The supramolecular structure of the GPCR rhodopsin in solution and native disc membranes

References

• Gether, U., 2000, Uncovering molecular mechanisms involved in activation of G protein-coupled receptors. Endocr. Rev., 21, 90 -113.
   PubMed Web of Science ®Google Scholar
• Mirzadegan, T., Benko, G., Filipek, S. and Palczewski, K., 2003, Sequence analyses of G-protein-coupled receptors: similarities to rhodopsin. Biochemistry, 42, 2759–2767.
   PubMed Web of Science ®Google Scholar
• Ballesteros, J. and Palczewski, K., 2001, G protein-coupled receptor drug discovery: implications from the crystal structure of rhodopsin. Curr. Opin. Drug Discov. Devel., 4, 561 -574.
   PubMedGoogle Scholar
• Ballesteros, J. A., Shi, L. and Javitch, J. A., 2001, Structural mimicry in G protein-coupled receptors: implications of the high- resolution structure of rhodopsin for structure-function analysis of rhodopsin-like receptors. Mol. Pharmacol., 60, 1 -19.
   PubMed Web of Science ®Google Scholar
• Pierce, K. L. and Lefkowitz, R. J., 2001, Classical and new roles of beta-arrestins in the regulation of G-protein-coupled recep- tors. Nat. Rev. Neurosci., 2, 727 -733.
   PubMed Web of Science ®Google Scholar
• Pierce, K. L., Premont, R. T. and Lefkowitz, R. J., 2002, Seven- transmembrane receptors. Nat. Rev. Mol. Cell Biol., 3, 639 - 650.
   PubMed Web of Science ®Google Scholar
• Limbird, L. E. and Lefkowitz, R. J., 1976, Negative cooperativity among beta-adrenergic receptors in frog erythrocyte mem- branes. J. Biol. Chem., 251, 5007 -5014.
   PubMed Web of Science ®Google Scholar
• Jordan, B. A. and Devi, L. A., 1999, G-protein-coupled receptor heterodimerization modulates receptor function. Nature, 399, 697 -700.
   PubMed Web of Science ®Google Scholar
• Rodbell, M., 1995, Nobel Lecture. Signal transduction: evolution of an idea. Biosci. Rep., 15, 117 -133.
   PubMedGoogle Scholar
• Angers, S., Salahpour, A. and Bouvier, M., 2001, Biochemical and biophysical demonstration of GPCR oligomerization in mammalian cells. Life Sci., 68, 2243 -2250.
   PubMedGoogle Scholar
• Angers, S., Salahpour, A. and Bouvier, M., 2002, Dimerization: an emerging concept for G protein-coupled receptor ontogeny and function. Annu. Rev. Pharmacol. Toxicol., 42, 409 -435.
   PubMed Web of Science ®Google Scholar
• Filizola, M., Olmea, O. and Weinstein, H., 2002, Prediction of heterodimerization interfaces of G-protein coupled receptors with a new subtractive correlated mutation method. Protein Eng., 15, 881 -885.
   PubMedGoogle Scholar
• Rios, C. D., Jordan, B. A., Gomes, I. and Devi, L. A., 2001, G- protein-coupled receptor dimerization: modulation of receptor function. Pharmacol. Ther., 92, 71 -87.
   PubMed Web of Science ®Google Scholar
• Terrillon, S. and Bouvier, M., 2004, Roles of G-protein-coupled receptor dimerization. EMBO Rep., 5, 30 -34.
   PubMed Web of Science ®Google Scholar
• Breitwieser, G. E., 2004, G protein-coupled receptor oligomer- ization: implications for G protein activation and cell signaling. Circ. Res., 94, 17 -27.
   PubMedGoogle Scholar
• Milligan, G., Ramsay, D., Pascal, G. and Carrillo, J. J., 2003, GPCR dimerisation. Life Sci., 74, 181 -188.
   PubMedGoogle Scholar
• Bai, M., 2004, Dimerization of G-protein-coupled receptors: roles in signal transduction. Cell Signal., 16, 175 -186.
   PubMed Web of Science ®Google Scholar
• Jones, K. A., Borowsky, B., Tamm, J. A., Craig, D. A., Durkin, M. M., Dai, M., Yao, W. J., Johnson, M., Gunwaldsen, C., Huang, L. Y., Tang, C., Shen, Q., Salon, J. A., Morse, K., Laz, T., Smith, K. E., Nagarathnam, D., Noble, S. A., Branchek, T. A. and Gerald, C., 1998, GABA(B) receptors function as a heteromeric assembly of the subunits GABA(B)R1 and GA- BA(B)R2. Nature, 396, 674 -679.
   PubMed Web of Science ®Google Scholar
• Margeta-Mitrovic, M., Jan, Y. N. and Jan, L. Y., 2001, Ligand- induced signal transduction within heterodimeric GABA(B) receptor. Proc. Natl Acad. Sci. USA, 98, 14643–14648.
   PubMed Web of Science ®Google Scholar
• Margeta-Mitrovic, M., Jan, Y. N. and Jan, L. Y., 2001, Function of GB1 and GB2 subunits in G protein coupling of GABA(B) receptors. Proc. Natl Acad. Sci. USA, 98, 14649–14654.
   PubMed Web of Science ®Google Scholar
• Kunishima, N., Shimada, Y., Tsuji, Y., Sato, T., Yamamoto, M., Kumasaka, T., Nakanishi, S., Jingami, H. and Morikawa, K., 2000, Structural basis of glutamate recognition by a dimeric metabotropic glutamate receptor. Nature, 407, 971 -977.
   PubMed Web of Science ®Google Scholar
• Chinault, S. L., Overton, M. C. and Blumer, K. J., 2004, Subunits of a yeast oligomeric G protein-coupled receptor are activated independently by agonist but function in concert to activate G protein heterotrimers. J. Biol. Chem., 279, 16091- 16100.
   PubMedGoogle Scholar
• Guo, W., Shi, L. and Javitch, J. A., 2003, The fourth transmembrane segment forms the interface of the dopamine D2 receptor homodimer. J. Biol. Chem., 278, 4385 -4388.
   PubMedGoogle Scholar
• Baneres, J. L. and Parello, J., 2003, Structure-based analysis of GPCR function: evidence for a novel pentameric assembly between the dimeric leukotriene B4 receptor BLT1 and the G- protein. J. Mol. Biol., 329, 815 -829.
   PubMed Web of Science ®Google Scholar
• McBee, J. K., Palczewski, K., Baehr, W. and Pepperberg, D. R., 2001, Confronting complexity: the interlink of phototransduction and retinoid metabolism in the vertebrate retina. Prog. Retin. Eye Res., 20, 469 -529.
   PubMed Web of Science ®Google Scholar
• Polans, A., Baehr, W. and Palczewski, K., 1996, Turned on by Ca2+! The physiology and pathology of Ca(2+)-binding proteins in the retina. Trends Neurosci., 19, 547 -554.
   Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Baylor, D. A., Lamb, T. D. and Yau, K. W., 1979, Responses of retinal rods to single photons. J. Physiol., 288, 613 -634.
   PubMed Web of Science ®Google Scholar
• Molday, R. S., 1998, Photoreceptor membrane proteins, photo- transduction, and retinal degenerative diseases. The Frieden- wald Lecture. Invest. Ophthalmol. Vis. Sci., 39, 2491 -2513.
   PubMedGoogle Scholar
• Humphries, M. M., Rancourt, D., Farrar, G. J., Kenna, P., Hazel, M., Bush, R. A., Sieving, P. A., Sheils, D. M., McNally, N., Creighton, P., Erven, A., Boros, A., Gulya, K., Capecchi, M. R. and Humphries, P., 1997, Retinopathy induced in mice by targeted disruption of the rhodopsin gene. Nature Genet., 15, 216 -219.
   PubMed Web of Science ®Google Scholar
• Lem, J., Krasnoperova, N. V., Calvert, P. D., Kosaras, B., Cameron, D. A., Nicolo, M., Makino, C. L. and Sidman, R. L., 1999, Morphological, physiological, and biochemical changes in rhodopsin knockout mice. Proc. Natl Acad. Sci. USA, 96, 736 - 741.
   PubMed Web of Science ®Google Scholar
• Filipek, S., Stenkamp, R. E., Teller, D. C. and Palczewski, K., 2003, G protein-coupled receptor rhodopsin: a prospectus. Annu. Rev. Physiol., 65, 851 -879.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Okada, T. and Palczewski, K., 2001, Crystal structure of rhodopsin: implications for vision and beyond. Curr. Opin. Struct. Biol., 11, 420 -426.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Stenkamp, R. E., Filipek, S., Driessen, C. A., Teller, D. C. and Palczewski, K., 2002, Crystal structure of rhodopsin: a template for cone visual pigments and other G protein-coupled receptors. Biochim. Biophys. Acta, 1565, 168 -182.
   PubMedGoogle Scholar
• Menon, S. T., Han, M. and Sakmar, T. P., 2001, Rhodopsin: structural basis of molecular physiology. Physiol. Rev., 81, 1659–1688.
   PubMedGoogle Scholar
• Filipek, S., Teller, D. C., Palczewski, K. and Stenkamp, R., 2003, The crystallographic model of rhodopsin and its use in studies of other G protein-coupled receptors. Annu. Rev. Biophys. Biomol. Struct., 32, 375 -397.
   PubMedGoogle Scholar
• Nair, K. S., Balasubramanian, N. and Slepak, V. Z., 2002, Signal-dependent translocation of transducin, RGS9-1-Gbeta5L complex, and arrestin to detergent-resistant membrane rafts in photoreceptors. Curr. Biol., 12, 421 -425.
   PubMedGoogle Scholar
• Seno, K., Kishimoto, M., Abe, M., Higuchi, Y., Mieda, M., Owada, Y., Yoshiyama, W., Liu, H. and Hayashi, F., 2001, Light- and guanosine 5?-3-O-(thio)triphosphate-sensitive locali- zation of a G protein and its effector on detergent-resistant membrane rafts in rod photoreceptor outer segments. J. Biol. Chem., 276, 20813–20816.
   PubMedGoogle Scholar
• Elliott, M. H., Fliesler, S. J. and Ghalayini, A. J., 2003, Cholesterol-dependent association of caveolin-1 with the trans- ducin alpha subunit in bovine photoreceptor rod outer seg- ments: disruption by cyclodextrin and guanosine 5?-O-(3- thiotriphosphate). Biochemistry, 42, 7892–7903.
   PubMedGoogle Scholar
• Fotiadis, D., Liang, Y., Filipek, S., Saperstein, D. A., Engel, A. and Palczewski, K., 2003, Atomic-force microscopy: rhodopsin dimers in native disc membranes. Nature, 421, 127 -128.
   PubMed Web of Science ®Google Scholar
• Fotiadis, D., Liang, Y., Filipek, S., Saperstein, D. A., Engel, A. and Palczewski, K., 2004, The G protein-coupled receptor rhodopsin in the native membrane. FEBS Letters, 564, 281 - 288.
   PubMed Web of Science ®Google Scholar
• Liang, Y., Fotiadis, D., Filipek, S., Saperstein, D. A., Palc- zewski, K. and Engel, A., 2003, Organization of the G protein- coupled receptors rhodopsin and opsin in native membranes. J. Biol. Chem., 278, 21655–21662.
   PubMedGoogle Scholar
• Filipek, S., Krzysko, K. A., Fotiadis, D., Liang, Y., 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, 1 -12.
   PubMedGoogle Scholar
• Ridge, K. D., Abdulaev, N. G., Sousa, M. and Palczewski, K., 2003, Phototransduction: crystal clear. Trends Biochem. Sci., 28, 479 -487.
   PubMed Web of Science ®Google Scholar
• Medina, R., Perdomo, D. and Bubis, J., 2004, The hydrody- namic properties of dark and light-activated states of n-dodecyl- [beta]-D-maltoside-solubilized bovine rhodopsin support the dimeric structure of both conformations. J. Biol. Chem ., 279, 39565 -39573.
   Google Scholar
• Arimoto, R., Kisselev, O. G., Makara, G. M. and Marshall, G. R., 2001, Rhodopsin-transducin interface: studies with conforma- tionally constrained peptides. Biophys. J., 81, 3285–3293.
   PubMed Web of Science ®Google Scholar
• Hamm, H. E., 2001, How activated receptors couple to G proteins. Proc. Natl Acad. Sci. USA, 98, 4819 -4821.
   PubMed Web of Science ®Google Scholar
• Marshall, G. R., 2001, Peptide interactions with G-protein coupled receptors. Biopolymers, 60, 246 -277.
   PubMedGoogle Scholar
• Liebman, P. A., Parker, K. R. and Dratz, E. A., 1987, The molecular mechanism of visual excitation and its relation to the structure and composition of the rod outer segment. Annu. Rev. Physiol., 49, 765 -791.
   Google Scholar
• Cone, R. A., 1972, Rotational diffusion of rhodopsin in the visual receptor membrane. Nat. New Biol., 236, 39 -43.
   PubMedGoogle Scholar
• Poo, M. and Cone, R. A., 1974, Lateral diffusion of rhodopsin in the photoreceptor membrane. Nature, 247, 438 -441.
   PubMed Web of Science ®Google Scholar
• Liebman, P. A. and Entine, G., 1974, Lateral diffusion of visual pigment in photoreceptor disk membranes. Science, 185, 457 - 459.
   PubMed Web of Science ®Google Scholar
• Saibil, H., Chabre, M. and Worcester, D., 1976, Neutron diffraction studies of retinal rod outer segment membranes. Nature, 262, 266 -270.
   PubMed Web of Science ®Google Scholar
• Downer, N. W. and Cone, R. A., 1985, Transient dichroism in photoreceptor membranes indicates that stable oligomers of rhodopsin do not form during excitation. Biophys. J., 47, 277 - 284.
   PubMedGoogle Scholar
• Papermaster, D. S., 1982, Preparation of retinal rod outer segments. Methods Enzymol., 81, 48 -52.
   PubMed Web of Science ®Google Scholar
• Heuberger, E. H., Veenhoff, L. M., Duurkens, R. H., Friesen, R. H. and Poolman, B., 2002, Oligomeric state of membrane transport proteins analyzed with blue native electrophoresis and analytical ultracentrifugation. J. Mol. Biol., 317, 591 -600.
   PubMedGoogle Scholar
• Papac, D. I., Thornburg, K. R., Bullesbach, E. E., Crouch, R. K. and Knapp, D. R., 1992, Palmitylation of a G-protein coupled receptor. Direct analysis by tandem mass spectrometry. J. Biol. Chem., 267, 16889–16894.
   PubMed Web of Science ®Google Scholar
• Hargrave, P. A., 1982, Rhodopsin chemistry, structure and topography. In N. N. Osbourne and G. J. Chader, eds Progress in Retinal Research (Pergamon Press, New York), pp. 1 -51.
   Google Scholar
• Jap, B. K., Zulauf, M., Scheybani, T., Hefti, A., Baumeister, W., Aebi, U. and Engel, A., 1992, 2D crystallization: from art to science. Ultramicroscopy, 46, 45 -84.
   PubMed Web of Science ®Google Scholar
• Liang, Y., Fotiadis, D., Maeda, T., Maeda, A., Modzelewska, A., Filipek, S., Saperstein, D. A., Engel, A. and Palczewski, K., 2004, Rhodopsin signaling and organization in heterozygote rhodopsin knockout mice. J. Biol. Chem ., 279, 48189 -48196.
   Google Scholar
• Scha¨ gger, H. and von Jagow, G., 1991, Blue native electro- phoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem., 199, 223 -231.
   PubMedGoogle Scholar
• Lee, S. P., O’Dowd, B. F. and George, S. R., 2003, Homo- and hetero-oligomerization of G protein-coupled receptors. Life Sci., 74, 173 -180.
   PubMed Web of Science ®Google Scholar
• Okada, T., Le Trong, I., Fox, B. A., Behnke, C. A., Stenkamp, R.E. and Palczewski, K., 2000, X-Ray diffraction analysis of three- dimensional crystals of bovine rhodopsin obtained from mixed micelles. J. Struct. Biol., 130, 73 -80.
   PubMed Web of Science ®Google Scholar
• Janz, J. M. and Farrens, D. L., 2004, Rhodopsin activation exposes a key hydrophobic binding site for the transducin alpha-subunit C-terminus. J. Biol. Chem., 279, 29767–29773.
   PubMed Web of Science ®Google Scholar
• Downer, N. W., 1985, Cross-linking of dark-adapted frog photoreceptor disk membranes. Evidence for monomeric rho- dopsin. Biophys. J., 47, 285 -293.
   PubMed Web of Science ®Google Scholar
• Hermanson, G. T., 1996, Bioconjugate techniques (Academic Press, San Diego).
   Google Scholar
• Cobb, C. E. and Beth, A. H., 1990, Identification of the eosinyl- 5-maleimide reaction site on the human erythrocyte anion- exchange protein: overlap with the reaction sites of other chemical probes. Biochemistry, 29, 8283–8290.
   PubMedGoogle Scholar
• Barclay, P. L. and Findlay, J. B., 1984, Labelling of the cytoplasmic domains of ovine rhodopsin with hydrophilic chemical probes. Biochem. J., 220, 75 -84.
   PubMedGoogle Scholar
• Imamoto, Y., Kataoka, M., Tokunaga, F. and Palczewski, K., 2000, Light-induced conformational changes of rhodopsin probed by fluorescent alexa594 immobilized on the cytoplasmic surface. Biochemistry, 39, 15225–15233.
   PubMedGoogle Scholar
• Ovchinnikov Yu, A., Abdulaev, N. G. and Bogachuk, A. S., 1988, Two adjacent cysteine residues in the C-terminal cytoplasmic fragment of bovine rhodopsin are palmitylated. FEBS Letters, 230, 1 -5.
   Google Scholar
• Gelasco, A., Crouch, R. K. and Knapp, D. R., 2000, Intrahelical arrangement in the integral membrane protein rhodopsin investigated by site-specific chemical cleavage and mass spectrometry. Biochemistry, 39, 4907 -4914.
   PubMedGoogle Scholar
• Cai, K., Klein-Seetharaman, J., Hwa, J., Hubbell, W. L. and Khorana, H. G., 1999, Structure and function in rhodopsin: effects of disulfide cross-links in the cytoplasmic face of rhodopsin on transducin activation and phosphorylation by rhodopsin kinase. Biochemistry, 38, 12893–12898.
   PubMed Web of Science ®Google Scholar
• Yang, K., Farrens, D. L., Altenbach, C., Farahbakhsh, Z. T., Hubbell, W. L. and Khorana, H. G., 1996, Structure and function in rhodopsin. Cysteines 65 and 316 are in proximity in a rhodopsin mutant as indicated by disulfide formation and interactions between attached spin labels. Biochemistry, 35, 14040–14046.
   PubMed Web of Science ®Google Scholar
• Yu, H., Kono, M. and Oprian, D. D., 1999, State-dependent disulfide cross-linking in rhodopsin. Biochemistry, 38, 12028- 12032.
   PubMedGoogle Scholar
• Saxton, W. O., 1996, Semper: Distortion compensation, selec- tive averaging, 3-D reconstruction, and transfer function correc- tion in a highly programmable system. J. Struct. Biol., 116, 230 -236.
   PubMedGoogle Scholar