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Yoshinori Shichida

Publications and source records attributed to Yoshinori Shichida.

At least 19 recordsLinked to original sources

Molecular properties of rhodopsin and rod function.

Signal transduction in rod cells begins with photon absorption by rhodopsin and leads to the generation of an electrical response. The response profile is determined by the molecular properties of the phototransduction components. To examine how the molecular properties of rhodopsin correlate with the rod-response profile, we have generated a knock-in mouse with rhodopsin replaced by its E122Q mutant, which exhibits properties different from those of wild-type (WT) rhodopsin. Knock-in mouse rods with E122Q rhodopsin exhibited a photosensitivity about 70% of WT. Correspondingly, their single-photon response had an amplitude about 80% of WT, and a rate of decline from peak about 1.3 times of WT. The overall 30% lower photosensitivity of mutant rods can be explained by a lower pigment photosensitivity (0.9) and the smaller single-photon response (0.8). The slower decline of the response, however, did not correlate with the 10-fold shorter lifetime of the meta-II state of E122Q rhodopsin. This shorter lifetime became evident in the recovery phase of rod cells only when arrestin was absent. Simulation analysis of the photoresponse profile indicated that the slower decline and the smaller amplitude of the single-photon response can both be explained by the shift in the meta-I/meta-II equilibrium of E122Q rhodopsin toward meta-I. The difference in meta-III lifetime between WT and E122Q mutant became obvious in the recovery phase of the dark current after moderate photobleaching of rod cells. Thus, the present study clearly reveals how the molecular properties of rhodopsin affect the amplitude, shape, and kinetics of the rod response.

Animals↗

Parietal-eye phototransduction components and their potential evolutionary implications.

The parietal-eye photoreceptor is unique because it has two antagonistic light signaling pathways in the same cell-a hyperpolarizing pathway maximally sensitive to blue light and a depolarizing pathway maximally sensitive to green light. Here, we report the molecular components of these two pathways. We found two opsins in the same cell: the blue-sensitive pinopsin and a previously unidentified green-sensitive opsin, which we name parietopsin. Signaling components included gustducin-alpha and Galphao, but not rod or cone transducin-alpha. Single-cell recordings demonstrated that Go mediates the depolarizing response. Gustducin-alpha resembles transducin-alpha functionally and likely mediates the hyperpolarizing response. The parietopsin-Go signaling pair provides clues about how rod and cone phototransduction might have evolved.

3',5'-Cyclic-GMP Phosphodiesterases↗

Structural changes in the Schiff base region of squid rhodopsin upon photoisomerization studied by low-temperature FTIR spectroscopy.

Low-temperature Fourier transform infrared (FTIR) spectroscopy is used to study squid rhodopsin at 77 K in investigating structural changes in the Schiff base region upon photoisomerization. The analysis of O-D stretching vibrations in D(2)O revealed that there are more internal water molecules near the retinal chromophore in squid rhodopsin than in bovine rhodopsin. Among nine O-D stretching vibrations of water in squid rhodopsin, eight peaks are identical between rhodopsin and 9-cis-rhodopsin (Iso). On the other hand, the isomer-specific O-D stretch of water was observed for rhodopsin (2451 cm(-)(1)) and Iso (2382 cm(-)(1)). Low frequencies of these bands suggest that the water forms a strong hydrogen bond with a negatively charged counterion. In addition, it was suggested that the hydrogen bond of the Schiff base is weaker in squid rhodopsin than in bacteriorhodopsin and bovine rhodopsin, and squid rhodopsin possessed similar hydrogen bonding strength for the Schiff base among rhodopsin, Iso, and bathorhodopsin. Most vibrational bands in the X-D stretch region originate from water O-D or the Schiff base N-D stretches, suggesting that the hydrogen bonding network in the Schiff base region of squid rhodopsin is composed of only water molecules. On the basis of these results, we propose that squid rhodopsin possesses a "bridge" water between the Schiff base and its counterion as well as squid retinochrome [Furutani, Y., Terakita, A., Shichida, Y., and Kandori, H. (2005) Biochemistry 44, 7988-7997], which is absent in vertebrate rhodopsin [Furutani, Y., Shichida, Y., and Kandori, H. (2003) Biochemistry 42, 9619-9625].

Animals↗

Assignment of the vibrational modes of the chromophores of iodopsin and bathoiodopsin: low-temperature fourier transform infrared spectroscopy of 13C- and 2H-labeled iodopsins.

To investigate the chromophore structures of iodopsin and its low-temperature photoproducts, we have assigned their vibrational bands in the Fourier transform infrared (FTIR) spectra using iodopsin samples that were reconstituted with a series of (13)C- and deuterium-labeled retinals. The analyses of the vibrational bands in the fingerprint and hydrogen-out-of-plane (HOOP) regions indicated that the structure of the chromophores in the iodopsin system differs near their centers from those in the rhodopsin system. Compared to rhodopsin, the chromophore of the batho intermediate of iodopsin is twisted in the C(12) to C(14) regions but is more planar around C(11) region. The large amount of twisting was reduced by removing the chloride ion from the iodopsin, suggesting that this twisting hinders the relaxation of the torsion near C(11) necessary for the transition to the lumi intermediate and thus results in the thermal reversion of the batho intermediate back to the iodopsin. From the analyses of the C=NH and C=ND stretching bands, we conclude that the displacement of the Schiff base region upon photoisomerization of the chromophore is restricted, as is the case for rhodopsin. These results indicated that iodopsin's chromophore has a unique structure near its center and that this difference is enhanced by the binding of chloride nearby.

Chlorides↗

Divergent selection on opsins drives incipient speciation in Lake Victoria cichlids.

Divergent natural selection acting on ecological traits, which also affect mate choice, is a key element of ecological speciation theory, but has not previously been demonstrated at the molecular gene level to our knowledge. Here we demonstrate parallel evolution in two cichlid genera under strong divergent selection in a gene that affects both. Strong divergent natural selection fixed opsin proteins with different predicted light absorbance properties at opposite ends of an environmental gradient. By expressing them and measuring absorbance, we show that the reciprocal fixation adapts populations to divergent light environments. The divergent evolution of the visual system coincides with divergence in male breeding coloration, consistent with incipient ecological by-product speciation.

Africa, Eastern↗

Recovery of rod-mediated a-wave during light-adaptation in mGluR6-deficient mice.

The purpose of this study was to compare the a-waves of mGluR6-deficient mice (KO) to that of wild-type mice (WT), and to determine whether the light-adapted electroretinogram of the KO mice originate exclusively from cones. Dark-adapted a-waves were recorded under the same conditions from both types of mice. With a 96-cd/m(2) background, the a-wave from both types of mice showed a rapid recovery over a 50-min period. The analysis of the a-waves in KO mice indicated that the recovery was determined mainly by the rod component. The light-adapted b-wave of WT mice showed no corresponding recovery. We conclude that rod contribution must be considered in the analyses of the light-adapted a-waves of KO mice.

Adaptation, Ocular↗

Farnesylation of retinal transducin underlies its translocation during light adaptation.

G proteins are posttranslationally modified by isoprenylation: either farnesylation or geranylgeranylation. The gamma subunit of retinal transducin (Talpha/Tbetagamma) is selectively farnesylated, and the farnesylation is required for light signaling mediated by transducin in rod cells. However, whether and how this selective isoprenylation regulates cellular functions remain poorly understood. Here we report that knockin mice expressing geranylgeranylated Tgamma showed normal rod responses to dim flashes under dark-adapted conditions but exhibited impaired properties in light adaptation. Of note, geranylgeranylation of Tgamma suppressed light-induced transition of Tbetagamma from membrane to cytosol, and also attenuated its light-dependent translocation from the outer segment to the inner region, an event contributing to retinal light adaptation. These results indicate that, while the farnesylation of transducin is interchangeable with the geranylgeranylation in terms of the light signaling, the selective farnesylation is important for visual sensitivity regulation by providing sufficient but not excessive membrane anchoring of Tbetagamma.

Adaptation, Ocular↗

Direct observation of the complex formation of GDP-bound transducin with the rhodopsin intermediate having a visible absorption maximum in rod outer segment membranes.

Rhodopsin is a photoreceptive protein that is present in rod photoreceptor cells, inducing a GDP-GTP exchange reaction on the retinal G-protein transducin (Gt) upon light absorption. This exchange reaction proceeds through at least three steps, which include the binding of photoactivated rhodopsin to GDP-bound Gt, the dissociation of GDP from the rhodopsin-Gt complex, and the binding of GTP to the nucleotide-unbound Gt. These steps have been thought to occur after the formation of the rhodopsin intermediate, meta-II; however, the extra formation of meta-II, which reflects the formation of a complex with Gt, was inhibited in the presence of excess GDP. Here, we use a newly developed CCD spectrophotometer to show that a meta-II precursor, meta-Ib, which has an absorption maximum at visible region, can bind to Gt in its GDP-bound form in urea-washed bovine rod outer segment membranes. The affinity of meta-Ib for GDP-bound Gt is about two times less than that of meta-II for GDP-unbound Gt, indicating that the extra formation of meta-II is observed at equilibrium even in the presence of the meta-Ib-Gt complex. This is the first identification of a complex that includes the GDP-bound form of G protein. Our results strongly suggest that the protein conformational change of the rhodopsin intermediate after binding to Gt is important for the induction of the nucleotide release from the alpha-subunit of Gt.

Absorption↗

Cephalochordate melanopsin: evolutionary linkage between invertebrate visual cells and vertebrate photosensitive retinal ganglion cells.

Animal photoreceptor cells can be classified into two distinct types, depending on whether the photopigment is borne on the membrane of a modified cilium (ciliary type) or apical microvilli (rhabdomeric type) [1]. Ciliary photoreceptors are well known as vertebrate rods and cones and are also found in several invertebrates. The rhabdomeric photoreceptor, in contrast, is a predominant type of invertebrate visual cell, but morphologically identifiable rhabdomeric photoreceptors have never been found in vertebrates. It is hypothesized that the rhabdomeric photoreceptor cell had evolved to be the photosensitive retinal ganglion cell for the vertebrate circadian photoentrainment [2, 3 and 4] owing to the fact that some molecules involved in cell differentiation are common among them [5]. We focused on the cephalochordate amphioxus because it is the closest living invertebrate to the vertebrates, and interestingly, it has rhabdomeric photoreceptor cells for putative nonvisual functions [6]. Here, we show that the amphioxus homolog of melanopsin [7, 8 and 9], the circadian photopigment in the photosensitive retinal ganglion cells of vertebrates, is expressed in the rhabdomeric photoreceptor cells of the amphioxus and that its biochemical and photochemical properties, not just its primary structure, are considerably similar to those of the visual rhodopsins in the rhabdomeric photoreceptor cells of higher invertebrates. The cephalochordate rhabdomeric photoreceptor represents an evolutionary link between the invertebrate visual photoreceptor and the vertebrate circadian photoreceptor.

Animals↗

FTIR studies of the photoactivation processes in squid retinochrome.

Retinochrome is a photoisomerase of the invertebrate visual system, which converts all-trans-retinal to the 11-cis configuration and supplies it to visual rhodopsin. In this paper, we studied light-induced structural changes in squid retinochrome by means of low-temperature UV-visible and Fourier transform infrared (FTIR) spectroscopy. In PC liposomes, lumi-retinochrome was stable in the wide temperature range between 77 and 230 K. High thermal stability of the primary intermediate in retinochrome is in contrast to the case in rhodopsins. FTIR spectroscopy suggested that the chromophore of lumi-retinochrome is in a relaxed planar 11-cis form, being consistent with its high thermal stability. The chromophore binding pocket of retinochrome appears to accommodate both all-trans and 11-cis forms without a large distortion, and limited protein structural changes between all-trans and 11-cis chromophores may be suitable for the function of retinochrome as a photoisomerase. The analysis of N-D and O-D stretching vibrations in D(2)O revealed that the hydrogen bond of the Schiff base is weaker in retinochrome than in bovine rhodopsin and bacteriorhodopsin, while retinochrome has a water molecule under strongly hydrogen-bonded conditions (O-D stretch at 2334 cm(-)(1)). The hydrogen bond of the water is further strengthened in lumi-retinochrome. The formation of meta-retinochrome accompanies deprotonation of the Schiff base, together with the peptide backbone alterations of alpha-helices, and possible formation of beta-sheets. It was found that the Schiff base proton is not transferred to its counterion, Glu181, but directly released to the aqueous phase in PC liposomes (pH 7.5). This suggests that the Schiff base environment is exposed to solvent in meta-retinochrome, which may be advantageous for the hydrolysis reaction of the Schiff base in the transport of 11-cis-retinal to its shuttle protein.

Animals↗

Molecular properties of rod and cone visual pigments from purified chicken cone pigments to mouse rhodopsin in situ.

We have investigated the molecular properties of rod and cone visual pigments to elucidate the differences in the molecular mechanism(s) of the photoresponses between rod and cone photoreceptor cells. We have found that the cone pigments exhibit a faster pigment regeneration and faster decay of meta-II and meta-III intermediates than the rod pigment, rhodopsin. Mutagenesis experiments have revealed that the amino acid residues at positions 122 and 189 in the opsins are the determinants for these differences. In order to study the relationship between the molecular properties of visual pigments and the physiology of rod photoreceptors, we used mouse rhodopsin as a model pigment because, by gene-targeting, the spectral properties of the pigment can be directly correlated to the physiology of the cells. In the present paper, we summarize the spectroscopic properties of cone pigments and describe our studies with mouse rhodopsin utilizing a high performance charge coupled device (CCD) spectrophotometer.

Animals↗

A rhodopsin exhibiting binding ability to agonist all-trans-retinal.

Rhodopsins are the members of the family of G protein-coupled receptors that have diverged from ligand-binding receptors into photoreceptive pigments. Vertebrate rhodopsins are able to bind the inverse agonist 11-cis-retinal but are unable to bind the agonist all-trans-retinal, indicating that vertebrate rhodopsin changed its binding ability during the course of molecular evolution. Here, we show that unlike vertebrate rhodopsin, amphioxus rhodopsin is still able to bind the agonist all-trans-retinal. The opsin of amphioxus rhodopsin can also bind 11-cis-retinal to form a photoreceptive pigment that can convert to a red-shifted photoproduct through cis-trans isomerization of the chromophore upon photon absorption. The red-shifted photoproduct is the stable G protein activating state. Incubation of the opsin with all-trans-retinal produces a G protein activating state that is spectroscopically and biochemically indistinguishable from the red-shifted photoproduct, indicating that the opsin possesses agonist-binding ability. The opsin exhibits an approximately 50-fold higher affinity for 11-cis-retinal than for all-trans-retinal, and mutational analyses revealed that Trp-265 situated in helix VI is important for the increase in binding affinity to 11-cis-retinal. These properties of amphioxus rhodopsin suggest that an ancestral rhodopsin increased the affinity for 11-cis-retinal by rearrangement of a structure including Trp-265 to act as a photoreceptor. In addition, an additional mechanism was acquired in vertebrate rhodopsin to prevent completely the binding of exogenous all-trans-retinal during molecular evolution.

Animals↗

Parallelism of amino acid changes at the RH1 affecting spectral sensitivity among deep-water cichlids from Lakes Tanganyika and Malawi.

Many examples of the appearance of similar traits in different lineages are known during the evolution of organisms. However, the underlying genetic mechanisms have been elucidated in very few cases. Here, we provide a clear example of evolutionary parallelism, involving changes in the same genetic pathway, providing functional adaptation of RH1 pigments to deep-water habitats during the adaptive radiation of East African cichlid fishes. We determined the RH1 sequences from 233 individual cichlids. The reconstruction of cichlid RH1 pigments with 11-cis-retinal from 28 sequences showed that the absorption spectra of the pigments of nine species were shifted toward blue, tuned by two particular amino acid replacements. These blue-shifted RH1 pigments might have evolved as adaptations to the deep-water photic environment. Phylogenetic evidence indicates that one of the replacements, A292S, has evolved several times independently, inducing similar functional change. The parallel evolution of the same mutation at the same amino acid position suggests that the number of genetic changes underlying the appearance of similar traits in cichlid diversification may be fewer than previously expected.

Adaptation, Physiological↗

Amino acid residues responsible for the meta-III decay rates in rod and cone visual pigments.

Vertebrate retinas have two types of photoreceptor cells, rods and cones, which contain visual pigments with different molecular properties. These pigments diverged from a common ancestor, and their difference in molecular properties originates from the difference in their amino acid residues. We previously reported that the difference in decay times of G protein-activating meta-II intermediates between the chicken rhodopsin and green-sensitive cone (chicken green) pigments is about 50 times. This difference only originates from the differences of two residues at positions 122 and 189 (Kuwayama, S., Imai, H., Hirano, T., Terakita, A., and Shichida, Y. (2002) Biochemistry 41, 15245-15252). Here we show that the meta-III intermediates exhibit about 700 times difference in decay times between the two pigments, and the faster decay in chicken green can be converted to the slower decay in rhodopsin by replacing the residues in chicken green with the corresponding rhodopsin residues. However, the inverse directional conversion did not occur when the two residues in rhodopsin were replaced by those of chicken green. Analysis using chimerical mutants derived from these pigments has demonstrated that amino acid residues responsible for the slow rhodopsin meta-III decay are situated at several positions throughout the C-terminal half of rhodopsin. Considering that rhodopsins evolved from cone pigments, it has been suggested that the molecular properties of rhodopsin have been optimized by mutations at several positions, and the chicken green mutants at two positions could be rhodopsin-like pigments transiently produced in the course of molecular evolution.

Amino Acid Sequence↗

Expression and localization of an exogenous G protein-coupled receptor fused with the rhodopsin C-terminal sequence in the retinal rod cells of knockin mice.

Vertebrate rod cell outer segments are highly differentiated compartments consisting of closely packed disk membranes, in which the photoreceptor rhodopsin is embedded at high density. To explore the unusually efficient mechanism of rhodopsin biosynthesis, folding and transport, we challenged it with the ectopic expression in rod cells of human endothelin receptor subtype B (hET(B)R) fused with the C-terminal 10 residues of rhodopsin, under the control of the mouse opsin promoter/enhancer, by gene targeted replacement (knockin), because the C-terminal eight residues are essential to target rhodopsin to the outer segment. The hET(B)R, a type-I G protein-coupled receptor, was successfully expressed and folded in a functional structure in the rod cells of knockin mice. However, while the mRNA level of hET(B)R was one tenth of that of rhodopsin, the hET(B)R protein level was approximately one-thousandth of the rhodopsin level in heterozygous mice, suggesting an intrinsically distinct efficiency in the production of functional receptor protein. In addition, a substantial fraction of the hET(B)R was successfully transported to the outer segment, suggesting that the addition of the C-terminal sequence of rhodopsin enabled hET(B)R to be translocated to the outer segment.

Animals↗

Generation of knock-in mice carrying third cones with spectral sensitivity different from S and L cones.

Red-green color vision in primates is unique in the sense that it is mediated by two photoreceptor cells that are indistinguishable in all aspects except for their visual pigments. In order to generate an animal model for investigation of the interaction between red-green inputs at the molecular level, we applied knock-in technology and X-chromosome inactivation machinery to make a mouse model with cone cells possessing visual pigments with different spectral sensitivities. We introduced a S308A point mutation into the Green opsin gene allele on the X-chromosome. This manipulation generated a 24 nm red-shift of absorption maximum in the cone pigment with negligible functional differences in other molecular properties. Amplitudes of responses in ERG and ganglion cell recordings of homozygotes were similar to those of wild-types, although the spectral sensitivities differed. Heterozygotes showed variable spectral sensitivities of ganglion cell responses due to the different integration of the native and the S308A cone inputs on the dendritic fields. In situ hybridization experiments showed that cone cells with respective pigments formed patch-like clusters of specific L cone-types, approximately 30 mum in diameter, which were randomly distributed in the dorsal region of the retinas. Since the patch-like clustering was arranged by X-inactivation, such clustering could be present in the peripheral retinas of New World monkeys with polymorphic L pigments, indicating that our mice would be a suitable model to study evolution of the mammalian color vision system.

Animals↗

Identification of a protanomalous chimpanzee by molecular genetic and electroretinogram analyses.

We determined the structures of long (L)-wavelength-sensitive and middle (M)-wavelength-sensitive opsin gene array of 58 male chimpanzees and we investigated relative sensitivity to red and green lights by electroretinogram flicker photometry. One subject had protanomalous color vision, while others had normal color vision. Unlike in humans, a polymorphic difference in the copy number of the genes and a polymorphic base substitution at amino acid position 180 were not frequently observed in chimpanzees.

Animals↗