Optimized method of G-protein-coupled receptor homology modeling: Its application to the discovery of novel CXCR7 ligands

Journal of Medicinal Chemistry

Volumn 56, Issue 11, 2013, Pages 4236-4251

  Yoshikawa, Yasushi ^a   Oishi, Shinya ^b   Kubo, Tatsuhiko ^b   Tanahara, Noriko ^b   Fujii, Nobutaka ^b   Furuya, Toshio ^a  

^a PharmaDesign Inc   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE A2A RECEPTOR; BETA 1 ADRENERGIC RECEPTOR; BETA 2 ADRENERGIC RECEPTOR; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR7; G PROTEIN COUPLED RECEPTOR; RHODOPSIN;

AMINO ACID SEQUENCE; ARTICLE; BIOLOGICAL ACTIVITY; CANCER CHEMOTHERAPY; CRYSTAL STRUCTURE; DNA TEMPLATE; DRUG TARGETING; FILTRATION; LIGAND BINDING; MOLECULAR DOCKING; MOLECULAR WEIGHT; PHARMACOPHORE; PHYSICAL CHEMISTRY; PROCESS OPTIMIZATION; PROTEIN STRUCTURE; SCREENING; SEQUENCE HOMOLOGY; SIMULATION;

AMINO ACID SEQUENCE; ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; LIGANDS; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; RADIOLIGAND ASSAY; RECEPTORS, CXCR; RECEPTORS, CXCR4; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SMALL MOLECULE LIBRARIES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84879043531     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm400307y     Document Type: Article

References (71)

1. Overington, J. P.; Al-Lazikani, B.; Hopkins, A. L. How many drug targets are there? Nat. Rev. Drug Discovery 2006, 5, 993-996 (Pubitemid 44835126)
2. Borshell, N.; Papp, T.; Congreve, M. Deal watch: Valuation benefits of structure-enabled drug discovery Nat. Rev. Drug Discovery 2011, 10, 166
3. Palczewski, K.; Kumasaka, T.; Hori, T.; Behnke, C. A.; Motoshima, H.; Fox, B. A.; Le Trong, I.; Teller, D. C.; Okada, T.; Stenkamp, R. E.; Yamamoto, M.; Miyano, M. Crystal structure of rhodopsin: A G protein-coupled receptor Science 2000, 289, 739-745 (Pubitemid 30650186)
4. 2 adrenergic G-protein-coupled receptor Nature 2007, 450, 383-387 (Pubitemid 350126755)
5. 2-adrenergic G protein-coupled receptor Science 2007, 318, 1258-1265 (Pubitemid 350172884)
6. 1-adrenergic G-protein-coupled receptor Nature 2008, 454, 486-491
7. 2A adenosine receptor bound to an antagonist Science 2008, 322, 1211-1217
8. Wu, B.; Chien, E. Y. T.; Mol, C. D.; Fenalti, G.; Liu, W.; Katritch, V.; Abagyan, R.; Brooun, A.; Wells, P.; Bi, F. C.; Hamel, D. J.; Kuhn, P.; Handel, T. M.; Cherezov, V.; Stevens, R. C. Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists Science 2010, 330, 1066-1071
9. Chien, E. Y. T.; Liu, W.; Zhao, Q.; Katritch, V.; Han, G. W.; Hanson, M. A.; Shi, L.; Newman, A. H.; Javitch, J. A.; Cherezov, V.; Stevens, R. C. Structure of the human dopamine D3 receptor in complex with a D2/D3 selective antagonist Science 2010, 330, 1091-1095
10. Shimamura, T.; Shiroishi, M.; Weyand, S.; Tsujimoto, H.; Winter, G.; Katritch, V.; Abagyan, R.; Cherezov, V.; Liu, W.; Han, G. W.; Kobayashi, T.; Stevens, R. C.; Iwata, S. Structure of the human histamine H1 receptor complex with doxepin Nature 2011, 475, 65-70
11. Hanson, M. A.; Roth, C. B.; Jo, E.; Griffith, M. T.; Scott, F. L.; Reinhart, G.; Desale, H.; Clemons, B.; Cahalan, S. M.; Schuerer, S. C.; Sanna, M. G.; Han, G. W.; Kuhn, P.; Rosen, H.; Stevens, R. C. Crystal structure of a lipid G protein-coupled receptor Science 2012, 335, 851-855
12. Haga, K.; Kruse, A. C.; Asada, H.; Yurugi-Kobayashi, T.; Shiroishi, M.; Zhang, C.; Weis, W. I.; Okada, T.; Kobilka, B. K.; Haga, T.; Kobayashi, T. Structure of the human M2 muscarinic acetylcholine receptor bound to an antagonist Nature 2012, 482, 547-551
13. Manglik, A.; Kruse, A. C.; Kobilka, T. S.; Thian, F. S.; Mathiesen, J. M.; Sunahara, R. K.; Pardo, L.; Weis, W. I.; Kobilka, B. K.; Granier, S. Crystal structure of the μ-opioid receptor bound to a morphinan antagonist Nature 2012, 485, 321-326
14. Granier, S.; Manglik, A.; Kruse, A. C.; Kobilka, T. S.; Thian, F. S.; Weis, W. I.; Kobilka, B. K. Structure of the δ-opioid receptor bound to naltrindole Nature 2012, 485, 400-404
15. Thompson, A. A.; Liu, W.; Chun, E.; Katritch, V.; Wu, H.; Vardy, E.; Huang, X.-P.; Trapella, C.; Guerrini, R.; Calo, G.; Roth, B. L.; Cherezov, V.; Stevens, R. C. Structure of the nociceptin/orphanin FQ receptor in complex with a peptide mimetic Nature 2012, 485, 395-399
16. Wu, H.; Wacker, D.; Mileni, M.; Katritch, V.; Han, G. W.; Vardy, E.; Liu, W.; Thompson, A. A.; Huang, X.-P.; Carroll, F. I.; Mascarella, S. W.; Westkaemper, R. B.; Mosier, P. D.; Roth, B. L.; Cherezov, V.; Stevens, R. C. Structure of the human κ-opioid receptor in complex with JDTic Nature 2012, 485, 327-332
17. 1 receptor J. Med. Chem. 2011, 54, 8195-8206
18. 2A adenosine receptor ligands J. Med. Chem. 2010, 53, 3748-3755
19. 2-adrenergic receptor ligands Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 6843-6848
20. Carlsson, J.; Coleman, R. G.; Setola, V.; Irwin, J. J.; Fan, H.; Schlessinger, A.; Sali, A.; Roth, B. L.; Shoichet, B. K. Ligand discovery from a dopamine D3 receptor homology model and crystal structure Nat. Chem. Biol. 2011, 7, 769-778
21. Tikhonova, I. G.; Sum, C. S.; Neumann, S.; Engel, S.; Raaka, B. M.; Costanzi, S.; Gershengorn, M. C. Discovery of novel agonists and antagonists of the free fatty acid receptor 1 (FFAR1) using virtual screening J. Med. Chem. 2008, 51, 625-633 (Pubitemid 351252290)
22. Engel, S.; Skoumbourdis, A. P.; Childress, J.; Neumann, S.; Deschamps, J. R.; Thomas, C. J.; Colson, A.-O.; Costanzi, S.; Gershengorn, M. C. A virtual screen for diverse ligands: discovery of selective G protein-coupled receptor antagonists J. Am. Chem. Soc. 2008, 130, 5115-5123 (Pubitemid 351537071)
23. Kiss, R.; Kiss, B.; Könczöl, A.; Szalai, F.; Jelinek, I.; László, V.; Noszál, B.; Falus, A.; Keseru, G. M. Discovery of novel human histamine H4 receptor ligands by large-scale structure-based virtual screening J. Med. Chem. 2008, 51, 3145-3153 (Pubitemid 351821875)
24. Katritch, V.; Rueda, M.; Lam, P. C.-H.; Yeager, M.; Abagyan, R. GPCR 3D homology models for ligand screening: Lessons learned from blind predictions of adenosine A2a receptor complex Proteins 2010, 78, 197-211
25. Cavasotto, C. N.; Orry, A. J. W.; Murgolo, N. J.; Czarniecki, M. F.; Kocsi, S. A.; Hawes, B. E.; O'Neill, K. A.; Hine, H.; Burton, M. S.; Voigt, J. H.; Abagyan, R. A.; Bayne, M. L.; Monsma, F. J., Jr. Discovery of novel chemotypes to a G-protein-coupled receptor through ligand-steered homology modeling and structure-based virtual screening J. Med. Chem. 2008, 51, 581-588 (Pubitemid 351252286)
26. Evers, A.; Klabunde, T. Structure-based drug discovery using GPCR homology modeling: Successful virtual screening for antagonists of the alpha1A adrenergic receptor J. Med. Chem. 2005, 48, 1088-1097 (Pubitemid 40270452)
27. Shacham, S.; Marantz, Y.; Bar-Haim, S.; Kalid, O.; Warshaviak, D.; Avisar, N.; Inbal, B.; Heifetz, A.; Fichman, M.; Topf, M.; Naor, Z.; Noiman, S.; Becker, O. M. PREDICT modeling and in-silico screening for G-protein coupled receptors Proteins 2004, 57, 51-86 (Pubitemid 39195884)
28. Abrol, R.; Bray, J. K.; Goddard, W. A., 3rd. Bihelix: Towards de novo structure prediction of an ensemble of G-protein coupled receptor conformations Proteins 2011, 80, 505-518
29. Worth, C. L.; Kleinau, G.; Krause, G. Comparative sequence and structural analyses of G-protein-coupled receptor crystal structures and implications for molecular models PLoS ONE 2009, 4, e7011
30. Kufareva, I.; Rueda, M.; Katritch, V.; Stevens, R. C.; Abagyan, R. Status of GPCR modeling and docking as reflected by community-wide GPCR Dock 2010 assessment Structure 2011, 19, 1108-1126
31. Balabanian, K.; Lagane, B.; Infantino, S.; Chow, K. Y. C.; Harriague, J.; Moepps, B.; Arenzana-Seisdedos, F.; Thelen, M.; Bachelerie, F. The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes J. Biol. Chem. 2005, 280, 35760-35766 (Pubitemid 41532769)
32. Burns, J. M.; Summers, B. C.; Wang, Y.; Melikian, A.; Berahovich, R.; Miao, Z.; Penfold, M. E. T.; Sunshine, M. J.; Littman, D. R.; Kuo, C. J.; Wei, K.; McMaster, B. E.; Wright, K.; Howard, M. C.; Schall, T. J. A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development J. Exp. Med. 2006, 203, 2201-2213 (Pubitemid 44352240)
33. Miao, Z.; Luker, K. E.; Summers, B. C.; Berahovich, R.; Bhojani, M. S.; Rehemtulla, A.; Kleer, C. G.; Essner, J. J.; Nasevicius, A.; Luker, G. D.; Howard, M. C.; Schall, T. J. CXCR7 (RDC1) promotes breast and lung tumor growth in vivo and is expressed on tumor-associated vasculature Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 15735-15740 (Pubitemid 350035369)
34. Monnier, J.; Boissan, M.; L'Helgoualc'h, A.; Lacombe, M.-L.; Turlin, B.; Zucman-Rossi, J.; Théret, N.; Piquet-Pellorce, C.; Samson, M. CXCR7 is up-regulated in human and murine hepatocellular carcinoma and is specifically expressed by endothelial cells Eur. J. Cancer 2012, 48, 138-148
35. Wang, J.; Shiozawa, Y.; Wang, J.; Wang, Y.; Jung, Y.; Pienta, K. J.; Mehra, R.; Loberg, R.; Taichman, R. S. The role of CXCR7/RDC1 as a chemokine receptor for CXCL12/SDF-1 in prostate cancer J. Biol. Chem. 2008, 283, 4283-4294
36. Hattermann, K.; Held-Feindt, J.; Lucius, R.; Müerköster, S. S.; Penfold, M. E. T.; Schall, T. J.; Mentlein, R. The chemokine receptor CXCR7 is highly expressed in human glioma cells and mediates antiapoptotic effects Cancer Res. 2010, 70, 3299-3308
37. Wijtmans, M.; Maussang, D.; Sirci, F.; Scholten, D. J.; Canals, M.; Mujić-Delić, A.; Chong, M.; Chatalic, K. L. S.; Custers, H.; Janssen, E.; de Graaf, C.; Smit, M. J.; de Esch, I. J. P.; Leurs, R. Synthesis, modeling and functional activity of substituted styrene-amides as small-molecule CXCR7 agonists Eur. J. Med. Chem. 2012, 51, 184-192
38. Gravel, S.; Malouf, C.; Boulais, P. E.; Berchiche, Y. A.; Oishi, S.; Fujii, N.; Leduc, R.; Sinnett, D.; Heveker, N. The peptidomimetic CXCR4 antagonist TC14012 recruits β-arrestin to CXCR7: Roles of receptor domains J. Biol. Chem. 2010, 285, 37939-37943
39. Kalatskaya, I.; Berchiche, Y. A.; Gravel, S.; Limberg, B. J.; Rosenbaum, J. S.; Heveker, N. AMD3100 is a CXCR7 ligand with allosteric agonist properties Mol. Pharmacol. 2009, 75, 1240-1247
40. Melikian, A.; Burns, J.; Mcmaster, B., E.; Schall, T.; Wright, J. J. Inhibitors of the binding of chemokines I-TAC or SDF-1 to the CCXCKR2 receptor. Patent WO2004058705, 2004.
41. Melikian, A.; Wright, J. J. K. Substituted arylamides. Patent WO2006038989, 2006.
42. Thomas, W. D.; Leleti, M. R.; Pennell, A. M. K. CXCR4 modulators. Patent WO2007115231, 2007.
43. Leleti, M. R.; Thomas, W. D.; Zhang, P.; Pennell, A. M. K. CXCR4 modulators. Patent WO2007115232, 2007.
44. Chen, X.; Fan, P.; Gleason, M., M.; Jaen, J., C.; Li, L.; Mcmahon, J., P.; Powers, J.; Zeng, Y.; Zhang, P. Modulators of CXCR7. Patent WO2010054006, 2010.
45. Okamoto, M.; Takayama, K.; Shimizu, T.; Ishida, K.; Takahashi, O.; Furuya, T. Identification of death-associated protein kinases inhibitors using structure-based virtual screening J. Med. Chem. 2009, 52, 7323-7327
46. Larkin, M. A.; Blackshields, G.; Brown, N. P.; Chenna, R.; McGettigan, P. A.; McWilliam, H.; Valentin, F.; Wallace, I. M.; Wilm, A.; Lopez, R.; Thompson, J. D.; Gibson, T. J.; Higgins, D. G. Clustal W and Clustal X version 2.0 Bioinformatics 2007, 23, 2947-2948 (Pubitemid 350162903)
47. Ballesteros, J.; Weinstein, H. Integrated methods for the construction of three-dimensional models of structure-function relations in G protein-coupled receptors Methods Neurosci. 1995, 25, 366-428
48. 2 adrenoceptor Nature 2011, 477, 549-555
49. 2A adenosine receptor Science 2011, 332, 322-327
50. Choe, H.-W.; Kim, Y. J.; Park, J. H.; Morizumi, T.; Pai, E. F.; Krauss, N.; Hofmann, K. P.; Scheerer, P.; Ernst, O. P. Crystal structure of metarhodopsin II Nature 2011, 471, 651-655
51. 2 adrenergic receptor-Gs protein complex Nature 2011, 469, 175-180
52. MOE Molecular Operating Environment; Chemical Computing Group Inc.: Montreal, Quebec, Canada, 2007.
53. ChemDiv Chemical Database; ChemDiv Inc.: San Diego, CA.
54. Brelot, A.; Heveker, N.; Montes, M.; Alizon, M. Identification of residues of CXCR4 critical for human immunodeficiency virus coreceptor and chemokine receptor activities J. Biol. Chem. 2000, 275, 23736-23744 (Pubitemid 30624660)
55. Gerlach, L. O.; Skerlj, R. T.; Bridger, G. J.; Schwartz, T. W. Molecular interactions of cyclam and bicyclam non-peptide antagonists with the CXCR4 chemokine receptor J. Biol. Chem. 2001, 276, 14153-14160
56. 262 of the chemokine receptor CXCR4 impairs its coreceptor function for human immunodeficiency virus-1 entry and abrogates the antagonistic activity of AMD3100 Mol. Pharmacol. 2001, 60, 164-173 (Pubitemid 32595244)
57. Gerlach, L. O.; Jakobsen, J. S.; Jensen, K. P.; Rosenkilde, M. R.; Skerlj, R. T.; Ryde, U.; Bridger, G. J.; Schwartz, T. W. Metal ion enhanced binding of AMD3100 to Asp262 in the CXCR4 receptor Biochemistry 2003, 42, 710-717 (Pubitemid 36133295)
58. Rosenkilde, M. M.; Gerlach, L.-O.; Jakobsen, J. S.; Skerlj, R. T.; Bridger, G. J.; Schwartz, T. W. Molecular mechanism of AMD3100 antagonism in the CXCR4 receptor: Transfer of binding site to the CXCR3 receptor J. Biol. Chem. 2004, 279, 3033-3041 (Pubitemid 38114296)
59. Wong, R. S. Y.; Bodart, V.; Metz, M.; Labrecque, J.; Bridger, G.; Fricker, S. P. Comparison of the potential multiple binding modes of bicyclam, monocylam, and noncyclam small-molecule CXC chemokine receptor 4 inhibitors Mol. Pharmacol. 2008, 74, 1485-1495
60. Labute, P.; Williams, C.; Feher, M.; Sourial, E.; Schmidt, J. M. Flexible alignment of small molecules J. Med. Chem. 2001, 44, 1483-1490 (Pubitemid 32852192)
61. Hall, S. E.; Mao, A.; Nicolaidou, V.; Finelli, M.; Wise, E. L.; Nedjai, B.; Kanjanapangka, J.; Harirchian, P.; Chen, D.; Selchau, V.; Ribeiro, S.; Schyler, S.; Pease, J. E.; Horuk, R.; Vaidehi, N. Elucidation of binding sites of dual antagonists in the human chemokine receptors CCR2 and CCR5 Mol. Pharmacol. 2009, 75, 1325-1336
62. MACCS; MDL Information Systems, Inc.: San Ramon, CA, 2002.
63. The UniProt Consortium. The Universal Protein Resource (UniProt) in 2010. Nucleic Acids Res. 2009, 38, D142-D148.
64. Gouy, M.; Guindon, S.; Gascuel, O. SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building Mol. Biol. Evol. 2010, 27, 221-224
65. Bernstein, F. C.; Koetzle, T. F.; Williams, G. J.; Meyer, E. F., Jr.; Brice, M. D.; Rodgers, J. R.; Kennard, O.; Shimanouchi, T.; Tasumi, M. The Protein Data Bank: A computer-based archival file for macromolecular structures J. Mol. Biol. 1977, 112, 535-542 (Pubitemid 8109216)
66. Wang, J.; Cieplak, P.; Kollman, P. A. How Well Does a Restrained Electrostatic Potential (RESP) Model Perform in Calculating Conformational Energies of Organic and Biological Molecules? J. Comput. Chem. 2000, 21, 1049-1074
67. Halgren, T. A. MMFF VII. Characterization of MMFF94, MMFF94s, and other widely available force fields for conformational energies and for intermolecular-interaction energies and geometries J. Comput. Chem. 1999, 20, 730-748 (Pubitemid 129652636)
68. Weininger, D. SMILES, a chemical language and information system. 1. Introduction to methodology and encoding rules J. Chem. Inf. Model. 1988, 28, 31-36 (Pubitemid 18574254)
69. Horio, K.; Muta, H.; Goto, J.; Hirayama, N. A simple method to improve the odds in finding "lead-like" compounds from chemical libraries Chem. Pharm. Bull. 2007, 55, 980-984 (Pubitemid 47026529)
70. Bayon: A simple and fast clustering tool. http://code.google.com/p/bayon/ (accessed September 2010).
71. Sadowski, J.; Gasteiger, J. From atoms and bonds to three-dimensional atomic coordinates: Automatic model builders Chem. Rev. 1993, 93, 2567-2581