Three-Layer ONIOM Studies of the Dark State of Rhodopsin: The Protonation State of Glu181

Journal of Molecular Biology

Volumn 383, Issue 1, 2008, Pages 106-121

  Hall, Katherine F ^a   Vreven, Thom ^b   Frisch, Michael J ^b   Bearpark, Michael J ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b GAUSSIAN INC   (United States)

Author keywords

computational; ONIOM; protonation state; QM MM; rhodopsin

Indexed keywords

GLUTAMIC ACID; RHODOPSIN; SCHIFF BASE;

ARTICLE; HYDROGEN BOND; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; PROTON TRANSPORT; X RAY ANALYSIS;

EID: 52049114905     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.08.007     Document Type: Article

References (77)

1. Baylor D. How photons start vision. Proc. Natl. Acad. Sci. USA 93 (1996) 560-565
2. Rasmussen S.G.F., Choi H.J., Rosenbaum D.M., Kobilka T.S., Thian F.S., Edwards P.C., et al. Crystal structure of the human beta(2) adrenergic G-protein-coupled receptor. Nature 450 (2007) 383-U4
3. Cherezov V., Rosenbaum D.M., Hanson M.A., Rasmussen S.G.F., Thian F.S., Kobilka T.S., et al. High-resolution crystal structure of an engineered human beta(2)-adrenergic G protein-coupled receptor. Science 318 (2007) 1258-1265
4. Rosenbaum D.M., Cherezov V., Hanson M.A., Rasmussen S.G.F., Thian F.S., Kobilka T.S., et al. GPCR engineering yields high-resolution structural insights into beta(2)-adrenergic receptor function. Science 318 (2007) 1266-1273
5. Palczewski K., Kumasaka T., Hori T., Behnke C.A., Motoshima H., Fox B.A., et al. Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289 (2000) 739-745
6. Teller D.C., Okada T., Behnke C.A., Palczewski K., and Stenkamp R.E. Advances in determination of a high-resolution three-dimensional structure of rhodopsin, a model of G-protein-coupled receptors (GPCRs). Biochemistry 40 (2001) 7761-7772
7. Okada T., Fujiyoshi Y., Silow M., Navarro J., Landau E.M., and Shichida Y. Functional role of internal water molecules in rhodopsin revealed by x-ray crystallography. Proc. Natl. Acad. Sci. USA 99 (2002) 5982-5987
8. Okada T., Sugihara M., Bondar A.N., Elstner M., Entel P., and Buss V. 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
9. Drews J. Drug discovery: a historical perspective. Science 287 (2000) 1960-1964
10. Filmore D. It's a GPCR world. Mod. Drug Discov. 7 (2004) 24-28
11. Nielsen I.B., Lammich L., and Andersen L.H. S-1 and S-2 excited states of gas-phase Schiff-base retinal chromophores. Phys. Rev. Lett. (2006) 96
12. Logunov S.L., Song L., and ElSayed M.A. Excited-state dynamics of a protonated retinal Schiff base in solution. J. Phys. Chem. 100 (1996) 18586-18591
13. Stuart J.A., and Birge R.R. In: Lee A.G. (Ed). Biomembranes Vol. 2A (1996), JAI Press, London 33-140
14. Shichi H. Characterization of the primary photochemical events in bacteriorhodopsin and rhodopsin. Biochemistry of Vision (1983), Academic Press, New York
15. Steinberg G., Ottolenghi M., and Sheves M. Pk(a) of the protonated Schiff-base of bovine rhodopsin-a study with artificial pigments. Biophys. J. 64 (1993) 1499-1502
16. Zhukovsky E.A., and Oprian D.D. Effect of carboxylic-acid side-chains on the absorption maximum of visual pigments. Science 246 (1989) 928-930
17. Sakmar T.P., Franke R.R., and Khorana H.G. Glutamic acid-113 serves as the retinylidene Schiff-base counterion in bovine rhodopsin. Proc. Natl. Acad. Sci. USA 86 (1989) 8309-8313
18. Birge R.R., Murray L.P., Pierce B.M., Akita H., Baloghnair V., Findsen L.A., and Nakanishi K. 2-Photon spectroscopy of locked-11-cis-rhodopsin-evidence for a protonated Schiff-base in a neutral protein-binding site. Proc. Natl. Acad. Sci. USA 82 (1985) 4117-4121
19. Creemers A.F.L., Klaassen C.H.W., Bovee-Geurts P.H.M., Kelle R., Kragl U., Raap J., et al. Solid state N-15 NMR evidence for a complex Schiff base counterion in the visual G-protein-coupled receptor rhodopsin. Biochemistry 38 (1999) 7195-7199
20. Yan E.C.Y., Kazmi M.A., Ganim Z., Hou J.M., Pan D.H., Chang B.S.W., et al. Retinal counterion switch in the photoactivation of the G protein-coupled receptor rhodopsin. Proc. Natl. Acad. Sci. USA 100 (2003) 9262-9267
21. Longstaff C., Calhoon R.D., and Rando R.R. Deprotonation of the Schiff-base of rhodopsin is obligate in the activation of the G-protein. Proc. Natl. Acad. Sci. USA 83 (1986) 4209-4213
22. Doukas A.G., Aton B., Callender R.H., and Ebrey T.G. Resonance Raman studies of bovine metarhodopsin-I and metarhodopsin-II. Biochemistry 17 (1978) 2430-2435
23. Ludeke S., Beck R., Yan E.C.Y., Sakmar T.P., Siebert F., and Vogel R. The role of Glu181 in the photoactivation of rhodopsin. J. Mol. Biol. 353 (2005) 345-356
24. Yan E.C.Y., Kazmi M.A., De S., Chang B.S.W., Seibert C., Marin E.P., et al. Function of extracellular loop 2 in rhodopsin: glutamic acid 181 modulates stability and absorption wavelength of metarhodopsin II. Biochemistry 41 (2002) 3620-3627
25. Peters K., Applebury M.L., and Rentzepis P.M. Primary photochemical event in vision-proton translocation. Proc. Natl. Acad. Sci. USA 74 (1977) 3119-3123
26. Martinez-Mayorga K., Pitman M.C., Grossfield A., Feller S.E., and Brown M.F. Retinal counterion switch mechanism in vision evaluated by molecular simulations. J. Am. Chem. Soc. 128 (2006) 16502-16503
27. Rohrig U.F., Guidoni L., and Rothlisberger U. Early steps of the intramolecular signal transduction in rhodopsin explored by molecular dynamics simulations. Biochemistry 41 (2002) 10799-10809
28. Han M., Dedecker B.S., and Smith S.O. Localization of the retinal protonated Schiff-base counterion in rhodopsin. Biophys. J. 65 (1993) 899-906
29. Ramos L., Chen M., Knox B.E., and Birge R.R. Regulation of photoactivation in vertebrate short wavelength visual pigments: protonation of the retinylidene Schiff base and a counterion switch. Biochemistry 46 (2007) 5330-5340
30. Wanko M., Hoffmann M., Strodet P., Koslowski A., Thiel W., Neese F., et al. Calculating absorption shifts for retinal proteins: computational challenges. J. Phys. Chem. B 109 (2005) 3606-3615
31. Wanko M., Hoffmann M., Frauenheim T., and Elstner M. Computational photochemistry of retinal proteins. J. Comput.-Aided Mol. Des. 20 (2006) 511-518
32. Andruniow T., Ferre N., and Olivucci M. Structure, initial excited-state relaxation, and energy storage of rhodopsin resolved at the multiconfigurational perturbation theory level. Proc. Natl. Acad. Sci. USA 101 (2004) 17908-17913
33. Coto P.B., Sinicropi A., De Vico L., Ferre N., and Olivucci M. Characterization of the conical intersection of the visual pigment rhodopsin at the CASPT2//CASSCF/AMBER level of theory. Mol. Phys. 104 (2006) 983-991
34. Coto P.B., Strambi A., Ferre N., and Olivucci M. The color of rhodopsins at the ab initio multiconfigurational perturbation theory resolution. Proc. Natl. Acad. Sci. USA 103 (2006) 17154-17159
35. Gascon J.A., and Batista V.S. Quantum mechanics/molecular mechanics (QM/MM) studies of energy storage, molecular rearrangements and changes in NMR chemical shifts due to the primary photochemical event in visual rhodopsin. Biophys. J. 88 (2005) 388A
36. Gascon J.A., Sproviero E.M., and Batista V.S. QM/MM study of the NMR spectroscopy of the retinyl chromophore in visual rhodopsin. J. Chem. Theor. Comput. 1 (2005) 674-685
37. Gascon J.A., Sproviero E.M., and Batista V.S. Computational studies of the primary phototransduction event in visual rhodopsin. Acc. Chem. Res. 39 (2006) 184-193
38. Fujimoto K., Hasegawa J.Y., Hayashi S., Kato S., and Nakatsuji H. Mechanism of color tuning in retinal protein: SAC-CI and QM/MM study. Chem. Phys. Lett. 414 (2005) 239-242
39. Matsuura A., Sato H., Houjou H., Saito S., Hayashi T., and Sakurai M. Accurate evaluation of the absorption maxima of retinal proteins based on a hybrid QM/MM method. J. Comput. Chem. 27 (2006) 1623-1630
40. Ponder J.W. TINKER 4.2 (2004), Washington University, Saint Louis, MO
41. Brunger A.T., Adams P.D., Clore G.M., Delano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system (CNS): a new software system for macromolecular structure determination. Acta Crystallogr., Sect. D: Biol. Crystallogr. 54 (1998) 905-921
42. Han M., and Smith S.O. High-resolution structural studies of the retinal-glu113 interaction in rhodopsin. Biophys. Chem. 56 (1995) 23-29
43. Han M., and Smith S.O. NMR constraints on the location of the retinal chromophore in rhodopsin and barthorhodopsin. Biochemistry 34 (1995) 1425-1432
44. Creemers A.F.L., Kiihne S., Bovee-Geurts P.H.M., DeGrip W.J., Lugtenburg J., and de Groot H.J.M. H-1 and C-13 MAS NMR evidence for pronounced ligand-protein interactions involving the ionone ring of the retinylidene chromophore in rhodopsin. Proc. Natl. Acad. Sci. USA 99 (2002) 9101-9106
45. Eilers M., Reeves P.J., Ying W.W., Khorana H.G., and Smith S.O. Magic angle spinning NMR of the protonated retinylidene Schiff base nitrogen in rhodopsin: expression of N-15-lysine- and C-13-glycine-labeled opsin in a stable cell line. Proc. Natl. Acad. Sci. USA 96 (1999) 487-492
46. Verhoeven M.A., Creemers A.F.L., Bovee-Geurts P.H.M., De Grip W.J., Lugtenburg J., and de Groot H.J.M. Ultra-high-field MAS NMR assay of a multispin labeled ligand bound to its G-protein receptor target in the natural membrane environment: electronic structure of the retinylidene chromophore in rhodopsin. Biochemistry 40 (2001) 3282-3288
47. Warshel A. Charge stabilization mechanism in visual and purple membrane pigments. Proc. Natl. Acad. Sci. USA 75 (1978) 2558-2562
48. Li J., Edwards P.C., Burghammer M., Villa C., and Schertler G.F.X. Structure of bovine rhodopsin in a trigonal crystal form. J. Mol. Biol. 343 (2004) 1409-1438
49. Buss V., Sugihara M., Entel P., and Hafner J. Thr94 and Wat2b effect protonation of the retinal chromophore in rhodopsin. Angew. Chem., Int. Ed. 42 (2003) 3245-3247
50. Sugihara M., Buss V., Entel P., and Hafner J. The nature of the complex counterion of the chromophore in rhodopsin. J. Phys. Chem. B 108 (2004) 3673-3680
51. Carravetta M., Zhao X., Johannessen O.G., Lai W.C., Verhoeven M.A., Bovee-Geurts P.H.M., et al. Protein-induced bonding perturbation of the rhodopsin chromophore detected by double-quantum solid-state NMR. J. Am. Chem. Soc. 126 (2004) 3948-3953
52. Touw S.I.E., de Groot H.J.M., and Buda F. Ab initio modeling of the spatial, electronic, and vibrational structure of Schiff base models for visual photoreceptors. J. Phys. Chem. B 108 (2004) 13560-13572
53. Lin S.W., Groesbeek M., van der Hoef I., Verdegem P., Lugtenburg J., and Mathies R.A. Vibrational assignment of torsional normal modes of rhodopsin: probing excited-state isomerization dynamics along the reactive C-11{double bond, short}C-12 torsion coordinate. J. Phys. Chem. B 102 (1998) 2787-2806
54. Palings I., Pardoen J.A., Vandenberg E., Winkel C., Lugtenburg J., and Mathies R.A. Assignment of fingerprint vibrations in the resonance Raman-spectra of rhodopsin, isorhodopsin, and bathorhodopsin-implications for chromophore structure and environment. Biochemistry 26 (1987) 2544-2556
55. Eyring G., Curry B., Broek A., Lugtenburg J., and Mathies R. Assignment and interpretation of hydrogen out-of-plane vibrations in the resonance Raman-spectra of rhodopsin and bathorhodopsin. Biochemistry 21 (1982) 384-393
56. Lai W.C., McLean N., Gansmuller A., Verhoeven M.A., Antonioli G.C., Carravetta M., et al. Accurate measurements of C-13-C-13 J-couplings in the rhodopsin chromophore by double-quantum solid-state NMR spectroscopy. J. Am. Chem. Soc. 128 (2006) 3878-3879
57. Schreiber M., Buss V., and Sugihara M. Exploring the Opsin shift with ab initio methods: geometry and counterion effects on the electronic spectrum of retinal. J. Chem. Phys. 119 (2003) 12045-12048
58. Pan D.H., and Mathies R.A. Chromophore structure in lumirhodopsin and metarhodopsin I by time-resolved resonance Raman microchip spectroscopy. Biochemistry 40 (2001) 7929-7936
59. Levine B.G., Ko C., Quenneville J., and Martinez T.J. Conical intersections and double excitations in time-dependent density functional theory. Mol. Phys. 104 (2006) 1039-1051
60. Sekharan S., Sugihara M., and Buss V. Origin of spectral tuning in rhodopsin-it is not the binding pocket. Angew. Chem., Int. Ed. 46 (2007) 269-271
61. Humphrey W., Lu H., Logunov I., Werner H.J., and Schulten K. Three electronic state model of the primary phototransformation of bacteriorhodopsin. Biophys. J. 75 (1998) 1689-1699
62. Cembran A., Bernardi F., Olivucci M., and Garavelli M. Counterion controlled photoisomerization of retinal chromophore models: a computational investigation. J. Am. Chem. Soc. 126 (2004) 16018-16037
63. Patel A.B., Crocker E., Reeves P.J., Getmanova E.V., Eilers M., Khorana H.G., and Smith S.O. Changes in interhelical hydrogen bonding upon rhodopsin activation. J. Mol. Biol. 347 (2005) 803-812
64. Fahmy K., Jager F., Beck M., Zvyaga T.A., Sakmar T.P., and Siebert F. Protonation states of membrane-embedded carboxylic-acid groups in rhodopsin and metarhodopsin-II-a Fourier-transform infrared-spectroscopy study of site-directed mutants. Proc. Natl. Acad. Sci. USA 90 (1993) 10206-10210
65. Dapprich S., Komaromi I., Byun K.S., Morokuma K., and Frisch M.J. A new ONIOM implementation in Gaussian98. Part I. The calculation of energies, gradients, vibrational frequencies and electric field derivatives. J. Mol. Struct.: THEOCHEM 462 (1999) 1-21
66. Humbel S., Sieber S., and Morokuma K. The IMOMO method: integration of different levels of molecular orbital approximations for geometry optimization of large systems: test for n-butane conformation and S(N)2 reaction: RCl+Cl. J. Chem. Phys. 105 (1996) 1959-1967
67. Svensson M., Humbel S., Froese R.D.J., Matsubara T., Sieber S., and Morokuma K. ONIOM: a multilayered integrated MO+MM method for geometry optimizations and single point energy predictions. A test for Diels-Alder reactions and Pt(P(t-Bu)(3))(2)+H-2 oxidative addition. J. Phys. Chem. 100 (1996) 19357-19363
68. Vreven T., and Morokuma K. On the application of the IMOMO (integrated molecular orbital plus molecular orbital) method. J. Comput. Chem. 21 (2000) 1419-1432
69. Vreven T., Byun K.S., Komaromi I., Dapprich S., Montgomery J.A., Morokuma K., and Frisch M.J. Combining quantum mechanics methods with molecular mechanics methods in ONIOM. J. Chem. Theor. Comput. 2 (2006) 815-826
70. Vreven T., and Morokuma K. Investigation of the S-0 → S-1 excitation in bacteriorhodopsin with the ONIOM(MO:MM) hybrid method. Theor. Chem. Acc. 109 (2003) 125-132
71. Cornell W.D., Cieplak P., Bayly C.I., Gould I.R., Merz K.M., Ferguson D.M., et al. A 2nd generation force-field for the simulation of proteins, nucleic-acids, and organic-molecules. J. Am. Chem. Soc. 117 (1995) 5179-5197
72. Frisch M.J., Trucks G.W., Schlegel H.B., Scuseria G.E., Robb M.A., Cheeseman J.R., et al. Gaussian Development Version, Revision F.X1 (2006), Gaussian, Inc., Wallingford, CT
73. Bearpark M.J., Ogliaro F., Vreven T., Boggio-Pasqua M., Frisch M.J., Larkin S.M., et al. CASSCF calculations for photoinduced processes in large molecules: choosing when to use the RASSCF, ONIOM and MMVB approximations. J. Photochem. Photobiol., A 190 (2007) 207-227
74. Vreven T., Morokuma K., Farkas O., Schlegel H.B., and Frisch M.J. Geometry optimization with QM/MM, ONIOM, and other combined methods. I. Microiterations and constraints. J. Comput. Chem. 24 (2003) 760-769
75. Vreven T., Frisch M.J., Kudin K.N., Schlegel H.B., and Morokuma K. Geometry optimization with QM/MM methods: II. Explicit quadratic coupling. Mol. Phys. 104 (2006) 701-714
76. Hratchian H.P., Parandekar P.V., Raghavachari K., Frisch M.J., and Vreven T. QM:QM electronic embedding using Mulliken atomic charges: energies and analytic gradients in an ONIOM framework. J. Chem. Phys. 128 (2008) 034107
77. Karadakov P.B., and Morokuma K. ONIOM as an efficient tool for calculating NMR chemical shielding constants in large molecules. Chem. Phys. Lett. 317 (2000) 589-596