Identification of sumoylation activating enzyme 1 inhibitors by structure-based virtual screening

Journal of Chemical Information and Modeling

Volumn 53, Issue 4, 2013, Pages 809-820

  Kumar, Ashutosh ^a   Ito, Akihiro ^a   Hirohama, Mikako ^a   Yoshida, Minoru ^a   Zhang, Kam Y J ^a  

^a RIKEN   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CHEMICAL ACTIVATION; DIAGNOSIS; ENZYMES; FREE ENERGY; LIGANDS; METABOLISM; MOLECULAR DYNAMICS; MOLECULES; UREA;

BINDING FREE ENERGY; MOLECULAR DYNAMICS SIMULATIONS; PROTEIN FLEXIBILITY; SIMILARITY SEARCH; SMALL MOLECULE INHIBITOR; SMALL-MOLECULE LIBRARY; THERAPEUTIC AGENTS; THERAPEUTIC TARGETS;

DIGITAL LIBRARIES;

CARBANILAMIDE DERIVATIVE; ENZYME INHIBITOR; LIGAND; UBIQUITIN PROTEIN LIGASE;

ALGORITHM; ARTICLE; CHEMISTRY; COMPUTER INTERFACE; DRUG ANTAGONISM; ENZYME ASSAY; HIGH THROUGHPUT SCREENING; HUMAN; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MOLECULAR LIBRARY; QUANTITATIVE STRUCTURE ACTIVITY RELATION; SUMOYLATION;

ALGORITHMS; ENZYME ASSAYS; ENZYME INHIBITORS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; LIGANDS; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; PHENYLUREA COMPOUNDS; QUANTITATIVE STRUCTURE-ACTIVITY RELATIONSHIP; SMALL MOLECULE LIBRARIES; SUMOYLATION; UBIQUITIN-ACTIVATING ENZYMES; USER-COMPUTER INTERFACE;

EID: 84876531626     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci300618e     Document Type: Article

References (70)

1. Baba, D.; Maita, N.; Jee, J. G.; Uchimura, Y.; Saitoh, H.; Sugasawa, K.; Hanaoka, F.; Tochio, H.; Hiroaki, H.; Shirakawa, M. Crystal structure of thymine DNA glycosylase conjugated to SUMO-1 Nature 2005, 435 (7044) 979-982
2. Geiss-Friedlander, R.; Melchior, F. Concepts in sumoylation: A decade on Nat. Rev. Mol. Cell Biol. 2007, 8 (12) 947-956
3. Johnson, E. S. Protein modification by SUMO Annu. Rev. Biochem. 2004, 73, 355-382
4. Palancade, B.; Doye, V. Sumoylating and desumoylating enzymes at nuclear pores: underpinning their unexpected duties? Trends Cell Biol. 2008, 18 (4) 174-183
5. Yeh, E. T. H. SUMOylation and De-SUMOylation: Wrestling with life's processes J. Biol. Chem. 2009, 284 (13) 8223-8227
6. Zhao, J. Sumoylation regulates diverse biological processes Cell. Mol. Life Sci. 2007, 64 (23) 3017-3033
7. Mukhopadhyay, D.; Dasso, M. Modification in reverse: the SUMO proteases Trends Biochem. Sci. 2007, 32 (6) 286-295
8. Hay, R. T. SUMO-specific proteases: A twist in the tail Trends Cell Biol. 2007, 17 (8) 370-376
9. Drag, M.; Salvesen, G. S. DeSUMOylating enzymes -SENPs IUBMB Life 2008, 60 (11) 734-742
10. Zuo, Y.; Cheng, J.-K. Small ubiquitin-like modifier protein-specific protease 1 and prostate cancer Asian J. Androl. 2009, 11 (1) 36-38
11. Lois, L. M.; Lima, C. D. Structures of the SUMO E1 provide mechanistic insights into SUMO activation and E2 recruitment to E1 EMBO J. 2005, 24 (3) 439-451
12. Olsen, S. K.; Capili, A. D.; Lu, X.; Tan, D. S.; Lima, C. D. Active site remodelling accompanies thioester bond formation in the SUMO E1 Nature 2010, 463 (7283) 906-912
13. Lu, X.; Olsen, S. K.; Capili, A. D.; Cisar, J. S.; Lima, C. D.; Tan, D. S. Designed semisynthetic protein inhibitors of Ub/Ubl E1 activating enzymes J. Am. Chem. Soc. 2010, 132 (6) 1748-1749
14. Capili, A. D.; Lima, C. D. Taking it step by step: mechanistic insights from structural studies of ubiquitin/ubiquitin-like protein modification pathways Curr. Opin. Struct. Biol. 2007, 17 (6) 726-735
15. Sarge, K. D.; Park-Sarge, O.-K. Sumoylation and human disease pathogenesis Trends Biochem. Sci. 2009, 34 (4) 200-205
16. Sarge, K. D.; Park-Sarge, O.-K.; Kwang, W. J. SUMO and Its Role in Human Diseases. In International Review of Cell and Molecular Biology; Academic Press: 2011; Vol. 288, Chapter 4, pp 167-183.
17. Pandolfi, P.; Vogt, P.; Seeler, J. S.; Bischof, O.; Nacerddine, K.; Dejean, A. SUMO, the Three Rs and Cancer. In Acute Promyelocytic Leukemia; Springer: Berlin, Heidelberg: 2007; Vol. 313, pp 49-71.
18. Lee, J.-S.; Thorgeirsson, S. S. Genome-scale profiling of gene expression in hepatocellular carcinoma: Classification, survival prediction, and identification of therapeutic targets Gastroenterology 2004, 127 (5, Supplement 1) S51-S55
19. McDoniels-Silvers, A. L.; Nimri, C. F.; Stoner, G. D.; Lubet, R. A.; You, M. Differential gene expression in human lung adenocarcinomas and squamous cell carcinomas Clin. Cancer Res. 2002, 8 (4) 1127-1138
20. Mo, Y.-Y.; Yu, Y.; Theodosiou, E.; Rachel, Ee, P. L.; Beck, W. T. A role for Ubc9 in tumorigenesis Oncogene 2005, 24 (16) 2677-2683
21. Wang, L.; Banerjee, S. Differential PIAS3 expression in human malignancy Oncol. Rep. 2004, 11 (6) 1319-1324
22. Cheng, J.; Bawa, T.; Lee, P.; Gong, L.; Yeh, E. T. Role of desumoylation in the development of prostate cancer Neoplasia 2006, 8 (8) 667-676
23. Bawa-Khalfe, T.; Cheng, J.; Lin, S. H.; Ittmann, M. M.; Yeh, E. T. SENP1 induces prostatic intraepithelial neoplasia through multiple mechanisms J. Biol. Chem. 2010, 285 (33) 25859-25866
24. Xu, Y.; Li, J.; Zuo, Y.; Deng, J.; Wang, L. S.; Chen, G. Q. SUMO-specific protease 1 regulates the in vitro and in vivo growth of colon cancer cells with the upregulated expression of CDK inhibitors Cancer Lett. 2011, 309 (1) 78-84
25. Truong, K.; Lee, T.; Chen, Y. SUMO modification of the E1 Cys domain inhibits its enzymatic activity J. Biol. Chem. 2012, 287 (19) 15154-15163
26. Kessler, J. D.; Kahle, K. T.; Sun, T.; Meerbrey, K. L.; Schlabach, M. R.; Schmitt, E. M.; Skinner, S. O.; Xu, Q.; Li, M. Z.; Hartman, Z. C.; Rao, M.; Yu, P.; Dominguez-Vidana, R.; Liang, A. C.; Solimini, N. L.; Bernardi, R. J.; Yu, B.; Hsu, T.; Golding, I.; Luo, J.; Osborne, C. K.; Creighton, C. J.; Hilsenbeck, S. G.; Schiff, R.; Shaw, C. A.; Elledge, S. J.; Westbrook, T. F. A SUMOylation-dependent transcriptional subprogram is required for Myc-driven tumorigenesis Science 2012, 335 (6066) 348-353
27. Soucy, T. A.; Smith, P. G.; Milhollen, M. A.; Berger, A. J.; Gavin, J. M.; Adhikari, S.; Brownell, J. E.; Burke, K. E.; Cardin, D. P.; Critchley, S.; Cullis, C. A.; Doucette, A.; Garnsey, J. J.; Gaulin, J. L.; Gershman, R. E.; Lublinsky, A. R.; McDonald, A.; Mizutani, H.; Narayanan, U.; Olhava, E. J.; Peluso, S.; Rezaei, M.; Sintchak, M. D.; Talreja, T.; Thomas, M. P.; Traore, T.; Vyskocil, S.; Weatherhead, G. S.; Yu, J.; Zhang, J.; Dick, L. R.; Claiborne, C. F.; Rolfe, M.; Bolen, J. B.; Langston, S. P. An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer Nature 2009, 458 (7239) 732-736
28. Fukuda, I.; Ito, A.; Hirai, G.; Nishimura, S.; Kawasaki, H.; Saitoh, H.; Kimura, K.; Sodeoka, M.; Yoshida, M. Ginkgolic acid inhibits protein SUMOylation by blocking formation of the E1-SUMO intermediate Chem. Biol. 2009, 16 (2) 133-140
29. Fukuda, I.; Ito, A.; Uramoto, M.; Saitoh, H.; Kawasaki, H.; Osada, H.; Yoshida, M. Kerriamycin B inhibits protein SUMOylation J. Antibiot. (Tokyo) 2009, 62 (4) 221-224
30. OMEGA, version 2.4.3; OpenEye Scientific Software, Inc.: Santa Fe, NM, 2012. www.eyesopen.com (accessed April 5, 2013).
31. Berman, H. M.; Westbrook, J.; Feng, Z.; Gilliland, G.; Bhat, T. N.; Weissig, H.; Shindyalov, I. N.; Bourne, P. E. The Protein Data Bank Nucleic Acids Res. 2000, 28 (1) 235-242
32. Molecular Operating Environment (MOE), version 2011.10; Chemical Computing Group, Inc.: Montreal, Quebec, Canada, 2011.
33. Trott, O.; Olson, A. J. AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading J. Comput. Chem. 2010, 31 (2) 455-461
34. Morris, G. M.; Huey, R.; Lindstrom, W.; Sanner, M. F.; Belew, R. K.; Goodsell, D. S.; Olson, A. J. AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility J. Comput. Chem. 2009, 30 (16) 2785-2791
35. Leaver-Fay, A.; Tyka, M.; Lewis, S. M.; Lange, O. F.; Thompson, J.; Jacak, R.; Kaufman, K. W.; Renfrew, P. D.; Smith, C. A.; Sheffler, W.; Davis, I. W.; Cooper, S.; Treuille, A.; Mandell, D. J.; Richter, F.; Ban, Y.-E. A.; Fleishman, S. J.; Corn, J. E.; Kim, D. E.; Lyskov, S.; Berrondo, M.; Mentzer, S.; PopoviÄ, Z.; Havranek, J. J.; Karanicolas, J.; Das, R.; Meiler, J.; Kortemme, T.; Gray, J. J.; Kuhlman, B.; Baker, D.; Bradley, P.; Michael, L. J.; Ludwig, B. Rosetta3: An object-oriented software suite for the simulation and design of macromolecules. In Methods in Enzymology, Academic Press: San Diego, 2011; Vol. 487, Chapter 19, pp 545-574.
36. Jakalian, A.; Bush, B. L.; Jack, D. B.; Bayly, C. I. Fast, efficient generation of high-quality atomic charges. AM1-BCC model: I. Method J. Comput. Chem. 2000, 21 (2) 132-146
37. Davis, I. W.; Baker, D. RosettaLigand docking with full ligand and receptor flexibility J. Mol. Biol. 2009, 385 (2) 381-392
38. Davis, I. W.; Raha, K.; Head, M. S.; Baker, D. Blind docking of pharmaceutically relevant compounds using RosettaLigand Protein Sci. 2009, 18 (9) 1998-2002
39. Meiler, J.; Baker, D. ROSETTALIGAND: Protein-small molecule docking with full side-chain flexibility Proteins 2006, 65 (3) 538-548
40. Srinivasan, J.; Cheatham, T. E.; Cieplak, P.; Kollman, P. A.; Case, D. A. Continuum solvent studies of the stability of DNA, RNA, and phosphoramidate-DNA helices J. Am. Chem. Soc. 1998, 120 (37) 9401-9409
41. 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.; Cheatham, T. E., 3rd Calculating structures and free energies of complex molecules: Combining molecular mechanics and continuum models Acc. Chem. Res. 2000, 33 (12) 889-897
42. Bashford, D.; Case, D. A. Generalized born models of macromolecular solvation effects Annu. Rev. Phys. Chem. 2000, 51, 129-152
43. Tsui, V.; Case, D. A. Theory and applications of the generalized born solvation model in macromolecular simulations Biopolymers 2000, 56 (4) 275-291
44. Simonson, T. Macromolecular electrostatics: Continuum models and their growing pains Curr. Opin. Struct. Biol. 2001, 11 (2) 243-252
45. Case, D. A. D.; T., A.; Cheatham, I., T.E.; Simmerling, C. L.; Wang, J.; Duke, R. E.; Luo, R.; Crowley, M.; Walker, R. C.; Zhang, W.; Merz, K. M.; Wang, B.; Hayik, S.; Roitberg, A.; Seabra, G.; Kolossvry, I.; Wong, K. F.; Paesani, J.; Vanicek, F.; Wu, X.; Brozell, S. R.; Steinbrecher, T.; Gohlke, H.; Yang, L.; Tan, C.; Mongan, J.; Hornak, V.; Cui, G.; Mathews, D. H.; Seetin, M. G.; Sagui, C.; Babin, V.; Kollman, P. A. AMBER, version 10; University of California: San Francisco, CA: 2008.
46. Hou, T.; Wang, J.; Li, Y.; Wang, W. Assessing the performance of the MM/PBSA and MM/GBSA methods. 1. The accuracy of binding free energy calculations based on molecular dynamics simulations J. Chem. Inf. Model. 2011, 51 (1) 69-82
47. Hou, T.; Wang, J.; Li, Y.; Wang, W. Assessing the performance of the molecular mechanics/Poisson Boltzmann surface area and molecular mechanics/generalized Born surface area methods. II. The accuracy of ranking poses generated from docking J. Comput. Chem. 2011, 32 (5) 866-877
48. Yang, T.; Wu, J. C.; Yan, C.; Wang, Y.; Luo, R.; Gonzales, M. B.; Dalby, K. N.; Ren, P. Virtual screening using molecular simulations Proteins 2011, 79 (6) 1940-1951
49. Gao, C.; Herold, J. M.; Kireev, D. Assessment of free energy predictors for ligand binding to a methyllysine histone code reader J. Comput. Chem. 2012, 33 (6) 659-665
50. Rastelli, G.; Rio, A. D.; Degliesposti, G.; Sgobba, M. Fast and accurate predictions of binding free energies using MM-PBSA and MM-GBSA J. Comput. Chem. 2009, 31 (4) 797-810
51. Darden, T.; York, D.; Pedersen, L. Particle mesh Ewald: An N·log(N) method for Ewald sums in large systems J. Chem. Phys. 1993, 98 (12) 10089-10092
52. Ryckaert, J.-P.; Ciccotti, G.; Berendsen, H. J. C. Numerical integration of the cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes J. Comput. Phys. 1977, 23 (3) 327-341
53. Onufriev, A.; Bashford, D.; Case, D. A. Exploring protein native states and large-scale conformational changes with a modified generalized born model Proteins: Struct., Funct., Bioinf. 2004, 55 (2) 383-394
54. Weiser, J.; Shenkin, P. S.; Still, W. C. Approximate atomic surfaces from linear combinations of pairwise overlaps (LCPO) J. Comput. Chem. 1999, 20 (2) 217-230
55. Oehme, D. P.; Brownlee, R. T.; Wilson, D. J. Effect of atomic charge, solvation, entropy, and ligand protonation state on MM-PB(GB)SA binding energies of HIV protease J. Comput. Chem. 2012, 33 (32) 2566-2580
56. Wichapong, K.; Lawson, M.; Pianwanit, S.; Kokpol, S.; Sippl, W. Postprocessing of protein-ligand docking poses using linear response MM-PB/SA: application to Wee1 kinase inhibitors J. Chem. Inf. Model. 2010, 50 (9) 1574-1588
57. Brown, S. P.; Muchmore, S. W. Rapid estimation of relative protein-ligand binding affinities using a high-throughput version of MM-PBSA J. Chem. Inf. Model. 2007, 47 (4) 1493-1503
58. Anisimov, V. M.; Ziemys, A.; Kizhake, S.; Yuan, Z.; Natarajan, A.; Cavasotto, C. N. Computational and experimental studies of the interaction between phospho-peptides and the C-terminal domain of BRCA1 J. Comput. Aided Mol. Des. 2011, 25 (11) 1071-1084
59. Srivastava, H. K.; Sastry, G. N. Molecular dynamics investigation on a series of HIV protease inhibitors: Assessing the performance of MM-PBSA and MM-GBSA approaches J. Chem. Inf. Model. 2012, 52 (11) 3088-3098
60. Okimoto, N.; Futatsugi, N.; Fuji, H.; Suenaga, A.; Morimoto, G.; Yanai, R.; Ohno, Y.; Narumi, T.; Taiji, M. High-performance drug discovery: Computational screening by combining docking and molecular dynamics simulations PLoS Comput. Biol. 2009, 5 (10) e1000528
61. Singh, N.; Warshel, A. Absolute binding free energy calculations: On the accuracy of computational scoring of protein-ligand interactions Proteins: Struct., Funct., Bioinf. 2010, 78 (7) 1705-1723
62. Anisimov, V. M.; Cavasotto, C. N. Quantum mechanical binding free energy calculation for phosphopeptide inhibitors of the Lck SH2 domain J. Comput. Chem. 2011, 32 (10) 2254-2263
63. Mikulskis, P.; Genheden, S.; Rydberg, P.; Sandberg, L.; Olsen, L.; Ryde, U. Binding affinities in the SAMPL3 trypsin and host-guest blind tests estimated with the MM/PBSA and LIE methods J. Comput.-Aided Mol. Des. 2012, 26 (5) 527-541
64. Sulea, T.; Cui, Q.; Purisima, E. O. Solvated Interaction Energy (SIE) for scoring protein-ligand binding affinities. 2. Benchmark in the CSAR-2010 scoring exercise J. Chem. Inf. Model. 2011, 51 (9) 2066-2081
65. Irwin, J. J.; Sterling, T.; Mysinger, M. M.; Bolstad, E. S.; Coleman, R. G. ZINC: A free tool to discover chemistry for biology J. Chem. Inf. Model. 2012, 52 (7) 1757-1768
66. MACCS Keys; MDL Information Systems, Inc.: San Leandro, CA
67. Rogers, D. J.; Tanimoto, T. T. A computer program for classifying plants Science 1960, 132 (3434) 1115-1118
68. Lipinski, C. A.; Lombardo, F.; Dominy, B. W.; Feeney, P. J. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings Adv. Drug Delivery Rev. 1997, 23 (1-3) 3-25
69. QikProp, version 3.4, Schrödinger, LLC, New York, NY, 2011.
70. Pinal, R. Effect of molecular symmetry on melting temperature and solubility Org. Biomol. Chem. 2004, 2 (18) 2692-2699