Fragment-based identification of a locus in the Sec7 domain of arno for the design of protein-protein interaction inhibitors

Journal of Medicinal Chemistry

Volumn 56, Issue 21, 2013, Pages 8497-8511

  Rouhana, Jad ^a,b,c   Hoh, Francois ^c   Estaran, Sébastien ^a   Henriquet, Corinne ^b   Boublik, Yvan ^d   Kerkour, Aziz ^c   Trouillard, Romain ^c   Martinez, Jean ^a   Pugnière, Martine ^b   Padilla, André ^c   Chavanieu, Alain ^a  

^a CNRS   (France)

^b CENTRE VAL D AURELLE   (France)

^c CENTRE DE BIOCHIMIE STRUCTURALE   (France)

^d Centre National de la Recherche Scientifique   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; ARNO GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PROTEIN INHIBITOR; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DRUG DESIGN; FLUORESCENCE ANALYSIS; FRAGMENT BASED DRUG DESIGN; GENE LOCUS; HUMAN; MOLECULAR DOCKING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; SURFACE PLASMON RESONANCE; SURFACE PROPERTY; X RAY CRYSTALLOGRAPHY;

ADP-RIBOSYLATION FACTOR 1; CRYSTALLOGRAPHY, X-RAY; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG DESIGN; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HIGH-THROUGHPUT SCREENING ASSAYS; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PROTEIN BINDING; STRUCTURE-ACTIVITY RELATIONSHIP; SULFONAMIDES;

EID: 84887948387     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm4009357     Document Type: Article

References (84)

1. Rojas, A. M.; Fuentes, G.; Rausell, A.; Valencia, A. The Ras protein superfamily: evolutionary tree and role of conserved amino acids J. Cell. Biol. 2012, 196, 189-201
2. Wennerberg, K.; Rossman, K. L.; Der, C. J. The Ras superfamily at a glance J. Cell Sci. 2005, 118, 843-846
3. Heasman, S. J.; Ridley, A. J. Multiple roles for RhoA during T cell transendothelial migration Small GTPases 2010, 1, 174-179
4. Heasman, S. J.; Ridley, A. J. Mammalian Rho GTPases: new insights into their functions from in vivo studies Nat. Rev. 2008, 9, 690-701
5. Nie, Z.; Hirsch, D. S.; Randazzo, P. A. Arf and its many interactors Curr. Opin. Cell Biol. 2003, 15, 396-404
6. Casanova, J. E. Regulation of Arf activation: the Sec7 family of guanine nucleotide exchange factors Traffic (Copenhagen, Denmark) 2007, 8, 1476-1485
7. Donaldson, J. G.; Jackson, C. L. ARF family G proteins and their regulators: roles in membrane transport, development and disease Nat. Rev. 2011, 12, 362-375
8. Jackson, C. L.; Casanova, J. E. Turning on ARF: the Sec7 family of guanine-nucleotide-exchange factors Trends Cell Biol. 2000, 10, 60-67
9. Moss, J.; Vaughan, M. Cytohesin-1 in 2001 Arch. Biochem. Biophys. 2002, 397, 156-161
10. Kolanus, W. Guanine nucleotide exchange factors of the cytohesin family and their roles in signal transduction Immunol. Rev. 2007, 218, 102-113
11. Robineau, S.; Chabre, M.; Antonny, B. Binding site of brefeldin A at the interface between the small G protein ADP-ribosylation factor 1 (ARF1) and the nucleotide-exchange factor Sec7 domain Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 9913-9918
12. Mossessova, E.; Corpina, R. A.; Goldberg, J. Crystal structure of ARF1 Sec7 complexed with brefeldin A and its implications for the guanine nucleotide exchange mechanism Mol. Cell 2003, 12, 1403-1411
13. Renault, L.; Guibert, B.; Cherfils, J. Structural snapshots of the mechanism and inhibition of a guanine nucleotide exchange factor Nature 2003, 426, 525-530
14. Hafner, M.; Schmitz, A.; Grune, I.; Srivatsan, S. G.; Paul, B.; Kolanus, W.; Quast, T.; Kremmer, E.; Bauer, I.; Famulok, M. Inhibition of cytohesins by secinH3 leads to hepatic insulin resistance Nature 2006, 444, 941-944
15. Viaud, J.; Zeghouf, M.; Barelli, H.; Zeeh, J. C.; Padilla, A.; Guibert, B.; Chardin, P.; Royer, C. A.; Cherfils, J.; Chavanieu, A. Structure-based discovery of an inhibitor of Arf activation by Sec7 domains through targeting of protein-protein complexes Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 10370-10375
16. Pan, H.; Yu, J.; Zhang, L.; Carpenter, A.; Zhu, H.; Li, L.; Ma, D.; Yuan, J. A novel small molecule regulator of guanine nucleotide exchange activity of the ADP-ribosylation factor and golgi membrane trafficking J. Biol. Chem. 2008, 283, 31087-31096
17. Spooner, R. A.; Watson, P.; Smith, D. C.; Boal, F.; Amessou, M.; Johannes, L.; Clarkson, G. J.; Lord, J. M.; Stephens, D. J.; Roberts, L. M. The secretion inhibitor Exo2 perturbs trafficking of Shiga toxin between endosomes and the trans-Golgi network Biochem. J. 2008, 414, 471-484
18. Boal, F.; Guetzoyan, L.; Sessions, R. B.; Zeghouf, M.; Spooner, R. A.; Lord, J. M.; Cherfils, J.; Clarkson, G. J.; Roberts, L. M.; Stephens, D. J. LG186: an inhibitor of GBF1 function that causes Golgi disassembly in human and canine cells Traffic (Copenhagen, Denmark) 2010, 11, 1537-1551
19. Saenz, J. B.; Sun, W. J.; Chang, J. W.; Li, J.; Bursulaya, B.; Gray, N. S.; Haslam, D. B. Golgicide A reveals essential roles for GBF1 in Golgi assembly and function Nat. Chem. Biol. 2009, 5, 157-165
20. Ohashi, Y.; Iijima, H.; Yamaotsu, N.; Yamazaki, K.; Sato, S.; Okamura, M.; Sugimoto, K.; Dan, S.; Hirono, S.; Yamori, T. AMF-26, a novel inhibitor of the Golgi system, targeting ADP-ribosylation factor 1 (Arf1) with potential for cancer therapy J. Biol. Chem. 2012, 287, 3885-3897
21. Stumpfe, D.; Bill, A.; Novak, N.; Loch, G.; Blockus, H.; Geppert, H.; Becker, T.; Schmitz, A.; Hoch, M.; Kolanus, W.; Famulok, M.; Bajorath, J. Targeting multifunctional proteins by virtual screening: structurally diverse cytohesin inhibitors with differentiated biological functions ACS Chem. Biol. 2010, 5, 839-849
22. Bill, A.; Schmitz, A.; Konig, K.; Heukamp, L. C.; Hannam, J. S.; Famulok, M. Anti-proliferative effect of cytohesin inhibition in gefitinib-resistant lung cancer cells PLoS One 2012, 7, e41179
23. Bill, A.; Blockus, H.; Stumpfe, D.; Bajorath, J.; Schmitz, A.; Famulok, M. A homogeneous fluorescence resonance energy transfer system for monitoring the activation of a protein switch in real time J. Am. Chem. Soc. 2011, 133, 8372-8379
24. Wilson, A. J. Inhibition of protein-protein interactions using designed molecules Chem. Soc. Rev. 2009, 38, 3289-3300
25. Bogan, A. A.; Thorn, K. S. Anatomy of hot spots in protein interfaces J. Mol. Biol. 1998, 280, 1-9
26. 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
27. Moreira, I. S.; Fernandes, P. A.; Ramos, M. J. Hot spots-a review of the protein-protein interface determinant amino-acid residues Proteins 2007, 68, 803-812
28. Coyne, A. G.; Scott, D. E.; Abell, C. Drugging challenging targets using fragment-based approaches Curr. Opin. Chem. Biol. 2010, 14, 299-307
29. Scott, D. E.; Coyne, A. G.; Hudson, S. A.; Abell, C. Fragment-based approaches in drug discovery and chemical biology Biochemistry 2012, 51, 4990-5003
30. Goldberg, J. Structural basis for activation of ARF GTPase: mechanisms of guanine nucleotide exchange and GTP-myristoyl switching Cell 1998, 95, 237-248
31. Kortemme, T.; Kim, D. E.; Baker, D. Computational alanine scanning of protein-protein interfaces Sci. STKE 2004, 2004, l2
32. Kortemme, T.; Baker, D. A simple physical model for binding energy hot spots in protein-protein complexes Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 14116-14121
33. Jain, A. N. Surflex: fully automatic flexible molecular docking using a molecular similarity-based search engine J. Med. Chem. 2003, 46, 499-511
34. Verdonk, M. L.; Cole, J. C.; Hartshorn, M. J.; Murray, C. W.; Taylor, R. D. Improved protein-ligand docking using GOLD Proteins 2003, 52, 609-623
35. McGovern, S. L.; Caselli, E.; Grigorieff, N.; Shoichet, B. K. A common mechanism underlying promiscuous inhibitors from virtual and high-throughput screening J. Med. Chem. 2002, 45, 1712-1722
36. McGovern, S. L.; Helfand, B. T.; Feng, B.; Shoichet, B. K. A specific mechanism of nonspecific inhibition J. Med. Chem. 2003, 46, 4265-4272
37. Seidler, J.; McGovern, S. L.; Doman, T. N.; Shoichet, B. K. Identification and prediction of promiscuous aggregating inhibitors among known drugs J. Med. Chem. 2003, 46, 4477-4486
38. Lifeng, C.; Gochin, M. Colloidal aggregate detection by rapid fluorescence measurement of liquid surface curvature changes in multiwell plates J. Biomol. Screening 2007, 12, 966-971
39. Feng, B. Y.; Shoichet, B. K. A detergent-based assay for the detection of promiscuous inhibitors Nat. Protoc. 2006, 1, 550-553
40. Baell, J. B.; Holloway, G. A. New substructure filters for removal of pan assay interference compounds (PAINS) from screening libraries and for their exclusion in bioassays J. Med. Chem. 2010, 53, 2719-2740
41. Rouhana, J.; Padilla, A.; Estaran, S.; Bakari, S.; Delbecq, S.; Boublik, Y.; Chopineau, J.; Pugniere, M.; Chavanieu, A. Kinetics of interaction between ADP-ribosylation factor-1 (Arf1) and the Sec7 domain of Arno guanine nucleotide exchange factor, modulation by allosteric factors, and the uncompetitive inhibitor brefeldin A J. Biol. Chem. 2013, 288, 4659-4672
42. Delbecq, S.; Auguin, D.; Yang, Y. S.; Lohr, F.; Arold, S.; Schetters, T.; Precigout, E.; Gorenflot, A.; Roumestand, C. The solution structure of the adhesion protein Bd37 from Babesia divergens reveals structural homology with eukaryotic proteins involved in membrane trafficking J. Mol. Biol. 2008, 375, 409-424
43. Basse, N.; Kaar, J. L.; Settanni, G.; Joerger, A. C.; Rutherford, T. J.; Fersht, A. R. Toward the rational design of p53-stabilizing drugs: probing the surface of the oncogenic Y220C mutant Chem. Biol. 2010, 17, 46-56
44. Brough, P. A.; Barril, X.; Borgognoni, J.; Chene, P.; Davies, N. G.; Davis, B.; Drysdale, M. J.; Dymock, B.; Eccles, S. A.; Garcia-Echeverria, C.; Fromont, C.; Hayes, A.; Hubbard, R. E.; Jordan, A. M.; Jensen, M. R.; Massey, A.; Merrett, A.; Padfield, A.; Parsons, R.; Radimerski, T.; Raynaud, F. I.; Robertson, A.; Roughley, S. D.; Schoepfer, J.; Simmonite, H.; Sharp, S. Y.; Surgenor, A.; Valenti, M.; Walls, S.; Webb, P.; Wood, M.; Workman, P.; Wright, L. Combining hit identification strategies: fragment-based and in silico approaches to orally active 2-aminothieno[2,3- d ]pyrimidine inhibitors of the Hsp90 molecular chaperone J. Med. Chem. 2009, 52, 4794-4809
45. Geschwindner, S.; Olsson, L. L.; Albert, J. S.; Deinum, J.; Edwards, P. D.; de Beer, T.; Folmer, R. H. Discovery of a novel warhead against beta-secretase through fragment-based lead generation J. Med. Chem. 2007, 50, 5903-5911
46. Klages, J.; Coles, M.; Kessler, H. NMR-based screening: a powerful tool in fragment-based drug discovery Analyst 2007, 132, 693-705
47. Mochalkin, I.; Miller, J. R.; Narasimhan, L.; Thanabal, V.; Erdman, P.; Cox, P. B.; Prasad, J. V.; Lightle, S.; Huband, M. D.; Stover, C. K. Discovery of antibacterial biotin carboxylase inhibitors by virtual screening and fragment-based approaches ACS Chem. Biol. 2009, 4, 473-483
48. Mayer, M.; Meyer, B. Characterization of ligand binding by saturation transfer difference NMR spectroscopy Angew. Chem., Int. Ed. 1999, 38, 1784-1788
49. Kemper, S.; Patel, M. K.; Errey, J. C.; Davis, B. G.; Jones, J. A.; Claridge, T. D. Group epitope mapping considering relaxation of the ligand (GEM-CRL): including longitudinal relaxation rates in the analysis of saturation transfer difference (STD) experiments J. Magn. Reson. 2010, 203, 1-10
50. Renault, L.; Christova, P.; Guibert, B.; Pasqualato, S.; Cherfils, J. Mechanism of domain closure of Sec7 domains and role in BFA sensitivity Biochemistry 2002, 41, 3605-3612
51. Chene, P. Drugs targeting protein-protein interactions ChemMedChem 2006, 1, 400-411
52. Ryan, D. P.; Matthews, J. M. Protein-protein interactions in human disease Curr. Opin. Struct. Biol. 2005, 15, 441-446
53. Arkin, M. R.; Whitty, A. The road less traveled: modulating signal transduction enzymes by inhibiting their protein-protein interactions Curr. Opin. Chem. Biol. 2009, 13, 284-290
54. Bower, J. F.; Pannifer, A. Using fragment-based technologies to target protein-protein interactions Curr. Pharm. Des. 2012, 18, 4685-4696
55. Bamborough, P.; Diallo, H.; Goodacre, J. D.; Gordon, L.; Lewis, A.; Seal, J. T.; Wilson, D. M.; Woodrow, M. D.; Chung, C. W. Fragment-based discovery of bromodomain inhibitors part 2: optimization of phenylisoxazole sulfonamides J. Med. Chem. 2012, 55, 587-596
56. Tsao, D. H. H.; Sutherland, A. G.; Jennings, L. D.; Li, Y. H.; Rush, T. S.; Alvarez, J. C.; Ding, W. D.; Dushin, E. G.; Dushin, R. G.; Haney, S. A.; Kenny, C. H.; Malakian, A. K.; Nilakantan, R.; Mosyak, L. Discovery of novel inhibitors of the ZipA/FtsZ complex by NMR fragment screening coupled with structure-based design Bioorg. Med. Chem. 2006, 14, 7953-7961
57. Valkov, E.; Sharpe, T.; Marsh, M.; Greive, S.; Hyvoenen, M. Targeting Protein-protein interactions and fragment-based drug discovery Top. Curr. Chem. 2012, 317, 145-179
58. Winter, A.; Higueruelo, A. P.; Marsh, M.; Sigurdardottir, A.; Pitt, W. R.; Blundell, T. L. Biophysical and computational fragment-based approaches to targeting protein-protein interactions: applications in structure-guided drug discovery Q. Rev. Biophys. 2012, 45, 383-426
59. Huang, N.; Jacobson, M. P. Binding-site assessment by virtual fragment screening PLoS One 2010, 5, e10109
60. Kumar, A.; Voet, A.; Zhang, K. Y. Fragment based drug design: from experimental to computational approaches Curr. Med. Chem. 2012, 19, 5128-5147
61. Zhang, C.; Lai, L. Towards structure-based protein drug design Biochem. Soc. Trans. 2011, 39, 1382-1386 (Suppl. following p 1386)
62. Evelyn, C. R.; Ferng, T.; Rojas, R. J.; Larsen, M. J.; Sondek, J.; Neubig, R. R. High-throughput screening for small-molecule inhibitors of LARG-stimulated RhoA nucleotide binding via a novel fluorescence polarization assay J. Biomol. Screening 2009, 14, 161-172
63. Coan, K. E.; Maltby, D. A.; Burlingame, A. L.; Shoichet, B. K. Promiscuous aggregate-based inhibitors promote enzyme unfolding J. Med. Chem. 2009, 52, 2067-2075
64. Coan, K. E.; Shoichet, B. K. Stoichiometry and physical chemistry of promiscuous aggregate-based inhibitors J. Am. Chem. Soc. 2008, 130, 9606-9612
65. Wilson, C. G. M.; Arkin, M. R. Small-molecule inhibitors of IL-2/IL-2R: lessons learned and applied Curr. Top. Microbiol. 2011, 348, 25-59
66. DiNitto, J. P.; Delprato, A.; Gabe Lee, M. T.; Cronin, T. C.; Huang, S.; Guilherme, A.; Czech, M. P.; Lambright, D. G. Structural basis and mechanism of autoregulation in 3-phosphoinositide-dependent Grp1 family Arf GTPase exchange factors Mol. Cell 2007, 28, 569-583
67. Lazer, G.; Katzav, S. Guanine nucleotide exchange factors for RhoGTPases: good therapeutic targets for cancer therapy? Cell. Signalling 2011, 23, 969-979
68. Boulay, P. L.; Schlienger, S.; Lewis-Saravalli, S.; Vitale, N.; Ferbeyre, G.; Claing, A. ARF1 controls proliferation of breast cancer cells by regulating the retinoblastoma protein Oncogene 2011, 30, 3846-3861
69. Abad-Zapatero, C.; Metz, J. T. Ligand efficiency indices as guideposts for drug discovery Drug Discovery Today 2005, 10, 464-469
70. Abad-Zapatero, C.; Perisic, O.; Wass, J.; Bento, A. P.; Overington, J.; Al-Lazikani, B.; Johnson, M. E. Ligand efficiency indices for an effective mapping of chemico-biological space: the concept of an atlas-like representation Drug Discovery Today 2010, 15, 804-811
71. Abad-Zapatero, C. Ligand efficiency indices for effective drug discovery Expert Opin. Drug Discovery 2007, 2, 469-488
72. Morelli, X.; Bourgeas, R.; Roche, P. Chemical and structural lessons from recent successes in protein-protein interaction inhibition (2P2I) Curr. Opin. Chem. Biol. 2011, 15, 475-481
73. Smith, P. A.; Tripp, B. C.; DiBlasio-Smith, E. A.; Lu, Z.; LaVallie, E. R.; McCoy, J. M. A plasmid expression system for quantitative in vivo biotinylation of thioredoxin fusion proteins in Escherichia coli Nucleic Acids Res. 1998, 26, 1414-1420
74. O'Callaghan C, A.; Byford, M. F.; Wyer, J. R.; Willcox, B. E.; Jakobsen, B. K.; McMichael, A. J.; Bell, J. I. BirA enzyme: production and application in the study of membrane receptor-ligand interactions by site-specific biotinylation Anal. Biochem. 1999, 266, 9-15
75. Kumano-Kuramochi, M.; Xie, Q.; Sakakibara, Y.; Niimi, S.; Sekizawa, K.; Komba, S.; Machida, S. Expression and characterization of recombinant C-terminal biotinylated extracellular domain of human receptor for advanced glycation end products (hsRAGE) in Escherichia coli J. Biochem. 2008, 143, 229-236
76. Zeeh, J. C.; Zeghouf, M.; Grauffel, C.; Guibert, B.; Martin, E.; Dejaegere, A.; Cherfils, J. Dual specificity of the interfacial inhibitor brefeldin a for arf proteins and sec7 domains J. Biol. Chem. 2006, 281, 11805-11814
77. Jain, A. N. Surflex-Dock 2.1: robust performance from ligand energetic modeling, ring flexibility, and knowledge-based search J. Comput.-Aided Mol. Des. 2007, 21, 281-306
78. Stalder, D.; Barelli, H.; Gautier, R.; Macia, E.; Jackson, C. L.; Antonny, B. Kinetic studies of the Arf activator Arno on model membranes in the presence of Arf effectors suggest control by a positive feedback loop J. Biol. Chem. 2011, 286, 3873-3883
79. Cherfils, J.; Menetrey, J.; Mathieu, M.; Le Bras, G.; Robineau, S.; Beraud-Dufour, S.; Antonny, B.; Chardin, P. Structure of the Sec7 domain of the Arf exchange factor ARNO Nature 1998, 392, 101-105
80. Battye, T. G.; Kontogiannis, L.; Johnson, O.; Powell, H. R.; Leslie, A. G. iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM Acta Crystallogr., Sect. D: Biol. Crystallogr. 2011, 67, 271-281
81. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 1994, 50, 760-763
82. Langer, G.; Cohen, S. X.; Lamzin, V. S.; Perrakis, A. Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7 Nat. Protoc. 2008, 3, 1171-1179
83. Emsley, P.; Lohkamp, B.; Scott, W. G.; Cowtan, K. Features and development of Coot Acta Crystallogr., Sect. D: Biol. Crystallogr. 2010, 66, 486-501
84. Laskowski, R. A.; Macarthur, M. W.; Moss, D. S.; Thornton, J. M. Procheck-a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 1993, 26, 283-291