Convergent evolution of tertiary structure in rhodopsin visual proteins from vertebrates and box jellyfish

Gerrard, Elliot; Mutt, Eshita; Nagata, Takashi; Koyanagi, Mitsumasa; Flock, Tilman; Lesca, Elena; Schertler, Gebhard F. X.; Terakita, Akihisa; Deupí, Xavier; Lucas, Robert J.

doi:10.1073/pnas.1721333115

Cited by 23 publications

(20 citation statements)

References 54 publications

(80 reference statements)

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“…These data were fitted with the template of an opsin retinaldehyde pigment (Govardovskii nomogram) 17 resulting in a peak wavelength ( λ max ) of 493 nm (Fig. 5h , red line), which is in accordance with the reported action spectrum of wild-type JellyOp 18 . This data and the fit (Eq.…”

Section: Resultssupporting

confidence: 75%

Optogenetic stimulation of Gs-signaling in the heart with high spatio-temporal precision

et al. 2019

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The standard technique for investigating adrenergic effects on heart function is perfusion with pharmaceutical agonists, which does not provide high temporal or spatial precision. Herein we demonstrate that the light sensitive Gs-protein coupled receptor JellyOp enables optogenetic stimulation of Gs-signaling in cardiomyocytes and the whole heart. Illumination of transgenic embryonic stem cell-derived cardiomyocytes or of the right atrium of mice expressing JellyOp elevates cAMP levels and instantaneously accelerates spontaneous beating rates similar to pharmacological β-adrenergic stimulation. Light application to the dorsal left atrium instead leads to supraventricular extrabeats, indicating adverse effects of localized Gs-signaling. In isolated ventricular cardiomyocytes from JellyOp mice, we find increased Ca2+ currents, fractional cell shortening and relaxation rates after illumination enabling the analysis of differential Gs-signaling with high temporal precision. Thus, JellyOp expression allows localized and time-restricted Gs stimulation and will provide mechanistic insights into different effects of site-specific, long-lasting and pulsatile Gs activation.

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Section: Resultssupporting

confidence: 75%

Optogenetic stimulation of Gs-signaling in the heart with high spatio-temporal precision

et al. 2019

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“…In addition to the contribution of Ser186 to the function of the Glu181 counterion, such functional coupling mediated by a polar residue at this site seems common among many rhodopsins regardless of the position of their counterion. Recently, we have revealed a new counterion position 94 in a Gs-coupled jellyfish opsin—and possibly in other cnidarian opsins—where Arg186 inhibits Glu181 from acting as a counterion likely by neutralizing the charge 16 . In this lineage, therefore, residues 186 and 181 still interact with each other—as we propose for spider Rh1—and may have an unknown function(s) other than stabilization of the PSB.…”

Section: Discussionmentioning

confidence: 99%

“…1a), strongly suggesting that the role of Glu181 is widely common, probably constituting the ancestral counterion. Very recently, we have discovered that Glu94 acts as the counterion in a Gs-coupled cnidarian opsin 16 .…”

Section: Introductionmentioning

confidence: 99%

The counterion–retinylidene Schiff base interaction of an invertebrate rhodopsin rearranges upon light activation

et al. 2019

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Animals sense light using photosensitive proteins—rhodopsins—containing a chromophore—retinal—that intrinsically absorbs in the ultraviolet. Visible light-sensitivity depends primarily on protonation of the retinylidene Schiff base (SB), which requires a negatively-charged amino acid residue—counterion—for stabilization. Little is known about how the most common counterion among varied rhodopsins, Glu181, functions. Here, we demonstrate that in a spider visual rhodopsin, orthologue of mammal melanopsins relevant to circadian rhythms, the Glu181 counterion functions likely by forming a hydrogen-bonding network, where Ser186 is a key mediator of the Glu181–SB interaction. We also suggest that upon light activation, the Glu181–SB interaction rearranges while Ser186 changes its contribution. This is in contrast to how the counterion of vertebrate visual rhodopsins, Glu113, functions, which forms a salt bridge with the SB. Our results shed light on the molecular mechanisms of visible light-sensitivity relevant to invertebrate vision and vertebrate non-visual photoreception.

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“…The absorption spectra of PxRh1_Gs and PxRh3_Gs are also indicated by green and magenta broken curves, respectively. Schematic drawings of seven transmembrane structures of butterfly opsins are also shown, in which helices and amino acid residues of PxRh1 and PxRh3 are indicated by green and magenta, respectively powerful tool for the investigation of spectral tuning mechanisms in addition to analyses of absorption characteristics of novel opsins [24] and counterions [30]. Several other Papilionid species also possess Rh1 and Rh3 [31].…”

Section: Resultsmentioning

confidence: 99%

Spectral tuning mediated by helix III in butterfly long wavelength-sensitive visual opsins revealed by heterologous action spectroscopy

et al. 2019

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Absorption spectra of opsin-based pigments are tuned from the UV to the red regions by interactions of the chromophore with surrounding amino acid residues. Both vertebrates and invertebrates possess long-wavelengthsensitive (LWS) opsins, which underlie color vision involving "red" sensing. The LWS opsins have independently evolved in each lineage, which suggests the existence of diverse mechanisms in spectral tuning. In vertebrate LWS opsins, the mechanisms underlying spectral tuning have been well characterized by spectroscopic analyses with recombinant pigments of wild type (WT) and mutant opsins. However in invertebrate LWS opsins including insect ones, the mechanisms are largely unknown due to the difficulty in obtaining recombinant pigments. Here we have overcome the problem by analyzing heterologous action spectra based on light-dependent changes in the second messenger in opsin-expressing cultured cells. We found that WTs of two LWS opsins of the butterfly, Papilio xuthus, PxRh3 and PxRh1 have the wavelengths of the absorption maxima at around 570 nm and 540 nm, respectively. Analysis of a series of chimeric mutants showed that helix III is crucial to generating a difference of about 15 nm in the wavelength of absorption maxima of these LWS opsins. Further site-directed mutations in helix III revealed that amino acid residues at position 116 and 120 (bovine rhodopsin numbering system) are involved in the spectral tuning of PxRh1 and PxRh3, suggesting a different spectral tuning mechanism from that of primate LWS opsins.

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Convergent evolution of tertiary structure in rhodopsin visual proteins from vertebrates and box jellyfish

Cited by 23 publications

References 54 publications

Optogenetic stimulation of Gs-signaling in the heart with high spatio-temporal precision

Optogenetic stimulation of Gs-signaling in the heart with high spatio-temporal precision

The counterion–retinylidene Schiff base interaction of an invertebrate rhodopsin rearranges upon light activation

Spectral tuning mediated by helix III in butterfly long wavelength-sensitive visual opsins revealed by heterologous action spectroscopy

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