Structure-based design of short peptide ligands binding onto the E. coli processivity ring

Journal of Medicinal Chemistry

Volumn 54, Issue 13, 2011, Pages 4627-4637

  Wolff, Philippe ^a   Oliéric, Vincent ^b   Briand, Jean Paul ^c   Chaloin, Olivier ^c   Dejaegere, Annick ^d   Dumas, Philippe ^a   Ennifar, Eric ^a   Guichard, Gilles ^e   Wagner, Jérôme ^a   Burnouf, Dominique Y ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b PAUL SCHERRER INSTITUTE   (Switzerland)

^c INSTITUT DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

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

^e UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; DNA POLYMERASE; HEPTAPEPTIDE; PENTAPEPTIDE;

ARTICLE; BINDING AFFINITY; CHEMICAL MODIFICATION; CRYSTAL STRUCTURE; DRUG DESIGN; ESCHERICHIA COLI; HYDROPHOBICITY; IC 50; LIGAND BINDING; MOLECULAR INTERACTION; NONHUMAN; STRUCTURE ACTIVITY RELATION; THERMODYNAMICS;

EID: 79960198988     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm200311m     Document Type: Article

References (49)

1. 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, 425-437
2. Gulbis, J. M.; Kelman, Z.; Hurwitz, J.; O'Donnell, M.; Kuriyan, J. Structure of the C-terminal region of p21(WAF1/CIP1) complexed with human PCNA Cell 1996, 87, 297-306 (Pubitemid 26359007)
3. Shamoo, Y.; Steitz, T. A. Building a replisome from interacting pieces: sliding clamp complexed to a peptide from DNA polymerase and a polymerase editing complex Cell 1999, 99, 155-166 (Pubitemid 29491782)
4. Matsumiya, S.; Ishino, Y.; Morikawa, K. Crystal structure of an archaeal DNA sliding clamp: proliferating cell nuclear antigen from Pyrococcus furiosus Protein Sci. 2001, 10, 17-23 (Pubitemid 32221160)
5. Johnson, A.; O'Donnell, M. Cellular DNA replicases: components and dynamics at the replication fork Annu. Rev. Biochem. 2005, 74, 283-315 (Pubitemid 40995509)
6. Fuchs, R. P.; Fujii, S. Translesion synthesis in Escherichia coli: lessons from the NarI mutation hot spot DNA Repair (Amst.) 2007, 6, 1032-1041 (Pubitemid 46880482)
7. Prakash, S.; Johnson, R. E.; Prakash, L. Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function Annu. Rev. Biochem. 2005, 74, 317-353 (Pubitemid 40995510)
8. Kleczkowska, H. E.; Marra, G.; Lettieri, T.; Jiricny, J. hMSH3 and hMSH6 interact with PCNA and colocalize with it to replication foci Genes Dev. 2001, 15, 724-736 (Pubitemid 32244901)
9. Lopez de Saro, F. J.; Marinus, M. G.; Modrich, P.; O'Donnell, M. The beta sliding clamp binds to multiple sites within MutL and MutS J. Biol. Chem. 2006, 281, 14340-14349 (Pubitemid 43848363)
10. 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, 11627-11632 (Pubitemid 32928779)
11. Wagner, J.; Fujii, S.; Gruz, P.; Nohmi, T.; Fuchs, R. P. The beta clamp targets DNA polymerase IV to DNA and strongly increases its processivity EMBO Rep. 2000, 1, 484-488
12. 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 (Amst.) 2002, 1, 703-708
13. Lenne-Samuel, N.; Wagner, J.; Etienne, H.; Fuchs, R. P. The processivity factor beta controls DNA polymerase IV traffic during spontaneous mutagenesis and translesion synthesis in vivo EMBO Rep. 2002, 3, 45-49 (Pubitemid 34144814)
14. Heltzel, J. M.; Maul, R. W.; Scouten Ponticelli, S. K.; Sutton, M. D. A model for DNA polymerase switching involving a single cleft and the rim of the sliding clamp Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 12664-12669
15. Jeruzalmi, D.; Yurieva, O.; Zhao, Y.; Young, M.; Stewart, J.; Hingorani, M.; O'Donnell, M.; Kuriyan, J. Mechanism of processivity clamp opening by the delta subunit wrench of the clamp loader complex of E. coli DNA polymerase III Cell 2001, 106, 417-428 (Pubitemid 32786986)
16. 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, 5883-5892 (Pubitemid 37408825)
17. 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, 1187-1197 (Pubitemid 38077239)
18. 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, 11116-11121
19. Wagner, J.; Etienne, H.; Fuchs, R. P.; Cordonnier, A.; Burnouf, D. Distinct beta-clamp interactions govern the activities of the Y family PolIV DNA polymerase Mol. Microbiol. 2009, 74, 1143-1151
20. Auffinger, P.; Hays, F. A.; Westhof, E.; Ho, P. S. Halogen bonds in biological molecules Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 16789-16794 (Pubitemid 39601317)
21. Rinnenthal, J.; Klinkert, B.; Narberhaus, F.; Schwalbe, H. Direct observation of the temperature-induced melting process of the Salmonella fourU RNA thermometer at base-pair resolution Nucleic Acids Res. 2010, 38, 3834-3847
22. Strazewski, P. Thermodynamic correlation analysis: hydration and perturbation sensitivity of RNA secondary structures J. Am. Chem. Soc. 2002, 124, 3546-3554 (Pubitemid 34407877)
23. Ackroyd, P. C.; Cleary, J.; Glick, G. D. Thermodynamic basis for sequence-specific recognition of ssDNA by an autoantibody Biochemistry 2001, 40, 2911-2922 (Pubitemid 32198294)
24. Voth, A. R.; Ho, P. S. The role of halogen bonding in inhibitor recognition and binding by protein kinases Curr. Top. Med. Chem. 2007, 7, 1336-1348 (Pubitemid 47484763)
25. Camacho, C. J.; Kimura, S. R.; DeLisi, C.; Vajda, S. Kinetics of desolvation-mediated protein-protein binding Biophys. J. 2000, 78, 1094-1105 (Pubitemid 30141539)
26. Vijayakumar, S.; Chapados, B. R.; Schmidt, K. H.; Kolodner, R. D.; Tainer, J. A.; Tomkinson, A. E. The C-terminal domain of yeast PCNA is required for physical and functional interactions with Cdc9 DNA ligase Nucleic Acids Res. 2007, 35, 1624-1637 (Pubitemid 46592882)
27. Arkin, M. R.; Randal, M.; DeLano, W. L.; Hyde, J.; Luong, T. N.; Oslob, J. D.; Raphael, D. R.; Taylor, L.; Wang, J.; McDowell, R. S.; Wells, J. A.; Braisted, A. C. Binding of small molecules to an adaptive protein-protein interface Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 1603-1608 (Pubitemid 36254494)
28. Goodman, M.; Felix, A.; Moroder, L.; Toniolo, C. H.-W. Synthesis of Peptides and Peptidomimetics; Thieme: Stuttgart, NY; Vol. E 22a-e.
29. Neimark, J.; Briand, J. P. Development of a fully automated multichannel peptide synthesizer with integrated TFA cleavage capability Pept. Res. 1993, 6, 219-228
30. Kaiser, E.; Colescott, R. L.; Bossinger, C. D.; Cook, P. I. Color test for detection of free terminal amino groups in the solid-phase synthesis of peptides Anal. Biochem. 1970, 34, 595-598
31. Lafont, V.; Schaefer, M.; Stote, R.; Altschuh, D.; Dejaegere, A. Protein-protein recognition and interaction hot spots in an antigen-antibody complex: free energy decomposition identifies "efficient amino acids Proteins: Struct. Funct. Bioinformatics 2007, 67, 418-434 (Pubitemid 46449417)
32. Kollman, P. A.; Massova, I.; Reyes, C.; Kuhn, B.; Huo, S.; Chong, L.; Lee, M.; Lee, T.; Duan, Y.; Wang, W.; Donini, O.; Cieplak, P.; Srinivasan, J.; Case, D. A. Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models Acc. Chem. Res. 2000, 33, 889-897 (Pubitemid 32056774)
33. Gohlke, H.; Kiel, C.; Case, D. A. Insights into protein-protein binding by binding free energy calculation and free energy decomposition for the Ras-Raf and Ras-RalGDS complexes J. Mol. Biol. 2003, 330, 891-913
34. Brooks, B. R.; Bruccoleri, R. E.; Olafson, B. D.; States, D. J.; Swaminathan, S.; M., K. CHARMM: A program for macromolecular energy minimization and dynamics calculations J. Comput. Chem. 1983, 4, 187-217
35. 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. K.; 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, 3586-3616 (Pubitemid 128576688)
36. Hendsch, Z. S.; Tidor, B. Electrostatic interactions in the GCN4 leucine zipper: substantial contributions arise from intramolecular interactions enhanced on binding Protein Sci. 1999, 8, 1381-1392 (Pubitemid 29328218)
37. Gouda, H.; Kuntz, I. D.; Case, D. A.; Kollman, P. A. Free energy calculations for theophylline binding to an RNA aptamer: Comparison of MM-PBSA and thermodynamic integration methods Biopolymers 2003, 68, 16-34 (Pubitemid 36098305)
38. Miranker, A.; Karplus, M. Functionality maps of binding sites: a multiple copy simultaneous search method Proteins 1991, 11, 29-34
39. Majeux, N.; Scarsi, M.; Apostolakis, J.; Ehrhardt, C.; Caflisch, A. Exhaustive docking of molecular fragments with electrostatic solvation Proteins 1999, 37, 88-105 (Pubitemid 29408922)
40. Sirockin, F.; Sich, C.; Improta, S.; Schaefer, M.; Saudek, V.; Froloff, N.; Karplus, M.; Dejaegere, A. Structure activity relationship by NMR and by computer: a comparative study J. Am. Chem. Soc. 2002, 124, 11073-11084 (Pubitemid 35025666)
41. Majeux, N.; Scarsi, M.; Caflisch, A. Efficient electrostatic solvation model for protein-fragment docking Proteins 2001, 42, 256-268 (Pubitemid 32047334)
42. Biertumpfel, C.; Basquin, J.; Suck, D.; Sauter, C. Crystallization of biological macromolecules using agarose gel Acta Crystallogr., Sect. D 2002, 58, 1657-1659 (Pubitemid 35181066)
43. Kabsch, W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants J. Appl. Crystallogr. 1993, 26, 795-800
44. Collaborative Computational Project, N., The CCP4 suite: programs for protein crystallography. Acta Crystallogr., Sect. D Biol. Crystallogr. D50 1994, 760-763.
45. Adams, P. D.; Grosse-Kunstleve, R. W.; Hung, L. W.; Loerger, T. R.; McCoy, A. J. PHENIX: building new software for automated crystallographic structure determination Acta Crystallogr., Sect. D Biol. Crystallogr. D50 2002, 58, 1948-1954 (Pubitemid 35337293)
46. Emsley, P.; Cowtan, K. Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D Biol. Crystallogr. D50 2004, 60, 2126-2132 (Pubitemid 41742764)
47. Brünger, A. T.; Adams, P. D.; Clore, G. M.; Delano, W. L.; Gros, P.; Grosse-Kuntsleve, R. V. Crystallography and NMR system: a new software suite for macromolecular structure determination Acta Crystallogr., Sect. D 1998, 54, 905-921
48. Chen, V. B.; Arendall, W. B. r.; Headd, J. J.; Keedy, D. A.; Immormino, R. M.; Kapral, G. J.; Murray, L. W.; Richardson, J. S. R.; D., C. MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr., Sect. D 2010, 66, 12-21
49. DeLano, W. L. The PyMOL Molecular Graphics System; DeLano Scientific LLC: Palo Alto, CA, USA, 2008.