Structure and dynamics of G-protein coupled receptors

Advances in Experimental Medicine and Biology

Volumn 796, Issue , 2014, Pages 37-54

  Vaidehi, Nagarajan ^a   Bhattacharya, Supriyo ^a   Larsen, Adrien B ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

Biogenic amines; Conformational states; Drug design; LItiCon; Multiscale method; Predictions; Thermostable mutants

Indexed keywords

ADENOSINE A2A RECEPTOR AGONIST; BETA 1 ADRENERGIC RECEPTOR; BETA 2 ADRENERGIC RECEPTOR; CHEMOKINE RECEPTOR CXCR1; CHEMOKINE RECEPTOR CXCR4; DOPAMINE 3 RECEPTOR; G PROTEIN COUPLED RECEPTOR; ISOPRENALINE; MUSCARINIC M2 RECEPTOR; MUSCARINIC M3 RECEPTOR; RHODOPSIN;

ARTICLE; CELL COMMUNICATION; CRYSTAL STRUCTURE; DRUG DESIGN; DRUG MECHANISM; DRUG RECEPTOR BINDING; HUMAN; LIGAND BINDING; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; THERMOSTABILITY; THREE DIMENSIONAL IMAGING; CONFORMATIONAL TRANSITION; FLUORESCENCE SPECTROSCOPY; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN STABILITY; STRUCTURE ACTIVITY RELATION;

HUMANS; LIGANDS; MEMBRANE PROTEINS; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, G-PROTEIN-COUPLED; THERMODYNAMICS;

EID: 84959205484     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-94-7-7423-0_3     Document Type: Article

References (92)

1. Ahuja S, Smith SO (2009) Multiple switches in G proteincoupled receptor activation. Trends Pharmacol Sci 30:494-502
2. Alexandrov AI, Mileni M, Chien EY, Hanson MA, Stevens RC (2008) Microscale fluorescent thermal stability assay for membrane proteins. Structure 16:351-359
3. Audet M, Bouvier M (2012) Restructuring G-protein coupled receptor activation. Cell 151:14-23
4. Balaraman GS, Bhattacharya S, Vaidehi N (2010) Structural insights into conformational stability of wild type and mutant beta1-adrenergic receptor. Biophys J 99:568-577
5. Ballesteros J, Weinstein J (1995) Integrated methods for modeling G-protein coupled receptors. Methods Neurosci 25:366-428
6. Bhattacharya S, Vaidehi N (2010) Computational mapping of the conformational transitions in agonist selective pathways of a G-protein coupled receptor. J Am Chem Soc 132(14):5205-5214
7. Bhattacharya S, Hall SE, Vaidehi N (2008a) Agonistinduced conformational changes in bovine rhodopsin: insight into activation of G-protein-coupled receptors. J Mol Biol 382:539-555
8. Bhattacharya S, Hall SE, Li H, Vaidehi N (2008b) Ligandstabilized conformational states of human beta(2) adrenergic receptor: insight into G-protein-coupled receptor activation. Biophys J 94(6):2027-2042
9. Bhattacharya S, Lam AR, Li H, Balaraman G, Niesen MJ, Vaidehi N (2013) Critical analysis of the successes and failures of homology models of G protein-coupled receptors. Proteins 81:729-739. doi:10.1002/prot.24195
10. Booth PJ, Curnow P (2009) Folding scene investigation: membrane proteins. Curr Opin Struct Biol 19(1):8-13
11. Bowie JU (2001) Stabilizing membrane proteins. Curr Opin Struct Biol 11:397-402
12. Bowie JU (2011) Membrane protein folding: how important are hydrogen bonds? Curr Opin Struct Biol 21:42-49
13. Cherezov V, Rosenbaum DM, Hanson MA, Rasmussen SG, Thian FS, Kobilka TS, Choi HJ, Kuhn P, Weis WI, Kobilka BK, Stevens RC (2007) High-resolution crystal structure of an engineered human beta2-adrenergic G-protein coupled receptor. Science 318: 1258-1265
14. Chien EY, Liu W, Zhao Q, Katritch V, Han GW, Hanson MA, Shi L, Newman AH, Javitch JA, Cherezov V, Stevens RC (2010) Structure of the human dopamine D3 receptor in complex with a D2/D3 selective antagonist. Science 330:1091-1095
15. Chiu ML, Tsang C, Grihalde N, MacWilliams MP (2008) Over-expression, solubilization and purification of Gprotein coupled receptors for structural biology. Comb Chem High Throughput Screen 11:439-462
16. Colombo G, Merz KM (1999) Stability and activity of mesophilic subtilisin E and its thermophilic homolog: insights from molecular dynamics simulations. J Am Chem Soc 121:6895-6903
17. Cooke RM, Koglin M, Errey JC, Marshall FH (2013) Preparation of purified GPCRs for structural studies. Biochem Soc Trans 41(1):185-190
18. Crozier PS, Stevens MJ, Woolf TB (2007) How a small change in retinal leads to G-protein activation: initial events suggested by molecular dynamics calculations. Proteins 66:559-574
19. Deupi X (2012) Quantification of structural distortions in the transmembrane helices of GPCRs. Methods Mol Biol 914:219-235
20. Doré AS, Robertson N, Errey JC, Ng I, Hollenstein K, Tehan B, Hurrell E, Bennett K, Congreve M, Magnani F, Tate CG, Weir M, Marshall FH (2011) Structure of the adenosine A2A receptor in complex with ZM241385 and xanthines XAC and caffeine. Structure 19(9):1283-1293
21. Dror RO, Arlow DH, Borhani DW, Jensen MØ, Piana S, Shaw DE (2009) Identification of two distinct inactive conformations of the beta2-adrenergic receptor reconciles structural and biochemical observations. Proc Natl Acad Sci U S A 106:4689-4694
22. Dror RO, Pan AC, Arlow DH, Borhani DW, Maragakis P, Shan Y, Xu H, Shaw DE (2011) Pathway and mechanism of drug binding to G-protein coupled receptors. Proc Natl Acad Sci U S A 108:13118-13123
23. Filizola M, Devi LA (2013) Grand opening of structureguided design for novel opioids. Trends Pharmacol Sci 34(1):6-12
24. Galandrin S, Oligny-Longpré G, Bouvier M (2007) The evasive nature of drug efficacy: implications for drug discovery. Trends Pharmacol Sci 2007(28):423-430
25. Galés C, Rebols RV, Hogue M, Trieu P, Brelt A, Hébert TE, Bouvier M (2005) Real-time monitoring of receptor and G-protein interactions in living cells. Nat Methods 2:177-184
26. Gouldson PR, Kidley NJ, Bywater RP, Psaroudakis G, Brooks HD, Diaz C, Shire D, Reynolds CA (2004) Toward the active conformations of rhodopsin and the beta2-adrenergic receptor. Proteins 56(1):67-84
27. Granier S, Kobilka B (2012) A new era of GPCR structural and chemical biology. Nat Chem Biol 8:670-673
28. Granier S, Manglik A, Kruse AC, Kobilka TS, Thian FS, Weis WI, Kobilka BK (2012) Structure of the δ-opioid receptor bound to naltrindole. Nature 485(7398):400-404
29. Grisshammer R (2009) Purification of recombinant G-protein coupled receptors. Methods Enzymol 463:631-645
30. Grossfield A, Pittman MC, Feller SE, Soubias O, Gawrisch K (2008) Internal hydration increases during activation of the G-protein-coupled receptor rhodopsin. J Mol Biol 381:478-486
31. Haga K, Kruse AC, Asada H, Yurugi-Kobayashi T, Shiroishi M, Zhang C, Weis WI, Okada T, Kobilka BK, Haga T, Kobayashi T (2012) Structure of the human M2 muscarinic acetylcholine receptor bound to an antagonist. Nature 482:547-551
32. Hall SE, Mao A, Nicolaidou V, Finelli M, Wise EL, Nedjai B, Kanjanapangka J, Harirchian P, Chen D, Selchau V, Ribeiro S, Schyler S, Pease JE, Horuk R, Vaidehi N (2009) Elucidation of binding sites of dual antagonists in the human chemokine receptors CCR2 and CCR5. Mol Pharm 75:1325-1336
33. Hamelberg D, de Oliveira CA, McCammon JA (2007) Sampling of slow diffusive conformational transitions with accelerated molecular dynamics. J Chem Phys 127(15):155102-155110
34. Hanson MA, Stevens RC (2009) Discovery of new GPCR biology: one receptor structure at a time. Structure 17(1):8-14
35. Hernandez G, Jenney FE, Adams MWW, LeMaster DM (2000) Millisecond time scale conformational flexibility in a hyperthermophile protein at ambient temperature. Proc Natl Acad Sci U S A 97:3166-3170
36. Hornak V, Ahuja S, Eilers M, Goncalves JA, Sheves M et al (2010) Light activation of rhodopsin: insights from molecular dynamics simulations guided by solid-state NMR distance restraints. J Mol Biol 396: 510-527
37. Hubbell WL, Altenbach C, Hubbell CM, Khorana HG (2003) Rhodopsin structure, dynamics, and activation: a perspective from crystallography, site directed spin labeling, sulfhydryl reactivity, and disulfide crosslinking. Adv Protein Chem 63:243-290
38. Isralewitz B, Gao M, Schulten K (2001) Steered molecular dynamics and mechanical functions of proteins. Curr Opin Struct Biol 11:224-230
39. Johnston JM, Aburi M, Provasi D, Bortolato A, Urizar E, Lambert NA, Javitch JA, Filizola M (2011) Making structural sense of dimerization interfaces of delta opioid receptor homodimers. Biochemistry 50(10):1682-1690
40. Katritch V, Cherezov V, Stevens RC (2012) Diversity and modularity of G-protein coupled receptor structures. Trends Pharmacol Sci 33:17-27
41. Kawate T, Gouaux E (2006) Fluorescence-detection size exclusion chromatography for precrystallization screening of integral membrane proteins. Structure 14:673-681
42. Kenakin T, Watson C, Muniz-Medina V, Christopoulos A, Novick S (2012) A simple method for quantifying functional selectivity and agonist bias. ACS Chem Neurosci 3:193-203
43. Khelashvili G, Grossfield A, Feller SE, Pitman MC, Weinstein H (2009) Structural and dynamic effects of cholesterol at preferred sites of interaction with rhodopsin identified from microsecond length molecular dynamics simulations. Proteins 76:403-417
44. Krishna A, Menon ST, Terry TJ, Sakmar TP (2002) Evidence that helix 8 of rhodopsin acts as a membrane-dependent conformational switch. Biochemistry 41:8298-8309
45. Kruse AC, Hu J, Pan AC, Arlow DH, Rosenbaum DM, Rosemond E, Green HF, Liu T, Chae PS, Dror RO, Shaw DE, Weis WI, Wess J, Kobilka BK (2012) Structure and dynamics of the M3 muscarinic acetylcholine receptor. Nature 482:552-556
46. Lebon G, Bennett K, Jazayeri A, Tate CG (2011a) Thermostabilization of an agonist bound conformation of the human adenosine A2A receptor. J Mol Biol 409:298-310
47. Lebon G, Warne T, Edwards PC, Bennett K, Langmead CJ, Leslie AG, Tate CG (2011b) Agonist bound adenosine A2A receptor structures reveal common features of GPCR activation. Nature 474:521-525
48. Magnani F, Shibata Y, Serrano-Vega MJ, Tate CG (2008) Co-evolving stability and conformational homogeneity of the human adenosine A2a receptor. Proc Natl Acad Sci U S A 105(31):10744-10749
49. Mailman RB, Murthy V (2010) Ligand functional selectivity advances our understanding of drug mechanisms and drug discovery. Neuropsychopharmacology 35:345-346
50. Manglik A, Kruse AC, Kobilka TS, Thian FS, Mathiesen JM, Sunahara RK, Pardo L, Weis WI, Kobilka BK, Granier S (2012) Crystal structure of the μ-opioid receptor bound to a morphinan antagonist. Nature 485(7398):321-326
51. Meinhold L, Clement D, Tehei M, Daniel R, Finney JL et al (2008) Protein dynamics and stability: the distribution of atomic fluctuations in thermophilic and mesophilic dihydrofolate reductase derived using elastic incoherent neutron scattering. Biophys J 94:4812-4818
52. Nedjai B, Li H, Stroke IL, Wise EL, Webb ML, Merritt JR, Henderson I, Klon AE, Cole AG, Horuk R, Vaidehi N, Pease JE (2011) Small-molecule chemokine mimetics suggest a molecular basis for the observation that CXCL10 and CXCL11 are allosteric ligands of CXCR3. Br J Pharmacol 166(3):912-923
53. Niesen M, Bhattacharya S, Vaidehi N (2011) Conformational selection upon ligand binding in G-protein coupled receptors. J Am Chem Soc 133(33):13197-13204
54. Niesen M, Bhattacharya S, Tate CG, Grisshammer R, Vaidehi N (2013) Thermostabilization of the "1-adrenergic receptor Correlates with Increased Entropy of the Inactive State. J Phys Chem 117(24):7283-7291
55. Nygaard R, Zou Y, Dror RO, Mildorf TJ, Arlow DH, Manglik A, Pan AC, Liu CW, Fung JJ, Bokoch MP, Thian FS, Kobilka TS, Shaw DE, Mueller L, Prosser RS, Kobilka BK (2013) The dynamic process of "2-adrenergic receptor activation. Cell 152(3):532-542
56. Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, Le Trong I, Teller DC, Okada T, Stenkamp RE, Yamamoto M, Miyano M (2000) Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289:739-745
57. Park JH, Scheerer P, Hoffman KP, Choe H-W, Ernst OP (2008) Crystal structure of the ligand-free G-protein coupled receptor opsin. Nature 454:183-187
58. Park SH, Das BB, Casagrande F, Tian Y, Nothnagel HJ, Chu M, Kiefer H, Maier K, De Angelis AA, Marassi FM, Opella SJ (2012) Structure of the chemokine receptor CXCR1 in phospholipid bilayers. Nature 491(7426):779-783
59. Provasi D, Artacho MC, Negri A, Mobarec JC, Filizola M (2011) Ligand induced modulation of the free energy landscape of the G-protein coupled receptors explored by adaptive biasing techniques. PLoS Comput Biol 7(10):e1002193
60. Rasmussen SG, DeVree BT, Zou Y, Kruse AC, Chung KY, Kobilka TS, Thian FS, Chae PS, Pardon E, Calinski D, Mathiesen JM, Shah ST, Lyons JA, Caffrey M, Gellman SH, Steyaert J, Skiniotis G, Weis WI, Sunahara RK, Kobilka BK (2011) Crystal structure of the "2-adrenergic receptor-Gs protein complex. Nature 477:549-555
61. Reiter E, Ahn S, Shukla AK, Lefkowitz RJ (2012) Molecular mechanism of "-arrestin biased agonism at seven transmembrane receptors. Ann Rev Pharmacol Toxicol 52:179-197
62. Roth CB, Hanson MA, Stevens RC (2008) Stabilization of the human beta2-adrenergic receptor TM4-TM3-TM5 helix interface by mutagenesis of Glu122(3.41), a critical residue in GPCR structure. J Mol Biol 376(5):1305-1319
63. Saam J, Tajkhorshid E, Havashi S, Schulten K (2002) Molecular dynamics investigation of primary photoinduced events in the activation of rhodopsin. Biophys J 83:3097-3112
64. Schertler GF (2005) Structure of rhodopsin and the metarhodopsin I photointermediate. Curr Opin Struct Biol 15:408-15
65. Serrano-Vega MJ, Tate CG (2009) Transferability of thermostabilizing mutations between beta adrenergic receptors. Mol Membr Biol 26:385-396
66. Serrano-Vega MJ, Magnani F, Shibata Y, Tate CG (2008) Conformational thermostabilization of the beta1-adrenergic receptor in a detergent resistant form. Proc Natl Acad Sci U S A 105(3):877-882
67. Shibata Y, White JF, Serrano-Vega MJ, Magnani F, Aloia AL, Grisshammer R, Tate CG (2009) Thermostabilization of the neurotensin receptor NTS1. J Mol Biol 2390(2):262-277
68. Shimamura T, Shiroishi M, Weyand S, Tsujimoto H, Winter G, Katritch V, Abagyan R, Cherezov V, Liu W, Han GW, Kobayashi T, Stevens RC, Iwata S (2011) Structure of the human histamine H1 receptor complex with doxepin. Nature 475:65-70
69. Stadler AM, Garvey CJ, Bocahut A, Sacquin-Mora S, Digel I et al (2012) Thermal fluctuations of haemoglobin from different species: adaptation to temperature via conformational dynamics. J R Soc Interface 9(76):2845-2855
70. Standfuss J, Xie G, Edwards PC, Burghammer M, Oprian DD, Schertler GF (2007) Crystal structure of a thermally stable rhodopsin mutant. J Mol Biol 372(5):1179-1188
71. Sterpone F, Melchionna S (2012) Thermophilic proteins: insight and perspective from in silico experiments. Chem Soc Rev 41(5):1665-1676
72. Steyaert J, Kobilka BK (2011) Nanobody stabilization of G-protein coupled receptor conformational states. Curr Opin Struct Biol 21:567-572
73. Swaminath G, Xiang Y, Lee TW, Steenhuis J, Parnot C, Kobilka BK (2004) Sequential binding of agonists to the beta2 adrenoceptor-kinetic evidence for intermediate conformational states. J Biol Chem 279:686-691
74. Swaminath G, Deupi X, Lee TW, Zhu W, Thian FS, Kobilka TS, Kobilka BK (2005) Probing the beta2 adrenoceptor binding site with catechol reveals differences in binding and activation by agonists and partial agonists. J Biol Chem 280:22165-22171
75. Tate CG (2012) A crystal clear solution for determining Gprotein coupled receptor structures. Trends Biochem Sci 37:343-352
76. Tate CG, Schertler GF (2009) Engineering G proteincoupled receptors to facilitate their structure determination. Curr Opin Struct Biol 19:386-395
77. Thompson AA, Liu W, Chun E, Katritch V, Wu H, Vardy E, Huang XP, Trapella C, Guerrini R, Calo G, Roth BL, Cherezov V, Stevens RC (2012) Structure of the nociceptin/orphanin FQ receptor in complex with a peptide mimetic. Nature 485(7398):395-399
78. Vaidehi N (2010) Dynamics and flexibility of G-protein coupled receptor conformations and their relevance to drug design. Drug Discov Today 15:951-957
79. Vaidehi N, Bhattacharya S (2011) Multiscale computational methods for mapping conformational ensembles of G-protein coupled receptors. Adv Protein Chem Struct Biol 85:253-280
80. Vaidehi N, Kenakin T (2010) The role of conformational ensembles of seven transmembrane receptors in functional selectivity. Curr Opin Pharmacol 10:775-781
81. Vilardaga JP, Bunemann M, Krasel C, Castro M, Lohse M (2003) Measurement of the millisecond activation switch of G protein-coupled receptors in living cells. Nat Biotechnol 21:807-812
82. Warne T, Serrano-Vega MJ, Baker JG, Moukhametzianov R, Edwards PC, Henderson R, Leslie AG, Tate CG, Schertler GF (2008) Structure of a beta1-adrenergic G-protein-coupled receptor. Nature 454(7203):486-491
83. Warne T, Edwards PC, Leslie AGW, Tate CG (2012) Crystal structures of a stabilized "1-adrenoceptor bound to the biased agonists bucindolol and carvedilol. Structure 20:841-849
84. White SH, Wimley WC (1999) Membrane protein folding and stability: physical principles. Annu Rev Biophys Biomol Struct 28:319-365
85. White JF, Noinaj N, Shibata Y, Love J, Kloss B, Xu F, Gvozdenovic-Jeremic J, Shah P, Shiloach J, Tate CG, Grisshammer R (2012) Structure of the agonist bound neurotensin receptor. Nature 490:508-513
86. Wintrode PL, Zhang DQ, Vaidehi N, Arnold FH, Goddard WA (2003) Protein dynamics in a family of laboratory evolved thermophilic enzymes. J Mol Biol 327:745-757
87. Wu B, Chien EY, Mol CD, Fenalti G, Liu W, Katritch V, Abagyan R, Brooun A, Wells P, Bi FC, Hamel DJ, Kuhn P, Handel TM, Cherezov V, Stevens RC (2010) Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists. Science 330(6007):1066-1071
88. Xu F, Wu H, Katritch V, Han GW, Jacobson KA, Gao ZG, Cherezov V, Stevens RC (2011) Structure of an agonist bound human A2A adenosine receptor. Science 332(6027):322-327
89. Yao X, Parnot C, Deupi X, Ratnala VRP, Swaminath G, Farrens D, Kobilka BK (2006) Coupling ligand structure to specific conformational switches in the beta2-adrenoceptor. Nat Chem Biol 2006(2):417422
90. Yao XJ, Ruiz G, Whorton MR, Rasmussen SG, De Vree BT, Deupi X, Sunahara RK, Kobilka B (2009) The effect of ligand efficacy on the formation and stability of a GPCR-G-protein complex. Proc Natl Acad Sci U S A 106:9501-9506
91. Zaitseva E, Brown MF, Vogel R (2010) Sequential rearrangement of interhelical networks upon rhodopsin activation in membranes: the Meta II(a) conformational substate. J Am Chem Soc 132:4815-4821
92. Zhang C, Srinivasan Y, Arlow DH, Fung JJ, Palmer D, Zheng Y, Green HF, Pandey A, Dror RO, Shaw DE, Weis WI, Coughlin SR, Kobilka BK (2012) High-resolution crystal structure of human proteaseactivated receptor 1. Nature 492(7429):387-392