Differential modes of peptide binding onto replicative sliding clamps from various bacterial origins

Journal of Medicinal Chemistry

Volumn 57, Issue 18, 2014, Pages 7565-7576

  Wolff, Philippe ^a   Amal, Ismail ^b   Oliéric, Vincent ^c   Chaloin, Olivier ^d   Gygli, Gudrun ^b,f,g   Ennifar, Eric ^a   Lorber, Bernard ^a   Guichard, Gilles ^e   Wagner, Jérôme ^a   Dejaegere, Annick ^b   Burnouf, Dominique Y ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^c PAUL SCHERRER INSTITUTE   (Switzerland)

^d CNRS   (France)

^e UNIVERSITÉ DE BORDEAUX   (France)

^f WAGENINGEN UNIVERSITY   (Netherlands)

^g WU Agrotechnology and Food Sciences Laboratory of Biochemistry ^*  (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; ARTICLE; BACILLUS SUBTILIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; DNA METABOLISM; ESCHERICHIA COLI; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR INTERACTION; MOLECULAR MODEL; NONHUMAN; ORTHOLOGY; PEPTIDE SYNTHESIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; SURFACE PLASMON RESONANCE; BACTERIA; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; DNA REPLICATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; PEPTIDE; PROTEIN BINDING;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; BACTERIA; BACTERIAL PROTEINS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DNA REPLICATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN BINDING; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; THERMODYNAMICS;

EID: 84907450541     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm500467a     Document Type: Article

References (36)

1. O'Donnell, M.; Langston, L.; Stillman, B. Principles and concepts of DNA replication in bacteria, archaea, and eukarya Cold Spring Harbor Perspect. Biol. 2013, 5 (7) 1-13
2. Fay, P. J.; Johanson, K. O.; McHenry, C. S.; Bambara, R. A. Size classes of products synthesized processively by DNA polymerase III and DNA polymerase III holoenzyme of Escherichia coli J. Biol. Chem. 1981, 256 (2) 976-983
3. Hingorani, M. M.; O'Donnell, M. Sliding clamps: a (tail)ored fit Curr. Biol. 2000, 10 (1) R25-R29
4. Becherel, O. J.; Fuchs, R. P.; Wagner, J. Pivotal role of the beta-clamp in translesion DNA synthesis and mutagenesis in E. coli cells DNA Repair 2002, 1 (9) 703-708
5. Dalrymple, B. P.; Kongsuwan, K.; Wijffels, G.; Dixon, N. E.; Jennings, P. A. A universal protein-protein interaction motif in the eubacterial DNA replication and repair systems Proc. Natl. Acad. Sci. U.S.A. 2001, 98 (20) 11627-11632
6. Lopez de Saro, F. J.; O'Donnell, M. Interaction of the beta sliding clamp with MutS, ligase, and DNA polymerase I Proc. Natl. Acad. Sci. U.S.A. 2001, 98 (15) 8376-8380
7. Wijffels, G.; Dalrymple, B. P.; Prosselkov, P.; Kongsuwan, K.; Epa, V. C.; Lilley, P. E.; Jergic, S.; Buchardt, J.; Brown, S. E.; Alewood, P. F.; Jennings, P. A.; Dixon, N. E. Inhibition of protein interactions with the beta 2 sliding clamp of Escherichia coli DNA polymerase III by peptides from beta 2-binding proteins Biochemistry 2004, 43 (19) 5661-5671
8. Bunting, K. A.; Roe, S. M.; Pearl, L. H. Structural basis for recruitment of translesion DNA polymerase Pol IV/DinB to the beta-clamp EMBO J. 2003, 22 (21) 5883-5892
9. Burnouf, D. Y.; Olieric, V.; Wagner, J.; Fujii, S.; Reinbolt, J.; Fuchs, R. P.; Dumas, P. Structural and biochemical analysis of sliding clamp/ligand interactions suggest a competition between replicative and translesion DNA polymerases J. Mol. Biol. 2004, 335 (5) 1187-1197
10. Wolff, P.; Olieric, V.; Briand, J. P.; Chaloin, O.; Dejaegere, A.; Dumas, P.; Ennifar, E.; Guichard, G.; Wagner, J.; Burnouf, D. Y. Structure-based design of short peptide ligands binding onto the E. coli processivity ring J. Med. Chem. 2011, 54 (13) 4627-4637
11. Yin, Z.; Kelso, M. J.; Beck, J. L.; Oakley, A. J. Structural and thermodynamic dissection of linear motif recognition by the E. coli sliding clamp J. Med. Chem. 2013, 56 (21) 8665-8673
12. Friedberg, E. C.; Lehmann, A. R.; Fuchs, R. P. Trading places: how do DNA polymerases switch during translesion DNA synthesis? Mol. Cell 2005, 18 (5) 499-505
13. Lehmann, A. R.; Niimi, A.; Ogi, T.; Brown, S.; Sabbioneda, S.; Wing, J. F.; Kannouche, P. L.; Green, C. M. Translesion synthesis: Y-family polymerases and the polymerase switch DNA Repair 2007, 6 (7) 891-899
14. Georgescu, R. E.; Yurieva, O.; Kim, S. S.; Kuriyan, J.; Kong, X. P.; O'Donnell, M. Structure of a small-molecule inhibitor of a DNA polymerase sliding clamp Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (32) 11116-11121
15. Wijffels, G.; Johnson, W. M.; Oakley, A. J.; Turner, K.; Epa, V. C.; Briscoe, S. J.; Polley, M.; Liepa, A. J.; Hofmann, A.; Buchardt, J.; Christensen, C.; Prosselkov, P.; Dalrymple, B. P.; Alewood, P. F.; Jennings, P. A.; Dixon, N. E.; Winkler, D. A. Binding inhibitors of the bacterial sliding clamp by design J. Med. Chem. 2011, 54 (13) 4831-4838
16. Notredame, C.; Higgins, D. G.; Heringa, J. T-Coffee: A novel method for fast and accurate multiple sequence alignment J. Mol. Biol. 2000, 302 (1) 205-217
17. Gui, W. J.; Lin, S. Q.; Chen, Y. Y.; Zhang, X. E.; Bi, L. J.; Jiang, T. Crystal structure of DNA polymerase III beta sliding clamp from Mycobacterium tuberculosis Biochem. Biophys. Res. Commun. 2011, 405 (2) 272-277
18. Argiriadi, M. A.; Goedken, E. R.; Bruck, I.; O'Donnell, M.; Kuriyan, J. Crystal structure of a DNA polymerase sliding clamp from a Gram-positive bacterium BMC Struct Biol. 2006, 6, 2
19. World Health Organization (WHO). WHO Report 2011:Global Tuberculosis Control; WHO: Geneva, Switzerland, 2011.
20. Bacillus: Cellular and Molecular Biology; Graumann, P., Ed.; Caister Academic Press: Norfolk, U.K., 2007.
21. Bruck, I.; O'Donnell, M. The DNA replication machine of a gram-positive organism J. Biol. Chem. 2000, 275 (37) 28971-28983
22. Klemperer, N.; Zhang, D.; Skangalis, M.; O'Donnell, M. Cross-utilization of the beta sliding clamp by replicative polymerases of evolutionary divergent organisms J. Biol. Chem. 2000, 275 (34) 26136-26143
23. Freire, E. Do enthalpy and entropy distinguish first in class from best in class? Drug Discovery Today 2008, 13 (19-20) 869-874
24. Spolar, R. S.; Record, M. T., Jr. Coupling of local folding to site-specific binding of proteins to DNA Science 1994, 263 (5148) 777-784
25. Kabsch, W. Automatic processing of rotation diffraction data from crystals of initially unknown symetry and cell constants J. Appl. Crystallogr. 1993, 26, 795-800
26. Collaborative Computational Project, N. he CCP4 suite: programs for protein crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 1993, D50, 760-763
27. Bricogne, G.; Blanc, E.; Brandl, M.; Flensburg, C.; Keller, P.; Paciorek, W.; Roversi, P; Sharff, A.; Smart, O. S.; Vonrhein, C.; Womack, T. O. BUSTER, version 1.10.0; Global Phasing Ltd: Cambridge, U.K., 2011.
28. Emsley, P.; Cowtan, K. Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, 60 (Pt 12 Pt 1) 2126-2132
29. McCoy, A. J.; Grosse-Kunstleve, R. W.; Adams, P. D.; Winn, M. D.; Storoni, L. C.; Read, R. J. Phaser crystallographic software J. Appl. Crystallogr. 2007, 40, 658-674
30. Chen, V. B.; Arendall, W. B., III; Headd, J. J.; Keedy, D. A.; Immormino, R. M.; Kapral, G. J.; Murray, L. W.; Richardson, J. S.; Richardson, D. C. MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 2010, 66 (Pt 1) 12-21
31. DeLano, W. L. The Pymol Molecular Graphic System; DeLano Scientific LLC: Palo Alto, CA, 2008.
32. Kong, X. P.; Onrust, R.; O'Donnell, M.; Kuriyan, J. Three-dimensional structure of the beta subunit of E. coli DNA polymerase III holoenzyme: a sliding DNA clamp Cell 1992, 69 (3) 425-437
33. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kale, L.; Schulten, K. Scalable molecular dynamics with NAMD J. Comput. Chem. 2005, 26 (16) 1781-1802
34. MacKerell, A. D.; Bashford, D.; Bellott, M.; Dunbrack, R. L.; Evanseck, J. D.; Field, M. J.; Fischer, S.; Gao, J.; Guo, H.; Ha, S.; Joseph-McCarthy, D.; Kuchnir, L.; Kuczera, K.; Lau, F. T.; Mattos, C.; Michnick, S.; Ngo, T.; Nguyen, D. T.; Prodhom, B.; Reiher, W. E.; Roux, B.; Schlenkrich, M.; Smith, J. C.; Stote, R.; Straub, J.; Watanabe, M.; Wiorkiewicz-Kuczera, J.; Yin, D.; Karplus, M. All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B 1998, 102 (18) 3586-3616
35. Mackerell, A. D., Jr.; Feig, M.; Brooks, C. L., III Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations J. Comput. Chem. 2004, 25 (11) 1400-1415
36. Lafont, V.; Schaefer, M.; Stote, R. H.; Altschuh, D.; Dejaegere, A. Protein-protein recognition and interaction hot spots in an antigen-antibody complex: free energy decomposition identifies "efficient amino acids" Proteins 2007, 67 (2) 418-434