Conformational states and dynamics of rhodopsin in micelles and bilayers

Biochemistry

Volumn 45, Issue 17, 2006, Pages 5538-5550

  Kusnetzow, Ana Karin ^a   Altenbach, Christian ^a   Hubbell, Wayne L ^a  

^a JULES STEIN EYE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPOSITION; CONFORMATIONS; CYTOLOGY; LIGHT ABSORPTION; MICELLES; MOLECULAR DYNAMICS; PARAMAGNETIC RESONANCE; PH EFFECTS;

DIGITONIN; DODECYL MALTOSIDE (DM); PHOSPHOLIPID BILAYERS; RHODOPSIN;

CHEMICAL SENSORS;

DIGITONIN; DODECYL MALTOSIDE; FUNCTIONAL GROUP; GLYCOSIDE; NITROXIDE; RHODOPSIN; UNCLASSIFIED DRUG;

ARTICLE; BILAYER MEMBRANE; CELL SURFACE; CONFORMATIONAL TRANSITION; CYTOPLASM; ELECTRON SPIN RESONANCE; LIGHT ABSORPTION; MICELLE; MOLECULAR DYNAMICS; PH; PHOSPHOLIPID BILAYER; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; SENSOR; TRANSMEMBRANE HELIX VI;

AMINO ACID SUBSTITUTION; ANIMALS; CYCLIC N-OXIDES; DIGITONIN; ELECTRON SPIN RESONANCE SPECTROSCOPY; GLUCOSIDES; LIPID BILAYERS; MEMBRANES, ARTIFICIAL; MESYLATES; MICELLES; PROTEIN CONFORMATION; RHODOPSIN; SPIN LABELS;

EID: 33646382407     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060101v     Document Type: Article

References (81)

1. Gether, U. (2000) Uncovering molecular mechanisms involved in activation of G protein-coupled receptors, Endocr. Rev. 21, 90-113.
2. 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., Yamanoto, M., and Miyano, M. (2000) Crystal structure of rhodopsin: a G protein-coupled receptor, Science 289, 739-745.
3. Teller, D. C., Okada, T., Behnke, C. A., Palczewski, K., and Stenkamp, R. E. (2001) Advances in determination of a high-resolution three-dimensional structure of rhodopsin, a model of G protein-coupled receptors (GPCRs), Biochemistry 40, 7761-7772.
4. Okada, T., Fujiyoshi, Y., Silow, M., Navarro, J., Landau, E. M., and Shichida, Y. (2002) Functional role of internal water molecules in rhodopsin revealed by X-ray crystallography, Proc. Natl. Acad. Sci. U.S.A. 99, 5982-5987.
5. Li, J., Edwards, P. C., Burghammer, M., Villa, C., and Schertler, G. F. (2004) Structure of bovine rhodopsin in a trigonal crystal form, J. Mol. Biol. 343, 1409-1438.
6. Lewis, J. W., and Kliger, D. S. (1992) Photointermediates of visual pigments, J. Bioenerg. Biomembr. 24, 201-210.
7. Melia, T. J., Cowan, C. W., Angleson, J. K., and Wensel, T. G. (1997) A comparison of the efficiency of G protein activation by ligand-free and light-activated forms of rhodopsin, Biophys. J. 73, 3182-3191.
8. Rao, V. R., and Oprian, D. D. (1996) Activating mutations of rhodopsin and other G protein-coupled receptors, Annu. Rev. Biophys. Biomol. Struct. 25, 287-314.
9. Vogel, R., and Siebert, F. (2001) Conformations of the active and inactive states of opsin, J. Biol. Chem. 276, 38487-38493.
10. Schoenlein, R. W., Peteanu, L. A., Mathies, R. A., and Shank, C. V. (1991) The first step in vision: femtosecond isomerization of rhodopsin, Science 254, 412-415.
11. Emeis, D., Kühn, H., Reichert, J., and Hofmann, K. P. (1982) Complex formation between metarhodopsin II and the GTP-binding protein in bovine photoreceptor membranes leads to a shift of the photoproduct equilibrium, FEBS Lett. 143, 29-34.
12. Heck, M., Schädel, S. A., Maretzki, D., Bartl, F., Ritter, E., Palczewski, K., and Hofmann, K. P. (2003) Signaling states of rhodopsin: formation of the storage form, metarhodopsin III, from active metarhodopsin II, J. Biol. Chem. 278, 3162-3169.
13. Longstaff, C., Calhoon, R. D., and Rando, R. R. (1986) Deprotonation of the Schiff base of rhodopsin is obligate in the activation of the G protein, Proc. Natl. Acad. Sci. U.S.A. 83, 4209-4213.
14. Sakmar, T. P., Franke, R. R., and Khorana, H. G. (1989) Glutamic acid-113 serves as the retinylidene Schiff base counterion in bovine rhodopsin, Proc. Natl. Acad. Sci. U.S.A. 86, 8309-8313.
15. Zhukovsky, E. A., and Oprian, D. D. (1989) Effect of carboxylic acid side chains on the absorption of visual pigments, Science 246, 928-930.
16. Yan, E. C. Y., Kazmi, M. A., Ganim, Z., Hou, J. M., Pan, D., Chang, B. S. W., Sakmar, T. P., and Mathies, R. A. (2003) Retinal counterion switch in the photoactivation of the G protein-coupled receptor rhodopsin, Proc. Natl. Acad. Sci. U.S.A. 100, 9262-9267.
17. Kim, J. M., Altenbach, C., Kono, M., Oprian, D. D., Hubbell, W. L., and Khorana, H. G. (2004) Structural origins of constitutive activation in rhodopsin: role of the K296/E113 salt bridge, Proc. Natl. Acad. Sci. U.S.A. 101, 12508-12513.
18. König, B., Welte, W., and Hofmann, K. P. (1989) Photoactivation of rhodopsin and interactions with transducin in detergent micelles. Effect of "doping" with steroid molecules, FEBS Lett. 257, 163-166.
19. Resek, J. F., Farahbakhsh, Z. T., Hubbell, W. L., and Khorana, H. G. (1993) Formation of the meta II photointermediate is accompanied by conformational changes in the cytoplasmic surface of rhodopsin, Biochemistry 32, 12025-12032.
20. Arnis, S., and Hofmann, K. P. (1993) Two different forms of metarhodopsin II: Schiff base deprotonation precedes proton uptake and signaling, Proc. Natl. Acad. Sci. U.S.A. 90, 7849-7853.
21. Stewart, J. G., Baker, B. N., and Williams, T. P. (1977) Evidence for conformeric states of rhodopsin, Biophys. Struct. Mech. 3, 19-29.
22. Bubis, J. (1998) Effects of detergents and lipids on transducin photoactivation by rhodopsin, Biol. Res. 31, 59-71.
23. Szundi, I., Lewis, J. W., and Kliger, D. S. (2005) Effect of digitonin on the rhodopsin meta I-meta II equilibrium, Photochem. Photobiol. 81, 866-873.
24. Ruprecht, J. J., Mielke, T., Vogel, R., Villa, C., and Schertler, G. F. (2004) Electron crystallography reveals the structure of metarhodopsin I, EMBO J. 23, 3609-3620.
25. Hubbell, W. L., Cafiso, D. S., and Altenbach, C. (2000) Identifying conformational changes with site-directed spin labeling, Nat. Struct. Biol. 7, 735-739.
26. Hubbell, W. L., Altenbach, C., Hubbell, C. M., and Khorana, H. G. (2003) Rhodopsin structure, dynamics, and activation: a perspective from cystallography, site-directed spin labeling, sulfhydryl reactivity, and disulfide cross-linking, Adv. Protein Chem. 63, 243-290.
27. Vogel, R., and Siebert, F. (2003) Fourier transform IR spectroscopy study for new insights into molecular properties and activation mechanisms of visual pigment rhodopsin, Biopolymers 73, 133-148.
28. Klein-Seetharaman, J., Yanamala, N. V., Javeed, F., Reeves, P. J., Getmanova, E. V., Loewen, M. C., Schwalbe, H., and Khorana, H. G. (2004) Differential dynamics in the G-protein coupled receptor rhodopsin revealed by solution NMR, Proc. Natl. Acad. Sci. U.S.A. 101, 3409-3413.
29. 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.
30. Farrens, D. L., Altenbach, C., Yang, K., Hubbell, W. L., and Khorana, H. G. (1996) Requirement of rigid-body motion of transmembrane helices for light activation of rhodopsin, Science 274, 768-770.
31. Janz, J. M., and Farrens, D. L. (2004) Rhodopsin activation exposes a key hydrophobic binding site for the transducin α-subunit C terminus, J. Biol. Chem. 279, 29767-29773.
32. Elling, C. E., Nielsen, S. M., and Schwartz, T. W. (1995) Conversion of antagonist-binding site to metal-ion site in the tachykinin NK-1 receptor, Nature 374, 74-77.
33. 2 adrenergic receptor, J. Pept. Res. 60, 317-321.
34. Knudsen, P., and Hubbell, W. L. (1978) Stability of rhodopsin in detergent solutions, Membr. Biochem. 1, 297-322.
35. Ramon, E., Marron, J., del Valle, L., Bosch, L., Andrés, A., Manyosa, J., and Garriga, P. (2003) Effect of dodecyl maltoside detergent on rhodopsin stability and function, Vision Res. 43, 3055-3061.
36. Kim, J. M., Altenbach, C., Thurmond, R. L., Khorana, H. G., and Hubbell, W. L. (1997) 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. U.S.A. 94, 14273-14278.
37. Krebs, A., Edwards, P. C., Villa, C., Li, J., and Schertler, G. F. (2003) The three-dimensional structure of bovine rhodopsin determined by electron cryomicroscopy, J. Biol. Chem. 278, 50217-50225.
38. Oprian, D. D., Molday, R. S., Kaufman, R. J., and Khorana, H. G. (1987) Expression of a synthetic bovine rhodopsin gene in monkey kidney cells, Proc. Natl. Acad. Sci. U.S.A. 84, 8874-8878.
39. Robinson, P. R. (2000) Assays for detection of constitutively active opsin, Methods Enzymol. 315, 207-218.
40. Patemostre, M. T., Roux, M., and Rigaud, J. L. (1988) Mechanisms of membrane protein insertion into liposomes during reconstitution procedures involving the use of detergents. 1. Solubilization of large unilamellar liposomes (prepared by reverse-phase evaporation) by Triton X-100, octyl glucoside, and sodium cholate, Biochemistry 27, 2668-2677.
41. Rigaud, J. L., Pitard, B., and Levy, D. (1995) Reconstitution of membrane proteins into liposomes: application to energy-transducing membrane proteins, Biochim. Biophys. Acta 1231, 223-246.
42. Niu, L., Kim, J. M., and Khorana, H. G. (2002) Structure and function in rhodopsin: asymmetric reconstitution of rhodopsin in liposomes, Proc. Natl. Acad. Sci. U.S.A. 99, 13409-13412.
43. Hong, K., and Hubbell, W. L. (1972) Preparation and properties of phospholipid bilayers containing rhodopsin, Proc. Natl. Acad. Sci. U.S.A. 69, 2617-2621.
44. Bartlett, G. R. (1959) Phosphorous assay in column chromatography, J. Biol. Chem. 234, 466-468.
45. Mangold, H. K. (1967) Aliphatic lipids, in Thin-layer Chromatography (Stahl, E., Ed.) pp 363-415, Springer-Verlag, Berlin and New York.
46. Bhattacharya, S., Ridge, K. D., Knox, B. E., and Khorana, H. G. (1992) Light-stable rhodopsin. I. A rhodopsin analog reconstituted with a nonisomerizable 11-cis retinal derivative, J. Biol. Chem. 267, 6763-6769.
47. Columbus, L., Kálai, T., Jekö, J., Hideg, K., and Hubbell, W. L. (2001) Molecular motion of spin labeled side chains in α-helices: analysis by variation of side chain structure, Biochemistry 40, 3828-3846.
48. Budil, D. E., Lee, S., Saxena, S., and Freed, J. H. (1996) Nonlinear-least-squares analysis of slow-motion EPR spectra in one and two dimensions using a modified Levenberg-Marquardt algorithm, J. Magn. Reson. 120, 155-189.
49. Freed, J. H. (1976) Theory of slow tumbling ESR spectra for nitroxides, in Spin Labeling. Theory and Applications (Berliner, L. J., Ed.) pp 53-132, Academic Press, New York.
50. Langen, R., Oh, K. J., Cascio, D., and Hubbell, W. L. (2000) Crystal structures of spin labeled T4 lysozyme mutants: implications for the interpretation of EPR spectra in terms of structure, Biochemistry 39, 8396-8405.
51. Liang, Z., Lou, Y., Freed, J. H., Columbus, L., and Hubbell, W. L. (2004) A multifrequency electron spin resonance study of T4 lysozyme dynamics using the slowly relaxing local structure model, J. Phys. Chem. B 108, 17649-17659.
52. Columbus, L., and Hubbell, W. L. (2004) Mapping backbone dynamics in solution with site-directed spin labeling: GCN5-58 bZip free and bound to DNA, Biochemistry 43, 7273-7287.
53. Lietzow, M. A., and Hubbell, W. L. (2004) Motion of spin label side chains in cellular retinol-binding protein: correlation with structure and nearest-neighbor interactions in an antiparallel β-sheet, Biochemistry 43, 3137-3151.
54. Lovell, S. C., Word, J. M., Richardson, J. S., and Richardson, D. C. (2000) The penultimate rotamer library, Proteins 40, 389-408.
55. Daemen, F. J. (1973) Vertebrate rod outer segment membranes, Biochim. Biophys. Acta 300, 255-288.
56. Gibson, N. J., and Brown, M. F. (1993) Lipid headgroup and acyl chain composition modulate the MI-MII equilibrium of rhodopsin in recombinant membranes, Biochemistry 32, 2438-2454.
57. Botelho, A. V., Gibson, N. J., Thurmond, R. L., Wang, Y., and Brown, M. F. (2002) Conformational energetics of rhodopsin modulated by nonlamellar-forming lipids, Biochemistry 41, 6354-6368.
58. Isas, J. M., Langen, R., Hubbell, W. L., and Haigler, H. T. (2004) Structure and dynamics of a helical hairpin that mediates calcium-dependent membrane binding of annexin B12, J. Biol. Chem. 279, 32492-32498.
59. Chabre, M., and le Maire, M. (2005) Monomeric G-protein-coupled receptor as a functional unit, Biochemistry 44, 9395-9403.
60. Liang, Y., Fotiadis, D., Filipek, S., Saperstein, D. A., Palczewski, K., and Engel, A. (2003) Organization of the G protein-coupled receptor rhodopsin and opsin in membranes, J. Biol. Chem. 278, 21655-21662.
61. Jastrzebska, B., Maeda, T., Zhu, L., Fotiadis, D., Filipek, S., Engel, A., Stenkamp, R. E., and Palczewski, K. (2004) Functional characterization of rhodopsin monomers and dimers in detergents, J. Biol. Chem. 279, 54663-54675.
62. Filipek, S., Krzysko, K., Fotiadis, D., Liang, J., Saperstein, D. A., Engel, A., and Palczewski, K. (2004) A concept for G-protein activation by G protein-coupled receptor dimers: the transducin/rhodopsin interface, Photochem. Photobiol Sci. 3, 628-638.
63. Altenbach, C., Yang, K., Farrens, D. L., Farahbakhsh, Z. T., Khorana, H. G., and Hubbell, W. L. (1996) Structural features and light-dependent changes in the cytoplasmic interhelical E-F loop region of rhodopsin: a site-directed spin-labeling study, Biochemistry 35, 12470-12478.
64. Schertler, G. F. (2005) Structure of rhodopsin and the meta-rhodopsin I photointermediate, Curr. Opin. Struct. Biol. 15, 408-415.
65. Medina, R., Perdomo, D., and Bubis, J. (2004) The hydrodynamic properties of dark- and light-activated states of n-dodecyl-β-D-maltoside-solubilized bovine rhodopsin support the dimeric structure of both conformations, J. Biol. Chem. 279, 39565-39573.
66. Baroin, A., Thomas, D. D., Osborne, B., and Devaux, P. F. (1977) Saturation transfer electron paramagnetic resonance on membrane-bound proteins. I. Rotational diffusion of rhodopsin in the visual receptor membrane, Biochem. Biophys. Res. Commun. 78, 442-447.
67. Kusumi, A., and Hyde, J. S. (1982) Spin-label saturation-transfer electron spin resonance detection of transient association of rhodopsin in reconstituted membranes, Biochemistry 21, 5978-5983.
68. Mchaourab, H. S., Lietzow, M. A., Hideg, K., and Hubbell, W. L. (1996) Motion of spin-labeled side chains in T4 lysozyme. Correlation with protein structure and dynamics, Biochemistry 35, 7692-7704.
69. Hong, K., and Hubbell, W. L. (1973) Lipid requirements for rhodopsin regenerability, Biochemistry 12, 4517-4523.
70. Columbus, L., and Hubbell, W. L. (2002) A new spin on protein dynamics, Trends Biochem. Sci. 27, 288-295.
71. Dan, A., and Safran, S. A. (1998) Effect of lipid characteristics on the structure of transmembrane proteins, Biophys. J. 75, 1410-1414.
72. Baldwin, P. A., and Hubbell, W. L. (1985) Effects of lipid environment on the light-induced conformational changes of rhodopsin. 2. Roles of lipid chain length, unsaturation, and phase state, Biochemistry 24, 2633-2639.
73. Brown, M. F. (1994) Modulation of rhodopsin function by properties of the membrane bilayer, Chem. Phys. Lipids 73, 159-180.
74. Krishna, A. G., Menon, S. T., Terry, T. J., and Sakmar, T. P. (2002) Evidence that helix 8 of rhodopsin acts as a membrane-dependent conformational switch, Biochemistry 41, 8298-8309.
75. Mouritsen, O. G., and Bloom, M. (1984) Mattress model lipid-protein interactions in membranes, Biophys. J. 46, 141-153.
76. Gruner, S. M. (1985) Intrinsic curvature hypothesis for biomembrane lipid composition: a role for nonbilayer lipids, Proc. Natl. Acad. Sci. U.S.A. 82, 3665-3669.
77. Gibson, N. J., and Brown, M. F. (1991) Role of phosphatidylserine in the MI-MII equilibrium of rhodopsin, Biochem. Biophys. Res. Commun. 176, 915-921.
78. Hessel, E., Heck, M., Muller, P., Herrmann, A., and Hofmann, K. P. (2003) Signal transduction in the visual cascade involves specific lipid-protein interactions, J. Biol. Chem. 278, 22853-22860.
79. α phase: A comparison of phosphatidylcholine and phosphatidylethanolamine membranes, Recent Res. Dev. Biophys. 3, 363-392.
80. II phases, Biochemistry 29, 8325-8333.
81. a values for phosphatidylserine and phosphatidylethanolamine in phosphatidylcholine host bilayers, Biophys. J. 49, 459-468.