Phosphatidylethanolamine enhances rhodopsin photoactivation and transducin binding in a solid supported lipid bilayer as determined using plasmon-waveguide resonance spectroscopy.

Flash photolysis studies have shown that the membrane lipid environment strongly influences the ability of rhodopsin to form the key metarhodopsin II intermediate. Here we have used plasmon-waveguide resonance (PWR) spectroscopy, an optical method sensitive to both mass and conformation, to probe the effects of lipid composition on conformational changes of rhodopsin induced by light and due to binding and activation of transducin (G(t)). Octylglucoside-solubilized rhodopsin was incorporated by detergent dilution into solid-supported bilayers composed either of egg phosphatidylcholine or various mixtures of a nonlamellar-forming lipid (dioleoylphosphatidylethanolamine; DOPE) together with a lamellar-forming lipid (dioleoylphosphatidylcholine; DOPC). Light-induced proteolipid conformational changes as a function of pH correlated well with previous flash photolysis studies, indicating that the PWR spectral shifts monitored metarhodopsin II formation. The magnitude of these effects, and hence the extent of the conformational transition, was found to be proportional to the DOPE content. Our data are consistent with previous suggestions that lipids having a negative spontaneous curvature favor elongation of rhodopsin during the activation process. In addition, measurements of the G(t)/rhodopsin interaction in a DOPC/DOPE (25:75) bilayer at pH 5 demonstrated that light activation increased the affinity for G(t) from 64 nM to 0.7 nM, whereas G(t) affinity for dark-adapted rhodopsin was unchanged. By contrast, in DOPC bilayers the affinity of G(t) for light-activated rhodopsin was only 18 nM at pH 5. Moreover exchange of GDP for GTP gamma S was also monitored by PWR spectroscopy. Only the light-activated receptor was able to induce this exchange which was unaffected by DOPE incorporation. These findings demonstrate that nonbilayer-forming lipids can alter functionally linked conformational changes of G-protein-coupled receptors in membranes, as well as their interactions with downstream effector proteins.

[1]  S. Lowen The Biophysical Journal , 1960, Nature.

[2]  W. Dreyer,et al.  Rhodopsin content in the outer segment membranes of bovine and frog retinal rods. , 1974, Biochemistry.

[3]  A. Lamola,et al.  Effects of detergents and high pressures upon the metarhodopsin I--metarhodopsin II equilibrium. , 1974, Biochemistry.

[4]  H. Kühn Light- and GTP-regulated interaction of GTPase and other proteins with bovine photoreceptor membranes , 1980, Nature.

[5]  L. Stryer,et al.  Flow of information in the light-triggered cyclic nucleotide cascade of vision. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[6]  W. Baehr,et al.  Characterization of bovine rod outer segment G-protein. , 1982, The Journal of biological chemistry.

[7]  N. Bennett,et al.  The G-protein of retinal rod outer segments (transducin). Mechanism of interaction with rhodopsin and nucleotides. , 1985, The Journal of biological chemistry.

[8]  W. Hubbell,et al.  Effects of lipid environment on the light-induced conformational changes of rhodopsin. 2. Roles of lipid chain length, unsaturation, and phase state. , 1985, Biochemistry.

[9]  H. Hamm,et al.  Mechanism of action of monoclonal antibodies that block the light activation of the guanyl nucleotide-binding protein, transducin. , 1987, The Journal of biological chemistry.

[10]  J. Beach,et al.  Lipid-protein interactions mediate the photochemical function of rhodopsin. , 1988, Biochemistry.

[11]  P. Hargrave,et al.  Three cytoplasmic loops of rhodopsin interact with transducin. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[12]  L. White,et al.  Hydrophobicity effects in the condensation of water films on quartz , 1990 .

[13]  P. Silberzan,et al.  Silanation of silica surfaces. A new method of constructing pure or mixed monolayers , 1991 .

[14]  M. Straume,et al.  Role of sn-1-saturated,sn-2-polyunsaturated phospholipids in control of membrane receptor conformational equilibrium: effects of cholesterol and acyl chain unsaturation on the metarhodopsin I in equilibrium with metarhodopsin II equilibrium. , 1992, Biochemistry.

[15]  M. Webb A continuous spectrophotometric assay for inorganic phosphate and for measuring phosphate release kinetics in biological systems. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[16]  T. Thorgeirsson,et al.  Effects of temperature on rhodopsin photointermediates from lumirhodopsin to metarhodopsin II. , 1993, Biochemistry.

[17]  N. J. Gibson,et al.  Lipid headgroup and acyl chain composition modulate the MI-MII equilibrium of rhodopsin in recombinant membranes. , 1993, Biochemistry.

[18]  K. Hofmann,et al.  Two different forms of metarhodopsin II: Schiff base deprotonation precedes proton uptake and signaling state. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[19]  H. Macleod,et al.  Conformational changes in rhodopsin probed by surface plasmon resonance spectroscopy. , 1994, Biochemistry.

[20]  M. Brown,et al.  Modulation of Rhodopsin Function by Properties of the Membrane Bilayer , 2022 .

[21]  Z. Salamon,et al.  Surface plasmon resonance spectroscopy studies of membrane proteins: transducin binding and activation by rhodopsin monitored in thin membrane films. , 1996, Biophysical journal.

[22]  H. Macleod,et al.  Coupled plasmon-waveguide resonators: a new spectroscopic tool for probing proteolipid film structure and properties. , 1997, Biophysical journal.

[23]  D. Kliger,et al.  Effects of pH on rhodopsin photointermediates from lumirhodopsin to metarhodopsin II. , 1998, Biochemistry.

[24]  Z. Diénès,et al.  Incorporation of rhodopsin in laterally structured supported membranes: observation of transducin activation with spatially and time-resolved surface plasmon resonance. , 1998, Biochemistry.

[25]  D. Farrens,et al.  Conformational Changes in Rhodopsin , 1999, The Journal of Biological Chemistry.

[26]  C Altenbach,et al.  Structural features and light-dependent changes in the sequence 306-322 extending from helix VII to the palmitoylation sites in rhodopsin: a site-directed spin-labeling study. , 1999, Biochemistry.

[27]  Surface Plasmon Resonance, Theory , 1999 .

[28]  Z. Salamon,et al.  Plasmon resonance spectroscopy: probing molecular interactions within membranes. , 1999, Trends in biochemical sciences.

[29]  D. C. Mitchell,et al.  Effect of protein hydration on receptor conformation: decreased levels of bound water promote metarhodopsin II formation. , 1999, Biochemistry.

[30]  J. Klein-Seetharaman,et al.  Structural features and light-dependent changes in the sequence 59-75 connecting helices I and II in rhodopsin: a site-directed spin-labeling study. , 1999, Biochemistry.

[31]  Kai Simons,et al.  Lipid rafts and signal transduction , 2000, Nature Reviews Molecular Cell Biology.

[32]  K. Palczewski,et al.  Crystal Structure of Rhodopsin: A G‐Protein‐Coupled Receptor , 2000, Science.

[33]  Z. Salamon,et al.  Plasmon resonance studies of agonist/antagonist binding to the human delta-opioid receptor: new structural insights into receptor-ligand interactions. , 2000, Biophysical journal.

[34]  Z. Salamon,et al.  Interaction of phosphatidylserine synthase from E. coli with lipid bilayers: coupled plasmon-waveguide resonance spectroscopy studies. , 2000, Biophysical journal.

[35]  John C. Lindon,et al.  Encyclopedia of spectroscopy and spectrometry , 2000 .

[36]  Z. Salamon,et al.  Optical anisotropy in lipid bilayer membranes: coupled plasmon-waveguide resonance measurements of molecular orientation, polarizability, and shape. , 2001, Biophysical journal.

[37]  J. Klein-Seetharaman,et al.  Structure and function in rhodopsin: mapping light-dependent changes in distance between residue 316 in helix 8 and residues in the sequence 60-75, covering the cytoplasmic end of helices TM1 and TM2 and their connection loop CL1. , 2001, Biochemistry.

[38]  D. C. Mitchell,et al.  Optimization of Receptor-G Protein Coupling by Bilayer Lipid Composition II , 2001, The Journal of Biological Chemistry.

[39]  A. Herrmann,et al.  Light-induced Reorganization of Phospholipids in Rod Disc Membranes* , 2001, The Journal of Biological Chemistry.

[40]  T. Sakmar,et al.  Rhodopsin: structural basis of molecular physiology. , 2001, Physiological reviews.

[41]  Burton J. Litman,et al.  Optimization of Receptor-G Protein Coupling by Bilayer Lipid Composition I , 2001, The Journal of Biological Chemistry.

[42]  J. Klein-Seetharaman,et al.  Structure and function in rhodopsin: mapping light-dependent changes in distance between residue 65 in helix TM1 and residues in the sequence 306-319 at the cytoplasmic end of helix TM7 and in helix H8. , 2001, Biochemistry.

[43]  Z. Salamon,et al.  Plasmon resonance spectroscopy: probing molecular interactions at surfaces and interfaces , 2001 .

[44]  R. Thurmond,et al.  Conformational energetics of rhodopsin modulated by nonlamellar-forming lipids. , 2002, Biochemistry.

[45]  D. C. Mitchell,et al.  Manipulation of cholesterol levels in rod disk membranes by methyl-beta-cyclodextrin: effects on receptor activation. , 2002, The Journal of biological chemistry.

[46]  Yoshinori Shichida,et al.  Functional role of internal water molecules in rhodopsin revealed by x-ray crystallography , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[47]  I. Alves,et al.  Direct Observation of G-protein Binding to the Human δ-Opioid Receptor Using Plasmon-Waveguide Resonance Spectroscopy* , 2003, Journal of Biological Chemistry.

[48]  H Gobind Khorana,et al.  Rhodopsin structure, dynamics, and activation: a perspective from crystallography, site-directed spin labeling, sulfhydryl reactivity, and disulfide cross-linking. , 2003, Advances in protein chemistry.

[49]  Graphical analysis of mass and anisotropy changes observed by plasmon-waveguide resonance spectroscopy can provide useful insights into membrane protein function. , 2004, Biophysical journal.

[50]  I. Alves,et al.  Selectivity, Cooperativity, and Reciprocity in the Interactions between the δ-Opioid Receptor, Its Ligands, and G-proteins* , 2004, Journal of Biological Chemistry.

[51]  Burton J. Litman,et al.  A role for phospholipid polyunsaturation in modulating membrane protein function , 2007, Lipids.