Structures of the Ultra-High-Affinity Protein-Protein Complexes of Pyocins S2 and AP41 and Their Cognate Immunity Proteins from Pseudomonas aeruginosa

Journal of Molecular Biology

Volumn 427, Issue 17, 2015, Pages 2852-2866

  Joshi, Amar ^a   Grinter, Rhys ^b   Josts, Inokentijs ^b   Chen, Sabrina ^a   Wojdyla, Justyna A ^a   Lowe, Edward D ^a   Kaminska, Renata ^a   Sharp, Connor ^a   McCaughey, Laura ^b   Roszak, Aleksander W ^b   Cogdell, Richard J ^b   Byron, Olwyn ^b   Walker, Daniel ^b   Kleanthous, Colin ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

bacteriocin; immunity protein; P aeruginosa.; pyocin AP41; pyocin S2

Indexed keywords

ASPARTIC ACID; BACTERIAL PROTEIN; BACTERIOCIN; COLICIN; DEOXYRIBONUCLEASE; GLYCINE; PYOCIN; PYOCIN AP41; PYOCIN S2; UNCLASSIFIED DRUG; MULTIPROTEIN COMPLEX; PROTEIN BINDING;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CRYSTAL STRUCTURE; ENZYME MECHANISM; GRAM NEGATIVE BACTERIUM; HYDROGEN BOND; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA; AMINO ACID SEQUENCE; DNA SEQUENCE; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN ANALYSIS; PROTEIN TERTIARY STRUCTURE; ULTRASTRUCTURE; X RAY CRYSTALLOGRAPHY;

ESCHERICHIA COLI; NEGIBACTERIA; PSEUDOMONAS AERUGINOSA;

AMINO ACID SEQUENCE; BASE SEQUENCE; COLICINS; CRYSTALLOGRAPHY, X-RAY; DEOXYRIBONUCLEASES; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; MUTATION; PHYLOGENY; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS AERUGINOSA; PYOCINS; SEQUENCE ANALYSIS, DNA;

EID: 84939262566     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2015.07.014     Document Type: Article

References (49)

1. M.P. Stumpf, T. Thorne, E. de Silva, R. Stewart, H.J. An, M. Lappe, and et al. Estimating the size of the human interactome Proc. Natl. Acad. Sci. U. S. A. 105 19 2008 6959 6964
2. M. Rebsamen, R.K. Kandasamy, and G. Superti-Furga Protein interaction networks in innate immunity Trends Immunol. 34 12 2013 610 619
3. J.B. Rothbard, and M.L. Gefter Interactions between immunogenic peptides and MHC proteins Annu. Rev. Immunol. 9 1991 527 565
4. D.P. Ryan, and J.M. Matthews Protein-protein interactions in human disease Curr. Opin. Struct. Biol. 15 4 2005 441 446
5. C. Kleanthous, and D. Walker Immunity proteins: Enzyme inhibitors that avoid the active site Trends Biochem. Sci. 26 10 2001 624 631
6. R. Wallis, K.Y. Leung, A.J. Pommer, H. Videler, G.R. Moore, R. James, and et al. Protein-protein interactions in colicin E9 DNase-immunity protein complexes. 2. Cognate and noncognate interactions that span the millimolar to femtomolar affinity range Biochemistry 34 42 1995 13751 13759
7. R. Wallis, G.R. Moore, R. James, and C. Kleanthous Protein-protein interactions in colicin E9 DNase-immunity protein complexes. 1. Diffusion-controlled association and femtomolar binding for the cognate complex Biochemistry 34 42 1995 13743 13750
8. W. Li, A.H. Keeble, C. Giffard, R. James, G.R. Moore, and C. Kleanthous Highly discriminating protein-protein interaction specificities in the context of a conserved binding energy hotspot J. Mol. Biol. 337 3 2004 743 759
9. A.H. Keeble, N. Kirkpatrick, S. Shimizu, and C. Kleanthous Calorimetric dissection of colicin DNase-immunity protein complex specificity Biochemistry 45 10 2006 3243 3254
10. A.H. Keeble, L.A. Joachimiak, M.J. Mate, N. Meenan, N. Kirkpatrick, D. Baker, and et al. Experimental and computational analyses of the energetic basis for dual recognition of immunity proteins by colicin endonucleases J. Mol. Biol. 379 4 2008 745 759
11. G. Papadakos, J.A. Wojdyla, and C. Kleanthous Nuclease colicins and their immunity proteins Q. Rev. Biophys. 45 1 2012 57 103
12. K.B. Levin, O. Dym, S. Albeck, S. Magdassi, A.H. Keeble, C. Kleanthous, and et al. Following evolutionary paths to protein-protein interactions with high affinity and selectivity Nat. Struct. Mol. Biol. 16 10 2009 1049 1055
13. K. Bernath, S. Magdassi, and D.S. Tawfik Directed evolution of protein inhibitors of DNA-nucleases by in vitro compartmentalization (IVC) and nano-droplet delivery J. Mol. Biol. 345 5 2005 1015 1026
14. L.A. Joachimiak, T. Kortemme, B.L. Stoddard, and D. Baker Computational design of a new hydrogen bond network and at least a 300-fold specificity switch at a protein-protein interface J. Mol. Biol. 361 1 2006 195 208
15. T. Kortemme, L.A. Joachimiak, A.N. Bullock, A.D. Schuler, B.L. Stoddard, and D. Baker Computational redesign of protein-protein interaction specificity Nat. Struct. Mol. Biol. 11 4 2004 371 379
16. M.A. Riley Molecular mechanisms of bacteriocin evolution Annu. Rev. Genet. 32 1998 255 278
17. B.L. Stoddard Homing endonuclease structure and function Q. Rev. Biophys. 38 1 2005 49 95
18. A.J. Pommer, R. Wallis, G.R. Moore, R. James, and C. Kleanthous Enzymological characterization of the nuclease domain from the bacterial toxin colicin E9 from Escherichia coli Biochem. J. 334 Pt 2 1998 387 392
19. A.J. Pommer, S. Cal, A.H. Keeble, D. Walker, S.J. Evans, U.C. Kuhlmann, and et al. Mechanism and cleavage specificity of the H-N-H endonuclease colicin E9 J. Mol. Biol. 314 4 2001 735 749
20. C. Kleanthous, U.C. Kuhlmann, A.J. Pommer, N. Ferguson, S.E. Radford, G.R. Moore, and et al. Structural and mechanistic basis of immunity toward endonuclease colicins Nat. Struct. Biol. 6 3 1999 243 252
21. T.P. Ko, C.C. Liao, W.Y. Ku, K.F. Chak, and H.S. Yuan The crystal structure of the DNase domain of colicin E7 in complex with its inhibitor Im7 protein Structure 7 1 1999 91 102
22. M.J. Mate, and C. Kleanthous Structure-based analysis of the metal-dependent mechanism of H-N-H endonucleases J. Biol. Chem. 279 33 2004 34763 34769
23. U.C. Kuhlmann, A.J. Pommer, G.R. Moore, R. James, and C. Kleanthous Specificity in protein-protein interactions: The structural basis for dual recognition in endonuclease colicin-immunity protein complexes J. Mol. Biol. 301 5 2000 1163 1178
24. W. Li, S.J. Hamill, A.M. Hemmings, G.R. Moore, R. James, and C. Kleanthous Dual recognition and the role of specificity-determining residues in colicin E9 DNase-immunity protein interactions Biochemistry 37 34 1998 11771 11779
25. N.A. Meenan, A. Sharma, S.J. Fleishman, C.J. Macdonald, B. Morel, R. Boetzel, and et al. The structural and energetic basis for high selectivity in a high-affinity protein-protein interaction Proc. Natl. Acad. Sci. U. S. A. 107 22 2010 10080 10085
26. M.A. Riley Positive selection for colicin diversity in bacteria Mol. Biol. Evol. 10 5 1993 1048 1059
27. D.J. Wilson, and G. McVean Estimating diversifying selection and functional constraint in the presence of recombination Genetics 172 3 2006 1411 1425
28. Y. Tan, and M.A. Riley Positive selection and recombination: Major molecular mechanisms in colicin diversification Trends Ecol. Evol. 12 9 1997 348 351
29. Y. Michel-Briand, and C. Baysse The pyocins of Pseudomonas aeruginosa Biochimie 84 5-6 2002 499 510
30. R. Wallis, K.Y. Leung, M.J. Osborne, R. James, G.R. Moore, and C. Kleanthous Specificity in protein-protein recognition: conserved Im9 residues are the major determinants of stability in the colicin E9 DNase-Im9 complex Biochemistry 37 2 1998 476 485
31. K.C. Hsia, K.F. Chak, P.H. Liang, Y.S. Cheng, W.Y. Ku, and H.S. Yuan DNA binding and degradation by the HNH protein ColE7 Structure 12 2 2004 205 214
32. A.J. Pommer, U.C. Kuhlmann, A. Cooper, A.M. Hemmings, G.R. Moore, R. James, and et al. Homing in on the role of transition metals in the HNH motif of colicin endonucleases J. Biol. Chem. 274 38 1999 27153 27160
33. J.A. Wojdyla, S.J. Fleishman, D. Baker, and C. Kleanthous Structure of the ultra-high-affinity colicin E2 DNase-Im2 complex J. Mol. Biol. 417 1-2 2012 79 94
34. A.H. Keeble, and C. Kleanthous The kinetic basis for dual recognition in colicin endonuclease-immunity protein complexes J. Mol. Biol. 352 3 2005 656 671
35. K.B. Li ClustalW-MPI: ClustalW analysis using distributed and parallel computing Bioinformatics 19 12 2003 1585 1586
36. T. Miyake, N. Takebayashi, and D.E. Wolf Possible diversifying selection in the imprinted gene, MEDEA, in Arabidopsis Mol. Biol. Evol. 26 4 2009 843 857
37. R. Wallis, A. Reilly, A. Rowe, G.R. Moore, R. James, and C. Kleanthous In vivo and in vitro characterization of overproduced colicin E9 immunity protein Eur. J. Biochem. 207 2 1992 687 695
38. W. Kabsch Xds Acta Crystallogr. D Biol. Crystallogr. 66 Pt 2 2010 125 132
39. P.R. Evans, and G.N. Murshudov How good are my data and what is the resolution? Acta Crystallogr. D Biol. Crystallogr. 69 Pt 7 2013 1204 1214
40. M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, P.R. Evans, and et al. Overview of the CCP4 suite and current developments Acta Crystallogr. D Biol. Crystallogr. 67 Pt 4 2011 235 242
41. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallogr. 40 Pt 4 2007 658 674
42. G.N. Murshudov, P. Skubak, A.A. Lebedev, N.S. Pannu, R.A. Steiner, R.A. Nicholls, and et al. REFMAC5 for the refinement of macromolecular crystal structures Acta Crystallogr. D Biol. Crystallogr. 67 Pt 4 2011 355 367
43. P. Emsley, and K. Cowtan Coot: Model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 Pt 12 Pt 1 2004 2126 2132
44. V.A. Sole, E. Papillon, M. Cotte, P. Walter, and J. Susini A multiplatform code for the analysis of energy-dispersive X-ray fluorescence spectra Spectrochim. Acta B At. Spectrosc. 62 1 2007 63 68
45. P.D. Adams, P.V. Afonine, G. Bunkoczi, V.B. Chen, I.W. Davis, N. Echols, and et al. PHENIX: A comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 Pt 2 2010 213 221
46. W.L. DeLano The PyMOL Molecular Graphics System, Version 1.3r1 2010 Schrödinger, LLC New York, NY
47. E. Krissinel, and K. Henrick Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 3 2007 774 797
48. S.J. Fleishman, A. Leaver-Fay, J.E. Corn, E.M. Strauch, S.D. Khare, N. Koga, and et al. RosettaScripts: A scripting language interface to the Rosetta macromolecular modeling suite PLoS One 6 6 2011 e20161s
49. R. Das, and D. Baker Macromolecular modeling with rosetta Annu. Rev. Biochem. 77 2008 363 382