Launching spiking ligands into a protein-protein interface: A promising strategy to destabilize and break interface formation in a tRNA modifying enzyme

ACS Chemical Biology

Volumn 8, Issue 6, 2013, Pages 1163-1178

  Immekus, Florian ^a   Barandun, Luzi Jakob ^b   Betz, Michael ^a   Debaene, François ^c   Petiot, Stéphanie ^c   Sanglier Cianferani, Sarah ^c   Reuter, Klaus ^a   Diederich, François ^b   Klebe, Gerhard ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b ETH ZURICH   (Switzerland)

^c Lab Spectrom Masse Bio Organique   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC AMINO ACID; TRANSFER RNA;

ARTICLE; CRYSTALLOGRAPHY; ENZYME INHIBITION; ENZYME MODIFICATION; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE;

CRYSTALLOGRAPHY, X-RAY; DRUG DISCOVERY; DYSENTERY, BACILLARY; HUMANS; MODELS, MOLECULAR; PENTOSYLTRANSFERASES; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; RNA, TRANSFER; SHIGELLA; SMALL MOLECULE LIBRARIES; ZYMOMONAS;

EID: 84879755649     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb400020b     Document Type: Article

References (52)

1. Robert Koch Institut (2011) Epidemiol. Bull. 24, 215-217
2. Kotloff, K. L., Winickoff, J. P., Ivanoff, B., Clemens, J. D., Swerdlow, D. L., Sansonetti, P. J., Adak, G. K., and Levine, M. M. (1999) Global burden of Shigella infections: implications for vaccine development and implementation of control strategies Bull. World Health Organ. 651-666
3. Durand, J. M. B., Dagberg, B., Uhlin, B. E., and Björk, G. R. (2000) Transfer RNA modification, temperature and DNA superhelicity have a common target in the regulatory network of the virulence of Shigella flexneri: the expression of the virF gene Mol. Microbiol. 35, 924-935
4. Grädler, U., Gerber, H.-D., Goodenough-Lashua, D. M., Garcia, G. A., Ficner, R., Reuter, K., Stubbs, M. T., and Klebe, G. (2001) A new target for shigellosis: Rational design and crystallographic studies of inhibitors of tRNA-guanine transglycosylase J. Mol. Biol. 306, 455-467
5. Durand, J. M., Okada, N., Tobe, T., Watarai, M., Fukuda, I., Suzuki, T., Nakata, N., Komatsu, K., Yoshikawa, M., and Sasakawa, C. (1994) vacC, a virulence-associated chromosomal locus of Shigella flexneri, is homologous to tgt, a gene encoding tRNA-guanine transglycosylase (Tgt) of Escherichia coli K-12 J. Bacteriol. 176, 4627-4634
6. 6- isopentenyladenosine in tRNA of Shigella flexneri is required for expression of virulence genes J. Bacteriol. 179, 5777-5782
7. Brenk, R., Stubbs, M. T., Heine, A., Reuter, K., and Klebe, G. (2003) Flexible adaptations in the structure of the tRNA-modifying enzyme tRNA-guanine transglycosylase and their implications for substrate selectivity, reaction mechanism and structure-based drug design ChemBioChem 4, 1066-1077
8. Ritschel, T., Atmanene, C., Reuter, K., Van Dorsselaer, A., Sanglier-Cianferani, S., and Klebe, G. (2009) An integrative approach combining noncovalent mass spectrometry, enzyme kinetics and X-ray crystallography to decipher Tgt protein-protein and protein-RNA interaction J. Mol. Biol. 393, 833-847
9. Stengl, B., Meyer, E. A., Heine, A., Brenk, R., Diederich, F., and Klebe, G. (2007) Crystal structures of tRNA-guanine transglycosylase (TGT) in complex with novel and potent inhibitors unravel pronounced induced-fit adaptations and suggest dimer formation upon substrate binding J. Mol. Biol. 370, 492-511
10. Xie, W., Liu, X., and Huang, R. H. (2003) Chemical trapping and crystal structure of a catalytic tRNA guanine transglycosylase covalent intermediate Nat. Struct. Biol. 10, 781-788
11. Ritschel, T., Kohler, P. C., Neudert, G., Heine, A., Diederich, F., and Klebe, G. (2009) How to replace the residual solvation shell of polar active site residues to achieve nanomolar inhibition of tRNA-guanine transglycosylase ChemMedChem 4, 2012-2023
12. Fletcher, S. and Hamilton, A. D. (2006) Targeting protein-protein interactions by rational design: mimicry of protein surfaces J. R. Soc. Interface 3, 215-233
13. Chea, Y., Brooksa, B. R., and Marshall, G. R. (2006) Development of small molecules designed to modulate protein-protein interactions J. Comput.-Aided Mol. Design 20, 109-130
14. Morelli, X., Bourgeas, R., and Roche, P. (2011) Chemical and structural lessons from recent successes in protein-protein interaction inhibition (2P2I) Curr. Opin. Chem. Biol. 15, 475-481
15. Arkin, M. R. and Wells, J. A. (2004) Small molecule inhibitors of protein-protein interactions: progressing towards the dream Nat. Rev. Drug Discovery 3, 301-317
16. Sillerud, L. O. and Larson, R. S. (2005) Design and structure of peptide and peptidemimetic antagonists of protein-protein interaction Curr. Prot. Pept. Sci. 6, 151-169
17. Kohler, P. C., Ritschel, T., Schweizer, W. B., Klebe, G., and Diederich, F. (2009) High-affinity inhibitors of tRNA-guanine transglycosylase replacing the function of a structural water cluster Chem.-Eur. J. 15, 10809-10817
18. Hörtner, S. R., Ritschel, T., Stengl, B., Kramer, C., Schweizer, W. B., Wagner, B., Kansy, M., Klebe, G., and Diederich, F. (2007) Potent inhibitors of tRNA-guanine transglycosylase, an enzyme linked to the pathogenicity of the Shigella bacterium: Charge-assisted hydrogen bonding Angew. Chem., Int. Ed. 46, 8266-8269
19. Angew. Chem. 119, 8414-8417.
20. Fotsop, D. F., Roussi, F., Leverrier, A., Bretéché, A., and Guéritte, F. (2010) Biomimetic total synthesis of meiogynin A, an Inhibitor of Bcl-xL and Bak Interaction J. Org. Chem. 75, 7412-7415
21. Wright, J. A., Gaunt, M. J., and Spencer, J. B. (2006) Novel anti-Markovnikov regioselectivity in the Wacker reaction of styrenes Chem.-Eur. J. 12, 949-955
22. 19F NMR spectroscopy. Part 2. Extension to fluoromethyl, difluoromethyl, pentafluoroethyl, trifluoromethylthio and trifluoromethoxy groups New J. Chem. 30, 447-457
23. DiLabio, G. A., Ingold, K. U., Roydhouse, M. D., and Walton, J. C. (2004) Axial and equatorial cyclohexylacyl and tetrahydropyranyl-2-acyl radicals. An experimental and theoretical study Org. Lett. 6, 4319-4322
24. Wienken, C. J., Baaske, P., Rothbauer, U., Braun, D., and Duhr, S. (2010) Protein-binding assays in biological liquids using microscale thermophoresis Nat. Commun. 10.1038/ncomms1093
25. a shifts of ligands as driving force for high-affinity binding to TGT ChemBioChem 10, 716-727
26. Barandun, L. J., Immekus, F., Kohler, P. C., Tonazzi, S., Wagner, B., Wendelspiess, S., Ritschel, T., Heine, A., Kansy, M., Klebe, G., and Diederich, F. (2012) From lin -benzoguanines to lin -benzohypoxanthines as ligands for Zymomonas mobilis tRNA-guanine transglycosylase: Replacement of protein-ligand hydrogen bonding by importing water clusters Chem.-Eur. J. 18, 9246-9257
27. Fiser, A. and Šali, A. (2003) ModLoop: automated modeling of loops in protein structures Bioinformatics 19, 2500-2501
28. Fiser, A., Do, R. K. G., and Šali, A. (2000) Modeling of loops in protein structures Protein Sci. 9, 1753-1773
29. Allen, F. H. (2002) The Cambridge Structural Database: a quarter of a million crystal structures and rising Acta Crystallogr. B58, 380-388
30. McMillan, K., Adler, M., Auld, D. S., Baldwin, J. J., Blasko, E., Browne, L. J., Chelsky, D., Davey, D., Dolle, R. E., Eagen, K. A., Erickson, S., Feldman, R. I., Glaser, C. B., Mallari, C., Morrissey, M. M., Ohlmeyer, M. H. J., Pan, G., Parkinson, J. F., Phillips, G. B., Polokoff, M. A., Sigal, N. H., Vergona, R., Whitlow, M., Young, T. A., and Devlin, J. J. (2000) Allosteric inhibitors of inducible nitric oxide synthase dimerization discovered via combinatorial chemistry Proc. Nat. Acad. Sci. U.S.A. 97, 1506-1511
31. Landschulz, W. H., Johnson, P. F., and McKnight, S. L. (1988) The Leucine Zipper: A hypothetical structure common to a new class of DNA binding proteins Science 240, 1759-1764
32. Wada, A. (1976) The alpha-helix as an electric macro-dipole Adv Biophys 9, 1-63
33. Hol, W. G. J. (1985) The role of the α-helix dipole in protein function and structure Prog. Biophys. Mol. Biol. 45, 149-195
34. a values in proteins Proteins 48, 388-403
35. a values at the N-termini of α-helices Proteins 63, 621-635
36. Chacko, S., Silverton, E., Kam-Morgan, L., Smith-Gill, S., Cohen, G., and Davies, D. (1995) Structure of an antibody-lysozyme complex unexpected Effect of a conservative mutation J. Mol. Biol. 245, 261-274
37. Kussie, P. H., Gorina, S., Marechal, V., Elenbaas, B., Moreau, J., Levine, A. J., and Pavletich, N. P. (1996) Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain Science 274, 948-953
38. Clackson, T. and Wells, J. A. (1995) A hot spot of binding energy in a hormone-receptor interface Science 267, 383-386
39. Bogan, A. A. and Thorn, K. S. (1998) Anatomy of hot spots in protein interfaces J. Mol. Biol. 280, 1-9
40. Moreira, I. S., Fernandes, P. A., and Ramos, M. J. (2007) Hot spots-A review of the protein-protein interface determinant amino-acid residues Proteins 68, 803-812
41. Reuter, K. and Ficner, R. (1995) Sequence analysis and overexpression of the Zymomonas mobilis tgt gene encoding tRNA-guanine transglycosylase: Purification and biochemical characterization of the enzyme J. Bacteriol. 177, 5284-5288
42. Romier, C., Ficner, R., Reuter, K., and Suck, D. (1996) Purification, crystallization, and preliminary X-ray diffraction studies of tRNA-guanine transglycosylase from Zymomonas mobilis Proteins: Structure, Function Genet. 24, 516-519
43. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J.-S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr. D54, 905-921
44. Sheldrick, G. M. and Schneider, T. R. (1997) SHELXL: high-resolution refinement Methods Enzymol. 277, 319-343
45. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132
46. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26 (2) 283-291
47. Meyer, E. A., Donati, N., Guillot, M., Schweizer, W. B., Diederich, F., Stengl, B., Brenk, R., Reuter, K., and Klebe, G. (2006) Synthesis, biological evaluation, and crystallographic studies of extended guanine-based (lin -benzoguanine) inhibitors for tRNA-guanine transglycosylase (TGT) Helv. Chim. Acta 89, 573-597
48. Neudert, G. and Klebe, G. (2011) fconv: format conversion, manipulation and feature computation of molecular data Bioinformatics 27, 1021-1022
49. Case, D. A., Darden, T. A., Cheatham, T. E., Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Walker, R. C., Zhang, W., Merz, K. M., Roberts, B., Hayik, S., Roitberg, A., Seabra, G., Swails, J., Goetz, A. W., Kolossvai, I., Wong, K. F., Paesani, F., Vanicek, J., Wolf, R. M., Liu, J., Wu, X., Brozell, S. R., Steinbrecher, T., Gohlke, H., Cai, Q., Ye, X., Wang, J., Hsieh, M.-J., Cui, G., Roe, D. R., Mathews, D. H., Seetin, M. G., Salomon-Ferrer, R., Sagui, C., Babin, V., Luchko, T., Gusarov, S., Kovalenko, A., and Kollman, P. A. (2012) AMBER 12, University of California, San Francisco
50. Bruno, I. J., Cole, J. C., Edgington, P. R., Kessler, M., Macrae, C. F., McCabe, P., Pearson, J., and Taylor, R. (2002) New software for searching the Cambridge Structural Database and visualizing crystal structures Acta Crystallogr. B58, 389-397
51. Macrae, C. F., Bruno, I. J., Chisholm, J. A., Edgington, P. R., McCabe, P., Pidcock, E., Rodriguez-Monge, L., Taylor, R., van de Streek, J., and Wood, P. A. (2008) Mercury CSD 2.0-new features for the visualization and investigation of crystal structures J. Appl. Crystallogr. 41, 466-470
52. Eisenberg, D., Schwarz, E., Komarony, M., and Wall, R. (1984) Analysis of membrane and surface protein sequences with the hydrophobic moment plot J. Mol. Biol. 179, 125-142