Retinal Conformation Changes Rhodopsin's Dynamic Ensemble

Biophysical Journal

Volumn 109, Issue 3, 2015, Pages 608-617

  Leioatts, Nicholas ^a   Romo, Tod D ^a   Danial, Shairy Azmy ^a   Grossfield, Alan ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIA;

PROTEIN BINDING; RETINAL; RHODOPSIN;

ALLOSTERISM; AMINO ACID SEQUENCE; ANIMAL; BOVINE; CHEMISTRY; METABOLISM; MOLECULAR DYNAMICS; MOLECULAR GENETICS; PHOTON; PROTEIN TERTIARY STRUCTURE;

ALLOSTERIC REGULATION; AMINO ACID SEQUENCE; ANIMALS; CATTLE; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PHOTONS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RETINALDEHYDE; RHODOPSIN;

EID: 84938519689     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2015.06.046     Document Type: Article

References (80)

1. P. Mombaerts Seven-transmembrane proteins as odorant and chemosensory receptors Science 286 1999 707 711
2. S. Firestein The good taste of genomics Nature 404 2000 552 553
3. S. Granier, and B. Kobilka A new era of GPCR structural and chemical biology Nat. Chem. Biol. 8 2012 670 673
4. R. Fredriksson, and M.C. Lagerström H.B. Schiöth The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints Mol. Pharmacol. 63 2003 1256 1272
5. I. Bahar, and T.R. Lezon I.H. Shrivastava Normal mode analysis of biomolecular structures: functional mechanisms of membrane proteins Chem. Rev. 110 2010 1463 1497
6. J.P. Overington, B. Al-Lazikani, and A.L. Hopkins How many drug targets are there? Nat. Rev. Drug Discov. 5 2006 993 996
7. M.C. Lagerström, and H.B. Schiöth Structural diversity of G protein-coupled receptors and significance for drug discovery Nat. Rev. Drug Discov. 7 2008 339 357
8. K. Palczewski, and T. Kumasaka M. Miyano Crystal structure of rhodopsin: a G protein-coupled receptor Science 289 2000 739 745
9. R.J. Lefkowitz Historical review: a brief history and personal retrospective of seven-transmembrane receptors Trends Pharmacol. Sci. 25 2004 413 422
10. R. Nygaard, and T.M. Frimurer T.W. Schwartz Ligand binding and micro-switches in 7TM receptor structures Trends Pharmacol. Sci. 30 2009 249 259
11. E. Crocker, and M. Eilers S.O. Smith Location of Trp265 in metarhodopsin II: implications for the activation mechanism of the visual receptor rhodopsin J. Mol. Biol. 357 2006 163 172
12. C.E. Elling, and T.M. Frimurer T.W. Schwartz Metal ion site engineering indicates a global toggle switch model for seven-transmembrane receptor activation J. Biol. Chem. 281 2006 17337 17346
13. T.W. Schwartz, and T.M. Frimurer C.E. Elling Molecular mechanism of 7TM receptor activation - a global toggle switch model Annu. Rev. Pharmacol. Toxicol. 46 2006 481 519
14. L. Valentin-Hansen, and M. Groenen T.W. Schwartz The arginine of the DRY motif in transmembrane segment III functions as a balancing micro-switch in the activation of the β2-adrenergic receptor J. Biol. Chem. 287 2012 31973 31982
15. B. Trzaskowski, and D. Latek S. Filipek Action of molecular switches in GPCRs - theoretical and experimental studies Curr. Med. Chem. 19 2012 1090 1109
16. M. Mahalingam, and K. Martínez-Mayorga R. Vogel Two protonation switches control rhodopsin activation in membranes Proc. Natl. Acad. Sci. USA 105 2008 17795 17800
17. L. Shi, and G. Liapakis J.A. Javitch Beta2 adrenergic receptor activation. Modulation of the proline kink in transmembrane 6 by a rotamer toggle switch J. Biol. Chem. 277 2002 40989 40996
18. R.O. Dror, and D.H. Arlow D.E. Shaw Activation mechanism of the β2-adrenergic receptor Proc. Natl. Acad. Sci. USA 108 2011 18684 18689
19. N. Leioatts, and P. Suresh A. Grossfield Structure-based simulations reveal concerted dynamics of GPCR activation Proteins 82 2014 2538 2551
20. 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
21. A.W. Kahsai, and K. Xiao R.J. Lefkowitz Multiple ligand-specific conformations of the β2-adrenergic receptor Nat. Chem. Biol. 7 2011 692 700
22. R. Nygaard, and Y. Zou B.K. Kobilka The dynamic process of β(2)-adrenergic receptor activation Cell 152 2013 532 542
23. H.O. Onaran, and T. Costa Where have all the active receptor states gone? Nat. Chem. Biol. 8 2012 674 677
24. D.M. Perez, and S.S. Karnik Multiple signaling states of G-protein-coupled receptors Pharmacol. Rev. 57 2005 147 161
25. S. Bockenhauer, and A. Fürstenberg W.E. Moerner Conformational dynamics of single G protein-coupled receptors in solution J. Phys. Chem. B 115 2011 13328 13338
26. M. Zocher, and J.J. Fung D.J. Müller Ligand-specific interactions modulate kinetic, energetic, and mechanical properties of the human β2 adrenergic receptor Structure 20 2012 1391 1402
27. M. Bouvier Oligomerization of G-protein-coupled transmitter receptors Nat. Rev. Neurosci. 2 2001 274 286
28. O. Soubias, and K. Gawrisch The role of the lipid matrix for structure and function of the GPCR rhodopsin Biochim. Biophys. Acta 1818 2011 234 240
29. O. Soubias, and W.E. Teague Jr. K. Gawrisch Contribution of membrane elastic energy to rhodopsin function Biophys. J. 99 2010 817 824
30. 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
31. M.F. Brown Modulation of rhodopsin function by properties of the membrane bilayer Chem. Phys. Lipids 73 1994 159 180
32. S. Lüdeke, and M. Beck R. Vogel The role of Glu181 in the photoactivation of rhodopsin J. Mol. Biol. 353 2005 345 356
33. R. Vogel, and F. Siebert M. Sheves Modulating rhodopsin receptor activation by altering the pKa of the retinal Schiff base J. Am. Chem. Soc. 128 2006 10503 10512
34. K. Sato, and T. Morizumi Y. Shichida Direct observation of the pH-dependent equilibrium between metarhodopsins I and II and the pH-independent interaction of metarhodopsin II with transducin C-terminal peptide Biochemistry 49 2010 736 741
35. E. Lyman, and D.M. Zuckerman Ensemble-based convergence analysis of biomolecular trajectories Biophys. J. 91 2006 164 172
36. A. Grossfield, and D.M. Zuckerman Quantifying uncertainty and sampling quality in biomolecular simulations Annu. Rep. Comput. Chem. 5 2009 23 48
37. C. Neale, and J.C.Y. Hsu R. Pomès Indolicidin binding induces thinning of a lipid bilayer Biophys. J. 106 2014 L29 L31
38. J.H. Park, and P. Scheerer O.P. Ernst Crystal structure of the ligand-free G-protein-coupled receptor opsin Nature 454 2008 183 187
39. P. Scheerer, and J.H. Park O.P. Ernst Crystal structure of opsin in its G-protein-interacting conformation Nature 455 2008 497 502
40. M. Kono, and R.K. Crouch In vitro assays of rod and cone opsin activity: retinoid analogs as agonists and inverse agonists Methods Mol. Biol. 652 2010 85 94
41. R. Nussinov, and C.-J. Tsai Allostery in disease and in drug discovery Cell 153 2013 293 305
42. C.-J. Tsai, and R. Nussinov A unified view of "how allostery works." PLOS Comput. Biol. 10 2014 e1003394
43. H.N. Motlagh, and J.O. Wrabl V.J. Hilser The ensemble nature of allostery Nature 508 2014 331 339
44. H.N. Motlagh, and V.J. Hilser Agonism/antagonism switching in allosteric ensembles Proc. Natl. Acad. Sci. USA 109 2012 4134 4139
45. A. Grossfield, and M.C. Pitman K. Gawrisch Internal hydration increases during activation of the G-protein-coupled receptor rhodopsin J. Mol. Biol. 381 2008 478 486
46. K. Martínez-Mayorga, and M.C. Pitman M.F. Brown Retinal counterion switch mechanism in vision evaluated by molecular simulations J. Am. Chem. Soc. 128 2006 16502 16503
47. N. Leioatts, and B. Mertz M.F. Brown Retinal ligand mobility explains internal hydration and reconciles active rhodopsin structures Biochemistry 53 2014 376 385
48. 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
49. S.E. Feller, and K. Gawrisch Properties of docosahexaenoic-acid-containing lipids and their influence on the function of rhodopsin Curr. Opin. Struct. Biol. 15 2005 416 422
50. E.C.Y. Yan, and M.A. Kazmi R.A. Mathies Retinal counterion switch in the photoactivation of the G protein-coupled receptor rhodopsin Proc. Natl. Acad. Sci. USA 100 2003 9262 9267
51. J.-M. Kim, and C. Altenbach H.G. Khorana Structural origins of constitutive activation in rhodopsin: role of the K296/E113 salt bridge Proc. Natl. Acad. Sci. USA 101 2004 12508 12513
52. 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. USA 103 2006 4888 4893
53. J.B. Klauda, and R.M. Venable R.W. Pastor Update of the CHARMM all-atom additive force field for lipids: validation on six lipid types J. Phys. Chem. B 114 2010 7830 7843
54. A.D. MacKerell Jr., and D. Bashford M. Karplus All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B 102 1998 3586 3616
55. A.D. Mackerell Jr., M. Feig, and C.L. Brooks 3rd Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations J. Comput. Chem. 25 2004 1400 1415
56. A.D. MacKerell Jr., M. Feig, and C.L. Brooks 3rd Improved treatment of the protein backbone in empirical force fields J. Am. Chem. Soc. 126 2004 698 699
57. J. Huang, and A.D. MacKerell Jr. CHARMM36 all-atom additive protein force field: validation based on comparison to NMR data J. Comput. Chem. 34 2013 2135 2145
58. S. Zhu, M.F. Brown, and S.E. Feller Retinal conformation governs pKa of protonated Schiff base in rhodopsin activation J. Am. Chem. Soc. 135 2013 9391 9398
59. J.C. Phillips, and R. Braun K. Schulten Scalable molecular dynamics with NAMD J. Comput. Chem. 26 2005 1781 1802
60. D. Voet, and J. Voet Biochemistry 3rd ed 2004 Wiley Hoboken, NJ
61. J.-P. Ryckaert, G. Ciccotti, and H.J. Berendsen Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes J. Comput. Phys. 23 1977 327 341
62. S.E. Feller, and Y. Zhang B.R. Brooks Constant pressure molecular dynamics simulation: the Langevin piston method J. Chem. Phys. 103 1995 4613 4621
63. T. Schneider, and E. Stoll Molecular-dynamics study of a three-dimensional one-component model for distortive phase transitions Phys. Rev. B 17 1978 1302 1322
64. U. Essmann, and L. Perera L.G. Pedersen A smooth particle mesh Ewald method J. Chem. Phys. 103 1995 8577 8593
65. T.D. Romo, N. Leioatts, and A. Grossfield Lightweight object oriented structure analysis: tools for building tools to analyze molecular dynamics simulations J. Comput. Chem. 35 2014 2305 2318
66. J.-P. Changeux The feedback control mechanisms of biosynthetic L-threonine deaminase by L-isoleucine Cold Spring Harb. Symp. Quant. Biol. 26 1961 313 318
67. P.-W. Lau, and A. Grossfield M.F. Brown Dynamic structure of retinylidene ligand of rhodopsin probed by molecular simulations J. Mol. Biol. 372 2007 906 917
68. Y. Fukada, and T. Okano R.S. Liu Comparative study on the chromophore binding sites of rod and red-sensitive cone visual pigments by use of synthetic retinal isomers and analogues Biochemistry 29 1990 3133 3140
69. S. Srinivasan, and E. Ramon P. Garriga Binding specificity of retinal analogs to photoactivated visual pigments suggest mechanism for fine-tuning GPCR-ligand interactions Chem. Biol. 21 2014 369 378
70. S. Ahuja, and E. Crocker S.O. Smith Location of the retinal chromophore in the activated state of rhodopsin∗ J. Biol. Chem. 284 2009 10190 10201
71. V. Hornak, and S. Ahuja 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
72. T. Okada, and M. Sugihara V. Buss The retinal conformation and its environment in rhodopsin in light of a new 2.2 A crystal structure J. Mol. Biol. 342 2004 571 583
73. A.V. Struts, and G.F.J. Salgado M.F. Brown Structural analysis and dynamics of retinal chromophore in dark and meta I states of rhodopsin from 2H NMR of aligned membranes J. Mol. Biol. 372 2007 50 66
74. G.F.J. Salgado, and A.V. Struts M.F. Brown Deuterium NMR structure of retinal in the ground state of rhodopsin Biochemistry 43 2004 12819 12828
75. A.V. Struts, G.F.J. Salgado, and M.F. Brown Solid-state 2H NMR relaxation illuminates functional dynamics of retinal cofactor in membrane activation of rhodopsin Proc. Natl. Acad. Sci. USA 108 2011 8263 8268
76. G.F.J. Salgado, and A.V. Struts M.F. Brown Solid-state 2H NMR structure of retinal in metarhodopsin I J. Am. Chem. Soc. 128 2006 11067 11071
77. Y. Miao, and S.E. Nichols J.A. McCammon Activation and dynamic network of the M2 muscarinic receptor Proc. Natl. Acad. Sci. USA 110 2013 10982 10987
78. H.-W. Choe, and Y.J. Kim O.P. Ernst Crystal structure of metarhodopsin II Nature 471 2011 651 655
79. J.Y. Lee, and E. Lyman Agonist dynamics and conformational selection during microsecond simulations of the A(2A) adenosine receptor Biophys. J. 102 2012 2114 2120
80. B. Holst, and R. Nygaard T.W. Schwartz A conserved aromatic lock for the tryptophan rotameric switch in TM-VI of seven-transmembrane receptors J. Biol. Chem. 285 2010 3973 3985