Retinal ligand mobility explains internal hydration and reconciles active rhodopsin structures

Biochemistry

Volumn 53, Issue 2, 2014, Pages 376-385

  Leioatts, Nicholas ^a   Mertz, Blake ^b   Martínez Mayorga, Karina ^b   Romo, Tod D ^a   Pitman, Michael C ^c   Feller, Scott E ^d   Grossfield, Alan ^a   Brown, Michael F ^b,e  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b The University of Arizona   (United States)

^c IBM T J WATSON RESEARCH CENTER   (United States)

^d WABASH COLLEGE   (United States)

^e University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTORS; HYDROPHOBIC CORE; LIGAND MOBILITY; LIGHT ACTIVATION; MEMBRANE PROTEINS; MOLECULAR DYNAMICS SIMULATIONS; STRUCTURAL INFORMATION; X RAY CRYSTAL STRUCTURES;

BIOLOGICAL MEMBRANES; LIGANDS; MAMMALS; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEINS;

OPHTHALMOLOGY;

RETINAL; RHODOPSIN; TRYPTOPHAN; WATER;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DEUTERON NUCLEAR MAGNETIC RESONANCE; HYDRATION; INTERNAL HYDRATION; LIGAND BINDING; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN CONFORMATION; RNA TRANSLATION; SOLID STATE; VISUAL ORIENTATION; WATER TRANSPORT;

CRYSTALLOGRAPHY, X-RAY; LIGANDS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; RETINALDEHYDE; RHODOPSIN; TIME FACTORS; WATER;

EID: 84892685953     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi4013947     Document Type: Article

References (62)

1. Fredriksson, R., Lagerström, M. C., Lundin, L.-G., and Schiöth, H. B. (2003) The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints Mol. Pharmacol. 63, 1256-1272
2. Lefkowitz, R. J. (2004) Historical review: A brief history and personal retrospective of seven-transmembrane receptors Trends Pharmacol. Sci. 25, 413-422
3. Rosenbaum, D. M., Rasmussen, S. G. F., and Kobilka, B. K. (2009) The structure and function of G-protein-coupled receptors Nature 459, 356-363
4. Nygaard, R., Frimurer, T. M., Holst, B., Rosenkilde, M. M., and Schwartz, T. W. (2009) Ligand binding and micro-switches in 7TM receptor structures Trends Pharmacol. Sci. 30, 249-259
5. Hubbell, W. L., Altenbach, C., Hubbell, C. M., and Khorana, H. G. (2003) Rhodopsin structure, dynamics, and activation: A perspective from crystallography, site-directed spin labeling, sulfhydryl reactivity, and disulfide cross-linking Adv. Protein Chem. 63, 243-290
6. Mombaerts, P. (1999) Seven-transmembrane proteins as odorant and chemosensory receptors Science 286, 707-711
7. Firestein, S. (2000) The good taste of genomics Nature 404, 552-553
8. Howard, A. D., McAllister, G., Feighner, S. D., Liu, Q., Nargund, R. P., Van der Ploeg, L. H. T., and Patchett, A. A. (2001) Orphan G-protein-coupled receptors and natural ligand discovery Trends Pharmacol. Sci. 22, 132-140
9. Overington, J. P., Al-Lazikani, B., and Hopkins, A. L. (2006) How many drug targets are there? Nat. Rev. Drug Discovery 5, 993-996
10. Bahar, I., Lezon, T. R., Bakan, A., and Shrivastava, I. H. (2010) Normal mode analysis of biomolecular structures: Functional mechanisms of membrane proteins Chem. Rev. 110, 1463-1497
11. Granier, S. and Kobilka, B. (2012) A new era of GPCR structural and chemical biology Nat. Chem. Biol. 8, 670-673
12. Okada, T., Ernst, O. P., Palczewski, K., and Hofmann, K. P. (2001) Activation of rhodopsin: New insights from structural and biochemical studies Trends Biochem. Sci. 26, 318-324
13. Ballesteros, J. and Weinstein, H. (1995) Integrated methods for the construction of three-dimensional models and computational probing of structure-function relations in G protein-coupled receptors Methods Neurosci. 25, 366-428
14. Burns, M. E. and Baylor, D. A. (2001) Activation, deactivation, and adaptation in vertebrate photoreceptor cells Annu. Rev. Neurosci. 24, 779-805
15. Cooper, A. (1979) Energy uptake in the first step of visual excitation Nature 282, 531-533
16. Lewis, J. W., Kliger, D. S., and Krzystof, P. (2000) Absorption spectroscopy in studies of visual pigments: Spectral and kinetic characterization of intermediates Meth. Enzymol. 315, 164-178
17. Palczewski, K., Kumasaka, T., Hori, T., Behnke, C. A., Motoshima, H., Fox, B. A., Le Trong, I., Teller, D. C., Okada, T., Stenkamp, R. E., Yamamoto, M., and Miyano, M. (2000) Crystal structure of rhodopsin: A G protein-coupled receptor Science 289, 739-745
18. Okada, T., Sugihara, M., Bondar, A.-N., Elstner, M., Entel, P., and Buss, V. (2004) The retinal conformation and its environment in rhodopsin in light of a new 2.2 Å crystal structure J. Mol. Biol. 342, 571-583
19. Nakamichi, H. and Okada, T. (2006) Crystallographic analysis of primary visual photochemistry Angew. Chem. 45, 4270-4273
20. Nakamichi, H. and Okada, T. (2006) Local peptide movement in the photoreaction intermediate of rhodopsin Proc. Natl. Acad. Sci. U.S.A. 103, 12729-12734
21. Standfuss, J., Edwards, P. C., D'Antona, A., Fransen, M., Xie, G., Oprian, D. D., and Schertler, G. F. X. (2011) The structural basis of agonist-induced activation in constitutively active rhodopsin Nature 471, 656-660
22. Choe, H.-W., Kim, Y. J., Park, J. H., Morizumi, T., Pai, E. F., Krauß, N., Hofmann, K. P., Scheerer, P., and Ernst, O. P. (2011) Crystal structure of metarhodopsin II Nature 471, 651-655
23. Deupi, X., Edwards, P., Singhal, A., Nickle, B., Oprian, D., Schertler, G., and Standfuss, J. (2012) Stabilized G protein binding site in the structure of constitutively active metarhodopsin-II Proc. Natl. Acad. Sci. U.S.A. 109, 119-124
24. Scheerer, P., Park, J. H., Hildebrand, P. W., Kim, Y. J., Krauß, N., Choe, H.-W., Hofmann, K. P., and Ernst, O. P. (2008) Crystal structure of opsin in its G-protein-interacting conformation Nature 455, 497-502
25. Park, J. H., Scheerer, P., Hofmann, K. P., Choe, H.-W., and Ernst, O. P. (2008) Crystal structure of the ligand-free G-protein-coupled receptor opsin Nature 454, 183-187
26. Altenbach, C., Kusnetzow, A. K., Ernst, O. P., Hofmann, K. P., and Hubbell, W. L. (2008) High-resolution distance mapping in rhodopsin reveals the pattern of helix movement due to activation Proc. Natl. Acad. Sci. U.S.A. 105, 7439-7444
27. Patel, A. B., Crocker, E., Eilers, M., Hirshfeld, A., Sheves, M., and Smith, S. O. (2004) Coupling of retinal isomerization to the activation of rhodopsin Proc. Natl. Acad. Sci. U.S.A. 101, 10048-10053
28. Ruprecht, J. J., Mielke, T., Vogel, R., Villa, C., and Schertler, G. F. X. (2004) Electron crystallography reveals the structure of metarhodopsin I EMBO J. 23, 3609-3620
29. Crocker, E., Eilers, M., Ahuja, S., Hornak, V., Hirshfeld, A., Sheves, M., and Smith, S. O. (2006) Location of Trp265 in metarhodopsin II: Implications for the activation mechanism of the visual receptor rhodopsin J. Mol. Biol. 357, 163-172
30. Ahuja, S., Crocker, E., Eilers, M., Hornak, V., Hirshfeld, A., Ziliox, M., Syrett, N., Reeves, P. J., Khorana, H. G., Sheves, M., and Smith, S. O. (2009) Location of the retinal chromophore in the activated state of rhodopsin J. Biol. Chem. 284, 10190-10201
31. Hornak, V., Ahuja, S., Eilers, M., Goncalves, J. A., Sheves, M., Reeves, P. J., and Smith, S. O. (2010) Light activation of rhodopsin: Insights from molecular dynamics simulations guided by solid-state NMR distance restraints J. Mol. Biol. 396, 510-527
32. 2H NMR relaxation illuminates functional dynamics of retinal cofactor in membrane activation of rhodopsin Proc. Natl. Acad. Sci. U.S.A. 108, 8263-8268
33. Struts, A. V., Salgado, G. F. J., Martínez-Mayorga, K., and Brown, M. F. (2011) Retinal dynamics underlie its switch from inverse agonist to agonist during rhodopsin activation Nat. Struct. Mol. Biol. 18, 392-394
34. Mertz, B., Lu, M., Brown, M. F., and Feller, S. E. (2011) Steric and electronic influences on the torsional energy landscape of retinal Biophys. J. 101, L17-L19
35. Eilers, M., Goncalves, J. A., Ahuja, S., Kirkup, C., Hirshfeld, A., Simmerling, C., Reeves, P. J., Sheves, M., and Smith, S. O. (2012) Structural transitions of transmembrane helix 6 in the formation of metarhodopsin I J. Phys. Chem. B 116, 10477-10489
36. Martínez-Mayorga, K., Pitman, M. C., Grossfield, A., Feller, S. E., and Brown, M. F. (2006) Retinal counterion switch mechanism in vision evaluated by molecular simulations J. Am. Chem. Soc. 128, 16502-16503
37. Nevzorov, A. A., Moltke, S., Heyn, M. P., and Brown, M. F. (1999) Solid-state NMR line shapes of uniaxially oriented immobile systems J. Am. Chem. Soc. 121, 7636-7643
38. a of the retinal Schiff base J. Am. Chem. Soc. 128, 10503-10512
39. Lüdeke, S., Beck, M., Yan, E. C. Y., Sakmar, T. P., Siebert, F., and Vogel, R. (2005) The role of Glu181 in the photoactivation of rhodopsin J. Mol. Biol. 353, 345-356
40. 2H NMR of aligned membranes J. Mol. Biol. 372, 50-66
41. Grossfield, A., Pitman, M. C., Feller, S. E., Soubias, O., and Gawrisch, K. (2008) Internal hydration increases during activation of the G-protein-coupled receptor rhodopsin J. Mol. Biol. 381, 478-486
42. Lau, P.-W., Grossfield, A., Feller, S. E., Pitman, M. C., and Brown, M. F. (2007) Dynamic structure of retinylidene ligand of rhodopsin probed by molecular simulations J. Mol. Biol. 372, 906-917
43. Grossfield, A., Feller, S. E., and Pitman, M. C. (2006) A role for direct interactions in the modulation of rhodopsin by ω-3 polyunsaturated lipids Proc. Natl. Acad. Sci. U.S.A. 103, 4888-4893
44. Fitch, B. G., Germain, R. S., Mendell, M., Pitera, J., Pitman, M., Rayshubskiy, A., Sham, Y., Suits, F., Swope, W., Ward, T. J. C., Zhestkov, Y., and Zhou, R. (2003) Blue Matter, an application framework for molecular simulation on Blue Gene J. Parallel Distrib. Comput. 63, 759-773
45. MacKerell, A. D., Jr., Bashford, D., Bellott, M., Dunbrack, R. L., Jr., Evanseck, J. D., Field, M. J., Fischer, S., Gao, J., Guo, H., Ha, S., Joseph-McCarthy, D., Kuchnir, L., Kuczera, K., Lau, F. T. K., Mattos, C., Michnick, S., Ngo, T., Nguyen, D. T., Prodhom, B., Reiher, W. E., III, Roux, B., Schlenkrich, M., Smith, J. C., Stote, R., Straub, J., Watanabe, M., Wiórkiewicz-Kuczera, J., Yin, D., and Karplus, M. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B 102, 3586-3616
46. Feller, S. E. and MacKerell, A. D., Jr. (2000) An improved empirical potential energy function for molecular simulations of phospholipids J. Phys. Chem. B 104, 7510-7515
47. Nina, M., Smith, J. C., and Roux, B. (1993) Ab Initio quantum-chemical analysis of Schiff base-water interactions in bacteriorhodopsin J. Mol. Struct. 286, 231-245
48. Andersen, H. C. (1983) Rattle: A "velocity" version of the shake algorithm for molecular dynamics calculations J. Comput. Phys. 52, 24-34
49. Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., and Pedersen, L. G. (1995) A smooth particle mesh Ewald method J. Chem. Phys. 103, 8577-8593
50. Romo, T. D. and Grossfield, A. (2009) LOOS: An extensible platform for the structural analysis of simulations Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009, 2332-2335
51. Grossfield, A., Feller, S. E., and Pitman, M. C. (2007) Convergence of molecular dynamics simulations of membrane proteins Proteins: Struct., Funct., Bioinf. 67, 31-40
52. Brooks, B. R., Janežič, D., and Karplus, M. (1995) Harmonic analysis of large systems. I. Methodology J. Comput. Chem. 16, 1522-1542
53. a of protonated Schiff base in rhodopsin activation J. Am. Chem. Soc. 135, 9391-9398
54. Hayashi, S., Tajkhorshid, E., and Schulten, K. (2009) Photochemical reaction dynamics of the primary event of vision studied by means of a hybrid molecular simulation Biophys. J. 96, 403-416
55. Valsson, O., Campomanes, P., Tavernelli, I., Rothlisberger, U., and Filippi, C. (2013) Rhodopsin absorption from first principles: Bypassing common pitfalls J. Chem. Theory Comput. 9, 2441-2454
56. 2 Adrenergic receptor activation. Modulation of the proline kink in transmembrane 6 by a rotamer toggle switch J. Biol. Chem. 277, 40989-40996
57. Schwartz, T. W., Frimurer, T. M., Holst, B., Rosenkilde, M. M., and Elling, C. E. (2006) Molecular mechanism of 7TM receptor activation-a global toggle switch model Annu. Rev. Pharmacol. Toxicol. 46, 481-519
58. Huber, T., Botelho, A. V., Beyer, K., and Brown, M. F. (2004) Membrane model for the G-protein-coupled receptor rhodopsin: Hydrophobic interface and dynamical structure Biophys. J. 86, 2078-2100
59. Angel, T. E., Gupta, S., Jastrzebska, B., Palczewski, K., and Chance, M. R. (2009) Structural waters define a functional channel mediating activation of the GPCR, rhodopsin Proc. Natl. Acad. Sci. U.S.A. 106, 14367-14372
60. Angel, T. E., Chance, M. R., and Palczewski, K. (2009) Conserved waters mediate structural and functional activation of family A (rhodopsin-like) G protein-coupled receptors Proc. Natl. Acad. Sci. U.S.A. 106, 8555-8560
61. Nygaard, R., Valentin-Hansen, L., Mokrosinski, J., Frimurer, T. M., and Schwartz, T. W. (2010) Conserved water-mediated hydrogen bond network between TM-I, -II, -VI, and -VII in 7TM receptor activation J. Biol. Chem. 285, 19625-19636
62. Jastrzebska, B., Palczewski, K., and Golczak, M. (2011) Role of bulk water in hydrolysis of the rhodopsin chromophore J. Biol. Chem. 286, 18930-18937