Critical hydrogen bond formation for activation of the angiotensin ii type 1 receptor

Journal of Biological Chemistry

Volumn 288, Issue 4, 2013, Pages 2593-2604

  Cabana, Jérôme ^a   Holleran, Brian ^a   Beaulieu, Marie Éve ^a   Leduc, Richard ^a   Escher, Emanuel ^a   Guillemette, Gaétan ^a   Lavigne, Pierre ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION ANALYSIS; AMINO ACIDS; BINDING ENERGY; CHEMICAL ACTIVATION; HYDROGEN BONDS; HYDROPHOBICITY;

CONFORMATIONAL CHANGE; CONSTITUTIVELY ACTIVES; G PROTEIN COUPLED RECEPTORS; HYDROGEN-BOND FORMATION; HYDROPHOBIC RESIDUES; MOLECULAR DYNAMICS SIMULATIONS; RECEPTOR ACTIVATION; TRANS-MEMBRANE DOMAINS;

MOLECULAR DYNAMICS;

ANGIOTENSIN 1 RECEPTOR; MEMBRANE PROTEIN;

ARTICLE; BINDING AFFINITY; CELL ASSAY; CELL STRAIN HEK293; CONFORMATIONAL TRANSITION; HYDROGEN BOND; HYDROPHOBICITY; INTRACELLULAR SIGNALING; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR MODEL; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; SEQUENCE ALIGNMENT; STRUCTURAL HOMOLOGY;

EID: 84873813184     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.395939     Document Type: Article

References (77)

1. Katritch, V., Cherezov, V., and Stevens, R. C. (2012) Diversity and modularity ofGprotein-coupled receptor structures. Trends Pharmacol. Sci. 33, 17-27
2. 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., and Granier, S. (2012) Crystal structure of the μ-opioid receptor bound to a morphinan antagonist. Nature 485, 321-326
3. 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., and Stevens, R.C. (2012) Structure of the human κ-opioid receptor in complex with JDTic. Nature 485, 327-332
4. 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., and Stevens, R. C. (2012) Structure of the nociceptin/orphanin FQ receptor in complex with a peptide mimetic. Nature 485, 395-399
5. Granier, S., Manglik, A., Kruse, A. C., Kobilka, T. S., Thian, F. S., Weis, W. I., and Kobilka, B. K. (2012) Structure of the δ-opioid receptor bound to naltrindole. Nature 485, 400-404
6. Worth, C. L., Kleinau, G., and Krause, G. (2009) Comparative sequence and structural analyses of G-protein-coupled receptor crystal structures and implications for molecular models. PLoS One 4, e7011
7. Schwartz, T. W., Frimurer, T. M., Holst, B., Rosenkilde, M. M., and Elling, C. E. (2006) Molecular mechanism of 7TM receptor activation - a global toggle switch model. Annu. Rev. Pharmacol. Toxicol. 46, 481-519
8. Holst, B., Nygaard, R., Valentin-Hansen, L., Bach, A., Engelstoft, M. S., Petersen, P. S., Frimurer, T. M., and Schwartz, T. W. (2010) A conserved aromatic lock for the tryptophan rotameric switch in TM-VI of seventransmembrane receptors. J. Biol. Chem. 285, 3973-3985
9. Lebon, G., Warne, T., Edwards, P. C., Bennett, K., Langmead, C. J., Leslie, A. G., and Tate, C. G. (2011) Agonist-bound adenosine A2A receptor structures reveal common features of GPCR activation. Nature 474, 521-525
10. de Gasparo, M., Catt, K. J., Inagami, T., Wright, J. W., and Unger, T. (2000) International Union of Pharmacology. XXIII. The angiotensin II receptors. Pharmacol. Rev. 52, 415-472
11. Auger-Messier, M., Clement, M., Lanctot, P. M., Leclerc, P. C., Leduc, R., Escher, E., and Guillemette, G. (2003) The constitutively active N111GAT1 receptor for angiotensin II maintains a high affinity conformation despite being uncoupled from its cognate G protein Gq/11α. Endocrinology 144, 5277-5284
12. Arsenault, J., Cabana, J., Fillion, D., Leduc, R., Guillemette, G., Lavigne, P., and Escher, E. (2010) Temperature dependent photolabeling of the human angiotensin II type 1 receptor reveals insights into its conformational landscape and its activation mechanism. Biochem. Pharmacol. 80, 990-999
13. Clément, M., Cabana, J., Holleran, B. J., Leduc, R., Guillemette, G., Lavigne, P., and Escher, E. (2009) Activation induces structural changes in the liganded angiotensin II type 1 receptor. J. Biol. Chem. 284, 26603-26612
14. Wu, B., Chien, E. Y., 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., and Stevens, R.C. (2010) Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists. Science 330, 1066-1071
15. Bihoreau, C., Monnot, C., Davies, E., Teutsch, B., Bernstein, K. E., Corvol, P., and Clauser, E. (1993) Mutation of Asp74 of the rat angiotensin II receptor confers changes in antagonist affinities and abolishes G-protein coupling. Proc. Natl. Acad. Sci. U.S.A. 90, 5133-5137
16. Feng, Y. H., Zhou, L., Qiu, R., and Zeng, R. (2005) Single mutations at Asn295 and Leu305 in the cytoplasmic half of transmembrane α-helix domain 7 of the AT1 receptor induce promiscuous agonist specificity for angiotensin II fragments: a pseudo-constitutive activity. Mol. Pharmacol. 68, 347-355
17. Pérodin, J., Deraët, M., Auger-Messier, M., Boucard, A. A., Rihakova, L., Beaulieu, M. E., Lavigne, P., Parent, J. L., Guillemette, G., Leduc, R., and Escher, E. (2002) Residues 293 and 294 are ligand contact points of the human angiotensin type 1 receptor. Biochemistry 41, 14348-14356
18. Boucard, A. A., Roy, M., Beaulieu, M. E., Lavigne, P., Escher, E., Guillemette, G., and Leduc, R. (2003) Constitutive activation of the angiotensin II type 1 receptor alters the spatial proximity of transmembrane 7 to the ligand-binding pocket. J. Biol. Chem. 278, 36628-36636
19. Martin, S. S., Boucard, A. A., Clément, M., Escher, E., Leduc, R., and Guillemette, G. (2004) Analysis of the third transmembrane domain of the human type 1 angiotensin II receptor by cysteine scanning mutagenesis. J. Biol. Chem. 279, 51415-51423
20. Clément, M., Martin, S. S., Beaulieu, M. E., Chamberland, C., Lavigne, P., Leduc, R., Guillemette, G., and Escher, E. (2005) Determining the environment of the ligand binding pocket of the human angiotensin II type I (hAT1) receptor using the methionine proximity assay. J. Biol. Chem. 280, 27121-27129
21. Martin, S. S., Holleran, B. J., Escher, E., Guillemette, G., and Leduc, R. (2007) Activation of the angiotensin II type 1 receptor leads to movement of the sixth transmembrane domain: analysis by the substituted cysteine accessibility method. Mol. Pharmacol. 72, 182-190
22. Domazet, I., Holleran, B. J., Martin, S. S., Lavigne, P., Leduc, R., Escher, E., and Guillemette, G. (2009) The second transmembrane domain of the human type 1 angiotensin II receptor participates in the formation of the ligand binding pocket and undergoes integral pivoting movement during the process of receptor activation. J. Biol. Chem. 284, 11922-11929
23. Domazet, I., Martin, S. S., Holleran, B. J., Morin, M. E., Lacasse, P., Lavigne, P., Escher, E., Leduc, R., and Guillemette, G. (2009) The fifth transmembrane domain of angiotensin II Type 1 receptor participates in the formation of the ligand-binding pocket and undergoes a counterclockwise rotation upon receptor activation. J. Biol. Chem. 284, 31953-31961
24. Nygaard, R., Valentin-Hansen, L., Mokrosinski, J., Frimurer, T. M., and Schwartz, T. W. (2010) Conserved water-mediated hydrogen bond network between TM-I, -II, -VI, and -VII in 7TM receptor activation. J. Biol. Chem. 285, 19625-19636
25. Noda, K., Feng, Y. H., Liu, X. P., Saad, Y., Husain, A., and Karnik, S. S. (1996) The active state of the AT1 angiotensin receptor is generated by angiotensin II induction. Biochemistry 35, 16435-16442
26. Feng, Y. H., Miura, S., Husain, A., and Karnik, S. S. (1998) Mechanism of constitutive activation of the AT1 receptor: influence of the size of the agonist switch binding residue Asn111. Biochemistry 37, 15791-15798
27. Thomas, W. G., Qian, H., Chang, C. S., and Karnik, S. (2000) Agonistinduced phosphorylation of the angiotensin II (AT1A) receptor requires generation of a conformation that is distinct from the inositol phosphatesignaling state. J. Biol. Chem. 275, 2893-2900
28. Le, M. T., Vanderheyden, P. M., Szaszák, M., Hunyady, L., and Vauquelin, G. (2002) Angiotensin IV is a potent agonist for constitutive active human AT1 receptors. Distinct roles of the N- and C-terminal residues of angiotensin II during AT1 receptor activation. J. Biol. Chem. 277, 23107-23110
29. Miura, S., Zhang, J., Boros, J., and Karnik, S. S. (2003) TM2-TM7 interaction in coupling movement of transmembrane helices to activation of the angiotensin II type-1 receptor. J. Biol. Chem. 278, 3720-3725
30. Nikiforovich, G. V., Mihalik, B., Catt, K. J., and Marshall, G. R. (2005) Molecular mechanisms of constitutive activity: mutations at position 111 of the angiotensin AT1 receptor. J Pept. Res. 66, 236-248
31. Lee, C., Hwang, S. A., Jang, S. H., Chung, H. S., Bhat, M. B., and Karnik, S. S. (2007) Manifold active-state conformations in GPCRs: agonist-activated constitutively active mutant AT1 receptor preferentially couples to Gq compared to the wild-type AT1 receptor. FEBS Lett. 581, 2517-2522
32. Miura, S., Kiya, Y., Kanazawa, T., Imaizumi, S., Fujino, M., Matsuo, Y., Karnik, S. S., and Saku, K. (2008) Differential bonding interactions of inverse agonists of angiotensin II type 1 receptor in stabilizing the inactive state. Mol. Endocrinol. 22, 139-146
33. Bhuiyan, M. A., Hossain, M., Miura, S., Nakamura, T., Ozaki, M., and Nagatomo, T. (2009) Constitutively active mutant N111G of angiotensin II type 1 (AT1) receptor induces homologous internalization through mediation of AT1-receptor antagonist. J. Pharmacol. Sci. 111, 227-234
34. Bhuiyan, M. A., Hossain, M., Nakamura, T., Ozaki, M., and Nagatomo, T. (2010) Internalization of constitutively active N111G MUTANT of AT1 receptor induced by angiotensin II-receptor antagonists candesartan, losartan, and telmisartan: comparison with valsartan. J. Pharmacol. Sci. 112, 459-462
35. Yan, L., Holleran, B. J., Lavigne, P., Escher, E., Guillemette, G., and Leduc, R. (2010) Analysis of transmembrane domains 1 and 4 of the human angiotensin II AT1 receptor by cysteine-scanning mutagenesis. J. Biol. Chem. 285, 2284-2293
36. Guillemette, G., and Escher, E. (1983) Analysis of the adrenal angiotensin II receptor with the photoaffinity labeling method. Biochemistry 22, 5591-5596
37. Ballesteros, J. A., and Weinstein, H. (1995) in Methods in Neurosciences (Sealfon, S. C., ed) Vol. 25, pp. 366-428, Academic Press, Waltham, MA
38. Zhang, Y. (2007) Template-based modeling and free modeling by I-TASSER in CASP7. Proteins 69, Suppl. 8, 108-117
39. Roy, A., Kucukural, A., and Zhang, Y. (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5, 725-738
40. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477-486
41. Berendsen, H. J. C., van der Spoel, D., and van Drunen, R. (1995) GROMACS: a message-passing parallel molecular dynamics implementation. Comput. Phys. Commun. 91, 43-56
42. Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., and Berendsen, H. J. (2005) GROMACS: fast, flexible, and free. J. Comput. Chem. 26, 1701-1718
43. Hess, B., Kutzner, C., van der Spoel, D., and Lindahl, E. (2008) GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 4, 435-447
44. van der Spoel, D., and Hess, B. (2011) GROMACS - the road ahead. WIREs Comput. Mol. Sci. 1, 710-715
45. Kandt, C., Ash, W. L., and Tieleman, D. P. (2007) Setting up and running molecular dynamics simulations of membrane proteins. Methods 41, 475-488
46. Lemkul, J. A., and Bevan, D. R. (2009) Perturbation of membranes by the amyloid β-peptide: a molecular dynamics study. FEBS J. 276, 3060-3075
47. de Vries, A. H., Mark, A. E., and Marrink, S. J. (2004) The binary mixing behavior of phospholipids in a bilayer: a molecular dynamics study. J. Phys. Chem. B 108, 2454-2463
48. Lemkul, J. A., and Bevan, D. R. (2008) A comparative molecular dynamics analysis of the amyloid β-peptide in a lipid bilayer. Arch. Biochem. Biophys. 470, 54-63
49. Berweger, C. D., van Gunsteren, W. F., and Müller-Plathe, F. (1995) Force field parametrization by weak coupling. Re-engineering SPC water. Chem. Phys. Lett. 232, 429-436
50. Berger, O., Edholm, O., and Jähnig, F. (1997) Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys. J. 72, 2002-2013
51. Tieleman, D. P. (2004) The molecular basis of electroporation. BMC Biochem. 5, 10
52. Tieleman, D. P., Leontiadou, H., Mark, A. E., and Marrink, S. (2003) Simulation of pore formation in lipid bilayers by mechanical stress and electric fields. J. Am. Chem. Soc. 125, 6382-6383
53. MacCallum, J. L., and Tieleman, D. P. (2006) Computer simulation of the distribution of hexane in a lipid bilayer: spatially resolved free energy, entropy, and enthalpy profiles. J. Am. Chem. Soc. 128, 125-130
54. Anézo, C., de Vries, A. H., Höltje, H., Tieleman, D. P., and Marrink, S. (2003) Methodological issues in lipid bilayer simulations. J. Phys. Chem. B 107, 9424-9433
55. Werner, T., Morris, M. B., Dastmalchi, S., and Church, W. B. (2012) Structural modelling and dynamics of proteins for insights into drug interactions. Adv. Drug Deliv. Rev. 64, 323-343
56. Nose, S. (1984) A unified formulation of the constant temperature molecular dynamics methods. J. Chem. Phys. 81, 511-519
57. Hoover, W. G. (1985) Canonical dynamics: equilibrium phase-space distributions. Phys. Rev. A 31, 1695-1697
58. DeLano, W. L. (2010) The PyMOL Molecular Graphics System, version 1.3r1, Schrödinger, LLC, New York
59. Corpet, F. (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16, 10881-10890
60. Ehrhardt, C., Schmolke, M., Matzke, A., Knoblauch, A., Will, C., Wixler, V., and Ludwig, S. (2006) Polyethylenimine, a cost-effective transfection reagent. Signal Transduct. 6, 179-184
61. Cheng, Y., and Prusoff, W. H. (1973) Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem. Pharmacol. 22, 3099-3108
62. Kulińska, K., Kuliński, T., Lyubartsev, A., Laaksonen, A., and Adamiak, R. W. (2000) Spatial distribution functions as a tool in the analysis of ribonucleic acids hydration - molecular dynamics studies. Comput. Chem. 24, 451-457
63. Bhattacharya, S., Hall, S. E., Li, H., and Vaidehi, N. (2008) Ligand-stabilized conformational states of human β2 adrenergic receptor: insight into G-protein-coupled receptor activation. Biophys. J. 94, 2027-2042
64. Nygaard, R., Frimurer, T. M., Holst, B., Rosenkilde, M. M., and Schwartz, T. W. (2009) Ligand binding and micro-switches in 7TM receptor structures. Trends Pharmacol. Sci. 30, 249-259
65. Joseph, M.-P., Maigret, B., Bonnafous, J.-C., Marie, J., and Scheraga, H. A. (1995) A computer modeling postulated mechanism for angiotensin II receptor activation. J. Protein Chem. 14, 381-398
66. Fillion, D., Lemieux, G., Basambombo, L. L., Lavigne, P., Guillemette, G., Leduc, R., and Escher, E. (2010) The amino-terminus of angiotensin II contacts several ectodomains of the angiotensin II receptor AT1. J. Med. Chem. 53, 2063-2075
67. Oliveira, L., Costa-Neto, C. M., Nakaie, C. R., Schreier, S., Shimuta, S. I., and Paiva, A. C. (2007) The angiotensin II AT1 receptor structure-activity correlations in the light of rhodopsin structure. Physiol. Rev. 87, 565-592
68. Ahuja, S., and Smith, S. O. (2009) Multiple switches in G protein-coupled receptor activation. Trends Pharmacol. Sci. 30, 494-502
69. Colson, A. O., Perlman, J. H., Jinsi-Parimoo, A., Nussenzveig, D. R., Osman, R., and Gershengorn, M. C. (1998) A hydrophobic cluster between transmembrane helices 5 and 6 constrains the thyrotropin-releasing hormone receptor in an inactive conformation. Mol. Pharmacol. 54, 968-978
70. Warne, T., Edwards, P. C., Leslie, A. G., and Tate, C. G. (2012) Crystal structures of a stabilized β1-adrenoceptor bound to the biased agonists bucindolol and carvedilol. Structure 20, 841-849
71. Deupi, X., Edwards, P., Singhal, A., Nickle, B., Oprian, D., Schertler, G., and Standfuss, J. (2012) StabilizedGprotein binding site in the structure of constitutively active metarhodopsin-II. Proc. Natl. Acad. Sci. U.S.A. 109, 119-124
72. Standfuss, J., Edwards, P. C., D'Antona, A., Fransen, M., Xie, G., Oprian, D. D., and Schertler, G. F. (2011) The structural basis of agonist-induced activation in constitutively active rhodopsin. Nature 471, 656-660
73. Rasmussen, S. G., DeVree, B. T., Zou, Y., Kruse, A. C., Chung, K. Y., Kobilka, T. S., Thian, F. S., Chae, P. S., Pardon, E., Calinski, D., Mathiesen, J. M., Shah, S. T., Lyons, J. A., Caffrey, M., Gellman, S. H., Steyaert, J., Skiniotis, G., Weis, W. I., Sunahara, R. K., and Kobilka, B. K. (2011) Crystal structure of the β2-adrenergic receptor-Gs protein complex. Nature 477, 549-555
74. Park, S. H., Das, B. B., Casagrande, F., Tian, Y., Nothnagel, H. J., Chu, M., Kiefer, H., Maier, K., De Angelis, A. A., Marassi, F. M., and Opella, S. J. (2012) Structure of the chemokine receptor CXCR1 in phospholipid bilayers. Nature 491, 779-783
75. Sadée, W., Wang, D., and Bilsky, E. J. (2005) Basal opioid receptor activity, neutral antagonists, and therapeutic opportunities. Life Sci. 76, 1427-1437
76. Balmforth, A. J., Lee, A. J., Warburton, P., Donnelly, D., and Ball, S. G. (1997) The conformational change responsible for AT1 receptor activation is dependent upon two juxtaposed asparagine residues on transmembrane helices III and VII. J. Biol. Chem. 272, 4245-4251
77. Perlman, J. H., Colson, A. O., Wang, W., Bence, K., Osman, R., and Gershengorn, M. C. (1997) Interactions between conserved residues in transmembrane helices 1, 2, and 7 of the thyrotropin-releasing hormone receptor. J. Biol. Chem. 272, 11937-11942