Ligand binding determinants for angiotensin II type 1 receptor from computer simulations

Journal of Chemical Information and Modeling

Volumn 53, Issue 11, 2013, Pages 2874-2883

  Matsoukas, Minos Timotheos ^a,b   Cordomí, Arnau ^b   Ríos, Santiago ^b   Pardo, Leonardo ^b   Tselios, Theodore ^a  

^a UNIVERSITY OF PATRAS   (Greece)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

FREE ENERGY; LIGANDS; LIPID BILAYERS; MOLECULAR DYNAMICS; PHARMACODYNAMICS;

BINDING AFFINITIES; BINDING FREE ENERGY; G-PROTEIN COUPLED RECEPTORS; LIGAND RECEPTORS; MOLECULAR DYNAMICS SIMULATIONS; MOLECULAR MECHANISM; PHARMACOPHORE MODELING; STRUCTURAL MODELING;

BINDING ENERGY;

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN 1 RECEPTOR ANTAGONIST; ANGIOTENSIN II; CHEMOKINE RECEPTOR CXCR4; CXCR4 PROTEIN, HUMAN; LIGAND;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CHEMISTRY; CLASSIFICATION; HUMAN; LIPID BILAYER; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MOLECULAR GENETICS; PHYLOGENY; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; STRUCTURAL HOMOLOGY; THERMODYNAMICS;

AMINO ACID SEQUENCE; ANGIOTENSIN II; ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; BINDING SITES; HUMANS; LIGANDS; LIPID BILAYERS; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTOR, ANGIOTENSIN, TYPE 1; RECEPTORS, CXCR4; SEQUENCE ALIGNMENT; STRUCTURAL HOMOLOGY, PROTEIN; THERMODYNAMICS;

EID: 84888592896     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci400400m     Document Type: Article

References (70)

1. Smith, R. D.; Timmermans, P. B. Human angiotensin receptor subtypes Curr. Opin. Nephrol. Hypertens. 1994, 3, 112-122
2. de Gasparo, M.; Catt, K. J.; Inagami, T.; Wright, J. W.; Unger, T. International Union of Pharmacology. XXIII. The angiotensin II receptors Pharmacol. Rev. 2000, 52, 415-472
3. Steckelings, U. M.; Kaschina, E.; Unger, T. The AT2 receptor-A matter of love and hate Peptides 2005, 26, 1401-1409
4. Aulakh, G. K.; Sodhi, R. K.; Singh, M. An update on non-peptide angiotensin receptor antagonists and related RAAS modulators Life Sci. 2007, 81, 615-639
5. Vijayalakshmi, K.; Jananie, R.; Priya, V. Secondary metabolites of Cynodon dactylon as an antagonist to angiotensin II type1 receptor: Novel in silico drug targeting approach for diabetic retinopathy J. Pharmacol. Pharmacother. 2012, 3, 20-25
6. 1 angiotensin II receptor antagonist: Reorientation of imidazole pharmacophore groups in losartan reserves high receptor affinity and confirms docking studies J. Comput-Aided. Mol. Des. 2010, 24, 749-758
7. Maggioni, A. Efficacy of angiotensin receptor blockers in cardiovascular disease Cardiovasc. Drugs Ther. 2006, 20, 295-308
8. Lew, M. J.; Ziogas, J.; Christopoulos, A. Dynamic mechanisms of non-classical antagonism by competitive AT1 receptor antagonists Trends Pharmacol. Sci. 2000, 21, 376-381
9. Miura, S.-I.; Fujino, M.; Hanzawa, H.; Kiya, Y.; Imaizumi, S.; Matsuo, Y.; Tomita, S.; Uehara, Y.; Karnik, S. S.; Yanagisawa, H.; Koike, H.; Komuro, I.; Saku, K. Molecular mechanism underlying inverse agonist of angiotensin II type 1 receptor J. Biol. Chem. 2006, 281, 19288-19295
10. Sica, D.; White, W. B.; Weber, M. A.; Bakris, G. L.; Perez, A.; Cao, C.; Handley, A.; Kupfer, S. Comparison of the novel angiotensin II receptor blocker azilsartan medoxomil vs valsartan by ambulatory blood pressure monitoring J. Clin. Hypertens. 2011, 13, 467-472
11. Neutel, J. M.; Germino, W. F.; Punzi, H.; McBride, M.; Bryson, C. C.; Belder, R. Results of a double blind placebo controlled study to evaluate the efficacy and safety of PS433540 in human subjects with hypertension Circulation 2008, 118, S886-S886
12. Yi, S.; Kim, J. W.; Kim, T. E.; Kim, J.; Jun, Y. K.; Choi, J.; Yoon, S. H.; Choi, J. Y.; Song, S. H.; Shin, S. G.; Jang, I. J.; Yu, K. S. Effect of multiple doses of fimasartan, an angiotensin II receptor antagonist, on the steady-state pharmacokinetics of digoxin in healthy volunteers Int. J. Clin. Pharm. Ther. 2011, 49, 321-327
13. Day, P. W.; Rasmussen, S. G. F.; Parnot, C.; Fung, J. J.; Masood, A.; Kobilka, T. S.; Yao, X.-J.; Choi, H.-J.; Weis, W. I.; Rohrer, D. K.; Kobilka, B. K. A monoclonal antibody for G protein-coupled receptor crystallography Nat. Methods 2007, 4, 927-929
14. Serrano-Vega, M. J.; Magnani, F.; Shibata, Y.; Tate, C. G. Conformational thermostabilization of the beta1-adrenergic receptor in a detergent-resistant form Proc. Natl. Acad. Sci. 2008, 105, 877-882
15. Katritch, V.; Cherezov, V.; Stevens, R. C. Diversity and modularity of G protein-coupled receptor structures Trends Pharmacol. Sci. 2012, 33, 17-27
16. Katritch, V.; Cherezov, V.; Stevens, R. C. structure-Function of the G protein-coupled receptor superfamily Annu. Rev. Pharmacol. Toxicol. 2013, 53, 531-556
17. Liapakis, G.; Cordomí, A.; Pardo, L. The G-protein coupled receptor family: Actors with many faces Curr. Pharm. Des. 2012, 18, 175-185
18. Olivella, M.; Gonzalez, A.; Pardo, L.; Deupi, X. Relation between sequence and structure in membrane proteins Bioinformatics 2013, 29, 1589-1592
19. Hansson, T.; Marelius, J.; Aqvist, J. Ligand binding affinity prediction by linear interaction energy methods J. Comput-Aided. Mol. Des. 1998, 12, 27-35
20. Discovery Studio Modeling Environment, Release 3.5; Accelrys Software Inc.: San Diego, CA, 2012.
21. Cagigal, E.; Gonzalez, L.; Alonso, R. M.; Jimenez, R. M. pKa determination of angiotensin II receptor antagonists (ARA II) by spectrofluorimetry J. Pharm. Biomed. Anal. 2001, 26, 477-486
22. Li, H.; Sutter, J.; Hoffman, R. HypoGen: An automated system for generating 3D predictive pharmacophore models. In Pharmacophore Perception, Development and Use in Drug Design; Guner, O., Ed.; International University Line: 2000.
23. Marti-Renom, M. A.; Stuart, A. C.; Fiser, A.; Sanchez, R.; Melo, F.; Sali, A. Comparative protein structure modeling of genes and genomes Annu. Rev. Biophys. Biomol. Struct. 2000, 29, 291-325
24. 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
25. Ballesteros, J. A.; Weinstein, H. Integrated methods for the construction of three-dimensional models and computational probing of structure-function relations in G protein-coupled receptors. In Methods in Neurosciences; Stuart, C. S., Ed.; Academic Press: 1995; Vol. 25, pp 366-428.
26. Verdonk, M. L.; Cole, J. C.; Hartshorn, M. J.; Murray, C. W.; Taylor, R. D. Improved protein-ligand docking using GOLD Proteins: Struct., Funct., Bioinf. 2003, 52, 609-623
27. Krammer, A.; Kirchhoff, P. D.; Jiang, X.; Venkatachalam, C. M.; Waldman, M. LigScore: A novel scoring function for predicting binding affinities J. Mol. Graphics Modell. 2005, 23, 395-407
28. Gehlhaar, D. K.; Verkhivker, G. M.; Rejto, P. A.; Sherman, C. J.; Fogel, D. R.; Fogel, L. J.; Freer, S. T. Molecular recognition of the inhibitor AG-1343 by HIV-1 protease: Conformationally flexible docking by evolutionary programming Chem. Biol. 1995, 2, 317-324
29. Gehlhaar, D. K.; Bouzida, D.; Rejto, P. A. Reduced dimensionality in ligand-protein structure prediction: Covalent inhibitors of serine proteases and design of site-directed combinatorial libraries. In Rational Drug Design; American Chemical Society: 1999; Vol. 719, pp 292-311.
30. Jain, A. N. Scoring noncovalent protein-ligand interactions: A continuous differentiable function tuned to compute binding affinities J. Comput-Aided. Mol. Des. 1996, 10, 427-440
31. Muegge, I.; Martin, Y. C. A general and fast scoring function for protein-ligand interactions: A simplified potential approach J. Med. Chem. 1999, 42, 791-804
32. Berendsen, H. J. C.; van der Spoel, D.; van Drunen, R. GROMACS: A message-passing parallel molecular dynamics implementation Comput. Phys. Commun. 1995, 91, 43-56
33. Cordomi, A.; Edholm, O.; Perez, J. J. Effect of force field parameters on sodium and potassium ion binding to dipalmitoyl phosphatidylcholine bilayers J. Chem. Theory Comput. 2009, 5, 2125-2134
34. Bussi, G.; Donadio, D.; Parrinello, M. Canonical sampling through velocity rescaling J. Chem. Phys. 2007, 126, 14101-14107
35. Miyamoto, S.; Kollman, P. A. Settle: An analytical version of the SHAKE and RATTLE algorithm for rigid water models J. Comput. Chem. 1992, 13, 952-962
36. 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, 10089-10092
37. Lindorff-Larsen, K.; Piana, S.; Palmo, K.; Maragakis, P.; Klepeis, J. L.; Dror, R. O.; Shaw, D. E. Improved side-chain torsion potentials for the Amber ff99SB protein force field Proteins: Struct., Funct., Bioinf. 2010, 78, 1950-1958
38. Berger, O.; Edholm, O.; Jähnig, F. Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature Biophys. J. 1997, 72, 2002-2013
39. Bayly, C. I.; Cieplak, P.; Cornell, W.; Kollman, P. A. A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: The RESP model J. Phys. Chem. 1993, 97, 10269-10280
40. Cordomi, A.; Caltabiano, G.; Pardo, L. Membrane protein simulations using AMBER force field and berger lipid parameters J. Chem. Theory Comput. 2012, 8, 948-958
41. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; Nakatsuji, H.; Caricato, M.; Li, X.; Hratchian, H. P.; Izmaylov, A. F.; Bloino, J.; Zheng, G.; Sonnenberg, J. L.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Vreven, T.; Montgomery, J. A., Jr.; Peralta, J. E.; Ogliaro, F.; Bearpark, M.; Heyd, J. J.; Brothers, E.; Kudin, K. N.; Staroverov, V. N.; Kobayashi, R.; Normand, J.; Raghavachari, K.; Rendell, A.; Burant, J. C.; Iyengar, S. S.; Tomasi, J.; Cossi, M.; Rega, N.; Millam, J. M.; Klene, M.; Knox, J. E.; Cross, J. B.; Bakken, V.; Adamo, C.; Jaramillo, J.; Gomperts, R.; Stratmann, R. E.; Yazyev, O.; Austin, A. J.; Cammi, R.; Pomelli, C.; Ochterski, J. W.; Martin, R. L.; Morokuma, K.; Zakrzewski, V. G.; Voth, G. A.; Salvador, P.; Dannenberg, J. J.; Dapprich, S.; Daniels, A. D.; Ö, F.; Foresman, J. B.; Ortiz, J. V.; Cioslowski, J.; Fox, D. J. Gaussian∼09 Revision A.1; 2009.
42. Almlöf, M.; Brandsdal, B. O.; Åqvist, J. Binding affinity prediction with different force fields: Examination of the linear interaction energy method J. Comput. Chem. 2004, 25, 1242-1254
43. Åqvist, J.; Hansson, T. On the validity of electrostatic linear response in polar solvents J. Phys. Chem. 1996, 100, 9512-9521
44. Cheng, Y.; Prusoff, W. Relationship between inhibition constant (Ki) and concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic-reaction Biochem. Pharmacol. 1973, 22, 3099-3108
45. Gonzalez, A.; Cordomí, A.; Caltabiano, G.; Pardo, L. Impact of helix irregularities on sequence alignment and homology modeling of G protein-coupled receptors ChemBioChem 2012, 13, 1393-1399
46. Govaerts, C.; Blanpain, C.; Deupi, X.; Ballet, S.; Ballesteros, J. A.; Wodak, S. J.; Vassart, G.; Pardo, L.; Parmentier, M. The TXP motif in the second transmembrane helix of CCR5: A structural determinant of the chemokine-induced activation J. Biol. Chem. 2001, 276, 13217-13225
47. Deupi, X.; Olivella, M.; Govaerts, C.; Ballesteros, J. A.; Campillo, M.; Pardo, L. Ser and Thr residues modulate the conformation of pro-kinked transmembrane alpha-helices Biophys. J. 2004, 86, 105-115
48. Peeters, M. C.; van Westen, G. J. P.; Li, Q.; IJzerman, A. P. Importance of the extracellular loops in G protein-coupled receptors for ligand recognition and receptor activation Trends Pharmacol. Sci. 2011, 32, 35-42
49. Takezako, T.; Gogonea, C.; Saad, Y.; Noda, K.; Karnik, S. S. Network leaning" as a mechanism of insurmountable antagonism of the angiotensin II type 1 receptor by non-peptide antagonists J. Biol. Chem. 2004, 279, 15248-15257
50. Sansuk, K.; Deupi, X.; Torrecillas, I. R.; Jongejan, A.; Nijmeijer, S.; Bakker, R. A.; Pardo, L.; Leurs, R. A structural insight into the reorientation of transmembrane domains 3 and 5 during family A G protein-coupled receptor activation Mol. Pharmacol. 2011, 79, 262-269
51. Fierens, F. L.; Vanderheyden, P. M.; Gaborik, Z.; Minh, T. L.; Backer, J. P.; Hunyady, L.; Ijzerman, A.; Vauquelin, G. Lys(199) mutation of the human angiotensin type 1 receptor differentially affects the binding of surmountable and insurmountable non-peptide antagonists JRAAS 2000, 1, 283-288
52. Yasuda, N.; Miura, S.-i.; Akazawa, H.; Tanaka, T.; Qin, Y.; Kiya, Y.; Imaizumi, S.; Fujino, M.; Ito, K.; Zou, Y.; Fukuhara, S.; Kunimoto, S.; Fukuzaki, K.; Sato, T.; Ge, J.; Mochizuki, N.; Nakaya, H.; Saku, K.; Komuro, I. Conformational switch of angiotensin II type 1 receptor underlying mechanical stress-induced activation EMBO Rep. 2008, 9, 179-186
53. Wilcken, R.; Zimmermann, M. O.; Lange, A.; Joerger, A. C.; Boeckler, F. M. Principles and applications of halogen bonding in medicinal chemistry and chemical biology J. Med. Chem. 2012, 56, 1363-1388
54. Unal, H.; Jagannathan, R.; Bhat, M. B.; Karnik, S. S. Ligand-specific conformation of extracellular loop-2 in the angiotensin II type 1 receptor J. Biol. Chem. 2010, 285, 16341-16350
55. Gohlke, H.; Klebe, G. Approaches to the description and prediction of the binding affinity of small-molecule ligands to macromolecular receptors Angew. Chem., Int. Ed. Engl. 2002, 41, 2644-2676
56. González, A.; Murcia, M.; Benhamú, B.; Campillo, M.; López-Rodríguez, M. L.; Pardo, L. The importance of solvation in the design of ligands targeting membrane proteins MedChemComm 2011, 2, 160-164
57. Nicolai, E.; Cure, G.; Goyard, J.; Kirchner, M.; Teulon, J.-M.; Versigny, A.; Cazes, M.; Caussade, F.; Virone-Oddos, A.; Cloarec, A. Synthesis and SAR studies of novel triazolopyrimidine derivatives as potent, orally active angiotensin II receptor antagonists J. Med. Chem. 1994, 37, 2371-2386
58. Poss, M.; Gu, Z.; Ryono, D.; Reid, J.; Siebermcmaster, E.; Spitzmiller, E.; Dejneka, T.; Dickinson, K.; Williams, S.; Moreland, S.; Delaney, C.; Bird, J.; Waldron, T.; Schaeffer, T.; Heldberg, S.; Petrillo, E. 1-4-Substituted indoles-a potent and selective class of angiotensin-II receptor antagonists Bioorg. Med. Chem. Lett. 1994, 4, 145-150
59. Salimbeni, A.; Canevotti, R.; Paleari, F.; Poma, D.; Caliari, S.; Fici, F.; Cirillo, R.; Renzetti, A. R.; Subissi, A. N-3-substituted pyrimidinones as potent, orally active, AT1 selective angiotensin II receptor antagonists J. Med. Chem. 1995, 38, 4806-4820
60. Agelis, G.; Resvani, A.; Durdagi, S.; Spyridaki, K.; TuÌŠ mová, T.; Slaninova, J.; Giannopoulos, P.; Vlahakos, D.; Liapakis, G.; Mavromoustakos, T.; Matsoukas, J. The discovery of new potent non-peptide angiotensin II AT1 receptor blockers: A concise synthesis, molecular docking studies and biological evaluation of N-substituted 5-butylimidazole derivatives Eur. J. Med. Chem. 2012, 55, 358-374
61. Kim, K.; Qian, L.; Bird, J.; Dickinson, K.; Moreland, S.; Schaeffer, T.; Waldron, T.; Delaney, C.; Weller, H.; Miller, A. Quinoxaline N-oxide containing potent angiotensin-II receptor antagonists-synthesis, biological properties, and structure-activity-relationships J. Med. Chem. 1993, 36, 2335-2342
62. Wexler, R. R.; Greenlee, W. J.; Irvin, J. D.; Goldberg, M. R.; Prendergast, K.; Smith, R. D.; Timmermans, P. B. M. W. M. Nonpeptide angiotensin II receptor antagonists: The next generation in antihypertensive therapy J. Med. Chem. 1996, 39, 625-656
63. Wong, P. C.; Price, W. A.; Chiu, A. T.; Duncia, J. V.; Carini, D. J.; Wexler, R. R.; Johnson, A. L.; Timmermans, P. B. Nonpeptide angiotensin II receptor antagonists. XI. Pharmacology of EXP3174: An active metabolite of DuP 753, an orally active antihypertensive agent J. Pharmacol. Exp. Ther. 1990, 255, 211-217
64. Bhuiyan, M. A.; Hossain, M.; Miura, S.-i.; Nakamura, T.; Ozaki, M.; Nagatomo, T. Constitutively active mutant N111G of angiotensin II type 1 (AT1) receptor induces homologous internalization through mediation of AT1-receptor antagonist J. Pharmacol. Sci. 2009, 111, 227-234
65. Murugesan, N.; Tellew, J. E.; Gu, Z.; Kunst, B. L.; Fadnis, L.; Cornelius, L. A.; Baska, R. A. F.; Yang, Y.; Beyer, S. M.; Monshizadegan, H.; Dickinson, K. E.; Panchal, B.; Valentine, M. T.; Chong, S.; Morrison, R. A.; Carlson, K. E.; Powell, J. R.; Moreland, S.; Barrish, J. C.; Kowala, M. C.; Macor, J. E. Discovery of n-isoxazolyl biphenylsulfonamides as potent dual angiotensin II and endothelin a receptor antagonists J. Med. Chem. 2002, 45, 3829-3835
66. Ferrario, C. M.; Smith, R. D. Role of olmesartan in combination therapy in blood pressure control and vascular function Vasc. Health Risk Manage. 2010, 6, 701-709
67. Salimbeni, A.; Canevotti, R.; Paleari, F.; Bonaccorsi, F.; Renzetti, A. R.; Belvisi, L.; Bravi, G.; Scolastico, C. Nonpeptide angiotensin II receptor antagonists. synthesis, in vitro activity, and molecular modeling studies of n-[(heterobiaryl)methyl]imidazoles J. Med. Chem. 1994, 37, 3928-3938
68. Tamura, K.; Peterson, D.; Peterson, N.; Stecher, G.; Nei, M.; Kumar, S. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods Mol. Biol. Evol. 2011, 28, 2731-2739
69. Jones, D. T.; Taylor, W. R.; Thornton, J. M. The rapid generation of mutation data matrices from protein sequences Comput. Appl. Biosci. 1992, 8, 275-282
70. Felsenstein, J. Confidence limits on phylogenies: An approach using the bootstrap Evolution 1985, 39, 783-791