Interaction with Transducin Depletes Metarhodopsin III

Zimmermann, Kerstin; Ritter, Eglof; Bartl, Franz; Hofmann, Klaus Peter; Heck, M.

doi:10.1074/jbc.m406856200

Cited by 28 publications

(28 citation statements)

References 40 publications

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“…The concept of lipidic substances as full or partial ligand agonists is not novel. For (44) adjusted to highlight our experimental conditions. After initial photoactivation, an equilibrium between Meta-I and Meta-II rhodopsin is established within milliseconds.…”

Section: Discussionmentioning

confidence: 99%

Evidence for Specificity in Lipid-Rhodopsin Interactions

Soubias

Teague

Gawrisch

2006

Journal of Biological Chemistry

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The interaction of bovine rhodopsin with poly-and monounsaturated lipids was studied by 1 H MAS NMR with magnetization transfer from rhodopsin to lipid. Experiments were conducted on bovine rod outer segment (ROS) disks and on recombinant membranes containing lipids with polyunsaturated, docosahexaenoyl (DHA) chains. Poly-and monounsaturated lipids interact specifically with different sites on the rhodopsin surface. Rates of magnetization transfer from protein to DHA are lipid headgroup-dependent and increased in the sequence PC < PS < PE. Boundary lipids are in fast exchange with the lipid matrix on a time scale of milliseconds or shorter. All rhodopsin photointermediates transferred magnetization preferentially to DHA-containing lipids, but highest rates were observed for Meta-III rhodopsin. The experiments show clearly that the surface of rhodopsin has sites for specific interaction with lipids. Current theories of lipid-protein interaction do not account for such surface heterogeneity.Rhodopsin is the light receptor responsible for dim light vision in the rod photoreceptor cells of vertebrates. A large body of research demonstrated that efficiency of the rhodopsindependent steps of the visual process is exquisitely sensitive to membrane lipid composition, in particular to the content of -3 polyunsaturates (1-3). Retinal membranes of mammals, similar to synaptosomal membranes in brain, contain up to 50 mol % of docosahexaenoic acid (DHA, 2 22:6n3), a polyunsaturated fatty acid with 22 carbon atoms and six double bonds that are evenly distributed over the length of the chain (4).In earlier reconstitution experiments with bovine rhodopsin it was established that the equilibrium concentration of Meta-II rhodopsin increased with the concentration of DHA hydrocarbon chains in the lipid matrix (5-7). Also the headgroups of phospholipids had a significant effect on Meta-II formation (5, 7) and activation of G t (8, 9). It was observed that phosphatidylethanolamines (PE) and the negatively charged phosphatidylserines (PS) increased the amount of Meta-II.The influence of PS on the equilibrium was assigned to changes of the membrane electric surface potential (7). In contrast, the sensitivity of membranes to PE content correlated with an alteration of membrane curvature elasticity (10) as proposed for other membrane proteins by Navarro et al. (11), Jensen and Schutzbach (12), Gruner (13), Lindblom and coworkers (14), and Cantor (15). Litman and co-workers (6, 16) found a correlation between mobility and orientation of the fluorescence probe DPH in lipid bilayers, summarized as a membrane free volume parameter, and Meta-II formation. Furthermore, they observed a preference of rhodopsin to locate in domains rich in di-22:6n3-PC that formed in di-16:0-PC/ di-22:6-PC/cholesterol mixtures. Mouritsen proposed a link between hydrophobic thickness of lipid bilayers and activity of membrane proteins (18). Brown and co-workers (10) suggested that Meta-II has a greater hydrophobic thickness than Meta-I, and that the lipid bilayer...

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Section: Discussionmentioning

confidence: 99%

Evidence for Specificity in Lipid-Rhodopsin Interactions

Soubias

Teague

Gawrisch

2006

Journal of Biological Chemistry

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“…Spectroscopic data show that blue light absorption of the active Meta II state does not lead back to the ground state ( max ϭ 500 nm) to a significant extent but to a product with an absorption maximum at 475 nm (32). By UV-visible and FTIR difference spectroscopy, this blue light-induced photoproduct of Meta II could be identified as Meta III (33,34), a species already known as a side product of the thermal Meta II decay (9). Recent work has shown that this thermal product contains the chromophore in the Schiff base all-trans-15-syn configuration (35) and that the Meta III formed by light absorption is the same by all available criteria.…”

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confidence: 99%

“…The end product of the new light-induced pathway, Meta III, can form up to 80%, depending on the conditions, and has remarkable properties. Because of its long lifetime (up to hours (34)), it excludes the chromophore very efficiently from the regeneration pathway, which has led to the concept of a retinal storage form (34,37,38). Remarkably, the lifetime of Meta III depends on the presence of G-protein (34) and arrestin (39,40), which was interpreted as an "inverse catalysis" of receptor conversion by G-protein.…”

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confidence: 99%

“…Because of its long lifetime (up to hours (34)), it excludes the chromophore very efficiently from the regeneration pathway, which has led to the concept of a retinal storage form (34,37,38). Remarkably, the lifetime of Meta III depends on the presence of G-protein (34) and arrestin (39,40), which was interpreted as an "inverse catalysis" of receptor conversion by G-protein. Given the fact that these proteins undergo light-dependent transport, and that the rate of rhodopsin regeneration is affected by the decay of Meta II and Meta III in contrast to the phosphorylation rate (41), interesting possibilities of regulation are thereby opened.…”

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confidence: 99%

“…First, it can be anticipated that the residual activity of Meta III should lead to an increased noise level of the visual system (34). Under conditions of extended illumination and depending on the spectral composition of the incident light, a certain amount of Meta III accumulates (up to 80% under the (artificial) conditions of continuous blue illumination).…”

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Deactivation and Proton Transfer in Light-induced Metarhodopsin II/Metarhodopsin III Conversion

Ritter

Elgeti

Hofmann

et al. 2007

Journal of Biological Chemistry

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Vertebrate rhodopsin shares with other retinal proteins the 11-cis-retinal chromophore and the light-induced 11-cis/trans isomerization triggering its activation pathway. However, only in rhodopsin the retinylidene Schiff base bond to the apoprotein is eventually hydrolyzed, making a complex regeneration pathway necessary. Metabolic regeneration cannot be short-cut, and light absorption in the active metarhodopsin (Meta) II intermediate causes anti/syn isomerization around the retinylidene linkage rather than reversed trans/cis isomerization. A new deactivating pathway is thereby triggered, which ends in the Meta III "retinal storage" product. Using time-resolved Fourier transform infrared spectroscopy, we show that the identified steps of receptor activation, including Schiff base deprotonation, protein structural changes, and proton uptake by the apoprotein, are all reversed. However, Schiff base reprotonation is much faster than the activating deprotonation, whereas the protein structural changes are slower. The final proton release occurs with pK ≈ 4.5, similar to the pK of a free Glu residue and to the pK at which the isolated opsin apoprotein becomes active. A forced deprotonation, equivalent to the forced protonation in the activating pathway, which occurs against the unfavorable pH of the medium, is not observed. This explains properties of the final Meta III product, which displays much higher residual activity and is less stable than rhodopsin arising from regeneration with 11-cis-retinal. We propose that the anti/syn conversion can only induce a fast reorientation and distance change of the Schiff base but fails to build up the full set of dark ground state constraints, presumably involving the Glu 134 /Arg 135 cluster.The photoreceptor rhodopsin located in the retinal rods of the vertebrate eye contains the chromophore 11-cis-retinal bound by a protonated Schiff base to Lys 296 of the apoprotein (1). Light absorption triggers isomerization around the C 11 ϭC 12 double bond of the polyene chain of the chromophore (2-4), leading to the strained all-trans-form and storage of two thirds of the light energy in the chromophore-protein system (5-8). The receptor subsequently proceeds through a number of intermediates each characterized by its specific absorption spectrum in the UV-visible and mid infrared range. Related conformational changes of the binding pocket and of other, more remote parts of the apoprotein eventually lead to the active G-protein binding state, metarhodopsin II (Meta II).3 It is in equilibrium with its precursor metarhodopsin I (Meta I), depending on temperature and pH (9, 10) and on other factors such as lipids, protein environment, and pressure (11-15).The formation of the active species through the photointermediates has been described as a stepwise lowering of the stabilizing effect of the Schiff base counterion, which is a complex structure that comprises highly conserved Glu 181 and Glu 113 . In Meta I, the counterion appears to undergo a shift relative to the Schiff base, where...

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Influence of Arrestin on the Photodecay of Bovine Rhodopsin

et al. 2015

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Continued activation of the photocycle of the dim-light receptor rhodopsin leads to accumulation of all-trans-retinal in rod outer segments (ROS). This accumulation can damage the photoreceptor cell. For retinal homeostasis, deactivation processes are initiated in which the release of retinal is delayed. One of the processes involves binding of arrestin to rhodopsin. Here, we investigate the interaction of pre-activated truncated bovine visual arrestin (Tr) with rhodopsin in 1,2diheptanoyl-sn-glycero-3-phosphocholine (DHPC) micelles by solution NMR techniques and flash photolysis spectroscopy. Our results show that formation of the rhodopsin-arrestin complex markedly influences partitioning in the decay kinetics of rhodopsin that involves the simultaneous formation of meta II state and meta III state from the meta I state. Binding of Tr leads to an increase of meta III state population and consequently to a ~2-fold slower release of all-transretinal from rhodopsin.

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Interaction with Transducin Depletes Metarhodopsin III

Cited by 28 publications

References 40 publications

Evidence for Specificity in Lipid-Rhodopsin Interactions

Evidence for Specificity in Lipid-Rhodopsin Interactions

Deactivation and Proton Transfer in Light-induced Metarhodopsin II/Metarhodopsin III Conversion

Influence of Arrestin on the Photodecay of Bovine Rhodopsin

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