinhart, Anton ^a  

^a MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HISTIDINE; PROTEIN TSE1; PROTEIN TSI1; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; BURKHOLDERIA PHYTOFIRMANS; BURKHOLDERIACEAE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISULFIDE BOND; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME MECHANISM; HYDROGEN BOND; NONHUMAN; OPEN READING FRAME; PROTEIN CLEAVAGE; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PSEUDOMONAS AERUGINOSA; STRUCTURE ANALYSIS; TYPE VI SECRETION SYSTEM;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CATALYTIC DOMAIN; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; CYSTEINE PROTEASES; CYSTEINE PROTEINASE INHIBITORS; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STABILITY; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PSEUDOMONAS AERUGINOSA; STRUCTURAL HOMOLOGY, PROTEIN;

BURKHOLDERIA PHYTOFIRMANS; NEGIBACTERIA; PSEUDOMONAS AERUGINOSA;

EID: 84863648629     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040453     Document Type: Article

References (64)

1. Leplae R, Geeraerts D, Hallez R, Guglielmini J, Dreze P, et al. (2011) Diversity of bacterial type II toxin-antitoxin systems: a comprehensive search and functional analysis of novel families. Nucleic Acids Res 39 (13): 5513-5525.
2. Pandey DP, Gerdes K, (2005) Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Res 33 (3): 966-976.
3. Kolodkin-Gal I, Verdiger R, Shlosberg-Fedida A, Engelberg-Kulka H, (2009) A differential effect of E. coli toxin-antitoxin systems on cell death in liquid media and biofilm formation. PLoS One 4 (8): e6785.
4. Braun V, Pilsl H, Gross P, (1994) Colicins: structures, modes of action, transfer through membranes, and evolution. Arch Microbiol 161 (3): 199-206.
5. Riley MA, Wertz JE, (2002) Bacteriocins: evolution, ecology, and application. Annu Rev Microbiol 56: 117-137.
6. Cramer WA, Lindeberg M, Taylor R, (1999) The best offense is a good defense. Nat Struct Biol 6 (4): 295-297.
7. Hayes F, (2003) Toxins-antitoxins: plasmid maintenance, programmed cell death, and cell cycle arrest. Science 301 (5639): 1496-1499.
8. Fineran PC, Blower TR, Foulds IJ, Humphreys DP, Lilley KS, et al. (2009) The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair. Proc Natl Acad Sci U S A 106 (3): 894-899.
9. Engelberg-Kulka H, Amitai S, Kolodkin-Gal I, Hazan R, (2006) Bacterial programmed cell death and multicellular behavior in bacteria. PLoS Genet 2 (10): e135.
10. Engelberg-Kulka H, Glaser G, (1999) Addiction modules and programmed cell death and antideath in bacterial cultures. Annu Rev Microbiol 53: 43-70.
11. Gerdes K, Christensen SK, Lobner-Olesen A, (2005) Prokaryotic toxin-antitoxin stress response loci. Nat Rev Microbiol 3 (5): 371-382.
12. Fu Z, Donegan NP, Memmi G, Cheung AL, (2007) Characterization of MazFSa, an endoribonuclease from Staphylococcus aureus. J Bacteriol 189 (24): 8871-8879.
13. Pedersen K, Zavialov AV, Pavlov MY, Elf J, Gerdes K, et al. (2003) The bacterial toxin RelE displays codon-specific cleavage of mRNAs in the ribosomal A site. Cell 112 (1): 131-140.
14. Bernard P, Couturier M, (1992) Cell killing by the F plasmid CcdB protein involves poisoning of DNA-topoisomerase II complexes. J Mol Biol 226 (3): 735-745.
15. Schumacher MA, Piro KM, Xu W, Hansen S, Lewis K, et al. (2009) Molecular mechanisms of HipA-mediated multidrug tolerance and its neutralization by HipB. Science 323 (5912): 396-401.
16. Mutschler H, Gebhardt M, Shoeman RL, Meinhart A, (2011) A novel mechanism of programmed cell death in bacteria by toxin-antitoxin systems corrupts peptidoglycan synthesis. PLoS Biol 9 (3): e1001033.
17. Hartley RW, Smeaton JR, (1973) On the reaction between the extracellular ribonuclease of Bacillus amyloliquefaciens (barnase) and its intracellular inhibitor (barstar). J Biol Chem 248 (16): 5624-5626.
18. Papadakos G, Wojdyla JA, Kleanthous C, (2012) Nuclease colicins and their immunity proteins. Q Rev Biophys 45 (1): 57-103.
19. Cascales E, Buchanan SK, Duche D, Kleanthous C, Lloubes R, et al. (2007) Colicin biology. Microbiol Mol Biol Rev 71 (1): 158-229.
20. James R, Penfold CN, Moore GR, Kleanthous C, (2002) Killing of E coli cells by E group nuclease colicins. Biochimie 84 (5-6): 381-389.
21. Jani AJ, Cotter PA, (2010) Type VI secretion: not just for pathogenesis anymore. Cell Host Microbe 8 (1): 2-6.
22. Schwarz S, Hood RD, Mougous JD, (2010) What is type VI secretion doing in all those bugs? Trends Microbiol 18 (12): 531-537.
23. Hood RD, Singh P, Hsu F, Guvener T, Carl MA, et al. (2010) A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7 (1): 25-37.
24. Russell AB, Hood RD, Bui NK, LeRoux M, Vollmer W, et al. (2011) Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475 (7356): 343-347.
25. Bönemann G, Pietrosiuk A, Mogk A, (2010) Tubules and donuts: a type VI secretion story. Mol Microbiol 76 (4): 815-821.
26. Cascales E, (2008) The type VI secretion toolkit. EMBO Rep 9 (8): 735-741.
27. Cascales E, Cambillau C, (2012) Structural biology of type VI secretion systems. Philos Trans R Soc Lond B Biol Sci 367 (1592): 1102-1111.
28. Mougous JD, Cuff ME, Raunser S, Shen A, Zhou M, et al. (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312 (5779): 1526-1530.
29. Li M, Le Trong I, Carl MA, Larson ET, Chou S, et al. (2012) Structural Basis for Type VI Secretion Effector Recognition by a Cognate Immunity Protein. PLoS Pathog 8 (4): e1002613.
30. Zou T, Yao X, Qin B, Zhang M, Cai L, et al. (2012) Crystal structure of Pseudomonas aeruginosa Tsi2 reveals a stably folded superhelical antitoxin. J Mol Biol 417 (4): 351-361.
31. Anantharaman V, Aravind L, (2003) Evolutionary history, structural features and biochemical diversity of the NlpC/P60 superfamily of enzymes. Genome Biol 4 (2): R11.
32. Bateman A, Rawlings ND, (2003) The CHAP domain: a large family of amidases including GSP amidase and peptidoglycan hydrolases. Trends Biochem Sci 28 (5): 234-237.
33. Rigden DJ, Jedrzejas MJ, Galperin MY, (2003) Amidase domains from bacterial and phage autolysins define a family of gamma-D,L-glutamate-specific amidohydrolases. Trends Biochem Sci 28 (5): 230-234.
34. Holm L, Rosenstrom P, (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res 38 (Web Server issue): W545-549.
35. Xu Q, Abdubek P, Astakhova T, Axelrod HL, Bakolitsa C, et al. (2010) Structure of the gamma-D-glutamyl-L-diamino acid endopeptidase YkfC from Bacillus cereus in complex with L-Ala-gamma-D-Glu: insights into substrate recognition by NlpC/P60 cysteine peptidases. Acta Crystallogr Sect F Struct Biol Cryst Commun 66 (Pt 10): 1354-1364.
36. Xu Q, Sudek S, McMullan D, Miller MD, Geierstanger B, et al. (2009) Structural basis of murein peptide specificity of a gamma-D-glutamyl-l-diamino acid endopeptidase. Structure 17 (2): 303-313.
37. Aramini JM, Rossi P, Huang YJ, Zhao L, Jiang M, 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 (37): 9715-9717.
38. Storer AC, Menard R, (1994) Catalytic mechanism in papain family of cysteine peptidases. Methods Enzymol 244: 486-500.
39. Sudmeier JL, Bradshaw EM, Haddad KE, Day RM, Thalhauser CJ, et al. (2003) Identification of histidine tautomers in proteins by 2D 1H/13C(delta2) one-bond correlated NMR. J Am Chem Soc 125 (28): 8430-8431.
40. Miranda JJ, (2003) Position-dependent interactions between cysteine residues and the helix dipole. Protein Sci 12 (1): 73-81.
41. Derewenda ZS, Derewenda U, Kobos PM, (1994) (His)C epsilon-H.O = C
42. Robertus JD, Kraut J, Alden RA, Birktoft JJ, (1972) Subtilisin; a stereochemical mechanism involving transition-state stabilization. Biochemistry 11 (23): 4293-4303.
43. Hedstrom L, (2002) Serine protease mechanism and specificity. Chem Rev 102 (12): 4501-4524.
44. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215 (3): 403-410.
45. Russell AB, Singh P, Brittnacher M, Bui NK, Hood RD, et al. (2012) A Widespread Bacterial Type VI Secretion Effector Superfamily Identified Using a Heuristic Approach. Cell Host Microbe 11 (5): 538-549.
46. Fülöp V, Jones DT, (1999) Beta propellers: structural rigidity and functional diversity. Curr Opin Struct Biol 9 (6): 715-721.
47. Nakajima Y, Ito K, Toshima T, Egawa T, Zheng H, et al. (2008) Dipeptidyl aminopeptidase IV from Stenotrophomonas maltophilia exhibits activity against a substrate containing a 4-hydroxyproline residue. J Bacteriol 190 (23): 7819-7829.
48. Meng W, Brigance RP, Chao HJ, Fura A, Harrity T, et al. (2010) Discovery of 6-(aminomethyl)-5-(2,4-dichlorophenyl)-7-methylimidazo[1,2-a]pyrimidine-2-carboxa mides as potent, selective dipeptidyl peptidase-4 (DPP4) inhibitors. J Med Chem 53 (15): 5620-5628.
49. Temme C, Weissbach R, Lilie H, Wilson C, Meinhart A, et al. (2009) The Drosophila melanogaster Gene cg4930 Encodes a High Affinity Inhibitor for Endonuclease G. J Biol Chem 284 (13): 8337-8348.
50. Van Duyne GD, Standaert RF, Karplus PA, Schreiber SL, Clardy J, (1993) Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J Mol Biol 229 (1): 105-124.
51. Kabsch W, (1993) Automatic Processing of Rotation Diffraction Data from Crystals of Initially Unknown Symmetry and Cell Constants. J Appl Crystallogr 26: 795-800.
52. Sheldrick GM, (2008) A short history of SHELX. Acta Crystallogr A 64 (Pt 1): 112-122.
53. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60 (Pt 12 Pt 1): 2126-2132.
54. Collaborative Computational Project N (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50 (Pt 5): 760-763.
55. Winn MD, Isupov MN, Murshudov GN, (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr D Biol Crystallogr 57 (Pt 1): 122-133.
56. Brunger AT, (2007) Version 1.2 of the Crystallography and NMR system. Nat Protoc 2 (11): 2728-2733.
57. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54 (Pt 5): 905-921.
58. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, et al. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35 (Web Server issue): W375-383.
59. DeLano WL, (2002) The PyMOL Molecular Graphics System. DeLano Scientific LLC, San Carlos, California, USA.
60. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA, (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A 98 (18): 10037-10041.
61. Barton GJ, (1993) ALSCRIPT: a tool to format multiple sequence alignments. Protein Eng 6 (1): 37-40.
62. Livingstone CD, Barton GJ, (1993) Protein sequence alignments: a strategy for the hierarchical analysis of residue conservation. Comput Appl Biosci 9 (6): 745-756.
63. Kabsch W, (1976) A solution for the best rotation to relate two sets of vectors. Acta Crystallogr D Biol Crystallogr A32: 922-923.
64. Krissinel E, Henrick K, (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372 (3): 774-797.