Recent progress in the study of G protein-coupled receptors with molecular dynamics computer simulations

Biochimica et Biophysica Acta - Biomembranes

Volumn 1808, Issue 7, 2011, Pages 1868-1878

  Grossfield, Alan ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Convergence; G protein coupled receptor; Hydration; Lipid protein interactions; Molecular dynamics; Oligomerization

Indexed keywords

G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; OMEGA 3 FATTY ACID; RHODOPSIN; SCHIFF BASE;

ARTICLE; COMPUTER SIMULATION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; HUMAN; HYDRATION; ISOMERIZATION; LIGAND BINDING; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN PROTEIN INTERACTION; STRUCTURE ANALYSIS;

BIOPOLYMERS; COMPUTER SIMULATION; LIPIDS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; RECEPTORS, G-PROTEIN-COUPLED; SCHIFF BASES;

EID: 79955811328     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.03.010     Document Type: Review

References (131)

1. K. Lundstrom Latest development in drug discovery on G protein-coupled receptors Curr. Protein Pept. Sci. 7 2006 465 470 (Pubitemid 44524494)
2. J.P. Overington, B. Al-Lazikani, and A.L. Hopkins How many drug targets are there? Nat. Rev. Drug Discov. 5 2006 993 996 (Pubitemid 44835126)
3. R. Heilker, M. Wolff, C.S. Tautermann, and M. Bieler G-protein-coupled receptor- focused drug discovery using a target class platform approach Drug Discov. Today 14 2009 231 240
4. K. Palczewski, T. Kumasaka, T. Hori, C.A. Behnke, H. Motoshima, B.J. Fox, Trong Le, D.C. Teller, T. Okada, R.E. Stenkamp, M. Yamamoto, and M. Miyano Crystal structure of rhodopsin: a G protein-coupled receptor Science 289 2000 739 745 (Pubitemid 30650186)
5. T. Okada, Y. Fujiyoshi, M. Silow, J. Navarro, E.M. Landau, and Y. Shichida Functional role of internal water molecules in rhodopsin revealed by X-ray crystallography Proc. Natl Acad. Sci. U.S.A. 99 2002 5982 5987 (Pubitemid 34493251)
6. P.C. Edwards, J. Li, M. Burghammer, J.H. McDowell, C. Villa, P.A. Hargrave, and G.F.X. Schertler Crystals of native and modified bovine rhodopsins and their heavy atom derivatives J. Mol. Biol. 343 2004 1439 1450 (Pubitemid 39387835)
7. J. Li, P.C. Edwards, M. Burghammer, C. Villa, and G.F.X. Schertler Structure of bovine rhodopsin in a trigonal crystal form J. Mol. Biol. 343 2004 1409 1438 (Pubitemid 39387834)
8. T. Okada, M. Sugihara, A.N. Bondar, M. Elstner, P. Entel, and V. Buss The retinal conformation and its environment in rhodopsin in light of a new 2.2 angstrom crystal structure. J. Mol. Biol. 342 2004 571 583 (Pubitemid 39149759)
9. V. Cherezov, D.M. Rosenbaum, M.A. Hanson, S.G.F. Rasmussen, F.S. Thian, T.S. Kobilka, H.-J. Choi, P. Kuhn, W.I. Weis, B.K. Kobilka, and R.C. Stevens High- resolution crystal structure of an engineered human beta2-adrenergic G protein- coupled receptor Science 318 2007 1258 1265 (Pubitemid 350172884)
10. D.M. Rosenbaum, V. Cherezov, M.A. Hanson, S.G.F. Rasmussen, F.S. Thian, T.S. Kobilka, H.-J. Choi, X.-J. Yao, W.I. Weis, R.C. Stevens, and B.K. Kobilka GPCR engineering yields high-resolution structural insights into beta2- adrenergic receptor function Science 318 2007 1266 1273 (Pubitemid 350172885)
11. S.G.F. Rasmussen, H.-J. Choi, D.M. Rosenbaum, T.S. Kobilka, F.S. Thian, P.C. Edwards, M. Burghammer, V.R.P. Ratnala, R. Sanishvili, R.F. Fischetti, G.F.X. Schertler, W.I. Weis, and B.K. Kobilka Crystal structure of the human beta2 adrenergic g-protein-coupled receptor Nature 450 2007 383 387 (Pubitemid 350126755)
12. V.-P. Jaakola, M.T. Griffith, M.A. Hanson, V. Cherezov, E.Y.T. Chien, J.R. Lane, A.P. IJzerman, and R.C. Stevens The 2.6 angstrom crystal structure of a human A2A adenosine receptor bound to an antagonist Science 322 2008 1211 1217
13. T. Warne, M.J. Serrano-Vega, J.G. Baker, R. Moukhametzianov, P.C. Edwards, R. Henderson, A.G.W. Leslie, C.G. Tate, and G.F.X. Schertler Structure of a beta1-adrenergic G-protein-coupled receptor Nature 454 2008 486 491
14. P. Scheerer, J.H. Park, P.W. Hildebrand, Y.J. Kim, N. Krauss, H.-W. Choe, K.P. Hofmann, and O.P. Ernst Crystal structure of opsin in its G-protein-interacting conformation Nature 455 2008 497 502
15. J.H. Park, P. Scheerer, K.P. Hofmann, H.-W. Choe, and O.P. Ernst Crystal structure of the ligand-free G-protein-coupled receptor opsin Nature 454 2008 183 187 (Pubitemid 351969893)
16. D. Salom, D.T. Lodowski, R.E. Stenkamp, I.L. Trong, M. Golczak, B. Jastrzebska, T. Harris, J.A. Ballesteros, and K. Palczewski Crystal structure of a photoactivated deprotonated intermediate of rhodopsin Proc. Natl Acad. Sci. U.S.A. 103 2006 16123 16128 (Pubitemid 44715162)
17. E.Y.T. Chien, W. Liu, Q. Zhao, V. Katritch, G.W. Han, M.A. Hanson, L. Shi, A.H. Newman, J.A. Javitch, V. Cherezov, and R.C. Stevens Structure of the human dopamine d3 receptor in complex with a d2/d3 selective antagonist Science 330 2010 1091 1095
18. B. Wu, E.Y.T. Chien, C.D. Mol, G. Fenalti, W. Liu, V. Katritch, R. Abagyan, A. Brooun, P. Wells, F.C. Bi, D.J. Hamel, P. Kuhn, T.M. Handel, V. Cherezov, and R.C. Stevens Structures of the cxcr4 chemokine gpcr with small-molecule and cyclic peptide antagonists Science 330 2010 1066 1071
19. B.K. Kobilka, and X. Deupi Conformational complexity of G-protein-coupled receptors Trends Pharmacol. Sci. 28 2007 397 406 (Pubitemid 47087966)
20. B. Kobilka, and G.F.X. Schertler New G-protein-coupled receptor crystal structures: insights and limitations Trends Pharmacol. Sci. 29 2008 79 83
21. S. Topiol, and M. Sabio X-ray structure breakthroughs in the GPCR transmembrane region Biochem. Pharmacol. 78 2009 11 20
22. F. Fanelli, and P.G. De Benedetti Computational modeling approaches to structure-function analysis of G protein-coupled receptors Chem. Rev. 105 2005 3297 3351 (Pubitemid 41430812)
23. B. Alberts, D. Bray, J. Lewis, M. Raff, K. Roberts, and J.D. Watson Molecular Biology of the Cell third edition 1994 Garland Publishing Inc, New York
24. J.A. Ballesteros, and H. Weinstein Analysis and refinement of criteria for predicting the structure and relative orientations of transmembranal helical domains Biophys. J. 62 1992 107 109
25. G. Wald, and A.B. Clark Visual adaptation and chemistry of the rods J. Gen. Physiol. 21 1937 93 105
26. F. Boll Arch. Anat. Physiol. Physiol. Abstr. 4 1877 4 35
27. W.L. Hubbell, C. Altenbach, C.M. Hubbell, and H.G. Khorana Rhodopsin structure, dynamics, and activation: a perspective from crystallography, site-directed spin labeling, sulfhydryl reactivity, and disulfide cross-linking Adv. Protein Chem. 63 2003 243 290 (Pubitemid 36268430)
28. T.P. Sakmar, S.T. Menon, E.P. Marin, and E.S. Awad Rhodopsin: insights from recent structural studies Annu. Rev. Biophys. Biomol. Struct. 31 2002 443 484 (Pubitemid 34666841)
29. P.A. Baldwin, and W.L. Hubbell Effects of lipid environment on the light-induced conformational changes of rhodopsin: 2. Roles of lipid chain length, unsaturation, and phase state Biochemistry 24 1985 2633 2639 (Pubitemid 15015995)
30. N.J. Gibson, and M.F. Brown Lipid headgroup and acyl chain composition modulate the MI-MII equilibrium of rhodopsin in recombinant membranes Biochem. 32 1993 2438 2454 (Pubitemid 23094909)
31. M.F. Brown Modulation of rhodopsin function by properties of the membrane bilayer Chem. Phys. Lipids 73 1994 159 180 (Pubitemid 24299194)
32. M.F. Brown Influence of non-lamellar-forming lipids on rhodopsin Curr. Top. Membr. 44 1997 285 356
33. M.F. Brown Influence of nonlamellar-forming lipids on rhodopsin Lipid polymorphism and membrane Current Topics In Membranes 44 1997 285 356
34. K. Boesze-Battaglia, and A.D. Albert Fatty acid composition of bovine rod outer segment plasma membrane Exp. Eye Res. 49 1989 699 701 (Pubitemid 19264429)
35. W.L. Stone, C.C. Farnsworth, and E.A. Dratz A reinvestigation of the fatty acid content of bovine, rat and frog retinal outer segments Exp. Eye Res. 28 1979 387 397 (Pubitemid 9155105)
36. K. Boesze-Battaglia, T. Hennessey, and A.D. Albert Cholesterol heterogeneity in bovine rod outer segment disk membranes J. Biol. Chem. 264 1989 8151 8155 (Pubitemid 19137301)
37. S.E. Feller, and K. Gawrisch Properties of docosahexaenoic acid-containing lipids and their influence on the function of the GPCR rhodopsin Curr. Opin. Struct. Bio. 15 2005 416 422 (Pubitemid 41073832)
38. S.E. Feller, K. Gawrisch, and T.B. Woolf Rhodopsin exhibits a preference for solvation by polyunsaturated docosohexaenoic acid J. Am. Chem. Soc. 125 2003 4434 4435 (Pubitemid 36418686)
39. M.C. Pitman, A. Grossfield, F. Suits, and S.E. Feller Role of cholesterol and polyun- saturated chains in lipid-protein interactions: molecular dynamics simulation of rhodopsin in a realistic membrane environment J. Am. Chem. Soc. 127 2005 4576 4577 (Pubitemid 40489605)
40. A. Grossfield, S.E. Feller, and M.C. Pitman A role for direct interactions in the modulation of rhodopsin by omega-3 polyunsaturated lipids Proc. Natl Acad. Sci. U.S.A. 103 2006 4888 4893
41. O. Soubias, and K. Gawrisch Probing specific lipid-protein interaction by saturation transfer difference NMR spectroscopy J. Am. Chem. Soc. 127 2005 13110 13111 (Pubitemid 41377578)
42. A. Grossfield, S.E. Feller, and M.C. Pitman Contribution of omega-3 fatty acids to the thermodynamics of membrane protein solvation J. Phys. Chem. B 110 2006 8907 8909 (Pubitemid 43828975)
43. G. Khelashvili, A. Grossfield, S.E. Feller, M.C. Pitman, and H. Weinstein Structural and dynamic effects of cholesterol at preferred sites of interaction with rhodopsin identified from microsecond length molecular dynamics simulations Proteins 76 2009 403 417
44. I.D. Alves, G.F.J. Salgado, Z. Salamon, M.F. Brown, G. Tollin, and V.J. Hruby Phosphatidylethanolamine enhances rhodopsin photoactivation and transducin binding in a solid supported lipid bilayer as determined using plasmon-waveguide resonance spectroscopy Biophys. J. 88 2005 198 210 (Pubitemid 40070669)
45. O. Soubias, S.-L. Niu, D.C. Mitchell, and K. Gawrisch Lipid-rhodopsin hydrophobic mismatch alters rhodopsin helical content J. Am. Chem. Soc. 2008
46. P. H. Reggio, Drug addiction: from basic research to therapy, Springer, pp. 41-68.
47. B. Jastrzebska, T. Maeda, L. Zhu, D. Fotiadis, S. Filipek, A. Engel, R.E. Stenkamp, and K. Palczewski Functional characterization of rhodopsin monomers and dimers in detergents J. Biol. Chem. 279 2004 54663 54675 (Pubitemid 40053210)
48. P. Kota, P.J. Reeves, U.L. Rajbhandary, and H.G. Khorana Opsin is present as dimers in COS1 cells: identification of amino acids at the dimeric interface Proc. Natl Acad. Sci. U.S.A. 103 2006 3054 3059 (Pubitemid 43346423)
49. S.E. Mansoor, K. Palczewski, and D.L. Farrens Rhodopsin self-associates in asolectin liposomes Proc. Natl Acad. Sci. U.S.A. 103 2006 3060 3065 (Pubitemid 43346424)
50. M. Chabre, R. Cone, and H. Saibil Is rhodopsin dimeric in native retinal rods? Nature 426 2003 30 31 (Pubitemid 37432531)
51. D. Fotiadis, Y. Liang, S. Filipek, D.A. Saperstein, A. Engel, and K. Palczewski Rhodopsin dimers in native disc membranes Nature 421 2003 127 128 (Pubitemid 36090969)
52. D. Fotiadis, Y. Liang, S. Filipek, D.A. Saperstein, A. Engel, and K. Palczewski Is rhodopsin dimeric in native retinal rods? (reply) Nature 426 2003 31 (Pubitemid 37432532)
53. S. Filipek Organization of rhodopsin molecules in native membranes of rod cells-an old theoretical model compared to new experimental data J. Mol. Model Online 11 2005 385 391 (Pubitemid 41644674)
54. M. Filizola, and H. Weinstein The study of G-protein coupled receptor oligomerization with computational modeling and bioinformatics FEBS J. 272 2005 2926 2938 (Pubitemid 40904681)
55. M. Filizola, O. Olmea, and H. Weinstein Prediction of heterodimerization interfaces of G-protein coupled receptors with a new subtractive correlated mutation method Protein Eng. 15 2002 881 885 (Pubitemid 36172725)
56. X. Periole, T. Huber, S.-J. Marrink, and T.P. Sakmar G protein-coupled receptors self-assemble in dynamics simulations of model bilayers J. Am. Chem. Soc. 129 2007 10126 10132 (Pubitemid 47312953)
57. A.V. Botelho, T. Huber, T.P. Sakmar, and M.F. Brown Curvature and hydrophobic forces drive oligomerization and modulate activity of rhodopsin in membranes Biophys. J. 91 2006 4464 4477 (Pubitemid 44911035)
58. N.W. Downer Cross-linking of dark-adapted frog photoreceptor disk membranes. evidence for monomeric rhodopsin. Biophys. J. 47 1985 285 293 (Pubitemid 15139371)
59. R.A. Cone Rotational diffusion of rhodopsin in the visual receptor membrane Nat. New Biol. 236 1972 39 43
60. T.C. Edrington, M. Bennett, and A.D. Albert Calorimetric studies of bovine rod outer segment disk membranes support a monomeric unit for both rhodopsin and opsin Biophys. J. 95 2008 2859 2866
61. M. Chabre, and M. le Maire Monomeric G-protein-coupled receptor as a functional unit Biochemistry 44 2005 9395 9403 (Pubitemid 40962038)
62. T.H. Bayburt, A.J. Leitz, G. Xie, D.D. Oprian, and S.G. Sligar Transducin activation by nanoscale lipid bilayers containing one and two rhodopsins J. Biol. Chem. 282 2007 14875 14881 (Pubitemid 47093370)
63. O.P. Ernst, V. Gramse, M. Kolbe, K.P. Hofmann, and M. Heck Monomeric gprotein-coupled receptor rhodopsin in solution activates its g protein transducin at the diffusion limit Proc. Natl Acad. Sci. U.S.A. 104 2007 10859 10864 (Pubitemid 47175191)
64. S. Banerjee, T. Huber, and T.P. Sakmar Rapid incorporation of functional rhodopsin into nanoscale apolipoprotein bound bilayer (nabb) particles J. Mol. Biol. 377 2008 1067 1081
65. M.R. Whorton, M.P. Bokoch, S.G.F. Rasmussen, B. Huang, R.N. Zare, B. Kobilka, and R.K. Sunahara A monomeric g protein-coupled receptor isolated in a high-density lipoprotein particle efficiently activates its g protein Proc. Natl Acad. Sci. U.S.A. 104 2007 7682 7687 (Pubitemid 47185966)
66. M.R. Whorton, B. Jastrzebska, P.S.-H. Park, D. Fotiadis, A. Engel, K. Palczewski, and R.K. Sunahara Efficient coupling of transducin to monomeric rhodopsin in a phospholipid bilayer J. Biol. Chem. 283 2008 4387 4394
67. A. Grossfield, M.C. Pitman, S.E. Feller, O. Soubias, and K. Gawrisch Internal hydration increases during activation of the G-protein-coupled receptor rhodopsin J. Mol. Biol. 381 2008 478 486
68. T.D. Romo, A. Grossfield, and M.C. Pitman Concerted interconversion between ionic lock substates of the beta(2) adrenergic receptor revealed by microsecond timescale molecular dynamics Biophys. J. 98 2010 76 84
69. R.O. Dror, D.H. Arlow, D.W. Borhani, M. Jensen, S. Piana, and D.E. Shaw Identification of two distinct inactive conformations of the beta2-adrenergic receptor reconciles structural and biochemical observations Proc. Natl Acad. Sci. U.S.A. 106 2009 4689 4694
70. J.L. Klepeis, K. Lindorff-Larsen, R.O. Dror, and D.E. Shaw Long-timescale molecular dynamics simulations of protein structure and function Curr. Opin. Struct. Biol. 19 2009 120 127
71. E. Lyman, C. Higgs, B. Kim, D. Lupyan, J.C. Shelley, R. Farid, and G.A. Voth A role for a specific cholesterol interaction in stabilizing the apo configuration of the human A(2A) adenosine receptor Structure 17 2009 1660 1668
72. A. Grossfield, S.E. Feller, and M.C. Pitman Convergence of molecular dynamics simulations of membrane proteins Proteins 67 2007 31 40 (Pubitemid 46340124)
73. A. Grossfield, and D.M. Zuckerman Quantifying uncertainty and sampling quality in biomolecular simulations Annu. Rep. Comput. Chem. 5 2009 23 48
74. T.D. Romo, and A. Grossfield Validating and improving elastic network models with molecular dynamics simulations Proteins 79 2011 23 34
75. M. Filizola, and H. Weinstein Structural models for dimerization of G-protein coupled receptors: the opioid receptor homodimers Biopolymers 66 2002 317 325 (Pubitemid 36222409)
76. W. Guo, L. Shi, M. Filizola, H. Weinstein, and J.A. Javitch Crosstalk in G protein- coupled receptors: changes at the transmembrane homodimer interface determine activation Proc. Natl Acad. Sci. U.S.A. 102 2005 17495 17500 (Pubitemid 41740894)
77. M. Filizola, S.X. Wang, and H. Weinstein Dynamic models of G-protein coupled receptor dimers: indications of asymmetry in the rhodopsin dimer from molecular dynamics simulations in a popc bilayer J. Comput. Aided Mol. Des. 20 2006 405 416 (Pubitemid 44823879)
78. A. Bruno, A.E. Guadix, and G. Costantino Molecular dynamics simulation of the heterodimeric mGluR2/5HT2A complex. an atomistic resolution study of a potential new target in psychiatric conditions J. Chem. Inf. Model. 49 2009 1602 1616
79. P.S.-H. Park, D.T. Lodowski, and K. Palczewski Activation of G protein-coupled receptors: beyond two-state models and tertiary conformational changes Annu. Rev. Pharmacol. Toxicol. 48 2008 107 141 (Pubitemid 351738151)
80. J. Saam, E. Tajkhorshid, S. Hayashi, and K. Schulten Molecular dynamics investigation of primary photoinduced events in the activation of rhodopsin Biophys. J. 83 2002 3097 3112 (Pubitemid 36050036)
81. B. Borhan, M.L. Souto, H. Imai, Y. Shichida, and K. Nakanishi Movement of retinal along the visual transduction path Science 288 2000 2209 2212 (Pubitemid 30429605)
82. V. Lemaître, P. Yeagle, and A. Watts Molecular dynamics simulations of retinal in rhodopsin: from the dark-adapted state towards lumirhodopsin Biochemistry 44 2005 12667 12680 (Pubitemid 41377307)
83. P.S. Crozier, M.J. Stevens, and T.B. Woolf How a small change in retinal leads to G-protein activation: initial events suggested by molecular dynamics calculations Proteins: Struct., Funct., Bioinf. 66 2007 559 574 (Pubitemid 46106761)
84. V. Hornak, S. Ahuja, M. Eilers, J.A. Goncalves, M. Sheves, P.J. Reeves, and S.O. Smith Light activation of rhodopsin: insights from molecular dynamics simulations guided by solid-state nmr distance restraints J. Mol. Biol. 396 2010 510 527
85. E.C.Y. Yan, M.A. Kazmi, Z. Ganim, J.-M. Hou, D. Pan, B.S.W. Chang, T.P. Sakmar, and R.A. Mathies Retinal counterion switch in the photoactivation of the G protein-coupled receptor rhodopsin Proc. Natl Acad. Sci. U.S.A. 100 2003 9262 9267 (Pubitemid 37033917)
86. S. Lüdeke, M. Beck, E.C.Y. Yan, T.P. Sakmar, F. Siebert, and R. Vogel The role of glu181 in the photoactivation of rhodopsin J. Mol. Biol. 353 2005 345 356 (Pubitemid 41356617)
87. U.F. Röhrig, L. Guidoni, and U. Rothlisberger Early steps of the intramolecular signal transduction in rhodopsin explored by molecular dynamics simulations Biochemistry 41 2002 10799 10809 (Pubitemid 34971057)
88. U.F. Röhrig, L. Guidoni, A. Laio, I. Frank, and U. Rothlisberger A molecular spring for vision J. Am. Chem. Soc. 126 2004 15328 15329 (Pubitemid 39577437)
89. U.F. Röhrig, and D. Sebastiani Nmr chemical shifts of the rhodopsin chromophore in the dark state and in bathorhodopsin: a hybrid qm/mm molecular dynamics study J. Phys. Chem. B 112 2008 1267 1274 (Pubitemid 351257494)
90. F. Allen, G. Almasi, W. Andreoni, D. Beece, B.J. Berne, A. Bright, J. Brunheroto, C. Cascaval, J. Castanos, P. Coteus, P. Crumley, A. Curioni, M. Denneau, W. Donath, M. Eleftheriou, B. Fitch, B. Fleisher, C.J. Georgiou, R. Germain, M. Giampapa, D. Gresh, M. Gupta, R. Haring, H. Ho, P. Hochschild, S. Hummel, T. Jonas, D. Lieber, G. Martyna, K. Maturu, J. Moreira, D. Newns, M. Newton, R. Philhower, T. Picunko, J. Pitera, M. Pitman, R. Rand, A. Royyuru, V. Salapura, A. Sanomiya, R. Shah, Y. Sham, S. Singh, M. Snir, F. Suits, R. Swetz, W.C. Swope, N. Vishnumurthy, T.J.C. Ward, H. Warren, and R. Zhou Blue Gene: A vision for protein science using a petaflop supercomputer IBM Syst. J. 40 2001 310
91. B.G. Fitch, R.S. Germain, M. Mendell, J. Pitera, M. Pitman, A. Rayshubskiy, Y. Sham, F. Suits, W.C. Swope, T.J.C. Ward, Y. Zhestkov, and R. Zhou Blue Matter, an application framework for molecular simulation on Blue Gene J. Para. Distrib. Comp. 63 2003 759 773 (Pubitemid 37268365)
92. K. Martínez-Mayorga, M.C. Pitman, A. Grossfield, S.E. Feller, and M.F. Brown Retinal counterion switch mechanism in vision evaluated by molecular simulations J. Am. Chem. Soc. 128 2006 16502 16503 (Pubitemid 46032720)
93. G.F.J. Salgado, A.V. Struts, K. Tanaka, S. Krane, K. Nakanishi, and M.F. Brown Solid-state 2 H NMR structure of retinal in metarhodopsini J. Am. Chem. Soc. 128 2006 11067 11071 (Pubitemid 44300115)
94. M.F. Brown, M.P. Heyn, C. Job, S. Kim, S. Moltke, K. Nakanishi, A.A. Nevzorov, A.V. Struts, G.F.J. Salgado, and I. Wallat Solid-state 2H NMR spectroscopy of retinal proteins in aligned membranes Biochim. Biophys. Acta 1768 2007 2979 3000 (Pubitemid 350236102)
95. A.A. Nevzorov, S. Moltke, M.P. Heyn, and M.F. Brown Solid-state NMR line shapes of uniaxially oriented immobile systems J. Am. Chem. Soc. 121 1999 7636 7643
96. P.-W. Lau, A. Grossfield, S.E. Feller, M.C. Pitman, and M.F. Brown Dynamic structure of retinylidene ligand of rhodopsin probed by molecular simulations J. Mol. Biol. 372 2007 906 917 (Pubitemid 47371253)
97. D.P. Hurst, A. Grossfield, D.L. Lynch, S. Feller, T.D. Romo, K. Gawrisch, M.C. Pitman, and P.H. Reggio A lipid pathway for ligand binding is necessary for a cannabinoid G protein-coupled receptor J. Biol. Chem. 285 2010 17954 17964
98. D.C. Mitchell, and B.J. Litman Effect of ethanol on metarhodopsin II formation is potentiated by phospholipid polyunsaturation Biochemistry 33 1994 12752 12756 (Pubitemid 24352863)
99. D.C. Mitchell, J.T. Lawrence, and B.J. Litman Primary alcohols modulate the activation of the G protein-coupled receptor rhodopsin by a lipid-mediated mechanism J. Biol. Chem. 271 1996 19033 19036 (Pubitemid 26271559)
100. D.C. Mitchell, and B.J. Litman Effect of protein hydration on receptor conformation: decreased levels of bound water promote metarhodopsin II formation Biochemistry 38 1999 7617 7623
101. D.C. Mitchell, and B.J. Litman Effect of ethanol and osmotic stress on receptor conformation. reduced water activity amplifies the effect of ethanol on metarhodopsin II formation. J. Biol. Chem. 275 2000 5355 5360 (Pubitemid 30115165)
102. L. Pardo, X. Deupi, N. Dölker, M.L. López-Rodríguez, and M. Campillo The role of internal water molecules in the structure and function of the rhodopsin family of G protein-coupled receptors Chembiochem 8 2006 19 24 (Pubitemid 46121564)
103. T.E. Angel, M.R. Chance, and K. Palczewski Conserved waters mediate structural and functional activation of family a (rhodopsin-like) G protein-coupled receptors Proc. Natl Acad. Sci. U.S.A. 106 2009 8555 8560
104. T.E. Angel, S. Gupta, B. Jastrzebska, K. Palczewski, and M.R. Chance Structural waters define a functional channel mediating activation of the GPCR, rhodopsin Proc. Natl. Acad. Sci. USA 106 2009 14367 14372
105. T. Orban, S. Gupta, K. Palczewski, and M.R. Chance Visualizing water molecules in transmembrane proteins using radiolytic labeling methods Biochemistry 49 2010 827 834
106. K. Gawrisch, personal, communication, 2011.
107. E. Jardó n-Valadez, A.-N. Bondar, and D.J. Tobias Dynamics of the internal water molecules in squid rhodopsin Biophy. J. 96 2009 2572 2576
108. 2-adrenergic receptor J. Phys. Chem. B 114 2010 8374 8386
109. R. Baron, P. Setny, and J.A. McCammon Water in cavity-ligand recognition J. Am. Chem. Soc. 132 2010 12091 12097
110. F. Raimondi, M. Seeber, P.G. De Benedetti, and F. Fanelli Mechanisms of inter- and intramolecular communication in gpcrs and g proteins J. Am. Chem. Soc. 130 2008 4310 4325 (Pubitemid 351467662)
111. N.G. Sgourakis, and A.E. Garcia The membrane complex between transducin and dark-state rhodopsin exhibits large-amplitude interface dynamics on the sub- microsecond timescale: Insights from all-atom md simulations J. Mol. Biol. 398 2010 161 173
112. F. Fanelli, and D. Dell'Orco Rhodopsin activation follows precoupling with transducin: inferences from computational analysis Biochemistry 44 2005 14695 14700 (Pubitemid 41612248)
113. D. Dell'Orco, M. Seeber, and F. Fanelli Monomeric dark rhodopsin holds the molecular determinants for transducin recognition: insights from computational analysis FEBS Lett 5 581 2007 944 948 (Pubitemid 46282727)
114. T. Huber, S. Menon, and T.P. Sakmar Structural basis for ligand binding and specificity in adrenergic receptors: Implications for GPCR-targeted drug discovery Biochemistry 47 2008 11013 11023
115. S. Vanni, M. Neri, I. Tavernelli, and U. Rothlisberger Observation of "ionic lock" formation in molecular dynamics simulations of wild-type beta 1 and beta 2 adrenergic receptors Biochemistry 48 2009 4789 4797
116. J.A. Ballesteros, A.D. Jensen, G. Liapakis, S.G. Rasmussen, L. Shi, U. Gether, and J.A. Javitch Activation of the beta 2-adrenergic receptor involves disruption of an ionic lock between the cytoplasmic ends of transmembrane segments 3 and 6 J. Biol. Chem. 276 2001 29171 29177
117. D.A. Shapiro, K. Kristiansen, D.M. Weiner, W.K. Kroeze, and B.L. Roth Evidence for a model of agonist-induced activation of 5-hydroxytryptamine 2A serotonin receptors that involves the disruption of a strong ionic interaction between helices 3 and 6 J. Biol. Chem. 277 2002 11441 11449 (Pubitemid 34952912)
118. W.F. van Gunsteren, and J. Dolenc Biomolecular simulation: historical picture and future perspectives Biochem. Soc. Trans. 36 2008 11 15 (Pubitemid 351269612)
119. X. Zhang, D. Bhatt, and D.M. Zuckerman Automated sampling assessment for molecular simulations using the effective sample size J. Chem. Theory Comput. 6 2010 3048 3057
120. D.P. Hurst, A. Grossfield, D.L. Lynch, S. Feller, T.D. Romo, K. Gawrisch, M.C. Pitman, and P.H. Reggio A lipid pathway for ligand binding is necessary for a cannabinoid G protein-coupled receptor J. Biol. Chem. 2010
121. H. Flyvbjerg, and H.G. Petersen Error estimates on averages of correlated data J. Chem. Phys. 91 1989 461 466
122. B.A. Berg, and R. Harris From data to probability density without histograms Comp. Phys. Comm. 179 2008 443 448
123. J.D. Faráldo-Gomez, L.R. Forrest, M. Baaden, P.J. Bond, C. Domene, G. Patargias, J. Cutherbertson, and M.S.P. Sansom Conformational sampling and dynamics of membrane proteins from 10-nanosecond computer simulations Proteins 57 2004 783 791 (Pubitemid 39626999)
124. B. Hess Similarities between principal components of protein dynamics and random diffusion Phys. Rev. E 62 2000 8438 8448 (Pubitemid 32087906)
125. B. Hess Convergence of sampling in protein simulations Phys. Rev. E 65 2002 031910-10
126. T.D. Romo, and A. Grossfield LOOS: an extensible platform for the structural analysis of simulations Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009 2009 2332 2335
127. T.D. Romo, A. Grossfield, LOOS: A lightweight object-oriented software library, http://loos.sourceforge.net. (2010).
128. C. Chennubhotla, A.J. Rader, L.-W. Yang, and I. Bahar Elastic network models for understanding biomolecular machinery: from enzymes to supramolecular assemblies Phys. Biol. 2 2005 S173 S180
129. I. Bahar, T.R. Lezon, A. Bakan, and I. Shrivastava Normal mode analysis of biomolecular structures: functional mechanisms of membrane proteins Chem. Rev. 110 2010 1463 1497
130. A.J. Rader, G. Anderson, B. Isin, H.G. Khorana, I. Bahar, and J. Klein-Seetharam Identification of core amino acids stabilizing rhodopsin Proc. Nat. Acad. Sci. U.S.A. 101 2004 7246 7251 (Pubitemid 38638018)
131. B. Isin, A.J. Rader, H.K. Dhiman, J. Klein-Seetharaman, and I. Bahar Predisposition of the dark state of rhodopsin to functional changes in structure Proteins 65 2006 970 983 (Pubitemid 44772894)