Structure of the angiotensin receptor revealed by serial femtosecond crystallography

Cell

Volumn 161, Issue 4, 2015, Pages 833-844

  Zhang, Haitao ^a   Unal, Hamiyet ^b   Gati, Cornelius ^c   Han, Gye Won ^a   Liu, Wei ^d   Zatsepin, Nadia A ^d   James, Daniel ^d   Wang, Dingjie ^d   Nelson, Garrett ^d   Weierstall, Uwe ^d   Sawaya, Michael R ^e   Xu, Qingping ^f   Messerschmidt, Marc ^g   Williams, Garth J ^h   Boutet, Sébastien ^h   Yefanov, Oleksandr M ^c   White, Thomas A ^c   Wang, Chong ⁱ   Ishchenko, Andrii ^a   Tirupula, Kalyan C ^b   Desnoyer, Russell ^b   Coe, Jesse ^d   Conrad, Chelsie E ^d   Fromme, Petra ^d   Stevens, Raymond C ^a,j   Katritch, Vsevolod ^a   Karnik, Sadashiva S ^b   Cherezov, Vadim ^a   more..

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

^c DESY   (Germany)

^d ARIZONA STATE UNIVERSITY   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

^g BioXFEL Science and Technology Center   (United States)

^h SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

ⁱ HARVARD UNIVERSITY   (United States)

^j SHANGHAITECH UNIVERSITY   (China)

more..

Author keywords

[No Author keywords available]

Indexed keywords

AGTR1 PROTEIN, HUMAN; ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN 1 RECEPTOR ANTAGONIST; NAPHTHYRIDINE DERIVATIVE; ZD 7155;

AMINO ACID SEQUENCE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MUTAGENESIS; SEQUENCE ALIGNMENT; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; CRYSTALLOGRAPHY, X-RAY; HUMANS; MOLECULAR SEQUENCE DATA; MUTAGENESIS; NAPHTHYRIDINES; RECEPTOR, ANGIOTENSIN, TYPE 1; SEQUENCE ALIGNMENT;

EID: 84937761091     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.04.011     Document Type: Article

References (67)

1. H. Akazawa, M. Yano, C. Yabumoto, Y. Kudo-Sakamoto, and I. Komuro Angiotensin II type 1 and type 2 receptor-induced cell signaling Curr. Pharm. Des. 19 2013 2988 2995
2. P. Balakumar, and G. Jagadeesh Structural determinants for binding, activation, and functional selectivity of the angiotensin AT1 receptor J. Mol. Endocrinol. 53 2014 R71 R92
3. P. Balakumar, H.K. Bishnoi, and N. Mahadevan Telmisartan in the management of diabetic nephropathy: a contemporary view Curr. Diabetes Rev. 8 2012 183 190
4. J.A. Ballesteros, and H. Weinstein Integrated methods for the construction of three dimensional models and computational probing of structure-function relations in G-protein coupled receptors Methods Neurosci 25 1995 366 428
5. A. Barty, R.A. Kirian, F.R. Maia, M. Hantke, C.H. Yoon, T.A. White, and H. Chapman Cheetah: software for high-throughput reduction and analysis of serial femtosecond X-ray diffraction data J. Appl. Cryst. 47 2014 1118 1131
6. G. Bricogne, E. Blanc, M. Brandl, C. Flensburg, P. Keller, W. Paciorek, P. Roversi, A. Sharff, O.S. Smart, and C. Vonrhein Buster version 2.8.0 2009 Global Phasing Ltd Cambridge, United Kingdom
7. M. Burnier, and H.R. Brunner Angiotensin II receptor antagonists Lancet 355 2000 637 645
8. M. Caffrey, and V. Cherezov Crystallizing membrane proteins using lipidic mesophases Nat. Protoc. 4 2009 706 731
9. E. Chun, A.A. Thompson, W. Liu, C.B. Roth, M.T. Griffith, V. Katritch, J. Kunken, F. Xu, V. Cherezov, M.A. Hanson, and R.C. Stevens Fusion partner toolchest for the stabilization and crystallization of G protein-coupled receptors Structure 20 2012 967 976
10. M. de Gasparo, K.J. Catt, T. Inagami, J.W. Wright, and T. Unger International union of pharmacology. XXIII. The angiotensin II receptors Pharmacol. Rev. 52 2000 415 472
11. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
12. G. Fenalti, P.M. Giguere, V. Katritch, X.P. Huang, A.A. Thompson, V. Cherezov, B.L. Roth, and R.C. Stevens Molecular control of δ-opioid receptor signalling Nature 506 2014 191 196
13. M.L. Fu, H. Herlitz, W. Schulze, G. Wallukat, P. Micke, P. Eftekhari, K.G. Sjögren, A. Hjalmarson, W. Müller-Esterl, and J. Hoebeke Autoantibodies against the angiotensin receptor (AT1) in patients with hypertension J. Hypertens. 18 2000 945 953
14. T. Halgren Merck molecular force field I-V J Comp Chem 17 1995 490 641
15. Hart, P., Boutet, S., Carini, G., Dragone, A., Duda, B., Freytag, D., Haller, G., Herbst, R., Herrmann, S., Kenney, C., et al. (2012). The Cornell-SLAC Pixel Array Detector at LCLS. In Nuclear Science Symposium, Medical Imaging Conference.
16. S. Imaizumi, S. Miura, E. Yahiro, Y. Uehara, I. Komuro, and K. Saku Class- and molecule-specific differential effects of angiotensin II type 1 receptor blockers Curr. Pharm. Des. 19 2013 3002 3008
17. I.L. Junggren, X. Zhao, X. Sun, and T. Hedner Comparative cardiovascular effects of the angiotensin II type 1 receptor antagonists ZD 7155 and losartan in the rat J. Pharm. Pharmacol. 48 1996 829 833
18. H. Kamimori, S. Unabia, W.G. Thomas, and M.I. Aguilar Evaluation of the membrane-binding properties of the proximal region of the angiotensin II receptor (AT1A) carboxyl terminus by surface plasmon resonance Anal. Sci. 21 2005 171 174
19. P.A. Karplus, and K. Diederichs Linking crystallographic model and data quality Science 336 2012 1030 1033
20. V. Katritch, G. Fenalti, E.E. Abola, B.L. Roth, V. Cherezov, and R.C. Stevens Allosteric sodium in class A GPCR signaling Trends Biochem. Sci. 39 2014 233 244
21. M.G. Keane, and R.E. Pyeritz Medical management of Marfan syndrome Circulation 117 2008 2802 2813
22. W. Liu, D. Wacker, C. Gati, G.W. Han, D. James, D. Wang, G. Nelson, U. Weierstall, V. Katritch, and A. Barty Serial femtosecond crystallography of G protein-coupled receptors Science 342 2013 1521 1524
23. W. Liu, D. Wacker, C. Wang, E. Abola, and V. Cherezov Femtosecond crystallography of membrane proteins in the lipidic cubic phase Philos. Trans. R. Soc. Lond. B Biol. Sci. 369 2014 20130314
24. W. Liu, A. Ishchenko, and V. Cherezov Preparation of microcrystals in lipidic cubic phase for serial femtosecond crystallography Nat. Protoc. 9 2014 2123 2134
25. M.A. Lomize, I.D. Pogozheva, H. Joo, H.I. Mosberg, and A.L. Lomize OPM database and PPM web server: resources for positioning of proteins in membranes Nucleic Acids Res. 40 2012 D370 D376
26. T.K. Ma, K.K. Kam, B.P. Yan, and Y.Y. Lam Renin-angiotensin-aldosterone system blockade for cardiovascular diseases: current status Br. J. Pharmacol. 160 2010 1273 1292
27. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Cryst. 40 2007 658 674
28. S. Miura, J. Zhang, J. Boros, and S.S. Karnik TM2-TM7 interaction in coupling movement of transmembrane helices to activation of the angiotensin II type-1 receptor J. Biol. Chem. 278 2003 3720 3725
29. S. Miura, Y. Kiya, T. Kanazawa, S. Imaizumi, M. Fujino, Y. Matsuo, S.S. Karnik, and K. Saku Differential bonding interactions of inverse agonists of angiotensin II type 1 receptor in stabilizing the inactive state Mol. Endocrinol. 22 2008 139 146
30. S. Miura, S.S. Karnik, and K. Saku Review: angiotensin II type 1 receptor blockers: class effects versus molecular effects J. Renin Angiotensin Aldosterone Syst. 12 2011 1 7
31. S. Miura, N. Nakao, H. Hanzawa, Y. Matsuo, K. Saku, and S.S. Karnik Reassessment of the unique mode of binding between angiotensin II type 1 receptor and their blockers PLoS ONE 8 2013 e79914
32. S. Miura, A. Okabe, Y. Matsuo, S.S. Karnik, and K. Saku Unique binding behavior of the recently approved angiotensin II receptor blocker azilsartan compared with that of candesartan Hypertens. Res. 36 2013 134 139
33. H. Mozsolits, S. Unabia, A. Ahmad, C.J. Morton, W.G. Thomas, and M.I. Aguilar Electrostatic and hydrophobic forces tether the proximal region of the angiotensin II receptor (AT1A) carboxyl terminus to anionic lipids Biochemistry 41 2002 7830 7840
34. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D Biol. Crystallogr. 53 1997 240 255
35. L. Oliveira, C.M. Costa-Neto, C.R. Nakaie, S. Schreier, S.I. Shimuta, and A.C. Paiva The angiotensin II AT1 receptor structure-activity correlations in the light of rhodopsin structure Physiol. Rev. 87 2007 565 592
36. V.S. Ramanath, J.K. Oh, T.M. Sundt 3rd, and K.A. Eagle Acute aortic syndromes and thoracic aortic aneurysm Mayo Clin. Proc. 84 2009 465 481
37. R. Ramchandran, T. Takezako, Y. Saad, L. Stull, B. Fink, H. Yamada, S. Dikalov, D.G. Harrison, C. Moravec, and S.S. Karnik Angiotensinergic stimulation of vascular endothelium in mice causes hypotension, bradycardia, and attenuated angiotensin response Proc. Natl. Acad. Sci. USA 103 2006 19087 19092
38. T. Sano, K. Ohyama, Y. Yamano, Y. Nakagomi, S. Nakazawa, M. Kikyo, H. Shirai, J.S. Blank, J.H. Exton, and T. Inagami A domain for G protein coupling in carboxyl-terminal tail of rat angiotensin II receptor type 1A J. Biol. Chem. 272 1997 23631 23636
39. S.K. Shenoy, and R.J. Lefkowitz Angiotensin II-stimulated signaling through G proteins and beta-arrestin Sci. STKE 2005 2005 cm14
40. T. Takezako, C. Gogonea, Y. Saad, K. Noda, and S.S. Karnik "Network leaning" as a mechanism of insurmountable antagonism of the angiotensin II type 1 receptor by non-peptide antagonists J. Biol. Chem. 279 2004 15248 15257
41. Q. Tan, Y. Zhu, J. Li, Z. Chen, G.W. Han, I. Kufareva, T. Li, L. Ma, G. Fenalti, and J. Li Structure of the CCR5 chemokine receptor-HIV entry inhibitor maraviroc complex Science 341 2013 1387 1390
42. W.G. Thomas, K.M. Baker, T.J. Motel, and T.J. Thekkumkara Angiotensin II receptor endocytosis involves two distinct regions of the cytoplasmic tail. A role for residues on the hydrophobic face of a putative amphipathic helix J. Biol. Chem. 270 1995 22153 22159
43. W.G. Thomas, L. Pipolo, and H. Qian Identification of a Ca2+/calmodulin-binding domain within the carboxyl-terminus of the angiotensin II (AT1A) receptor FEBS Lett. 455 1999 367 371
44. A.A. Thompson, W. Liu, E. Chun, V. Katritch, H. Wu, E. Vardy, X.P. Huang, C. Trapella, R. Guerrini, and G. Calo Structure of the nociceptin/orphanin FQ receptor in complex with a peptide mimetic Nature 485 2012 395 399
45. M. Totrov, and R. Abagyan Flexible protein-ligand docking by global energy optimization in internal coordinates Proteins 1997 215 220
46. H. Unal, and S.S. Karnik Constitutive activity in the angiotensin II type 1 receptor: discovery and applications Adv. Pharmacol. 70 2014 155 174
47. H. Unal, R. Jagannathan, M.B. Bhat, and S.S. Karnik Ligand-specific conformation of extracellular loop-2 in the angiotensin II type 1 receptor J. Biol. Chem. 285 2010 16341 16350
48. H. Unal, R. Jagannathan, and S.S. Karnik Mechanism of GPCR-directed autoantibodies in diseases Adv. Exp. Med. Biol. 749 2012 187 199
49. U. Weierstall, D. James, C. Wang, T.A. White, D. Wang, W. Liu, J.C. Spence, R. Bruce Doak, G. Nelson, and P. Fromme Lipidic cubic phase injector facilitates membrane protein serial femtosecond crystallography Nat. Commun. 5 2014 3309
50. E.J. Whalen, S. Rajagopal, and R.J. Lefkowitz Therapeutic potential of β-arrestin- and G protein-biased agonists Trends Mol. Med. 17 2011 126 139
51. T.A. White, R.A. Kirian, A.V. Martin, A. Aquila, K. Nass, A. Barty, and H.N. Chapman CrystFEL: a software suite for snapshot serial crystallography J. Appl. Cryst. 45 2012 335 341
52. J.W. Wisler, K. Xiao, A.R. Thomsen, and R.J. Lefkowitz Recent developments in biased agonism Curr. Opin. Cell Biol. 27 2014 18 24
53. B. Wu, E.Y. Chien, C.D. Mol, G. Fenalti, W. Liu, V. Katritch, R. Abagyan, A. Brooun, P. Wells, and F.C. Bi Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists Science 330 2010 1066 1071
54. H. Wu, D. Wacker, M. Mileni, V. Katritch, G.W. Han, E. Vardy, W. Liu, A.A. Thompson, X.P. Huang, and F.I. Carroll Structure of the human κ-opioid receptor in complex with JDTic Nature 485 2012 327 332
55. Y. Xia, and R.E. Kellems Angiotensin receptor agonistic autoantibodies and hypertension: preeclampsia and beyond Circ. Res. 113 2013 78 87
56. M.A. Zaman, S. Oparil, and D.A. Calhoun Drugs targeting the renin-angiotensin-aldosterone system Nat. Rev. Drug Discov. 1 2002 621 636
57. C.C. Zhou, Y. Zhang, R.A. Irani, H. Zhang, T. Mi, E.J. Popek, M.J. Hicks, S.M. Ramin, R.E. Kellems, and Y. Xia Angiotensin receptor agonistic autoantibodies induce pre-eclampsia in pregnant mice Nat. Med. 14 2008 855 862
58. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, and R.W. Grosse-Kunstleve PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
59. T.N. Bhat Calculation of an Omit Map J. Appl. Cryst. 21 1988 279 281
60. S. Boutet, and G.J. Williams The Coherent X-ray Imaging (CXI) instrument at the Linac Coherent Light Source (LCLS) New J. Phys. 12 2010 035024
61. B.D. Bursulaya, M. Totrov, R. Abagyan, and C.L. Brooks 3rd Comparative study of several algorithms for flexible ligand docking J. Comput. Aided Mol. Des. 17 2003 755 763
62. V.B. Chen, W.B. Arendall 3rd, J.J. Headd, D.A. Keedy, R.M. Immormino, G.J. Kapral, L.W. Murray, J.S. Richardson, and D.C. Richardson MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr. D Biol. Crystallogr. 66 2010 12 21
63. M. Schapira, M. Totrov, and R. Abagyan Prediction of the binding energy for small molecules, peptides and proteins J. Mol. Recognit. 12 1999 177 190
64. F.Y. Siu, M. He, C. de Graaf, G.W. Han, D. Yang, Z. Zhang, C. Zhou, Q. Xu, D. Wacker, J.S. Joseph, W. Liu, J. Lau, V. Cherezov, V. Katritch, M.W. Wang, and R.C. Stevens Structure of the human glucagon class B G-protein-coupled receptor Nature 499 2013 444 449
65. J. Söding, A. Biegert, and A.N. Lupas The HHpred interactive server for protein homology detection and structure prediction Nucleic Acids Res. 33 2005 W244 W248
66. H. Unal, R. Jagannathan, A. Bhatnagar, K. Tirupula, R. Desnoyer, and S.S. Karnik Long range effect of mutations on specific conformational changes in the extracellular loop 2 of angiotensin II type 1 receptor J. Biol. Chem. 288 2013 540 551
67. T.A. White, A. Barty, F. Stellato, J.M. Holton, R.A. Kirian, N.A. Zatsepin, and H.N. Chapman Crystallographic data processing for free-electron laser sources Acta Crystallogr. D Biol. Crystallogr. 69 2013 1231 1240