Location of Trp265 in metarhodopsin II: implications for the activation mechanism of the visual receptor rhodopsin

Journal of Molecular Biology

Volumn 357, Issue 1, 2006, Pages 163-172

  Crocker, Evan ^a   Eilers, Markus ^a   Ahuja, Shivani ^a   Hornak, Viktor ^a   Hirshfeld, Amiram ^b   Sheves, Mordechai ^b   Smith, Steven O ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

G protein coupled receptor; Magic angle spinning; Retinal chromophore; Rotamer toggle switch; Solid state NMR

Indexed keywords

BETA IONONE; MEMBRANE PROTEIN; RHODOPSIN; TRYPTOPHAN;

ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CHROMATOPHORE; CONTROLLED STUDY; HUMAN; HUMAN CELL; LIGHT DARK CYCLE; NUCLEAR MAGNETIC RESONANCE; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SOLID STATE MAGIC ANGLE SPINNING NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

EID: 33644772378     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.12.046     Document Type: Article

References (60)

1. S.T. Menon, M. Han, and T.P. Sakmar Rhodopsin: structural basis of molecular physiology Physiol. Rev. 81 2001 1659 1688
2. U. Gether, and B.K. Kobilka G protein-coupled receptors. II. Mechanism of agonist activation J. Biol. Chem. 273 1998 17979 17982
3. S. Madabushi, A.K. Gross, A. Philippi, E.C. Meng, T.G. Wensel, and O. Lichtarge Evolutionary trace of G protein-coupled receptors reveals clusters of residues that determine global and class-specific functions J. Biol. Chem. 279 2004 8126 8132
4. S.S. Karnik, C. Gogonea, S. Patil, Y. Saad, and T. Takezako Activation of G-protein-coupled receptors: a common molecular mechanism Trends Endocrinol. Metab. 14 2003 431 437
5. 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 Advan. Protein Chem. 63 2003 243 290
6. D.L. Farrens, C. Altenbach, K. Yang, W.L. Hubbell, and H.G. Khorana Requirement of rigid-body motion of transmembrane helices for light activation of rhodopsin Science 274 1996 768 770
7. S.P. Sheikh, T.A. Zvyaga, O. Lichtarge, T.P. Sakmar, and H.R. Bourne Rhodopsin activation blocked by metal-ion-binding sites linking transmembrane helices C and F Nature 383 1996 347 350
8. K. Palczewski, T. Kumasaka, T. Hori, C.A. Behnke, H. Motoshima, and B.A. Fox Crystal structure of rhodopsin: a G protein-coupled receptor Science 289 2000 739 745
9. 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 Å crystal structure J. Mol. Biol. 342 2004 571 583
10. A.B. Patel, E. Crocker, M. Eilers, A. Hirshfeld, M. Sheves, and S.O. Smith Coupling of retinal isomerization to the activation of rhodopsin Proc. Natl Acad. Sci. USA 101 2004 10048 10053
11. Crocker, E. (2005). Structural changes of a light-activated G protein-coupled receptor determined by solid-state NMR: channeling light energy into the visual pigment rhodopsin. PhD thesis, Stony Brook University.
12. 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
13. H. Luecke, B. Schobert, H.T. Richter, J.P. Cartailler, and J.K. Lanyi Structural changes in bacteriorhodopsin during ion transport at 2 angstrom resolution Science 286 1999 255 260
14. A. Aharoni, A. Khatchatouriants, A. Manevitch, A. Lewis, and M. Sheves Protein-β-ionone ring interactions enhance the light-induced dipole of the chromophore in bacteriorhodopsin J. Phys. Chem. Ser. B 107 2003 6221 6225
15. X. Luo, D. Zhang, and H. Weinstein Ligand-induced domain motion in the activation mechanism of a G-protein-coupled receptor Protein Eng. 7 1994 1441 1448
16. M.S.P. Sansom, and H. Weinstein Hinges, swivels and switches: the role of prolines in signalling via transmembrane α-helices Trends Pharmacol. Sci. 21 2000 445 451
17. 2 adrenoceptor EMBO J. 16 1997 6737 6747
18. 2 Adrenergic receptor activation - modulation of the proline kink in transmembrane 6 by a rotamer toggle switch J. Biol. Chem. 277 2002 40989 40996
19. L. Shi, and J.A. Javitch The binding site of aminergic G protein-coupled receptors: the transmembrane segments and second extracellular loop Annu. Rev. Pharmacol. Toxicol. 42 2002 437 467
20. 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
21. P.J.R. Spooner, J.M. Sharples, S.C. Goodall, P.H.M. Bovee-Geurts, M.A. Verhoeven, and J. Lugtenburg The ring of the rhodopsin chromophore in a hydrophobic activation switch within the binding pocket J. Mol. Biol. 343 2004 719 730
22. M. Han, J.H. Lou, K. Nakanishi, T.P. Sakmar, and S.O. Smith Partial agonist activity of 11-cis-retinal in rhodopsin mutants J. Biol. Chem. 272 1997 23081 23085
23. M. Han, S.W. Lin, S.O. Smith, and T.P. Sakmar The effects of amino acid replacements of glycine 121 on transmembrane helix 3 of rhodopsin J. Biol. Chem. 271 1996 32330 32336
24. M. Han, S.W. Lin, M. Minkova, S.O. Smith, and T.P. Sakmar Functional interaction of transmembrane helices 3 and 6 in rhodopsin - replacement of phenylalanine 261 by alanine causes reversion of phenotype of a glycine 121 replacement mutant J. Biol. Chem. 271 1996 32337 32342
25. H. Saito, S. Tuzi, and A. Naito Empirical versus nonempirical evaluation of secondary structure of fibrous and membrane proteins by solid-state NMR: a practical approach Annu. Rep. NMR Spectrosc. 36 1998 79 121
26. R. Richarz, and K. Wüthrich C-13 NMR chemical-shifts of common amino acid residues measured in aqueous solutions of linear tetrapeptides H-Gly-Gly-X-L-Ala-OH Biopolymers 17 1978 2133 2141
27. Schmidt-Rohr, K. & Spiess, H. W. (1994). Multidimensional Solid-State NMR and Polymers. pp. 1-496. Academic Press, London.
28. E. Crocker, A.B. Patel, M. Eilers, S. Jayaraman, E. Getmanova, and P.J. Reeves Dipolar assisted rotational resonance NMR of tryptophan and tyrosine in rhodopsin J. Biomol. NMR 29 2004 11 20
29. S.O. Smith, I. Palings, M.E. Miley, J. Courtin, H. de Groot, and J. Lugtenburg Solid-state NMR studies of the mechanism of the opsin shift in the visual pigment rhodopsin Biochemistry 29 1990 8158 8164
30. G.S. Harbison, P.P.J. Mulder, H. Pardoen, J. Lugtenburg, J. Herzfeld, and R.G. Griffin High-resolution carbon-13 NMR of retinal derivatives in the solid state J. Am. Chem. Soc. 107 1985 4809 4816
31. G.B. Cohen, T. Yang, P.R. Robinson, and D.D. Oprian Constitutive activation of opsin: influence of charge at position 134 and size at position 296 Biochemistry 32 1993 6111 6115
32. J.M. Kim, C. Altenbach, R.L. Thurmond, H.G. Khorana, and W.L. Hubbell Structure and function in rhodopsin: rhodopsin mutants with a neutral amino acid at E134 have a partially activated conformation in the dark state Proc. Natl Acad. Sci. USA 94 1997 14273 14278
33. 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
34. 2A receptor by disruption of the ionic lock of the arginine cage Int. J. Quantum Chem. 88 2002 65 75
35. E.C.Y. Yan, M.A. Kazmi, Z. Ganim, J.M. Hou, D.H. Pan, and B.S.W. Chang Retinal counterion switch in the photoactivation of the G protein-coupled receptor rhodopsin Proc. Natl Acad. Sci. USA 100 2003 9262 9267
36. W. Liu, M. Eilers, A.B. Patel, and S.O. Smith Helix packing moments reveal diversity and conservation in membrane protein structure J. Mol. Biol. 337 2004 713 729
37. M. Eilers, A.B. Patel, W. Liu, and S.O. Smith Comparison of helix interactions in membrane and soluble α-bundle proteins Biophys. J. 82 2002 2720 2736
38. A.B. Patel, E. Crocker, P.J. Reeves, E.V. Getmanova, M. Eilers, H.G. Khorana, and S.O. Smith Changes in interhelical hydrogen bonding upon rhodopsin activation J. Mol. Biol. 347 2005 803 812
39. S.W. Lin, and T.P. Sakmar Specific tryptophan UV-absorbance changes are probes of the transition of rhodopsin to its active state Biochemistry 35 1996 11149 11159
40. B.J. Ebersole, I. Visiers, H. Weinstein, and S.C. Sealfon Molecular basis of partial agonism: orientation of indoleamine ligands in the binding pocket of the human serotonin 5-HT2A receptor determines relative efficacy Mol. Pharmacol. 63 2003 36 43
41. M. Chabre, and J. Breton Orientation of aromatic residues in rhodopsin. Rotation of one tryptophan upon the meta I to meta II transition after illumination Photochem. Photobiol. 30 1979 295 299
42. J.J. Ruprecht, T. Mielke, R. Vogel, C. Villa, and G.F.X. Schertler Electron crystallography reveals the structure of metarhodopsin I EMBO J. 23 2004 3609 3620
43. M.E. Burns, and D.A. Baylor Activation, deactivation, and adaptation in vertebrate, photoreceptor cells Annu. Rev. Neurosci. 24 2001 779 805
44. J.M. Klco, C.B. Wiegand, K. Narzinski, and T.J. Baranski Essential role for the second extracellular loop in C5a receptor activation Nature Struct. Mol. Biol. 12 2005 320 326
45. 2+ as a structural and functional probe Ann. NY Acad. Sci. 994 2003 1 11
46. P.J. Reeves, J.M. Kim, and H.G. Khorana Structure and function in rhodopsin: a tetracycline-inducible system in stable mammalian cell lines for high-level expression of opsin mutants Proc. Natl Acad. Sci. USA 99 2002 13413 13418
47. P.J. Reeves, R.L. Thurmond, and H.G. Khorana Structure and function in rhodopsin: high level expression of a synthetic bovine opsin gene and its mutants in stable mammalian cell lines Proc. Natl Acad. Sci. USA 93 1996 11487 11492
48. 13C-glycine labeled opsin in a stable cell line Proc. Natl Acad. Sci. USA 96 1999 487 492
49. R. Dulbecco, and G. Freeman Plaque production by the polyoma virus Virology 8 1959 396 397
50. M. Eilers, W.W. Ying, P.J. Reeves, H.G. Khorana, and S.O. Smith Magic angle spinning nuclear magnetic resonance of isotopically labeled rhodopsin Methods Enzymol. 343 2002 212 222
51. 13C-labeled retinals Pure Appl. Chem. 57 1985 753 762
52. R.R. Franke, T.P. Sakmar, R.M. Graham, and H.G. Khorana Structure and function in rhodopsin. Studies of the interaction between the rhodopsin cytoplasmic domain and transducin J. Biol. Chem. 267 1992 14767 14774
53. M. Han, M. Groesbeek, S.O. Smith, and T.P. Sakmar Role of the C9 methyl group in rhodopsin activation: characterization of mutant opsins with the artificial chromophore 11-cis-9-demethylretinal Biochemistry 37 1998 538 545
54. K. Fahmy, F. Jäger, M. Beck, T.A. Zvyaga, T.P. Sakmar, and F. Siebert 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
55. M. Beck, F. Siebert, and T.P. Sakmar Evidence for the specific interaction of a lipid molecule with rhodopsin which is altered in the transition to the active state metarhodopsin II FEBS Letters 436 1998 304 308
56. S. Arnis, and K.P. Hofmann Two different forms of metarhodopsin II: Schiff base deprotonation precedes proton uptake and signaling state Proc. Natl Acad. Sci. USA 90 1993 7849 7853
57. G. Metz, X. Wu, and S.O. Smith Ramped-amplitude cross polarization in magic angle spinning NMR J. Magn. Reson. ser. A 110 1994 219 227
58. A.E. Bennett, C.M. Rienstra, M. Auger, K.V. Lakshmi, and R.G. Griffin Heteronuclear decoupling in rotating solids J. Chem. Phys. 103 1995 6951 6958
59. 1H dipolar-assisted rotational resonance in magic-angle spinning NMR Chem. Phys. Letters 344 2001 631 637
60. J.A. Ballesteros, and H. Weinstein Integrated methods for the construction of three dimensional models and computational probing of structure-function relations in G-protein coupled receptors Methods Neurosci. 25 1995 366 428